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Trace metal contents in wild edible mushrooms growing on serpentine andvolcanic soils on the island of Lesvos, Greece

M. Aloupi a,n, G. Koutrotsios a,1, M. Koulousaris a, N. Kalogeropoulos b

a Water and Air Analysis Laboratory, Department of Environment, University of the Aegean, GR-81100 Mytilene, Greeceb Laboratory of Chemistry, Biochemistry, Physical Chemistry of Foods, Department of Nutrition and Dietetics, Harokopio University, GR-17671 Athens, Greece

a r t i c l e i n f o

Article history:

Received 28 June 2011Received in revised form

7 November 2011

Accepted 16 November 2011Available online 14 December 2011

Keywords:

Trace metal

Wild edible mushroom

Serpentine soil

Volcanic soil

Greece

a b s t r a c t

The objectives of this survey were (1) to assess for the first time the Cd, Cu, Cr, Fe, Mn, Ni, Pb and Zn

contents in wild edible mushrooms (Russula delica, Lactarius sanguifluus, Lactarius semisanguifluus,Lactarius deliciosus, Suillus bellinii) from the island of Lesvos, (2) to investigate the metals’ variability

among the species, as well as in relation to the chemical composition of the underlying soil, comparing

mushrooms collected from volcanic and serpentine substrates and (3) to estimate metal intake by the

consumption of the mushrooms under consideration. The trace metals in 139 samples were determined

by flame or flameless atomic absorption spectroscopy. The median metal concentrations were as

follows: Cd: 0.14; Cr: 0.10; Cu: 8.51; Fe: 30.3; Mn: 5.26; Ni: 0.34; Pb: 0.093 and Zn: 64.50, all in

mg kg1 dry weight. The observed concentrations are among the lowest reported for mushrooms from

Europe or Turkey, while Pb and Cd values did not exceed the limits set by the European Union.

Significant species- and substrate-related differences in the metal contents were found, but the

variability did not follow a uniform pattern for all the metals in all mushroom species. As a general

trend, the mushrooms growing in serpentine sites contained higher Cd, Cr and Ni than those from

volcanic sites. The calculated bioconcentration factors (BCFs) showed that none of the mushrooms can

be regarded as a metal bioaccumulator, although BCF values slightly above unity were found for Zn in

the three Lactarius species, and for Cu in R. delica.

The studied mushrooms could supply considerable amounts of essential metals such as Zn and Cr.On the other hand, the consumption of R. delica collected from volcanic soils could provide 12% of the

Cd daily tolerable intake and as high as 53% when collected from serpentine soils. Nonetheless, our

results indicate that the regular consumption of wild edible mushrooms from Lesvos is quite safe for

human health.

& 2011 Elsevier Inc. All rights reserved.

1. Introduction

Mushrooms are valuable health foods, both for their texture

and flavor as well as for their low energy content, high proportion

of indigestible fiber, specific b-glucans and antioxidant constitu-

ents (Kalač , 2009). In addition they contain significant amounts of vitamins, minerals and trace elements like Fe, Zn, Se, K (Elmastas-

et al., 2007; Kalač , 2009). The chemical composition of mush-

rooms is the main cause for their therapeutic properties in

preventing diseases such as hypertension (Talpur et al., 2002),

hypercholesterolemia ( Jeong et al., 2010) and several types of

cancer (Lavi et al., 2006; Sullivan et al., 2006). Various wild edible

mushroom species exhibit significant antioxidant activity, and

therefore, can be used as an easily accessible source of natural

antioxidants, as a potential food supplement, or in the pharma-

ceutical industry (Elmastas- et al., 2007).

The consumption of wild growing mushrooms has been pre-

ferred over that of cultivated ones in many countries of centraland eastern Europe, and is considered to be increasing, even in

the developed world (Agrahar-Murugkar and Subbulakshmi,

2005). The collection of mushrooms in Greece, although more

restricted than in some other European countries such as Poland,

France or Italy, is part of the national tradition and they have been

an important ingredient in both traditional cuisine and gastro-

nomy (Keltemidis, 2005).

From an ecological point of view, mushrooms exert a major

influence on biogeochemical processes involving soil, rock and

mineral surfaces, and the plant root–soil interface, and play a key

role in the cycling of elements and the transformation of both

organic and inorganic substrates. These processes can affect plant

Contents lists available at SciVerse ScienceDirect

journal homepage: www .elsevier.com/locate/ecoenv

Ecotoxicology and Environmental Safety

0147-6513/$- see front matter & 2011 Elsevier Inc. All rights reserved.

doi:10.1016/j.ecoenv.2011.11.018

n Corresponding author.

E-mail address: [email protected] (M. Aloupi).1 Present address: Laboratory of General and Agricultural Microbiology,

Department of Agricultural Biotechnology, Agricultural University of Athens,

GR-11855 Athens, Greece.

Ecotoxicology and Environmental Safety 78 (2012) 184–194

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productivity and the mobility of toxic elements and substances,

with socioeconomic consequences even on human health (Gadd,

2007). Furthermore, ectomycorrhizal fungi may increase plant

tolerance to heavy metals, as for example in plants growing on Ni

and Cr rich serpentine soils (Aggangan et al., 1998).

Compared to green plants, mushrooms can accumulate large

amounts of some toxic heavy metals, such as Pb and Cd ( Sesli and

Tuzen, 1999; Demirbas-, 2001; Alonso et al., 2003; Falandysz et al.,

2007; Konuk et al., 2007; Chudzyjski and Falandysz, 2008;Brzostowski et al., 2011a, 2011b; Falandysz et al., 2011; Garcı́a

et al., 2009; Gucia et al., in press; Jarzyńska et al., 2011). A well

documented example is the high accumulative capacity of

Agaricus macrosporus and other Agaricus species for Cd, and of Coprinus comatus for Pb (Garcı́a et al., 1998 and references

therein; Melgar et al., 1998 and references therein). Many other

metals are essential for fungal growth and metabolism (e.g. Ca,

Cu, Fe, Mg, K, Na and Zn). Both essential and non-essential metals

can cause toxic effects to living organisms, including fungi, when

present above certain threshold concentrations (Gadd, 1993).

Metals exert toxic effects in many ways, e.g. by causing break-

down of cellular and organelle membranes, blocking operational

groups of significant biological molecules such as enzymes or

interacting with systems, which normally protect against harmful

effects of free radicals generated during normal metabolism

(Gadd, 2007). Nevertheless many fungi have developed a variety

of mechanisms, both active and incidental, which allow them to

survive, grow and flourish on substrates with high metal levels

(Branco, 2010). Serpentine soils are typically inhospitable for

many plants because of their soil chemistry, with high levels of

potentially phytotoxic elements like Ni, Cr, Co and sometimes Mn

and/or Cu (Chiarucci and Baker 2007; Branco, 2010; Kazakou

et al., 2010). These stressful environmental conditions result in

limited flora diversity along with high endemism and ecotypic

specialization (Branco, 2010 and references therein; Kazakou

et al., 2010). However, there is strong evidence that this general

trend is not followed by ectomycorrhizal fungi, which show no

specialization to edaphic chemical composition. On the contrary,

it appears that serpentine soils support higher fungal diversitythan non-serpentine ones (Branco, 2010).

On the island of Lesvos, Greece, about 60 species of mush-

rooms have been identified up to now in the herbarium of the

Agricultural University of Athens (Dimou and Polemis, personal

communication) but no studies on their heavy metal content have

been undertaken. In this study we assess the concentrations of Cd,

Cu, Cr, Fe, Mn, Ni, Pb and Zn in five mushroom species from the

island of Lesvos (Russula delica, Lactarius sanguifluus, Lactarius

semisanguifluus, Lactarius deliciosus, Suillus bellinii), all of which

are common and frequently consumed by the local population.

In addition, we examine the impact of species identity and of the

geochemical composition of the substrate on trace metal varia-

bility by comparing the metal concentrations of mushroomsoriginating from serpentine and non-serpentine soils. Finally,

we undertake an estimation of the dietary metal intakes by the

consumption of the wild mushrooms concerned.

2. Materials and methods

2.1. Sampling

Mushroom samples of five of the most common wild growing species, namely

Russula delica, Lactarius sanguifluus, Lactarius semisanguifluus, Lactarius deliciosus

and Suillus bellinii ( Table 1), were collected on the island of Lesvos, NE Aegean,

Greece, in November 2009. Each species was collected from two different sites:

R. delica, L. sanguifluus and S. bellinii were collected from one site on serpentine

soils and one on volcanic, while L. semisanguifluus and L. delicious were collected

from two sites, both located on volcanic soils (Fig. 1). Sampling from serpentinesoils was based on the geological map of Lesvos (Hecht, 1972–1975) and

confirmed by the presence of Alyssum lesbiacum, a serpentine endemic species

(Kramer et al., 1997). Metal concentrations in the serpentine and non-serpentine

soils were obtained from the survey of Kazakou et al. (2010). Ten to fifteen

individuals of each species were collected from each site, adding up to a total of

139 samples. Both types of sampling sites were in sparse pine forest and were

distant from human activities so that they could be considered as unpolluted.

Identification of each species was based on standard reference books (Phillips,

1981; Konstantinidis, 2009).

2.2. Analytical procedures

The fruiting bodies of the fungi were thoroughly cleaned with a soft tissue

from soil and substrate debris, chopped into pieces using plastic knifes and

weighed within 24 h after collection. This was followed by freeze-drying for 48 h

(to constant weight) and, finally, pulverization in an agate mortar. Freeze drying

was conducted in samples pre-frozen at 50 1C overnight, using a Labconco

FreeZone 4.5 laboratory apparatus. Operating conditions were set at 40 1C

collector temperature and at o5 mBar vacuum level. Water content was calcu-

lated on the basis of water loss during freeze-drying. The pulverized samples were

digested with conc. HNO3 in a Mars Xpress system (CEM), according to the

US EPA’s Method 3051A (2007). Metal determinations were performed in a

Table 1

Mushroom species collected with corresponding family, habitat and edibility according to the literature.

Species Family Habitat Edibility Reference

Lactarius delici osus Russulaceae Associated with Pinus, m os tly on neutr al and calcareou s s oils G ood Basso (1999)

Lactarius sanguifluus Russulaceae Associated with Pinus on calcareous soils Excellent Basso (1999)

Lactarius semisanguifluus Russulaceae Associated with Pinus, mostly at grazed sites on calcareous soil Excellent Basso (1999)

Russula delica Russulaceae Deciduous and coniferous woods, and forests on calcareous soils Good Galli (2003)

Suillus bellinii Suillaceae Coastal pine forests of Mediterranean Europe Moderate Galli (2000)

Fig. 1. Mushroom sampling sites on the island of Lesvos (Ru de¼R. delica; La de¼L. deliciosus; La sa¼L. sanguifluus; La se¼L. semisanguifluus; Su be¼S. bellinii).

M. Aloupi et al. / Ecotoxicology and Environmental Safety 78 (2012) 184–194 185


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Perkin-Elmer 5100ZL atomic absorption spectrometer with Zeeman background

correction. The graphite furnace technique was used for the determination of Cd,

Cr, Ni and Pb, while flame AAS was used for the determination of Cu, Fe and Zn.

All chemicals used in the determinations were of Suprapur grade supplied by

Merck, and the water used was from a Milli-Q water purification system

(18.2 MO cm). Sample handling in the laboratory was carried out in a Class 100

NUAIRE (NU 154-524E) laminar flow hood to avoid contamination.

2.3. Analytical quality control

The performance of the analytical method for the determination of metals was

assessed according to the guidelines of EURACHEM/CITAC (2000). Blank samples

were included in every digestion batch. In all cases, blank values were below the

limits of detection of the corresponding analytical techniques. The trueness of

metal determinations was assessed by the analysis of the BCR 278, Mussel Tissue

Reference Material, certified by the Community Bureau of Reference, which has

been used regularly for the laboratory’s internal quality control of the method. For

all metals the measured values were within the acceptance range of the certified

value (certified value72 sd). Since the certified reference material used did not

closely match the samples’ matrix, the trueness was additionally checked by

means of recovery tests in spiked samples, which resulted in recovery rates of 92–

103% in all cases. The precision of the analytical procedure was estimated with 14

duplicate tests (10% of the total sample size). The overall precisions, expressed as

reproducibility standard deviation, were 0.09, 0.19, 0.23, 0.08, 0.12, 0.18, 0.15 and

0.08 for Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn, respectively. Finally, the limits of

detection, calculated as three standard deviations of nine independent replicates

of a dilute sample and expressed in dry mushroom weight, were 0.02, 0.01, 0.13,1.41, 0.22, 0.02, 0.06 and 0.13 mg kg1 for Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn,

respectively.

2.4. Statistical analysis

All statistical tests were performed with SPSS 16.0. Concentrations below the

limit of detection were recorded only for Pb and they were replaced by the half of

this value (i.e. the limit of detection).

A two-way ANOVA was used to test the significance of the species and of the

type of substrate as well as their interaction on metal content and on BCFs for the

species collected from sites with different geochemical background. The signifi-

cant interactions were further examined for simple main effects, that is the effect

of each factor separately for each level of the other factor. All other differences

were tested by one-way ANOVA. The Levene’s test was used to examine the

homogeneity of variance of groups. Should a significant difference be assessed by

the ANOVA, post hoc multiple comparisons tests were run to further detect which

means are significantly different from each other. Gabriel and Games-Howell tests

were used in the cases of equal or unequal variances, respectively.

A cluster analysis was performed to investigate the relationships among the

species with regard to metal concentrations. ‘Between groups linkage’ was used as

the clustering method and squared Euclidean distance as the measure of distance.

Before the analysis the data were standardized to their z scores in order to

eliminate scale effects.

3. Results and discussion

The descriptive statistics for water and heavy metal content of

the wild-growing edible mushrooms from Lesvos are shown in

Table 2.

3.1. Water content

The water content of the studied mushrooms was on average

90.6%, ranging between 80.0% and 96.8% (Table 2). These values

were similar to the 85–95% water content range mentioned in the

recent reports on the composition and nutritional value of wild

mushrooms from Europe (Kalač , 2009), Northern Greece (Ouzouni

and Riganakos, 2007; Ouzouni et al., 2009) and Turkey (C- ayır

et al., 2010). They also confirmed the mean water content of 90%,

which is often used for fresh–dry weight conversions (Kalač ,2009).

3.2. Metal concentrations and bioconcentration factors

All metal concentrations are expressed on a dry weight basis,

unless otherwise specified. The overall concentrations in the

mushroom samples are shown in Table 2. The ranges of concen-

trations spread over one to two orders of magnitude, not only

among the various species but even within the same species, as

for Fe and Pb in S. bellinii, with both the overall minimum and

maximum concentrations occurring in this species. This finding is

in accordance with the literature, since a two-fold variability of

trace metals’ levels in mushrooms is often encountered (Michelot

et al., 1998; Gadd, 2007; Nováč ková et al., 2007). Furthermore,

Table 2

Water content (%) and metal concentrations (mg kg1 dw) in wild growing edible mushrooms from Lesvos.

Species Water content Cd Cr Cu Fe Mn Ni Pb Zn

Russula delica Mean 89.7 0.64 0.57 25.0 24.6 5.4 2.43 0.078 39.9

Sd 2.7 0.58 0.81 4.7 10.6 2.5 2.85 0.049 9.0

Median 90.4 0.51 0.077 24.7 20.7 4.8 0.23 0.073 39.6

Range 8 0.8– 93 .5 0 .07 –2 .1 2 0 .0 2– 2.84 1 9.1– 34 .4 1 4.9– 62 .7 2 .4 –1 4.7 0.05 –1 0.21 0.02 9– 0.20 9 2 3.6– 60 .8

N 29 29 29 29 29 29 29 29 29

Suillus bellinii Mean 94.9 0.06 0.32 9.7 37.7 10.5 2.87 0.191 52.5

Sd 0.9 0.04 0.56 5.2 28.1 6.0 3.62 0.130 15.4

Median 94.9 0.05 0.15 9.2 32.8 10.2 0.49 0.190 57.8

Range 9 3.2– 96 .8 0 .02 –0 .1 8 0 .0 4– 2.74 3 .5 –2 4.1 1 1.7– 13 5.8 2 .8 –2 5.3 0.06 –1 1.12 0.02 7– 0.51 9 2 6.3– 78 .8

N 28 28 28 28 28 28 28 27 28

Lactarius semisanguifluus Mean 89.6 0.16 2.03 9.3 47.9 5.1 2.88 0.097 70.4

Sd 2.9 0.10 1.21 3.7 20.8 1.5 1.79 0.052 22.0

Median 90.6 0.15 2.11 8.2 42.9 4.9 2.73 0.107 64.0

Range 8 0.0– 93 .2 0 .06 –0 .6 1 0 .0 3– 4.23 4 .6 –2 4.0 1 6.9– 99 .3 1 .9 –7 .8 0.07 –6 .6 7 0.03 1– 0.18 7 3 9.0– 13 6.4

N 30 30 30 30 30 30 30 30 30

Lactarius deliciosus Mean 88.9 0.15 0.04 6.9 29.8 5.7 0.24 0.126 81.1

Sd 1.8 0.06 0.01 1.4 7.6 1.3 0.05 0.043 15.4

Median 89.1 0.14 0.04 7.0 27.8 5.7 0.22 0.129 78.5

Range 8 5.3– 91 .8 0 .06 –0 .2 5 0 .0 1– 0.07 3 .9 –1 0.6 2 0.3– 52 .9 3 .3 –7 .9 0.11 –0 .3 4 0.03 0– 0.18 2 6 2.8– 12 0.8

N 24 23 23 23 24 24 23 23 24

Lactarius sanguifluus Mean 89.9 0.21 0.28 7.0 34.6 4.7 0.59 0.076 103.2

Sd 2.6 0.12 0.40 2.5 9.3 1.2 0.53 0.034 23.4

Median 90.5 0.16 0.07 6.2 32.4 4.3 0.33 0.077 105.0

Rang e 84.5 –94.4 0.08 –0.59 0.02–1 .81 4.0–1 5.4 2 1.6–5 1.1 3.0–7 .8 0.1 6–2 .46 0.031 –0.162 57 .4–17 9.0

N 28 25 28 28 28 28 28 28 28

M. Aloupi et al. / Ecotoxicology and Environmental Safety 78 (2012) 184–194186


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the variability in metal concentrations has been found consis-

tently higher in mushrooms than in plants (Kalač , 2010).

In comparison to mushrooms collected from unpolluted sites

in other European countries and Asia Minor, the mushrooms from

Lesvos contain relatively low levels for all the metals studied.

The only likely exception to this is the Cr content in L. semisangui-

fluus, which is consistently higher in mushrooms from both

sampling sites (n¼30 individuals) than in other Lactarius species

in the present or in previous surveys. Fig. 2 depicts the concen-trations found in the current survey along with values reported in

the literature for the same species and/or other species of the

same genus (Michelot et al., 1998; Sesli and Tuzen, 1999, 2006;

Demirbas-, 2001; Is-iloğlu et al., 2001; Carvalho et al., 2005; Cocchi

et al., 2006; Sesli, 2006; Sesli and Dalman, 2006; Sesli and Tuzen,

2006; Konuk et al., 2007; Ouzouni and Riganakos, 2007; Ouzouni

et al., 2007, 2009; Tuzen et al., 2007; Colak et al., 2009; Ouzouni

et al., 2009; Campos and Tejera, 2011; C- ayır et al., 2010).

The usual metal contents of European mushrooms, as reviewed

by Kalač (2010), are also shown.

Furthermore, the Cd and Pb contents in the mushrooms from

Lesvos did not exceed the statutory limits of 0.2 and 0.3 mg kg 1

fresh weight, respectively, for edible mushrooms (corresponding

to 2.0 and 3.0 mg kg1 dry weight, assuming a mean water

content of 90%), established by the EU (Commission Regulation

No 1881/2006, 2006). The only marginal exceptions were two

samples of R. delica, which had Cd concentrations just above the

limit (2.1 mg kg1).

According to the literature, a number of factors affect metalcontent in the fruiting bodies of mushrooms, thus accounting for

the observed scatter of concentrations. These factors include

species-dependence, substrate composition, the age of the myce-

lium and the interval between fructification events, metal pollu-

tion at the sampling site and biochemical and chemical

parameters of the substrate, such as pH or carrier molecules

(Gast et al., 1988; Lepˇ sová and Mejstˇ rı́k, 1988; Gadd, 1993;

Michelot et al., 1998; Kalač and Svoboda, 2000; Nikkarinen and

Mertanen, 2004; Kalač , 2010). On the contrary, the age and size

of the fruiting body, and atmospheric deposition are considered

0.001

0.010

0.100

1.000

10.000

100.000

1000.000

10000.000

R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .

V a r i o u s s p p .

R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


C ( m g / K g D W )

CuCr Cd Fe

0.001

0.010

0.100

1.000

10.000

100.000

1000.000

10000.000

R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


R u d e

R u s p p .

L a d e

L a s a

L a s e

L a s p p .

S u b e

S u s p p .


C ( m

g / K g D W )

NiMn Pb Zn

Fig. 2. Comparison of metal levels in mushrooms from the island of Lesvos () with mushrooms from Europe and Asia Minor (—). White bars represent usual metal

concentrations in various European species from unpolluted areas reported by Kalač (2010). Wherever data were reported in fresh weight, a mean water content of 90%

was considered to convert the values to dry weight. Abbreviations are as follows: Ru de¼R. delica; Ru spp.¼other Russula. species; La de¼L. deliciosus; La sa¼L. sanguifluus;

La se¼L. semisanguifluus; La spp¼other Lactarius species; Su be¼S. bellinii; Su spp.¼other Suillus species; various spp.¼various species.



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of lesser importance (Kalač and Svoboda, 2000; Kalač , 2010).

Moreover, most of the metals are distributed unevenly within a

fruiting body, with the highest contents usually found in the cap,

particularly in the hymenophore, lower in the spores and in the

rest of cap and even lower in the stipe (Garcı́a et al., 1998; Melgar

et al., 1998; Alonso et al., 2003; Falandysz et al., 2007; Chudzyjski

and Falandysz, 2008; Kalač , 2010; Brzostowski et al., 2011a,

2011b; Falandysz et al., 2011; Gucia et al., in press; Jarzyńska

et al., 2011).The effect of two main factors, species and type of substrate,

on metal concentrations was examined in the present survey.

Since we were able to collect only three of the five species from

the two different types of substrate (serpentine and volcanic-

derived soils) that dominate the geology of the western and

central part of the island of Lesvos, the data set was subjected

to two separate analyses: a two-way ANOVA to test the signifi-

cance of both species and type of substrate as well as their

interaction in R. delica, L. sanguifluus and S. bellinii and a one-way

ANOVA to test the dependence of metal concentrations on the

species, for all five species collected in volcanic soils.

Furthermore, in order to evaluate the ability of the studied

mushrooms to accumulate or exclude metals from their substrate,

the bioconcentration factor (BCF) was calculated for each metal

(Table 3) as the ratio between the metal concentration in the

whole fruiting body and its total concentration in the underlying

soil. Metal concentrations in soils in the vicinity of the mushroom

sampling sites were obtained by Kazakou et al. (2010). BCFs are

often calculated on the basis of ‘‘bioavailable’’ or ‘‘labile’’, that is

weak acid extractable, metal concentrations (Chudzyjski and

Falandysz, 2008; Brzostowski et al., 2011a; Gucia et al., in press;

Jarzyńska et al., 2011), whereas in other cases total metal

contents in soils, like in this survey, are used (Alonso et al.,

2003; Komárek et al., 2007; Frankowska et al., 2010; Falandysz

et al., 2011). Since the bioavailable fraction of various metals in

soils is a rather small fraction of their total concentrations

(Nikkarinen and Mertanen, 2004; Chudzyjski and Falandysz,

2008) the BCFs calculated by these two methods may obviously

be quite different, as shown by Komárek et al. (2007).If BCF values exceed unity the species is regarded as a

bioaccumulator of the metal and, vice versa, if BCFo1 the species

is characterized as a bioexclusor. In this context, the very low

BCFs found for all the analyzed metals in all the mushrooms

under consideration suggest that none of the species clearly act as

a metal bioaccumulator, with the marginal exception of the three

Lactarius species with regard to Zn and of R. delica with regard to

Cu, for which BCFs slightly above unity were found.

3.3. Effect of the type of substrate

The F test and its statistical significance ( p) for the factorsSpecies and Substrate and for their interaction, as calculated by

the two-way ANOVA, are shown in Table 4 and the mean

concentrations of metals for each species and type of substrate

are presented in Fig. 3.

The effect of the two factors on concentrations was not uniform

for all the metals under consideration. Significantly higher levels of

Cd, Cr and Ni were found in the mushrooms from serpentine soils

(main effect of type of substrate significant at po0.001) but the

accumulation of these metals varied by species, since the interaction

term was statistically significant. Species was not a significant factor

for Cr, in contrast to Cd and Ni, since it explained only 5.6% of the

total variance of the metal content (partial eta-squared¼0.056),

while the corresponding values for Cd and Ni were 53.4% and 29.9%,

respectively. This was due to the more uniform distribution of the Crcontent among the three species within each type of substrate, in

comparison with Cd and Ni. More specifically, the simple main effect

analysis showed that R. delica contained more Cd and Cr when

collected from the serpentine soils, followed by L. sanguifluus, while

S. bellinii had similar Cd and Cr content in both substrates. As for Ni,

S. bellinii and R. delica had much higher contents than L. sanguifluus

in the serpentine substrate. In contrast to the previous metals, Mn

was similar or higher in mushrooms from volcanic soils, the

concentrations being higher in S. bellinii, while no difference in

relation to the type of substrate was detected in L. sanguifluus.

The type of substrate was not significant as a main factor for Cu and

Zn but there was a strong interaction between species and substrate,

with R. delica and S. bellinii having a higher content of both metals in

the serpentine than in the volcanic sites and with the opposite trend

in L. sanguifluus. Finally, Fe and Pb concentrations were not affected

by the type of substrate whatsoever, as manifested by the lack of

significance of both the substrate and the interaction of spe-

cies substrate terms. A strong dependence of the concentrations

Table 3

BCFs (mean values) of metals in mushrooms from serpentine and volcanic soils of Lesvos. Asterisks indicate statistically different BCFs in volcanic and serpentine

substrates at a¼0.05.

Species Type of substrate Cr Cu Fe Mn Ni Pb Zn

L. sanguifluus Volcanic 0.0006 0.23 0.0007n 0.006 0.004n 0.003 1.63n

Serpentine 0.0003 0.25 0.0005 0.004 0.001 0.002 1.11

R. delica Volcanic 0.0004 1.07 0.0005n 0.009n 0.002 0.003 0.70n

Serpentine 0.0006 1.01 0.0003 0.003 0.003 0.004 0.46

S. bellinii Volcanic 0.0013n 0.44 0.0008n 0.02n 0.002 0.009 0.99n

Serpentine 0.0002 0.36 0.0004 0.004 0.003 0.006 0.55

L. semisanguifluus Volcanic 0.0276 0.37 0.0011 0.007 0.038 0.003 1.01

L. deliciosus Volcanic 0.0004 0.27 0.0007 0.008 0.003 0.005 1.26

Table 4

F test (degrees of freedom in parentheses) of the two-way ANOVA and its statistical significance ( p) for species, substrate and their interaction in R. delica, L. sanguifluus and

S. bellinii from serpentine and volcanic substrates of Lesvos.

Cd Cr Cu Fe Mn Ni Pb Zn

Species F (2, 79) 43.54 2.33 155.89 4.49 34.65 16.89 17.37 122.98

p o0.001 0.104 o0.001 0.014 o0.001 o0.001 o0.001 o0.001

Substrate F (1, 79) 36.39 35.50 0.60 0.58 44.93 120.74 2.59 2.26

p o0.001 o0.001 0.443 0.450 o0.001 o0.001 0.111 0.137

Species substrate F (2, 79) 23.30 4.87 5.86 1.33 21.72 18.96 2.49 4.66

p o0.001 0.010 0.004 0.270 o0.001 o0.001 0.090 0.012



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Fig. 3. Mean metal concentrations (in mg kg1) in L. sanguifluus (La sa), R. delica (Ru de) and S. bellinii (Su be) from serpentine (s) and volcanic (ns) soils of Lesvos (the error

bars show the 95% confidence interval of the mean).



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of all metals on species was revealed by the two-way ANOVA

( po0.001 for all metals). This is discussed below, along with the rest

of the species.

The substrate on which mushrooms grow seems to be the

main source of fungal trace element uptake (Lepˇ sová and

Mejstˇ rı́k, 1988; Gadd, 1993; Gadd, 2007) and the natural geology

and geochemistry of the substrate seems to have a strong impact

on trace element concentrations in mushrooms (Nikkarinen and

Mertanen, 2004). The complex geological composition of theisland of Lesvos results in significant differences in the chemical

composition of the derived soil, hence leading to differences in

the metal content of mushrooms. According to Kazakou et al.

(2010), the serpentine soils of Lesvos contain much higher Cr

(1118–4863 mg kg1) and Ni (1197–3326 mg kg1) than the

non-serpentine soils (81.9 mg kg1 and 84.4 mg kg1, respec-

tively). These pronounced differences are not proportionately

reflected in metal concentrations in the species collected from

both substrates, as already mentioned, as well as in their BCFs.

The statistical analysis (two-way ANOVA) revealed higher BCFs

for Ni in L. sanguifluus and for Cr in S. bellinii from volcanic than

from serpentine soils, while R. delica had equal BCFs for both

metals in both types of substrate. A reverse relationship between

metal content in soils and BCFs was found in many cases in the

past and was attributed to the restriction in the efficiency of

metal accumulation caused by toxic effects of metals at high

concentrations (Alonso et al., 2003 and references therein).

It appears, thus, that a proportional increase in Cr and Ni soil

levels is not a consistent trend for all mushroom species growing

on serpentine soils.

It is possible that the Cd enrichment in R. delica and

L. sanguifluus from the serpentine sites could also be attributed to

higher metal content in serpentine soils, but no sound conclusion

can be drawn since data for Cd distribution in Lesvos soils were not

provided by Kazakou et al. (2010). Nonetheless high concentrations

of Cd are a general characteristic of the chemistry of serpentine

soils (Shallari et al., 1998; Cornara et al., 2007; Oze et al., 2008 and

references therein), while concentrations of 1–2 orders of magni-

tude lower were found in soils developed over igneous rocks(Nikkarinen and Mertanen, 2004; Doelsch et al., 2006; Sultan

et al., 2011). On the other hand, although quite low Cd content

were found in 12 species of wild edible mushrooms from granitic

soils in NW Spain, Cd levels in Agaricus macrosporus from the same

area were noticeably high (Melgar et al., 1998), underlining that

species-specific metabolic or ecological features often interfere

with the geochemical features of the substrate in determining

the metal levels in mushrooms. Moreover, this assumption is

supported by the statistical significance of the interaction between

species and substrate found in this work.

As mentioned above, Mn content of S. bellinii and R. delica was

significantly higher in mushrooms from volcanic soils. This differ-

ence is the opposite of the relationship in the soils themselves

(Kazakou et al., 2010) although the dissimilarity between the twosubstrates was not as pronounced as for Cr and Ni. Both these

relationship can explain the higher BCFs for Mn calculated in

volcanic than in serpentine soils. Our results show that the type

of substrate did not consistently affect Cu and Zn levels in mush-

rooms, since no uniform trend was observed in the three species

investigated. The same was also true for BCFs for Cu, although

higher BCFs were found for Zn in the volcanic than in serpentine

substrate, which could be attributed to the lower Zn content of the

latter type of soils (Kazakou et al., 2010). This finding is further

corroborated by the conclusion of Gast et al. (1988) that Zn and, to

a lesser degree, Cu concentrations in 21 mushroom species from

the Netherlands and Belgium were independent of soil concentra-

tions but significantly dependent on inter-specific differences

arising from the essential biochemical role of both metals to livingorganisms. Finally, each of the three mushroom species had similar

Fe and Pb contents in both volcanic and serpentine soils and the

variance in their concentrations is explained only by species-

specific differences, which are consistent in both types of soil,

although serpentine soils in Lesvos contain twice as much Fe and

approximately equal levels of Pb compared to the non-serpentine

ones (Kazakou et al., 2010). These relative Fe and Pb abundances in

mushrooms and soils explain the statistical evidence of higher

BCFs for Fe in volcanic than in serpentine soils and equal BCFs for

Pb in both types of soils.

From the above discussion it appears that the role of the type

of substrate in determining trace metal concentrations in mush-

rooms is not straightforward but its manifestation varies with the

species as well as with the metal. Furthermore, significant

geochemical differences are more clearly reflected in mushroom

content in trace metals, as in the case of Cr and Ni, while

differences of a smaller extent may be overwhelmed by a number

of other factors affecting metal uptake by mushrooms.

3.4. Effect of the species identity

Since the geochemical composition of the substrate has been

found to play a role in regulating the metal content of the

mushrooms studied here, the potential preferences of the various

species towards accumulation of specific metals was investigated

in mushrooms collected from the same type of substrate, i.e. soils

derived from volcanic rocks. The variability of metal concentra-

tions among the species was tested by one-way ANOVA and the

results are summarized in Table 5 and shown in Fig. 4.

For all metals, significant differences of means were found

among the species at the o0.001 level. The post hoc multiple

comparisons tests revealed some well-defined trends in the

preference of some species to accumulate or exclude metals.R. delica had significantly higher Cu than all the other species,

S. bellinii preferentially accumulated Mn and Pb, whereas the

highest levels of Cr, Ni and Fe were found in L. semisanguifluus, the

latter metal being equivalently abundant in S. bellinii, as well. Zn

was found in significantly higher levels in L. sanguifluus. On the

other hand, significantly lower concentrations of Zn were found in

R. delica, of Cd in S. bellinii and of Cu in L. sanguifluus. Apart from

these pronounced differences the distribution of the metals

among the species did not exhibit a clear pattern as subgroups

of species with non-significantly different means often over-lapped. The one-way ANOVA of the calculated BCFs (for all metals

but Cd) leads to very similar conclusions.

In accordance to our results, a preferential accumulation of Cu

but also Cd, Pb and Zn was reported in R. delica over L. deliciosus

from the C- anakkale Province of Turkey (C- ayır et al., 2010) but the

Table 5

F test (degrees of freedom in parentheses) of the one-way ANOVA and its statistical significance ( p) of metal concentrations in mushroom species from volcanic soils of

Lesvos.

Cd Cr Cu Fe Mn Ni Pb Zn

Species F (4, 92) 8.69 93.30 151.65 12.05 49.25 61.69 25.81 54.36

p o0.001 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001 o0.001



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differences between concentrations among various species were

not statistically tested. Since Cu was an order of magnitude higher

in R. delica than in L. deliciosus the deduction could be considered

as reliable, but this may not be the case for the other metals.

Furthermore, Ouzouni et al. (2009) reported high Cu but low Cd

concentrations in R. delica from West Macedonia and Epirus,

Fig. 4. Mean metal concentrations (in mg kg1) in R. delica (Ru de), L. deliciosus (La de), L. sanguifluus (La sa), L. semisanguifluus (La se) and S. bellinii (Su be) from volcanic

soils of Lesvos (the error bars show the 95% confidence interval of the mean and the dot-lines the homogeneous subgroups found by the post hoc Games-Howell test).



9/11

Greece. On the other hand, a minimum Cu level of 4.2 mg kg 1

was reported by Campos and Tejera (2011) for L. sanguifluus in a

survey including 15 species collected from quartzite acidic soils in

Spain, the species with the next lowest Cu content being

L. deliciosus (5.4 mg kg1). These results were very close to ours,

as far as both the values per se and the ranking of species are

concerned. Another study on metal concentrations in 6 species of

wild edible mushrooms from a traffic-polluted area in Balıkesir,

Turkey, found the lowest Cd and Cu levels in L. semisanguifluus,and slightly higher metal content in L. sanguifluus (Is-iloğlu et al.,

2001). The lowest Cu content was also found in L. deliciosus by

Carvalho et al. (2005) in a study on 6 species from Portugal and

the second lowest among 28 species by Alonso et al. (2003) in

northwest Spain.

Summarizing the above information, it appears that the three

Lactarius species under consideration do not tend to accumulate

high amounts of Cu, in contrast to R. delica, which seems to take

up Cu from its substrate more effectively. The tendency of these

species towards Cd accumulation remains ambiguous. Since the

aforementioned surveys were held in both contaminated and

non-contaminated areas, the impact of anthropogenic origin

might be a potential explanation for this discrepancy, the natural

scarcity of the metal taken into consideration.

The intra-specific variation in the selective uptake of Cr and Ni by

L. semisanguifluus was noticeable, manifesting itself as a 1–2 orders

of magnitude magnification of concentrations in comparison to the

remaining four species (to a much lesser extent this was also found

for Fe). The enrichment of all the three metals in L. semisanguifluus in

relation to the other Lactarius species was still valid when statisti-

cally tested in a subset of data comprising only the three Lactarius

species collected from exactly the same site, thus eliminating the

potential influence of other environmental factors on metal levels

(F (2, 38)¼300.9, po0.001 for Cr; F (2, 38)¼151.9, po0.001 for Ni;

F (2, 38)¼31.7, po0.001 for Fe). Moreover, the levels of Cr and Ni in

L. semisanguifluus of non-serpentine provenance are twice as high

for Cr and similar for Ni compared to those in mushrooms from the

serpentine sampling sites. A high bioaccumulation capacity of

L. deliciosus for Zn was reported by Alonso et al. (2003), in a surveycomprising another 27 species of various nutritional modes from

northwest Spain. Relatively high Zn was also found for L. deliciosus in

our survey, but a consistent conclusion of the tendency of the

species regarding Zn uptake cannot be drawn since the two surveys

do not include any other species in common. Additionally, the

survey by Alonso et al. (2003) was carried out in both contaminated

and non-contaminated areas.

The highest Mn and Pb concentrations have been found in

S. bellinii. A tendency of some Suillus species to accumulate Mn

has previously been recorded (Michelot et al., 1998), but an

assessment of the affinity of S. bellinii for Mn or Pb could not be

made since, to our knowledge, no data of the metal content of this

species have been published yet.

The grouping of the species under consideration in relation to all

the studied metals was examined by cluster analysis (Fig. 5). The

only similarity was found between L. deliciosus and L. sanguifluus, all

other species forming single-species groups. It is worth noticing that

species not only in the same family but even of the same genus have

apparently developed diversified processes to interact with themetal burden in their growing environment. A close relationship

between L. deliciosus and L. sanguifluus was also reported by Campos

and Tejera (2011) in a cluster analysis based upon the concentra-

tions of Al, Zn, Cu and Rb, i.e. the metals with the higher absorption

rate from the substrate, performed on 15 species from Spain.

The authors attributed this relation to similarities regarding the

nutritional behavior of the two Lactarius species, being both ecto-

mycorrhizae of the genus Pinus as opposed to species exerting other

nutritional strategies such as saprobes on soil organic matter.

Although in the present survey all the studied species share the

same nutritional mode (ectomycorrhizae) it appears that the inter-

connection between L. deliciosus and L. sanguifluus still holds. Both

species had intermediate to low levels of all the examined metals.

On the other hand the interaction of L. semisanguifluus with metals

seems to be markedly different from the other two Lactarius species

and this is probably due to its great affinity for Cr, Fe and Ni. S.

bellinii and R. delica are located between the previously discussed

groups in the dendrogram, the first one characterized by high Mn

and Pb and low Cd content and the latter by high Cu and Cd and low

Cr, Fe, Ni, Pb and Zn concentrations.

3.5. Dietary intake

In order to calculate the potential trace element intake through

the consumption of wild edible mushrooms from Lesvos, we con-

sidered 60 kg as the weight of an average consumer, in agreement

with the EU Scientific Committee for Food Adult Weight parameter

(Ouzouni et al., 2007) and assumed a serving of mushrooms equal to

300 g of fresh weight, which contains 30 g of dry matter (Kalač andSvoboda, 2000; Svoboda et al., 2000). The intake calculations were

made on the basis of the average metal content in mushrooms,

regardless of the type of substrate, since collection for human

consumption takes place at random, in both serpentine and volcanic

localities. The results of intake and the respective percent coverage of

recommended daily intakes (RDI) or tolerable daily intakes (TDI) are

shown in Table 6.

The great variability in metal contents of mushrooms resulted

in an accordingly great variability in metal dietary intake.

The highest intakes of the toxic metals Pb and Cd were provided

by S. bellinii and R. delica, respectively. The potential intake of Cd

through the consumption of a serving of R. delica was 32% of the

recommended by the World Health Organization value for daily

intake of the metal, reaching 53% when collected from serpentinesoils (not shown in Table 6). Nonetheless, the intake of both toxic

metals through the consumption of wild mushrooms from

Lesvos is well below their tolerable values. R. delica and

S. bellinii were the most important suppliers of Cu and Mn,

respectively. L. semisanguifluus is expected to supply the higher

amounts of Cr, reaching 30.5% of the RDI, followed by R. delica. Ni

content in one serving of R. delica, S. bellinii and L. semisanguifluus

represented 10–12% of the TDI, while the Ni intake by the

consumption of R. delica and S. bellinii from the serpentine

substrate could reach 22.2% and 26.3% of the TDI, respectively

(data not shown in Table 6). Finally, the consumption of one

serving of wild mushrooms from Lesvos could cover 8–12% and

9–23% of the RDI values for Fe and Zn, contributing to the human

nutritional requirements for these essential metals.

Fig. 5. Dendrogram of the cluster analysis on the mushroom species from volcanic

soils of Lesvos, in relation to their metal contents.



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4. Conclusions

This first survey of metal contents in 5 wild edible mushrooms

from Lesvos showed low levels of the studied metals in comparison

to mushrooms from Europe or Asia Minor, probably due to the

absence of seriously polluting human activities on the island.

Furthermore, the dietary metal intake through consumption of

wild mushrooms from the island does not seem to pose any threat

to human health.

Both the substrate geochemistry and the species identity were

found to affect mushroom metal contents, although not in a

uniform way. In general, mushrooms growing on serpentine soils

had considerably higher Cr and Ni contents compared to those

from volcanic areas. However it was found that R. delica took upboth metals proportionally from the soil, S. bellinii took up only Ni,

while L. sanguifluus seemed to control metal concentrations, being

less affected by the metal levels in the soil. The elevated Cd

concentrations recorded in the mushrooms from the serpentine

sites could also be attributed to enhanced levels of the metal in

the soils, as literature data indicate, but further investigation is

needed to confirm this assumption. The calculation of the BCFs

showed that all the species under consideration acted as bioex-

clusors of all the metals studied, with the exception of the three

Lactarius species and of R. delica, which could marginally be

regarded as bioconcentrators of Zn and Cu, respectively.

Mushroom selectivity towards metal uptake was examined by

considering only those specimens growing on soils of volcanic

origin, so as to eliminate the effect of the substrate composition.The statistical analysis revealed a species-specific interaction of

the studied mushrooms with the various metals, still valid in

species of the same genus. Specifically, R. delica showed a stronger

affinity for Cu, S. bellinii for Mn and Pb, L. semisanguifluus for Cr, Ni

and Fe and L. sanguifluus for Zn.

Despite the large number of publications on the subject, the

complex interactions between mushroom species and metals in

the environment still remain obscure and their study is still

challenging. This is probably due to the fact that the metal

concentrations in mushrooms are influenced by both biotic and

abiotic variables. This survey has shown that for a better under-

standing of the processes involved in metal uptake by mush-

rooms, the metal variability in the substrate should be taken into

consideration, either these metals originate from natural or from

pollution sources. In this view, the most illustrative way to

determine the metal uptake by mushrooms from their substrate

is to determine the metal concentrations in the underlying soil

and to calculate their BCFs.

Acknowledgments

This work was supported by the Research Unit of the Uni-

versity of the Aegean. The authors would like to thank Elisabeth

Zagle, for her participation in the analyses, Dimitris Dimou and

Dr. Elias Polemis for providing information on mushroom biodi-

versity on Lesvos, and Dr. Triantaphyllos Akriotis for his com-ments on the manuscript.

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Estimation of trace element intake (mg) and percent coverage of recommended or tolerable upper level of metal intake (in parentheses), through consumption of one

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Mushroom species Cd Cr Cu Fe Mn Ni Pb Zn

Russula delica 0.019070 .01 7 0 .0 1770 .0 24 0 .7 5070.140 0.7470.32 0.1 6270 .07 4 0 .0 7370 .08 5 0 .0 0270.001 1 .2070.27

(31.8) (8.5) (2.5) (5.9) (5.4) (10.1) (1.1) (8.9)

Suillus bellinii 0.001870 .00 1 0 .0 1070 .01 7 0 .2 9270.1 54 1.1370.84 0.3 1570 .1 81 0 .0 8670 .1 09 0 .0 0670.004 1 .5870.46

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Lactarius sanguifluus 0.006370 .00 4 0 .0 0870 .01 2 0 .2 0970.074 1.0470.28 0.1 4170 .03 7 0 .0 1870 .01 6 0 .0 0270.001 3 .1070.70

(10.5) (4.0) (0.7) (8.3) (4.7) (2.5) (1.1) (22.9)

Lactarius semisanguifluus 0.004870 .00 3 0 .0 6170 .0 36 0 .2 7870.1 11 1.4470.63 0.1 5370 .04 4 0 .0 8670 .05 4 0 .0 0370.001 2 .1170.66

(8.1) (30.5) (0.9) (11.5) (5.1) (11.9) (1.4) (15.6)

Recommended or tolerable

daily intake (mg/day)

0.060b 0.20 30b 10-15 3.0 0.72 0.214b 12-15

Reference TDIc RDId TDIe RDIf RDIf TDIc TDIc RDIf

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