ESTRUCTURA DE LAS COMUNIDADES Y ZONACIÓN DE LA …
185
ESTRUCTURA DE LAS COMUNIDADES Y ZONACIÓN DE LA MACROFAUNA EN PLAYAS ARENOSAS DE ANDALUCÍA OCCIDENTAL. EFECTO DE LA ACTIVIDAD HUMANA SOBRE LAS COMUNIDADES INTERMAREALES M ª José Reyes Martínez Tesis Doctoral Sevilla, Diciembre 2014
Transcript of ESTRUCTURA DE LAS COMUNIDADES Y ZONACIÓN DE LA …
ESTRUCTURA DE LAS COMUNIDADES Y
ZONACIOacuteN DE LA MACROFAUNA EN
PLAYAS ARENOSAS DE ANDALUCIacuteA
OCCIDENTAL EFECTO DE LA ACTIVIDAD
HUMANA SOBRE LAS COMUNIDADES
INTERMAREALES
M ordf Joseacute Reyes Martiacutenez
Tesis Doctoral
Sevilla Diciembre 2014
ESTRUCTURAS DE LAS COMUNIDADES Y ZONACIOacuteN DE LA
MACROFAUNA EN PLAYAS ARENOSAS DE ANDALUCIacuteA
OCCIDENTAL EFECTO DE LA ACTIVIDAD HUMANA SOBRE LAS
COMUNIDADES INTERMAREALES
Mordf Joseacute Reyes Martiacutenez
Tesis Doctoral
Sevilla Diciembre 2014
Francisco Joseacute Garciacutea Garciacutea Catedraacutetico de Zoologiacutea del Departamento de
Sistemas Fiacutesicos Quiacutemicos y Naturales de la Universidad Pablo de Olavide y
Juan Emilio Saacutenchez Moyano Profesor Titular del Departamento de Zoologiacutea
de la Universidad de Sevilla
CERTIFICAN
Que la presente memoria titulada ldquoEstructura de las comunidades y
zonacioacuten de la macrofauna en playas arenosas de Andaluciacutea Occidental
Efecto de la actividad humana sobre las comunidades intermarealesrdquo
presentada por Mordf Joseacute Reyes Martiacutenez para optar al Grado de Doctora por la
Universidad Pablo de Olavide ha sido realizada bajo su direccioacuten y autorizan
su presentacioacuten y defensa
Y para que asiacute conste expiden y firman la presente certificacioacuten en Sevilla a 3
de Diciembre de 2014
Dr D Francisco Joseacute Garciacutea Garciacutea Dr D Juan Emilio Saacutenchez Moyano
Agradecimientos
Y llegoacute el inesperado momento de los agradecimientos Tengo a tantas personas a las
que agradecer que espero no extenderme mucho
En primer lugar quiero dar las gracias a mis directores a Paco y a Emilio por la
confianza depositada en mi para la realizacioacuten de esta Tesis que todaviacutea no me creo
que haya terminado Hoy tengo sentimientos contradictorios por un lado alegriacutea y
satisfaccioacuten personal por haberlo logrado pero por otro no puedo dejar de sentir
cierta nostalgia porque esta etapa haya llegado a su fin Gracias a Paco por
escucharme cuando llamaba a su puerta diciendo ldquoTengo un problemardquo por la
incalculable ayuda prestada durante todo este tiempo y por los consejos ofrecidos en
los tiacutepicos momentos de crisis existencial Esta crisis tambieacuten se extendioacute al para mi
tenebroso mundo de la estadiacutestica en el que Emilio siempre lograba sacar luz Me
llevo guardados grandes momentos con vosotros no puedo evitar sonreiacuter al
acordarme de nuestros muestreos en los que sin quererlo poniacuteamos a prueba nuestra
integridad fiacutesica y como no emocional Hasta en alguna ocasioacuten recuerdo que casi
conseguimos traernos toda la arena de la playahellip iquestpero que no arreglaba nuestra
tortilla y quesito del descanso aunque fuera prefabricada en ese momento era gloria
Hay tantos momentos que no seriacutea posible describirlos todos Lo que si es cierto es
que hoy veo las playas desde una manera diferente y es gracias a vosotros
Carmen te llegoacute el momento Nos conocimos hace mucho tiempo y el destino quiso
que de nuevo emprendieacuteramos este camino juntas Gracias por tu gran ayuda en los
muestreos por las horas y horas compartidas en el laboratorio en el que nuestras
charlas haciacutean mucho maacutes ameno el paso del tiempo perdidas entre las muestras en
busca de nuestro tesoro particular los bichitos rositas Gracias por las charlas
constructivas y por ayudarme en los momentos que los que estaba maacutes que peacuterdida
No puedo olvidarme de todas aquellas personas que sin conocerme me abrieron las
puertas de sus laboratorios y de las que he aprendido cosas de incalculable valor
Todas esas estancias han sido clave para mi y para que esta tesis haya salido adelante
Gracias a Francesca Rossi que fue la primera en ldquoacogermerdquo cuando auacuten casi no habiacutea
salido del cascaroacuten aprendiacute mucho de aquella experiencia a Valeria Veloso y a Carlos
Borzone por la inmejorable estancia en Brasil y por todos sus consejos Gracias a Diego
Lercari por ensentildearme a ver las playas desde una perspectiva diferente por toda su
dedicacioacuten y especialmente por su paciencia gran parte de esta tesis ha sido gracias a
ti Gracias a todas las ldquomeninasrdquo del laboratorio de Pontal y como olvidarme del equipo
Undecimar gracias chicos haceacuteis que estaacutes estancias merezcan doblemente la pena
Es momento de agradecer a todas esas personas que me han ayudado en los
muestreos poniendo su granito de arena (y nunca mejor dicho) en esta tesis Tambieacuten
a todo el personal del Parque de los Toruntildeos por sus facilidades y gran ayuda durante
los muestreos y a los organismos puacuteblicos que han financiado tanto esta tesis (Junta
de Andaluciacutea a traveacutes de sus Proyectos de Excelencia) como las estancias disfrutadas
(Universidad Pablo de Olavide y AUIP)
Quiero agradecer tambieacuten a mi familia a mis hermanas y en especial a mis padres a
quieacuten hoy dedico esta tesis por todo el apoyo prestado durante este tiempo Siempre
habeacuteis confiado en mi aunque al principio no entendierais del todo bien mi diversioacuten
por ir a sacar kilos y kilos de arena de las playas Siempre me habeacuteis animado a seguir
mis suentildeos por muy alocados que fueran os habeacuteis sentido orgullosos y me habeacuteis
hecho creer que podiacutea conseguir todo lo que me propusiera y que esto era ldquopan
comidordquo
Gracias a Aacutelvaro mi gran pilar y sustento Tu eres de todos el que maacutes ha vivido esto
gracias por ser capaz de sacar siempre el lado bueno de las cosas y por el ldquoiquestQueacute no
sale hoy No te preocupes mantildeana seraacute otro diacuteardquo Siempre has confiado en mi incluso
cuando yo no era capaz de hacerlo Gracias por no cansarte de animarme incluso
cuando este trabajo se convertiacutea en lo primero me has acompantildeado en muchas de mis
aventuras playeras y has disfrutado y celebrado como nadie cuando llegaban buenas
noticias Se que tambieacuten para ti hoy las playas son algo maacutes y eso me enorgullece
Hasta vamos a las playas cargados con bolsitas por si nos encontramos alguacuten bichito
que recoger para el laboratorio iquestquieacuten nos lo habraacute pegado
Y por uacuteltimo a mis nintildeas gracias a Inma a Luciacutea y a Aacutengeles por los aacutenimos en los
momentos de flaqueza por las charlas constructivas por esas visitas sorpresa y salidas
ldquoobligadasrdquo para olvidarnos de todo Gracias por entenderme por aceptar aunque
fuera a regantildeadientes que no pudiera estar en todos los momentos porque el deber
me llamabahellip y por celebrar las alegriacuteas y como no los fracasos como solo nosotras
sabemos hacerlo Me habeacuteis valorado como nadie incluso alguna que otra se llevoacute el
premio de venir a muestrear y contar gente en esos interminables diacuteas de verano
Siempre os estareacute agradecida porque esta tesis es hoy tambieacuten gracias a vosotras Y
a Luciacutea y a Inma porque el ldquoea po nardquo puede ser y seraacute nuestro siempre
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
A Aerts K Vanagt T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-
Rodriguez MP Calderoacuten J Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-22
Brooks A R Purdy CN Bell SS Sulak KJ 2006 The benthic community of the eastern US continental shelf A literature synopsis of benthic faunal resources Continental Shelf Research 26 804-818
Anfuso E Ponce R Gonzaacutelez-Castro C Forja JM 2010 Coupling between the thermohaline chemical and biological fields during summer 2006 in the northeast continental shelf of the Gulf of Caacutediz (SW Iberian Peninsula) Scientia Marina 74 47 ndash 56
Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Bayed A 2003 Influence of morphodynamic and hidroclimatic factors on the macrofauna of
Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
Southern Brazil Brazilian Archives of Biology and Technology 44 351-364 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Colombini I Aloia A Fallaci M Pezzoli G Chelazzi L 2000 Temporal and spatial use of
stranded wrack by the macrofauna of a tropical sandy beach Marine Biology 136 531-541
Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
Conference on Engineering Dynamics in the Surf Zone (Sydney) 208-214 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1-12
Defeo O Jaramillo E Lyonnet A 1992 Community structure and intertidal zonation of the macroinfauna on the Atlantic coast of Uruguay Journal of Coastal Research 8 830-839
5 References
Capiacutetulo 2
54
Degraer S Volckaert A Vincx M 2003 Macrobenthic zonation patterns along a morphodynamical continuum of macrotidal low tide barrip and ultra-dissipative sandy beaches Estuarine Coastal and Shelf Science 56 459-468
Degraer S Mouton I De Neve L Vincx M 1999 Community structure and zonation of the macroinfauna on the Antlantic coast of Uruguay Journal of Coastal Research 8 830-839
Dexter DM 1983 Community structure of intertidal sandy beaches in New South Wales Australia In McLachlan A and T Erasmus (Eds) Sandy Beaches as Ecosystems The Hague Junk
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
G Gonccedilalves SC Anastaacutecio PM Pardal AM Cardoso PG Ferreira SM Marques JC
2009 Sandy beach macrofaunal communities on the western coast of Portugal ndashIs there a steady structure under similar exposed conditions Estuarine Coastal and Shelf Science 81 555-568
Guitian FJ Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de Compostela Espantildea
J Jaramillo E McLachlan A Coetzee P 1993 Intertidal zonation patterns of macroinfauna
over a range of exposed sandy beaches in south central Chile Marine Ecology Progress Series 101 105-118
Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
Jaramillo E Duarte C Contreras H 2000 Sandy beaches macroinfauna from the coast of Ancud Isla Chiloeacute southern Chile Revista Chilena de Historia Natural 73 771-786
L Lercari D Defeo O 2006 Large-scale diversity and abundance trends in sandy beach
macrofauna along full gradients of salinity and morphodynamics Estuarine Coastal and Shelf Science 68 27-35
M Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and
morphology a conceptual beach model Journal of Coastal Research 9 785-800 Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3 for Windows MjM Software Design Gleneden Beach Oregon
McEvoy EG Sundberg P 1993 Patterns of trace metal accumulation in Swedish marine nemerteans Hydrobiologia 226 273-280
Capiacutetulo 2
55
McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal sands Journal of Coastal Research 6 57-71
McLachlan A 1996 Physical factors in benthic ecology effects of changing sand particle size on beach fauna Marine Ecology Progress Series 131 205-217
McLachlan A Brown AC 2006 The ecology of sandy shores Elsevier Burlington McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities
Journal of Coastal Research 21 674-687 McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna
communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27-38
Munilla T San Vicente C 2005 Suprabenthic biodiversity of Catalan beaches (NW Mediterranean) Acta Oecologica 27 81-91
P
Papageorgiou N Arvanitidis C Eleftheriou A 2006 Multicausal environmental severity A flexible framework for microtidal sandy beaches and the role of polychaetes as an indicator taxon Estuarine Coastal and Shelf Science 70 643-653
Perez-Domingo S Castellanos C Junoy J2008 The sandy beach macrofauna of Gulf of Gabeacutes (Tunisia) Marine Ecology 29 51-59
Prieto L Garciacutea CM Corzo A Ruiz-Segura J Echevarriacutea F 1999 Phytoplankton bacterioplankton and nitrate reductase activity distribution in relation to physical structure in the northern Alboraacuten Sea and Gulf of Cadiz (southern Iberian Peninsula) Instituto Espantildeol de Oceanografiacutea 15 401-411
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodil IF Lastra M Loacutepez J 2007 Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain) Hidrobiologiacutea 579 301-316
Rodil IF Compton TJ Lastra M 2012 Exploring Macroinvertebrate Species distributions at Regional and Local Scales across a Sandy Beach Geographic Continuum PloS One (7) 6 e39609
Ruiz-Delgado MC Vieira JV Veloso VG Reyes-Martiacutenez MJ Azevedo IS Borzone CA Saacutechez-Moyano JE Garciacutea-Garciacutea FJ 2014 The role of wrack deposits for supralittoral arthropods An example using Atlantic sandy beaches of Brazil and Spain Estuarine Coastal and Shelf Science 136 61-71
S Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal
zonation metrics and their variability Marine Ecology Progress Series 478 43-55 Sobrino I Jimeacutenez MP Ramos F Baro J 1994 Descripcioacuten de las pesqueriacuteas demersales
de la Regioacuten Suratlaacutentica Espantildeola Instituto Espantildeol de Oceanografiacutea 151 3-79 Souza JR Borzone CA 2000 Population dynamics and secondary production of Scolelepis
squamata (Polychaeta Spionidae) in an exposed sandy beach of southern Brazil Bulletin of marine science 67 221-233
Speybroeck J Bonte D Courtens W Gheskiere T Grootaert P Maelfait JP Mathys M Provoost S Sabbe K Stienen EWM 2006 Beach nourishment an ecologically sound coastal defence alternative A review Aquatic Conservation Marine and Freshwater Ecosystems 16 419-435
Capiacutetulo 2
56
Speyboreck J Alsteens L Vincx M Degraer S 2007 Understanding the life of a sandy beach polychaete of functional importance - Scolelepis squamata (Polychaeta Spionidae) on Belgian sandy beaches (northeastern Atlantic North Sea) Estuarine Coastal and Shelf Science 74 109-118
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Ter Braak CJF 1995 Ordination In Jongman RHG ter Braak CJF van Tongeren OFR
(Eds) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge United Kingdom pp 91
Torres MA Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Caacutediz ecosystem (South-western Spain) Ecological Modelling 26 26-44
Trask PD 1950 Applied sedimentation Jon Wiley and Sons Inc New York
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349-357
V Veiga P Rubal M Cacauelos E Maldonado C Sousa-Pinto I 2014 Spatial variability of
macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
100
Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
101
3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
104
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
Sho
re b
ird
s
Pis
civo
rou
s b
ird
s
Eura
sia
n O
yste
rca
tch
er
Co
asta
l fis
h
Ba
thyp
ore
ia p
ela
gic
a
Cu
mo
psi
s fa
gei
Biv
alvi
a
De
cap
od
a
Dis
pio
un
cin
ata
Do
na
x tr
un
culu
s
Eury
dic
e a
ffin
is
Mys
ida
Gly
cera
tri
da
ctyl
a
Ha
uto
riu
s a
ren
ari
us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
Boos K Gutow L Mundry R Franke HD 2010 Sediment preference and burrowing behaviour in the sympatric brittlestars Ophiura albida Forbes 1839 and Ophiura ophiura (Linnaeus 1758) (Ophiuroidea Echinodermata) Journal of Experimental Marine Biology and Ecology 393 176ndash181
Brearey D M 1982 The feeding ecology and foraging behaviour of sanderline Calidris alba and turnstone Arenaria interpres at Teesmouth NEEngland Durham theses Dirham University
Brey T 2001 Population Dynamics in Benthic Invertebrates A virtual Handbook httpthomas-breydesciencevirtualhandbook
5 References
Capiacutetulo 4
116
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Byron C Link J Costa-Pierce B Bengston D 2011 Modeling ecological carrying capacity of shellfish aquaculture in highly flushed temperate lagoons Aquaculture 314 87ndash99
C Cammen LM 1980 Ingestion rate an empirical model for aquatic deposit feeders and
detritivores Oecologia 44 303-310 Chartosia N Kitsos MS Koukouras A 2010 Seasonal Diet of Portumnus Latipes (Pennat
1777) (Decopoda Portunidae) Crustaceana 83 1101-1113 Christensen V Pauly D 1992 ECOPATH II a software for balancing steady-state ecosystem
models and calculating network characteristics Ecological Modelling 61 169-185 Christensen V Pauly D 1995 Fish production catches and the carrying capacity of the
world oceans Naga 18 34-40 Christensen V Walters CJ 2004 ECOPATH with ECOSIM methods capabilities and
limitations Ecological Modelling 172 109-139 Christensen V Walters CJ Pauly D 2005 Ecopath with Ecosim a UserrsquosGuide November
2005 edition Fisheries Centre University of British ColumbiaVancouver Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide
November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
Coll M Palomera I Tudela S Sardagrave F 2006 Trophic flows ecosystem structure and fishing impacts in the South Catalan Sea Northwestern Mediterranean Journal of Marine Systems 59 63ndash96
Colleacuteter M Gascuel D Eucotin JM Morais L 2012 Modelling trophic flows in ecosystems to assess the efficiency of marine protected area (MPA) a case study on the coast of Seacuteneacutegal Ecological modeling 232 1-13
Colombini I Brilli M Fallaci M Gagnarli E Chelazzi L 2011 Food webs of sandy beach macroinvertebrate community using stable isotopes analysis Acta Oecologica 37 422-432
D Dauer DM Maybury CA Ewing RM 1981 Feeding behaviour and general ecology of
several spionid polychaetes from the Chesapeake Bay Journal of Experimental Marine Biology and Ecology 54 21-38
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beache macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman D Schlacher T Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1ndash12
Dennel R 1933 The habitats and feeding mechanism of the Amphipod Haustorius arenarius Slabber Journal of the Linnean Society of London Zoology 38 363-388
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan J Hubbard D McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58 133-148
Capiacutetulo 4
117
F Fabiano M Marin V Paoli C Vassallo P 2009 Methods for the sustainability evaluation
of coastal zone Journal of Mediterranean Ecology 10 5ndash11 Fanini L Cantarino CM F Scapini F 2005 Relationships between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fauchal K 1979 The diet of worms A study of polychaete feeding guilds Oceanography and Marine Biology An Annual Review 7 193-284
Field JG Wulff F Mann KH 1989 The need to analyse ecological networks In Wulff F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Coastal and Estuarine Studies Springer-Verlag Berlin 3ndash12
Freire J 1996 Feeding ecology of Liocarcinus depurator (Decapoda Portunidae) in the Riade Arousa (Galicia north-west Spain) effects of habitat season and life history Marine Biology 126 297-311
Froese R Pauly D 2012 FishBase World Wide Web Electronic Publication wwwfishbaseorg
G Gaedke U 1995 A comparison of whole-community and ecosystem approaches (biomass
size distributions food web analysis network analysis simulation models) to study the structure function and regulation of pelagic food webs Journal of Plankton Research 17 1273ndash1305
Guerra-Garciacutea JM Tierno de Figueroa JM Navarro-Barranco C Ros M Saacutenchez-Moyano JE Moreira J 2014 Dietary analysis of the marine Amphipods (Crustacea Peracarida) form the Iberian Peninsula Journal of Sea Research 85 508-517
H Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives
Proceedings of the Royal Society of London B 2701871-1878 Heppleston PB 1971 The feeding Ecology of Oystercatchers (Haematopus ostralegus L) in
winter in Northern Scotland Journal of Animal Ecology 40 651-672 Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a highenergy
beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585 Heymans JJ Ulanowicz RE Bondavalli C 2002 Network analysis of the South Florida
Everglades graminoid marshes and comparison with nearby cypress ecosystems Ecological Modelling 149 5-23
Holdich DM 1981 Opportunistic Feeding Behaviour in a Predatory Isopod Crustaceana 41 101-103
Hsing-Juh L Xiao-Xun D Kwang-Tsao S Huei-Meei S Wen-Tseng L Hwey-Lian H Lee-Shing F Jia-Jang H 2006 Trophic structure and functioning in a eutrophic and poorly flushed lagoon in southwestern Taiwan Marine Environmental Research 62 61ndash82
J Jones DA Pierpoint CJ 1997 Ecology and taxonomy of the genus Eurudice (Ispoda
Cirolanidae) form sand beaches on the Iberian Peninsula Journal of the Marine Biological Association of the United Kingdom 77 55-76
Capiacutetulo 4
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K Kay JJ Graham LA Ulanowicz RE 1989 A detailed guide to network analysis In Wulff
F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Springer Berlin 32 15ndash61
Knox GA 2001 The ecology of seashores CRC Press Boca Raton Florida USA
L Leguerrier D Degreacute D Niquil N 2007 Network analysis and inter-ecosystem comparison
of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove SW France) Estuarine Coastal and Shelf Science 74 403-418
Lercari D Defeo O 2003 Variation of a sandy beach macrobenthic community along a human-induced environmental gradient Estuarine Coastal and Shelf Science 58S 17ndash24
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lewis L Bodegom P Rozema J Janssen G 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172ndash181
Libralato S Coll M Tempesta M Santojanni A Spoto M Palomera I Arneri E Solidoro C 2010 Food-web traits of protected and exploited areas of the Adriatic Sea Biological Conservation 143 2182ndash2194
Lindeman RL 1942 The trophic-dynamic aspect of ecology Ecology 23 399ndash418
M Marcstroumlm V Mascher JW 1979 Weights and fat in Lapwings Vanellus vanellus and
Oystercatchers Haematopus ostralegus starved to death during a cold spell in spring Ornis Scandinavica 10 235-240
Mcdermott JJ Roe P 1985 Food Feeding Behaviour and Feeding Ecology of Nemerteans American Zoologist 25 113-125
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Coastal Management 71 256-368
Moreira F 1995 The winter feeding ecology of Avocets Recuvirostra avosetta on intertidal areas II Diet and feeding mechanisms Ibis 137 99-108
N Navarro-Barranco C Tierno-de-Figueroa JM Guerra-Garciacutea JM Saacutenchez-Tocino L and
Garciacutea-Goacutemez JC 2013 Feeding habits of amphipods (Crustacea Malacostraca) from shallow soft bottom communities Comparison between marine caves and open habitats Journal of Sea Research 78 1-7
Nilsson SG Nilsson IN 1976 Numbers food consumption and fish predation by birds in Lake Moacuteckeln southern Sweden Ornis Scandinavica 7 61-70
O Odum HT 1969 The strategy of ecosystem development Science 164 262-270 Odum E 1971 Fundamentals of ecology Philadelphia Saunders
Capiacutetulo 4
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Ortiz M Wolff M 2002 Trophic model of four benthic communities in Tongoy Bay (Chile) comparative analysis and preliminary assessment of management strategies Journal of Experimental Marine Biology and Ecology 268 205ndash235
P Parsons T Maila Y Lalli C 1984 A Manual of Chemical and Biological Methods for
Seawater Analysis Pergamon Patriacutecio J Ulanowicz RE Pardal MA Marques JC 2004 Ascendency as an ecological
indicator a case study of estuarine pulse eutrophication Estuarine Coastal and Shelf Science 60 23-35
Patriacutecio J Marques JC 2006 Mass balanced models of the food web in three areas along a gradient of eutrophication symptoms in the south arm of the Mondego estuary (Portugal) Ecological modelling 197 21ndash34
Peacuterez-Hurtado A Goss-Custard JD Garciacutea F 1997 The diet of wintering waders in Caacutediz Bay southwest Spain Bird study 44 45-52
Phong LT Dam AA Udo HMJ Mensvoort MEF Tri LQ Steenstra FA Zijpp AJ 2010 An agro-ecological evaluation of aquaculture integration into farming systems of the Mekong Delta Agriculture Ecosystems and Environment 138 232ndash241
Poppe GT Goto Y 1993 European Seashells Vol II (Scaphopoda Bivalvia Cephalopoda) Verlag Christa Hemmen Wiesbaden Germany
R Rosado-Soloacuterzano R Guzman del Proo S 1998 Preliminary trophic structure model for
Tampamachoco lagoon Veracruz Mexico Ecological Modelling 109 141ndash154
S San Vicente C Sorbe JC 1993 Biologie du Mysidaceacute suprabenthique Schistomysis parkeri
Norman 1892 dans la zone sud du Golfe de Gascogne (Plage dHendaye) Crustaceana 65 222-252
Scapini F 2003 Beaches ndash What Future An integrated approach to the ecology of sandy beaches (Editorial) Estuarine Coastal and Shelf Science 58S 1-3
Selleslagh J Lobry J Amara R Brylinski JM Boeumlt P 2013 Trophic functioning of coastal ecosystems along an anthropogenic pressure gradient A French case study with emphasis on a small and low impacted estuary Estuarine Coastal and Shelf Science 112 73-85
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Richardson D McLean I 2008 Impacts of off-road vehicles (ORVs) on macrobenthic assemblages on sandy beaches Environmental Management 41 878ndash892
T Theilacker GH Kimball AS 1984 Rotifers and copepods as larval fish foods California
Cooperative Oceanic Fisheries Investigations XXV 80-84 Torrecilla-Roca I Guerra-Garciacutea JM 2012 Fedding habits of the peracarid crustaceans
associated to the alga Fucus spiralis in Tarifa Island Caacutediz (Southern Spain) Zoologia baetica 23 39-47
Torres M Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Cadiz ecosystem (South-western Spain) Ecological Modelling 265 26ndash 44
Capiacutetulo 4
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Turpie JK Hockey PAR 1997 Adaptative variation in the foraging behaviour of Grey Plover Pluvialis squatarola and Whimbrel Numenius pheopus Ibis 139 289-298
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Ulanovick RE 1984Community measures of marine food networks and their possible applications Fashman MJR (ed) Flows of energy and materials in marine ecosystems Plenum Press New York 23-47
Ulanowicz R E 1986 Growth and Development Ecosystem Phenology Springer-Verlag New York 203
Ulanowicz RE Puccia CJ 1990 Mixed trophic impact in ecosystems Coenoses 5 7-16
V Vasallo P Paoili C Fabiano M 2012 Ecosystem level analysis of sandy beaches using
thermodynamic and network analyses A study case in the NW Mediterranean Sea Ecological Indicators 15 10ndash17
Vega-Cendejas ME Arreguiacuten-Saacutenchez F Hernaacutendez M 1993 Trophic fluxes on the Campeche Bank Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 206-213
Veloso VG Silva ES Caetano CHS Cardoso R 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510ndash515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Villanueva MC Lalegraveyegrave P Albaret JJ Laeuml R Tito de Morais L Moreau J 2006 Comparative analysis of trophic structure and interactions of two tropical lagoons Ecological Modelling 197 461-477
Vinebrooke RD Cottingham KL Norberg J 2004 Implications of multiple stressors on biodiversity and ecosystem functioning the role of species co-tolerance Oikos 104 451-457
Y Yang Y Chen H Yang Z 2010 Assessing changes of trophic interactions during once
anthropogenic water supplement in Baiyangdian Lake Procedia Environmental Sciences 2 1169ndash1179
Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
Capiacutetulo 6
153
2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
6
7
8
9
10
11
12
Capiacutetulo 8
184
esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
13
14
15
16
185
ESTRUCTURAS DE LAS COMUNIDADES Y ZONACIOacuteN DE LA
MACROFAUNA EN PLAYAS ARENOSAS DE ANDALUCIacuteA
OCCIDENTAL EFECTO DE LA ACTIVIDAD HUMANA SOBRE LAS
COMUNIDADES INTERMAREALES
Mordf Joseacute Reyes Martiacutenez
Tesis Doctoral
Sevilla Diciembre 2014
Francisco Joseacute Garciacutea Garciacutea Catedraacutetico de Zoologiacutea del Departamento de
Sistemas Fiacutesicos Quiacutemicos y Naturales de la Universidad Pablo de Olavide y
Juan Emilio Saacutenchez Moyano Profesor Titular del Departamento de Zoologiacutea
de la Universidad de Sevilla
CERTIFICAN
Que la presente memoria titulada ldquoEstructura de las comunidades y
zonacioacuten de la macrofauna en playas arenosas de Andaluciacutea Occidental
Efecto de la actividad humana sobre las comunidades intermarealesrdquo
presentada por Mordf Joseacute Reyes Martiacutenez para optar al Grado de Doctora por la
Universidad Pablo de Olavide ha sido realizada bajo su direccioacuten y autorizan
su presentacioacuten y defensa
Y para que asiacute conste expiden y firman la presente certificacioacuten en Sevilla a 3
de Diciembre de 2014
Dr D Francisco Joseacute Garciacutea Garciacutea Dr D Juan Emilio Saacutenchez Moyano
Agradecimientos
Y llegoacute el inesperado momento de los agradecimientos Tengo a tantas personas a las
que agradecer que espero no extenderme mucho
En primer lugar quiero dar las gracias a mis directores a Paco y a Emilio por la
confianza depositada en mi para la realizacioacuten de esta Tesis que todaviacutea no me creo
que haya terminado Hoy tengo sentimientos contradictorios por un lado alegriacutea y
satisfaccioacuten personal por haberlo logrado pero por otro no puedo dejar de sentir
cierta nostalgia porque esta etapa haya llegado a su fin Gracias a Paco por
escucharme cuando llamaba a su puerta diciendo ldquoTengo un problemardquo por la
incalculable ayuda prestada durante todo este tiempo y por los consejos ofrecidos en
los tiacutepicos momentos de crisis existencial Esta crisis tambieacuten se extendioacute al para mi
tenebroso mundo de la estadiacutestica en el que Emilio siempre lograba sacar luz Me
llevo guardados grandes momentos con vosotros no puedo evitar sonreiacuter al
acordarme de nuestros muestreos en los que sin quererlo poniacuteamos a prueba nuestra
integridad fiacutesica y como no emocional Hasta en alguna ocasioacuten recuerdo que casi
conseguimos traernos toda la arena de la playahellip iquestpero que no arreglaba nuestra
tortilla y quesito del descanso aunque fuera prefabricada en ese momento era gloria
Hay tantos momentos que no seriacutea posible describirlos todos Lo que si es cierto es
que hoy veo las playas desde una manera diferente y es gracias a vosotros
Carmen te llegoacute el momento Nos conocimos hace mucho tiempo y el destino quiso
que de nuevo emprendieacuteramos este camino juntas Gracias por tu gran ayuda en los
muestreos por las horas y horas compartidas en el laboratorio en el que nuestras
charlas haciacutean mucho maacutes ameno el paso del tiempo perdidas entre las muestras en
busca de nuestro tesoro particular los bichitos rositas Gracias por las charlas
constructivas y por ayudarme en los momentos que los que estaba maacutes que peacuterdida
No puedo olvidarme de todas aquellas personas que sin conocerme me abrieron las
puertas de sus laboratorios y de las que he aprendido cosas de incalculable valor
Todas esas estancias han sido clave para mi y para que esta tesis haya salido adelante
Gracias a Francesca Rossi que fue la primera en ldquoacogermerdquo cuando auacuten casi no habiacutea
salido del cascaroacuten aprendiacute mucho de aquella experiencia a Valeria Veloso y a Carlos
Borzone por la inmejorable estancia en Brasil y por todos sus consejos Gracias a Diego
Lercari por ensentildearme a ver las playas desde una perspectiva diferente por toda su
dedicacioacuten y especialmente por su paciencia gran parte de esta tesis ha sido gracias a
ti Gracias a todas las ldquomeninasrdquo del laboratorio de Pontal y como olvidarme del equipo
Undecimar gracias chicos haceacuteis que estaacutes estancias merezcan doblemente la pena
Es momento de agradecer a todas esas personas que me han ayudado en los
muestreos poniendo su granito de arena (y nunca mejor dicho) en esta tesis Tambieacuten
a todo el personal del Parque de los Toruntildeos por sus facilidades y gran ayuda durante
los muestreos y a los organismos puacuteblicos que han financiado tanto esta tesis (Junta
de Andaluciacutea a traveacutes de sus Proyectos de Excelencia) como las estancias disfrutadas
(Universidad Pablo de Olavide y AUIP)
Quiero agradecer tambieacuten a mi familia a mis hermanas y en especial a mis padres a
quieacuten hoy dedico esta tesis por todo el apoyo prestado durante este tiempo Siempre
habeacuteis confiado en mi aunque al principio no entendierais del todo bien mi diversioacuten
por ir a sacar kilos y kilos de arena de las playas Siempre me habeacuteis animado a seguir
mis suentildeos por muy alocados que fueran os habeacuteis sentido orgullosos y me habeacuteis
hecho creer que podiacutea conseguir todo lo que me propusiera y que esto era ldquopan
comidordquo
Gracias a Aacutelvaro mi gran pilar y sustento Tu eres de todos el que maacutes ha vivido esto
gracias por ser capaz de sacar siempre el lado bueno de las cosas y por el ldquoiquestQueacute no
sale hoy No te preocupes mantildeana seraacute otro diacuteardquo Siempre has confiado en mi incluso
cuando yo no era capaz de hacerlo Gracias por no cansarte de animarme incluso
cuando este trabajo se convertiacutea en lo primero me has acompantildeado en muchas de mis
aventuras playeras y has disfrutado y celebrado como nadie cuando llegaban buenas
noticias Se que tambieacuten para ti hoy las playas son algo maacutes y eso me enorgullece
Hasta vamos a las playas cargados con bolsitas por si nos encontramos alguacuten bichito
que recoger para el laboratorio iquestquieacuten nos lo habraacute pegado
Y por uacuteltimo a mis nintildeas gracias a Inma a Luciacutea y a Aacutengeles por los aacutenimos en los
momentos de flaqueza por las charlas constructivas por esas visitas sorpresa y salidas
ldquoobligadasrdquo para olvidarnos de todo Gracias por entenderme por aceptar aunque
fuera a regantildeadientes que no pudiera estar en todos los momentos porque el deber
me llamabahellip y por celebrar las alegriacuteas y como no los fracasos como solo nosotras
sabemos hacerlo Me habeacuteis valorado como nadie incluso alguna que otra se llevoacute el
premio de venir a muestrear y contar gente en esos interminables diacuteas de verano
Siempre os estareacute agradecida porque esta tesis es hoy tambieacuten gracias a vosotras Y
a Luciacutea y a Inma porque el ldquoea po nardquo puede ser y seraacute nuestro siempre
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
A Aerts K Vanagt T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-
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Brooks A R Purdy CN Bell SS Sulak KJ 2006 The benthic community of the eastern US continental shelf A literature synopsis of benthic faunal resources Continental Shelf Research 26 804-818
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Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
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Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
Southern Brazil Brazilian Archives of Biology and Technology 44 351-364 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Colombini I Aloia A Fallaci M Pezzoli G Chelazzi L 2000 Temporal and spatial use of
stranded wrack by the macrofauna of a tropical sandy beach Marine Biology 136 531-541
Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
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D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
Conference on Engineering Dynamics in the Surf Zone (Sydney) 208-214 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1-12
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Capiacutetulo 2
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E Emery KO 1961 A simple method of measuring beach profiles Limnology and
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Capiacutetulo 2
55
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Munilla T San Vicente C 2005 Suprabenthic biodiversity of Catalan beaches (NW Mediterranean) Acta Oecologica 27 81-91
P
Papageorgiou N Arvanitidis C Eleftheriou A 2006 Multicausal environmental severity A flexible framework for microtidal sandy beaches and the role of polychaetes as an indicator taxon Estuarine Coastal and Shelf Science 70 643-653
Perez-Domingo S Castellanos C Junoy J2008 The sandy beach macrofauna of Gulf of Gabeacutes (Tunisia) Marine Ecology 29 51-59
Prieto L Garciacutea CM Corzo A Ruiz-Segura J Echevarriacutea F 1999 Phytoplankton bacterioplankton and nitrate reductase activity distribution in relation to physical structure in the northern Alboraacuten Sea and Gulf of Cadiz (southern Iberian Peninsula) Instituto Espantildeol de Oceanografiacutea 15 401-411
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodil IF Lastra M Loacutepez J 2007 Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain) Hidrobiologiacutea 579 301-316
Rodil IF Compton TJ Lastra M 2012 Exploring Macroinvertebrate Species distributions at Regional and Local Scales across a Sandy Beach Geographic Continuum PloS One (7) 6 e39609
Ruiz-Delgado MC Vieira JV Veloso VG Reyes-Martiacutenez MJ Azevedo IS Borzone CA Saacutechez-Moyano JE Garciacutea-Garciacutea FJ 2014 The role of wrack deposits for supralittoral arthropods An example using Atlantic sandy beaches of Brazil and Spain Estuarine Coastal and Shelf Science 136 61-71
S Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal
zonation metrics and their variability Marine Ecology Progress Series 478 43-55 Sobrino I Jimeacutenez MP Ramos F Baro J 1994 Descripcioacuten de las pesqueriacuteas demersales
de la Regioacuten Suratlaacutentica Espantildeola Instituto Espantildeol de Oceanografiacutea 151 3-79 Souza JR Borzone CA 2000 Population dynamics and secondary production of Scolelepis
squamata (Polychaeta Spionidae) in an exposed sandy beach of southern Brazil Bulletin of marine science 67 221-233
Speybroeck J Bonte D Courtens W Gheskiere T Grootaert P Maelfait JP Mathys M Provoost S Sabbe K Stienen EWM 2006 Beach nourishment an ecologically sound coastal defence alternative A review Aquatic Conservation Marine and Freshwater Ecosystems 16 419-435
Capiacutetulo 2
56
Speyboreck J Alsteens L Vincx M Degraer S 2007 Understanding the life of a sandy beach polychaete of functional importance - Scolelepis squamata (Polychaeta Spionidae) on Belgian sandy beaches (northeastern Atlantic North Sea) Estuarine Coastal and Shelf Science 74 109-118
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Ter Braak CJF 1995 Ordination In Jongman RHG ter Braak CJF van Tongeren OFR
(Eds) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge United Kingdom pp 91
Torres MA Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Caacutediz ecosystem (South-western Spain) Ecological Modelling 26 26-44
Trask PD 1950 Applied sedimentation Jon Wiley and Sons Inc New York
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349-357
V Veiga P Rubal M Cacauelos E Maldonado C Sousa-Pinto I 2014 Spatial variability of
macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
100
Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
101
3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
104
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
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us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
Boos K Gutow L Mundry R Franke HD 2010 Sediment preference and burrowing behaviour in the sympatric brittlestars Ophiura albida Forbes 1839 and Ophiura ophiura (Linnaeus 1758) (Ophiuroidea Echinodermata) Journal of Experimental Marine Biology and Ecology 393 176ndash181
Brearey D M 1982 The feeding ecology and foraging behaviour of sanderline Calidris alba and turnstone Arenaria interpres at Teesmouth NEEngland Durham theses Dirham University
Brey T 2001 Population Dynamics in Benthic Invertebrates A virtual Handbook httpthomas-breydesciencevirtualhandbook
5 References
Capiacutetulo 4
116
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
Byron C Link J Costa-Pierce B Bengston D 2011 Modeling ecological carrying capacity of shellfish aquaculture in highly flushed temperate lagoons Aquaculture 314 87ndash99
C Cammen LM 1980 Ingestion rate an empirical model for aquatic deposit feeders and
detritivores Oecologia 44 303-310 Chartosia N Kitsos MS Koukouras A 2010 Seasonal Diet of Portumnus Latipes (Pennat
1777) (Decopoda Portunidae) Crustaceana 83 1101-1113 Christensen V Pauly D 1992 ECOPATH II a software for balancing steady-state ecosystem
models and calculating network characteristics Ecological Modelling 61 169-185 Christensen V Pauly D 1995 Fish production catches and the carrying capacity of the
world oceans Naga 18 34-40 Christensen V Walters CJ 2004 ECOPATH with ECOSIM methods capabilities and
limitations Ecological Modelling 172 109-139 Christensen V Walters CJ Pauly D 2005 Ecopath with Ecosim a UserrsquosGuide November
2005 edition Fisheries Centre University of British ColumbiaVancouver Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide
November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
Coll M Palomera I Tudela S Sardagrave F 2006 Trophic flows ecosystem structure and fishing impacts in the South Catalan Sea Northwestern Mediterranean Journal of Marine Systems 59 63ndash96
Colleacuteter M Gascuel D Eucotin JM Morais L 2012 Modelling trophic flows in ecosystems to assess the efficiency of marine protected area (MPA) a case study on the coast of Seacuteneacutegal Ecological modeling 232 1-13
Colombini I Brilli M Fallaci M Gagnarli E Chelazzi L 2011 Food webs of sandy beach macroinvertebrate community using stable isotopes analysis Acta Oecologica 37 422-432
D Dauer DM Maybury CA Ewing RM 1981 Feeding behaviour and general ecology of
several spionid polychaetes from the Chesapeake Bay Journal of Experimental Marine Biology and Ecology 54 21-38
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beache macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman D Schlacher T Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1ndash12
Dennel R 1933 The habitats and feeding mechanism of the Amphipod Haustorius arenarius Slabber Journal of the Linnean Society of London Zoology 38 363-388
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan J Hubbard D McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58 133-148
Capiacutetulo 4
117
F Fabiano M Marin V Paoli C Vassallo P 2009 Methods for the sustainability evaluation
of coastal zone Journal of Mediterranean Ecology 10 5ndash11 Fanini L Cantarino CM F Scapini F 2005 Relationships between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fauchal K 1979 The diet of worms A study of polychaete feeding guilds Oceanography and Marine Biology An Annual Review 7 193-284
Field JG Wulff F Mann KH 1989 The need to analyse ecological networks In Wulff F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Coastal and Estuarine Studies Springer-Verlag Berlin 3ndash12
Freire J 1996 Feeding ecology of Liocarcinus depurator (Decapoda Portunidae) in the Riade Arousa (Galicia north-west Spain) effects of habitat season and life history Marine Biology 126 297-311
Froese R Pauly D 2012 FishBase World Wide Web Electronic Publication wwwfishbaseorg
G Gaedke U 1995 A comparison of whole-community and ecosystem approaches (biomass
size distributions food web analysis network analysis simulation models) to study the structure function and regulation of pelagic food webs Journal of Plankton Research 17 1273ndash1305
Guerra-Garciacutea JM Tierno de Figueroa JM Navarro-Barranco C Ros M Saacutenchez-Moyano JE Moreira J 2014 Dietary analysis of the marine Amphipods (Crustacea Peracarida) form the Iberian Peninsula Journal of Sea Research 85 508-517
H Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives
Proceedings of the Royal Society of London B 2701871-1878 Heppleston PB 1971 The feeding Ecology of Oystercatchers (Haematopus ostralegus L) in
winter in Northern Scotland Journal of Animal Ecology 40 651-672 Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a highenergy
beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585 Heymans JJ Ulanowicz RE Bondavalli C 2002 Network analysis of the South Florida
Everglades graminoid marshes and comparison with nearby cypress ecosystems Ecological Modelling 149 5-23
Holdich DM 1981 Opportunistic Feeding Behaviour in a Predatory Isopod Crustaceana 41 101-103
Hsing-Juh L Xiao-Xun D Kwang-Tsao S Huei-Meei S Wen-Tseng L Hwey-Lian H Lee-Shing F Jia-Jang H 2006 Trophic structure and functioning in a eutrophic and poorly flushed lagoon in southwestern Taiwan Marine Environmental Research 62 61ndash82
J Jones DA Pierpoint CJ 1997 Ecology and taxonomy of the genus Eurudice (Ispoda
Cirolanidae) form sand beaches on the Iberian Peninsula Journal of the Marine Biological Association of the United Kingdom 77 55-76
Capiacutetulo 4
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K Kay JJ Graham LA Ulanowicz RE 1989 A detailed guide to network analysis In Wulff
F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Springer Berlin 32 15ndash61
Knox GA 2001 The ecology of seashores CRC Press Boca Raton Florida USA
L Leguerrier D Degreacute D Niquil N 2007 Network analysis and inter-ecosystem comparison
of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove SW France) Estuarine Coastal and Shelf Science 74 403-418
Lercari D Defeo O 2003 Variation of a sandy beach macrobenthic community along a human-induced environmental gradient Estuarine Coastal and Shelf Science 58S 17ndash24
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lewis L Bodegom P Rozema J Janssen G 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172ndash181
Libralato S Coll M Tempesta M Santojanni A Spoto M Palomera I Arneri E Solidoro C 2010 Food-web traits of protected and exploited areas of the Adriatic Sea Biological Conservation 143 2182ndash2194
Lindeman RL 1942 The trophic-dynamic aspect of ecology Ecology 23 399ndash418
M Marcstroumlm V Mascher JW 1979 Weights and fat in Lapwings Vanellus vanellus and
Oystercatchers Haematopus ostralegus starved to death during a cold spell in spring Ornis Scandinavica 10 235-240
Mcdermott JJ Roe P 1985 Food Feeding Behaviour and Feeding Ecology of Nemerteans American Zoologist 25 113-125
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Coastal Management 71 256-368
Moreira F 1995 The winter feeding ecology of Avocets Recuvirostra avosetta on intertidal areas II Diet and feeding mechanisms Ibis 137 99-108
N Navarro-Barranco C Tierno-de-Figueroa JM Guerra-Garciacutea JM Saacutenchez-Tocino L and
Garciacutea-Goacutemez JC 2013 Feeding habits of amphipods (Crustacea Malacostraca) from shallow soft bottom communities Comparison between marine caves and open habitats Journal of Sea Research 78 1-7
Nilsson SG Nilsson IN 1976 Numbers food consumption and fish predation by birds in Lake Moacuteckeln southern Sweden Ornis Scandinavica 7 61-70
O Odum HT 1969 The strategy of ecosystem development Science 164 262-270 Odum E 1971 Fundamentals of ecology Philadelphia Saunders
Capiacutetulo 4
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Ortiz M Wolff M 2002 Trophic model of four benthic communities in Tongoy Bay (Chile) comparative analysis and preliminary assessment of management strategies Journal of Experimental Marine Biology and Ecology 268 205ndash235
P Parsons T Maila Y Lalli C 1984 A Manual of Chemical and Biological Methods for
Seawater Analysis Pergamon Patriacutecio J Ulanowicz RE Pardal MA Marques JC 2004 Ascendency as an ecological
indicator a case study of estuarine pulse eutrophication Estuarine Coastal and Shelf Science 60 23-35
Patriacutecio J Marques JC 2006 Mass balanced models of the food web in three areas along a gradient of eutrophication symptoms in the south arm of the Mondego estuary (Portugal) Ecological modelling 197 21ndash34
Peacuterez-Hurtado A Goss-Custard JD Garciacutea F 1997 The diet of wintering waders in Caacutediz Bay southwest Spain Bird study 44 45-52
Phong LT Dam AA Udo HMJ Mensvoort MEF Tri LQ Steenstra FA Zijpp AJ 2010 An agro-ecological evaluation of aquaculture integration into farming systems of the Mekong Delta Agriculture Ecosystems and Environment 138 232ndash241
Poppe GT Goto Y 1993 European Seashells Vol II (Scaphopoda Bivalvia Cephalopoda) Verlag Christa Hemmen Wiesbaden Germany
R Rosado-Soloacuterzano R Guzman del Proo S 1998 Preliminary trophic structure model for
Tampamachoco lagoon Veracruz Mexico Ecological Modelling 109 141ndash154
S San Vicente C Sorbe JC 1993 Biologie du Mysidaceacute suprabenthique Schistomysis parkeri
Norman 1892 dans la zone sud du Golfe de Gascogne (Plage dHendaye) Crustaceana 65 222-252
Scapini F 2003 Beaches ndash What Future An integrated approach to the ecology of sandy beaches (Editorial) Estuarine Coastal and Shelf Science 58S 1-3
Selleslagh J Lobry J Amara R Brylinski JM Boeumlt P 2013 Trophic functioning of coastal ecosystems along an anthropogenic pressure gradient A French case study with emphasis on a small and low impacted estuary Estuarine Coastal and Shelf Science 112 73-85
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Richardson D McLean I 2008 Impacts of off-road vehicles (ORVs) on macrobenthic assemblages on sandy beaches Environmental Management 41 878ndash892
T Theilacker GH Kimball AS 1984 Rotifers and copepods as larval fish foods California
Cooperative Oceanic Fisheries Investigations XXV 80-84 Torrecilla-Roca I Guerra-Garciacutea JM 2012 Fedding habits of the peracarid crustaceans
associated to the alga Fucus spiralis in Tarifa Island Caacutediz (Southern Spain) Zoologia baetica 23 39-47
Torres M Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Cadiz ecosystem (South-western Spain) Ecological Modelling 265 26ndash 44
Capiacutetulo 4
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Turpie JK Hockey PAR 1997 Adaptative variation in the foraging behaviour of Grey Plover Pluvialis squatarola and Whimbrel Numenius pheopus Ibis 139 289-298
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Ulanovick RE 1984Community measures of marine food networks and their possible applications Fashman MJR (ed) Flows of energy and materials in marine ecosystems Plenum Press New York 23-47
Ulanowicz R E 1986 Growth and Development Ecosystem Phenology Springer-Verlag New York 203
Ulanowicz RE Puccia CJ 1990 Mixed trophic impact in ecosystems Coenoses 5 7-16
V Vasallo P Paoili C Fabiano M 2012 Ecosystem level analysis of sandy beaches using
thermodynamic and network analyses A study case in the NW Mediterranean Sea Ecological Indicators 15 10ndash17
Vega-Cendejas ME Arreguiacuten-Saacutenchez F Hernaacutendez M 1993 Trophic fluxes on the Campeche Bank Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 206-213
Veloso VG Silva ES Caetano CHS Cardoso R 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510ndash515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Villanueva MC Lalegraveyegrave P Albaret JJ Laeuml R Tito de Morais L Moreau J 2006 Comparative analysis of trophic structure and interactions of two tropical lagoons Ecological Modelling 197 461-477
Vinebrooke RD Cottingham KL Norberg J 2004 Implications of multiple stressors on biodiversity and ecosystem functioning the role of species co-tolerance Oikos 104 451-457
Y Yang Y Chen H Yang Z 2010 Assessing changes of trophic interactions during once
anthropogenic water supplement in Baiyangdian Lake Procedia Environmental Sciences 2 1169ndash1179
Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
Capiacutetulo 6
153
2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
6
7
8
9
10
11
12
Capiacutetulo 8
184
esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
13
14
15
16
185
Francisco Joseacute Garciacutea Garciacutea Catedraacutetico de Zoologiacutea del Departamento de
Sistemas Fiacutesicos Quiacutemicos y Naturales de la Universidad Pablo de Olavide y
Juan Emilio Saacutenchez Moyano Profesor Titular del Departamento de Zoologiacutea
de la Universidad de Sevilla
CERTIFICAN
Que la presente memoria titulada ldquoEstructura de las comunidades y
zonacioacuten de la macrofauna en playas arenosas de Andaluciacutea Occidental
Efecto de la actividad humana sobre las comunidades intermarealesrdquo
presentada por Mordf Joseacute Reyes Martiacutenez para optar al Grado de Doctora por la
Universidad Pablo de Olavide ha sido realizada bajo su direccioacuten y autorizan
su presentacioacuten y defensa
Y para que asiacute conste expiden y firman la presente certificacioacuten en Sevilla a 3
de Diciembre de 2014
Dr D Francisco Joseacute Garciacutea Garciacutea Dr D Juan Emilio Saacutenchez Moyano
Agradecimientos
Y llegoacute el inesperado momento de los agradecimientos Tengo a tantas personas a las
que agradecer que espero no extenderme mucho
En primer lugar quiero dar las gracias a mis directores a Paco y a Emilio por la
confianza depositada en mi para la realizacioacuten de esta Tesis que todaviacutea no me creo
que haya terminado Hoy tengo sentimientos contradictorios por un lado alegriacutea y
satisfaccioacuten personal por haberlo logrado pero por otro no puedo dejar de sentir
cierta nostalgia porque esta etapa haya llegado a su fin Gracias a Paco por
escucharme cuando llamaba a su puerta diciendo ldquoTengo un problemardquo por la
incalculable ayuda prestada durante todo este tiempo y por los consejos ofrecidos en
los tiacutepicos momentos de crisis existencial Esta crisis tambieacuten se extendioacute al para mi
tenebroso mundo de la estadiacutestica en el que Emilio siempre lograba sacar luz Me
llevo guardados grandes momentos con vosotros no puedo evitar sonreiacuter al
acordarme de nuestros muestreos en los que sin quererlo poniacuteamos a prueba nuestra
integridad fiacutesica y como no emocional Hasta en alguna ocasioacuten recuerdo que casi
conseguimos traernos toda la arena de la playahellip iquestpero que no arreglaba nuestra
tortilla y quesito del descanso aunque fuera prefabricada en ese momento era gloria
Hay tantos momentos que no seriacutea posible describirlos todos Lo que si es cierto es
que hoy veo las playas desde una manera diferente y es gracias a vosotros
Carmen te llegoacute el momento Nos conocimos hace mucho tiempo y el destino quiso
que de nuevo emprendieacuteramos este camino juntas Gracias por tu gran ayuda en los
muestreos por las horas y horas compartidas en el laboratorio en el que nuestras
charlas haciacutean mucho maacutes ameno el paso del tiempo perdidas entre las muestras en
busca de nuestro tesoro particular los bichitos rositas Gracias por las charlas
constructivas y por ayudarme en los momentos que los que estaba maacutes que peacuterdida
No puedo olvidarme de todas aquellas personas que sin conocerme me abrieron las
puertas de sus laboratorios y de las que he aprendido cosas de incalculable valor
Todas esas estancias han sido clave para mi y para que esta tesis haya salido adelante
Gracias a Francesca Rossi que fue la primera en ldquoacogermerdquo cuando auacuten casi no habiacutea
salido del cascaroacuten aprendiacute mucho de aquella experiencia a Valeria Veloso y a Carlos
Borzone por la inmejorable estancia en Brasil y por todos sus consejos Gracias a Diego
Lercari por ensentildearme a ver las playas desde una perspectiva diferente por toda su
dedicacioacuten y especialmente por su paciencia gran parte de esta tesis ha sido gracias a
ti Gracias a todas las ldquomeninasrdquo del laboratorio de Pontal y como olvidarme del equipo
Undecimar gracias chicos haceacuteis que estaacutes estancias merezcan doblemente la pena
Es momento de agradecer a todas esas personas que me han ayudado en los
muestreos poniendo su granito de arena (y nunca mejor dicho) en esta tesis Tambieacuten
a todo el personal del Parque de los Toruntildeos por sus facilidades y gran ayuda durante
los muestreos y a los organismos puacuteblicos que han financiado tanto esta tesis (Junta
de Andaluciacutea a traveacutes de sus Proyectos de Excelencia) como las estancias disfrutadas
(Universidad Pablo de Olavide y AUIP)
Quiero agradecer tambieacuten a mi familia a mis hermanas y en especial a mis padres a
quieacuten hoy dedico esta tesis por todo el apoyo prestado durante este tiempo Siempre
habeacuteis confiado en mi aunque al principio no entendierais del todo bien mi diversioacuten
por ir a sacar kilos y kilos de arena de las playas Siempre me habeacuteis animado a seguir
mis suentildeos por muy alocados que fueran os habeacuteis sentido orgullosos y me habeacuteis
hecho creer que podiacutea conseguir todo lo que me propusiera y que esto era ldquopan
comidordquo
Gracias a Aacutelvaro mi gran pilar y sustento Tu eres de todos el que maacutes ha vivido esto
gracias por ser capaz de sacar siempre el lado bueno de las cosas y por el ldquoiquestQueacute no
sale hoy No te preocupes mantildeana seraacute otro diacuteardquo Siempre has confiado en mi incluso
cuando yo no era capaz de hacerlo Gracias por no cansarte de animarme incluso
cuando este trabajo se convertiacutea en lo primero me has acompantildeado en muchas de mis
aventuras playeras y has disfrutado y celebrado como nadie cuando llegaban buenas
noticias Se que tambieacuten para ti hoy las playas son algo maacutes y eso me enorgullece
Hasta vamos a las playas cargados con bolsitas por si nos encontramos alguacuten bichito
que recoger para el laboratorio iquestquieacuten nos lo habraacute pegado
Y por uacuteltimo a mis nintildeas gracias a Inma a Luciacutea y a Aacutengeles por los aacutenimos en los
momentos de flaqueza por las charlas constructivas por esas visitas sorpresa y salidas
ldquoobligadasrdquo para olvidarnos de todo Gracias por entenderme por aceptar aunque
fuera a regantildeadientes que no pudiera estar en todos los momentos porque el deber
me llamabahellip y por celebrar las alegriacuteas y como no los fracasos como solo nosotras
sabemos hacerlo Me habeacuteis valorado como nadie incluso alguna que otra se llevoacute el
premio de venir a muestrear y contar gente en esos interminables diacuteas de verano
Siempre os estareacute agradecida porque esta tesis es hoy tambieacuten gracias a vosotras Y
a Luciacutea y a Inma porque el ldquoea po nardquo puede ser y seraacute nuestro siempre
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
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Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
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D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
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multivariate direct gradient analysis Ecology 67 1167-1179 Ter Braak CJF 1995 Ordination In Jongman RHG ter Braak CJF van Tongeren OFR
(Eds) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge United Kingdom pp 91
Torres MA Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Caacutediz ecosystem (South-western Spain) Ecological Modelling 26 26-44
Trask PD 1950 Applied sedimentation Jon Wiley and Sons Inc New York
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349-357
V Veiga P Rubal M Cacauelos E Maldonado C Sousa-Pinto I 2014 Spatial variability of
macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
100
Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
101
3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
104
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
Sho
re b
ird
s
Pis
civo
rou
s b
ird
s
Eura
sia
n O
yste
rca
tch
er
Co
asta
l fis
h
Ba
thyp
ore
ia p
ela
gic
a
Cu
mo
psi
s fa
gei
Biv
alvi
a
De
cap
od
a
Dis
pio
un
cin
ata
Do
na
x tr
un
culu
s
Eury
dic
e a
ffin
is
Mys
ida
Gly
cera
tri
da
ctyl
a
Ha
uto
riu
s a
ren
ari
us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
Boos K Gutow L Mundry R Franke HD 2010 Sediment preference and burrowing behaviour in the sympatric brittlestars Ophiura albida Forbes 1839 and Ophiura ophiura (Linnaeus 1758) (Ophiuroidea Echinodermata) Journal of Experimental Marine Biology and Ecology 393 176ndash181
Brearey D M 1982 The feeding ecology and foraging behaviour of sanderline Calidris alba and turnstone Arenaria interpres at Teesmouth NEEngland Durham theses Dirham University
Brey T 2001 Population Dynamics in Benthic Invertebrates A virtual Handbook httpthomas-breydesciencevirtualhandbook
5 References
Capiacutetulo 4
116
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Byron C Link J Costa-Pierce B Bengston D 2011 Modeling ecological carrying capacity of shellfish aquaculture in highly flushed temperate lagoons Aquaculture 314 87ndash99
C Cammen LM 1980 Ingestion rate an empirical model for aquatic deposit feeders and
detritivores Oecologia 44 303-310 Chartosia N Kitsos MS Koukouras A 2010 Seasonal Diet of Portumnus Latipes (Pennat
1777) (Decopoda Portunidae) Crustaceana 83 1101-1113 Christensen V Pauly D 1992 ECOPATH II a software for balancing steady-state ecosystem
models and calculating network characteristics Ecological Modelling 61 169-185 Christensen V Pauly D 1995 Fish production catches and the carrying capacity of the
world oceans Naga 18 34-40 Christensen V Walters CJ 2004 ECOPATH with ECOSIM methods capabilities and
limitations Ecological Modelling 172 109-139 Christensen V Walters CJ Pauly D 2005 Ecopath with Ecosim a UserrsquosGuide November
2005 edition Fisheries Centre University of British ColumbiaVancouver Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide
November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
Coll M Palomera I Tudela S Sardagrave F 2006 Trophic flows ecosystem structure and fishing impacts in the South Catalan Sea Northwestern Mediterranean Journal of Marine Systems 59 63ndash96
Colleacuteter M Gascuel D Eucotin JM Morais L 2012 Modelling trophic flows in ecosystems to assess the efficiency of marine protected area (MPA) a case study on the coast of Seacuteneacutegal Ecological modeling 232 1-13
Colombini I Brilli M Fallaci M Gagnarli E Chelazzi L 2011 Food webs of sandy beach macroinvertebrate community using stable isotopes analysis Acta Oecologica 37 422-432
D Dauer DM Maybury CA Ewing RM 1981 Feeding behaviour and general ecology of
several spionid polychaetes from the Chesapeake Bay Journal of Experimental Marine Biology and Ecology 54 21-38
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beache macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman D Schlacher T Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1ndash12
Dennel R 1933 The habitats and feeding mechanism of the Amphipod Haustorius arenarius Slabber Journal of the Linnean Society of London Zoology 38 363-388
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan J Hubbard D McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58 133-148
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117
F Fabiano M Marin V Paoli C Vassallo P 2009 Methods for the sustainability evaluation
of coastal zone Journal of Mediterranean Ecology 10 5ndash11 Fanini L Cantarino CM F Scapini F 2005 Relationships between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fauchal K 1979 The diet of worms A study of polychaete feeding guilds Oceanography and Marine Biology An Annual Review 7 193-284
Field JG Wulff F Mann KH 1989 The need to analyse ecological networks In Wulff F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Coastal and Estuarine Studies Springer-Verlag Berlin 3ndash12
Freire J 1996 Feeding ecology of Liocarcinus depurator (Decapoda Portunidae) in the Riade Arousa (Galicia north-west Spain) effects of habitat season and life history Marine Biology 126 297-311
Froese R Pauly D 2012 FishBase World Wide Web Electronic Publication wwwfishbaseorg
G Gaedke U 1995 A comparison of whole-community and ecosystem approaches (biomass
size distributions food web analysis network analysis simulation models) to study the structure function and regulation of pelagic food webs Journal of Plankton Research 17 1273ndash1305
Guerra-Garciacutea JM Tierno de Figueroa JM Navarro-Barranco C Ros M Saacutenchez-Moyano JE Moreira J 2014 Dietary analysis of the marine Amphipods (Crustacea Peracarida) form the Iberian Peninsula Journal of Sea Research 85 508-517
H Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives
Proceedings of the Royal Society of London B 2701871-1878 Heppleston PB 1971 The feeding Ecology of Oystercatchers (Haematopus ostralegus L) in
winter in Northern Scotland Journal of Animal Ecology 40 651-672 Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a highenergy
beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585 Heymans JJ Ulanowicz RE Bondavalli C 2002 Network analysis of the South Florida
Everglades graminoid marshes and comparison with nearby cypress ecosystems Ecological Modelling 149 5-23
Holdich DM 1981 Opportunistic Feeding Behaviour in a Predatory Isopod Crustaceana 41 101-103
Hsing-Juh L Xiao-Xun D Kwang-Tsao S Huei-Meei S Wen-Tseng L Hwey-Lian H Lee-Shing F Jia-Jang H 2006 Trophic structure and functioning in a eutrophic and poorly flushed lagoon in southwestern Taiwan Marine Environmental Research 62 61ndash82
J Jones DA Pierpoint CJ 1997 Ecology and taxonomy of the genus Eurudice (Ispoda
Cirolanidae) form sand beaches on the Iberian Peninsula Journal of the Marine Biological Association of the United Kingdom 77 55-76
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K Kay JJ Graham LA Ulanowicz RE 1989 A detailed guide to network analysis In Wulff
F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Springer Berlin 32 15ndash61
Knox GA 2001 The ecology of seashores CRC Press Boca Raton Florida USA
L Leguerrier D Degreacute D Niquil N 2007 Network analysis and inter-ecosystem comparison
of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove SW France) Estuarine Coastal and Shelf Science 74 403-418
Lercari D Defeo O 2003 Variation of a sandy beach macrobenthic community along a human-induced environmental gradient Estuarine Coastal and Shelf Science 58S 17ndash24
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lewis L Bodegom P Rozema J Janssen G 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172ndash181
Libralato S Coll M Tempesta M Santojanni A Spoto M Palomera I Arneri E Solidoro C 2010 Food-web traits of protected and exploited areas of the Adriatic Sea Biological Conservation 143 2182ndash2194
Lindeman RL 1942 The trophic-dynamic aspect of ecology Ecology 23 399ndash418
M Marcstroumlm V Mascher JW 1979 Weights and fat in Lapwings Vanellus vanellus and
Oystercatchers Haematopus ostralegus starved to death during a cold spell in spring Ornis Scandinavica 10 235-240
Mcdermott JJ Roe P 1985 Food Feeding Behaviour and Feeding Ecology of Nemerteans American Zoologist 25 113-125
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Coastal Management 71 256-368
Moreira F 1995 The winter feeding ecology of Avocets Recuvirostra avosetta on intertidal areas II Diet and feeding mechanisms Ibis 137 99-108
N Navarro-Barranco C Tierno-de-Figueroa JM Guerra-Garciacutea JM Saacutenchez-Tocino L and
Garciacutea-Goacutemez JC 2013 Feeding habits of amphipods (Crustacea Malacostraca) from shallow soft bottom communities Comparison between marine caves and open habitats Journal of Sea Research 78 1-7
Nilsson SG Nilsson IN 1976 Numbers food consumption and fish predation by birds in Lake Moacuteckeln southern Sweden Ornis Scandinavica 7 61-70
O Odum HT 1969 The strategy of ecosystem development Science 164 262-270 Odum E 1971 Fundamentals of ecology Philadelphia Saunders
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Ortiz M Wolff M 2002 Trophic model of four benthic communities in Tongoy Bay (Chile) comparative analysis and preliminary assessment of management strategies Journal of Experimental Marine Biology and Ecology 268 205ndash235
P Parsons T Maila Y Lalli C 1984 A Manual of Chemical and Biological Methods for
Seawater Analysis Pergamon Patriacutecio J Ulanowicz RE Pardal MA Marques JC 2004 Ascendency as an ecological
indicator a case study of estuarine pulse eutrophication Estuarine Coastal and Shelf Science 60 23-35
Patriacutecio J Marques JC 2006 Mass balanced models of the food web in three areas along a gradient of eutrophication symptoms in the south arm of the Mondego estuary (Portugal) Ecological modelling 197 21ndash34
Peacuterez-Hurtado A Goss-Custard JD Garciacutea F 1997 The diet of wintering waders in Caacutediz Bay southwest Spain Bird study 44 45-52
Phong LT Dam AA Udo HMJ Mensvoort MEF Tri LQ Steenstra FA Zijpp AJ 2010 An agro-ecological evaluation of aquaculture integration into farming systems of the Mekong Delta Agriculture Ecosystems and Environment 138 232ndash241
Poppe GT Goto Y 1993 European Seashells Vol II (Scaphopoda Bivalvia Cephalopoda) Verlag Christa Hemmen Wiesbaden Germany
R Rosado-Soloacuterzano R Guzman del Proo S 1998 Preliminary trophic structure model for
Tampamachoco lagoon Veracruz Mexico Ecological Modelling 109 141ndash154
S San Vicente C Sorbe JC 1993 Biologie du Mysidaceacute suprabenthique Schistomysis parkeri
Norman 1892 dans la zone sud du Golfe de Gascogne (Plage dHendaye) Crustaceana 65 222-252
Scapini F 2003 Beaches ndash What Future An integrated approach to the ecology of sandy beaches (Editorial) Estuarine Coastal and Shelf Science 58S 1-3
Selleslagh J Lobry J Amara R Brylinski JM Boeumlt P 2013 Trophic functioning of coastal ecosystems along an anthropogenic pressure gradient A French case study with emphasis on a small and low impacted estuary Estuarine Coastal and Shelf Science 112 73-85
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Richardson D McLean I 2008 Impacts of off-road vehicles (ORVs) on macrobenthic assemblages on sandy beaches Environmental Management 41 878ndash892
T Theilacker GH Kimball AS 1984 Rotifers and copepods as larval fish foods California
Cooperative Oceanic Fisheries Investigations XXV 80-84 Torrecilla-Roca I Guerra-Garciacutea JM 2012 Fedding habits of the peracarid crustaceans
associated to the alga Fucus spiralis in Tarifa Island Caacutediz (Southern Spain) Zoologia baetica 23 39-47
Torres M Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Cadiz ecosystem (South-western Spain) Ecological Modelling 265 26ndash 44
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Turpie JK Hockey PAR 1997 Adaptative variation in the foraging behaviour of Grey Plover Pluvialis squatarola and Whimbrel Numenius pheopus Ibis 139 289-298
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Ulanovick RE 1984Community measures of marine food networks and their possible applications Fashman MJR (ed) Flows of energy and materials in marine ecosystems Plenum Press New York 23-47
Ulanowicz R E 1986 Growth and Development Ecosystem Phenology Springer-Verlag New York 203
Ulanowicz RE Puccia CJ 1990 Mixed trophic impact in ecosystems Coenoses 5 7-16
V Vasallo P Paoili C Fabiano M 2012 Ecosystem level analysis of sandy beaches using
thermodynamic and network analyses A study case in the NW Mediterranean Sea Ecological Indicators 15 10ndash17
Vega-Cendejas ME Arreguiacuten-Saacutenchez F Hernaacutendez M 1993 Trophic fluxes on the Campeche Bank Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 206-213
Veloso VG Silva ES Caetano CHS Cardoso R 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510ndash515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Villanueva MC Lalegraveyegrave P Albaret JJ Laeuml R Tito de Morais L Moreau J 2006 Comparative analysis of trophic structure and interactions of two tropical lagoons Ecological Modelling 197 461-477
Vinebrooke RD Cottingham KL Norberg J 2004 Implications of multiple stressors on biodiversity and ecosystem functioning the role of species co-tolerance Oikos 104 451-457
Y Yang Y Chen H Yang Z 2010 Assessing changes of trophic interactions during once
anthropogenic water supplement in Baiyangdian Lake Procedia Environmental Sciences 2 1169ndash1179
Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
Capiacutetulo 6
153
2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
6
7
8
9
10
11
12
Capiacutetulo 8
184
esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
13
14
15
16
185
Agradecimientos
Y llegoacute el inesperado momento de los agradecimientos Tengo a tantas personas a las
que agradecer que espero no extenderme mucho
En primer lugar quiero dar las gracias a mis directores a Paco y a Emilio por la
confianza depositada en mi para la realizacioacuten de esta Tesis que todaviacutea no me creo
que haya terminado Hoy tengo sentimientos contradictorios por un lado alegriacutea y
satisfaccioacuten personal por haberlo logrado pero por otro no puedo dejar de sentir
cierta nostalgia porque esta etapa haya llegado a su fin Gracias a Paco por
escucharme cuando llamaba a su puerta diciendo ldquoTengo un problemardquo por la
incalculable ayuda prestada durante todo este tiempo y por los consejos ofrecidos en
los tiacutepicos momentos de crisis existencial Esta crisis tambieacuten se extendioacute al para mi
tenebroso mundo de la estadiacutestica en el que Emilio siempre lograba sacar luz Me
llevo guardados grandes momentos con vosotros no puedo evitar sonreiacuter al
acordarme de nuestros muestreos en los que sin quererlo poniacuteamos a prueba nuestra
integridad fiacutesica y como no emocional Hasta en alguna ocasioacuten recuerdo que casi
conseguimos traernos toda la arena de la playahellip iquestpero que no arreglaba nuestra
tortilla y quesito del descanso aunque fuera prefabricada en ese momento era gloria
Hay tantos momentos que no seriacutea posible describirlos todos Lo que si es cierto es
que hoy veo las playas desde una manera diferente y es gracias a vosotros
Carmen te llegoacute el momento Nos conocimos hace mucho tiempo y el destino quiso
que de nuevo emprendieacuteramos este camino juntas Gracias por tu gran ayuda en los
muestreos por las horas y horas compartidas en el laboratorio en el que nuestras
charlas haciacutean mucho maacutes ameno el paso del tiempo perdidas entre las muestras en
busca de nuestro tesoro particular los bichitos rositas Gracias por las charlas
constructivas y por ayudarme en los momentos que los que estaba maacutes que peacuterdida
No puedo olvidarme de todas aquellas personas que sin conocerme me abrieron las
puertas de sus laboratorios y de las que he aprendido cosas de incalculable valor
Todas esas estancias han sido clave para mi y para que esta tesis haya salido adelante
Gracias a Francesca Rossi que fue la primera en ldquoacogermerdquo cuando auacuten casi no habiacutea
salido del cascaroacuten aprendiacute mucho de aquella experiencia a Valeria Veloso y a Carlos
Borzone por la inmejorable estancia en Brasil y por todos sus consejos Gracias a Diego
Lercari por ensentildearme a ver las playas desde una perspectiva diferente por toda su
dedicacioacuten y especialmente por su paciencia gran parte de esta tesis ha sido gracias a
ti Gracias a todas las ldquomeninasrdquo del laboratorio de Pontal y como olvidarme del equipo
Undecimar gracias chicos haceacuteis que estaacutes estancias merezcan doblemente la pena
Es momento de agradecer a todas esas personas que me han ayudado en los
muestreos poniendo su granito de arena (y nunca mejor dicho) en esta tesis Tambieacuten
a todo el personal del Parque de los Toruntildeos por sus facilidades y gran ayuda durante
los muestreos y a los organismos puacuteblicos que han financiado tanto esta tesis (Junta
de Andaluciacutea a traveacutes de sus Proyectos de Excelencia) como las estancias disfrutadas
(Universidad Pablo de Olavide y AUIP)
Quiero agradecer tambieacuten a mi familia a mis hermanas y en especial a mis padres a
quieacuten hoy dedico esta tesis por todo el apoyo prestado durante este tiempo Siempre
habeacuteis confiado en mi aunque al principio no entendierais del todo bien mi diversioacuten
por ir a sacar kilos y kilos de arena de las playas Siempre me habeacuteis animado a seguir
mis suentildeos por muy alocados que fueran os habeacuteis sentido orgullosos y me habeacuteis
hecho creer que podiacutea conseguir todo lo que me propusiera y que esto era ldquopan
comidordquo
Gracias a Aacutelvaro mi gran pilar y sustento Tu eres de todos el que maacutes ha vivido esto
gracias por ser capaz de sacar siempre el lado bueno de las cosas y por el ldquoiquestQueacute no
sale hoy No te preocupes mantildeana seraacute otro diacuteardquo Siempre has confiado en mi incluso
cuando yo no era capaz de hacerlo Gracias por no cansarte de animarme incluso
cuando este trabajo se convertiacutea en lo primero me has acompantildeado en muchas de mis
aventuras playeras y has disfrutado y celebrado como nadie cuando llegaban buenas
noticias Se que tambieacuten para ti hoy las playas son algo maacutes y eso me enorgullece
Hasta vamos a las playas cargados con bolsitas por si nos encontramos alguacuten bichito
que recoger para el laboratorio iquestquieacuten nos lo habraacute pegado
Y por uacuteltimo a mis nintildeas gracias a Inma a Luciacutea y a Aacutengeles por los aacutenimos en los
momentos de flaqueza por las charlas constructivas por esas visitas sorpresa y salidas
ldquoobligadasrdquo para olvidarnos de todo Gracias por entenderme por aceptar aunque
fuera a regantildeadientes que no pudiera estar en todos los momentos porque el deber
me llamabahellip y por celebrar las alegriacuteas y como no los fracasos como solo nosotras
sabemos hacerlo Me habeacuteis valorado como nadie incluso alguna que otra se llevoacute el
premio de venir a muestrear y contar gente en esos interminables diacuteas de verano
Siempre os estareacute agradecida porque esta tesis es hoy tambieacuten gracias a vosotras Y
a Luciacutea y a Inma porque el ldquoea po nardquo puede ser y seraacute nuestro siempre
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
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Brooks A R Purdy CN Bell SS Sulak KJ 2006 The benthic community of the eastern US continental shelf A literature synopsis of benthic faunal resources Continental Shelf Research 26 804-818
Anfuso E Ponce R Gonzaacutelez-Castro C Forja JM 2010 Coupling between the thermohaline chemical and biological fields during summer 2006 in the northeast continental shelf of the Gulf of Caacutediz (SW Iberian Peninsula) Scientia Marina 74 47 ndash 56
Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Bayed A 2003 Influence of morphodynamic and hidroclimatic factors on the macrofauna of
Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
Southern Brazil Brazilian Archives of Biology and Technology 44 351-364 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Colombini I Aloia A Fallaci M Pezzoli G Chelazzi L 2000 Temporal and spatial use of
stranded wrack by the macrofauna of a tropical sandy beach Marine Biology 136 531-541
Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
Conference on Engineering Dynamics in the Surf Zone (Sydney) 208-214 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1-12
Defeo O Jaramillo E Lyonnet A 1992 Community structure and intertidal zonation of the macroinfauna on the Atlantic coast of Uruguay Journal of Coastal Research 8 830-839
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Degraer S Mouton I De Neve L Vincx M 1999 Community structure and zonation of the macroinfauna on the Antlantic coast of Uruguay Journal of Coastal Research 8 830-839
Dexter DM 1983 Community structure of intertidal sandy beaches in New South Wales Australia In McLachlan A and T Erasmus (Eds) Sandy Beaches as Ecosystems The Hague Junk
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
G Gonccedilalves SC Anastaacutecio PM Pardal AM Cardoso PG Ferreira SM Marques JC
2009 Sandy beach macrofaunal communities on the western coast of Portugal ndashIs there a steady structure under similar exposed conditions Estuarine Coastal and Shelf Science 81 555-568
Guitian FJ Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de Compostela Espantildea
J Jaramillo E McLachlan A Coetzee P 1993 Intertidal zonation patterns of macroinfauna
over a range of exposed sandy beaches in south central Chile Marine Ecology Progress Series 101 105-118
Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
Jaramillo E Duarte C Contreras H 2000 Sandy beaches macroinfauna from the coast of Ancud Isla Chiloeacute southern Chile Revista Chilena de Historia Natural 73 771-786
L Lercari D Defeo O 2006 Large-scale diversity and abundance trends in sandy beach
macrofauna along full gradients of salinity and morphodynamics Estuarine Coastal and Shelf Science 68 27-35
M Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and
morphology a conceptual beach model Journal of Coastal Research 9 785-800 Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3 for Windows MjM Software Design Gleneden Beach Oregon
McEvoy EG Sundberg P 1993 Patterns of trace metal accumulation in Swedish marine nemerteans Hydrobiologia 226 273-280
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McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal sands Journal of Coastal Research 6 57-71
McLachlan A 1996 Physical factors in benthic ecology effects of changing sand particle size on beach fauna Marine Ecology Progress Series 131 205-217
McLachlan A Brown AC 2006 The ecology of sandy shores Elsevier Burlington McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities
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communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27-38
Munilla T San Vicente C 2005 Suprabenthic biodiversity of Catalan beaches (NW Mediterranean) Acta Oecologica 27 81-91
P
Papageorgiou N Arvanitidis C Eleftheriou A 2006 Multicausal environmental severity A flexible framework for microtidal sandy beaches and the role of polychaetes as an indicator taxon Estuarine Coastal and Shelf Science 70 643-653
Perez-Domingo S Castellanos C Junoy J2008 The sandy beach macrofauna of Gulf of Gabeacutes (Tunisia) Marine Ecology 29 51-59
Prieto L Garciacutea CM Corzo A Ruiz-Segura J Echevarriacutea F 1999 Phytoplankton bacterioplankton and nitrate reductase activity distribution in relation to physical structure in the northern Alboraacuten Sea and Gulf of Cadiz (southern Iberian Peninsula) Instituto Espantildeol de Oceanografiacutea 15 401-411
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodil IF Lastra M Loacutepez J 2007 Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain) Hidrobiologiacutea 579 301-316
Rodil IF Compton TJ Lastra M 2012 Exploring Macroinvertebrate Species distributions at Regional and Local Scales across a Sandy Beach Geographic Continuum PloS One (7) 6 e39609
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S Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal
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squamata (Polychaeta Spionidae) in an exposed sandy beach of southern Brazil Bulletin of marine science 67 221-233
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Speyboreck J Alsteens L Vincx M Degraer S 2007 Understanding the life of a sandy beach polychaete of functional importance - Scolelepis squamata (Polychaeta Spionidae) on Belgian sandy beaches (northeastern Atlantic North Sea) Estuarine Coastal and Shelf Science 74 109-118
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macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
100
Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
101
3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
104
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
Sho
re b
ird
s
Pis
civo
rou
s b
ird
s
Eura
sia
n O
yste
rca
tch
er
Co
asta
l fis
h
Ba
thyp
ore
ia p
ela
gic
a
Cu
mo
psi
s fa
gei
Biv
alvi
a
De
cap
od
a
Dis
pio
un
cin
ata
Do
na
x tr
un
culu
s
Eury
dic
e a
ffin
is
Mys
ida
Gly
cera
tri
da
ctyl
a
Ha
uto
riu
s a
ren
ari
us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
Boos K Gutow L Mundry R Franke HD 2010 Sediment preference and burrowing behaviour in the sympatric brittlestars Ophiura albida Forbes 1839 and Ophiura ophiura (Linnaeus 1758) (Ophiuroidea Echinodermata) Journal of Experimental Marine Biology and Ecology 393 176ndash181
Brearey D M 1982 The feeding ecology and foraging behaviour of sanderline Calidris alba and turnstone Arenaria interpres at Teesmouth NEEngland Durham theses Dirham University
Brey T 2001 Population Dynamics in Benthic Invertebrates A virtual Handbook httpthomas-breydesciencevirtualhandbook
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C Cammen LM 1980 Ingestion rate an empirical model for aquatic deposit feeders and
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1777) (Decopoda Portunidae) Crustaceana 83 1101-1113 Christensen V Pauly D 1992 ECOPATH II a software for balancing steady-state ecosystem
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2005 edition Fisheries Centre University of British ColumbiaVancouver Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide
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Coll M Palomera I Tudela S Sardagrave F 2006 Trophic flows ecosystem structure and fishing impacts in the South Catalan Sea Northwestern Mediterranean Journal of Marine Systems 59 63ndash96
Colleacuteter M Gascuel D Eucotin JM Morais L 2012 Modelling trophic flows in ecosystems to assess the efficiency of marine protected area (MPA) a case study on the coast of Seacuteneacutegal Ecological modeling 232 1-13
Colombini I Brilli M Fallaci M Gagnarli E Chelazzi L 2011 Food webs of sandy beach macroinvertebrate community using stable isotopes analysis Acta Oecologica 37 422-432
D Dauer DM Maybury CA Ewing RM 1981 Feeding behaviour and general ecology of
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Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beache macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman D Schlacher T Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1ndash12
Dennel R 1933 The habitats and feeding mechanism of the Amphipod Haustorius arenarius Slabber Journal of the Linnean Society of London Zoology 38 363-388
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan J Hubbard D McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58 133-148
Capiacutetulo 4
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F Fabiano M Marin V Paoli C Vassallo P 2009 Methods for the sustainability evaluation
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Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fauchal K 1979 The diet of worms A study of polychaete feeding guilds Oceanography and Marine Biology An Annual Review 7 193-284
Field JG Wulff F Mann KH 1989 The need to analyse ecological networks In Wulff F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Coastal and Estuarine Studies Springer-Verlag Berlin 3ndash12
Freire J 1996 Feeding ecology of Liocarcinus depurator (Decapoda Portunidae) in the Riade Arousa (Galicia north-west Spain) effects of habitat season and life history Marine Biology 126 297-311
Froese R Pauly D 2012 FishBase World Wide Web Electronic Publication wwwfishbaseorg
G Gaedke U 1995 A comparison of whole-community and ecosystem approaches (biomass
size distributions food web analysis network analysis simulation models) to study the structure function and regulation of pelagic food webs Journal of Plankton Research 17 1273ndash1305
Guerra-Garciacutea JM Tierno de Figueroa JM Navarro-Barranco C Ros M Saacutenchez-Moyano JE Moreira J 2014 Dietary analysis of the marine Amphipods (Crustacea Peracarida) form the Iberian Peninsula Journal of Sea Research 85 508-517
H Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives
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winter in Northern Scotland Journal of Animal Ecology 40 651-672 Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a highenergy
beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585 Heymans JJ Ulanowicz RE Bondavalli C 2002 Network analysis of the South Florida
Everglades graminoid marshes and comparison with nearby cypress ecosystems Ecological Modelling 149 5-23
Holdich DM 1981 Opportunistic Feeding Behaviour in a Predatory Isopod Crustaceana 41 101-103
Hsing-Juh L Xiao-Xun D Kwang-Tsao S Huei-Meei S Wen-Tseng L Hwey-Lian H Lee-Shing F Jia-Jang H 2006 Trophic structure and functioning in a eutrophic and poorly flushed lagoon in southwestern Taiwan Marine Environmental Research 62 61ndash82
J Jones DA Pierpoint CJ 1997 Ecology and taxonomy of the genus Eurudice (Ispoda
Cirolanidae) form sand beaches on the Iberian Peninsula Journal of the Marine Biological Association of the United Kingdom 77 55-76
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K Kay JJ Graham LA Ulanowicz RE 1989 A detailed guide to network analysis In Wulff
F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Springer Berlin 32 15ndash61
Knox GA 2001 The ecology of seashores CRC Press Boca Raton Florida USA
L Leguerrier D Degreacute D Niquil N 2007 Network analysis and inter-ecosystem comparison
of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove SW France) Estuarine Coastal and Shelf Science 74 403-418
Lercari D Defeo O 2003 Variation of a sandy beach macrobenthic community along a human-induced environmental gradient Estuarine Coastal and Shelf Science 58S 17ndash24
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lewis L Bodegom P Rozema J Janssen G 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172ndash181
Libralato S Coll M Tempesta M Santojanni A Spoto M Palomera I Arneri E Solidoro C 2010 Food-web traits of protected and exploited areas of the Adriatic Sea Biological Conservation 143 2182ndash2194
Lindeman RL 1942 The trophic-dynamic aspect of ecology Ecology 23 399ndash418
M Marcstroumlm V Mascher JW 1979 Weights and fat in Lapwings Vanellus vanellus and
Oystercatchers Haematopus ostralegus starved to death during a cold spell in spring Ornis Scandinavica 10 235-240
Mcdermott JJ Roe P 1985 Food Feeding Behaviour and Feeding Ecology of Nemerteans American Zoologist 25 113-125
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Coastal Management 71 256-368
Moreira F 1995 The winter feeding ecology of Avocets Recuvirostra avosetta on intertidal areas II Diet and feeding mechanisms Ibis 137 99-108
N Navarro-Barranco C Tierno-de-Figueroa JM Guerra-Garciacutea JM Saacutenchez-Tocino L and
Garciacutea-Goacutemez JC 2013 Feeding habits of amphipods (Crustacea Malacostraca) from shallow soft bottom communities Comparison between marine caves and open habitats Journal of Sea Research 78 1-7
Nilsson SG Nilsson IN 1976 Numbers food consumption and fish predation by birds in Lake Moacuteckeln southern Sweden Ornis Scandinavica 7 61-70
O Odum HT 1969 The strategy of ecosystem development Science 164 262-270 Odum E 1971 Fundamentals of ecology Philadelphia Saunders
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Ortiz M Wolff M 2002 Trophic model of four benthic communities in Tongoy Bay (Chile) comparative analysis and preliminary assessment of management strategies Journal of Experimental Marine Biology and Ecology 268 205ndash235
P Parsons T Maila Y Lalli C 1984 A Manual of Chemical and Biological Methods for
Seawater Analysis Pergamon Patriacutecio J Ulanowicz RE Pardal MA Marques JC 2004 Ascendency as an ecological
indicator a case study of estuarine pulse eutrophication Estuarine Coastal and Shelf Science 60 23-35
Patriacutecio J Marques JC 2006 Mass balanced models of the food web in three areas along a gradient of eutrophication symptoms in the south arm of the Mondego estuary (Portugal) Ecological modelling 197 21ndash34
Peacuterez-Hurtado A Goss-Custard JD Garciacutea F 1997 The diet of wintering waders in Caacutediz Bay southwest Spain Bird study 44 45-52
Phong LT Dam AA Udo HMJ Mensvoort MEF Tri LQ Steenstra FA Zijpp AJ 2010 An agro-ecological evaluation of aquaculture integration into farming systems of the Mekong Delta Agriculture Ecosystems and Environment 138 232ndash241
Poppe GT Goto Y 1993 European Seashells Vol II (Scaphopoda Bivalvia Cephalopoda) Verlag Christa Hemmen Wiesbaden Germany
R Rosado-Soloacuterzano R Guzman del Proo S 1998 Preliminary trophic structure model for
Tampamachoco lagoon Veracruz Mexico Ecological Modelling 109 141ndash154
S San Vicente C Sorbe JC 1993 Biologie du Mysidaceacute suprabenthique Schistomysis parkeri
Norman 1892 dans la zone sud du Golfe de Gascogne (Plage dHendaye) Crustaceana 65 222-252
Scapini F 2003 Beaches ndash What Future An integrated approach to the ecology of sandy beaches (Editorial) Estuarine Coastal and Shelf Science 58S 1-3
Selleslagh J Lobry J Amara R Brylinski JM Boeumlt P 2013 Trophic functioning of coastal ecosystems along an anthropogenic pressure gradient A French case study with emphasis on a small and low impacted estuary Estuarine Coastal and Shelf Science 112 73-85
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Richardson D McLean I 2008 Impacts of off-road vehicles (ORVs) on macrobenthic assemblages on sandy beaches Environmental Management 41 878ndash892
T Theilacker GH Kimball AS 1984 Rotifers and copepods as larval fish foods California
Cooperative Oceanic Fisheries Investigations XXV 80-84 Torrecilla-Roca I Guerra-Garciacutea JM 2012 Fedding habits of the peracarid crustaceans
associated to the alga Fucus spiralis in Tarifa Island Caacutediz (Southern Spain) Zoologia baetica 23 39-47
Torres M Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Cadiz ecosystem (South-western Spain) Ecological Modelling 265 26ndash 44
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U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Ulanovick RE 1984Community measures of marine food networks and their possible applications Fashman MJR (ed) Flows of energy and materials in marine ecosystems Plenum Press New York 23-47
Ulanowicz R E 1986 Growth and Development Ecosystem Phenology Springer-Verlag New York 203
Ulanowicz RE Puccia CJ 1990 Mixed trophic impact in ecosystems Coenoses 5 7-16
V Vasallo P Paoili C Fabiano M 2012 Ecosystem level analysis of sandy beaches using
thermodynamic and network analyses A study case in the NW Mediterranean Sea Ecological Indicators 15 10ndash17
Vega-Cendejas ME Arreguiacuten-Saacutenchez F Hernaacutendez M 1993 Trophic fluxes on the Campeche Bank Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 206-213
Veloso VG Silva ES Caetano CHS Cardoso R 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510ndash515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Villanueva MC Lalegraveyegrave P Albaret JJ Laeuml R Tito de Morais L Moreau J 2006 Comparative analysis of trophic structure and interactions of two tropical lagoons Ecological Modelling 197 461-477
Vinebrooke RD Cottingham KL Norberg J 2004 Implications of multiple stressors on biodiversity and ecosystem functioning the role of species co-tolerance Oikos 104 451-457
Y Yang Y Chen H Yang Z 2010 Assessing changes of trophic interactions during once
anthropogenic water supplement in Baiyangdian Lake Procedia Environmental Sciences 2 1169ndash1179
Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
Capiacutetulo 6
153
2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
6
7
8
9
10
11
12
Capiacutetulo 8
184
esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
13
14
15
16
185
ti Gracias a todas las ldquomeninasrdquo del laboratorio de Pontal y como olvidarme del equipo
Undecimar gracias chicos haceacuteis que estaacutes estancias merezcan doblemente la pena
Es momento de agradecer a todas esas personas que me han ayudado en los
muestreos poniendo su granito de arena (y nunca mejor dicho) en esta tesis Tambieacuten
a todo el personal del Parque de los Toruntildeos por sus facilidades y gran ayuda durante
los muestreos y a los organismos puacuteblicos que han financiado tanto esta tesis (Junta
de Andaluciacutea a traveacutes de sus Proyectos de Excelencia) como las estancias disfrutadas
(Universidad Pablo de Olavide y AUIP)
Quiero agradecer tambieacuten a mi familia a mis hermanas y en especial a mis padres a
quieacuten hoy dedico esta tesis por todo el apoyo prestado durante este tiempo Siempre
habeacuteis confiado en mi aunque al principio no entendierais del todo bien mi diversioacuten
por ir a sacar kilos y kilos de arena de las playas Siempre me habeacuteis animado a seguir
mis suentildeos por muy alocados que fueran os habeacuteis sentido orgullosos y me habeacuteis
hecho creer que podiacutea conseguir todo lo que me propusiera y que esto era ldquopan
comidordquo
Gracias a Aacutelvaro mi gran pilar y sustento Tu eres de todos el que maacutes ha vivido esto
gracias por ser capaz de sacar siempre el lado bueno de las cosas y por el ldquoiquestQueacute no
sale hoy No te preocupes mantildeana seraacute otro diacuteardquo Siempre has confiado en mi incluso
cuando yo no era capaz de hacerlo Gracias por no cansarte de animarme incluso
cuando este trabajo se convertiacutea en lo primero me has acompantildeado en muchas de mis
aventuras playeras y has disfrutado y celebrado como nadie cuando llegaban buenas
noticias Se que tambieacuten para ti hoy las playas son algo maacutes y eso me enorgullece
Hasta vamos a las playas cargados con bolsitas por si nos encontramos alguacuten bichito
que recoger para el laboratorio iquestquieacuten nos lo habraacute pegado
Y por uacuteltimo a mis nintildeas gracias a Inma a Luciacutea y a Aacutengeles por los aacutenimos en los
momentos de flaqueza por las charlas constructivas por esas visitas sorpresa y salidas
ldquoobligadasrdquo para olvidarnos de todo Gracias por entenderme por aceptar aunque
fuera a regantildeadientes que no pudiera estar en todos los momentos porque el deber
me llamabahellip y por celebrar las alegriacuteas y como no los fracasos como solo nosotras
sabemos hacerlo Me habeacuteis valorado como nadie incluso alguna que otra se llevoacute el
premio de venir a muestrear y contar gente en esos interminables diacuteas de verano
Siempre os estareacute agradecida porque esta tesis es hoy tambieacuten gracias a vosotras Y
a Luciacutea y a Inma porque el ldquoea po nardquo puede ser y seraacute nuestro siempre
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
A Aerts K Vanagt T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-
Rodriguez MP Calderoacuten J Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-22
Brooks A R Purdy CN Bell SS Sulak KJ 2006 The benthic community of the eastern US continental shelf A literature synopsis of benthic faunal resources Continental Shelf Research 26 804-818
Anfuso E Ponce R Gonzaacutelez-Castro C Forja JM 2010 Coupling between the thermohaline chemical and biological fields during summer 2006 in the northeast continental shelf of the Gulf of Caacutediz (SW Iberian Peninsula) Scientia Marina 74 47 ndash 56
Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Bayed A 2003 Influence of morphodynamic and hidroclimatic factors on the macrofauna of
Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
Southern Brazil Brazilian Archives of Biology and Technology 44 351-364 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Colombini I Aloia A Fallaci M Pezzoli G Chelazzi L 2000 Temporal and spatial use of
stranded wrack by the macrofauna of a tropical sandy beach Marine Biology 136 531-541
Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
Conference on Engineering Dynamics in the Surf Zone (Sydney) 208-214 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1-12
Defeo O Jaramillo E Lyonnet A 1992 Community structure and intertidal zonation of the macroinfauna on the Atlantic coast of Uruguay Journal of Coastal Research 8 830-839
5 References
Capiacutetulo 2
54
Degraer S Volckaert A Vincx M 2003 Macrobenthic zonation patterns along a morphodynamical continuum of macrotidal low tide barrip and ultra-dissipative sandy beaches Estuarine Coastal and Shelf Science 56 459-468
Degraer S Mouton I De Neve L Vincx M 1999 Community structure and zonation of the macroinfauna on the Antlantic coast of Uruguay Journal of Coastal Research 8 830-839
Dexter DM 1983 Community structure of intertidal sandy beaches in New South Wales Australia In McLachlan A and T Erasmus (Eds) Sandy Beaches as Ecosystems The Hague Junk
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
G Gonccedilalves SC Anastaacutecio PM Pardal AM Cardoso PG Ferreira SM Marques JC
2009 Sandy beach macrofaunal communities on the western coast of Portugal ndashIs there a steady structure under similar exposed conditions Estuarine Coastal and Shelf Science 81 555-568
Guitian FJ Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de Compostela Espantildea
J Jaramillo E McLachlan A Coetzee P 1993 Intertidal zonation patterns of macroinfauna
over a range of exposed sandy beaches in south central Chile Marine Ecology Progress Series 101 105-118
Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
Jaramillo E Duarte C Contreras H 2000 Sandy beaches macroinfauna from the coast of Ancud Isla Chiloeacute southern Chile Revista Chilena de Historia Natural 73 771-786
L Lercari D Defeo O 2006 Large-scale diversity and abundance trends in sandy beach
macrofauna along full gradients of salinity and morphodynamics Estuarine Coastal and Shelf Science 68 27-35
M Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and
morphology a conceptual beach model Journal of Coastal Research 9 785-800 Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3 for Windows MjM Software Design Gleneden Beach Oregon
McEvoy EG Sundberg P 1993 Patterns of trace metal accumulation in Swedish marine nemerteans Hydrobiologia 226 273-280
Capiacutetulo 2
55
McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal sands Journal of Coastal Research 6 57-71
McLachlan A 1996 Physical factors in benthic ecology effects of changing sand particle size on beach fauna Marine Ecology Progress Series 131 205-217
McLachlan A Brown AC 2006 The ecology of sandy shores Elsevier Burlington McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities
Journal of Coastal Research 21 674-687 McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna
communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27-38
Munilla T San Vicente C 2005 Suprabenthic biodiversity of Catalan beaches (NW Mediterranean) Acta Oecologica 27 81-91
P
Papageorgiou N Arvanitidis C Eleftheriou A 2006 Multicausal environmental severity A flexible framework for microtidal sandy beaches and the role of polychaetes as an indicator taxon Estuarine Coastal and Shelf Science 70 643-653
Perez-Domingo S Castellanos C Junoy J2008 The sandy beach macrofauna of Gulf of Gabeacutes (Tunisia) Marine Ecology 29 51-59
Prieto L Garciacutea CM Corzo A Ruiz-Segura J Echevarriacutea F 1999 Phytoplankton bacterioplankton and nitrate reductase activity distribution in relation to physical structure in the northern Alboraacuten Sea and Gulf of Cadiz (southern Iberian Peninsula) Instituto Espantildeol de Oceanografiacutea 15 401-411
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodil IF Lastra M Loacutepez J 2007 Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain) Hidrobiologiacutea 579 301-316
Rodil IF Compton TJ Lastra M 2012 Exploring Macroinvertebrate Species distributions at Regional and Local Scales across a Sandy Beach Geographic Continuum PloS One (7) 6 e39609
Ruiz-Delgado MC Vieira JV Veloso VG Reyes-Martiacutenez MJ Azevedo IS Borzone CA Saacutechez-Moyano JE Garciacutea-Garciacutea FJ 2014 The role of wrack deposits for supralittoral arthropods An example using Atlantic sandy beaches of Brazil and Spain Estuarine Coastal and Shelf Science 136 61-71
S Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal
zonation metrics and their variability Marine Ecology Progress Series 478 43-55 Sobrino I Jimeacutenez MP Ramos F Baro J 1994 Descripcioacuten de las pesqueriacuteas demersales
de la Regioacuten Suratlaacutentica Espantildeola Instituto Espantildeol de Oceanografiacutea 151 3-79 Souza JR Borzone CA 2000 Population dynamics and secondary production of Scolelepis
squamata (Polychaeta Spionidae) in an exposed sandy beach of southern Brazil Bulletin of marine science 67 221-233
Speybroeck J Bonte D Courtens W Gheskiere T Grootaert P Maelfait JP Mathys M Provoost S Sabbe K Stienen EWM 2006 Beach nourishment an ecologically sound coastal defence alternative A review Aquatic Conservation Marine and Freshwater Ecosystems 16 419-435
Capiacutetulo 2
56
Speyboreck J Alsteens L Vincx M Degraer S 2007 Understanding the life of a sandy beach polychaete of functional importance - Scolelepis squamata (Polychaeta Spionidae) on Belgian sandy beaches (northeastern Atlantic North Sea) Estuarine Coastal and Shelf Science 74 109-118
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Ter Braak CJF 1995 Ordination In Jongman RHG ter Braak CJF van Tongeren OFR
(Eds) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge United Kingdom pp 91
Torres MA Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Caacutediz ecosystem (South-western Spain) Ecological Modelling 26 26-44
Trask PD 1950 Applied sedimentation Jon Wiley and Sons Inc New York
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349-357
V Veiga P Rubal M Cacauelos E Maldonado C Sousa-Pinto I 2014 Spatial variability of
macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
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Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
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3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
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4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
Sho
re b
ird
s
Pis
civo
rou
s b
ird
s
Eura
sia
n O
yste
rca
tch
er
Co
asta
l fis
h
Ba
thyp
ore
ia p
ela
gic
a
Cu
mo
psi
s fa
gei
Biv
alvi
a
De
cap
od
a
Dis
pio
un
cin
ata
Do
na
x tr
un
culu
s
Eury
dic
e a
ffin
is
Mys
ida
Gly
cera
tri
da
ctyl
a
Ha
uto
riu
s a
ren
ari
us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
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Vega-Cendejas ME Arreguiacuten-Saacutenchez F Hernaacutendez M 1993 Trophic fluxes on the Campeche Bank Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 206-213
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Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
Capiacutetulo 6
153
2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
6
7
8
9
10
11
12
Capiacutetulo 8
184
esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
13
14
15
16
185
A mis padres
Iacutendice de contenidos
Capiacutetulo 1 Introduccioacuten General 100
1 Ambiente Fiacutesico 111
2 Macrofauna 15
3 Degradacioacuten de las playas 21
4 Objetivos y estructura de la tesis 27
5 Bibligrafiacutea 29
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on sandy
beaches along the Gulf of Caacutediz (SW Spain) 32
1 Introduction 34
2 Material and Methods 36
3 Results 39
4 Discussion 46
5 References 53
6 Appendix 57
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human trampling an
urban vs natural beach system approach 59
1 Introduction 61
2 Material and Methods 63
3 Results 67
4 Discussion 78
5 References 83
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic functioning
87
1 Introduction 89
2 Material and Methods 91
3 Results 101
4 Discussion 110
5 References 115
6 Appendix 121
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in Southwestern
Spain 125
1 Introduction 127
2 Material and Methods 130
3 Results 133
4 Discussion 140
5 References 144
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment 148
1Introduction 150
2 Material and Methods 153
3 Results 157
4 Discussion 162
5 References 165
Capiacutetulo 7 Discusioacuten general 168
Capiacutetulo 8 Conclusiones generales 181
Capiacutetulo 1
Introduccioacuten general
Capiacutetulo 1
11
1 Ambiente Fiacutesico
La Tierra podriacutea describirse como un planeta costero De hecho 1634701 km
de la superficie terrestre corresponde a zonas costeras lo que supondriacutea si
pudieacuteramos estirarla recorrer 402 veces el ecuador Dentro de la categoriacutea de zonas
costeras se incluye una amplia variedad de sistemas tales como playas rocosas
acantilados humedales y especialmente playas arenosas (Burke et al 2001 Martiacutenez
et al 2007)
Las costas arenosas definidas como ldquoacumulaciones de arenardquo son ecosistemas
muy dinaacutemicos y complejos localizados en una franja relativamente estrecha donde la
tierra se encuentra con el mar y donde pueden identificarse tres componentes baacutesicos
la zona cercana a la costa o ldquonearshorerdquo la playa y el sistema dunar todos ellos
interconectados para una funcioacuten principal el transporte de sedimento
Los procesos hidrodinaacutemicos (olas mareas y corrientes marinas) influenciados
por la accioacuten eoacutelica juegan un papel clave en este transporte aunque su incidencia
variacutea a lo largo de toda la superficie costera creaacutendose asiacute un gradiente transversal en
el que es posible distinguir tres zonas principales (Fig 1)
Zona de asomeramiento o ldquoshoalingrdquo En esta zona las olas entran en
aguas menos profundas y como consecuencia se produce una disminucioacuten
de la velocidad y longitud de onda Las olas que son portadores eficientes
de energiacutea responden a este cambio aumentando su altura y asiacute se
consigue mantener un flujo de energiacutea constante Como consecuencia de
este proceso el sedimento es resuspendido y transportado poco a poco
hacia la costa
Zona de rompiente o ldquosurfrdquo En esta zona la cresta de la ola es tan
empinada que se vuelve inestable se curva hacia adelante y se produce lo
que se conoce comuacutenmente como rotura Es la parte maacutes dinaacutemica del
sistema costero debido a la energiacutea liberada por olas al romperse Este
proceso puede generar diversos tipos de corrientes corrientes hacia la
costa (ldquoonshore currentsrdquo) paralelas a la costa (ldquolong-shore currents) y
1 Ambiente fiacutesico
Capiacutetulo 1
12
perpendiculares o de resaca (ldquorip currentsrdquo) que producen un importante
transporte activo de sedimento
Zona de batida o ldquoswashrdquo En esta zona las olas entran en contacto
directo con la orilla colapsan y se transforma en una fina capa de agua
que se desplaza hacia arriba En este proceso el agua se filtra
parcialmente por el sedimento y el agua resultante del lavado regresa de
nuevo al mar Aquiacute es posible distinguir entre dos sub-zonas una cubierta
siempre por el agua o sublitoral y otra no saturada o mediolitoral que
suele quedar al descubierto durante la bajamar
Por encima de estas tres zonas se encuentra el aacuterea supralitoral caracterizada
por presentar siempre arena seca y con un tamantildeo de grano maacutes fino que en el resto
dada su proximidad con el sistema dunar
Fig1 Perfil tiacutepico de una costa arenosa donde se muetran sus principales componentes (Tomado de McLachlan 1983)
11 Morfodinaacutemica
La cantidad e intensidad de la accioacuten de las olas el tipo y tamantildeo del sedimento
asiacute como la amplitud de las mareas dan lugar a una amplia variedad de playas con
diferentes caracteriacutesticas fiacutesicas y topograacuteficas tambieacuten conocido como
morfodinaacutemica Diferentes iacutendices han sido empleados para caracterizar las playas
desde el punto de vista morfodinaacutemico Quizaacutes el maacutes utilizado para este propoacutesito es
el paraacutemetro de velocidad de caiacuteda adimensional o paraacutemetro de Dean que tiene en
cuenta la altura de ola (H) el periodo (T) y la velocidad de sedimentacioacuten (Ws)
Capiacutetulo 1
13
(Gourlay 1968 Dean 1973) Este iacutendice permite clasificar a las playas en tres
categoriacuteas reflectivas disipativas e intermedias
Las playas reflectivas (Ωlt2) se caracterizan por presentar un oleaje de pequentildea
altura y un tamantildeo medio de grano que oscila de medio a grueso No presentan zona
de surf por lo que las olas rompen directamente en el perfil de la playa dando lugar
una zona de batida dinaacutemica y turbulenta con una pendiente relativamente empinada
Por el contrario las playas disipativas (Ωgt5) presentan una zona de batida
praacutecticamente plana y maacutes benigna ya que cuentan con una amplia zona de surf
donde las olas rompen y disipan su energiacutea En esta categoriacutea las olas son de mayor
altura y el tamantildeo medio del grano por lo general es fino Las playas reflectivas por lo
general drenan mayores voluacutemenes de agua y a mayor velocidad que las playas
disipativas debido al tipo de sedimento Ambas son playas bien oxigenadas y solo en
algunos casos cuando las playas disipativas presentan un sedimento muy fino pueden
darse condiciones reductoras en las capas maacutes profundas del sedimento (McLachlan y
Turner 1994) Por uacuteltimo existe una amplia gama de playas que presentan
caracteriacutesticas mixtas entre los dos casos extremos anteriores caracterizadas por su
alta variabilidad temporal y que son denominadas playas intermedias (2ltΩlt5)
Otro iacutendice morfodinaacutemico ampliamente utilizado es el rango mareal relativo
(RTR) (Masselink y Short 1993) que hace referencia a la importancia de olas y mareas
en el control de la morfodinaacutemica Clasifica las playas en tres amplios grupos en
funcioacuten de la altura de la ola (H) y el rango de marea (TR)
De esta forma podemos encontrar (1) playas dominadas por las olas cuando RTR
es menor a 3 (2) dominada por las mareas cuando RTR es mayor a 10 (3) mixta o
RTR= TRH
Ω= H T Ws
Capiacutetulo 1
14
modificada por la mareas cuando los valores de RTR se encuentran entre los
anteriores
Es posible combinar ambos iacutendices para obtener una clasificacioacuten maacutes precisa
del tipo de playa (Fig 2)
El iacutendice del estado de la playa (BSI) es otro paraacutemetro de clasificacioacuten de la
morfodinaacutemica que se utiliza para comparar playas sujetas a diferentes rangos de
marea y que hace referencia a la capacidad de olas y mareas para mover el sedimento
(McLachlan et al 1993) Existen ademaacutes otros iacutendices de clasificacioacuten que se
diferencian de los anteriores principalmente porque no tienen en cuenta los
paraacutemetros del oleaje dada la dificultad de realizar estas medidas en los estudios de
campo y en el caso de hacerlas si estas medidas puntuales se consideran
representativas Asiacute es posible identificar el iacutendice del estado de la playa (BDI) y el
iacutendice de la playa (BI) El BDI (Soares 2003) utiliza medidas de la pendiente y del
tamantildeo grano y es pescialmente recomendable para trabajos a pequentildea escala
espacial donde no existan diferencias en el rango de marea de las playas de estudio El
BI (McLachlan y Dorvlo 2005) por su parte ademaacutes de englobar los paraacutemetros
medidos por el iacutendice BDI incluye el rango mareal de la playa
Fig 2 Clasificacioacuten de la morfodinaacutemica de las playas basada en el paraacutemetro Dean y el Rango Mareal Relativo (Tomado de Defeo y McLachlan 2005)
Capiacutetulo 1
15
2 Macrofauna
Aunque aparentemente puedan parecer desprovistas de vida las playas
arenosas presentan gran variedad de seres vivos La mayoriacutea de los filos de
invertebrados estaacuten presentes ya sea como formas intersticiales o como miembros de
la macrofauna En este tipo de ecosistemas por lo general se entiende como
macrofauna aquellas formas de vida que quedan retenidas en una malla de criba con
una luz de 1 mm (Bishop y Hartley 1986)
Las comunidades de macrofauna de invertebrados son el componente mejor
estudiado de la biota de playas dominadas principalmente por Crustaacuteceos Moluscos y
Poliquetos aunque tambieacuten en la zona supralitoral de la playa pueden existir
importantes poblaciones de insectos (McLachlan y Brown 2006)
Estas comunidades estaacuten influenciadas por diferentes factores fiacutesicos que
pueden ser agrupados en (1) la textura y movimiento del sedimento (tamantildeo de
grano coeficiente de seleccioacuten fluidez dinaacutemica de erosioacutenacrecioacuten) (2) el ldquoclima del
swashrdquo (periodicidad velocidad y turbulencia del agua) y (3) exposicioacuten y humedad de
la playa (Defeo y McLachlan 2013) Por ello la macrofauna desarrolla importantes
adaptaciones que le permiten vivir en estos ambientes tan dinaacutemicos resultado de la
inestabilidad del sustrato y la accioacuten del oleaje De esta forma las caracteriacutesticas
principales son la raacutepida capacidad de enterramiento para evitar el arrastre por las
olas y el alto grado de movilidad Los mecanismos sensoriales son igualmente
importantes ya que permite a estos animales orientarse y mantener sus posiciones en
la orilla Asiacute la macrofauna presenta ritmos de migracioacuten en acorde con la subida y
bajada de las mareas y normalmente nocturnos que les permite maximizar los
recursos alimenticios y atenuar la depredacioacuten (McLachlan y Brown 2006)
El macrobentos desempentildea muacuteltiples funciones necesarias para mantener la
integridad funcional de las playas asiacute regeneran nutrientes (Cisneros et al 2011)
sirven de unioacuten entre sistemas terrestres y marinos a traveacutes de la incorporacioacuten del
material depositado por los estuarios (Schlacher y Connolly 2009) sirven de alimento
para peces y aves (Peterson et al 2006) y consumen y descomponen algas varadas
(Lastra et al 2008)
2 Macrofauna
Capiacutetulo 1
16
21 Patrones de distribucioacuten
211 Patrones a meso-escala Zonacioacuten
La macrofauna no se distribuye de igual manera por todo el intermareal sino
que las especies se restringen a determinadas aacutereas de la playa en funcioacuten de los
paraacutemetros ambientales que eacutestas presentan creando asiacute un gradiente conocido como
zonacioacuten Diferentes autores han descrito la zonacioacuten de las playas (McLachlan y
Jaramillo 1995) pudieacutendose identificar 4 categoriacuteas (1) Sin zonacioacuten evidente (2) 2
zonas una localizada por encima del nivel alcanzado por la marea alta y ocupada por
organismos que respiran aire y otra zona por debajo formada por organismos que
respiran agua (Brown en McLachlan y Brown 2006) (3) 3 zonas basadas en la
distribucioacuten de crustaacuteceos (Dahl 1952) y (4) 4 zonas fiacutesicas basadas en el contenido de
humedad del sedimento (Salvat 1964) (Fig3)
Fig3 Esquemas de zonacioacuten de la fauna en playas arenosas (Tomado de McLachlan y Brown 2006)
Capiacutetulo 1
17
El modelo maacutes ampliamente reconocido es el de 3 zonas basadas en la
propuesta de Dahl Asiacute es posible identificar una zona supralitoral de arena seca y
dominada por organismos que respiran aire tales como anfiacutepodos de la familia
Talitridae isoacutepodos de las familias Cirolanidae y Oniscidae y decaacutepodos Ocypodidae
Esta fauna vive fuera de la zona de swash pero puede hacer uso de ella para
reproducirse y alimentarse A continuacioacuten se encuentra la zona litoral o mediolitoral
que se extiende desde la arena seca hasta la zona donde el sedimento estaacute saturado
de agua La fauna tiacutepica incluye isoacutepodos cirolaacutenidos anfiacutepodos de la familia
Haustoridae y poliquetos espioacutenidos Y por uacuteltimo se encuentra la zona sublitoral
localizada en la zona de saturacioacuten de agua Aquiacute se encuentra una gran variedad de
fauna como bivalvos de la familia Donacidae misidaacuteceos y diversas familias de
anfiacutepodos y poliquetos
Aunque eacutesta es una clasificacioacuten tiacutepica la zonacioacuten es un proceso dinaacutemico y
complejo de manera que el nuacutemero de zonas no es fijo pudiendo variar en funcioacuten de
las caracteriacutesticas que presenten las playas Por ejemplo las playas reflectivas suelen
presentar menos zonas (Aerts et al 2004 Brazeiro y Defeo 1996 Veloso et al 2003) y
en algunos casos en las playas disipativas se produce una fusioacuten de las aacutereas
inferiores Incluso han sido detectadas variaciones estacionales que se producen
cuando las especies ocupan niveles maacutes altos durante primavera y verano que durante
otontildeo e invierno (Defeo et al 1986 Schlacher y Thompson 2013)
211 Patrones a macro-escala
Dado que las comunidades de macrofauna se estructuran en base a las
respuestas de las diferentes especies a las caracteriacutesticas ambientales es faacutecil
entender que los descriptores de la comunidad (riqueza densidad y biodiversidad)
cambien en funcioacuten de la morfodinaacutemica de la playa Asiacute uno de los paradigmas
principales en ecologiacutea de playas arenosas (Hipoacutetesis de Exclusioacuten del Swash (SEH)
McLachlan et al 1993) establece que los descriptores de la comunidad aumentan de
playas reflectivas a disipativas Ademaacutes ha sido probado que la riqueza de especies
tambieacuten experimenta un aumento con la achura del intermareal de tal forma que las
Capiacutetulo 1
18
playas disipativas suponen ambientes maacutes benignos para el desarrollo de la
macrofauna bentoacutenica que las reflectivas (McLachlan y Dorvlo 2005) (Fig 4)
Fig4 Modelo conceptual relacionando las respuestas de los descriptores de la comunidad al tipo de playa Reflectiva (R) Intermedia (I) Disipativa (D) Ultra disipativa (UD) y terraza mareal (TF) (Modificado de Defeo y McLachlan 2005)
La identificacioacuten de patrones a una escala latitudinal no es una tarea faacutecil
debido a la dificultad de compilar bases de datos a nivel mundial Auacuten asiacute se ha
identificado un aumento de la riqueza de especies desde playas templadas a
tropicales explicado principalmente por la mayor presencia de playas disipativas en
zonas templadas La abundancia por el contrario aumenta hacia playas tropicales lo
que pudiera estar relacionado con la disponibilidad de alimento ya que estas zonas
son mucho maacutes productivas (McLachlan y Brown 2006 Defeo y McLachlan 2013)
22 Redes troacuteficas
En estos ecosistemas se producen importantes redes troacuteficas que dependen
principalmente de aportes marinos como el fitoplancton zooplancton algas
faneroacutegamas y carrontildea (Fig 5) Es posible identificar tres redes troacuteficas (1) una red
microbiana en la zona de surf formada por bacterias ciliados flagelados y otro tipo de
Capiacutetulo 1
19
microfitoplancton Estos componentes subsisten de los exudados del fitoplancton y de
otras formas de carbono orgaacutenico disuelto (DOC) De la gran abundancia de este
sistema y la raacutepida utilizacioacuten del carbono se concluye que estos microbios consumen
una parte importante de la produccioacuten primaria en los ecosistemas marinos (2) otra
red formada por organismos intersticiales incluyendo bacterias protozoos y
meiofauna Se abastecen de materiales orgaacutenicos disueltos y particulados que son
depositados en la arena por la accioacuten del oleaje y la marea Este sistema tiene especial
relevancia en el procesamiento de materiales orgaacutenicos limpian y purifican el agua de
la zona surf mineralizan los materiales orgaacutenicos que recibe y devuelven los nutrientes
al mar por lo que son vistos como un importante filtro natural y por uacuteltimo (3) se
encuentra una red macroscoacutepica formada por zooplancton macrofauna aves y peces
La macrofauna juega un papel clave en la transferencia de energiacutea dado que se
alimenta en gran medida de zooplancton y es depredada por peces y aves que se
desplazan fuera del sistema (McLachlan y Brown 2006)
Puesto que estos ecosistemas dependen principalmente de los insumos
provenientes del mar el tamantildeo de la playa la proximidad a la fuente de alimento asiacute
como las caracteriacutesticas de la zona de surf son factores determinantes en el aporte de
alimentos y en el soporte de estas cadenas troacuteficas Asiacute las playas disipativas son por
lo general sistemas muy productivos donde la produccioacuten primaria es producida por
el fitoplancton de la zona de surf Esta alta produccioacuten in situ junto con el patroacuten de
circulacioacuten del agua caracteriacutesticas de estas playas que promueve la retencioacuten del
fitoplancton (Heymans y McLachlan 1996) han llevado a considerar a estos sistemas
como semi-cerrados Por el contrario las playas reflectivas carecen de produccioacuten in
situ por lo que las fuentes de alimentos estaacuten supeditadas a los insumos de material
orgaacutenico tanto del mar como de la tierra (McLachlan y Brown 2006) En este contexto
estudios recientes sobre flujos de energiacutea en playas con diferente morfodinaacutemica han
determinado que las playas disipativas son sistemas maacutes complejos que las playas
reflectivas con mayores niveles troacuteficos reflejo de la mayor diversidad con mayores
conexiones troacuteficas altas transferencias energeacuteticas y superiores tasas de produccioacuten
(Lercari et al 2010)
Capiacutetulo 1
20
Fig5 Red troacutefica tiacutepica de una playa arenosa (Obtenido de McLachlan y Brown 2006)
Capiacutetulo 1
21
3 Degradacioacuten de las playas
A nivel mundial existe un crecimiento continuado de la poblacioacuten en la zona
costera de hecho se espera que en 2025 maacutes del 75 de la poblacioacuten viva dentro de
los 100 km proacuteximos a la costa (Bulleri y Chapman 2010) Ademaacutes de un uso
residencial las playas son enclaves idoacuteneos para el desarrollo de actividades
recreativas y son el principal destino vacacional para turistas por lo que suponen un
pilar baacutesico en la economiacutea de muchos paiacuteses costeros
Las playas arenosas proporcionan servicios ecoloacutegicos uacutenicos como son el
transporte y almacenamiento de sedimentos la filtracioacuten y purificacioacuten del agua la
descomposicioacuten de materia orgaacutenica y contaminantes la mineralizacioacuten y reciclaje de
nutrientes el almacenamiento de agua el mantenimiento de la biodiversidad y
recursos geneacuteticos l abastecimiento de presas para animales terrestres y acuaacuteticos y
ademaacutes proporcionan lugares idoacuteneos para la anidacioacuten de aves y para la criacutea de peces
entre otros (Defeo et al 2009)
A pesar de la importancia de estas funciones normalmente los valores
ecoloacutegicos de las playas se perciben como algo secundario a su valor econoacutemico Asiacute la
accioacuten humana sobre la costa genera una creciente presioacuten sobre las playas a una
escala sin precedentes Ademaacutes estos ecosistemas estaacuten sometidos al denominado
estreacutes costero o ldquocoastal squeezerdquo derivado de las presiones provocadas tanto por la
urbanizacioacuten y transformacioacuten del sistema terrestre adyacente como por las
modificaciones ocurridas en el medio marino (cambio climaacutetico residuoshellip) Por lo
general las playas son ambientes resilientes capaces de hacer frente a perturbaciones
naturales (ej tormentas variaciones climaacuteticashellip) sin cambiar sustancialmente sus
caracteriacutesticas y su funcionalidad El problema viene cuando esta flexibilidad se ve
mermada como consecuencia de las actividades humanas (Schlacher et al 2007)
Las actividades antroacutepicas sobre las playas son muy variadas y actuacutean a
muacuteltiples escalas espaciales y temporales y no soacutelo afectan a las poblaciones de
macrofauna sino que tienen una recupercusioacuten indirecta sobre aquellas especies que
utilizan al bentos como fuente de alimento como son las aves y peces que en muchas
3 Degradacioacuten de las playas
Capiacutetulo 1
22
ocasiones se encuentran bajo alguna figura de proteccioacuten o son de intereacutes pesquero
Las principales fuentes de perturbacioacuten pueden observarse en el siguiente graacutefico (Fig
6)
31 Recreacioacuten
Los efectos de estas presiones son perceptible a escalas temporales que van
desde semanas a meses y a escalas espaciales de lt1 a 10 km Uno de los principales
impactos derivados de las actividades de recreo es el pisoteo Determinar el efecto de
esta actividad sobre las comunidades fauniacutesticas es una tarea difiacutecil ya que
normalmente las aacutereas maacutes ocupadas coinciden con las zonas maacutes urbanizadas y
transformadas donde operan otros agentes perturbadores Auacuten asiacute existen indicios de
que las poblaciones y comunidades de macrofauna responden negativamente a este
impacto (Moffett el al 1998 Weslawski et al 2000 Fanini et al 2014) debido
principalmente cambios en la estabilidad de la arena y al aplastamiento directo de los
Fig 6 Modelo conceptual y diagrama esquemaacutetico que muestra las escalas espacio-temporales en la que los diferentes impacto actuacutean en las comunidades de macrofauna de playas arenosas (Tomado de Defeo y Mclachlan 2005)
Capiacutetulo 1
23
individuos (Brown y McLachlan 2002) Las actividades humanas realizadas en las
playas tambieacuten generan connotaciones negativas para aquellas especies que habitan el
sistema dunar alterando el comportamiento normal de las aves que puede reducir su
probabilidad de supervivencia (Verhulst et al 2001)
Las actividades de recreacioacuten tambieacuten incluyen el uso de vehiacuteculos por las
playas y dunas que conlleva las mismas consecuencias que el pisoteo humano pero
con una mayor intensidad Ademaacutes el uso de vehiacuteculo es extremadamente dantildeino
para el sistema dunar puesto que modifica sus caracteriacutesticas fiacutesicas y destruye tanto
las dunas crecientes como la vegetacioacuten que las cubre y estabiliza
32 Contaminacioacuten limpieza y regeneracioacuten de playas
El creciente uso de las playas como lugares de recreo obliga a las autoridades a
limpiar con regularidad durante el periodo estival aunque en muchos casos es
realizada durante todo el antildeo Durante la limpieza no solo se retiran aquellos residuos
no deseados sino que se eliminan todo tipo de residuos orgaacutenicos marinos e incluso se
retiran propaacutegulos de vegetacioacuten dunar imprescindibles para proteger al sistema de la
erosioacuten
Los aportes orgaacutenicos son esencialmente importantes para la macrofauna de
playas especialmente para las especies supralitorales ya que les proporcionan
alimento y refugio frente a la desecacioacuten (Colombini y Chelazzi 2003) Asiacute la retirada
de estos aportes priva al ecosistema de una importante entrada nutricional Ademaacutes
las maacutequinas utilizadas para la limpieza mecaacutenica remueven y filtran la arena por lo
que no solo se absorben residuos sino tambieacuten organismos Estas maacutequinas a su vez
generan una mortalidad directa de los individuos por aplastamiento (Llewellyn y
Shackley 1996)
Los contaminantes incluyen a una amplia variedad de materiales de origen
antropogeacutenicos que pueden afectar a la fisiologiacutea reproduccioacuten comportamiento y
en definitiva a la supervivencia de todos los organismos de playas En particular los
vertidos de agua residuales son de especial importancia ya que la contaminacioacuten por
bacterias o patoacutegenos no solo suponen un problema para la salud de la poblacioacuten
Capiacutetulo 1
24
humana sino para la de todo el ecosistema playa El enriquecimiento orgaacutenico
producido como consecuencia es una de las principales causas de alteracioacuten en la
ocurrencia distribucioacuten y abundancia de la fauna bentoacutenica costera (Ferreira et al
2011) De hecho las aacutereas extremadamente contaminadas sufren una peacuterdida de
diversidad dado que solo unas pocas especies son capaces de tolerar tales
concentraciones de contaminantes Esto modifica los procesos ecoloacutegicos y reducen la
complejidad de las redes troacuteficas de estos ecosistemas (Lerberg et al 2000) Otra de
las fuentes de contaminacioacuten potencialmente destructiva son los derrames de
petroacuteleo que ademaacutes de tener un efecto toacutexico por los hidrocarburos aromaacuteticos
generan efectos fiacutesicos que producen la obstruccioacuten de los mecanismos de alimentos
de organismos filtradores Todo esto resulta en un disminucioacuten de los paraacutemetros
ecoloacutegicos asiacute como en un reduccioacuten yo extincioacuten de especies bentoacutenicas (Veiga et al
2009)
La transformacioacuten que sufren las aacutereas costeras unido a la mala gestioacuten que se
hace en ellas provocan que la erosioacuten sea otro gran problema al que se encuentran
sometidas las playas En 1996 ya se estimaba que el 70 de los intermareales
presentaban problemas erosivos (Bird 1996) La utilizacioacuten de sedimento como
relleno para elevar y aumentar la extensioacuten de las playas o tambieacuten llamado
regeneracioacuten es una de las teacutecnicas maacutes utilizadas para combatir la peacuterdida de playa El
efecto maacutes evidente de la regeneracioacuten sobre la macrofauna de playas estaacute
relacionado con el espesor de la capa de sedimento que se deposita que suele variar
de uno a cuatro metros siendo estos uacuteltimos los maacutes utilizados (Menn et al 2003) La
mayoriacutea de los invertebrados son incapaces de tolerar una sobrecarga de arena de maacutes
de 1 metro por lo que cabe suponer que la mayoriacutea de la macrofauna no sobreviviraacute al
proceso de regeneracioacuten (Leewis et al 2012) Estos efectos pueden ser agravados si se
producen cambios en las caracteriacutesticas del sedimento (tamantildeo medio de grano
coeficiente de seleccioacutenhellip) cambios en la morfologiacutea de la playa o modificacioacuten de la
pendiente dado la estrecha relacioacuten que existe entre las caracteriacutesticas fiacutesicas de la
playa y la macrofauna que las habita Ademaacutes la maquinaria utilizada tambieacuten es una
importante fuente de mortalidad por aplastamiento y de compactacioacuten de sedimento
que afecta a los espacios intersticiales capilaridad retencioacuten de agua permeabilidad e
intercambio de gases y nutrientes (Peterson et al 2000)
Capiacutetulo 1
25
33 Desarrollo costero e infraestructuras
Otra de las soluciones maacutes ampliamente utilizada para combatir el creciente
problema erosivo es la construccioacuten de las llamadas estructuras artificiales de
defensa siendo las maacutes empleadas los diques espigones y rompeolas Los espigones
son estructuras perpendiculares a la costa disentildeadas para acumular sedimento
Aunque esta funcioacuten soacutelo se consigue hacia un lado del espigoacuten en la direccioacuten de la
corriente mientras que al otro lado de la estructura se favorece la erosioacuten (Nordstrom
2013) Los espigones ademaacutes cambian los patrones de refraccioacuten de las olas producen
corrientes de resaca en sus inmediaciones y ademaacutes crean diferencias de pendientes y
de sedimento entre ambos lados del espigoacuten
Los diques por otro lado son estructuras paralelas a la costa construidos
principalmente en las zonas urbanizadas para protegerlas de la accioacuten directa de las
olas Estas estructuras producen una peacuterdida constante de la playa ya que interrumpen
el importante transporte de sedimento con el sistema dunar que en la mayoriacutea de los
casos ya se encuentra destruido Por uacuteltimo los rompeolas son tambieacuten estructuras
construidas paralelas a la costa pero localizadas en alta mar ya sean sumergidas o no
con el objetivo de reducir o eliminar la energiacutea de las olas y contribuir a la deposicioacuten
de sedimento en las playas adyacentes
Todas estas estructuras causan cambios significativos en el haacutebitat y por tanto generan
importantes impactos ecoloacutegicos que pueden ser difiacuteciles de detectar a corto plazo
(Jaramillo et al 2002) La principal consecuencia de la construccioacuten de estas
estructuras es un estrechamiento de la playa peacuterdida de haacutebitat y una disminucioacuten
directa de la diversidad y abundancia de la biota La calidad del haacutebitat tambieacuten puede
verse desmejorada puesto que en playas modificadas se detecta una menor
deposicioacuten de material orgaacutenico marino (Heerhartz et al 2014) esencial para el
correcto funcionamiento troacutefico de estos ecosistemas
Capiacutetulo 1
26
34 Explotacioacuten
La pesqueriacutea artesanal de invertebrados o marisqueo es la forma maacutes comuacuten
de explotacioacuten en las playas y pueden tener un impacto significativo en la fauna Las
especies objetivo del marisqueo no ocurren de igual manera en toda la playa sino que
se distribuyen a parches por lo que la extraccioacuten intensiva puede agotar las
agrupaciones maacutes densas y alterar el reclutamiento Estas actividades tambieacuten causan
mortalidad accidental tanto de las especies objetivo como de las que no lo son y
pueden alterar el sedimento con la remocioacuten lo que puede reducir la calidad del
haacutebitat y la idoneidad para el desarrollo normal de las especies (Defeo et al 2009)
35 Cambio climaacutetico
El calentamiento global debido a la liberacioacuten de gases de efecto invernadero y
en particular al dioacutexido de carbono unido a la destruccioacuten masiva de bosques genera
problemas reales y sustanciales para el medio ambiente (Brown y McLachlan 2002)
Aunque los cambios fiacutesicos en respuesta al cambio climaacutetico global son auacuten inciertos
en las playas arenosas la respuesta ecoloacutegica como cambios en la fenologiacutea fisiologiacutea
rangos de distribucioacuten y en la composicioacuten de las comunidades son cada vez maacutes
evidentes El aumento de la temperatura puede ser un factor criacutetico para muchas
especies de macrofauna y especialmente para las endeacutemicas ya que la mayoriacutea no
presenta estadiacuteos larvarios dispersivos que le permitan ampliar su rango de
distribucioacuten a otras aacutereas donde las caracteriacutesticas ambientales fueran maacutes acordes a
sus necesidades fisioloacutegicas Los cambios de temperaturas producen ademaacutes
modificaciones significativas en el sistema planctoacutenico y como consecuencia en las
poblaciones bentoacutenicas de playas dada la importancia que tiene el plancton como
fuente de alimento Otra de las consecuencias del cambio climaacutetico es el aumento del
nivel del mar debido a la expansioacuten teacutermica de los oceacuteanos y al derretimiento de los
glaciares terrestres y del casquete polar antaacutertico Este aumento genera una migracioacuten
progresiva de las playas hacia el interior lo que resulta imposible en costas
urbanizadas por lo que la desaparicioacuten de las mismas seraacute la consecuencia maacutes
probable
Capiacutetulo 1
27
4 Objetivos y estructura de la tesis
A lo largo de esta introduccioacuten se ha podido comprobar que las playas arenosas
son ecosistemas extremadamente complejos y variables habitados por una gran
diversidad de vida bien adaptada al dinamismo predominante y con una estructura
bien definida principalmente en respuesta a los factores fiacutesicos Existe una creencia
general de que los mejores servicios que pueden proporcionar las playas son los
relacionados con la recreacioacuten pero estos ecosistemas presentan innumerables
funciones muchas de las cuales son esenciales para los humanos A pesar de ello las
playas se encuentran sometidas a una importante transformacioacuten debido al intenso
desarrollo costero y al uso que se hace de estos ecosistemas que afectan de igual
modo a sus caracteriacutesticas fiacutesicas bioloacutegicas y ecoloacutegicas Un hecho indiscutible es que
la modificacioacuten de estas caracteriacutesticas naturales tendraacute una repercusioacuten directa sobre
aquellos factores socio-econoacutemicos de las playas tan valorados por la sociedad actual
La realizacioacuten de esta tesis doctoral tiene el principal objetivo de colaborar en la
evaluacioacuten de las condiciones ambientales de las playas de Andaluciacutea Occidental hasta
la fecha desconocidas que sirva como base para determinar las consecuencias de las
interferencias antropogeacutenicas en las playas y en los riesgos que sufren estos
ecosistemas por la falta de normas especiacuteficas para la proteccioacuten de su biodiversidad y
de su equilibrio bioloacutegico Asiacute en primer lugar se analizan las comunidades de
macrofauna de 12 playas de Andaluciacutea Occidental sus patrones de zonacioacuten y las
variables abioacuteticas maacutes influyentes en esta distribucioacuten asiacute como las principales
caracteriacutesticas fiacutesicas y morfodinaacutemicas de dichas playas (Capiacutetulo 2) Con este primer
capiacutetulo se pretende informar acerca de la gran biodiversidad que habita nuestros
intermareales arenosos Los siguientes capiacutetulos estaacuten centrados en las consecuencias
sobre las caracteriacutesticas bioacuteticas principalmente de determinadas actividades
humanas Asiacute en el Capiacutetulo 3 se evaluacutea el efecto del pisoteo humano en los
paraacutemetros comunitarios y en la estructura taxonoacutemica de la comunidad A la vez que
se trata de determinar a un nivel poblacional queacute especies son las maacutes vulnerables a
este tipo de impacto El Capiacutetulo 4 muestra el efecto de la urbanizacioacuten costera a una
escala ecosisteacutemica es decir las implicaciones de esta actividad en la estructura
4 Objetivos y estructura de la tesis doctoral
Capiacutetulo 1
28
troacutefica en el funcionamiento y en los flujos de energiacutea de las playas Seguidamente en
el Capiacutetulo 5 se investiga el resultado de la construccioacuten de estructuras de defensa en
este caso un espigoacuten en las variables fiacutesicas y bioloacutegicas de las playas Por uacuteltimo en
esta Tesis doctoral se resalta la capacidad de adaptacioacuten de algunas especies que se
aprovechan de las actividades humanas realizadas en las playas para su propia
supervivencia Asiacute en el Capiacutetulo 6 se describe la actividad del gasteroacutepodo Cyclope
neritea en presencia de mariscadores como un ejemplo de facilitacioacuten troacutefica
Capiacutetulo 1
29
5 Bibliografiacutea
A
Artes K Vanarte T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-Rodriguez MP Calderoacuten J and Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-
B
Bird ECF 1996 Beach management Geostudies John Wiley amp Sons Ltd Chichester Bishop JD Hartley JP 1986 Comparison of the fauna retained on 05 mm and 10 mm
meshes form benthic samples taken in the Beatrice Oilfield Moray Firth Scotland Proceeding of the Royal Society of Edinburgh 91 247-262
Brazeiro A Defeo O 1996 Macroinfauna zonation in microtidal sandy beaches is it possible to identify patterns in such variable environments Estuarine Coastal and Shelf Science 42 523-536
Brown AC McLachlan A 2002 Sandy shore ecosystems and the threats facing them some predictions for the year 2025 Environmental Conservation 29 62-77
Bulleri F Chapman MG 2010 The introduction of coastal infrastructure as a driver of change in marine environments Journal of Applied Ecology 47 26ndash35
Burke L Kura Y Kasem K Revenga C Spalding M McAllister D 2001 Coastal Ecosystems Washington DC World Resources Institute 93 pp
C Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination
of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloS One 6 e23724
Colombini I Chelazzi L 2003 Influence of marine allochthonous input on sandy beach communities Oceanography and Marine Biology an Annual Review 41 115ndash159
D Dal E 1952 Some aspects of the ecology and zonation of the fauna of sandy beaches Oikos
4 1-27 Dean RF 1973 Heuristic models of sand transport in the surf zone Proceedings of
Conference on Engineering Dynamics in the Surf Zone Sydney pp 208-214 Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy
beaches macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
F Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human
use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira JG Andersen JH Borja A Bricker SB Camp J Cardoso da Silva M Garceacutes E Heiskanen AS Humborg C Ignatiades L Lancelot C Menesguen A Tett P
5 Bibliografiacutea
Capiacutetulo 1
30
Hoepffner N Claussen U 2011 Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive Estuarine Coastal and Shelf Science 93 117ndash131
G Gourlay MR 1968 Beach and dune erosion test Delft Hydraulics Laboratory Report nordm
M935M936 H Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline
Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 1256-1268
Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a high-energy beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585
J Jaramillo E Contreras H Bollinger A 2002 Beach and faunal response to the construction
of a seawall in a sandy beach of south central Chile Journal of Coastal Research 18 523ndash529
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Bodegoma PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lerberg SB Holland AF Sanger DM 2000 Responses of tidal creek macrobenthic communities to the effects of watershed development Estuaries 23 838 ndash 853
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Llewellyn PJ Shackley SE 1996 The effects of mechanical beach-cleaning on invertebrate populations British Wildlife 7 147ndash155
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological Economics 63 254-272
Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and morphology a conceptual beach model Journal of Coastal Research 9 785-800
McLachlan A 1983 Sandy beach ecology ndash a review InMcLachlan A Erasmus T (eds) Sandy beaches as ecosystems Junk The Hague pp 321ndash380
McLachlan A Jaramillo E Donn TE Wessels F 1993 San beach macrofauna communities a geographical comparison Journal of Coastal Research 15 27-38
McLachlan A Turner J 1994 The interstitial environment of sandy beaches PZNI Marine Ecology 15 177-211
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21674ndash687
Capiacutetulo 1
31
McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington MA USA
Menn I Junghans C Reise K 2003 Buried alive effects of beach nourishment on the infauna of an erosive shore in the North Sea Senckenbergiana Marina 32125ndash45
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
N
Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal and Shelf Science 150 11-23
P Peterson CH Bishop MJ Johnson GA DrsquoAnna LM Manning LM 2006 Exploiting
beach filling as an unaffordable experiment benthic intertidal impacts propagating upwards to shorebirds Journal of Experimental Marine Biology and Ecology 338 205ndash221
Peterson CH Hickerson DHM Johnson GG 2000 Short-term consequences of nourishment and bulldozing on the dominant large invertebrates of a sandy beach Journal of Coastal Research 16368ndash78
S Salvat B 1964 Les conditions hydrodynamiques interstitielles des sediments meubles
intertidaux et la repartition verticale de la fauna endogee Academic das Sciences (Paris) Comptes Rendus 259 15761579
Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal zonation metrics and their variability Marine Ecology Progress Series 47843-55
Soares AG 2003 Sandy beach morphodynamics and macrobenthic communities in temperate subtropical and tropical regions ndash a macroecological approach Tesis doctoral University of Port Elizabeth South Africa
V Veiga P Rubal M Besteiro C 2009 Shallow sublittoral meiofauna communities and
sediment polycyclic aromatic hydrocarbons (PAHs) content on the Galician coast (NW Spain) six months after the Prestige oil spill Marine Pollution Bulletin 58 581-588
Veloso VG Caetano CHS Cardoso RS 2003 Composition structure and zonation of intertidal macroinfauna in relation to physical factors in microtidal sandy beaches at Rio de Janeiro State Brazil Scientia Marina 67 393-402
Verhulst S Oosterbeek K Ens BJ 2001 Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers Biological Conservation 101 375ndash380
W Weslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus saltator
Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 2977-87
Capiacutetulo 1
Capiacutetulo 2 Biodiversity and distribution of macrofauna assemblages on
sandy beaches along the Gulf of Caacutediz (SW Spain)
Capiacutetulo 2
33
Abstract
To date biodiversity and zonation patterns of macrofauna in sandy beaches
along the coast of the Gulf of Caacutediz (SW Spain) have never been analysed In the
current study the macrofauna communities inhabiting sandy beaches and their
environmental characteristics are described Mapping is an useful tool for future
protection and conservation strategies and to estimate the response of biota to
habitat changes A total of 66 macrofauna taxa were recorded in 12 sandy beaches
ranging from 4 to 33 species Abundance reached 932 specimens The individual
zonation pattern ranged from two or three zones regardless of the morphodynamic
state A common zonation pattern of the whole set of beaches was established
comprising three across-shore biological zones Generally the supralittoral zone was
typified by the air-breathing amphipod (Talitrus saltator) and Coleoptera
Curculionidae The middle zone was dominated by true intertidal species such as
Haustoriidae amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis)
Spionidae polychaetes (Scolelepis squamata) and Nemerteans and the lower or
sublittoral zone was typified by Pontoporeiidae amphipods mysids and spionid
polychaetes Sediment moisture average grain size organic-matter content and
elevation were the main predictor variables of zonation patterns
Keywords sandy beaches benthic macrofauna zonation pattern environmental
variables Gulf of Cadiz
Capiacutetulo 2
34
1 Introduction
The Gulf of Cadiz is located in the south-western Iberian Peninsula between
Cape St Vincent (Portugal) and the Strait of Gibraltar (Spain) which connects the
Atlantic Ocean and Mediterranean Sea The Spanish coastal area of this gulf stretches
some 300 km between Ayamonte (Huelva province) and Tarifa (Cadiz province) The
area is influenced mainly by the mouths of the rivers Guadiana Piedras Tinto Odiel
Guadalete and Guadalquivir and is dominated by estuarine zones and extensive sandy
beaches many of which are faced by discontinuous rocky-shore platform (Benavente
et al 2002) especially on the Cadiz coast
The general circulation in the Gulf of Cadiz is predominantly anticyclonic with
short-term variation influenced by winds This region is characterized by a mean water-
surface temperature ranging from 18ordmC to 22ordmC a salinity range of 363 to 365permil and
average nutrient concentration (nitrate phosphate and silicate) about 033 008 137
μM respectively (Anfuso et al 2010) with a chlorophyll-a concentration of around 10-
40 mgm2 (Prieto et al 1999) These features provide a suitable habitat for the
development of several species which make this system a very diverse and productive
area (Sobrino et al 1994) Many species inhabiting the Gulf of Cadiz have economic
value therefore the Gulf of Cadiz is considered an area with great socio-economic
importance in fisheries and shellfish gathering (Torres et al 2013) Frequently these
species use sandy shores as nursery areas of juveniles (Baldoacute and Drake 2002) feeding
on invertebrates (Speybroeck et al 2007) and can use biogenic structures (eg tubes
mounds burrows) constructed by the invertebrates as refuge from predation (Allen
Brooks et al 2006)
Furthermore the shores provide a large range of services to the ecosystem as
sediment and water storage decomposition of organic matter and pollutants wave
dissipation water filtration and purification nutrient recycling maintenance of
biodiversity and functional link between marine and terrestrial environments where
macrofauna plays a key role (Defeo et al 2009) Moreover in Spain the favourable
climatic conditions make the coastal environments attractive to the tourism for several
1 Introduction
Capiacutetulo 2
35
months per year and beaches constitute a major economic resource (Anfuso et al
2003)
Despite the importance of the sandy beaches and the amplitude of coastal line
area occupied in the study area data on biotic and abiotic characteristics are scarce
On the Spanish Gulf of the Cadiz coast works have focused on studying the physical
characteristics of sandy beaches in restricted areas in relation to their
morphodynamics (Anfuso et al 2003) and their morphological changes associated
with meteorological events (Buitrago and Anfuso 2011) The few studies that have
described the fauna inhabiting the beaches have focused on macrofauna from
estuarine beaches (Mayoral et al 1994) or on the supralittoral arthropods associated
with wrack deposits (Ruiz-Delgado et al 2014) Thus regarding macrofaunal
community there is a notable lack of information in this region
Increasing human interest in sandy beaches mainly for leisure and the
associated urbanization which involves destruction of natural environments makes it
necessary to identify and map the macrofauna inhabiting sandy beaches as well as to
establish management tools for a better use of these marine environments
environment (Martins et al 2013) and to estimate the potential response of biota to
future habitat changes
The aim of this study is provide the first description of macrofauna
communities inhabiting sandy beaches and their environmental characteristics For
this (1) the physical and morphodynamic characteristics of 12 sandy beaches along
Gulf of Cadiz coast were defined (2) the macrofauna communities inhabiting sandy
beaches were characterized (3) the zonation pattern of macrofauna was determined
and (4) the influence of environmental factors on the zonation patterns were explored
Capiacutetulo 2
36
2
21 Study area
The study area comprises 12 sandy beaches along the Spanish coast of the Gulf
of Cadiz from Hoyo beach (37ordm 11 55 N - 07ordm 17 45 W) near to the border of
Portugal to Los Lances beach (36ordm 02 31 N - 05ordm 38 08031 W) in the area near the
Strait of Gibraltar (Fig 1)
22 Sampling procedures
The beaches were sampled during spring low tides between March-May 2011
Six transects were established perpendicular to shoreline spaced over a 100-m-long
Fig1 Study area showing the 12 sandy beaches sampled
2 Material and Methods
Capiacutetulo 2
37
stretch on each beach Each transect was divided into 10 equidistant sampling levels to
cover the entire intertidal area (Fig 2) The first sampling level was located in the
swash zone and the last one meter above the highest tide line At each sampling
level samples were collected with a 25-cm-diameter plastic core to a depth of 20 cm
A total of 60 samples were collected within a total sampled area of 375 m2 per beach
In temperate beaches this area is considered sufficient to collect 90 of all the
macrofauna (Jaramillo et al 1995) Samples were sieved on site through a 1 mm
mesh-sized sieve collected in a labelled plastic bag and preserved in 70 ethanol
stained Rose Bengal Additionally one sediment sample was taken at each sampling
level with a plastic tube (35 cm diameter) buried 15 cm deep to analyse the mean
grain size sorting coefficient (Trask 1950) sand moisture and organic matter of the
sediment
In the laboratory the macrofauna were quantified and identified to the lowest
taxonomic level possible The mean-grain-size was determined following the method
proposed by Guitiaacuten and Carballas (1976) This method discriminates different
granulometric fractions when the sediment composition is mainly sand and the pelitic
fraction is low (less than 5) Sand moisture was determined measuring the weight
loss after drying the samples at 90degC The organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC
To characterize the morphodynamic state the relative tidal range (RTR)
(Masselink and Short 1993) the Beach Index (BI) (McLachlan and Dorvlo 2005) the
Beach State Index (BSI) (McLachlan et al 1993) and the dimensionless fall-velocity
parameter (Deanrsquos parameter) (Dean 1973) were used The beach face slope was
estimated by the height difference according to Emery (1961) The height and wave
period were taken from an oceanographic database of Puertos del Estado (Spanish
Ministry of Public Works)
Capiacutetulo 2
38
23 Data analysis
Univariate analyses were used to characterize the faunal communities present
in each beach studied calculating the Margalef species for richness index (d) Shannon-
Wiener for the diversity index (H) and Pielou for the evenness index (J) using the
PRIMER software package
The zonation pattern in each beach studied was identified using cluster
analysis based on the BrayndashCurtis similarity matrix followed by a similarity profile test
(SIMPROF) (Clarke and Gorley 2006) to evaluate the significance of the classification
(plt005) Previously abundance data were fourth-root transformed to down weight
the contribution of the major abundant species
Once the zonation patterns were defined in each beach a modal pattern of
zonation was established for the entire set of beaches For this species from each
sampling level were pooled based on zones identified by cluster analysis Then a single
matrix of ldquospecies x zonerdquo for each beach was generated and all of them were
combined into a global matrix This global biological matrix was fourth-root
transformed and subjected to non-metric multi-dimensional scaling ordination (n-
MDS) Furthermore the similarity percentages analysis (SIMPER) in order to find the
typifying species in each zone established for the entire set of beaches from the Gulf of
Cadiz were performed Beaches that did not present a clear zonation pattern were
Fig2 Sampling procedure on each beach
Capiacutetulo 2
39
excluded from these analyses All multivariate analyses were performed with PRIMER-
E v61 (PRIMER-E ltd) (Clarke and Warwick 2001)
To determine associations of macrofauna communities with environmental
variables a canonical correspondence analysis (CCA) was applied (Ter Braak 1986)
First a global biological matrix was submitted to detrended correspondence analysis
(DCA) in order to measure the gradient lengths and to ensure an unimodal species
response Gradient length of the first axis was greater than 30 SD and a CCA
ordination method was used For this analysis only the most abundant species were
taken into account (gt 6 of total contribution in each biological zone identified) after
fourth-root transformation
Environmental parameters matrix was transformed (Log (x+1)) and
standardized prior to reducing extreme values and providing better canonical
coefficient comparisons Only variables significantly related with the fauna variation
were included (plt 005) for this each variable was analysed separately and its
significance was tested using a Monte Carlo permutation test (999 permutations) (Ter
Braak 1995)
In CCA analysis the statistical significance of canonical eigenvalues and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
3
31 Beach characteristics
The physical characteristics of the 12 beaches studied are shown in Table 1 The
slope of the beaches ranged from 1109 at Hoyo beach to 1843 at Cortadura The
mean grain size classified according to the Wentworth scale ranged from coarse sand
in Hoyo and Zahara beaches to fine sand in La Bota Valdelagrana Levante Cortadura
Los Lances La Barrosa and Costa Ballena The sorting coefficient varied from
3 Results
Capiacutetulo 2
40
moderately good (125) to moderate (160) Organic-matter content in the entire set of
beaches was low from 031 in Matalascantildeas to 292 in La Barrosa
According to the tidal range (TR) and relative tidal range (RTR) the beaches
were categorized as mesotidal dominated by waves The beaches showed a wide range
of morphodynamic types classified by Deanrsquos parameter as intermediate (La Barrosa
Matalascantildeas Mazagoacuten El Terroacuten and Zahara) dissipative (Cortadura Costa Ballena
La Bota Levante Los Lances and Valdelagrana) and reflective (El Hoyo) BSI index
values classified most of beaches as intermediate to dissipative with high energy
except for Zahara and Hoyo which were intermediate beaches with lower-middle
energy
Table 1 Physical characterization of studied beaches a Beach length (m) b Median grain size (mm) c Organic matter content ()
32 Macrofauna
A total of 63 macrofauna taxa were recorded from the beaches of the Gulf of
Cadiz (Table A1) Crustaceans were the most diverse taxa with 23 species followed by
polychaetes (22 species) insects and molluscs (9 and 8 species respectively) Table A1
shows the total abundance total species Margalefrsquos species richness Shannon-Wiener
Beaches L a Slope(1m) Mgs b Sand type Sorting Dean RTR BI BSI OM c
Cortadura 2500 8431 020 fine 125 773 202 281 155 081
Costa Ballena 4500 2999 023 fine 135 591 227 231 143 068
Hoyo 2800 1099 065 coarse 154 16 227 136 092 062
La Barrosa 4000 176 047 medium 155 242 205 176 103 292
La Bota 3800 4659 022 fine 133 523 27 251 136 089
Levante 4600 2646 022 fine 143 632 249 225 142 075
Los Lances 4300 2476 023 fine 135 641 107 194 119 057
Matalascantildeas 4200 1397 041 medium 134 259 234 177 11 031
Mazagoacuten 5500 1584 049 medium 157 21 241 175 105 062
El Terroacuten 3500 2952 042 medium 145 253 227 209 109 048
Valdelagrana 1880 1769 021 fine 16 68 228 211 148 119
Zahara 2900 115 051 coarse 175 226 158 143 093 083
Capiacutetulo 2
41
diversity index and Pieloursquos evenness index La Bota and Levante had the highest
richness with 33 and 24 species respectively while the lowest value was found in
Matalascantildeas (4 species) The abundance was also highly variable ranging from 85 to
932 individuals The lowest value of diversity (H) were observed in Matalascantildeas
beach (040) while the highest value was found at Levante beach (268) The evenness
index ranged from 029 to 086
In terms of density the polychaete Scolelepis squamata was dominant
assuming 28 of total density followed by the amphipods Haustorius arenarius and
Siphonoecetes sabatieri each accounted for 15 of the total On the other hand
Scolelepis squamata Pontocrates arenarius and Haustorius arenarius were the most
frequent species (present in the 100 and the 90 of the total beaches sampled
respectively) although their abundance varied between beaches
33 Zonation
Across-shore species distribution in each beach studied is shown in Fig 3
Cluster ordination and SIMPROF test identified beaches with two biological zones such
as Cortadura Los Lances and Valdelagrana and with three zones such as Costa
Ballena Hoyo La Barrosa La Bota Levante Mazagoacuten El Terroacuten and Zahara
Exceptionally Matalascantildeas did not present a clear zonation pattern For this analysis
the sampling levels where no species were presented were removed
Capiacutetulo 2
42
Fig3 Zonation pattern in each studied beach defined by similar profile (SIMPROF) Black lines represent significant evidences of community structure (plt005) Red lines indicate no significant evidences
Capiacutetulo 2
43
Fig3 Continued
Fig3 Continued
Capiacutetulo 2
44
C1
Cb1H1Ba1
Bo1
Le1La1
M1
T1
V1
Z1
C2Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2Cb3H3
Ba3
Bo3
Le3
La3
M3
T3
Z3
2D Stress 018
A global zonation pattern of the entire set of beaches from Spanish Gulf of Cadiz
coast could be derived from the individual across-shore species distribution therefore
faunal zones identified at each beach were gathered for a global MDS ordination (Fig
4) SIMPER analysis performed on this ordination showed a degree of similarity
between all lower zones of 40 where Pontocrates arenarius Gastrosaccus sanctus
and Scolelepis squamata registered the highest percentages of contribution (178
172 and 110 respectively) The middle zones presented a similarity of about 30
The polychaeta Scolelepis squamata (3770) the isopod Eurydice affinis (2640) the
amphipod Haustorius arenarius (1156) and Nemerteans (995) highlighted the
similarity in faunal composition between all middle zones Finally upper zones showed
a 20 similarity and the typifying species were the air-breathing amphipod Talitrus
saltator (567) and the Coleoptera Curculionidae (34)
Fig4 n-MDS ordination for the global zonation pattern Black triangles represent the lower zones gray inverted triangles correspond to the middle zones and black quadrate represent the upper zones of the whole studied beaches
Capiacutetulo 2
45
Biologically density values decreased from the lower to the upper zone In the
lower and middle zones the most abundant taxa were crustaceans and polychaetes
while in the upper zones besides crustaceans insects were dominant (Fig 5)
34 Relationship between environmental variables and macrofauna
Environmental variables significantly related to the fauna variation tested by
Monte Carlo permutation test were elevation (p=0002) sand moisture (p=0001)
organic-matter content (p=0015) and grain size (p=0001) However these predictor
variables were not strongly correlated (r2lt 05) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0001) and for eigenvalues
(p=0001) showing a significant relationship between biological data and predictor
environmental variables
Faunal Zone
Den
sity (
ind
m2)
0
20
40
60
80
100
120
Crustacea
Polychaeta
Insecta
Mollusca
Nemertea
Lower Middle Upper
Fig5 Mean total density (plusmn SE) of the taxa found in the lower middle and upper zones
Capiacutetulo 2
46
CCA results show that the total variation of data was 249 (inertia) while the
total variation explained was 0802 (sum of all canonical eigenvalues) Pearson species-
environmental correlations were relatively high 093 for Axis 1 and 082 for Axis 2 The
first axis explained 66 of the total variation explained and correlated positively with
elevation (0745) and negatively with sand moisture (-0887) and organic-matter
content (-0465) The second axis accounted for some 20 of total variation explained
and correlated mainly with medium grain size (0806)
The ordination diagram of CCA (Fig 6) presented a gradient of zones (lower
middle and upper) marked mainly by the first axis and showed that crustaceans
(Bathyporeia pelagica Eurydice affinis E pulchra Gastrosaccus sanctus G spinifer
Haustorius arenarius Pontocrates arenarius and Siphonoecetes sabatieri) and
polychaeta (Scolelepis squamata) responded positively to sand moisture and organic-
matter content but responded negatively to elevation increasing their density to the
left along the first axis Coleoptera and Talitrus saltator exhibited the opposite pattern
Density of Nemerteans was the least explained by these environmental variables
Nemerteans P arenarius S sabatieri and G sanctus also responded positively
to medium-coarse grain size while the density of Bathyporeia pelagica Donax
trunculus and Coleoptera sp 1 were more influenced by fine grain size due to their
distribution along the second axis
4
41 Macrofauna
This study describes for the first time the macrofauna communities that
inhabit the sandy beaches from Spanish coast of the Gulf of Cadiz Due to the
widespread geographic distribution and the different physical characteristics of the
selected sandy beaches the results of the current study can be considered a good
characterization of the whole community in the study area
4 Discussion
Capiacutetulo 2
47
Fig6 Triplot resulting from CCA analysis Crosses show the most abundant species in each zone The lower zones are represented by triangles middle zones by inverted triangles and upper zones by circles Arrows represent explanatory variables (Moist= Sand moisture Mgs= Median grain size Elev=Elevation OM= organic matter content)
C1
Cb1
H1
Ba1 Bo1
Le1
La1
M1
T1
V1
Z1
C2
Cb2
H2
Ba2
Bo2
Le2
M2
T2
V2
Z2
Cb3 H3
B3
Le3
La3 M3 T3
Z3
B pelagica
E affinis
E pulchra
G sanctus
G spinifer
H arenarius
P arenarius
S sabatieri
T saltator
S squamata
Coleoptera sp 2 Coleoptera sp 1
Curculinadae
P bimaculata
D trunculus
Nemertea
Elev
OM
Mgs
Moisture
Axis 1
Axis 2
Capiacutetulo 2
48
Since sandy beaches are extremely dynamic ecosystems with hostile conditions
for life the numbers of taxa adapted to live under these conditions are low compared
with other coastal systems however the study area showed relatively high species
richness (from 4 to 33 species) This value is similar to that reported in nearby
latitudes such as northern Spain where from 9 to 31 species have been found (Rodil
et al 2006)
Beaches showed a wide range of morphodynamic types and in general
terms a trend to increase species richness from reflective to dissipative beaches was
observed according to McLachlan et al (1993) La Bota showed the highest species
richness This beach is one of the most sheltered of the entire set of beaches located
near mouth of Piedras River where the influence of wave action is lower This is also
reflected in the RTR that presented high values in this sandy beach The highest
richness value found in La Bota supports the general trend of biotic variables to
increase with exposure as shown by other authors (Dexter 1992 Jaramillo and
McLachlan 1993 Rodil et al 2007) Although salinity is considered a factor related
negatively to species richness (Lercari and Defeo 2006) the mouth of Piedras river has
salinity values very close to those of the ocean (Mayoral et al 1994) Therefore a
possible effect of salinity would not be expected Abundance and richness of
macrofauna is higher where the food supply is higher (Rodil et al 2012) so that it is
also possible that the river mouth increases available food enabling the establishment
and development of more species Munilla and San Vicente (2005) showed that the
Catalan beaches nearest to Ebro River have the greatest density of species
Crustaceans polychaetes and molluscs were usually dominant among the
macrofauna of sandy beaches (McLachlan and Brown 2006) In our study amphipod
and isopod crustaceans and spionid polychaetes were the most abundant and diverse
taxa in fact 74 of all individuals collected belong to six species of these groups
Bathyporeia pelagica Haustorius arenarius Pontocrates arenarius Siphonoecetes
sabatieri Eurydice affinis and Scolelepis squamata
Little importance is given to Nemerteans which are normally not considered
typical taxa on sandy beaches due to residual contributions that they exhibit although
this taxon is considered a useful bioindicator (McEvoy and Sundberg 1993)
Capiacutetulo 2
49
On sandy beaches of south-western Spain Nemertean abundance was similar
to that of molluscs showing high occurrence (67 of the total sampled beaches)
highlighting the importance of Nemerteans in these latitudes Similarly Talitrus
saltator was frequently found on the sandy beaches studied This sand-hopper is
recognized as a good biomonitor of trace-metal pollution and the effect of human
trampling (Ugolini et al 2008)
The dominant and most frequent species occurring on every beach studied was
the polychaete Scolelepis squamata This species has a wide geographical distribution
(Souza and Borzone 2000) and is also the most abundant species in many beaches
around the world (Barros et al 2001 Degreaer et al 2003 Papageorgiou et al 2006)
42 Macrofauna Zonation
Faunal zonation is defined as the distribution of species throughout the
intertidal zone where each zone is inhabited by a characteristic species closely related
to the particular abiotic features of each area A recent study on macrofauna
assemblage distribution stated that traditional ways of establishing zonation pattern
such as kite diagrams and ordination techniques imply a high degree of subjectivity
(Veiga et al 2014) As a means of exploring the zonation patterns of sandy beaches
from the Spanish Gulf of Cadiz coast more formal tests (cluster analysis and SIMPROF)
were used for each beach with the goal to establishing an overall zonation pattern
that explains the distribution of macrofauna species on sandy beaches of this
geographical region
The zonation of macrofauna on sandy beaches has been undertaken around the
world (Defeo et al 1992 McLachlan 1996 Jaramillo et al 2000 Barros et al 2001
Rodil et al 2006 Gonccedilalves et al 2009 Schlacher and Thompson 2013 Veiga et al
2014) Macrofauna across-shore distribution is highly variable ranging from 1 to 5
zones although 3 biological areas are most common (see Schlacher and Thompson
2013) In the current study 67 of total beaches presented 3 distinct biological zones
and 25 showed 2 zones
Capiacutetulo 2
50
Jaramillo et al (1993) determined that intermediate and dissipative beaches
include three faunal zones whereas the reflective beaches have only two Along the
Spanish coast of Gulf of Cadiz this pattern was not found In fact the more dissipative
beaches showed two biological zones while beaches closest to the reflective state
(Hoyo and Mazagoacuten) had 3 zones In general terms the number of zones alternated
independently of the Dean parameter Thus no clear evidence was found to support
the contention that the number of zones is closely related to morphodynamics These
results corroborate the conclusion drawn by Schlacher and Thompson (2013) who
detected no significant correlation between habitat metric (habitat dimensions
sediment properties and morphodynamic state) and the number of faunal zones
Although the number of biological zones varied among beaches a common
zonation pattern was possible to establish for the entire set of beaches studied This
was performed in order to characterize the most typical species inhabiting each zone
The general pattern showed 3 biological zones In general the supralittoral zone was
typified by air-breathing amphipods (Talitrus saltator) and coleopteran Curculionidae
The middle zone was dominated by true intertidal species such as Haustoriidae
amphipods (Haustorius arenarius) Cirolanidae isopods (Eurydice affinis) Spionidae
polychaetes (Scolelepis squamata) and Nemerteans and the lower or sublittoral zone
was typified by amphipods belonging to Pontoporeiidae family mysids and spionid
polychaetes The distribution of the species in each zone corresponds to findings in
other nearby temperate sandy beaches such as in the northern coast of Spain Tunisia
and Morocco (Bayed 2003 Rodil et al 2006 Perez-Domingo et al 2008)
Diversity and densities of individuals increase towards the lower zones This is a
general feature found in numerous studies of sandy beaches worldwide (McLachlan
1990 Jaramillo et al 1993 Rodil et al 2006 Gonccedilalves et al 2009) Some authors
have determined that this pattern could be due to a reflection of the high subtidal
diversity and short periods to air exposure allowing more species to inhabit zones
closest to the seawater (Degraer et al 1999 Aerts et al 2004) The high abundance
found in the lower areas of all the beaches studied evidences how important these
environments are as potential sources of food to other predatory species (fish and
birds)
Capiacutetulo 2
51
43 Relationship between environmental variables and macrofauna
Distribution of macrofauna is related to the tolerance of these communities to
different environmental variables (McLachlan and Brown 2006) Although the
relationship between species and the environment could change with the scale of
study (Rodil et al 2012) abiotic predictor variables at the local scale were examined
Beach slope and grain size have been identified as main factors controlling the
macrofauna distribution throughout the intertidal zone (Jaramillo et al 1993
McLachlan et al 1993) Results from CCA analysis showed that sand moisture and the
organic-matter content in addition to the elevation and the grain size were the main
environmental variables controlling the macrofauna distribution across the shore in
sandy beaches of the Gulf of Cadiz coast
Lower and middle zones presented an internal gradient influenced mainly by
average grain size Thus species inhabit these zones were Pontocrates arenarius
Siphonoecetes sabatieri and Nemerteans closely related with coarse grain size while
Donax trunculus and Bathyporeia pelagica were related to fine grain size
The most abundant species in upper zone such as the talitrid amphipod Talitrus
saltator and coleopterans were positively correlated with elevation but negatively with
sand moisture and organic-matter content Grain size was not a good explanatory
variable for these species In fact Ugolini et al (2008) found no relationship between
sand-hopper abundance and the sand-grain size Although these species showed
significant relationship with abiotic variables other factors not taken into account
could affect the distribution of these species For example it has been reported that
stranded material (eg macrophytes macroalgae) provide a physical structure which
can be used as shelter or breeding site and as food source by supralittoral arthropods
(Colombini et al 2000) and the age of these deposits plays a significant role in the
structure of upper-shore assemblages (Ruiz-Delgado et al 2014)
In conclusion beaches from Spanish coast of Gulf of Cadiz are characterized by
high biodiversity including major bioindicator species and by a clear zonation of
macrofauna The overall distribution pattern involves three biological zones the
supralittoral zone typified by air-breathing amphipods and coleopterans the middle
Capiacutetulo 2
52
zone dominated by Haustoriidae amphipods Cirolanidae isopods Spionidae
polychaetes and Nemerteans and the sublittoral zone typified by amphipods
belonging to Pontoporeiidae family mysids and spionid polychaetes The macrofauna
across-shore distribution is influenced primarily by sand moisture organic-matter
content elevation and grain size Other factors such as wrack deposit and organic
inputs from rivers and estuaries could influence the abundance and distribution of
macrofauna inhabiting sandy beaches Thus future studies are needed to elucidate
whether the presence of stranded material could affect the global zonation patterns in
sandy beaches
Capiacutetulo 2
53
5
A Aerts K Vanagt T Degraer S Guartatanga S Wittoeck J Fockedey N Cornejo-
Rodriguez MP Calderoacuten J Vincx M 2004 Macrofaunal community structure and zonation of an Ecuadorian sandy beach (bay of Valdivia) Belgian Journal of Zoology 134 15-22
Brooks A R Purdy CN Bell SS Sulak KJ 2006 The benthic community of the eastern US continental shelf A literature synopsis of benthic faunal resources Continental Shelf Research 26 804-818
Anfuso E Ponce R Gonzaacutelez-Castro C Forja JM 2010 Coupling between the thermohaline chemical and biological fields during summer 2006 in the northeast continental shelf of the Gulf of Caacutediz (SW Iberian Peninsula) Scientia Marina 74 47 ndash 56
Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Bayed A 2003 Influence of morphodynamic and hidroclimatic factors on the macrofauna of
Moroccan sandy beaches Estuarine Coastal and Shelf Science 58 71-82 Baldoacute F Drake P 2002 A multivariate approach to the feeding habits of smallfishes in the
Guadalquivir Estuary Journal of Fish Biology 61 21-32 Barros F Borzone CA Rosso S 2001 Macroinfauna of Six Beaches near Guaratuba Bay
Southern Brazil Brazilian Archives of Biology and Technology 44 351-364 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Colombini I Aloia A Fallaci M Pezzoli G Chelazzi L 2000 Temporal and spatial use of
stranded wrack by the macrofauna of a tropical sandy beach Marine Biology 136 531-541
Clarke KR Gorley RN 2006 PRIMER v6 user manualtutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D Dean RG 1973 Heuristic models of sand transport in the surf zone Proceedings of a
Conference on Engineering Dynamics in the Surf Zone (Sydney) 208-214 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1-12
Defeo O Jaramillo E Lyonnet A 1992 Community structure and intertidal zonation of the macroinfauna on the Atlantic coast of Uruguay Journal of Coastal Research 8 830-839
5 References
Capiacutetulo 2
54
Degraer S Volckaert A Vincx M 2003 Macrobenthic zonation patterns along a morphodynamical continuum of macrotidal low tide barrip and ultra-dissipative sandy beaches Estuarine Coastal and Shelf Science 56 459-468
Degraer S Mouton I De Neve L Vincx M 1999 Community structure and zonation of the macroinfauna on the Antlantic coast of Uruguay Journal of Coastal Research 8 830-839
Dexter DM 1983 Community structure of intertidal sandy beaches in New South Wales Australia In McLachlan A and T Erasmus (Eds) Sandy Beaches as Ecosystems The Hague Junk
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
G Gonccedilalves SC Anastaacutecio PM Pardal AM Cardoso PG Ferreira SM Marques JC
2009 Sandy beach macrofaunal communities on the western coast of Portugal ndashIs there a steady structure under similar exposed conditions Estuarine Coastal and Shelf Science 81 555-568
Guitian FJ Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de Compostela Espantildea
J Jaramillo E McLachlan A Coetzee P 1993 Intertidal zonation patterns of macroinfauna
over a range of exposed sandy beaches in south central Chile Marine Ecology Progress Series 101 105-118
Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
Jaramillo E Duarte C Contreras H 2000 Sandy beaches macroinfauna from the coast of Ancud Isla Chiloeacute southern Chile Revista Chilena de Historia Natural 73 771-786
L Lercari D Defeo O 2006 Large-scale diversity and abundance trends in sandy beach
macrofauna along full gradients of salinity and morphodynamics Estuarine Coastal and Shelf Science 68 27-35
M Masselink G Short AD 1993 The effect of tide range on beach morphodynamics and
morphology a conceptual beach model Journal of Coastal Research 9 785-800 Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3 for Windows MjM Software Design Gleneden Beach Oregon
McEvoy EG Sundberg P 1993 Patterns of trace metal accumulation in Swedish marine nemerteans Hydrobiologia 226 273-280
Capiacutetulo 2
55
McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal sands Journal of Coastal Research 6 57-71
McLachlan A 1996 Physical factors in benthic ecology effects of changing sand particle size on beach fauna Marine Ecology Progress Series 131 205-217
McLachlan A Brown AC 2006 The ecology of sandy shores Elsevier Burlington McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities
Journal of Coastal Research 21 674-687 McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna
communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27-38
Munilla T San Vicente C 2005 Suprabenthic biodiversity of Catalan beaches (NW Mediterranean) Acta Oecologica 27 81-91
P
Papageorgiou N Arvanitidis C Eleftheriou A 2006 Multicausal environmental severity A flexible framework for microtidal sandy beaches and the role of polychaetes as an indicator taxon Estuarine Coastal and Shelf Science 70 643-653
Perez-Domingo S Castellanos C Junoy J2008 The sandy beach macrofauna of Gulf of Gabeacutes (Tunisia) Marine Ecology 29 51-59
Prieto L Garciacutea CM Corzo A Ruiz-Segura J Echevarriacutea F 1999 Phytoplankton bacterioplankton and nitrate reductase activity distribution in relation to physical structure in the northern Alboraacuten Sea and Gulf of Cadiz (southern Iberian Peninsula) Instituto Espantildeol de Oceanografiacutea 15 401-411
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodil IF Lastra M Loacutepez J 2007 Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain) Hidrobiologiacutea 579 301-316
Rodil IF Compton TJ Lastra M 2012 Exploring Macroinvertebrate Species distributions at Regional and Local Scales across a Sandy Beach Geographic Continuum PloS One (7) 6 e39609
Ruiz-Delgado MC Vieira JV Veloso VG Reyes-Martiacutenez MJ Azevedo IS Borzone CA Saacutechez-Moyano JE Garciacutea-Garciacutea FJ 2014 The role of wrack deposits for supralittoral arthropods An example using Atlantic sandy beaches of Brazil and Spain Estuarine Coastal and Shelf Science 136 61-71
S Schlacher TA Thompson L 2013 Spatial structure on ocean-exposed sandy beaches faunal
zonation metrics and their variability Marine Ecology Progress Series 478 43-55 Sobrino I Jimeacutenez MP Ramos F Baro J 1994 Descripcioacuten de las pesqueriacuteas demersales
de la Regioacuten Suratlaacutentica Espantildeola Instituto Espantildeol de Oceanografiacutea 151 3-79 Souza JR Borzone CA 2000 Population dynamics and secondary production of Scolelepis
squamata (Polychaeta Spionidae) in an exposed sandy beach of southern Brazil Bulletin of marine science 67 221-233
Speybroeck J Bonte D Courtens W Gheskiere T Grootaert P Maelfait JP Mathys M Provoost S Sabbe K Stienen EWM 2006 Beach nourishment an ecologically sound coastal defence alternative A review Aquatic Conservation Marine and Freshwater Ecosystems 16 419-435
Capiacutetulo 2
56
Speyboreck J Alsteens L Vincx M Degraer S 2007 Understanding the life of a sandy beach polychaete of functional importance - Scolelepis squamata (Polychaeta Spionidae) on Belgian sandy beaches (northeastern Atlantic North Sea) Estuarine Coastal and Shelf Science 74 109-118
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Ter Braak CJF 1995 Ordination In Jongman RHG ter Braak CJF van Tongeren OFR
(Eds) Data Analysis in Community and Landscape Ecology Cambridge University Press Cambridge United Kingdom pp 91
Torres MA Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Caacutediz ecosystem (South-western Spain) Ecological Modelling 26 26-44
Trask PD 1950 Applied sedimentation Jon Wiley and Sons Inc New York
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349-357
V Veiga P Rubal M Cacauelos E Maldonado C Sousa-Pinto I 2014 Spatial variability of
macrobenthic zonation on exposed sandy beaches Journal of Sea Research 90 1-9
Capiacutetulo 2
57
Species composition C CB H Ba Bo Le La Ma M T V Z
Crustacea
Ampelisca sp 1
Apherusa sp 1
Atylus swammerdami 1 1 9
Bathyporeia pelagica 4 66 28 23
Bodotria pulchella 3
Cumella pygmaea 10
Cumopsis fagei 1 1 2 1 1 1 1
Diogenes pugilator 35 1
Eocuma dollfusi 1 1
Eurydice affinis 19 3 10 6 17 10 19 42 2
Eurydice pulchra 1 12 12 9
Gastrosaccus sanctus 1 3 8 4 2 7 2 8 1 16
Gastrosaccus spinifer 2 6 3 4 18 7
Haustorius arenarius 68 352 1 19 16 2 15 8 1 6 1
Lekanesphaera cf weilli 7 17 1 5 7 11 1
Processa sp 1
Liocarcinus depuratus 1
Mysidae sp 2
Paguridae 1 1
Pontocrates arenarius 3 3 12 45 1 3 19 7 20 39 26
Portunnus latipes 2 6 2 1
Siphonoecetes sabatieri 8 436 6 21 11
Talitrus saltator 4 19 15 4 10
Polychaeta
Aponuphis bilineata 1
Capitella capitata 1
Dispio uncinata 1 4 2 4
Eteone sp 2
Flabelligeridae 2 8
Glycera capitata 3 5
Glycera tridactyla 5 4
Hesionides arenaria 2
Magelona papilliformis 9
Nephthys cirrosa 3 3 11 1 9
Nephthys hombergii 2
Onuphis eremita 7
Ophelia radiata 12
Paraonis fulgens 6 1
Phyllodocidae sp 19
6 Appendix
Table A1 Number of individual total species a Margalef species richness b
Shannon diversity index and c Pielou evenness index
Capiacutetulo 2
58
C CB H Ba Bo Le La Ma M T V Z
Saccocirrus sp 26 6 20 2 35
Scolelepis squamata 6 17 23 2 223 28 4 260 8 14 299 1
Spiophanes sp 3
Spionidae sp1 2
Spionidae sp2 1
Sthenelais boa 3
Terebellidae sp 1
Insecta
Carabidae sp 1
Coleoptera sp1 7
Coleoptera sp2 5
Curculionidae sp 1 1 1 3
Phaleria bimaculata 1 1
Pogonus sp 1
Scarabaeidae sp 1
Staphylinidae sp 1 1
Tenebrionidae sp 3
Mollusca
Chamaelea gallina 1
Corbula gibba 3
Donax trunculus 2 7 103 5 2 11 20
Mactra stultorum 1 4
Nassarius incrassatus 1
Nassarius vaucheri 4
Tapes sp 1
Tellina tenuis 2
Nemertea
Nemertea sp 82 1 9 1 1 1 9 54
Abundance 130 491 221 107 932 140 85 286 108 159 363 156
Total species 19 15 18 16 33 24 10 4 10 13 10 12
da 370 226 315 321 468 465 203 053 192 237 153 218
Hrsquob 184 111 215 195 176 268 198 040 192 206 081 179
Jc 062 041 074 070 050 084 086 029 083 080 035 072
Capiacutetulo 3 Response of intertidal sandy-beach macrofauna to human
trampling an urban vs natural beach system approach
Capiacutetulo 3
60
Abstract
Sandy beaches are subjected to intense stressors derived mainly from the
increasing pattern of beach urbanization also these ecosystems are a magnet for
tourists who prefer these locations for leisure and holiday destinations increasing the
factors adversely impinging on beaches This study evaluated the effect of human
trampling on macrofauna assemblages inhabit intertidal areas of sandy beaches using
a BACI design For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector with a low
density of users and a transitional area with high level of human occupancy Physical
variables were constant over time in each sector whereas differences in the intensity
of human use between sectors were found Density variations and changes in
taxonomic structure of the macrofauna over time were shown by PERMANOVA
analysis in the urban and transitional locations whereas the protected sector remained
constant throughout the study period The amphipod Bathyporeia pelagica appeared
to be unable to tolerate high human pressure intensities therefore the use as
bioindicator of these types of impact is recommended
Keywords Sandy beaches macrofauna bioindicator human trampling
tourism disturbance
Capiacutetulo 3
61
1
Ecosystems across the world are being damaged due to the rapid expansion of
the human population (Defeo et al 2009) Coastal areas are particularly vulnerable to
this phenomenon especially given that 41 of the global population lives within the
coastal limits (Martiacutenez et al 2007)
In addition to residential uses coastal areas ndash and sandy beaches in particular ndash
have long been a magnet for tourists (Jennings 2004) who prefer these locations for
recreational activities and holiday destinations Beach ecosystems are therefore
subjected to intense stressors as a result of increasing coastal infrastructure the
development of shoreline armoring beach nourishment resource exploitation
pollution and grooming (Schlacher et al 2007) These activities are mainly the result
of the increasing pattern of urbanization of beaches and the improvements of tourist
facilities This trend in which economic sustainability is preferred over biological
sustainability leads to substantial environmental costs (Davenport and Davenport
2006) that threaten the ecological integrity of coastal systems (Lucrezi et al 2009)
Tourism warrants particular attention since it is the economic engine of many
countries (Davenport and Davenport 2006) and involves large numbers of visitors to
beaches especially in the summer season The high level of human occupation can
disrupt coastal ecosystems through a wide range of activities such as camping
(Hocking and Twyfors 1997) the use of off-road vehicles (Schlacher and Thompson
2008) and other recreational pursuits (Fanini et al 2014) These actions can modify
the natural physical characteristics of beaches and have a direct effect on macrofauna
communities and their distribution patterns which can in turn result in a significant
loss of biodiversity (Defeo et al 2009) A direct effect of the various activities carried
out on beaches is human trampling The effect of trampling on faunal communities is
an important topic that has been addressed for different ecosystems such as rocky
shores (Ferreira and Rosso 2009) coral reefs (Rodgers and Cox 2003) and mudflats
(Rossi et al 2007) On sandy beaches this issue has been considered from different
perspectives for example at the population level the effect of human trampling has
been well analyzed for supralittoral species of talitrid amphipods (Weslawski et al
1 Introduction
Capiacutetulo 3
62
2000 Ugolini et al 2008 Veloso et al 2008 2009) or ocypodid decapods (Barros
2001 Lucrezi et al 2009) On the other hand at the community level the impact of
human trampling has been addressed both in controlled experiments (Moffet et al
1998) and by field observations involving comparison of highly trampled areas with
control zones (Jaramillo et al 1996 Veloso et al 2006) The results of these studies
have shown a decrease in the abundance of macrofauna within the trampled area
However this pattern cannot normally be directly attributed to trampling itself since
the highly trampled areas correspond to highly urbanized zones and the response of
species may thus be due to a set of influential factors inherent to coastal development
or lsquocompound threatsrsquo (Schlacher et al 2014) rather than to the isolated effect of
trampling To our knowledge only Schlacher and Thompson (2012) have evaluated the
isolated effect of trampling by comparing trampled (access point) and control areas on
a beach unmodified by human action However the temporal scale was not considered
in that study
When the effect of an impact is analyzed it is recommended that the
experimental designs consider samplings on different time-scales both before and
after a proposed development that may have an impact and on different spatial-scales
(Underwood 1994) The information obtained in this way can be used to distinguish
between natural changes and those that are attributable to impacts and it also allows
the magnitude of the impact to be measured (Underwood 1992)
BeforeAfterControlImpact (BACI) design enables the exploration of a wide
range of responses such as changes in abundance diversity richness biomass or
body condition (Torres et al 2011) BACI is therefore a robust design to detect human
impacts (Aguado-Gimeacutenez et al 2012)
Beach fauna plays a major role in the functioning of beach ecosystems
(McLachlan and Brown 2006) Benthos are involved in nutrient regeneration (Cisneros
et al 2011) they are trophic links between marine and terrestrial systems (Dugan
1999 Lercari et al 2010) and are stranded material decomposers (Dugan et al 2003
Lastra et al 2008) The identification of factors that cause disturbance is therefore a
crucial task in maintaining the continuity of sandy beach ecosystems If one primarily
considers human trampling supralittoral species have traditionally been viewed as
Capiacutetulo 3
63
highly vulnerable (McLachlan and Brown 2006) although the swash beach area which
is inhabited by the greatest diversity of macrofauna is most commonly used by people
(Schlacher and Thompson 2012) Studies aimed at determining the effects of
pedestrian activity with an emphasis on intertidal species are scarce despite their
potential as a tool in the design of management plans and conservation policies in
these ecosystems (Jaramillo et al 1996) The objective of the study reported here was
to quantify and evaluate the effect of human trampling on macrofauna assemblages
that inhabit the intertidal area of sandy beaches in a gradient of human pressure The
study was carried out using a BACI design In this context the trajectory of density
richness diversity index and community taxonomic structure were evaluated before
and after an episode of high tourist occupancy In addition the most vulnerable
species that can be considered as indicators of these types of impact were explored
2
21 Study area
The study was carried out in three sectors of a sandy beach with an
anthropogenic pressure gradient The beach is located in Caacutediz Bay in the
southwestern region of the Iberian Peninsula (Fig 1) Caacutediz Bay is a shallow (maximum
depth of 20 m) mesotidal basin (maximum tide 37 m) with a mean wave height of 1 m
(Benavente et al 2002) This coastal area has a subtropical climate with a mean
annual temperature of 19 ordmC and the prevailing winds blow from the West and East
(Del Riacuteo et al 2013)
The urban sector of Valdelagrana (36deg3413N 6deg1329W) has a high level of
urban development (housing and hotels) and high human occupancy during the
summer season The backshore is occupied by constructions and tourism
infrastructure (eg parking spaces streets boardwalks) which have destroyed the
vegetation cover and the dunes system (personal observation) Moreover this sector
2 Material and Methods
Capiacutetulo 3
64
is subject to daily mechanical grooming of beach sand to remove debris In contrast
Levante (36deg3253N 6deg1334W) is a pristine sector that belongs to a protected area
(Los Toruntildeos Metropolitan Park) In this area the salt-marsh system in the backshore
area is preserved (Veloso et al 2008) and there is a well-developed dune system that
reaches 2 m in height and 50 m in width with natural vegetation cover that is a key
area for nesting and shelter for marine birds species (Buitrago and Anfuso 2011) This
area can only be reached on foot The intermediate sector (36deg3338N 6deg1326W) is
located in the transitional area between Valdelagrana and Levante This area is not
urbanized and is located within Los Toruntildeos Metropolitan Park The backshore includes
a dune system with vegetation cover interrupted by an access path Visitors also have
other facilities and a tourist train transports people from the park entrance to this
sector The protected and intermediate sectors are manually groomed (daily) to
remove human debris selectively
Fig1 Study area showing Caacutediz Bay and locations of the 3 studied sectors Urban sector Valdelagrana (V) Protected sector Levante (L) and Intermediate sector (I)
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
V
I
L
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Capiacutetulo 3
65
22 Sampling procedures
The largest tourist influx in Spain occurs during the summer months (June to
August) As a consequence six sampling campaigns were conducted in each sector
(urban intermediate and protected) during spring tides three in each sector before
the tourist season (March April May 2011) and three in each sector after (September
October November 2011)
At each site six equidistant and across-shore transects were placed in a 100 m
long-shore area Each transect comprised 10 equidistant points from the high tide
water mark to the swash zone to cover the entire intertidal area At each sampling
level fauna samples were collected with a 25-cm diameter plastic core to a depth of
20 cm Samples were sieved on site through a 1-mm mesh sieve preserved in 70
ethanol and stained with Rose Bengal Sediment samples were also collected at each
sampling level with a plastic tube (35-cm diameter) buried at a depth of 20 cm The
beach-face slope was estimated by the height difference according to Emery (1961)
The macrofauna were quantified and identified in the laboratory and the
sediment characteristics (mean grain size sorting coefficient sand moisture and
organic matter content) were determined The mean grain size was determined by
sieving dry sediment through a graded series of sieves (5 2 1 05 025 0125 and
0063 mm) according to the method described by Guitiaacuten and Carballas (1976) Sand
moisture was measured by the weight loss after drying the sediment at 90 degC The
organic matter content was estimated as the difference between dry sediment weight
and sediment weight after calcination at 500 degC
The number of users observed at each sector was used as a proxy to quantify
the human trampling intensity A total of six human censuses were conducted three
censuses were performed (1 census per month at each sector) at the spring tide during
the period of the greatest inflow of visitors (June July and August 2011) and three
censuses were conducted before impact The counts were performed every 30
minutes for a 6 hour period (until high tide) and were conducted in the same zone as
the macrofauna sampling in an area of 50 m along the shore times beach width In addition
to the number of beach visitors the activities undertaken by them were recorded
Capiacutetulo 3
66
23 Data analysis
The potential impact of human trampling on the macrofauna assemblages was
analyzed using a modified BACI method that contrasts data from urban intermediate
and protected locations before and after the impact Here urban and protected zones
operate as impacted and control locations respectively The null hypothesis that
significant differences did not exist in the benthic assemblages and univariate
descriptors (density richness and Shannonrsquos diversity index) before and after the
impact period was tested separately for each sector
The design for the analyses included three factors Beach (Be three levels
urban intermediate and protected fixed) time (Ti two levels before and after
fixed) and sampling period (Sp six levels random and nested in Ti) According to this
approach the effect of human trampling is shown by a statistically significant lsquobeach times
timersquo interaction
The variation over time in the multivariate structure of macrofauna
assemblages and univariate variables was tested by permutational multivariate
analyses of variance (PERMANOVA) (Anderson 2001 2005) using 9999 permutations
An additional p-value obtained by the Monte Carlo test was used when the number of
permutations was not sufficient (lt150) Abiotic variables and human trampling
(number of people as a proxy) were subjected to the same design in order to detect
changes in the physical characteristics and number of users between sectors
Multivariate patterns were based on BrayndashCurtis dissimilarities and univariate
abiotic and human trampling analysis on Euclidean distance similarity matrices on
fourth-root transformed data for biotic measures When the interaction of interest
was significant post hoc pair-wise comparisons were performed to identify the
sources of these significant differences The homogeneity of dispersion was tested
using the PERMDISP routine (Anderson et al 2008)
A non-metric multidimensional scaling ordination (nMDS) of lsquobeach times timersquo
interaction centroids was performed to display differences in community structure
The SIMPER routine was employed to detect most species that contribute to the
dissimilarity in cases where significant differences in the PERMANOVA analysis were
Capiacutetulo 3
67
identified To detect whether the variation shown in the Simper analysis was natural or
induced by human impact the trajectory of species density over time was tested by
PERMANOVA design analysis and this was compared between sectors
All univariate and multivariate analyses were performed with PRIMER-E v61
and PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Warwick 2006)
Pearsonrsquos correlations were used to determine the relationship between
changes in the macrobenthos density and human trampling intensity (number of users
as a proxy) This analysis was conducted with the software PASW Statistics 18
3
31 Physical environment
Abiotic variables were constant over time in each sector and significant
variations were not detected from the period prior to impact to that after impact
within each sector (p (perm)gt 005) or between the beach sectors (p(perm) gt 005 for
all variables Table 1) The urban sector had fine sediment (mean grain size of 230 plusmn 18
microm before and 240 plusmn 56 microm after) a moderate mean sorting coefficient (154 plusmn 015
before 146 plusmn 016 after) and a mean sediment moisture content of 17 plusmn 4 before
impact and 165 plusmn 3 after The organic matter content increased slightly after impact
compared to that determined before impact (13 plusmn 078 and 092 plusmn 024
respectively) but this difference was not statistically significant The intermediate and
protected sectors had a fine median grain size in both periods (180 plusmn 17 microm and 186 plusmn
15 microm before 201 plusmn 52 microm and 212 plusmn 60 microm after respectively) The mean sorting
coefficient was moderate in both sectors (153 plusmn 023 and 148 plusmn 019 before 158 plusmn
021 and 161 plusmn 024 after) The mean sand moisture content was the same in both
areas before impact (17 plusmn 3) and after impact (18 plusmn 2) The organic matter content
in the intermediate and protected sectors varied slightly from before (094 plusmn 014
102 plusmn 028 respectively) to after (102 plusmn 029 106 plusmn 022 respectively) The
beach profile and slope did not differ substantially during the study in any sector and
the slope remained constant at 2 plusmn 05
3 Results
Capiacutetulo 3
68
Table 1 Permutational multivariate analyses of variance (PERMANOVA) testing differences in physical variables between sectors (Be urban intermediate and protected) and time (Ti before and after) Sampling period (Sp) was considered as a random variable
Table 2 Permanova result testing for differences in human trampling impact (using the number of users as a proxy) between sectors before and during impact and pair-wise comparison of term Be times Ti for pairs of levels of factor (a) Beach and (b) Time Urb = Urban sector Int = Intermediate sector and Protec = Protected sector Bef = before impact and Dur = During impact
Median grain size Sorting Sand moisture Orgnic matter content
Source df MS F P (perm) MS F P(perm) MS F P (perm) MS F P(perm)
Be 2 009 178 022 002 042 066 4012 230 017 4045 227 016 Ti 1 003 063 050 001 026 071 10195 698 010 10266 666 010 Sp(Ti) 4 005 175 013 006 147 022 1460 147 022 1542 153 020 Be x Ti 2 000 009 091 006 110 037 3116 179 022 3160 177 023 Be x Sp(Ti) 8 005 178 007 006 150 018 1744 176 009 1784 177 009 Res 54 003 004 990 1009
Source df MS Pseudo-F P(perm)
Be 2 2052 1907 0001
Ti 1 22805 47950 0104
Sp(Ti) 4 047 062 0639
BexTi 2 4393 4083 00001
Bex Sp(Ti) 8 107 141 0190
Res 252 076 Total 269
a) Pair-wise test Groups t P(MC)
Before Urb - Int 706 012 Urb - Protec 1117 040 Int - Protec 965 028
During Urb - Int 707 0017 Urb - Protec 1117 0008 Int - Protec 965 0011
b) Pair-wise test Groups t P(MC)
Urban bef- dur 3457 00001
Intermediate bef- dur 2976 00001
Protected bef- dur 072 0507
Capiacutetulo 3
69
32 Human use
The human trampling (number of visitors as proxy) registered significant
different trajectories over time (ldquobeach times timerdquo interaction p (perm) = 00001 Table
2) The pair-wise test for this significant interaction showed that during impact the
number of users was significantly higher on the urban and the intermediate sectors
(p(MC)lt 005 Table 2a) while before impact no differences were detected between
sectors (p (MC) gt 005 Table 2b) Also within sectors both showed significant
difference from before to during impact (p (MC) = 0001 Table 2b) while at the
protected no differences were detected (p (MC) = 0507 Table 2b)
The number of visitors in the sampling area over a diurnal time period before
and during impact (summer season) in each sector is shown in Fig 2 During impact
urban and intermediate sectors showed a similar evolution with an influx peak
between 1200 and 1400 h after which the number of beach users constantly
decreased during the afternoon while at the protected sector the number of users was
constant over time By contrast before impact the tree sector presented the same
lower flow of visitors reached a maximum of 15 visitors in the urban sector
The activities performed by users in the three sectors also differed In the urban
and intermediate sector about 80 of the activities included relaxation sunbathing
picnics ballgames and building sandcastles whereas in the protected sector 100 of
the users surveyed were walking and angling
Capiacutetulo 3
70
Fig2 Number of beach visitor counted (mean plusmn SD) per patch (50 m along shore x beach width) and per hour in each sector
Val
Lev 1
Lev2
Time (hours)
num
ber
of
beach v
isito
rs
0
50
100
150
200
250
300
350
Urban
Intermediate
Protected
1000 1100 1200 1300 1400 1500 1600 1700
During impact
Time (hours)
0
5
10
15
20 Urban
Intermediate
Protected
num
ber
of
beach v
isito
rs
1000 1100 1200 1300 1400 1500 1600 1700
Before impact
Capiacutetulo 3
71
33 Community composition and univariate descriptors
In total 26 species were found during the study period Crustaceans were the
most diverse taxa (14 species) followed by polychaetes (six species) molluscs (four
species) nemertea and echinodermata (a single species each) The contributions of the
major taxonomic groups in the community in each sector over time are shown in Fig 3
Before impact the dominant taxon in all areas was crustaceans After impact however
crustacean contributions decreased by 16 in the protected area and in the
intermediate and urban zones this decrease was 68 and 60 respectively
Amphipoda and Cumacea were the orders that decreased most markedly In the
protected sector there was an increase of 24 in the contribution of the polychaete
population after impact whereas in the urban and intermediate sector the increases
were 60 and 85 respectively These increases were primarily due to an increase in
individuals of the order Spionida
For community descriptors PERMANOVA showed variations over time for
density only with a significant lsquobeach times timersquo interaction (p (perm) = 003) The pair-
wise comparison of this interaction showed differences from before to after impact in
the urban and intermediate sectors (p (MC) lt 005) but differences were not found in
the protected area (Table 3) The density in the protected sector increased over time
(2122 plusmn 286 indm2 before and 2408 plusmn 486 indm2 after impact) whereas at the
other locations the opposite pattern was observed In the urban sector the density
varied from 1584 plusmn 174 indm2 before impact to 82 plusmn 218 indm2 after impact while
in the intermediate site the density decreased from 3315 plusmn 39 indm2 before impact to
918 plusmn 108 indm2 after impact (Fig 4)
Significant time differences were not found in the richness and diversity index
(p (perm) gt 005) Nonetheless the community descriptors showed a more stable
response than in the other areas although a decrease in these variables was observed
in the protected sector
A global significant and negative correlation was found between macrobenthos
density and the number of users (r = 036 p = 0003) A Personrsquos correlation between
these two factors was also performed in each sector In the urban and intermediate
Capiacutetulo 3
72
Urban Before Crustacea
Mollusca
Polychaeta
Nemertea
Urban After
Intermediate AfterIntermediate Before
Protected Before Protected After
sectors a significant and negative correlation was found (r = ndash021 p = 001 r = ndash042
p = 0001 respectively) while in the protected sector the correlation was not
significant (r = ndash001 p = 084) despite the fact that these factors were negatively
correlated
Fig3 Pie charts representing the proportion of taxa in the community in each sector and before and after impact
Capiacutetulo 3
73
Table 3 Results of three-way PERMANOVA and pair-wise comparisons testing for differences in univariate measures Only taxa showing a significant lsquobeach times timersquo interaction are shown
Richness Diversity index Density Bathyporeia pelagica
Source df MS F P MS F P MS F P MS F P
Be 2 160 490 00396 318 15002 00028 1406 669 00213 997 1516 0012
Ti 1 1149 1296 01028 1534 2647 01019 8860 754 00987 11395 806 0046
Sp(Ti) 4 088 477 00014 057 346 00084 1174 693 00001 1731 1163 00001
BexTi 2 057 175 02344 124 588 0295 1213 577 00318 1483 2261 00007
BexSp(Ti) 8 033 176 00878 021 126 02517 210 124 02665 066 044 089
Res 414 018 016 169 149
Total 431
Pair-wise test
Density
B pelagica
groups t P (MC) t P (MC)
Urban bef after 311 00359 456 00096
Intermediate bef after 279 0048 341 00292
Protected bef after 093 04024 0868 04403
Capiacutetulo 3
74
34 Multivariate analysis
Macrofauna assemblages changed from before to after impact with a
significant ldquobeach times timerdquo interaction (p (perm) = 00008) Pair-wise comparisons
indicate that the taxonomic structure of the macrofauna at the impacted site changed
statistically from before to after impact (p (MC) = 00001) The same trend was
observed in the intermediate sector while in the protected sector no differences were
detected The PERMANOVA test also showed a significant effect on the beach factor
(p(perm) lt 001) (Table 4)
Fig 4 Temporal variation (mean plusmnSE) in each sector of a) richness b) density (indm2) and c) diversity index Black bars represent before impact and white bars represent after impact
0
1
2
3
4
5
6
0
100
200
300
400
Before
After
00
02
04
06
08
10
12
14
a b
c
Urban Intermediate Protected Urban Intermediate Protected
Urban Intermediate Protected
Capiacutetulo 3
75
Table 4 PERMANOVA result testing for differences in macrofauna assemblages between
sectors and pair-wise of term BexTi interaction
Source df MS Pesudo-F P(perm) Pair-wise test Groups T P(MC)
Be 2 23377 910 00002 Urban bef aft 433 00001 Ti 1 95410 1822 0099 Intermediate bef aft 355 00001 Sp(Ti) 4 52345 234 00003 Protected bef aft 155 00714 BexTi 2 12944 504 00008
BexSp(Ti) 8 2568 115 02277
Res 414 22305
Total 431 23377
The differences in the structure of the community can be observed in the nMDS
plot (Fig 5) where the direction of change over time was different for the urban and
intermediate sector compared with the protected At each sector there was not any
heterogeneity in multivariate dispersion over time (PERMDISP Urban F1142 = 293
p(perm)= 013 Intermediate F1142 = 419 p(perm)= 006 Protected F1142= 248
p(perm)= 014)
Fig5 Non metric multidimensional scalinf ordination (nMDS) based on Bray-Crustis dissimilarity measure of centroids of each sector and after and before impact Triangles represents urban sector squares intermediate and circles represents the protected sector Black figures indicate before impact and white figures after impact
2D Stress 0
Capiacutetulo 3
76
The SIMPER test showed a high dissimilarity in the communities between
before and after impact both in the urbanized (9242 ) and intermediate (9022)
sectors (Table 5) In both areas the amphipod Bathyporeia pelagica the polychaete
Scolelepis squamata the mollusc Donax trunculus and the cumacea Cumopsis fagei
were the taxa that contributed the most to the temporal differences accounting for
56 of the total dissimilarity between sampling periods in the urban sector and 46 in
the intermediate sector Moreover the polychaete Paraonis fulgens and the amphipod
Pontocrates arenarius also contributed greatly to the differences between periods in
the intermediate sector The complete list of species that contributed to the
differences between times in each sector is shown in Table 5
Table 5 SIMPER analysis to evaluate the contributions of taxa to dissimilarities from before to after impact in urban and intermediate sectors
Groups Urban before amp Urban after Average dissimilarity 9242
Before After Species Urban sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Bathyporeia pelagica 146 0 1567 088 1696 1696 Scolelepis squamata 051 112 1494 069 1617 3313
Cumopsis fagei 134 003 1121 089 1213 4526 Donax trunculus 066 065 1046 065 1132 5657 Pontocrates arenarius 071 008 773 059 836 6493 Mactra stoultorum 059 0 504 044 546 7039 Eurydice affinis 03 004 441 033 478 7517 Nepthys hombergii 028 018 355 044 384 7901 Corbula gibba 026 02 322 046 349 825 Dispio uncinata 029 013 309 038 335 8584 Paraonis fulgens 031 006 297 041 322 8906 Glycera tridactyla 023 014 265 038 287 9193
Capiacutetulo 3
77
Table 5 Continued Groups Intermediate Before amp Intermediate After Average dissimilarity 9022
Of all set the species identified in the SIMPER analysis only Bathyporeia
pelagica showed a significant ldquobeach times timerdquo interaction (p (perm) lt 005) (Table 3) In
the protected sector Bathyporeia pelagica decreased it density after the impact (276
2 plusmn 497 indm2 compared to 591 plusmn 178 before impact) but not as pronouncedly as in
the other two sectors In the intermediate sector density decreased from 906 plusmn 196
indm2 before impact to 24 plusmn 7 indm2 after impact while in the urban sector no
individuals were found after impact (from 362 plusmn 82 indm2 to 0 indm2) Furthermore
was recorded a change in density of three species Thus the density of Eurydice affinis
and Haustorius arenarius increased after impact in the protected area while in the
other sectors decreased while Pontocrates arenarius densities followed the same
pattern of decline in all sectors after the impact but was less pronounced in the
protected sector Nonetheless these differences were not detected in PERMANOVA
analysis (Fig 6)
Before After
Species Intermediate sector AvAbund AvAbund AvDiss DissSD Contrib Cum
Cumopsis fagei 218 012 1387 123 1538 1538 Bathyporeia pelagica 179 024 1288 089 1428 2965 Scolelepis squamata 026 093 768 058 851 3817 Donax trunculus 095 065 754 075 836 4652 Paraonis fulgens 095 025 618 074 685 5338 Pontocrates arenarius 078 042 614 071 681 6018 Gastrosaccus sanctus 086 0 496 063 55 6568 Corbula gibba 067 011 449 06 498 7066
Haustorius arenarius 036 04 447 05 495 7562 Glycera tridactyla 032 021 304 046 337 7898 Nepthys hombergii 02 024 288 04 319 8217 Dispio uncinata 026 027 266 047 295 8513 Eurydice affinis 021 019 262 036 29 8803 Mactra stoultorum 029 008 236 031 262 9065
Capiacutetulo 3
78
4
In this study the response of macrofauna assemblages that inhabit sandy
beaches to human trampling which occurs mainly in the summer season was
analysed For this purpose three contrasting sectors of the same beach were
investigated an urban area with a high level of visitors a protected sector belonging to
a natural park with a low density of users and an intermediate zone also within the
natural park but with high level of human occupancy
Density of macrofauna and community composition showed different
trajectories over time in each sector The urban and intermediate sectors followed the
same pattern ie a drastic reduction in species density and a significant change in the
structure of the community from before to after impact However the protected
Fig6 Mean density (plusmn SE) of a) Bathyporeia pelagica b) Eurydice affinis c) Haustorius
arenarius and d) Pontocrates arenarius
4 Discussion
indm
2
0
20
40
60
80
100
120
140
0
5
10
15
20
25
30Before
After
a) b)
indm
2
0
20
40
60
80
100
120
140c)
0
5
10
15
20
Urban Intermediate Protected Urban Intermediate Protected
d)
Capiacutetulo 3
79
sector showed a greater stability throughout the study period without significant
changes in the community descriptors It is well known that macrofauna vary withing a
beach in the along-shore directions according to the susceptibility of each species to
environmental factors So changes in sand particle size swash climate
morphodynamicshellip can explain these variations patterns (Defeo and McLachlan 2005)
Our results showed that physical variables remained constant over time in each sector
and between sectors so it appears not to be the main inducing factor of variation
Although seasonal variations may also affect macrofauna communities (Harris et al
2011) our study is developed in a small spatial scale insufficient so that biotic
differences may be due to this phenomenon
Human activity is also considered an additional sources of variability (Defeo and
McLachlan 2005) since the number of beach users differed statistically between
sectors and was negatively correlated with the species density the biotic variation can
be tentatively attributed to the human trampling activity
In many cases it is difficult to disentangle the effects of trampling from those
generated by other impacts inherent to coastal development (see Schlacher and
Thomposn 2012) The factors that are most valued by visitors to a beach have been
identified as cleanliness beach comfort and safety good access parking areas and
good facilities (such as restaurants bars boulevard access to the beach litter bins and
shower facilities) (Roca and Villares 2008 Rolfe and Gregg 2012) Thus to promote
and support tourism beach managers initiate infrastructure improvements that
transform the beaches into increasingly urbanised areas and become increasing
stressors on these ecosystems Although tourism causes economic benefits it is
usually associated with substantial environmental costs (Davenport and Davenport
2006) Different studies concerning nourishment (Leewis et al 2012 Schlacher et al
2012 Peterson et al 2014) beach cleaning (Dugan and Hubbard 2010 Gilburn 2012)
and coastal armouring (Dugan et al 2008 Hubbard et al 2014) have shown the
negative effects of these actions on the beach fauna mainly because they cause
changes in the habitat destroy the dune systems change the natural physical
characteristics of the beaches eliminate food sources and reduce habitats and shelter
areas among others Furthermore these actions indirectly affect other components of
Capiacutetulo 3
80
the food chain such as shorebirds and fish due to a reduction in their food sources
(Defeo et al 2009) Consistent with this our results showed that the urban area
before impact had the lowest values of community descriptors also the correlation
coefficient between benthos density and number of user was lower than in the
intermediate sector which could suggest that in the urban area other factors are
influencing the density decreased ie coastal armouring and urbanization
The effect of trampling can be addressed experimentally but the results will
probably not reflect natural conditions (Ugolini et al 2008) due to the inability to
mimic real impact on both the temporal and spatial scales This is because temporally
experiments have a fixed period and do not last as long as the real impact and
spatially because they are performed within limited areas which might be avoided by
the beach fauna by simply moving to undisturbed areas The transitional zone
selected in this study is a suitable enclave to study the effect of trampling on
macrofauna communities uncoupled from other factors This area had natural
characteristics (without manmade structures backshore with dune systemshellip) but like
the urban sector receives a large tourist influx during the summer due to facilities
that are provided for human access Thus the high correlation coefficient found
between macrofauna density suggest that trampling itself has a negative effect on the
beach fauna causing a decrease in density and altering the composition of the
community
At population level amphipods have been traditionally considered as
bioindicators especially supralittoral species belonging to the family Talitridae
(Weslawski et al 2000 Fanini et al 2005 Ugolini et al 2008 Veloso et al 2009) In
fact Veloso et al 2008 in a previous study performed in the same beach showed
differences in Talitrus saltator density between sectors Talitrid populations in the
protected and intermediate sites were maintained throughout the year while in the
urban area were nonexistent So the absence of this species combined with the
results obtained in this study show the negative connotations that urban beaches have
on the macrofauna inhabiting it for the high number of beach visitors that it receives
as well as the great modifications that are subjects
Capiacutetulo 3
81
Beyond Talitritridae family species of Haustoridae Pontoporeiidae
Oedicerotidae and also Cirolanidae isopods have been considered to be susceptible to
the enrichment of organic matter (Chaouti and Bayed 2009) although very little is
known about the ecological implications of human activities Haustorius arenarius
Pontocrates arenarius and Eurydice affinis showed changes in their densities
throughout the study that may be due to pedestrian activity but only changes in
Bathyporeia pelagica were significant In all sectors this amphipod density fallen after
impact The decline was more severe in the intermediate and urban sectors where
density reached minimums values even no specimen was found The annual cycle of
Bathyporeia genus includes two reproductive peaks in spring and autumn (Fish and
Preece 1970 Mettam 1989) so the decline behavior observed suggest that these
species are highly vulnerable to trampling impact The way in which it activity
negatively affects beach communities probably is a result of sediment compaction
which might hinder burrowing reducing the probability of survival (Ugolini et al 2008)
or increasing the probability of being killed by direct crushing (Rossi et al 2007) In
addition to affect at population and community level human trampling may also have
consequences at the ecosystem level in fact protected beaches are more complex
organized mature and active environments than urbanized beaches (Reyes-Martiacutenez
et al 2014)
Although the potential for recovery of the beach fauna has not been addressed
in this study since the study area has been subjected to human impact for years the
ldquobefore impactrdquo state considered here could be seen as a reflection of subsequent
recovery Thus although trampling causes a significant decrease in species density
maintainance of the natural characteristics of the beaches (like occur at intermediate
sector) might enable possible recovery of the community (see Carr 2000) However
when intensive use by beach visitors occurs in urbanised areas a long-term loss of
biodiversity is the consequence which might become irreversible Furthermore the
stability of the communities of macrofauna found within the protected area highlights
the importance of these areas in the conservation and maintenance of biodiversity
Given the important role of macrofauna on the beaches (McLachlan and Brown
2006) as well as the many services provided by these ecosystems (Defeo et al 2009)
Capiacutetulo 3
82
it is critical that management policies focus on the protection of these areas and
recover and restore those that have already been degraded Although
recommendations that consider macrofauna are being developed for managers to
ensure the suitable use of beaches (McLachlan et al 2013) it is still not sufficient
because they are rarely applied and these ecosystems continued to be ignored in
conservation initiatives (Harris et al 2014)
In conclusion the human trampling is an important disturbing agent of the
macrobenthos that inhabits sandy beaches This factor acts decreasing benthic
densities and consequently a change in the community occurs When this activity is
performed in highly urbanized areas a long-term irreversible loss biodiversity could
happen Not all species respond similarly to an impact and it seems that the amphipod
Bathyporeia pelagica is highly sensitive to human trampling pressure therefore it use
as bioindicator of this impact type is recommended Although areas that maintain
natural features might have a high recovery capacity future studies should be
performed to test this hypothesis
Capiacutetulo 3
83
5
A Aguado-Gimeacutenez F Piedecusa MAGutieacuterrez JM Garciacutea-Charton JA Belmonte A
2012 Benthic recoveryt after fish farming cessation A ldquobeyond-BACIrdquo approach Marine Pollution Bulletin 64 729-738
Anderson MJ 2001 A new method for non-parametric multivariate analysis ofvariance Austral Ecology 26 32ndash46
Anderson MJ 2005 Permanova a FORTRAN computer program for permutational multivariate analysis of variance Auckland Department of Statistics University of Auckland New Zealand
Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Barros F 2001 Ghost crabs as a tool for rapid assessment of human impacts on exposed
sandy beaches Biological Conservation 97 399-404 Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes J 2002 Utility of morphodynamic
characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chaouti A Bayed A 2009 Categories of importance as a promising approach to valuate and
conserve ecosystem integrity the case study of Asilah sandy beach (Morocco) In Bayed A (ed) Sandy beaches and coastal zone management Proceedings of the Fifth International Symposium on Sandy Beaches (Rabat Morocco) Travaux de lInstitut Scientifique 6 107-110
Cisneros KO Smit AJ Laudien J Schoeman DS 2011 Complex dynamic combination of physical chemical and nutritional variables controls spatiotemporal variation of sandy beach community structure PloSone 6 e23724
Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth
D Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on
coastal environments a review Estuarine Coastal and Shelf Science 67 280-292 Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final
5 References
Capiacutetulo 3
84
Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan JE Hubbard DM McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58S 133-148
Dugan JE Hubbard DM Rodil IF Revell DL Schroeter S 2008 Ecological effects of coastal armoring on sandy beaches Marine Ecology 29 160-170
Dugan JE Hubbard DM 2010 Loss of Coastal Strand Habitat in Southern California The Role of Beach Grooming Estuaries and Coasts 33 67ndash77
E Emery KO 1961 A simple method of measuring beach profiles Limnology and
Oceanography 6 90-93
F Fanini L Cantarino CM Scapini F 2005 Relationship between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fanini L Zampicinini G Pafilis E 2014 Beach parties a case study on recreational human use of the beach and its effects on mobile arthropod fauna Ethology Ecology amp Evolution 26 69-79
Ferreira MN Rosso S 2009 Effects of human trampling on a rocky shore fauna on the Sao Paulo coast southeastern Brazil Brazilian Journal of Biology 69 993-999
Fish JD Preece GS 1970 The annual reproductive patterns of Bathyporeia pilosa andBathyporeia pelagica (Crustacea Amphipoda) Journal of the Marine Biological Association of the United Kingdom 50 475-488
G Gilburn AS 2012 Mechanical grooming and beach award status are associated with low
strandline biofiversity in Scotland Estuarine Coastal and Shelf Science 107 81-88
H Harris L Nel R Smale M Schoeman D 2011 Swash away Storm impacts on sandy
beach macrofaunal communities Estuarine Coastal and Shelf Science 94 210-221 Harris L Campbell EE Nel R Schoeman D 2014 Rich diversity strong endemism but
poor protection addressing the neglect of sandy beach ecosystems in coastal conservation planning Diversity and Distributions 1-16
Hockings M Twyford K 1997 Assessment and management of beach camping within Fraser Island World Heritage Area South East Queensland Australian Journal of Environmental Management 4 25ndash39
Hubbard DM Dugan JE Schooler NK Viola SM 2014 Local extirpations and regional declines of endemic upper beach invertebrates in southern California Estuarine Coastal and Shelf Science 150 67-75
Jaramillo E Contreras H Quijon P 1996 Macroinfauna and human disturbance in a sandy beach of south-central Chile Revista Chilena de Historia Natural 69 655-663
Jennings S 2004 Coastal tourism and shoreline management Annals of Tourism Research 31 899-922
Capiacutetulo 3
85
L Lastra M Page HM Dugan JE Hubbard DM Rodil IF 2008 Processing of
allochthonous macrophyte subsidies by sandy beach consumers estimates of feeding rates and impacts on food resources Marine Biology 154 163ndash174
Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lucrezi S Schlacher TA Robinson W 2009 Human disturbance as a cause of bias in ecological indicators for sandy beaches experimental evidence for the effects of human trampling on ghost crabs (Ocypode spp) Ecological Indicators 9 913-921
M Martiacutenez ML Intralawan A Vaacutezquez G Peacuterez-Maqueo O Sutton P Landgrave R
2007 The coasts of our world Ecological economic and social importance Ecological economics 63 254-272
Mettam C 1989 The life cycle of Bathyporeia pilosa Lindstroumlm (Amphipoda) in a stressful low salinity environment Scientia Marina 53 543-550
McLachlan A 1983 Sandy beach ecology e a review In McLachlan AErasmus T (Eds) Sandy Beaches as Ecosystems Junk The HagueThe Netherlands
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
Moffet MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on sandy beach macrofauna Journal of Coastal Conservation 4 87-90
P Peterson CH Bishop MJ DrsquoAnna LM Johnson GA 2014 Multi-year persistence of
beach habitat degradation from nourishment using coarse shelly sediments Science of the Total Environment 487 481ndash492
R Reyes-Martiacutenez MJ Lercari D Ruiz-Delgado MC Saacutenchez-Moyano JE Jimeacutenez-
Rodriacuteguez A Peacuterez-Hurtado A Garciacutea-Garciacutea FJ 2014 Human pressure on sandy beaches implications for tropgic functioning Estuaries and CoastsDoi 101007s12237-014-9910-6
Roca E Villares M 2008 Public perceptions for evaluating beach quality in urban and semi-natural environments Ocean amp Coastal Management 51 314-329
Rodgers KS Cox EF 2003 The effects of trampling on Hawaiian corals along a gradient of human use Biological Conservation 112 383ndash389
Rolfe J Gregg D 2012Valuing beach recreation across a regional area The Great Barrier Reef in Australia Ocean amp Coastal Management 69 282-290
Rossi F Forster RM Montserrat F Ponti M Terlizzi A Ysebaert T Middelburg JJ 2007 Human trampling as short-term disturbance on intertidal mudflats effects on
Capiacutetulo 3
86
macrofauna biodiversity and population dynamics of bivalves Marine Biology 151 2077-2090
S Schlacher TA Dugan J Schoeman DS Lastra M Jones A Scapini F McLachlan A
Defeo O 2007 Sandy beaches at the brink Diversity and Distributions 13 556ndash560 Schlacher TA Noriega R Jones A Dye T 2012 The effects of beach nourishment on
benthic invertebrates in eastern Australia Impacts and variable recovery Science of the Total Environment 435ndash436 411ndash417
SchlacherTA Schoeman DS Jones AR Dugan JE Hubbard DM Defeo O Peterson CH Weston MA Maslo B Olds AD Scapini F Nel R Harris LR Lucrezi S Lastra M Huijbers CM Connolly RM 2014 Metrics to assess ecological condition change and impacts in sandy beach ecosystems Journal of Environmental Management 144 322ndash335
Schlacher TA Thompson LMC 2008 Physical impacts caused by off-road vehicles (ORVs) to sandy beaches spatial quantification of car tracks on an Australian barrier island Journal of Coastal Research 24 234ndash242
Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123ndash132
T Torres A Palaciacuten C Seoane J Alonso JC 2011 Assessing the effects of a highway on a
threatened species using BeforendashDuringndashAfter and BeforendashDuringndashAfter-ControlndashImpact designs Biological Conservation 144 2223ndash2232
U Ugolini A Ungherese G Somigli S Galanti G Baroni D Borghini F Cipriani N
Nebbiai M Passaponti M S Focardi F 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
Underwood A J 1992 Beyond BACI the detection of environmental impacts onpopulations in the real but variable world Journal of Experimental Marine Biology and Ecology 161 145ndash178
Underwood A J 1994 On Beyond BACI Sampling Designs that Might Reliably Detect Environmental Disturbances Ecological Applications 4 3ndash15
V Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea
F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
WWeslawski JM Stanek A Siewert A Beer N 2000 The sandhopper (Talitrus
saltator Montagu 1808) on the Polish Baltic Coast Is a victim of increased tourism Oceanological Studies 29 77ndash87
Capiacutetulo 4 Human pressure on sandy beaches Implications for trophic
functioning
Capiacutetulo 4
88
Abstract
The effect of coastal development and tourism occupancy on the structure and
trophic networks of sandy beaches were analysed for the first time using mass-
balanced trophic models Ecopath models were applied to two beaches representative
of different anthropogenic pressures a beach located inside a protected area and an
urbanised beach with tourism infrastructure and high levels of visitors Models
comprised 28 compartment at the protected beach and 27 compartments at the
urbanised beaches including detritus phytoplankton zooplankton invertebrates
fishes and birds Results revealed that the protected area had higher values of total
system throughput biomass ascendency and capacity reflecting a more complex
organised mature and active system compared to the urbanised beach Finally
different indicators of stress were analysed and we suggest the Finn cycling index as an
indicator of anthropogenic impact on sandy beaches
Keywords Ecopath food web sandy beaches human disturbance Spain
Capiacutetulo 4
89
1
Sandy beaches are dynamic transitional environments between marine and
terrestrial zones (Defeo and McLachlan 2005) Despite their arid and barren
appearance sandy beaches systems are inhabited by diverse forms of life which
develop different abilities to adapt to dynamism and the hostile conditions
characteristic of these environments (Defeo et al 2009) The macrofaunal organisms
residing in sandy beaches play a major role in the ecological functioning coexisting
with primary producers (eg diatoms) decomposers such as bacteria secondary
consumers such as zooplankton meiobenthos and top-level predators such as fishes
and birds (Knox 2001 McLachlan and Brown 2006) All of these components create
significant and complex food webs where organisms ingest diverse food sources
derived both from the sea (Knox 2001 McLachlan and Brown 2006) and the land
(Scapini 2003) and are assimilated egested excreted respired and finally converted
to new biomass (Knox 2001)
Sandy beaches are especially vulnerable to human impacts from recreation
cleaning nourishment urban development pollution and exploitation (Defeo et al
2009) Furthermore several investigations have demonstrated how these impacts that
affect the abiotic environment can modify communities populations and individuals
alter biodiversity (Lercari and Defeo 2003 Veloso et al 2006 Schlacher et al 2008
Lewis et al 2012) and ultimately reduce ecosystem resilience (Fabiano et al 2009
Vinebrooke et al 2004) These changes might also be reflected in a disruption of the
trophic structure functioning and ecosystem dynamism Therefore a consideration of
all ecosystem components the energy flows and network characteristics is a
fundamental aspect that should be considered when evaluating human impacts on
beaches (Field et al 1989 Gaedke 1995)
Mass-balanced models are useful tools for exploring potential impacts in
environmental functioning and how these changes can be propagated through trophic
interactions (Christensen and Pauly 1992) Modelling has been performed for almost
all aquatic ecosystem types (Baird and Ulanowicz 1989 Villanueva et al 2006
Colleacuteter et al 2012 Angelini et al 2013) and some models have been implemented to
1 Introduction
Capiacutetulo 4
90
clarify the trophic functioning of sandy beaches Heymans and Mclachlan (1996)
constructed a food web model and carbon budget for Sundays beach located in the
Eastern Cape (South Africa) to describe the energy flow cycling and global properties
of this ecosystem Similarly Ortiz and Wolf (2002) modelled different coastal
environments in Tongoy Bay (Chile) to identify the trophic characteristics at a small
scale of four benthic habitats (seagrass meadows sandndashgravel sand and mud) More
recently Lercari et al (2010) investigated the role of morphodynamics in the
complexity and functioning of sandy beach food webs on the east coast of Uruguay
and Vasallo et al (2012) modelled the trophic structure in six sandy beaches
distributed along the Ligurian Coast in Italy in order to evaluate the beach benthic
ecosystem via thermodynamic and network analyses
Furthermore these types of trophic models have been widely used to address
the effects of human impact on the trophic structure and functioning of diverse marine
ecosystems For example the ecosystem level effects of fishing were intensively
assessed in a variety of studies worldwide (eg Rosado-Soloacuterzano and Guzman del
Proo 1998 Christensen and Pauly 1995 Coll et al 2006 Torres et al 2013 Blamey
et al 2014) aquaculture activities were also analysed using trophic models (eg
Phong et al 2010 Byron et al 2011) and human impacts in estuaries were also
successfully explored (Patriacutecio and Marques 2006 Baeta et al 2011 Selleslagh et al
2013)
Despite the increasing interest in trophic functioning of sandy beaches
(Bergamino et al 2011 Colombini et al 2011 Schlacher and Connolly 2009)
knowledge about how human action can influence these ecosystems traits is
rudimentary (Defeo et al 2009) In order to contribute in this gap a necessary step is
a comparison between pristine and perturbed conditions in order to disentangle the
effects of natural and human induced variations and define reference states (Selleslagh
et al 2012) Thus the Levante-Valdelagrana system presents a protected and a very
low-impacted beach that can be considered as a reference location contrasting with a
highly urbanised sector
The objective of this study is to assess the effect of urbanisation and tourist
occupancy on trophic structure functioning and network features of sandy beaches
Capiacutetulo 4
91
using mass-balance models In the current study two comprehensive food webs on a
protected beach and an urban beach used for tourism and recreation were
constructed for the first time
2
21 Study area
Trophic models for two sandy beaches located in the Bay of Cadiz on the
southwest Iberian Peninsula (Atlantic coast south west of Spain) (Fig 1) were
implemented The Bay of Cadiz is a shallow (maximum depth of 17 m) mesotidal basin
(maximum 37 m) with a mean wave height of 1m (Benavente 2000) and a mean
annual temperature of 19ordmC The selected beaches Valdelagrana (36deg3413N
6deg1329W) and Levante (36deg3253N 6deg1334W) are 1880 m and 4300 m long
respectively are dissipative (Ω = 63) with a gentle slope (2) and fine sand (020 mm)
These beaches conform to a sole coastal arch but present different anthropogenic
pressure levels Thus Levante beach is a low impacted and protected system that is
regarded as a control site and Valdelagrana is a large perturbed system acting as an
impacted site
Quantitative indicators such as the Conservation Index (CI) and the Index of
Recreational Potential (RI) were used in order to determine beach conditions and
existing human use of the area (McLachlan et al 2013)(Table 1) CI takes into account
1) the extent nature and condition of the dunes their well-developed vegetation and
their connection with the beach 2) presence of iconic and endangered species and 3)
the macrobenthic community abundance and species richness In contrast RI is based
on 1) available infrastructures to support recreational activities (eg beach access
toilets etc) 2) beach safety and health status and 3) physical carrying capacity CI and
RI values range from 0 to 10 in order of increasing conservation value or recreation
potential Information for estimations of indices was obtained from personal
observations and the Spanish Ministry of Agriculture Nature and Food Quality
(httpwwwmagramagobesescostasserviciosguia-playas)
2 Material and Methods
Capiacutetulo 4
92
Map data copy 2014 Google based on BCN IGN Spain0 1 km
Valdelagrana
Levante
Atlantic Ocean - Caacutediz Bay
36 31rsquo N
36 34rsquo N
6 12rsquo W6 15rsquo W
Spain
Los Toruntildeos Park
El Puerto de Santa
Mariacutea (Caacutediz)
Table 1 CI and RI scores for urban (Valdelagana) and protected (Levante) beaches
Beach name Dune status Iconic species Macro-benthos CI Infraestructure Safety health
Carrying
capacity RI
Levante 4 3 2 9 1 3 1 5
Well developed dune
system litltle
disturbance
Significant nesting area
for marine birds
Rich fauna dissipative
and long beach
No infrastructure
and limited
access
Low hazards
and clean Intermediate
Valdelagrana 0 1 2 3 5 3 1 9
Backshore with urban
development
Low numbers of marine
birds not nesting
Rich fauna dissipative
and long beach
Excellent access
and
infraestructures
Low hazards
and clean Intrermediate
Fig1 Map of Iberian Peninsula and zoom on Caacutediz Bay showing the location of the beaches modeled Valdelagrana (urban sector) and Levante (protected sector Los Toruntildeos Metropolitan Park)
Capiacutetulo 4
93
22 Modelling approach
Ecopath with Ecosim (EwE) software (version 610) (Christensen et al 2008)
was used to model the trophic structure and biomass flows of the two beaches The
static model Ecopath is a mass-balance model where the production of each
functional group or species (components or compartments) is equal to the sum of
predation non-predatory losses and exports Each component of the model is defined
by two basic equations (Christensen and Pauly 1992) The first equation describes
how the production term for each group can be split in components
(
) sum
(
)
where Bi Bj is the biomass of the prey and predator respectively (PB)i is the
productionbiomass ratio or total mortality (Z) in steady-state conditions (Allen 1971)
EEi is the ecotrophic efficiency defined as the ratio between flow out and flow into
each group or the proportion of the production is used in the ecosystem (values of this
ratio should be between 0 and 1) (QB)j is the food consumption per biomass unit of j
DCij is the proportion of every prey i in the stomach content of predator j Yi is exports
from fishing catches (Y rate in this study is zero because catch rates are not
considered) Ei is other export and BAi is the biomass accumulation rate for (i)
The second basic equation consists of balancing the energy within each
compartment
The model uses the linkages between production and consumption of the
groups so if one of the basic parameters per group (B PB QB or EE) is unknown
Ecopath can estimate it based on information for the other three (Christensen et al
2008)
UtedfeedunassimilaRnrespiratioPproductionQnConsumptio
Capiacutetulo 4
94
The two models developed represent the annual average situation for 2011
Both were built using biomass density in grams dry weight per square meter (g
dwm2) Models included 27 and 28 compartments in urban and protected beaches
respectively Functional groups were categorised based on similarities in trophic roles
(diet composition) and other biological features (type of habitat distribution
population parameters and maximum body size) in order to obtain homogeneous
characteristics among the species within a group More abundant species were left as
individual species in the models in order to accurately represent their roles in the
beach system This provided a clear advantage by allowing specific production and
consumption rates to be used thus avoiding averaging between species (Christensen
et al 2008) Hence most invertebrates and oystercatchers were treated as individual
compartments whereas fishes other birds and plankton were defined as grouped
compartments The specific composition of modelled groups and the information
sources can be seen in Table 2
The total area in which each group occurs was assessed by previous analyses of
macrofauna zonation in the beaches studied (unpublished data)
The pedigree routine was used to test the quality of input data in the model
Values ranged from 0 to 1 suggesting low and high precision respectively
23 Basic input
231 Macrofauna
Data for invertebrate biomass were obtained from six seasonal samplings
three conducted in summer and three in winter during spring tides in 2011 For each
beach samples were collected along six transects perpendicular to the coastline
spaced over a 100 m long stretch Each transect was divided into 10 equidistant
sampling levels to cover the entire intertidal area At each sampling level samples
were collected using a core of 25 cm diameter penetrating to a depth of 20 cm
Samples were sieved on site through a 1 mm mesh-size sieve collected in a labelled
plastic bag and preserved in 70 ethanol stained with Rose Bengal Once the species
Capiacutetulo 4
95
had been identified and counted the organisms were dried at 90ordmC for 24 h and
weighed Biomass was calculated by multiplying density by individual dry weight in
order to obtain the biomass density Global average biomass data were included in the
model
The PB ratio for invertebrates was calculated according to Brey (2001) based
on individual body mass and annual seawater temperature (19ordmC) For some
amphipods and isopods PB were estimated using Ecopath assuming an Ecotrophic
Efficency value of 095 as recommended elsewhere (Arreguiacuten-Saacutenchez et al 1993
Vega-Cendejas et al 1993) The QB ratio for invertebrates was estimated using the
following equation log(Q) = -0420 + 0742 Log(W) (Cammen 1980) where W is the
individual body dry weight
232 Top-level predators
Bird data for both beaches were obtained by a seasonal census (foot survey)
conducted in 2011 The abundance of species feeding during the sampling period was
registered Biomass was obtained by multiplying the mean abundance for each species
by individual weight Wet weight (Ww) was converted into dry weight (Dw) following
the conversion factor Ww = 318 Dw (Marcstroumlm and Mascher 1979) Consumption
was estimated using the equation log (F) = -0293 + 0850 times log W (Nilsson and
Nilsson 1976) where F is the food consumption per day and W is the weight of the
bird Food consumption was transformed into QB by considering the biomass and the
time spent in the area for each species For bird groups a gross conversion efficiency
value (PQ) of 005 was assumed (Christensen et al 2008) Fish biomass was mainly
obtained from published data for Los Toruntildeos Metropolitan Park (Arias and Drake
1999) For fish the conversion factor for Ww to Dw QB and total mortality (~PB)
were obtained from Fishbase (Froese and Pauly 2012) considering an annual mean
temperature of 19ordmC
Capiacutetulo 4
96
233 Zooplankton
Zooplankton density was obtained by in situ sampling in the surf zone (1 m
depth) at the same time as macrofauna sampling 10 L of water were filtered through a
zooplankton net (250 microm) and samples were preserved in 4 formalin Using a
binocular microscope Zooplankton were counted and identified Biomass was
calculated by multiplying the density by the mean dry weight of zooplankton following
Theilacker and Kimball (1984) The PB value was calculated according to Brey (2001)
and the QB value was obtained from the Gulf of Cadiz ecosystem (Torres et al 2013)
234 Primary producers
Phytoplankton was measured from water samples (2 L of seawater 1m depth)
collected during macrofauna samplings Biomass was estimated from the Chlorophyll a
(Chl a) concentration by acetone 90 extraction and spectrophotometric analysis
(Pearsons et al 1984) The Chl a concentration was converted to Dw following the
conversion factor 1 mg Chl a = 100 mg Dw The PB value was taken from the Ecopath
model of the Gulf of Cadiz ecosystem (Torres et al 2013)
235 Detritus
The stock of dead organic matter was modelled on two compartments
sediment detritus and seawater detritus Quantitative sediment detritus samples were
collected with the same sampling procedure as macrofauna samples Biomass was
estimated by the organic matter content of the sediment per square metre ie the
difference between sediment dry weight and sediment weight after calcination at
500degC
The biomass of detritus in seawater was estimated as total organic suspended
solids Thus 1 L of seawater was filtered through Whatman GFF filters and dried at
105degC and was calcined at 500degC The difference between the two weights was
considered as the total organic solid content of the sample
Capiacutetulo 4
97
236 Diet composition
Diet composition was extracted from published data and specifically for some
invertebrates the gut contents were analysed (Table 2) This analysis was performed
following the methodology of Bello and Cabrera (1999) which has been used recently
for both aquatic and terrestrial species and especially for amphipods (Navarro-
Barranco et al 2013 Torrecilla-Roca and Guerra-Garciacutea 2012) Individuals were
introduced into vials with Hertwigrsquos liquid and heated at 65ordmC for 5 to 24 h depending
on the type of cuticle and the gut contents of specimens were analysed under the
microscope
24 Model parameterisation and analysis
Models were considered valid (mass-balanced) when ecotrophic efficiency (EE)
was less than 1 for all groups when gross food conversion efficiency or PQ ranged
between 01 and 03 for most groups and when respiration was consistent with
physiological constraints (Christensen and Walters 2004)
When balancing the models the initial input parameters for several
compartments were adjusted to fulfil the basic assumptions and thermodynamic
constraints (see above) In this particular study the initial inputs and outputs based on
our field data were very close to the values required for mass balance thus only
manual adjustment of diet matrices was necessary This adjustment was performed
mainly for those groups with a high degree of uncertainty in this modelled information
As a result input values were consistent and they produced coherent models with
minor modifications of the estimated input data The obtained Pedigree Indices for
both beaches (046) indicate an acceptable quality of the models (Christensen et al
2005 Villanueva et al 2006) Diet matrix information before and after balancing of
the models are described in detail in the Electronic Supplementary Material (ESM)
In addition to the input parameters the following variables were analysed for
each functional group ecotrophic efficiency (EE) trophic level (TL) and omnivory index
(OI)
Capiacutetulo 4
98
Moreover the models allow the analysis of several ecosystem level traits
(Libralato et al 2010)
- Indicators of biomass flows in the system Total consumption (Q) Total export (E)
Total respiration (R) Sum of all flows to the detritus (FD) Total system throughput
(TST) Sum of all production (secondary and primary production)(P) Net primary
production (NPP) and Total biomass excluding all functional groups defined as detritus
(B)
- Indicators based on total flows and biomass in the system Total primary
productiontotal respiration (PPR) Net System Production (NP) Total primary
productiontotal biomass (PPB) Total biomasstotal system throughputs (BTST)
Total biomass total production (BP) Total respirationtotal biomass (RB)
- Measures of connectance and cycling Connectance index (CI) System omnivory
index (SOI) Finnrsquos cycling index (FCI) and Finnrsquos mean path length (FPL)
Network-analysis based metrics Ascendency scaled by the TST which is related to the
average mutual information in a system (A) Development capacity (C) indicate the
upper limit for A System overhead (O) Relative ascendency (AC) and internal relative
ascendency (AiCi)
- Measures of efficiency in energy transfers Transfer Efficiency calculated as a
comprehensive geometric average for the whole food web (TE)
In addition trophic relationships were described by the Lindeman spine
(Lindeman 1942) a routine that aggregates the ecosystem into discrete trophic levels
Thus it was possible to estimate the transfer efficiencies and flows between all groups
within the system The food chain that results from these procedures can be compared
with lsquospinesrsquo from other systems
Interactions between groups were analysed by mixed trophic impact (MTI)
analysis (Ulanowicz and Pucicia 1990) This allows the visualisation of the combined
direct and indirect trophic impacts that an infinitesimal increase in any of the groups is
predicted to have on all the other groups This therefore indicates the possible impact
that the change in biomass of one group would produce on the biomass of the other
groups in a steady-state system (Christensen et al 2008)
Capiacutetulo 4
99
Table 2 Model compartments and data source of the basic input in urban (Valdelagrana) and protected (Levante) beaches
Valdelagrana components Levante components B PB QB Diet
1 Piscivorous birds Sternula albifrons Hydroprogne caspia Thalasseus
sandvicensis Phalacrocorax carbo
Sternula albifrons Hydroprogne caspia Thalasseus sandvicensis Ardea cinerea Egretta garzetta Phalacrocorax carbo
27 12 22 26
2 Coastal fish Sparus aurata Dicentrarchus labrax Dicentrarchus
punctatus Sparus aurata Dicentrarchus labrax Dicentrarchus punctatus 15 15 15 34 15
3 Shorebirds Calidris alba Limosa lapponica Numenius
phaeopus Charadrius alexandrinus Charadrius hiaticulata Himantopus himantopus
Actitis hypoleucos Arenaria interpres Calidris alpina Calidris alba Limosa lapponica Numenius arquata Numenius phaeopus Tringa nebularia Tringa totanus Charadrius alexandrinus Charadrius hiaticula Pluvialis squatarola
Recurvirostra avosetta
27 12 22 162123
29
4 Eurasian Oystercatcher Haematopus ostralegus Haematopus ostralegus 27 12 22 17
5 Nemertea 27 7 8 20
6 Decapoda Diogenes pugilator Liocarcinus depurator
Portumnus latipes Diogenes pugilator Liocarcinus depurator Portumnus latipes 27 7 8 9 14
7 Glycera tridactyla 27 7 8 10 13
8 Paraonis fulgens 27 7 8 10 13
9 Eurydice affinis 27 7 8 19 27
10 Bivalvia Corbula gibba Dosinia lupinus Mactra stoultorum Corbula gibba Dosinia lupinus Mactra stoultorum 27 7 8 24
11 Donax trunculus 27 7 8 24
12 Zooplankton nauplii cladoceran copepod rotifer nauplii cladoceran copepod rotifer 27 7 28
13 Dispio uncinata 27 7 8 10 13
14 Scolelepis squamata 27 7 8 10 13
15 Onuphis eremita 27 7 8 10 13
Capiacutetulo 4
100
Table 2 Continued
Valdelagrana components Levante components B PB QB Diet
16 Nepthys hombergii 27 7 8 10 13
17 Pontocrates arenarius 27 7 8 16 27
18 Ophiura ophiura 27 7 8 5
19 Bathyporeia pelagica 27 7 8 227
20 Cumopsis fagei 27 7 8 16 27
21 Mysida Gastrosaccus spinifer Schistomysis parkeri Gastrosaccus spinifer Schistomysis parkeri 27 7 8 2527
22 Haustorius arenarius 27 7 8 11 27
23 Lekanespahera
rugicauda 27 7 8 18 27
24 Siphonoecetes
sabatieri 27 7 8 16 27
25 Talitrus saltator Not include 27 7 8 16 27
26 Phytoplankton filamentous algae Coscinodiscus sp diatoms
dinoflagellates filamentous algae Coscinodiscus sp diatoms dinoflagellates 27 28
27 Detritus (sediment) 27
28 Detritus (water) 27
(1) Arcas 2004 (2) d Acoz 2004 (3) Arias 1980 (4) Arias and Drake 1999 (5) Boos et al 2010 (6) Brearey 1982 (7) Brey 2001 (8) Cammen 1980 (9) Chartosia et al 2010 (10)Dauer et al 1981 (11)
Dennel 1933 (12) Estimated by EwE (13) Fauchal 1979 (14) Freire 1996 (15) Froese and Pauly 2012 (16) Guerra-Garciacutea et al 2014 (17) Heppleston 1971 (18) Holdich 1981 (19) Jones and Pierpoint
1997 (20) Mcdermott and Roe 1985 (21) Moreira 1995 (22) Nilsson and Nilsson 1976 (23) Peacuterez-Hurtado et al 1997 (24) Poppe and Goto 1993 (25) San Vicente and Sorbe 1993 (26) SeoBirdlife
wwwenciclopediadelasaveses (27)This study (28) Torres et al 2013 (29) Turpie and Hockey 1997
Capiacutetulo 4
101
3
The urban beach has low conservation value and high recreational power (CI =
3 and RI = 9) (Table 1) The backshore is occupied by infrastructure (parking spaces
streets promenade seafront amenities etc) replacing the dune system and
vegetation The beach presents a high physical carrying capacity with an extensive
supralittoral beach zone which is used for human recreational purposes at all times
The beach is used by residents and tourists all year round with a peak during the
summer season The protected beach has high conservation value and low recreational
power (CI = 9 and RI = 5) (Table 1) The beach is situated within the Los Toruntildeos
Metropolitan Park (Cadiz Bay Natural Park) and has a wide backshore (~ 250 m)
occupied by a well-developed system of dune ridges that barely reach 2 m in height
and 50 m in width and possess a natural vegetation cover that is an important nesting
area for several species of marine birds (Buitrago and Anfuso 2011) Vehicular access
is absent The beach has a high physical carrying capacity but human activity is limited
to some fisherman and walkers visiting the area The beach is protected and managed
by the National Park service
Table 3 provides a summary of main output data (biomass trophic level
ecotrophic efficiencies production consumption gross food conversion efficiency and
omnivory index) from the final models
3 Results
Capiacutetulo 4
102
Table 3 Basic estimates values of the mass-balanced models protected bech -Levante (Lev) urban beach -Valdelagrana (Val) Trophic level (TL) Biomass (B g of dry weightm2) Productionbiomass (PB year-1 ) ConsumptionBiomass (QB year-1) Ecotrophic efficiency (EE) ProductionConsumption (PQ) Omnivory index (OI) Parameters estimated by Ecopath are in bold
Model compartments TL B PB QB EE
PQ OI
Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val Lev Val
1 Piscivorous birds 412 414 000029 000024 495 563 9906 11252 000 000 005 005 000 000
2 Coastal fish 312 314 007322 007322 042 042 414 414 093 088 010 010 048 049
3 Shorebirds 310 313 001046 000042 323 471 6454 9421 000 000 005 005 025 061
4 Eurasian Oystercatcher 310 313 002525 000280 216 216 4311 4311 000 000 005 005 014 000
5 Nemertea 261 233 000086 000043 240 240 6854 6854 016 028 004 004 049 035
6 Decapoda 237 243 001971 001105 276 336 6002 7267 092 010 005 005 036 040
7 Glycera tridactyla 224 222 000139 000056 386 434 10817 12870 063 027 004 003 026 027
8 Paraonis fulgens 221 238 000023 000004 735 672 26077 23392 076 080 003 003 018 029
9 Eurydice affinis 212 236 000390 000025 708 762 16791 18424 079 010 004 004 022 039
10 Bivalvia 210 213 046745 149097 125 088 4338 3126 090 018 003 003 015 018
11 Donax trunculus 210 213 694331 222644 077 079 2772 2839 016 003 003 003 015 018
12 Zooplankton 205 214 065000 065000 2653 2653 9040 9040 091 095 029 029 005 014
13 Dispio uncinata 204 229 000131 000095 389 419 10985 12223 057 052 004 003 004 024
14 Scolelepis squamata 204 229 000615 000755 663 607 16006 14568 019 062 004 004 004 024
15 Onuphis eremita 203 205 000068 000037 445 394 13486 11323 056 048 003 003 012 013
16 Nepthys hombergii 202 213 000230 000163 383 396 10685 8000 036 093 004 005 015 021
17 Pontocrates arenarius 201 201 000096 000115 549 598 24325 19120 078 081 004 003 008 002
18 Ophiura ophiura 200 200 018775 009388 146 146 3238 3238 057 083 004 004 014 015
19 Bathyporeia pelagica 200 200 000307 000122 552 564 27470 27076 081 095 003 004 000 000
20 Cumopsis fagei 200 200 000433 000211 490 431 13139 23539 084 029 005 004 000 000
21 Mysida 200 200 000059 000039 047 076 19728 20836 006 097 004 004 000 000
22 Haustorius arenarius 200 200 002302 000025 586 641 14086 15570 070 022 004 004 000 000
23 Lekanespahera rugicauda 200 200 000218 000003 619 619 13847 13847 021 019 004 004 000 000
24 Siphonoecetes sabatieri 200 200 000001 000003 549 363 35944 35944 041 007 004 004 000 000
25 Talitrus saltator 200 - 000026 - 443 - 11111 - 071 - 004 - 003 -
26 Phytoplankton 100 100 100500 100500 15804 15800 000 000 095 071 000 000
27 Detritus (sediment) 100 100 2067 2127 000 032
28 Detritus (water) 100 100 327250 325000 012 000
Capiacutetulo 4
103
In terms of biomass distribution among food-web components both beaches
shared a common structure Detritus in the sediment composed the bulk of the system
organic matter (ca 2000 g Dwm2) whereas water detritus and phytoplankton
biomass were much lower (ca 33 and 1005 g Dwm2 respectively) With respect to
the macrofauna the mollusc Donax trunculus Bivalvia and the echinoderm Ophiura
ophiura were the species with the highest biomass in both beaches Peracarids and
polychaete species possess a relatively low biomass ranging from 0001 to 00005
of the total biomass in the protected site and 00002 and 00005 of total biomass in
urbanised beach (Table 3)
The ecotrophic efficiencies ranged between 0 and 096 The highest EE values
reflecting high predation in non-perturbed beach corresponded to the primary
producer followed by Coastal fish and Zooplankton whereas in perturbed beach the
amphipod Bathyporeia pelagica Zooplankton and the polychaete Nepthys hombergi
were the main producers The EE values of all compartments of birds were estimated
at 0 because no predation was considered for them Low rates of EE were found in
Mysida and Nemerteans in an unperturbed beach and Donax trunculus and
Siphonoecetes sabatieri in a perturbed beach
At protected site Coastal fish and Nemerteans were the groups that preyed on
the most trophic groups with values of omnivory index (OI) of 048 and 049
respectively However specialised model compartment was Haustorius arenarius
which prey mainly on Detritus and Phytoplankton At urban site the highest OI
corresponded with Shorebirds and Coastal fish whereas lower values of OI were
found for Cumopsis fagei Bivalvia Mysida and H arenarius
The trophic interactions between functional groups in both beaches are
illustrated in Fig 2 Each compartment of the trophic structure is represented by a
node in flow diagrams so that the size of each node is proportional to the logarithm of
the biomass These diagrams show that different system groups were organised into
four trophic levels Top-level predators (TLs from three to four) coincident on both
beaches were composed of the following vertebrates piscivorous birds shorebirds
Eurasian oystercatcher and coastal fish Most invertebrates were placed near trophic
level two whereas detritus and phytoplankton corresponded to trophic level one by
definition
Capiacutetulo 4
104
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
Decapoda
Dispio uncinata
Donax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenarius Lekanesphaera rugicauda
Nemertea
Nepthys hombergii
Onuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Talitrus saltator
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
a)
Fig2 Flow diagrams of protected beach-Levante (a) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
105
4
3
2
1
Shorebirds
Piscivorous birds
Eurasian OystercatcherCoastal fish
Bathyporeia pelagicaCumopsis fagei
Bivalvia
DecapodaDispio uncinataDonax trunculus
Eurydice affinis
Mysida
Glycera tridactyla
Haustorius arenariusLekanesphaera rugicauda
Nemertea
Nepthys hombergiiOnuphis eremita
Ophiura ophiura
Paraonis fulgens
Pontocrates arenarius
Scolelepis squamata
Siphonoecetes sabatieri
Zooplankton
Phytoplankton
Detritus (sediment)
Detritus (water)
b)
Fig2 Flow diagrams of urban beach-Valdelagrana (b) food webs Nodes size is proportional to biomass Gray lines show the relationship between trophic guilds Values are expressed in gDW m-2 y-1
Capiacutetulo 4
106
Estimates of the energy flows ecosystem energetic and network properties of
the protected and perturbed beaches are shown in Table 4 Common features of both
ecosystems were evident in the magnitude and partitioning of flows Even though the
urbanised beach had a total system throughput (TST) that was 25 less than
protected the percentage consumption exports and respiratory flows remained
constant between the beaches and were predominated by consumption followed by
respiration and flows of detritus Another common trait among the ecosystems was
the lower connectance consistent with the low values of OI
Several differences between both beaches were evident when considering
indicators based on production respiration and cycling (Table 4) The total respiration
was higher in non-perturbed site which produced a negative net system production on
this beach contrasting with the positive value obtained in the urban site In addition
the protected beach showed the highest total FCI and the lowest predatory cycling
Concerning network analysis-based metrics ascendency and development capacity
were high in the undisturbed beach The relative ascendency (AC) and internal
relative ascendency (AiCi) were 44 and 45 respectively on the protected beach
and 41 and 30 respectively on urbanised beach
Energy flows between discrete trophic levels in the protected and urbanised
beaches were expressed as Lindeman spines (Fig 3) A similar structure and
functioning was also evident on these diagrams There was an analogous biomass
distribution among TLs as well as the same predominance of primary production as the
principal source of organic matter for both food webs However some differences in
flows can be observed At urban beach TL two consumed a total of 94 and 6 of
primary producer and detritus respectively In this system primary producers
contributed 54 of the total flow that returned to detritus whereas the lowest
contribution was provided by the higher trophic level However on the protected
beach 78 of the primary producers and 22 of detritus were consumed by TL two A
total of 7150 gm2year returned to detritus with TL two mostly contributing to this
backflow (83) In both beaches the transfer efficiencies from detritus were higher
than from primary producers Moreover the overall transfer efficiency was 17 and
Capiacutetulo 4
107
22 for unperturbed and perturbed beaches respectively where the most efficient
trophic transfer throughout both systems occurred from TL two to TL three
Table 4 Comparison of main system statistics between protected (Levante) and urban (Valdelagrana) beaches Ascendency and Overhead are in of total Capacity and internal Ascendency in of internal Capacity
Levante Valdelagrana Units
Sum of all consumption 2886 1756 g DW m-2 y-1
Sum of all exports 299 767 g DW m-2 y-1
Sum of all respiratory flows 2069 1199 g DW m-2 y-1
Sum of all flows into detritus 715 842 g DW m-2 y-1
Total system throughput 5970 4564 g DW m-2 y-1
Sum of all production 1828 1794 g DW m-2 y-1
Calculated total net primary production 1588 1588 g DW m-2 y-1
Total primary productiontotal respiration 08 13
Net system production -481 389 g DW m-2 y-1
Total primary productiontotal biomass 168 285
Total biomasstotal throughput 00 00
Total biomass (excluding detritus) 94 56 g DW m-2
Connectance Index 02 02
System Omnivory Index 01 02
Ascendency 984 (442) 7393 (413 ) Flowbits
Internal Ascendency 1112 (5) 76 (42 ) Flowbits
Overhead 1240 (558 ) 10517 (587 ) Flowbits
Capacity 2224 (100) 1791 (100) Flowbits
Internal Capacity 3027 (136) 1882 (105) Flowbits
Finns cycling index 41 17
Predatory cycling index 07 26
Finns mean path length 25 23
Capiacutetulo 4
108
A summary of the mixed trophic impact analysis representing only the species
that had a greater impact on the trophic system in the studied sandy beaches is shown
in Fig 4 In general in both systems phytoplankton sediment and water detritus
showed a positive impact on most ecological groups especially those found in
intermediate trophic levels In contrast zooplankton showed a negative relationship
with all components of the trophic structure in both beaches Piscivorous birds and
coastal fishes acted in a similar way in most trophic compartments although they
showed some differences between beaches both trophic guilds had a negative impact
on themselves
Protected beach- Levante
Urbanised beach - Valdelagrana
Fig3 Lindeman spine showing the trophic flows transfer through the successive trophic levels in two sandy beaches Levante (a protected site) and Valdelagrana (b urban site)
Capiacutetulo 4
109
The impact effect of these top-level predators was also higher in the perturbed
beach Shorebirds unlike other -level predators showed a greater impact on the non-
perturbed beach This guild had a mainly negative effect on the amphipods Talitrus
saltator and Siphonoecetes sabatieri The effect of shorebirds was of little importance
the urbanised area
Sho
re b
ird
s
Pis
civo
rou
s b
ird
s
Eura
sia
n O
yste
rca
tch
er
Co
asta
l fis
h
Ba
thyp
ore
ia p
ela
gic
a
Cu
mo
psi
s fa
gei
Biv
alvi
a
De
cap
od
a
Dis
pio
un
cin
ata
Do
na
x tr
un
culu
s
Eury
dic
e a
ffin
is
Mys
ida
Gly
cera
tri
da
ctyl
a
Ha
uto
riu
s a
ren
ari
us
Leka
nes
ph
aer
a ru
gic
au
da
Ne
me
rte
a
Nep
thys
ho
mb
erg
ii
On
up
his
ere
mit
a
Op
hiu
ra o
ph
iura
Pa
rao
nis
fulg
ens
Po
nto
cra
tes
are
na
riu
s
Sco
lele
pis
sq
ua
ma
ta
Sip
ho
no
ecet
es s
ab
ati
eri
Talit
rus
salt
ato
r
Zoo
pla
nkt
on
Ph
yto
pla
nkt
on
De
trit
us
(se
dim
en
t)
De
trit
us
(wat
er)
-1-05
005
Piscivorous birds
-1-05
005
Coastal fish
-1-05
005
Shore birds
-1-05
005
Zooplankton
-1-05
005
Phytoplankton
-1-05
005
Detritus (sediment)
-1-05
005
Detritus (water)
Fig4 Mixed trophic impact of main compartments in both sandy beaches Black bars correspond with non-perturbed beach (Levante) and grey bars correspond with perturbed beach (Valdelagrana) Positive interactions are represented by bars pointing upwards and negative interactions by bars pointing downwards
Capiacutetulo 4
110
4
We analysed the trophic structure of sandy beaches with contrasting levels of
human pressure driven by urbanisation Even than the consideration of a major
number of control and impacted sites (not available in the studied region) could
improve the statistical power of the analysis our results are clear In general terms
the ecosystem structure and trophic function of the urbanised and non-urbanised sites
were relatively similar Both beaches had similar trophic levels OIs and connectance
showing similar linkages within the food web Both ecosystems also showed a similar
biomass allocation between trophic levels and analogous flow distribution where
most flows were assigned to consumption followed by respiration This pattern can be
observed in other intertidal sandy habitats (Ortiz et al 2002 Lercari et al 2010) Both
systems also showed a global transfer efficiency (~2) lower than the expected 10
Although both beaches showed a trophic structure formed by analogous
ecological compartments the beaches differed in the number and composition of
some trophic groups Shorebird group consisted of 6 species in the disturbed beach
and 13 species in the undisturbed beach most of which with higher biomass The same
pattern occurred for the group of piscivorous birds in which the number of group
components was higher in the unperturbated beach For invertebrates there was an
additional compartment in the protected site the amphipod Talitrus saltator a species
considered an indicator of human disturbance in sandy beaches (Fanini et al 2005
Ugolini et al 2008 Veloso et al 2008) This specie also constitutes an important food
source for some shorebirds (Dugan 2003) This interaction can be seen in the MTI
analysis that showed the strong influence that shorebirds generated on these
amphipods in the non-urbanised beach The Levante beach inside a protected area
(Los Toruntildeos Metropolitan Park) is used for many birds for migratory wintering and
breeding activities Since the abundance and distribution of birds on sandy beaches
might be related to the type and availability of food resources (Dugan 1999) the
protected beaches could provide more food resources for shorebirds A similar pattern
in the biomass and trophic level distribution was found in sandy beaches with
markedly different morphodynamics (Lercari et al 2010) Reflective beaches
4 Discussion
Capiacutetulo 4
111
considered as stressful habitats display lower trophic levels top-level predators with
less richness abundance and biomass than dissipative beaches This could be
considered as analogous to our results where less-stressed beaches develop a more
complex trophic structure
The analysis of discrete trophic levels (Lindeman 1942) showed that a large
percentage of primary production was consumed whereas a low proportion was
converted to detritus in both beaches In addition both systems showed a DH ratio
lt10 suggesting that food webs were more dependent on herbivory for the generation
of TST This might be due to the high biomass of bivalves found in both ecosystems
which feeds mainly on phytoplankton This dependence on herbivory has been
observed in the trophic functioning of other sandy beaches (Lercari et al 2010) The
high utilisation of primary production was also shown by the high ecotrophic
efficiencies of this compartment Furthermore the fact that transfer efficiencies from
primary producers were lower than from detritus also suggests that this resource may
be limiting in sandy beaches The detritus compartment showed an opposite pattern
with lower utilisation by the food chain MTI analysis showed that detritus plays an
important role as a source of food and in structuring food webs in both sandy beaches
suggesting a possible bottom-up control effect This trend can be observed in other
ecosystem where detritus plays a major role in the trophic structure due to the
positive effect generated to all other functional groups (Torres et al 2013) The large
biomass of detritus found and the higher transfer efficiencies from it suggest that
there might be a production surplus of this resource which is not limiting
Furthermore the lower amount of living biomass that ends up as detritus highlights
the importance of exogenous sources such as wrack subsidies as a component of
detritus and as a food source for invertebrates on sandy beaches (Dugan et al 2003)
Diverse indices describing trophic network attributes have been considered as
possible indicators of stress (eg the Finn cycling index Ascendency System Omnivory
etc) The proportion of recycled matter is higher in more mature and less disturbed
systems Odum (1969) and Ulanowicz (1984) concluded that this index increased in
more-stressed systems as a homeostatic response to perturbation Patriacutecio et al
(2004) estimated that ascendency values were related to the level of disturbance thus
high values of this index were associated with non-eutrophic areas This is consistent
Capiacutetulo 4
112
with the findings of Baird and Ulanowicz (1993) who established that both ascendency
and capacity would decrease in a system affected by disturbance or pollution stress
Furthermore Selleslagh et al (2013) determined that the OI responded positively to
anthropogenic disturbance It should be emphasised that these indices as indicators of
disturbance were used for estuarine ecosystems and usually for eutrophication as a
source of contamination
In the present study these indices were tested for the first time in two sandy
beaches with different stress level Our results agree with the findings of Baird and
Ulanowicz (1993) and Patriacutecio et al (2004) since the disturbed site shows lower
values of ascendency and capacity than the undisturbed beach Protected beach
showed OI values that were slightly higher than those for the urbanised area
Therefore this indicator on sandy beaches should be interpreted with caution The
greatest differences between beaches were observed in the cycling capacity measured
by the FCI index In the non-perturbed beach recycling was 23-fold higher than in the
perturbed site This pattern was also observed in Baiyangdian Lake (China) (Yang et al
2010) where the trophic attributes were analysed before and after an anthropogenic
impact showing that FCI decreased by 20 after the impact The same pattern was
observed in Danshuei River Estuary (Taiwan) (Hsing-Juh et al 2006) a hypoxic estuary
affected by untreated sewage effluent where the recycling index showed the lowest
values compared to other similar ecosystems that were not perturbed Thus our
result following Odum (1969) shows that undisturbed beaches have a greater
retentiveness Therefore the FCI index could be considered as a potential indicator of
human disturbance on sandy beaches
Some of these indices also describe the state of ecosystem development (Kay
et al 1989) The higher values of relative ascendency (AC) and the internal relative
ascendency (AiCi) at the unperturbed beach suggest that this area is more stable
more organised and more highly developed than the urbanised beach Also the
difference between AC and AiCi quantifies the dependency on external factors
(Leguerrier et al 2007) The difference in the protected site was 1 while in the
urbanised beach was 10 suggesting that the perturbed area is more influenced by
external factors Furthermore the perturbed beach showed a higher value of
Capiacutetulo 4
113
Overhead which is associated with systems in earlier stages of development
(Ulanowicz 1986)
The total primary productiontotal respiration ratio displayed lower values of
ecosystem metabolism in the non-urbanised beach This might be due to higher
respiration rates in this beach This ratio is considered (Odum 1971) to be a descriptor
of ecosystem maturity because in immature ecosystems production exceeded
respiration Thus the non-perturbed beach showed a greater maturity than the
impacted beach Moreover the net system production display negative values in the
protected beach This parameter is based on respiration thus the difference can also
be due to this or to a greater import of primary production to fulfil the trophic needs
of the dominant bivalves which have a higher biomass than those in urban beach This
conclusion was also reached by Ortiz and Wolf in other sandy habitats where the
negative values of production were attributed to the trophic activity of bivalves
Furthermore TST showed the total activity of the ecosystem (Heymans et al 2002)
and accordingly the non-urbanised site was the most active beach
Previous information on the area (unpublished data) focused on the
community level demonstrated strong differences in the macrobenthic communities
between both beaches especially in summer when the touristic activity was higher
The urban site showed lower densities of species species richness and biomass than
the protected beach At the end of the summer both beaches become similar These
changes are not completely reflected in the ecosystem-level models because they
consider an average annual situation that might mask a seasonal-scale impact
Similarities found between beaches can also be seen as a positive effect generated by
the establishment of protected areas such as Los Toruntildeos Metropolitan Park In this
sense the protected area could have a positive effect on the maintenance of beach
fauna providing a biomass refuge and allowing the spill-over (Halpern and Warner
2003) of certain groups such as top-level predators to the urbanised and be part of it
trophic structure
In conclusion we have tested the potential of using Ecopath with Ecosim (EwE)
to provide useful information to distinguish changes in ecosystem structure and
functioning in perturbednon-perturbed sandy beaches Selected beaches had the
same physical climate and morphodynamic conditions so that the differences found
Capiacutetulo 4
114
could be attributed to the impact caused by the urbanisation and occupation of each
beach In general terms the trophic functionings of both beaches were analogous but
the protected area appeared more complex organised mature and active than the
urbanised beach Network analysis remark a trophic disturbance at the urbanised area
especially the Finn cycling index which we suggest as an indicator of anthropogenic
impacts in sandy beaches The models provide useful information and could represent
the status of the trophic functioning of two sandy beaches and the effectiveness of the
protected areas
Capiacutetulo 4
115
5
A d Acoz CU 2004 The genus Bathyporeia Lindstroumlm 1855 in western Europe (Crustacea
Amphipoda Pontoporeiidae) 2004 Zoologische Verhandelingen 28 3-162 Allen RR 1971 Relation between production and biomass Journal of the Fisheries Research
Board of Canada 28 1573-1581 Angelini R Morais R Catella C Resende E Libralato S 2013 Aquatic food webs of the
oxbow lakes in the Pantanal A new site for fisheries guaranteed by alternated control Ecological Modelling 253 82ndash 96
Arcas J 2004 Dieta y seleccioacuten de presas del andarriacuteos chico Actitis Hypoleucos durante el invierno Ardeola 51 203-213
Arias A 1980 Crecimiento reacutegimen alimentario y reproduccioacuten de la dorada (Sparus aurata L) y del robalo (Dicentrarchus labrax L) en los esteros de Caacutediz Investigacioacuten Pesquera 44 59-83
Arias AM Drake P 1999 Fauna acuacuteatica de las salinas del Parque Natural de la Bahiacutea de Caacutediz Enpresa de Gestioacuten Medioambiental Junta de Andaluciacutea DLEspantildea
Arreguiacuten-Saacutenchez F Valero E Chaacutevez EA 1993 A trophic box model of the coastal fish communities of the Southwestern Gulf of Mexico In Christensen V amp D Pauly Trophic models of Aquatic Ecosystems ICLARM Conference Proceedings 26 Philippines pp 197-205
B Baeta A Niquil N J Marques J Patriacutecio J 2011 Modelling the effects of eutrophication
mitigation measures and an extreme flood event on estuarine benthic food webs Ecological Modelling 222 1209ndash1221
Baird D Ulanowicz RE 1989 The seasonal dynamic of the Chesapeake Bay ecosystem Ecological Monographs 59 329ndash364
Baird D Ulanowicz RE 1993 Comparative study on the trophic structure cycling and ecosystem properties of four tidal estuaries Marine Ecology Progress Series 99 221-237
Bello CL Cabrera MI 1999 Uso de la teacutecnicamicrohistoloacutegica de Cavender y Hansen en la identificacioacuten de insectos acuaacuteticos Boletiacuten Entomoloacutegico Venezolano 14 77ndash79
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Bergamino L Lercari D Defeo O 2011 Food web structure of sandy beaches temporal and spatial variation using stable isotope analysis Estuarine Coastal and Shelf Science 91 536ndash543
Blamey L Plagaacutenyi E Branch G 2014 Was overfishing of predatory fish responsible for a lobster-induced regime shift in the Benguela Ecological Modelling 273 140ndash150
Boos K Gutow L Mundry R Franke HD 2010 Sediment preference and burrowing behaviour in the sympatric brittlestars Ophiura albida Forbes 1839 and Ophiura ophiura (Linnaeus 1758) (Ophiuroidea Echinodermata) Journal of Experimental Marine Biology and Ecology 393 176ndash181
Brearey D M 1982 The feeding ecology and foraging behaviour of sanderline Calidris alba and turnstone Arenaria interpres at Teesmouth NEEngland Durham theses Dirham University
Brey T 2001 Population Dynamics in Benthic Invertebrates A virtual Handbook httpthomas-breydesciencevirtualhandbook
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Byron C Link J Costa-Pierce B Bengston D 2011 Modeling ecological carrying capacity of shellfish aquaculture in highly flushed temperate lagoons Aquaculture 314 87ndash99
C Cammen LM 1980 Ingestion rate an empirical model for aquatic deposit feeders and
detritivores Oecologia 44 303-310 Chartosia N Kitsos MS Koukouras A 2010 Seasonal Diet of Portumnus Latipes (Pennat
1777) (Decopoda Portunidae) Crustaceana 83 1101-1113 Christensen V Pauly D 1992 ECOPATH II a software for balancing steady-state ecosystem
models and calculating network characteristics Ecological Modelling 61 169-185 Christensen V Pauly D 1995 Fish production catches and the carrying capacity of the
world oceans Naga 18 34-40 Christensen V Walters CJ 2004 ECOPATH with ECOSIM methods capabilities and
limitations Ecological Modelling 172 109-139 Christensen V Walters CJ Pauly D 2005 Ecopath with Ecosim a UserrsquosGuide November
2005 edition Fisheries Centre University of British ColumbiaVancouver Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide
November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
Coll M Palomera I Tudela S Sardagrave F 2006 Trophic flows ecosystem structure and fishing impacts in the South Catalan Sea Northwestern Mediterranean Journal of Marine Systems 59 63ndash96
Colleacuteter M Gascuel D Eucotin JM Morais L 2012 Modelling trophic flows in ecosystems to assess the efficiency of marine protected area (MPA) a case study on the coast of Seacuteneacutegal Ecological modeling 232 1-13
Colombini I Brilli M Fallaci M Gagnarli E Chelazzi L 2011 Food webs of sandy beach macroinvertebrate community using stable isotopes analysis Acta Oecologica 37 422-432
D Dauer DM Maybury CA Ewing RM 1981 Feeding behaviour and general ecology of
several spionid polychaetes from the Chesapeake Bay Journal of Experimental Marine Biology and Ecology 54 21-38
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beache macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman D Schlacher T Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems A review Estuarine Coastal and Shelf Science 81 1ndash12
Dennel R 1933 The habitats and feeding mechanism of the Amphipod Haustorius arenarius Slabber Journal of the Linnean Society of London Zoology 38 363-388
Dugan J 1999 Utilization of sandy beaches by shorebirds relationships to population characteristics of macrofauna prey species and beach morphodynamics Draft Final Technical Report Outer Continental Shelf Study Caramillo CA Minerals Management Service
Dugan J Hubbard D McCrary M Pierson M 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed beaches of southern California Estuarine Coastal and Shelf Science 58 133-148
Capiacutetulo 4
117
F Fabiano M Marin V Paoli C Vassallo P 2009 Methods for the sustainability evaluation
of coastal zone Journal of Mediterranean Ecology 10 5ndash11 Fanini L Cantarino CM F Scapini F 2005 Relationships between the dynamics of two
Talitrus saltator populations and the impacts of activities linked to tourism Oceanologia 47 93ndash112
Fauchal K 1979 The diet of worms A study of polychaete feeding guilds Oceanography and Marine Biology An Annual Review 7 193-284
Field JG Wulff F Mann KH 1989 The need to analyse ecological networks In Wulff F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Coastal and Estuarine Studies Springer-Verlag Berlin 3ndash12
Freire J 1996 Feeding ecology of Liocarcinus depurator (Decapoda Portunidae) in the Riade Arousa (Galicia north-west Spain) effects of habitat season and life history Marine Biology 126 297-311
Froese R Pauly D 2012 FishBase World Wide Web Electronic Publication wwwfishbaseorg
G Gaedke U 1995 A comparison of whole-community and ecosystem approaches (biomass
size distributions food web analysis network analysis simulation models) to study the structure function and regulation of pelagic food webs Journal of Plankton Research 17 1273ndash1305
Guerra-Garciacutea JM Tierno de Figueroa JM Navarro-Barranco C Ros M Saacutenchez-Moyano JE Moreira J 2014 Dietary analysis of the marine Amphipods (Crustacea Peracarida) form the Iberian Peninsula Journal of Sea Research 85 508-517
H Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives
Proceedings of the Royal Society of London B 2701871-1878 Heppleston PB 1971 The feeding Ecology of Oystercatchers (Haematopus ostralegus L) in
winter in Northern Scotland Journal of Animal Ecology 40 651-672 Heymans JJ McLachlan A 1996 Carbon budget and network analysis of a highenergy
beachsurf zone ecosystem Estuarine Coastal and Shelf Science 43 484ndash585 Heymans JJ Ulanowicz RE Bondavalli C 2002 Network analysis of the South Florida
Everglades graminoid marshes and comparison with nearby cypress ecosystems Ecological Modelling 149 5-23
Holdich DM 1981 Opportunistic Feeding Behaviour in a Predatory Isopod Crustaceana 41 101-103
Hsing-Juh L Xiao-Xun D Kwang-Tsao S Huei-Meei S Wen-Tseng L Hwey-Lian H Lee-Shing F Jia-Jang H 2006 Trophic structure and functioning in a eutrophic and poorly flushed lagoon in southwestern Taiwan Marine Environmental Research 62 61ndash82
J Jones DA Pierpoint CJ 1997 Ecology and taxonomy of the genus Eurudice (Ispoda
Cirolanidae) form sand beaches on the Iberian Peninsula Journal of the Marine Biological Association of the United Kingdom 77 55-76
Capiacutetulo 4
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K Kay JJ Graham LA Ulanowicz RE 1989 A detailed guide to network analysis In Wulff
F Field JG Mann KH (Eds) Network Analysis in Marine Ecology Methods and Applications Springer Berlin 32 15ndash61
Knox GA 2001 The ecology of seashores CRC Press Boca Raton Florida USA
L Leguerrier D Degreacute D Niquil N 2007 Network analysis and inter-ecosystem comparison
of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove SW France) Estuarine Coastal and Shelf Science 74 403-418
Lercari D Defeo O 2003 Variation of a sandy beach macrobenthic community along a human-induced environmental gradient Estuarine Coastal and Shelf Science 58S 17ndash24
Lercari D Bergamino L Defeo O 2010 Trophic models in sandy beaches with contrasting morphodynamics comparing ecosystem structure and biomass flow Ecological Modelling 221 2751ndash2759
Lewis L Bodegom P Rozema J Janssen G 2012 Does beach nourishment have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172ndash181
Libralato S Coll M Tempesta M Santojanni A Spoto M Palomera I Arneri E Solidoro C 2010 Food-web traits of protected and exploited areas of the Adriatic Sea Biological Conservation 143 2182ndash2194
Lindeman RL 1942 The trophic-dynamic aspect of ecology Ecology 23 399ndash418
M Marcstroumlm V Mascher JW 1979 Weights and fat in Lapwings Vanellus vanellus and
Oystercatchers Haematopus ostralegus starved to death during a cold spell in spring Ornis Scandinavica 10 235-240
Mcdermott JJ Roe P 1985 Food Feeding Behaviour and Feeding Ecology of Nemerteans American Zoologist 25 113-125
McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington Massachusetts
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Coastal Management 71 256-368
Moreira F 1995 The winter feeding ecology of Avocets Recuvirostra avosetta on intertidal areas II Diet and feeding mechanisms Ibis 137 99-108
N Navarro-Barranco C Tierno-de-Figueroa JM Guerra-Garciacutea JM Saacutenchez-Tocino L and
Garciacutea-Goacutemez JC 2013 Feeding habits of amphipods (Crustacea Malacostraca) from shallow soft bottom communities Comparison between marine caves and open habitats Journal of Sea Research 78 1-7
Nilsson SG Nilsson IN 1976 Numbers food consumption and fish predation by birds in Lake Moacuteckeln southern Sweden Ornis Scandinavica 7 61-70
O Odum HT 1969 The strategy of ecosystem development Science 164 262-270 Odum E 1971 Fundamentals of ecology Philadelphia Saunders
Capiacutetulo 4
119
Ortiz M Wolff M 2002 Trophic model of four benthic communities in Tongoy Bay (Chile) comparative analysis and preliminary assessment of management strategies Journal of Experimental Marine Biology and Ecology 268 205ndash235
P Parsons T Maila Y Lalli C 1984 A Manual of Chemical and Biological Methods for
Seawater Analysis Pergamon Patriacutecio J Ulanowicz RE Pardal MA Marques JC 2004 Ascendency as an ecological
indicator a case study of estuarine pulse eutrophication Estuarine Coastal and Shelf Science 60 23-35
Patriacutecio J Marques JC 2006 Mass balanced models of the food web in three areas along a gradient of eutrophication symptoms in the south arm of the Mondego estuary (Portugal) Ecological modelling 197 21ndash34
Peacuterez-Hurtado A Goss-Custard JD Garciacutea F 1997 The diet of wintering waders in Caacutediz Bay southwest Spain Bird study 44 45-52
Phong LT Dam AA Udo HMJ Mensvoort MEF Tri LQ Steenstra FA Zijpp AJ 2010 An agro-ecological evaluation of aquaculture integration into farming systems of the Mekong Delta Agriculture Ecosystems and Environment 138 232ndash241
Poppe GT Goto Y 1993 European Seashells Vol II (Scaphopoda Bivalvia Cephalopoda) Verlag Christa Hemmen Wiesbaden Germany
R Rosado-Soloacuterzano R Guzman del Proo S 1998 Preliminary trophic structure model for
Tampamachoco lagoon Veracruz Mexico Ecological Modelling 109 141ndash154
S San Vicente C Sorbe JC 1993 Biologie du Mysidaceacute suprabenthique Schistomysis parkeri
Norman 1892 dans la zone sud du Golfe de Gascogne (Plage dHendaye) Crustaceana 65 222-252
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Selleslagh J Lobry J Amara R Brylinski JM Boeumlt P 2013 Trophic functioning of coastal ecosystems along an anthropogenic pressure gradient A French case study with emphasis on a small and low impacted estuary Estuarine Coastal and Shelf Science 112 73-85
Schlacher TA Connolly RM 2009 Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches Ecosystems 12 311-321
Schlacher TA Richardson D McLean I 2008 Impacts of off-road vehicles (ORVs) on macrobenthic assemblages on sandy beaches Environmental Management 41 878ndash892
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associated to the alga Fucus spiralis in Tarifa Island Caacutediz (Southern Spain) Zoologia baetica 23 39-47
Torres M Coll M Heymans JJ Christensen V Sobrino I 2013 Food-web structure of and fishing impacts on the Gulf of Cadiz ecosystem (South-western Spain) Ecological Modelling 265 26ndash 44
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Nebbiai M Passaponti M Focardi S 2008 The amphipod Talitrus saltator as a bioindicator of human trampling on sandy beaches Marine Environmental Research 65 349ndash357
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Capiacutetulo 4
121
6
Table A1 Predatoryprey matrix of Levante beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia guilliamsoniana000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 024 003 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 001 000 000 000 002 000 000 004 000 005 000 000 005 005 043 005 000 000 000 000 000 000
7 Bivalvia 044 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 003 000 000 015 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 001 000 000 002 000 000 000 001 000 000 003 000 005 000 000 005 005 007 005 000 000 000 000 000 000
10 Donax trunculus 015 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 001 000 000 000 001 000 000 000 000 005 000 000 005 005 000 005 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 001 000 000 002 000 000 000 002 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000 000
14 Haustorius arenarius 002 000 000 009 000 000 000 013 000 000 029 000 043 000 000 041 041 000 041 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 001 000 000 002 000 000 000 001 000 000 003 000 004 000 000 004 004 000 004 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 001 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
19 Ophiura ophiura 009 000 000 000 000 000 000 068 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 000 001 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 001 001 012 001 000 000 000 000 000 000
22 Scolelepis squamata 003 000 000 011 000 000 000 007 000 000 015 000 023 000 000 022 022 000 020 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000 000
26 Phytoplankton 000 000 000 016 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 100
27 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 100 000
28 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000 000
29 Import 021 000 000 007 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000 000
6 Apendix
Capiacutetulo 4
122
Table A2 Predatoryprey matrix of Valdegrana beach before balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 020 003 000 000 000 000 000
6 Cumopsis fagei 000 000 000 002 000 000 000 002 000 000 004 000 006 000 000 006 006 034 006 000 000 000 000 000
7 Bivalvia 017 000 096 023 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 024 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 002 000 000 000 002 000 000 005 000 008 000 000 008 008 000 008 000 000 000 000 000
10 Donax trunculus 005 000 004 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 001 001 000 001 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 008 001 000 000 000 000 000
13 Glycera tridactyla 000 000 000 001 000 000 000 001 000 000 003 000 000 000 000 005 005 000 005 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 001 001 000 001 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 001 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 001 000 000 000 002 000 000 005 000 007 000 000 007 007 000 007 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 001 000 002 000 000 002 002 000 002 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 072 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 001 000 000 002 000 003 000 000 003 003 022 003 000 000 000 000 000
22 Scolelepis squamata 000 000 000 014 000 000 000 017 000 000 043 000 067 000 000 064 064 000 062 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 033 000 025 033 000 000 000 000 000 000 000 000 000 033 000 025 000 000
25 Phytoplankton 000 000 000 017 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 100
26 Detritus (sediment) 000 000 000 000 033 033 000 000 025 000 000 033 000 033 033 000 000 014 002 000 033 025 033 000
27 Detritus (water) 000 000 000 000 033 033 033 000 025 033 000 033 000 033 033 000 000 000 000 033 033 025 033 000
28 Import 078 000 000 006 000 000 000 000 000 000 030 000 000 000 000 000 000 000 000 000 000 000 000 000
Capiacutetulo 4
123
Table A3 Predatoryprey matrix of Levante beach after balancing the model
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400 2500
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 000 000 000 000 000 000 000 000 000 012 000 000 001 000 001 000 000 001 000 000 000 000
6 Cumopsis fagei 001 000 000 001 000 000 000 001 000 000 000 000 000 000 000 003 000 000 000 000 000 000 000 000 000
7 Bivalvia 010 000 042 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 004 000 000 008 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 047 000 038 040 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 001 000 000 000 000 000 000 001 000 000 000 000 000 000 000 015 000 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 003 000 000 004 000 000 000 003 000 000 004 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 005 000 000 002 000 000 000 009 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 000 000 000 000 000 000 000 000 000 002 000 000 000 000 000 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Talitrus saltator 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
25 Zooplankton 000 000 000 000 000 000 006 000 004 006 000 000 000 000 000 000 000 000 000 020 000 004 000 000 005
26 Phytoplankton 000 000 000 000 000 000 060 000 001 060 000 000 000 003 020 000 000 000 000 020 000 010 006 000 040
27 Detritus (sediment) 000 000 000 000 090 090 000 025 041 000 038 087 046 092 067 016 044 058 040 000 068 037 089 080 000
28 Detritus (water) 000 000 000 000 005 005 000 000 055 000 000 007 000 005 010 000 000 000 000 060 000 049 005 000 055
29 Import 028 000 020 043 005 005 034 060 000 034 057 006 039 000 003 064 055 040 060 000 031 000 000 020 000
Capiacutetulo 4
124
Prey predator 100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2100 2200 2300 2400
1 Shorebirds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
2 Piscivorous birds 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
3 Eurasian Oystercatcher 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
4 Coastal fish 000 100 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
5 Bathyporeia pelagica 000 000 000 001 000 000 000 000 000 000 001 000 002 000 000 007 000 002 000 000 000 000 000 000
6 Cumopsis fagei 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 001 000 000 000 000 000 000
7 Bivalvia 017 000 096 038 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
8 Decapoda 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
9 Dispio uncinata 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000 000 000 000
10 Donax trunculus 005 000 004 013 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
11 Eurydice affinis 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 000 000
12 Mysida 000 000 000 000 000 000 000 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 000 000
13 Glycera tridactyla 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
14 Haustorius arenarius 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
15 Lekanespahera rugicauda 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
16 Nemertea 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
17 Nepthys hombergii 000 000 000 000 000 000 000 001 000 000 001 000 001 000 000 001 000 000 000 000 000 000 000 000
18 Onuphis eremita 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
19 Ophiura ophiura 000 000 000 000 000 000 000 014 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
20 Paraonis fulgens 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
21 Pontocrates arenarius 000 000 000 001 000 000 000 000 000 000 001 000 000 000 000 001 000 000 000 000 000 000 000 000
22 Scolelepis squamata 000 000 000 001 000 000 000 001 000 000 011 000 007 000 000 000 005 000 000 000 000 000 000 000
23 Siphonoecetes sabatieri 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000 000
24 Zooplankton 000 000 000 000 000 000 008 000 025 008 000 000 000 000 000 000 000 000 000 033 000 025 000 013
25 Phytoplankton 000 000 000 000 020 020 060 000 025 060 000 020 000 010 033 000 000 000 000 033 014 025 010 080
26 Detritus (sediment) 000 000 000 000 070 070 000 023 025 000 035 050 050 080 033 025 054 057 039 000 075 025 080 000
27 Detritus (water) 000 000 000 000 010 010 000 000 025 000 000 030 000 010 033 000 000 000 000 033 000 025 010 008
28 Import 078 000 000 043 000 000 032 060 000 032 050 000 039 000 000 064 040 040 061 000 011 000 000 000
Table A4 Predatoryprey matrix of Valdelagrana beach after balancing the model
Capiacutetulo 5 Groynes as habitat beaches modifiers A case study in
Southwestern Spain
Capiacutetulo 5
126
Abstract
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring and are defined as shore-perpendicular structures
installed for the purpose of maintaining the beach behind them or controlling the
transport along-shore of sand In this two year study the effects on macrofauna
assemblages and on physical characteristics of sandy beach by a single groyne built
nearby an estuary were evaluated For this we compare community parameters and
abiotic variables at different sites varying distances from the groyne Results revealed
significant changes in the sediment features and in richness density and diversity
index between sites and consistently between years Higher values of community
descriptors were found on sites closer to the groyne Although some species can even
be favored by these changes like the mollusc Donax trunculus any modification of the
natural characteristics of an ecosystem must be viewed with caution
Keywords sandy beach coastal armouring human impact groyne macrofauna
physical features
Capiacutetulo 5
127
1
Coastal development in response to human requirements has led to a
progressive modification and disturbance of sandy beaches that are particularly fragile
and vulnerable to human induced activities (see Defeo et al 2009) Thus the
structures derived from this development including harbours piers seafront
promenade and defense structures among other disrupt the normal sediment
transport and produce a substantial increase of erosion processes on these ecosystems
(Pinn et al 2005) making it necessary further initiatives eg beach nourishment Baird
et al in 1985 determined that 70 of the sandy shores around the world were in
recession so it is possible that the increased pressure on coastal ecosystems would
have raised this percentage
The Spanish coastal area covers 6584 km which 2237 km are sandy beaches
The major extension of these ecosystems makes coastal tourism a main driver of the
economy in this country
Only in the southwestern Spanish coast during the last century a recession
rates of 1m per year was recorded (Muntildeoz-Perez and Enriquez 1998) The continuous
loss of beach sand develops a conflict with the ldquosun and beachrdquo tourism model (Del
Riacuteo et al 2013) therefore hard engineering solutions like groynes seawall and
breakwaters in addition to beach nourishment are the most common practices
included in coastal management plans to address the erosion process but in many
cases more than solution increase the erosion problem
Groynes are one of the oldest types of structures commonly used for stabilizing
beaches in costal armouring (Basco and Pope 2004) The coastal armouring refers to
artificial structures located in coastal areas whose main objective is to combat
erosion Groynes are defined as shore-perpendicular structures installed for the
purpose of maintaining the beach behind them or controlling the transport along-
shore of sand (Kraus et al 1994) Multiple and equidistant groynes arranged along the
beach are normally used inducing accretion on the updrift side and erosion on the
1 Introduction
Capiacutetulo 5
128
downdrift side and result in a more complex topography across and along-shore than
previous to construction (Nordstrom 2013)
Researchers have endeavored to determine the effect of these structures on
the physical characteristics of coastal systems for example Morales et al (2004)
showed how a sandy beach was transformed in an erosional beach due to a groyne
acted as physical barrier that interrupted the supply of sand to the beach and
modified wave refraction and changed wave divergence zone Also these structures
influence the properties of soft sediments like grain size organic matter content redox
conditionshellip( Bull et al 1998 Burcharth et al 2007) and affect the evolution of beach
width (Bernatchez and Fraser 2012) Although these consequences occur at local
scale may also expand to the whole coastline (Burcharth et al 2007) for example
reducing the coastal resilience of storm events and increasing the risk of flooding
(Bernatchez and Fraser 2012) in addition to ecological implications
It is known that sandy beaches are inhabited by a large variety of life (Defeo
and McLachlan 2005) which interact in important food chains and play a key role on
these ecosystems functioning (McLachlan and Brown 2006) Although different
research have shown as beach fauna are vulnerable to human activities especially as a
result of changes in the physical characteristics of coastal ecosystems (ie Lercari and
Defeo 2003 Dugan and Hubbard 2006 Schlacher and Thompson 2012 Leewis et al
2012 Bessa et al 2014 Becchi et al 2014) the effect generated by defense
structures on beach fauna is still limited preventing obtain global conclusions Thus
the ecological implications by hard engineering solutions in coastal management and
conservation rarely are considered (Dugan and Hubbard 2010)
Dugan and Hubbard (2010) determined that coastal armouring had strong
effects on the upper zone of beaches and ecological implications for gulls and seabirds
affected the use of beach habitat for these species and decreased the prey resource
availability Heerhartz et al (2014) showed how armored beaches had substantially
less wrack and demonstrated loss of connectivity across the marine-terrestrial
ecosystems associated to armoring strategies Macrofauna inhabiting sandy beaches
depends heavily on allochthonous inputs (Brown and McLachlan 1990) since they are
an important food resource for birds and fishes any change in the availability and
Capiacutetulo 5
129
input of either stranded wrack or phytoplankton could alter energy flow to higher
trophic levels (Dugan et al 2003)
Focusing on intertidal macrofauna Walker et al (2008) and Becchi et al
(2004) showed that hard engineering structures such as groynes and breakwaters have
ecological effects on biological attributes of the beach fauna In perpendicular
structures an increase in biological attributes in depositional nearby areas were found
while in breakwater the opposite pattern occurred In both cases the response of
macrofauna was measured at a maximum distance of 250 m from the groyne and 100
from the breakwater So the effect of these structures at larger spatial scale is still
unknown
In this study the effects on macrofauna assemblages and on physical
characteristics of sandy beach by a single groyne built nearby an estuary were
evaluated Since only one side of the groyne is available for beach fauna it is possible
that response of this biota be different to that shown by previous works that have
been conducted on both side on multiple groynes extended along the beach or
located in the central beach part Thus to our knowledge this is the first time that a
groyne with these features is studied Specifically the differences in community
descriptors like richness and density the structure of macrobenthic assemblages
morphodynamics and physical features (median grain size organic matter content
moisture sorting coefficient beach width and slope) were compared between sites
located at different distances from the groyne The large spatial scale included in our
sampling design up to 6000 m from the engineering structure aimed to determine
more precisely the spatial extent of the impact
Capiacutetulo 5
130
2
21 Study area
This study was carried out in Punta Umbriacutea beach (37ordm11rsquo9035rdquoN
6ordm58rsquo1403rdquoW) located on the northern sector of Gulf of Caacutediz in south-western of
the Spanish coast (Fig 1) The Huelva coast covers 145 km mainly composed for sandy
beaches In this sector the tidal regime is mesotidal with a mean tidal range of 210 m
(Pendoacuten et al 1998) and medium wave energy up to 05 m in height that coming
from the southwest as the dominant wind flow (Morales et al 2004) The coastline
orientation induces a littoral drift from west to east that redistributing high levels of
sediment along the coast (from 180000 to 300000 m3year) (Rodriacuteguez-Ramiacuterez et al
2003)
Punta Umbriacutea beach is interrupted by Tinto and Odiel rivers estuary This
estuary consists of two channels separated by a succession of sandy ridges and
saltmarshes sub-parallel to the coast where important commercial and fishing
harbour are situated On study beach a groyne 1 km long of natural rock was
constructed in 1984 perpendicular to the shoreline in order to avoid sand inputs and
to stabilize the tidal channel that allows access to fishing harbours (Morales et al
2004)
2 Material and Methods
Fig1 Map of study area showing the six study sites along Punta Umbriacutea beach On site 6 is the Groyne located and is shown in the image Map data copy 2014 Google based on BCN IGN Spain
Spain
Punta Umbriacutea
1
2
3
4
561 km0
Capiacutetulo 5
131
22 Sampling design
Sampling occurred twice on March 2013 and March 2014 during spring low
tides Samples were collected over six sites established at different distances from the
groyne Site 1 located at 6000 m site 2 at 3000 m site 3 at 2000 m site 4 at 500 m
site 5 at 150 m and site 6 immediately continuous to the structure Within each site six
equidistant transect were established perpendicular to the shoreline in a 100 m long-
shore area Each transect comprised 10 equidistant points from high tide water mark
to swash zone At each sampling point a sample was collected for macrofauna analysis
with a 25-cm-diameter plastic core to a depth of 20 cm Samples were sieved on site
through a 1 mm mesh-size sieve collected in a labelled plastic bag and preserved in
70 ethanol stained with Rose Bengal At each sampling level a sample for sediment
features were also collected with a 35 cm diameter plastic tube buried 20 cm deep
The beach-face slope was estimated by the height difference according to Emery
(1961)
In the laboratory macrofauna were separated from remaining sediment
quantified and identified to the lowest taxonomic level possible usually species Four
sediment variables were analysed Median grain size and sorting coefficient were
determined by sieving sediment samples trough a nested mesh sizes (0063 0125
025 05 1 2 and 5 mm) previously dried at 90ordmC for 72 h following Guitiaacuten and
Carballas (1976) sand moisture was determined measuring the weight loss after
drying the samples at 90degC and the organic-matter content was estimated as the
difference between dry sediment weight and sediment weight after calcination at
500degC Morphodynamic state in each site was characterized by the Beach Index (BI)
(McLachlan and Dorvlo 2005) the Beach State Index (BSI) (McLachlan et al 1993) and
the dimensionless fall-velocity parameter (Deanrsquos parameter) (Dean 1973)
23 Data analysis
Permutational multivariate analysis of variance (PERMANOVA) (Anderson
2001 2008) were used to test differences in univariate descriptors (richness density
Capiacutetulo 5
132
and diversity index) in multivariate structure of macrofauna assemblages and in
physical characteristics between sites
The design included two factors Site (Si six levels fixed) and Year (Ye two
levels fixed) and was based on 9999 permutations under reduced model When the
permutations was not sufficient (lt150) an additional p value obtained by the Monte
Carlo test was used Physical variables and univariate parameters were based on
Euclidean distance similarity matrices while multivariate patterns were based on Brayndash
Curtis dissimilarities
In order to test homogeneity of dispersion in all data sets PERMDISP routine
was used (Anderson et al 2008) and data were fourth-root transformed to fulfill this
assumption
A non-metric multidimensional scaling ordination (nMDS) of ldquosite x yearrdquo
interaction centroids was performed to display differences in community structure If
significant differences in the PERMANOVA analysis were identified SIMPER routine
was performed in order to detect species that most contribute to the dissimilarity
All of the above analyses were performed with PRIMER-E v61 and
PERMANOVA + (PRIMER-E ltd) (Anderson et al 2008 Clarke and Gorley 2006)
A canonical correspondence analysis (CCA) (Ter Braak 1986) was applied in
order to determine associations of macrofauna communities with environmental
variables Previously a detrended correspondence analysis (DCA) was used to measure
the gradient lengths and to ensure an unimodal species response (gradient length of
the first axis was greater than 30 SD) For this analysis only the most abundant taxa
were taken into account and were fourth-root transformed while environmental
parameters matrix was Log (x+1) transformed and standardized prior to reducing
extreme values and providing better canonical coefficient comparisons
The statistical significance of canonical eigenvalues in CCA analysis and the
significance of the first two axes were tested by a Monte Carlo test (999
permutations) DCA and CCA were carried out with statistical software package PC-
ORD (McCune and Medford 1997)
Capiacutetulo 5
133
3
31 Physical features
Morphodynamic characterization width and slope of sites are presented in
Table 1 Deanacutes parameter classified sites as intermediate (sites 1-3) and dissipative
(sites 4-6) and BSI index values classified sites as intermediate to dissipative with high
energy The width of the intertidal and slope differed at each site Width increased
from site 1 to 6 while the slope decreased with proximity to the groyne
The sediment features of sites showed the same trend during the whole study period
(Fig 2 Table 2) The median grain size decreased from medium sand at site 1(208φ plusmn
011 in 2013 and 187φ plusmn 019 in 2014) to fine sand at site 6 (262φ plusmn 006 in 2013 and
27 φ plusmn 028 in 2014) The organic matter content varied with proximity to the groyne
The lowest organic content was shown in site 2 (07 plusmn 03 in 2013 and 04 plusmn 01 in
2014) while the maximum rates was found in site 6 (16 plusmn05 in 2013 and 19 plusmn 03
in 2014) Sediment moisture also varied between areas the highest average values
were in sites closer to the groyne (sites 4 5 and 6) The sediment in general was well
sorted (S0lt117) in all sites PERMANOVA test showed significant differences among
sites in the overall sediment features (Table 2) Only in organic matter variable was a
significant ldquoSi x Yerdquo interaction due to a significant differences on site 2 and 4 between
years
Table 1 Comparison of morphodynamics features slope and width of the six study sites Average values of the two years are represented
Width (m) Slope () BI Dean BSI
S1 47 62 202 466 133
S2 73 42 206 343 120
S3 72 44 217 498 135
S4 140 19 279 860 160
S5 163 19 265 861 160
S6 160 16 269 901 160
3 Results
Capiacutetulo 5
134
Table 2 Summary of PERMANOVA test and pair-wise comparison testing differences on the sediment features Si sites Ye Year
Median grain size Organic matter Sorting Moisture
Source df MS F P MS F P MS F P MS F P
Si 5 085 5590 00001 096 4013 00001 022 969 00001 339 726 00001
Ye 1 0002 015 069 002 102 031 004 205 016 018 038 054
Si x Ye 5 001 032 032 006 257 003 001 074 058 050 107 037
Res 108 001 002 002 046
Total 119
Pair-wise test
Organic matter
groups t P (MC)
Site 1 2013-2014 078 0489
Site 2 2013-2014 278 0016
Site 3 2013-2014 108 0297
Site 4 2013-2014 295 001
Site 5 2013-2014 094 0368
Site 6 2013-2014 188 0075
Capiacutetulo 5
135
32 Univariate patterns
A total of 29 taxa were collected comprising amphipods (5) cumaceans (1)
isopods (3) mysidaceans (2) bivalves (3) insects (3) polychaetes (11) and nemerteans
(1)
Species richness density (indm2) and Shannon diversity index showed
significant differences between sites (p (perm) = 00001) consistently between years
ldquoSite x Yearrdquo interaction p (perm) = 0734 for richness p (perm) = 05069 for density
and p (perm) = 05162) for diversity index (Table 3) In both years the maximum
macrofauna richness and density were obtained in sites closer to the groyne (Fig 3)
Richness ranged from 4 plusmn 089 (site 3) to 166 plusmn 16 (site 6) in 2013 and from 416 plusmn
075 (site 2) to 15plusmn12 (site 6) in 2014 Moreover density ranged from 23 plusmn 23 (site 1)
to 446 plusmn 135 (site 6) in 2013 and from 205 plusmn 74 (site 2) to 386 plusmn 134 (site 6) in 2014
The Shannon diversity index followed the opposite pattern the greater diversity was
found in the far groyne site (Site 1) in both years
33 Multivariate patterns
The structure of macrobenthic assemblages changed significantly between sites
(p (perm) = 00001) and was consistent between years (ldquoSi x Yerdquo p (perm) = 00981)
(Table 3) This spatially structured changes in beach fauna community were also
illustrated by the nMDS which showed the centroids of this interaction (Fig 4)
SIMPER analysis showed that 6 species contributed at least to 50 of the average
dissimilarities between sites the amphipods Bathyporeia pelagica and Pontocrates
arenarius the isopod Eurydice affinis the bivalve Donax trunculus and the polychaete
Scolelepis squamata (Fig 5) The average dissimilarity among sites was high Within
sites closer to the groyne (sites 4-5-6) the dissimilarity was about 80 while inward far
site (1-2-3) dissimilarity was about 95 Dissimilarity between far sites closer sites was
also higher over than 90
Capiacutetulo 5
136
Table 3 Permanova results permorfed to test differences in macrofaunal assemblages and univariate descriptors Richness density and Shannon
diversity index between sites and years
Macrofaunal assemblages Richness Density Diversity index
Source df MS F P MS F P MS F P MS F P
Si 5 59585 3195 00001 992 2797 00001 1477 5682 00001 5191 5191 00001
Ye 1 3536 186 01015 018 051 04675 163 062 0433 194 061 044
Si x Ye 5 2668 143 0955 019 055 0734 225 086 0513 268 1085 051
Res 708 1864 003 259 314
Total 719
Fig3 Variation of univariate descriptors (richness density and Shannon index) recorded at six study sites at both years Mean values (plusmn SD) are represented
sites
1 2 3 4 5 6
0
5
10
15
20
25
30Moisture
ph
i00
05
10
15
20
25
30
35
1 2 3 4 5 6
Sites
Median grain size
00
05
10
15
20
25
30
1 2 3 4 5 6
Sites
Organic matter content
Sites
1 2 3 4 5 6
00
05
10
15
20
25Sorting
00
05
10
15
20
25
30
2013
2014
1 2 3 4 5 6
Organic matter content
Capiacutetulo 5
137
Bathyporeia pelagica
indm
2
0
5
10
15
20
25
30Pontocrates arenarius
0
2
4
6
8
10
Eurydice affinis
indm
2
0
2
4
6
8
10
12
14Scolelepis squamata
0
50
100
150
200
250
Donax trunculus
Sites
1 2 3 4 5 6
ind
m2
0
50
100
150
200
250
20132014
1
2
3
4 5
6
1
2 3
4 5
6
2D Stress 001
Fig 5 Density (mean indm2 plusmn SD) at each site of species identified by SIMPER analysis as typifying
Capiacutetulo 5
138
34 Macrofauna- environmental variables relationships
Environmental variables (median grain size sorting coefficient organic matter
content and sediment moisture) were significantly related to the fauna variation
tested by Monte Carlo permutation test (plt005) The Monte Carlo test for the set of
environmental variables was significant for both axes (p=0008) and for eigenvalues
(p=0003) showing a significant relationship between biological data and predictor
environmental variables
CCA results showed that environmental variables explained 501 of
macrofauna density variation Pearson species-environmental correlations were
relatively high 093 for Axis 1 and 072 for Axis 2 Most of the variance was explained
by the first axis (explained 80 of the total variation explained) and was correlated
positively with sorting coefficient (0829) and negatively with median grain size (-
0913) sand moisture (-0919) The second and third axis accounted for 15 and 5 of
total variation explained respectively The axis 2 was correlated negatively mainly with
organic matter content (-0503) (Table 4) (Fig 6)
Table 4 Axis summary statistics obtained from CCA analysis
Axis 1 Axis 2 Axis 3
Eigenvalue
0106 0019 0006
Variance in species data
of variance explained 405 74 22
Cumulative explained
405 479 501
Pearson Correlation Spp-Envt 0939 0724 0670
Capiacutetulo 5
139
1
2
3 4
5
6 1
2 3 4
5
6
Bathyporeia pelagica
Cumopsis fagei
Donax trunculus
Eurydice affinis
Gastrosaccus sanctus
Gastrosaccus spinifer
Glycera tridactyla
Haustorius arenarius
Magelona papilliforme Nemertea
Nepthys cirrosa
Onuphis eremita
Pontocrates arenarius
Scolelepis squamata
Mgs Sort Mo
Moist
Axis 1
Axis 2
2013
2014
Fig6 Triplot resulting from CCA analysis Black circles represents the most abundant species in each site Arrows are explanatory variables Moist= Sand moisture Mgs= Median grain size Sort=Sorting MO= organic matter content
Capiacutetulo 5
140
4
In the current study the effects of a groyne on intertidal beach fauna and on
physical and morphodynamics features were evaluated In contrast to previously
studies about defence structure on sandy beaches (Walker et al 2008) the adjacent
beach was sampled entirety to a distance of 6000 m from the construction in order to
detect the effect of groyne extends far
Focusing on physical and sediment features the results showed that
engineering construction likes groynes have significant effects on these variables
consistent in the two years sampled Thus at the closest areas finer sediment best
sorted and with greater organic matter content was found It appears that the groyne
favors the deposition of fine sediment altering the littoral drift of sediment along-
shore which could promote the retention of water and nutrients from the mouth of
nearby rivers Groynes can also modify the wind and the eolian transport of sediment
as well modify wave process (Hanley et al 2014)
The results showed that variations in physical characteristics of the sediment
were spread to a distance of 500 meters (site 4) since from here the abiotic variables
change and stay stable in the remaining beach This finding was also observed by
Walker et al (2008) who detected a change in the attributes of the sediment on the
north-side of a groyne located on Palm beach (Australia) where sediment deposition
occurs but the effect was limited to the first 15 meters So it appears that the size of
the building and their position on the beach could determine the extent of the effect
The deposition of sediment also increased the width beach at the nearby sites
and a decrease in their slope causing changes in morphodynamics state of each site
being nearby areas more dissipative
Physical variability in sandy beaches has been identified as the primary force
controlling macroinfaunal communities (McLachlan 1983) in fact our results revealed
that predictor abiotic variables explained a large portion of the variability of the beach
fauna Also the morphodynamic state determines the attributes of the benthic
communities (Defeo and McLachlan 2005) increase in richness density total
abundance and biomass from microtidal reflective beaches to macrotidal dissipative
4 Discussion
Capiacutetulo 5
141
beaches (McLachlan 1990 Jaramillo et al 1995) In addition Rodil et al 2006
indicated that slope and beach length were the most important factors explaining
variability in species density These assertions could explain the higher densities and
richness found in areas near to the groyne This pattern were similar to those obtained
by Walker et al (2008) who found that species richness was higher in areas near to
the groyne in the depositional side while Fanini et al (2009) showed that repetitive
groynes built parallel to coastline act as ecological barriers especially in supralittoral
species Not all engineering structures act the same way for example Becchi et al
(2014) showed that in breakwaters density and richness of beach fauna were lower in
nearby areas Thus the magnitude of the influence of different engineer construction
seems to be related to the habitat complexity introduced by them and the way this
habitat complexity modulates the environmental forces (Sueiro et al 2011)
Changes in taxonomic community structure were also evident between sites
and the amphipods Bathyporeia pelagica and Pontocrates arenarius the isopod
Eurydice affinis the spionid Scolelepis squamata and the mollusc Donax trunculus
contributed especially to differences inter-sites Of all these species it seems that D
trunculus was the most favored specie by the new induced conditions since high
densities were found in sites near to the groyne (sites 4-6) while in remote areas was
almost inexistent This bivalve is one of the better-known species in eastern Atlantic
waters and occurs primarily in the intertidal zone of sandy beaches (De la Huz et al
2002) Over the past few decades numerous studies have related life habits of these
bivalves to sedimentary characteristics and D trunculus have been used as sentinel
species for biomonitoring studies in sandy beaches (Tlili et al 2011) D trunculus is a
substrate-sensitive organism in finer sand increase their burrowing rate growth and
metabolism (De la Huz et al 2002) Thus site nearby to groyne have optimal features
for increase the ecological efficience of D trunculus and their densities consequently
Groynes and other hard engineering constructions also have been identified
like urban structures that provide a new substrate for colonization of new species
growing on them and may influence the dispersal of some organisms (Pinn et al 2005)
which may result in an increase of local abundance and species diversity (Glasby and
Connell 1999) But this enhancement in the biological attributes of the community
Capiacutetulo 5
142
and the potential positive effect generated by engineering structures should viewed
cautiously as recommended by Glasby and Connell (1999) since may occur in response
to an environmental impact
An environmental disturbance must be defined as any change from average
natural conditions and may result in an increased of biological attributes near to
impacted sites (Clarke and Warwick 2001) therefore the increases in abundances
relative to natural conditions are indeed impacts (Glasby and Connell 1999)
Information prior construction of this groyne were no available so a temporal
variation study comparing before-after impact that could explain the evolution of the
macrofauna communities along time was not possible and either a comparative study
on both sides of the groyne since in the other side was located the mouth of Tinto and
Odiel rivers
Despite these the site 1 considered in the current study and located at 6000 m
from the groyne could be considered as a reference site where there was no
influence of the groyne structure and whose characteristics could be considered as
natural conditions in absence of disturbance Thus site 1 although the richness and
density were lower than those site closest to the groyne this zone presented the
greatest diversity of the whole study
In summary this study shows how engineering structures such as groynes
result in major changes in the ecosystems where they are located These changes are
related to modification in natural features of the beaches in the first instance by
modifying the sedimentological attributes and the natural morphodynamics of
beaches Benthic communities inhabiting the sandy beaches respond to these changes
by altering both their biological attributes and the taxonomic structure of their
community Some species can even be favored by these changes But any modification
of the natural characteristics of an ecosystem must be viewed with caution
In this study it is shown how the groyne increases the width of the beach as a result of
sediment deposition It is possible that over time these accumulations eventually
exceed the breakwater which will make necessary future actions to dredge the canal
and the beach itself which will have dire consequences for the ecosystem
Capiacutetulo 5
143
Therefore although at first glance the changes observed could be interpreted
as a positive effect should not be considered as such since any modification of the
natural conditions of an area should be considered an impact
Future studies in the longer term on the evolution of the beach in both abiotic
and biologically features are of special interest for future decision-making in the
management policies of these structures
Capiacutetulo 5
144
5
A Anderson MJ 2001 A new method for non-parametric multivariate analysis of variance
Austral Ecology 26 32ndash46 Anderson MJ Gorley RN Clarke KR 2008 PERMANOVA for PRIMER guide to software
and statistical methods PRIMERndashE Ltd Plymouth United Kingdom
B Basco DR Pope J 2003 Groin functional design guidance from the Coastal Engineering
Manual Journal of Coastal Research 33 121-130 Becchi C Ortolani I Muir A Cannicci S 2014 The effects of breakwaters on the structure
of marine soft-bottom assemblages A case study from a North-Western Mediterranean basin Marine Pollution Bulletin 87 131-139
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Queacutebec Canada Journal of Coastal Research 28 1550ndash1566
Bessa F Gonccedilalves SC Franco JN Andreacute JN Cunha PP Marques JC 2014 Temporal changes in macrofauna as response indicator to potential human pressures on sandy beaches Ecological Indicators 41 49ndash57
Brown A C M cLachlan A 1990 lsquoEcology o f Sandy Shores Elsevier Amsterdam Bull CFJ Davis AM Jones R 1998 The Influence of Fish-Tail Groynes (or Breakwaters) on
the Characteristics of the Adjacent Beach at Llandudno North Wales Journal of Coastal Research 14 93-105
BurcharthHF HawkinsSJ ZanuttighB LambertiA2007 EnvironmentalDesign Guidelines for Low Crested Coastal Structures Elsevier Amsterdam
C Clarke KR Gorley RN 2006 PRIMER v6 User ManualTutorial PRIMER-E Plymouth Clarke KR Warwick RM 2001 Change in Marine Communities An Approach to Statistical
Analysis and Interpretation second ed PRIMER-E Plymouth
D De la Huz R Lastra M Loacutepez J 2002 The influence of sediment grain size on burrowing
growth and metabolism of Donax trunculus L (Bivalvia Donacidae) Journal of Sea Research 47 85-95
Dean RG 1973 Heuristic models of sand transport in the surf zone In First Australian Conference on Coastal Engineering 1973 Engineering Dynamics of the Coastal Zone Sydney NSW Institution of Engineers Australia 1973 215-221
Defeo O McLachlan A 2005 Patterns processes and regulatory mechanisms in sandy beach macrofauna a multi-scale analysis Marine Ecology Progress Series 295 1-20
Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Del Riacuteo L Gracia FJBenavente J 2013 Shoreline change patterns in sandy coasts A case study in SW Spain Geomorphology 196 252ndash266
Dugan JE Hubbard DM McCrary MD Pierson MO 2003 The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California Estuarine Coastal and Shelf Science 58 25-40
Dugan JE Hubbard DM 2006 Ecological responses to coastal armoring on exposed sandy beaches Shore and Beach 74 10ndash16
5 References
Capiacutetulo 5
145
Dugan JE and Hubbard DM 2010 Ecological effects of coastal armoring A summary of recent results for exposed sandy beaches in southern California in Shipman H Dethier MN Gelfenbaum G Fresh KL and Dinicola RS eds 2010 Puget Sound Shorelines and the Impacts of ArmoringmdashProceedings of a State of the Science Workshop May 2009 US Geological Survey Scientific Investigations Report 2010-5254 p 187-194
F Fanini L Marchetti GM Scapini F Defeo O 2009 Effects of beach nourishment and
groynes building on population and community descriptors of mobile arthropodofauna Ecological indicator 9 167-178
G Glasby TM Connell SD 1999 Urban structures as Marine habitats Ambio 7 595-598 Guitian F Carballas J 1976 Teacutecnicas de anaacutelisis de suelos Pico Sacro Santiago de
CompostelaEspantildea
H Hanley ME Hoggart SPG Simmonds DJ Bichot A Colangelo MA Bozzeda F
Heurtefeux H Ondiviela B Ostrowski R Recio M Trude R Zawadzka-Kahlau Thompson EC 2014 Shifting sands Coastal protection by sand banks beaches and dunes Coastal Engineering 87 136-146
Heerhartz SM Dethier MN Toft JD Cordell JR Ogston AS 2014 Effects of Shoreline Armoring on Beach Wrack Subsidies to the Nearshore Ecotone in an Estuarine Fjord Estuaries and Coasts 37 256ndash1268
J Jaramillo E McLachlan A Dugan J 1995 Total sample area and estimates of species
richness in exposed sandy beaches Marine Ecology Progress Series 119 311-314
K Kraus NC Hanson H Blomgren SH 1994 Modern functional design of groin systems In
Coastal Engineering Proceeding of the Twenty-fourth Coastal Engineering Conference American Society of Civil Engineers New York pp 1327-1342
L Lercari D Defeo O 2003Variation of a sandy beach macrobenthic community along a
human-induced environmental gradient Estuarine Coastal and Shelf Science 58 17ndash24 Leewis L Van Bodegom PM Rozema J Janssen GM 2012 Does beach nourishment
have long-term effects on intertidal macroinvertebrate species abundance Estuarine Coastal and Shelf Science 113 172-181
M McCune B Medford MJ 1997 PC-ORD Multivariate analysis of ecological data Version 3
for Windows MjM Software Design Gleneden Beach Oregon McLachlan A 1990 Dissipative beaches and macrofauna communities on exposed intertidal
sands Journal of Coastal Research 6 57-71 McLachlan A Erasmus T 1983 Sandy beach as ecosystems W Junk The Hague McLachlan A Brown AC 2006 The ecology of sandy shores Academic Press Burlington
Massachusetts
Capiacutetulo 5
146
McLachlan A Dorvlo A 2005 Global patterns in sandy beach macrobenthic communities Journal of Coastal Research 21 674ndash687
McLachlan A Jaramillo E Donn TE Wessels F 1993 Sandy beach macrofauna communities and their control by the physical environment a geographical comparison Journal of Coastal Research 15 27ndash 38
Morales JA Borrego J Ballesta M 2004 Influence of harbour constructions on morphosedimentary changes in the Tinto-Odiel estuary mouth (south-west Spain) Environmental Geology 46 151ndash164
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
Muntildeoz-Perez JJ Lopez de San Roman-Blanco B Gutierrez-Mas JM Moreno L Cuena GJ 2001 Cost of beach maintenance in the Gulf of Cadiz (SW Spain) Coastal Engineering 42 143ndash153
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
P Pendoacuten JG Morales JA Borrego J Jimenez I Lopez M 1998 Evolution of estuarine
facies in a tidal channel environment SW Spain evidence for a change from tide- to wave-domination Marine Geology 147 43-63
Pinn E H Mitchell K Corkill J 2005 The assemblages of groynes in relation to substratum age aspect and microhabitat Estuarine Coastal and Shelf Science 62 271-282
R Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Rodriacuteguez-Ramiacuterez A Ruiz F Caacuteceres LM Rodriacuteguez-Vidal J Pino R Muntildeoz JM 2003 Analysis of the recent storm record in the southwestern Spanish coast implications for littoral management Journal of the Total Environment 303 189-201
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sueiro M Bortolus A Schwindt E 2011 Habitat complexity and community composition
relationships between different ecosystem engineers and the associated macroinvertebrate assemblages Helgoland Marine Research 65 467477
T Ter Braak CJE 1986 Canonical correspondence analysis a new eigenvector technique for
multivariate direct gradient analysis Ecology 67 1167-1179 Tlili S Meacutetais I Boussetta H Mouneyrac C 2010 Linking changes at sub-individual and
population levels in Donax trunculus Assessment of marine stress Chemosphere 81692-700
Capiacutetulo 5
147
W Walker SJ Schlacher TA Thompson LMC 2008 Habitat modification in a dynamic
environment The influence of a small artificial groyne on macrofaunal assemblages of a sandy beach Estuarine Coastal and Shelf Science 79 2434
Y Yepes V Medina JR 2005 Land use tourism models in Spanish coast areas A case study of
the Valencia region Journal of coastal research 49 83-88
Capiacutetulo 6 Does the gathering of shellfish affect the behavior of scavenger
gastropods on sandy beaches A field experiment
Capiacutetulo 6
149
Abstract
Carrion on beaches can be an unpredictable and ephemeral resource over time
and it is affected by the tidal regime where the ground is frequently washed by
incoming tides In this ecosystem economic activity such as the commercial harvesting
of molluscs in coastal areas leads to the presence of discarded damaged and dying
specimens of bivalves on the sand Thus although on sandy beaches carrion usually
represents a minor food source human harvesting activity can be of major importance
to scavengers During low tide intertidal scavenger gastropods remain buried in the
substrate and emerge when they detect carrion However in some instances these
gastropods emerge in response to mechanical disturbance regardless of the presence
of food The study reported here concerns the effect of human activity such as
trampling on sandy beaches during shellfish gathering on the behavior of the
scavenger gastropod Cyclope neritea in terms of emersion and food location The goal
was achieved by carrying out short-term field experiments on a sandy beach on the
European Atlantic coast (SW Spain) The results demonstrate that in a similar way to
the presence of carrion on the ground human trampling affects the behavior of C
neritea which emerges to the surface of the sediment and moves on the ground It is
hypothesized that this is a potential trophic facilitation by shellfishers because the
emersion and movement of gastropods at low tide is induced during the period when
the amount of food on the ground increases due to shellfish gathering Nevertheless
the increase in activity implies a higher predation risk for scavengers when they
emerge from the sand In order to avoid predation gastropods generally use alarm
cues such as the detection of damaged conspecifics as an anti-predatory strategy The
behavioral response of C neritea to the presence of damaged conspecifics was also
studied The results of this study highlight the fact that scavengers emerge from the
sediment in response to trampling and the presence of carrion on the sediment
surface and although the presence of damaged conspecifics may act as a cue to
gastropods C neritea does not respond to this stimulus until it makes contact with
them
Keywords Sandy beach human trampling scavenger behaviour Cyclope neritea
Capiacutetulo 6
150
1
Human activities such as shellfish gathering may influence the structure and
populations of the invertebrate community (McKillup and McKillup 1997 Morton and
Britton 2003) Facilitation has been defined as ldquoencounters between organisms that
benefit at least one of the participants and cause harm to neitherrdquo (Stachowicz 2001)
For example the presence of humans may affect the prey populations but also may
favor the development of other species that either compete with them or feed on
carrion In this case the relation is called lsquotrophic facilitationrsquo (Daleo et al 2005) On
beaches carrion may be an unpredictable and ephemeral resource in time and this is
affected by the tidal regime where the ground is frequently washed by incoming tides
However although carrion usually represents a minor food source on sandy beaches it
can attain major importance with a trophic facilitator such as humans (McLachlan and
Brown 2006)
Carrion deposited on the sand implies a higher predation risk for scavengers
which have to emerge from the sand therefore the carrion should be quickly detected
and consumed by scavengers (Morton and Britton 2003 Morton and Jones 2003) To
avoid predation the use of alarm cues is common in aquatic organisms (Daleo et al
2012) For example the detection of damaged conspecifics by scavenger gastropods is
frequently used as an anti-predatory strategy (Stenzler and Atema 1977 McKillup and
McKillup 1994 Davenport and Moore 2002 Morton and Britton 2003 Daleo et al
2012)
The effect of trampling on shores has been extensively studied (eg Beauchamp
and Gowing 1982 Davenport and Davenport 2006 Farris et al 2013) and it is
associated with economic activities such as tourism and commercial harvesting in
coastal areas (Sarmento and Santos 2012 Schlacher and Thompson 2012 Veloso et
al 2008) The literature shows that human trampling clearly has negative effects on
the fauna of sandy beaches (eg Moffet et al 1998 Farris et al 2013 Reyes-Martinez
et al 2015) and this is considered to be a major cause of biodiversity loss (Andersen
1995) A common source of disturbance is repeated human trampling on the substrate
and shellfish harvesting (Sheehan et al 2010)
1 Introduction
Capiacutetulo 6
151
Very few studies have focused on the effects of thixotropy (the property of
certain gels to decrease in viscosity when shaken and return to the semisolid state
upon standing Dorgan et al 2006) or dilatancy (the increase in volume due to the
expansion of pore space when particles begin to move (Duran 2000) of the sand
caused by human trampling on living invertebrates buried in the sand (Wieser 1959
Dorgan et al 2006)
Although previous studies have not been published on the responses of
scavengers to human trampling it is possible that these animals find and consume
carrion quickly if they are able to detect the food rapidly In this sense it might be
hypothesized that an increase in the activity of gastropods caused by trampling could
exert a trophic facilitation effect because snails increase their mobility which allows
them to find carrion faster than when they are buried and are inactive in the sediment
In Southern Europe the bivalve Solen marginatus the grooved razor clam is a
commercial species that burrows in the soft bottom This species is exploited in natural
beds in intertidal and shallow subtidal areas of estuaries and beaches Over the year
and especially during the spring and summer months this area is harvested
intensively The removal techniques used frequently cause injury to the bodies of the
clams whereupon specimens are left on the sand as carrion In addition shellfish
gatherers tend to leave damaged grooved razors that are smaller than the required
commercial sizes so these also remain dying on the sand as potential carrion for
scavengers (Peacuterez-Hurtado and Garciacutea personal observation) (Fig 1)
The nassariid Cyclope neritea is a burrowing marine snail that is found in
shallow and intertidal habitats with medium to fine sand This species has dense
populations in areas of Levante beach where S marginatus harvesting is intense Like
other nassariids C neritea is predominantly a scavenger (Bachelet et al 2004)
although it also ingests sand together with bacteria and diatoms (Southward et al
1997) This species has a native distribution range in the Mediterranean Black Sea and
Atlantic coasts of the Iberian Peninsula to the southern part of the Bay of Biscay
(northern Spain) (Sauriau 1991 Southward et al 1997) The distribution spreads
northwards along the French Atlantic coast up to the entrance of the English Channel
which indicates human-induced introductions as the probable cause for the spread
Capiacutetulo 6
152
(Simon-Bouhet et al 2006 Couceiro et al 2008)
During low tide C neritea usually remains buried in the substrate (Morton
1960) but it sometimes emerges in response to mechanical disturbances (Bedulli
1977) In this sense the observations of Bedulli (1977) could serve as a basis for the
hypothesis that the effect of human trampling on the sediment stimulates the snail to
intensify its activity which could lead it to detect food more quickly C neritea and S
marginatus co-occur in sandy beaches of Southern Spain and the bivalve discarded by
shellfishermen is a potential source of food for the gastropod
In this context by using C neritea as an experimental subject the objectives of
this work were to describe how a gastropod scavenger responds to the presence of
human trampling food and damaged congeners during low tides on a sandy beach
On considering the goals of this study the following questions were raised
- Is there a change in the behavior of C neritea due to stimuli caused by the
trampling of shellfishermen and the presence of carrion
- Does the presence of damaged congeners have a negative effect on the
appoach of C neritea to prey as a defensive response to reduce the risk of predation
Fig 1 Cyclope neritea on carrion of Solen marginatus
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2
21 Study area
Field experiments were carried out at Levante beach during the days of spring
tides from April to May of 2013This beach is 42 Km long and is a preserved site within
the Cadiz Bay Natural Park located in southern Spain (36ordm3258 N 6ordm1335 W) (Fig
2) This is a dissipative beach that has a mesotidal regime (with tidal amplitude up to
32 m) with up to 150 m of beach uncovered at low water during the spring tides This
site is bordered to the east by a densely urbanized site (Valdelagrana) and to the west
by the mouth of the San Pedro River with presence of native vegetation dunes and a
salt marsh in the post-beach During the study period the air temperature at Levante
beach ranged from 199 to 216 ordmC the ground temperature ranged from 176 to 207
ordmC and the interstitial water had a salinity of 36
The area in which the experiments were carried out was selected as it is the
zone in which C neritea is abundant and where Solen marginatus harvesting is intense
In addition the distance to the line of low tide allowed the plots to be exposed while
2 Material and Metodhds
6ordm 18 W 6ordm 12rsquo W0 1 km
Source Map data copy2014 GeoBasis-DeBKG (copy2009) Google based on BCN IGN Spain
Levante
Atlantic Ocean - Caacutediz Bay
6ordm 12rsquo W6ordm16rsquo W
36ordm 34rsquo N
36ordm 32rsquo N
Fig2 Map of study area showing Levante beach location
Capiacutetulo 6
154
the experiments were carried out At this site which is located approximately 140 m
from the lower level of the tide there is an abundant population of the snail C neritea
(40 specimensm2 personal observation) Throughout the year and especially during
the spring and summer months the area is harvested intensively by around 20
shellfishermen collecting grooved razor clams (Solen marginatus) Shellfishermen
spend an average of two and half hours at low tide collecting an average of 10 Kg of
razor clams per person with a total of around 200 Kg of bivalves collected per day
Approximately 10ndash15 of the catch is damaged during harvesting Thus some 20ndash25
Kg of crushed razor clams is discarded and these are left on the sand as potential
carrion for scavengers (Peacuterez-Hurtado and Garciacutea personal observation)
22 Effect of human trampling on the activity of Cyclope neritea
To determine the influence of the disturbance caused by trampling induced by
sellfish on the activity of C neritea during low tide 24 plots of 1 m2 were laid out on
the midtide zone parallel to the coastline Plots were allocated to two groups of 12
plots each Plots were set 2 m apart in order to avoid interference between plots (Fig
3) During the experiment one group of plots remained undisturbed while the
remaining 12 were subjected to disturbance which involved walking for 3 minutes on
the plots prior to counting the individual C neritea specimens located on the surface
Trampling started 5 minutes before each census (during the 2 minutes prior to the
census the plots were kept undisturbed in order to avoid the burial of gastropods
caused by trampling) the trampling was conducted by people of similar body mass at a
frequency of 50 steps per minute (similar to that produced by shellfish gatherers as
they move in search of bivalves Hurtado and Garciacutea personal observation) The snails
located on the surface of each plot were counted every 15 minutes To avoid
disturbance on the plots caused by the movement of researchers during the census
counts were performed from a distance of at least 1 m from the edge of each plot The
distance between the low-water mark and the plots was measured as each census was
carried out The counts were made while the tide was ebbing and flooding and the
experiment was ended when the plots were covered by incoming water
Capiacutetulo 6
155
23 Influence of trampling and the presence of food on C neritea activity
In an effort to determine whether the presence of food affects the response of
C neritea to trampling an experimental design similar to that outlined above was
repeated but with the added factor of the presence of food (S marginatus carrion) In
this case 24 plots of 1 m2 were laid out 12 plots were perturbed by trampling as in
the previous experiment and 12 were left undisturbed For each treatment 6 pieces
of razor clam (ca 5 g each) were randomly deposited on 6 plots just before starting the
experiment During trampling care was taken to avoid stepping on food samples in
order to avoid burial Censuses were taken every 15 minutes for 2 hours
24 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The next experiment was aimed at testing the hypothesis that damaged C
neritea specimens act as food or as a danger signal to the other snails approaching the
food A total of 36 plots of 1 m2 were laid out in 9 plots clam carrion was provided
recently deceased C neritea specimens were placed in another 9 plots in 9 plots a
mixture of clam carrion + recently deceased snails were set out and another 9 plots
were considered as controls without the remains of clams or snails Every 5 minutes
over a period of 35 minutes a count was made of the C neritea specimens that had
arrived to feed on the carrion or those on the surface of the plots that did not make
contact with the carrion In plots with carrion 6 pieces of razor clam (ca 5 g each)
were randomly deposited on each plot In plots that only contained recently deceased
C neritea 6 pieces of crushed snails (ca 5 g each) were randomly deposited on each
plot In plots with carrion plus recently deceased snails 6 pieces of a mixture of each
(ca 5 g) were randomly deposited
25 Statistical analyses
The differences between treatments for all experimental designs were analyzed
by repeated measures analysis of variance with sampling time used as a within-subject
Capiacutetulo 6
156
factor and the other treatments (disturbed vs undisturbed food vs no food supply
damaged conspecifics vs no damaged conspecifics) as among-subject factors As the
sphericity assumption was violated (Mauchlys sphericity test) the Greenhousendash
Geisser correction was applied In some cases the data were log (x + 1) transformed
prior to analysis after verifying the homogeneity of variances (Levene test)
Homogeneous groups for among-subject factors were separated by a Studentndash
NewmanndashKeuls (SNK) test while within-subject factors were separated by the
Bonferroni test In the case of significant interactions multiple comparisons between
factors were made by the Bonferroni test In the experiment on the effect of trampling
on C neritea activity a t-test was applied to determine whether the mean abundance
values in each treatment differed significantly between ebbing and flooding time
Statistical analyses were conducted with the software PASW Statistics 18
Fig3Pictures showing the sampling procedure
Capiacutetulo 6
157
3
31 Effect of human trampling on the activity of C neritea
Trampled and undisturbed plots differed significantly (F(124) = 21655 plt
00001) throughout the sampling period (F(7624) = 84 plt 00001) with an interaction
between the two factors (F(7624) = 445 plt 00001) (Table 1 Fig 4) According to the
Bonferroni test the mean number of specimens found was significantly higher in
trampled plots than in undisturbed ones (plt0001) except at the end of the
experimental period during flooding Furthermore the number of C neritea that
emerged onto the surface in trampled plots also varied depending on the tidal cycle
The abundance values in these plots were significantly higher during ebbing than
during flooding (t = 365 p lt001) Nevertheless the undisturbed plots did not show
differences during the experiment except when the water reached the plots (t = ndash047
pgt005) in which case the snails emerged to the surface regardless of the treatment
(disturbed and undisturbed)
df MS F
Within-subject test (Greenhouse-Geisser correction) Time
762
0633
8400
Time x Treatment 76 0335 4452
Error 1675 0075
Among-subject test
Treatment 1 13439 216550
Error 22 0062
3 Results
Table 1 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed) as
an among-subject factor Degrees of freedom df plt00001
Capiacutetulo 6
158
32 Influence of trampling and the presence of food on C neritea activity
A low number of individuals were observed in the plots without food while
plots with added carrion showed a higher number of C neritea specimens on the
surface (Fig 3) The undisturbed control plots in which food was not provided showed
the lowest number of specimens Significant differences were observed between
disturbance treatment (greater number of individuals in trampled plots) (F(148) = 658
plt 001) and food treatment (more individuals in plots with food) (F(148) = 9557 plt
00001) (Table 2) Significant differences were also found over time (F4548= 1127 plt
00001) The number of snails that emerged on the surface increased in all plots when
the tide rose and water reached the plots (Fig 5) Significant interactions were not
found in this case
Fig4 Mean (plusmn SE n = 12) abundance of C neritea specimens for each period of 15 minutes after the start of the experiment Circles trampled plots triangles undisturbed plots dashed line distance from the plots to the tidal line
Capiacutetulo 6
159
df MS F
Within-subject test (Greenhouse-Geisser correction)
Time 446 0378 1127
Time x Treatment 446 0014 040
Time x Food 446 0058 173
Time x Treat x Food 446 0031 091
Error 8927 0034
Among-subject test
Treatment 1 1135 658
Food 1 16480 9557
Treatment X Food 1 0317 184
Error 20 0172
Table 2 Results from a repeated-measures ANOVA showing differences in Cyclope neritea
abundance with time as a within-subject factor and treatment (trampled vs undisturbed)
and the presence of food as among-subject factors Degrees of freedom df plt00001
plt001
Fig5 Mean (plusmn SE n = 6) abundance of C neritea specimens during the experiment Black circle trampled plots with clam carrion white circle trampled plots without clam carrion black triangle undisturbed plots with clam carrion white triangle undisturbed plots without clam carrion dashed line distance from the plots to the tidal level
Capiacutetulo 6
160
33 Response of feeding activity by C neritea in the presence of damaged
conspecifics
The abundance of C neritea observed on the carrion or found lying on the sand
varied significantly between treatments (on the carrion F(336) = 466 and plt001 on
the sand F(336) = 1929 and plt00001) and these patterns proved to be consistent over
time (on the carrion F(3636) = 432 and plt0001 on the sand F(3636) = 556 and
plt00001) (Table 3) Significant interactions were not found between treatments and
time in the abundance of specimens on carrion but significant interactions were found
when considering the specimens lying on the sandy ground (F(11836) = 214 and
plt001) The abundance of snails on the carrion was significantly higher in plots that
contained only clam carrion in comparison to the other treatments (SNK tests plt005
Fig 6a) However abundance did not differ significantly between the clam carrion +
damaged snails and the damaged snail treatments or between the latter and the
control plots (SNK tests pgt005) On the other hand the abundance of C neritea lying
on the sand without making contact with the food was similar in clam carrion and clam
carrion + damaged snail treatments and was significantly higher than that found for
the other treatments (SNK tests plt005 Fig 6b)
df MS F df MS F
On carrion On sand
Within-subject test (Greenhouse-Geisser correction)
Time 360 0086 432 393 0157 556
Time xTreatment 1080 0031 157 1179 0060 214
Error 11525 0020 12577 0028
Among-subject test
Treatment 3 0930 466 3 3523 1929
Error 32 0200 32 0183
Table 3 Results from a repeated-measures ANOVA showing differences in Cyclope neritea abundance observed on the carrion or on the sand with time as a within-subject factor and treatment (control food supply food supply+injured conspecific injured conspecific) as an among-subject factor Degrees of freedom df plt00001 plt0001 plt001
Capiacutetulo 6
161
Fig6 a) Mean (plusmn SE n = 9) abundance of C neritea specimens on clam carrion or damaged gastropods during the experiment b) Mean (plusmn SE n = 9) abundance of C neritea specimens on the plots without making contact with clam carrion or damaged gastropods during the experiment Diamonds plots with clam carrions black squares plots with clam carrions and injured gastropods inverted triangles plots with injured gastropods dark circle control plots
Capiacutetulo 6
162
4
Cyclope neritea responds to the presence of food by rising to the surface
However in the absence of carrion the specimens remain buried throughout the tidal
cycle until the flooding of the plots during the rising tide The results obtained in this
work show for the first time how the mechanical effect of human trampling on sandy
beaches may influence the behavior of C neritea which emerges from the sand
despite the absence of food To date it is not known whether mechanical disturbance
caused by trampling of shellfishermen serves as a warning device to scavengers about
the possible presence of fresh carrion Nevertheless the results of the present study
imply that scavenger snails such as C neritea are sensitive to human trampling over
the sediment in which they are buried and this induces their rise to the surface during
a time in which shellfishermen are discarding bivalve carrion along the beach It seems
that a trophic facilitation exists between C neritea and shellfishermen because C
neritea comes to the surface in the trampled plots even when there is no food on the
ground Furthermore trampling appears to increase the snailrsquos activity thus inducing it
to find food more easily
The presence of carrion in the intertidal zone is an ephemeral resource that is
affected by the rhythm of the tides (Morton and Jones 2003) which in turn also
influences the scavenger populations Therefore the discarding of animal carcasses
helps to increase the densities of scavengers (Schlacher et al 2013) For example
carrion may result from the activities of benthic predators (Oliver et al 1985) and
waders (Daleo et al 2005) As occurs on Levante beach shellfishing on sandy beaches
offers dead and dying bivalves that are consumed by scavengers In addition during
the extraction of bivalves shellfishermen continuously move along the tide line while
it is ebbing Our data on the effect of food and the action of trampling on the activity
of C neritea demonstrate that the presence of carrion stimulates the emersion of the
snail during low tide and this process is reinforced when trampling occurs
4 Discussion
Capiacutetulo 6
163
Invertebrate scavengers have a trade-off between rising to the surface to
obtain food or staying buried to evade predators (Daleo et al 2012) In some cases
the vibration transmitted through the sediment by waders leads to the emersion of
invertebrates thus facilitating predation by birds (Pienkowsky 1983 Keeley 2001
Cestari 2009) In this case the mechanical perturbation through the sediment is
considered to be a negative factor for invertebrates that inhabit the intertidal
environment In the area under investigation wading birds are potential predators of
C neritea However C neritea remains were not detected in the feces or pellets of
these birds on Levante beach (Peacuterez-Hurtado personal observation) which supports
the view that there are no major risks of predation at low tide for this gastropod
Therefore the emergence of the gastropods from the sediment even when there is no
food on the surface suggests that the effect of trampling by shellfishermen harvesting
S marginatus in the sediment could serve as a positive stimulus for C neritea since
surfacing facilitates food detection rather than a negative stimulus that increases the
likelihood of predation
The variation in the behavior of C neritea observed in undisturbed plots over
the tidal cycle ie emerging when the sand is covered with water during high tide
indicates a relationship between the tide pattern and the activity of this snail
regardless of stimuli such as trampling or food Similar behavior for the gastropod
Polynice incei was described by Kitching et al (1987) who correlated the activity
patterns of this species with the tides and registered activity peaks approximately one
hour behind the tidal peaks However this behavior is not general for all gastropod
species for example the nassariid Nassarius dorsatus retreats into the sand when
contact is made by the rising tide (Morton and Jones 2003)
Gastropods are well-endowed with chemoreceptors and they can detect and
respond to chemical signals which trigger a response to food (Crisp 1978 Morton and
Yuen 2000 Ansell 2001) or the avoidance of predators (Jacobsen and Stabell 1999
Daleo et al 2012) In the present study C neritea did not emerge when damaged
conspecifics were added to the plots This suggests that the detection of damaged
conspecifics is an anti-predatory strategy of C neritea as occurs with other scavenger
snails (Davenport and Moore 2002 Morton and Britton 2003 Daleo et al 2012) or
Capiacutetulo 6
164
the gastropod remains buried because it does not detect the stimulus When damaged
conspecifics were added to clam carrion the reaction of C neritea did not coincide
with that of other scavengers Whereas other scavenger gastropods remain buried
(Davenport and Moore 2002 Morton and Britton 2003) C neritea emerged to the
surface The rejection response to the presence of damaged snails of the same species
only occurred when the specimens made contact with the food since the amount of
snails feeding on carrion was greatly reduced when damaged conspecific snails were
present This situation is consistent with the idea that although the detection of the
presence of damaged conspecifics may be an anti-predatory strategy C neritea has a
very limited capacity to perceive this chemical stimulus In the study area C neritea
were normally observed feeding on razor clams Solen marginatus crushed and
discarded by shellfishermen and on the fleshy remains of Cerastoderma edule and
Mactra spp previously opened and partially consumed by Oystercatchers
(Haematopus ostralegus) Secondly this scavenger snail feeds on the corpses of fish
and marine invertebrates such as shrimps and crabs However there is no evidence of
cannibalism in the specimens of C neritea (Garciacutea and Peacuterez-Hurtado personal
observation) This observation is consistent with C neritea declining to approach the
remains of conspecifics
Based on the information described above it can be concluded that mechanical
disturbances caused in sediment by the trampling of shellfish gatherers could induce C
neritea to emerge from the sand even when the natural tendency is to remain buried
when no food is available The presence of carrion on the ground also influences the
activity of C neritea at low tide with an increase in its activity in areas disturbed by
trampling On the other hand although the tendency to emerge when clam carrion is
available persists in the presence of damaged conspecifics the number of specimens
that make contact with food is nevertheless low This finding could indicate that the
defense mechanism that transmits olfactory signals between conspecifics is limited to
distances of a few centimeters during the ebbing tide Therefore this stimulus would
not be as effective and preventive signal against predators
Capiacutetulo 6
165
5
A Andersen AN 1995 Resistance of Danish coastal vegetation types to human trampling
Biological Conservation 71 223-230 Ansell AD 2001 Dynamics of aggregations of a gastropod predatorscavenger on a New
Zealand harbour beach Journal of Molluscan Studies 67 329-341
B Bachelet G Simon-Bouhet B Desclaux C Garciacutea-Meunier P Mairesse G Montaudouin
X de Raigneacute H Randriambao K Sauriau PG Viard F 2004 Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea origin and effects on resident fauna Marine Ecology Progress Series 276 147-159
Beauchamp KA Gowing MM 1982 A quantitative assessment of human trampling effects on a rocky intertidal community Marine Environmental Research 7 279ndash293
Bedulli D 1977 Possible alterations caused by temperature on exploration rhythms in Cyclope neritea (L) (Gastropoda Prosobranchia) Bollettino de Zoologia 44 43-50
C Cestari C 2009 Foot-trembling behaviour in Semipalmated Plover Charadrius semipalpatus
reveals prey on surface of Brazilian beaches Biota Neotropica 9 299-301 Couceiro L Miacuteguez A Ruiz JM Barreiro R 2008 Introduced status of Cyclope neritea
(Gastropoda Nassariidae) in the NW Iberian peninsula confirmed by mitochondrial sequence data Marine Ecology Progress Series 354 141-146
Crisp M 1978 Effects of feeding on the behaviour of Nassarius species (Gastropoda Prosobranchia) Journal of the Marine Biological Associatiob of the United Kindom 58 659-669
D
Daleo P Alberti J Avaca MS Narvarte M Martinetto P Iribarne O 2012 Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics Marine Biology 159 2359-2365
Daleo P Escapa M Isacch JP Ribeiro P Iribarne O 2005 Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay Jorunal of Experimental Marine Biology and Ecology 325 27-34
Davenport J Davenport JL 2006 The impact of tourism and personal leisure transport on coastal environments a review Estuarine Coastal and Shelf Science 67 280-292
Davenport J Moore PG 2002 Behavioural responses of the netted dogwhelk Nassarius reticulates to olfactory signals derived from conspecific and nonconspecific carrion Journal of the Marine Biological Associatiob of the United Kindom 82 967-969
Dorgan KM Jumars PA Johnson BD Boudreau BP 2006 Macrofaunal burrowing the medium is the message Oceanography and Marine Biology 44 85-141
Duran J 2000 Sands Powers and Grains An Introduction to Physics of Granular Materials Springer New York
F Farris E Pisanua S Ceccherellia G Filigheddua R 2013 Human trampling effects on
Mediterranean coastal dune plants Plant Biosystem 147 1043-1051
5 References
Capiacutetulo 6
166
G Goeij Pd Luttikhuizen PC Meer Jvd Piersma T 2001 Facilitation on an intertidal
mudflat the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica Oecologia 126 500-506
J Jacobsen HP Stabell OB 1999 Predator-induced alarm responses in the common
periwinkle Littorina littorea dependence on season light conditions and chemical labelling of predators Marine Biology 134 551-557
K Keeley BR 2001 Foot-trembling in the spur-winged plover (Vanellus miles novaehollandiae)
Notornis 48 59-60 Kitching RL Kughes JM Chapman HF 1987 Tidal rhythms in activity in the intertidal
gastropod Polinices incei (Philippi) Journal of Ethology 5 125-129
M McKillup SC McKillup RV 1994 The decision to feed by a scavenger in relation to the risks
of predation and starvation Oecologia 97 41-48 McKillup SC McKillup RV 1997 Effect of food supplementation on the growth of an
intertidal scavenger Marine Ecology Progress Series 148 109-114 McLachlan A Brown AC 2006 The Ecology of Sandy Shores Academic Press Burlington
MA Moffett MD McLachlan A Winter PED De Ruyck AMC 1998 Impact of trampling on
sandy beach macrofauna Journal og Coastal Conservation 4 87-90 Morton B Britton JC 2003 The behaviour and feeding ecology of a suite of gastropod
scavengers at Watering Cove Burrup Peninsula Western Australia in Wells FE Walker DI Jones DS (Eds) The Marine Flora and fauna of Dampier Western Australia Western Australian Museum Perth pp 147-171
Morton B Jones DS 2003 The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae Buccinidae) in Princess Royal Harbour Albany Western Australia Journal of Molluscan Studies 69 151-156
Morton B Yuen WY 2000 The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong the gastropod Nassarius festivus (Powys) and the hermit crab Diogenes edwardsii (De Haan) Journal of Experimental Marine Biology and Ecology 246 1-29
Morton JE 1960 The habits of Cyclope neritea a style-bearing stenoglossan gastropod Proceeding of the Malacological Society of Londond 34 96-105
O Oliver JS Kvitek RG Slattery PN 1985 Walrus feeding disturbance scavenging habits and
recolonization of the Bering Sea benthos Journal of Experimental Marine Biology and Ecology 91 233-246
P Pienkowski MW 1983 Surface activity of some intertidal invertebrates in relation to
temperature and the foraging behaviour of their shorebird predators Marine Ecology Progress Series 11 141-150
Capiacutetulo 6
167
R Reyes-Martiacutenez MJ Ruiz-Delgado MC Saacutenchez-Moyano JE Garciacutea-Garciacutea FJ 2015
Response of intertidal sandy-beach macrofauna to human trampling An urban vs natural beach system approach Marine Environmental Research 103 36-45
S Sarmento VC Santos PJP 2012 Trampling on coral reefs tourism effects on harpacticoid
copepods Coral Reefs 31 135-146 Sauriau PG 1991 Spread of Cyclope neritea (Mollusca Gastropoda) along the north-eastern
Atlantic coasts in relation to oyster culture and to climatic fluctuations Marine Biology 109 299-309
Schlacher TA Thompson L 2012 Beach recreation impacts benthic invertebrates on ocean-exposed sandy shores Biological Conservation 147 123-132
Schlacher TA Strydom S Connolly RM 2013 Multiple scavengers respond rapidly to pulsed carrion resources at the land-ocean interface Acta Oecologica 48 7-12
Sheehan EV Coleman RA Thompson RC Attrill MJ 2010 Crab-tiling reduces the diversity of estuarine infauna Marine Ecology Progress Series 411 137-148
Simon-Bouhet B Garciacutea-Meunier P Viard F 2006 Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France evidence from mitochondrial sequence data Molescular Ecology 15 1699-1711
Southward AJ Southward EC Dando PR Hughes JA Kennicutt MC Alcala-Herrera J Leahy Y 1997 Behaviour and feeding of the nassariid gastropod Cyclope neritea abundant at hydrothermal brine seeps off Milos (Aegean sea) Journal of the Marine Biological Associatiob of the United Kindom 77 753-771
Stenzler D Atema J 1977 Alarm response of the marine mud snail Nassarius obsoletus specificity and behavioural priority Journal of Chemical Ecology 3 159-171
V Veloso VG Neves G Lozano M Peacuterez-Hurtado A Gago CG Hortas F Garciacutea FJ
2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
W Wieser W 1959 The effect of grain size on the distribution of small invertebrates inhabiting
the beaches of Puget Sound Limnology and Oceanography 4 181-194
168
Capiacutetulo 7
Discusioacuten general
Capiacutetulo 7
169
Durante el transcurso de esta tesis doctoral se han abordado diferentes
aspectos de la ecologiacutea de playas arenosas y en particular la incidencia de
determinadas actividades humanas sobre estos ecosistemas Esto ha sido planteado a
diferentes escalas de estudio tanto a un nivel poblacional y comunitario como a una
escala ecosisteacutemica Asiacute en este capiacutetulo se discuten de manera global las
implicaciones de los resultados obtenidos
En nuestro paiacutes los estudios sobre la ecologiacutea y funcionamiento de playas
arenosas se han circunscrito en su mayoriacutea al norte de la peniacutensula Estos estudios han
descrito las comunidades de macrofauna y sus patrones de zonacioacuten (Rodil et al 2006
Bernardo-Madrid et al 2013) han determinado que factores ambientales son los maacutes
influyentes en la distribucioacuten del bentos (Rodil y Lastra 2004 Lastra et al 2006) a la
vez que se han estudiado las consecuencias de los desastres naturales derivados de la
actividad humana (por ejemplo el derrame de petrolero Prestige) en las comunidades
de invertebrados de las playas (de la Huz et al 2005 Junoy et al 2005 2013) Pero
Espantildea tiene un aacuterea costera de maacutes de 6500 km y muchos de ellos corresponden a
playas arenosas que todaviacutea hoy permanecen inexplorados Un ejemplo es la
comunidad autoacutenoma de Andaluciacutea en la que la informacioacuten referente a los
intermareales es muy escasa Los estudios existentes se han centrado en el margen
occidental costero y relacionados sobre todo con la determinacioacuten de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas asiacute como con los cambios fiacutesicos
producidos en respuesta a eventos meteoroloacutegicos (Benavente et al 2002 Anfuso et
al 2003 Buitrago y Anfuso 2011 del Riacuteo et al 2013) Referente a la macrofauna solo
se han realizado estudios en playas estuarinas localizadas en la desembocadura del riacuteo
Piedras (Huelva) (Mayoral et al 1994) y el efecto del material varado sobre la fauna
supralitoral de los intermareales (Ruiacutez-Delgado et al 2015) Por lo que se careciacutea de
una evaluacioacuten maacutes completa de la biodiversidad presente en las playas arenosas de
Andaluciacutea occidental
De esta forma en el Capiacutetulo 2 de la presente memoria se describe el estado
actual de 12 de playas de Andaluciacutea occidental con el que se contribuye al
conocimiento de las comunidades de invertebrados y de sus patrones de zonacioacuten de
Capiacutetulo 7
170
las variables ambientales maacutes influyentes en la distribucioacuten del bentos asiacute como de las
caracteriacutesticas fiacutesicas y morfodinaacutemicas de las playas ademaacutes de poner a prueba
algunas de las principales hipoacutetesis de la ecologiacutea de playas De este trabajo se
desprende que la mayoriacutea de las playas de Andaluciacutea occidental son esencialmente
ricas y abundantes en biodiversidad con presencia de especies consideradas por la
comunidad cientiacutefica como bioindicadorss y con un patroacuten de distribucioacuten basado
principalmente en tres zonas Ademaacutes las playas estudiadas presentan un amplio
rango de caracteriacutesticas fiacutesicas y estados morfodinaacutemicos
Este estudio presenta una limitacioacuten evidente como es la falta de replicacioacuten
temporal de forma que las fluctuaciones estacionales en los paraacutemetros de las
comunidades de invertebrados no quedan mostradas A pesar de este inconveniente
la amplia escala espacial en la que se ha llevado a cabo hace posible considerar este
estudio como una fuente de informacioacuten fiable
Los trabajos en los que se identifica caracteriza y se mapea la comunidad
bentoacutenica aunque son de caracter descriptivo son de especial relevancia por
ejemplo para identificar aacutereas protegidas asiacute como para establecer herramientas de
gestioacuten para un uso adecuado de los ecosistemas marinos (Martins et al 2013) ya
que representan una ldquoimagenrdquo estaacutetica de la comunidad en su estado de mayor
diversidad
Por ejemplo McLachlan et al (2013) idearon una simple pero a la vez robusta
herramienta para evaluar las condiciones en las que se encuentran las playas y
determinar su idoneidad para un uso recreacional o de conservacioacuten
Fig1 Esquema en el que se representa el Indice de Recreacioacuten y Conservacioacuten para
mostrar el uso maacutes adecuado de la playa (Tomado de McLachan et al 2013)
Capiacutetulo 7
171
De esta forma surgioacute el iacutendice de conservacioacuten (CI) en el que se cuantifica la
presencia de dunas de especies protegidas y la abundancia y diversidad de
macrofauna y el iacutendice de recreacioacuten (RI) basado en la presencia de infraestructuras
fuentes de contaminacioacuten y la capacidad de carga de las playas Ambos iacutendices deben
combinarse para determinar la estrategia de gestioacuten maacutes adecuada (Fig 1)
Estos trabajos son ademaacutes la base para el desarrollo de otras investigaciones
y especialmente uacutetiles para estimar la respuesta de la fauna a futuros cambios en el
haacutebitat asiacute como para la realizacioacuten de estudios comparativos con otras aacutereas ya que
entender como variacutea espacialmente la macrofauna de los intermareales a lo largo de
gradientes ambientales (a una escala latitudinal) es un tema central en ecologiacutea de
playas que aunque actualmente estaacute mejor entendido sigue existiendo mucha
controversia debido principalmente a la dificultad de obtener bases de datos a nivel
mundial (ver Defeo y McLachlan 2013)
Por otro lado las playas son potentes imanes para el turismo y en Espantildea al
igual que en otros paiacuteses costeros el llamado turismo de ldquosol y playardquo tiene una
importancia clave para la economiacutea Esta dependencia de los intermareales para el
crecimiento econoacutemico genera importantes dantildeos en estos ecosistemas tanto por el
intenso desarrollo costero que se hace en ellos como por las diferentes actividades
que soportan Asiacute entender como todas estas actividades afectan a las playas es de
especial importancia para mantener su continuidad De esta forma los capiacutetulos 3 4 y
5 de esta tesis arrojan luz a como diferentes actividades humanas modifican al
ecosistema en general
En el capiacutetulo 3 se ha estudiado el efecto del pisoteo humano en las
comunidades de invertebrados comparando los cambios producidos en los atributos
comunitarios antes y despueacutes del verano periodo de mayor afluencia turiacutestica Aunque
ya existiacutean algunos trabajos previos sobre el efecto de esta actividad es raro que se
utilicen contrastes espacio-temporales en el campo y en muchos casos los efectos
hipoteacuteticos del pisoteo no pueden ser loacutegicamente separados de otros posibles
factores tales como estructuras de defensa urbanizacioacuten costera y limpieza de la
playa entre otros (Barca-Bravo et al 2008 Veloso et al 20062008 2009)
Capiacutetulo 7
172
Dado que la macrofauna vive en ambientes con caracteriacutesticas muy dinaacutemicas
que promueven la plasticidad conductual el raacutepido enterramiento y la movilidad de
los organismos parece loacutegico pensar que las especies de playa deben ser
relativamente resistentes al pisoteo (Schlacher y Thompson 2012) pero como
muestran los resultado del trabajo esto no es del todo cierto En zonas altamente
pisoteadas se observa una reduccioacuten draacutestica de los paraacutemetros de las comunidades
especialmente en la densidad de individuos y cambios en la estructura taxonoacutemica de
la comunidad mientras que en las zonas protegidas no se producen diferencias y la
poblacioacuten se mantiene estable Este trabajo ha permitido tambieacuten identificar aquellas
especies maacutes sensibles al pisoteo y que pudieran ser utilizadas como bioindicadores de
dicho impacto
En el Capiacutetulo 4 tambieacuten se estudia el efecto de la urbanizacioacuten costera a nivel
de ecosistema y por primera vez se han utilizado los modelos de balance de masas
para identificar perturbacioacuten en playas arenosas Ecopath es una herramienta uacutetil para
poner de relieve las principales caracteriacutesticas de las redes alimentarias y los procesos
que intervienen en las interacciones troacuteficas y en los flujos de energiacutea Asiacute los modelos
construidos para las dos playas sintetizan e integran una gran cantidad de informacioacuten
bioloacutegica con el fin de lograr una representacioacuten integrada del ecosistema que
contribuyan a entender los aspectos baacutesicos de su estructura y funcionamiento
(Christensen et al 2008) De una forma resumida los resultados obtenidos en este
capiacutetulo mostraron que la playa protegida es un sistema mucho maacutes complejo
organizado y maduro lo que se podriacutea traducir en una mayor capacidad de resiliencia
que la zona urbana
La urbanizacioacuten de la costa y la construccioacuten de estructuras de ingenieriacutea es un
fenoacutemeno que se viene produciendo desde hace cientos de antildeos modificando
progresivamente el sistema costero Sin embargo hasta hace relativamente poco
tiempo los potenciales impactos ambientales de estos cambios permaneciacutean poco
explorados (Chapman y Underwood 2011 Nordstrom 2013)
Aunque la construccioacuten de estructuras de defensa tiene el objetivo principal de
luchar contra la erosioacuten estudios recientes han mostrados que la playas donde se
Capiacutetulo 7
173
emplazan presentan una reduccioacuten de su anchura entorno al 44 y al 85 incluso en
algunos casos se ha perdido la totalidad del intermareal (Bernatchez y Fraser 2012)
Esta peacuterdida de playa trae consecuencias evidentes para la fauna ademaacutes de
reducir la resiliencia costera frente eventos naturales como las tormentas ya que en
tales circunstancias las playas no son capaces de absorber tan eficazmente la fuerte
energiacutea de las olas asociada a estos temporales
En el Capiacutetulo 5 de la presente tesis se exploran las consecuencias de un tipo
de estructura de defensa en las caracteriacutesticas fiacutesicas y bioloacutegicas de una playa Los
principales efectos son una modificacioacuten sustancial de las caracteriacutesticas
sedimentoloacutegicas perfil anchura y morfodinaacutemica de las zonas maacutes cercanas al
espigoacuten En estas zonas se observa ademaacutes un incremento de la riqueza y densidad
provocada principalmente por el aumento del nuacutemero de individuos de la especie
Donax trunculus que parece verse favorecida por las nuevas condiciones del
sedimento Aunque este aumento de los paraacutemetros comunitarios puede verse como
un efecto positivo dado el intereacutes pesquero de este molusco es en la zona maacutes
alejada que consideramos fuera de la influencia del espigoacuten donde se observan los
mayores iacutendices de biodiversidad
En la Introduccioacuten de este trabajo se realizoacute una revisioacuten general de las
principales actividades humanas perturbadoras de las playas y se hizo referencia a la
pesqueriacutea artesanal de invertebrados o marisqueo Aunque esta actividad no es de las
maacutes agresivas tiene un impacto significativo en las especies objeto de la recolecta
sobre todo si no se hacen seguimientos temporales de las poblaciones para determinar
el mejor momento para su extraccioacuten (Defeo et al 2009) Ademaacutes genera una
importante mortalidad accidental sobre todo cuando el tamantildeo de los individuos no
es el adecuado para su consumo Pero esta actividad puede tener cierto ldquoefecto
positivordquo sobre otras especies que son capaces de modificar su comportamiento en
respuesta al marisqueo Asiacute en el Capiacutetulo 6 se estudia el comportamiento troacutefico del
gasteroacutepodo carrontildeero Cyclope neritea en respuesta a esta actividad Los resultados
mostraron que esta especie es capaz de responder al estiacutemulo del pisoteo inducido por
los mariscadores saliendo a la superficie presuponiendo que habraacute carrontildea
Capiacutetulo 7
174
disponible En ausencia de pisoteo son a su vez capaces de detectar la carrontildea
depositada desenterraacutendose para alimentarse Pero el salir a la superficie los hace
vulnerables y pueden convertirse en presa faacutecil para ciertas especies de aves poniendo
en juego su propia supervivencia En el caso de C neritea la presencia de congeacuteneres
heridos no parece ser detectada a grandes distancias por lo que este estiacutemulo no
resulta tan eficaz contra los depredadores como sucede con otras especies de
gasteroacutepodos carrontildeeros
De estos capiacutetulos se desprende que los efectos ecoloacutegicos derivados de las
actividades humanas se extienden maacutes allaacute de la disminucioacuten de la densidad
abundancia diversidad y de cambios en la estructura de las comunidades de
invertebrados ya que tambieacuten se ve afectado el funcionamiento global del ecosistema
que induce la peacuterdida de sus funcionalidades Por esto mantener los servicios
proporcionados por las playas muchos de los cuales son de especial importancia para
la actividad humana requiere de un compromiso por parte de los planes y poliacuteticas de
conservacioacuten
Actualmente en Espantildea existe un documento sobre las directrices que deben
seguirse ante cualquier actuacioacuten realizada en las playas elaborado por el Ministerio
de Medio Ambiente y su Direccioacuten General de Costas cuyo objetivo fundamental es el
de ofrecer una guiacutea para aquellas actividades realizadas en el litoral
Como actuaciones en el litoral se incluyen aquellas actividades destinadas a la
preservacioacuten y mejora de la franja litoral a la proteccioacuten de la playa como espacio
natural con altos valores ambientales a la optimizacioacuten de los recursos de las playas y
a la adaptacioacuten de las mismas al cambio climaacutetico entre muchas otras Ademaacutes como
accioacuten previa a cualquier actuacioacuten se establece la obligatoriedad de gestionar las
playas iguiendo los criterios mostrados en la figura 2
Aunque se reconoce un gran avance dado la consideracioacuten de las playas como
un ecosistema todas las pautas para las gestioacuten del litoral tienen un corte fiacutesico y se
proponen medidas como la construccioacuten de estructuras de defensa y la regeneracioacuten
de playas ignorando por completo las afecciones sobre la fauna de invertebrados que
las habita
Capiacutetulo 7
175
Dada la creciente informacioacuten cientiacutefica sobre la respuesta de la macrofauna a
las diferentes actuaciones humanas el estudio de las especies presentes asiacute como la
identificacioacuten de aquellas que son bioindicadoras deberiacutea ser una pauta indispensable
en la gestioacuten Se incluye ademaacutes la necesidad de concienciar a la poblacioacuten sobre la
dinaacutemica de las playas con el objetivo de evitar el alarmismo social que provocan las
transformaciones naturales de los litorales arenosos Esta medida deberiacutea extenderse
tambieacuten al conocimiento sobre los valores intriacutensecos de las playas (biodiversidad y
funcionalidad) sin olvidar la importancia del material orgaacutenico varado actualmente
considerado por la sociedad como ldquobasurardquo
Proponer medidas para mitigar el efecto de las actividades humanas como el
pisoteo y la urbanizacioacuten en las playas es extremadamente complicado Algunas
recomendaciones se basan en el estudio de la capacidad de carga de las playas y
controlar el nuacutemero de usuarios que acceden a eacutestas (McLachlan et al 2013) Esta
medida aunque es especialmente uacutetil para proteger a la fauna no es del todo realista
puesto que socialmente no seraacute aceptada y tampoco ganaraacute ninguacuten compromiso
Fig 2 Esquema conceptual de la gestioacuten de playas en las actuaciones realizadas en las playas Obtenido del documento de Directrices Sobre Actuaciones en Playa del Ministerio de Medio Ambiente (Espantildea)
Capiacutetulo 7
176
poliacutetico (Schlacher y Thompson 2012) Otra medida maacutes praacutectica es limitar el uso a
secciones especiacuteficas de las playas Esto ya se viene haciendo por ejemplo para
proteger las dunas donde en la mayoriacutea de los casos el acceso es restringido De esta
forma una medida a aplicar seriacutea el establecimiento en cada playa de una ldquoaacuterea marina
protegidardquo (MPA) Este concepto hace referencia a aquellas zonas en las que las
actividades humanas que causan reducciones en las poblaciones ya sea directamente
a traveacutes de la explotacioacuten o indirectamente a traveacutes de la alteracioacuten del haacutebitat son
eliminadas o muy reducidas (Carr 2000) Las MPA son una herramienta utilizada a
nivel mundial para la gestioacuten de la pesca la conservacioacuten de especies y haacutebitats para
mantener el funcionamiento del ecosistema la capacidad de recuperacioacuten y la
preservacioacuten de la biodiversidad (Agardy 1997 Sobel y Dahlgren 2004) Existen datos
que indican que los beneficios de establecer una MPA se traducen en un aumento
promedio del 446 en biomasa del 166 en la densidad de especies del 21 en la
riqueza y del 28 en el tamantildeo de los organismos (Lester 2009) por lo que
ecoloacutegicamente las zonas marinas protegidas han demostrado ser eficaces en la
proteccioacuten o reduccioacuten de la degradacioacuten de los haacutebitats y ecosistemas y en el
aumento de los paraacutemetros poblacionales Las MPA ademaacutes de ser un reservorio de
biodiversidad favorecen el llamado ldquospilloverrdquo o efecto derrame (Halpern y Warner
2003) en el que las especies son capaces de moverse a otras aacutereas y colonizarlas Dado
todos los beneficios contrastados en el medio marino instaurar estas zonas de
proteccioacuten en las playas seriacutea una medida muy uacutetil y perfectamente aplicable
Centraacutendonos en la urbanizacioacuten costera uno de los principales problemas de
las estructuras artificiales es que aumentan la complejidad del haacutebitat y actuacutean como
auteacutenticas barreras ecoloacutegicas impidiendo la movilidad de las especies a lo largo de la
playa Asiacute es necesario que el disentildeo y la construccioacuten de las estructuras de ingenieriacutea
costera sean muy cuidadosos si se quieren alcanzar objetivos ecoloacutegicos En muchos
casos se propone el uso de un material maacutes permeable que permita la movilidad a
traveacutes de la estructura incluso se proponen medidas para que el disentildeo no genere
cambios tan sustanciales en la anchura y la pendiente de la misma puesto que las
especies intermareales migran con la marea y si la anchura de la playa es demasiado
Capiacutetulo 7
177
extensa y sobrepasa la capacidad de movimiento de la especie seraacute muy probable que
eacutesta acabe desapareciendo (Chapman y Underwood 2013) El caso de que estas
estructuras se utilicen para evitar el acuacutemulo de sedimento que impide el acceso a un
puerto pesquero como en el caso de nuestro estudio el objetivo ecoloacutegico entra en
conflicto directo con el econoacutemico y las posibilidades de llegar a un equilibrio se ven
considerablemente mermadas
Para conservar la biodiversidad y las caracteriacutesticas ecosisteacutemicas de las playas
la gestioacuten costera debe ir incorporando progresivamente todos los aspectos ecoloacutegicos
de estos sistemas que todaviacutea hoy son ignorados y no solo centrarse en mantener las
caracteriacutesticas fiacutesicas de las playas en condiciones para su uso por el ser humano con
actividades que tienen importantes costos ecoloacutegicos Ademaacutes es de especial
importancia que la sociedad tome conciencia de que la degradacioacuten de las playas no
solo supone la peacuterdida de un paisaje o de las especies que las habita sino tambieacuten de
los bienes y servicios que todos los elementos de ese ecosistema sus relaciones y su
funcionamiento suponen para el bienestar humano (Millennium Ecosystem
Assessment 2005)
Capiacutetulo 7
178
A Agardy T 1997 Marine Protected Areas and Ocean Conservation R E Landes Publ
Academic Press AustinTX Anfuso G Martiacutenez del Pozo JA Gracia FJ Loacutepez-Aguayo F 2003 Long-shore
distribution of morphodynamic beach states along an apparently homogeneous coast in SW Spain Journal of Coastal Conservation 9 49-56
B Barca-Bravo S Servia MJ Cobo F Gonzalez MA 2008 The effect of human use of sandy
beaches on developmental stability of Talitrus saltator (Montagu 1808) (Crustacea Amphipoda) A study on fluctuating asymmetry Marine Ecology 29 91-98
Bernardo-Madrid R Martiacutenez-Vaacutequez JM Vieacuteitez JM Junoy J 2013 Two year study of swash zone suprabenthos of two Galician beaches (NW Spain) Journal of Sea Research 83 152162
Bernatchez P Fraser C 2012 Evolution of Coastal Defence Structures and Consequences for Beach Width Trends Quebec Canada Journal of Coastal Research 28 1550-1566
Benavente J Del Riacuteo L Anfuso G Gracia FJ Reyes L 2002 Utility of morphodynamic characterisation in the prediction of beach damage by storms Journal of Coastal Research 36 56-64
Buitrago NR Anfuso G 2011 Morphological changes at Levante Beach (Caacutediz SW Spain) associated with storm events during the 2009-2010 winter seasons Journal of Coastal Research 64 1886-1890
C Carr MH 2000 Marine protected areas challenges and opportunities for understanding and
conserving coastal marine ecosystems Environmental Conservation 27 106ndash109 Chapman MG Underwood AJ 2011 Evaluation of ecological engineering of ldquoarmoredrdquo
shorelines to improve their value as habitat Journal of Experimental Marine Biology and Ecology 400 302-313
Christensen V Walters CJ Pauly D Forest R 2008 Ecopath with Ecosim amp User Guide November 2008 Edition Fisheries Centre Universitty of British Columbia Vancouver 235
D Defeo O McLachlan A Schoeman DS Schlacher TA Dugan J Jones A Lastra M
Scapini F 2009 Threats to sandy beach ecosystems a review Estuarine Coastal and Shelf Science 81 1-12
Defeo O McLachlan A 2013 Global patterns in sandy beach macrofauna Species richness abundance biomass and body size Geomorphology 199 106-114
De la Huz R Lastra M Junoy J Castellanos C Vieacuteitez JM 2005 Biological impacts of oil pollution and cleaning in the intertidal zone of exposed sandy beaches Preliminary study of the ldquoPrestigerdquo oil spill Estuarine Coastal and Shelf Science 65 19-29
Del Riacuteo L Gracia FJ Benavente J 2013 Morphological and evolutionary classification of sandy beaches in Cadiz coast (SW Spain) In Conley DC Masselink G Russell PE and OrsquoHare TJ (eds) Proceedings 12th International Coastal Symposium (Plymouth England) Journal of Coastal Research Special Issue 65 2113-2118
Bibliografiacutea
Capiacutetulo 7
179
H
Halpern BJ Warner RR 2003 Matching marine reserve design to reserve objectives Proceedings of the Royal Society of London B 2701871-1878
J Junoy J Castellanos C Vieacuteitez JM De la Huz MR Lastra M 2005 The macroinfauna of
the Galician sandy beaches (NW Spain) affected by the Prestige oil-spill Marine Pollution Bulletin 50 526-536
Jouny J Castellanos C Vieacuteitez JM Riera R 2013 Seven years of the macroinfauna monitoring at Ladeira beach (Corrubedo Bay NW Spain) after Prestige oil spill Oceanologia 55 393-407
L Lastra M De la Huz R Saacutenchez-Mata AG Rodil IF Aertes K Beloso S Loacutepez J 2006
Ecology of exposed sandy beaches in northern Spain Environmental factors controlling macrofauna communities
Lester SE Halpern BS Grorud-Colvert K Lubchenco J Ruttenberg BI Gaines SD Airameacute S Warner RR 2009 Biological effects within no-take marine reserves a global synthesis Marine Ecology Progess Series 384 33-46
M Martins R Quintito V Rodriacuteguez AM 2013 Diversity and spatial distribution patterns of
the soft-bottom macrofauna communities on the Portuguese continental shelf Journal of Sea Research 83 173-186
Mayoral MA Loacutepez-Serrano L Vieacuteitez JM 1994 MayoralMacrofauna bentoacutenica intermareal de 3 playas de la desembocadura del riacuteo Piedras (Huelva Espantildea) Boletiacuten Real Sociedad Espantildeola de Historia Natural 91 231- 240
Millennium Ecosystem Assessment 2005(httpwwwmillenniumassessmentorgenindexhtml)
McLachlan A Defeo O Jaramillo E Short AD 2013 Sandy beach conservation and recreation Guidelines for optimising management strategies for multi-purpose use Ocean amp Conservation 71 256-268
N Nordstrom KF 2013 Living with shore protection structures A review Estuarine Coastal
and Shelf Science 150 11-23
R Rodil IF Lastra M 2004 Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain Estuarine Coastal and Shelf Science 61 37-44
Rodil IF Lastra M Saacutenchez-Mata AG 2006 Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes North coast of Spain Estuarine Coastal and Shelf Science 67 267-279
Ruiz-Delgado MC Reyes-Martiacutenez MJ Saacutenchez-Moyano JE Loacutepez-Peacuterez J Garciacutea-Garciacutea FJ 2015 Distribution patterns of suppralittoral arthropods wrack deposits as a source of food and refuge on exposed sandy beacjes (SW Spain) Hydrobiologia 742 205-219
Capiacutetulo 7
180
S Schlacher TA Thompson LMC 2012 Beach recreation impacts benthic invertebrates on
ocean-exposed sandy shores Biological Conservation 147 123ndash132 Sobel J Dahlgren C 2004 Marine reserves a guide to science design and use Island Press
Washington DC V Veloso VG Silva ES Caetano CHS Cardoso RS 2006 Comparison between the
macroinfauna of urbanized and protected beaches in Rio de Janeiro State Brazil Biological Conservation 127 510-515
Veloso VG Neves G Lozano M Perez-Hurtado A Gago CG Hortas F Garciacutea-Garciacutea F 2008 Responses of talitrid amphipods to a gradient of recreational pressure caused by beach urbanization Marine Ecology 29 126-133
Veloso VG Sallorenzo IA Ferreira BCA Souza GN 2009 Atlantorchestoidea brasiliensis (Crustacea Amphipoda) as an indicator of disturbance caused by urbanization of a beach ecosystem Brazilian Journal of Oceanography 58 13-21
Capiacutetulo 8
Conclusiones generales
Capiacutetulo 8
182
Las playas del Golfo de Caacutediz se caracterizan por presentar una alta
biodiversidad de invertebrados donde se incluyen especies consideradas como
bioindicadoras y por un claro patroacuten de zonacioacuten de la comunidad
La distribucioacuten general de los invertebrados en las playas de estudio se
reuacutene en tres zonas bien diferenciadas La zona supralitoral habitada por anfiacutepodos de
la familia Talitridae y coleoacutepteros de la familia Curculionidae A continuacioacuten se
encuentra una zona mediolitoral caracterizada por isoacutepodos Cirolanidae anfiacutepodos
Haustoriidae poliquetos Spionidae y nemertinos Y por uacuteltimo se identifica una zona
sublitoral tipificada por misidaacuteceos poliquetos (Spionidae) y anfiacutepodos
(Pontoporeiidae)
Las principales variables abioacuteticas influyentes en el patroacuten de zonacioacuten son la
humedad del sedimento el contenido en materia orgaacutenica la pendiente de la playa y
el tamantildeo medio de grano Otros factores no considerados en este estudio tales
como el material varado y los insumos orgaacutenicos de riacuteos y estuarios podriacutean influir en
la abundancia y distribucioacuten de la macrofauna que habita las playas arenosas
Las actividades humanas tales como el pisoteo son importantes agentes
perturbadores de la macrofauna de playas Las principales consecuencias son la
disminucioacuten de la densidad y el cambio en la estructura taxonoacutemica de la comunidad
mientras que las caracteriacutesticas fiacutesicas de los intermareales no parecen verse afectadas
por el pisoteo humano
Algunas especies parecen ser poco tolerantes al pisoteo asiacute el anfiacutepodo
Bathyporeia pelagica resultoacute ser la especie mas sensible a esta perturbacioacuten
pudieacutendose considerar como un bioindicador de este tipo de impacto
1
2
3
4
5
Capiacutetulo 8
183
La urbanizacioacuten costera y la intensidad de usuarios en las playas no solo
tienen consecuencias a nivel poblacional y comunitario ya que el funcionamiento
ecosistemo tambieacuten se ve afectado
Ecopath con Ecosim es una herramienta uacutetil para dectar en playas arenosas
cambios en la estructura y el funcionamiento a nivel de ecosistema
Aunque de forma general las playas urbanizada y protegida estudiadas
presentan un funcionamiento troacutefico anaacutelogo dado el similar nuacutemero de
compartimentos un anaacutelisis maacutes exhaustivo de las caracteriacutesticas de las redes troacuteficas
mostroacute que la playa protegida es un sistema maacutes complejo organizado maduro y
activo que la playa urbanizada
Diferentes indicadores de perturbacioacuten fueron puestos a prueba para
determinar su potencial en el estudio de playas arenosas De esta forma las mayores
diferencias entre las playas fueron dadas por el iacutendice de Finn que puede ser
considerado como un indicador de presioacuten antropogeacutenica en intermareales arenosos
Otras actividades humanas como la construccioacuten de estructuras de defensa
(por ejemplo espigones) que tienen como principal objetivo contrarrestar el efecto de
la erosioacuten generan importantes modificaciones en el ecosistema playa
Los espigones modifican las caracteriacutesticas fiacutesicas sedimentoloacutegicas y
morfodinaacutemicas de las playas De esta forma las zonas maacutes cercanas al espigoacuten se
caracterizaron por una mayor anchura de la playa menor pendiente menor tamantildeo
de grano y una mayor tendencia al estado disipativo
Las comunidades de macrofauna controladas en gran medida por las
variables ambientales se adaptan los cambios generados por el espigoacuten En las zonas
maacutes cercanas a eacuteste resulta una mayor riqueza y densidad de especies Aunque esto
pueda verse como un efecto positivo no hay que olvidar que cualquier modificacioacuten
de las caracteriacutesticas naturales de una zona debe tratarse con cautela En relacioacuten con
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esto aunque algunos paraacutemetros problaciones fueron maacutes elevados en las zonas maacutes
cercanas al espigoacuten fue en el aacuterea maacutes alejada del agente perturbador la que presentoacute
un mayor iacutendice de biodiversidad
La presencia de carrontildea en la superficie del sustrato influye sobre la
actividad de Cyclope neritea que sale a la superficie Esta actividad es mayor en areas
donde hay pisoteo
Aunque existe una tendencia a salir a la superficie cuando hay carrontildea
disponible el acceso al alimento sin embargo estaacute limitado por la presencia de
congeacuteneres heridos
El mecanismo de defensa que supone la transmisioacuten de sentildeales olfativas
producida por congeacuteneres heridos de C neritea queda limitado a distancias de pocos
centiacutemetros por lo que este estiacutemulo no resutla tan eficaz contra los depredadores
como sucede con otras especies de gasteroacutepodos carrontildeeros
La gestioacuten costera debe crear nuevas herramientas asiacute como utilizar
aquellas propuestas por la comunidad cientiacutefica para incorporar los aspectos
ecoloacutegicos de las playas que todaviacutea hoy permanecen ignorados Asiacute mismo es
necesario que la sociedad tome conciencia de la importancia de los intermareales
como ecosistemas maacutes allaacute de la importancia de estos lugares como aacutereas de recreo
ya que conservar la biodiversidad y la funcionalidad de las playas debe ser una tarea de
todos
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