Food and Chemical Toxicology 58 (2013) 249–254

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Food and Chemical Toxicology

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Bioconcentration of chromium in edible mushrooms: Influence

of environmental and genetic factors
M.A. García, J. Alonso, M.J. Melgar ⇑
Department of Toxicology, Faculty of Veterinary Science. University of Santiago de Compostela, 27002 Lugo, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Chromium concentrations were determined in 167 samples of wild edible mushrooms, collected from
Received 22 March 2013 three different sites (urban, traffic and pastureland areas) in Lugo (NW Spain). The hymenophore (H)
Accepted 26 April 2013 and the rest of the fruiting body (RFB) were analysed separately. The analyses were performed using
Available online 3 May 2013
inductively coupled plasma optical emission spectrometry (ICP-OES). The highest mean chromium levels
(mg/kg dry weight) of 3.5 and 8.0, 4.5 and 6.2, and 6.2 and 4.3 were found in Lycoperdon utriforme, Copri-
Keywords: nus comatus and Agaricus campestris in H and RFB, respectively. The highest concentrations of chromium
Chromium
were observed in terrestrial saprophytic species in relation to mycorrhizal species. With respect to the
Edible mushrooms
Bioconcentration factors
underlying substrates, chromium concentration was lowest in the pastureland area (24.6 mg/kg dw).
Ecology All mushroom species were bioexclusors of chromium (BCF < 1) with statistically significant differences
(p < 0.001). The consumption of mushrooms harvested from the areas investigated poses no toxicological
risk to human health due to chromium.
Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction
Mushrooms constitute part of the human diet because they pro-
vide nutrients: carbohydrates, proteins, vitamins and minerals
(Kalač, 2009; Reis et al., 2012), nutraceuticals (Barros et al., 2008),
and other compounds with antihyperglycemic and antioxidant
activities (Ribeiro et al., 2007; Gursoy et al., 2009; Sarikurkcu
et al., 2010; Liu et al., 2012). Moreover, mushrooms are considered
a delicacy, they are part of the traditional culinary culture of some
countries, they are generally consumed worldwide and, in some
countries/regions, they are very popular (Falandysz and Borovička,
2013). Given their relative position in the food chain, the occurrence
of high metal contents in mushrooms is considered important be-
cause the presence of some metals, mainly cadmium, mercury and
lead, may constitute a possible toxicological hazard. Mushrooms
that are grown in natural habitats, geochemically anomalous areas
and anthropogenically polluted soils can uptake metals and concen-
trate them in the edible parts; thus, these toxic metals represent
serious threats to the environment, animals and humans (Řanda
and Kučera, 2004; Gursoy et al., 2009; Aloupi et al., 2012; Falandysz
et al., 2012a,b). However, many elements, such as Fe, Zn, Mn, Cr and
Se, are essential for human metabolism in low concentrations be-
cause they are enzyme activators. These elements become toxic as
their concentration increases. The process of heavy-metal accumu-
lation in mushrooms is species-dependent (Figueiredo et al., 2007;
Isildak et al., 2004; Li et al., 2011; Falandysz et al., 2012c). Several
⇑ Corresponding author. Tel.: +34 982 822206; fax: +34 982 822001.
E-mail address: mj.melgar@usc.es (M.J. Melgar).
already reported studies have evaluated the contents of toxic metals
in mushrooms to tentatively characterise pollution bioindicators
through bioconcentration factors, to investigate the relationship be-
tween the metal concentration in mushrooms and in the underlying
soil where mushrooms grow, or to evaluate metal intake through
the consumption of contaminated mushrooms (Demirbasß, 2001;
Sivrikaya et al., 2002; Zaichick, 2002; Mendil et al., 2004; Jonnalag-
adda et al., 2006; Dogan et al., 2006; Muñoz et al., 2006; Yamac et al.,
2007; Falandysz et al., 2008, 2012a; Gucia et al., 2012a). Although
the main factors that contribute to the accumulation of metals by
mushrooms have not been well identified, the uptake of metals is
determined by several conditions, specifically, environmental prop-
erties (e.g., the metal contents in soil, water and air, the pH and the
substrate composition) and genetic properties (e.g., the ecology, the
species and the morphological portion) (Falandysz et al., 2007; Gar-
cía et al., 2008; Campos et al., 2009; Melgar et al., 2009; Falandysz
et al., 2012c; Jarzyńska and Falandysz, 2012a,b). For example, in
contaminated aqueous solutions, pH was experimentally deter-
mined to be decisive in the biosorption of metals by Agaricus
macrosporus (Melgar et al., 2007).
Chromium (Cr) is a metallic element that can exist in several
oxidation states; the trivalent and hexavalent states are the most
important biological forms. Chromium is the tenth most abundant
element in the earth’s mantle, and it is used extensively for several
industrial purposes in both its tri- and hexavalent forms, depend-
ing upon the final use of the end product; these industrial
applications include electroplating, timber treatment, pulp produc-
tion, mineral ore, and petroleum refining (Wang et al., 2011). Chro-
mium is ubiquitous in nature; it occurs in air, water, soil and

0278-6915/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.fct.2013.04.049
250 M.A. García et al. / Food and Chemical Toxicology 58 (2013) 249–254

biological materials. It is therefore considered a bioelement with Table 1

important metabolic functions. Hexavalent chromium is highly Chromium concentrations (mg/kg dw) in the analysed species of mushrooms. The
number of samples (n), the parts, the mean concentrations, the standard deviations,
toxic; it exhibits genotoxic and carcinogenic actions in both ani- the range, the BCF, and the coefficients of Pearson correlations (r) are indicated.
mals and humans (Macfie et al., 2010). In addition to the different
biological and toxicological properties of the various chromium Species n Part Mean ± SD Range BCF r

species, their mobilisation from soils and their uptake by vegeta- Agaricus campestris L. 7 H 6.2 ± 5.0 1.8–16 0.24 0.398
bles also differ depending upon several factors, including the RFB 4.3 ± 2.4 1.7–8.7 0.22 0.080

microbial activity and the organic contents in the soil. Agaricus urinascens 12 H 3.2 ± 0.86 2.3–5.5 0.21 0.019*
Both CrIII and CrVI are taken up by plants: CrVI is taken actively (Jul. Schäff. & F.H. RFB 3.5 ± 0.93 2.4–5.4 0.24 0.156
Moller) Singer
by sulphate carriers and is immediately converted to CrIII in roots;
CrIII is taken up passively and is retained by the ion-exchange sites Agaricus silvicola 5 H 4.5 ± 2.2 2.3–8.0 0.25 0.757
(Vittad.) Peck RFB 3.3 ± 0.52 2.8–4.2 0.26 0.019*
of cell walls. Chromium concentrations in plants follow the general
order: roots > leaves > fruits (Van Paemel et al., 2010). Moreover, Agrocybe cylindracea 4 H 2.2 ± 0.24 2.0–2.4 (1)
(DC.) Marie RFB 1.8 ± 0.26 1.4–2.0
whereas CrIII is strongly retained in soil particles, CrVI is weakly ad-
sorbed and is readily available for plant uptake (Figueiredo et al., Amanita rubescens 11 H 2.5 ± 0.55 1.7–3.3 0.25 0.386
Pers. RFB 3.6 ± 1.1 2.7–5.9 0.34 0.360
2007).
Feed and food contain chromium in both inorganic forms and Boletus aereus Bull. 3 H 2.8 ± 0.29 2.5–3.1 0.06 0.803
RFB 3.8 ± 0.27 3.5–4.0 0.09 0.414
organic complexes; however, the precise speciation of dietary
chromium compounds is not known (EFSA, 2009). Boletus badius (Fr.) Fr. 9 H 2.4 ± 0.70 1.6–3.8 0.21 0.717
RFB 3.6 ± 0.57 2.7–4.9 0.33 0.598
All of the previous studies conducted on the Cr in mushrooms
reported the total Cr content, although one group of authors did Boletus edulis Bull. 10 H 2.8 ± 1.2 1.5–5.7 0.24 0.235
RFB 3.8 ± 1.2 1.1–5.3 0.32 0.358
specifically analyse the content of CrVI (Figueiredo et al., 2007).
The aim of the present investigation was to determine the accu- Boletus pinophilus 9 H 4.0 ± 1.7 2.3–7.3 0.24 0.028*
Pilát & Dermek RFB 4.4 ± 2.8 2.0–11 0.22 0.530
mulation capacity (concentration or exclusion) of total chromium
in the fruiting bodies of some edible mushrooms (cultivated and Boletus reticulatus 3 H 3.8 ± 0.92 3.1–4.8 0.13 0.391
Schaeff. RFB 3.0 ± 0.69 2.4–3.7 0.10 0.853
wild species) in relation to various factors, including the growth
substrate (metal content, acidity, and organic matter content), Lycoperdon utriforme 3 H 3.5 ± 1.7 2.2–5.4 0.21 0.046*
Bull. RFB 8.0 ± 7.2 2.8–16 0.30 0.418
the species and ecology (mycorrhizal and saprophytic), and the
morphological part (hymenophore and rest of the fruiting body). Cantharellus cibarius 11 H 0.67 ± 0.76 0.25–2.9 0.04 0.147
Fr. RFB 0.78 ± 1.2 0.13–4.2 0.05 0.138
We also evaluated the contribution of mushrooms to the daily hu-
man intake of this trace metal. Clitocybe nebularis 9 H 1.7 ± 1.0 0.28–2.6 0.09 0.330
(Batsch) P. Kumm. RFB 3.0 ± 2.3 0.20–6.4 0.12 0.641
Coprinus comatus 7 H 4.5 ± 3.1 1.8–10 0.22 0.511
2. Materials and methods (O.F. Müll) Pers. RFB 6.2 ± 4.8 2.7–16 0.29 0.224
Fistulina hepatica 4 H 3.1 ± 1.2 2.2–4.8 (1)
2.1. Sampling
(Schaeff.) With. RFB 3.9 ± 1.0 2.4–4.7
Fruiting bodies and the underlying substrate were collected from three different Hydnum repandum L. 8 H 2.2 ± 0.84 1.1–3.3 0.20 0.043*
sites: urban, traffic and pastureland areas in the province of Lugo (Galicia, NW RFB 2.6 ± 0.79 0.83–3.4 0.22 0.479
Spain) during 2009 and 2010. The species were selected in relation to their culinary
Lactarius deliciosus L. 9 H 5.2 ± 4.4 1.3–15 0.53 0.194
quality, commercialisation, and frequency in the areas of study.
(Gray) RFB 3.4 ± 2.6 0.84–8.5 0.32 0.046*
In total, 167 samples of edible mushrooms belonging to 22 species of Basidiomy-
cetes fungi (Table 1) were collected: 12 mycorrhizals, 8 saprophytes (terrestrial) and Leccinum scabrum 5 H 2.6 ± 0.72 1.8–3.7 0.25 0.355
2 saprophytes (lignicolous). (Bull.) Gray RFB 3.1 ± 0.65 2.2–4.0 0.32 0.587
Simultaneously, the upper soil horizons (0–10 cm, after the superficial layer of Lepista nuda (Bull.) 9 H 3.6 ± 1.9 1.5–7.0 0.37 0.434
organic detritus was removed) were also collected at appropriate sampling places. Cooke RFB 3.2 ± 1.8 2.0–7.6 0.31 0.252
A total of 50 underlying soil samples, where mushrooms grow, were analysed.
These samples were cleaned (not washed), cut and separated into two parts: the Macrolepiota procera 10 H 2.9 ± 1.4 1.2–5.3 0.18 0.576
hymenophore (H) and the rest of the fruiting body (RFB) (e.g., the cap, except the (Scop.) Singer RFB 2.3 ± 1.2 0.83–4.5 0.16 0.039*
hymenophore, and the stalk). Russula cyanoxantha 10 H 2.8 ± 2.7 0.71–9.1 0.11 0.499
Fresh mushrooms, after being cleaned of the plant and substrate debris with a (Schaeff.) Fr. RFB 2.8 ± 2.7 1.1–9.8 0.15 0.171
plastic knife, were air-dried for several days and further dried in an oven at 50 °C
Tricholoma 9 H 0.97 ± 0.38 0.49–1.7 0.09 0.076
until the samples reached a constant weight (approximately 40 h); the samples
portentosum (Fr.) RFB 0.80 ± 0.50 0.39–1.7 0.06 0.585
were subsequently pulverised in an agate mortar. Sub-samples (between 0.3 and
Quél.
0.5 g) of powdered mushrooms were wet-digested with 8 ml of concentrated nitric
acid (Suprapur, Merck) in closed PTFE vessels in a microwave oven (ETHOS 20, Mile- *
Significant difference, p < 0.05, (1) Wood-decaying and/or cultivated fungal
stone). The digested samples were diluted to a final volume of 50 ml with deionised species.
water. All samples were analysed in triplicate (García et al., 2009).
Soil substrate samples were dried at room temperature for several weeks and
then sieved through a pore size of 2 mm. A representative sample of up to 0.5 g
was digested in 10 ml of concentrated nitric acid (Suprapur, Merck) for 10 min in
The argon flow was regulated to 15 ml/min, the sample flow was regulated to
a closed PTFE vessel in a microwave oven (ETHOS 20, Milestone). The extract ob-
1.5 ml/min, and the potential was 1300 W (García et al., 2008).
tained was filtered through Whatman No. 42 filter paper into a volumetric flask
The accuracy of the method was evaluated using reagent blanks and standard
and was brought to a final volume of 50 ml with deionised water.
reference materials. A reagent blank and standard reference material (Lichen,
IAEA-336, International Atomic Energy Agency) were included to verify the accu-
2.2. Analyses racy and precision of the digestion and subsequent analysis procedure. Discrepan-
cies between certified values and concentrations quantified were below 10%
The dissolved metals were analysed via inductively coupled plasma optical (3.93%).The results obtained for 10 replicate analyses of this standard material
emission spectrometry (ICP-OES) on a Perkin Elmer OPTIMUM 4300 DV with the were:
use of the WinLab32 software package. The wavelengths of 267.707, 205.562 and
283.552 nm were used for the analysis of chromium. The integration time was var- Certified value: 1.06 mg/kg dw; range: 0.84–1.23.
ied between 1 and 5 s, with three replicates per sample. The detection limit was Measured value: 1.072 ± 0.23.
0.6 ng/kg. Recovery (%): 106.3 ± 14.1.
 M.A. García et al. / Food and Chemical Toxicology 58 (2013) 249–254
In day-by-day runs, with every set of 10 mushrooms samples one blank sample
was digested, diluted and analysed. For blank samples no major interferences were
for the element quantified.
2.3. Soil pH and organic matter
Distilled water (25 ml) was added to 10 g of air-dried soil sample, and the mix-
ture was left for 1 h at 25 °C. The pH of the mixture was subsequently measured
using a pH meter (GLP 21, CRISON). The soil’s organic matter content was deter-
mined gravimetrically after combustion of the organic matter within the soil sam-
ple (2 g, air-dried) at 550 °C for 16 h in a furnace horn (Select-Horn, SELECTA)
(Falandysz and Bielawski, 2007).
2.4. Statistical analysis
Statistical analyses were performed using analysis of variance (ANOVA). All data
were statistically analysed using the SPSS software package, version 19.0.
Variances in the metal levels in mushrooms due to the species, ecology and
morphological parts of the various mushroom samples were examined using a 3-
way ANOVA. The limit of statistical significance was set at p < 0.05. In the following
sections, the chromium concentrations are expressed as mg/kg on a dry-weight ba-
sis. The correlations between inter-Cr soil and inter-Cr fruiting bodies were exam-
ined using Pearson’s and partial correlation coefficients.
3. Results and discussion
The chromium contents are related to the species of mushroom,
the collecting site of the sample, the age of the fruiting bodies and
mycelium, and the distance of the sampling site from a source of
pollution. In this work, at least four factors could affect the chro-
mium concentrations of the edible mushrooms: species, ecology,
the morphological part and soil characteristics, such as metal lev-
els, pH and organic matter. These factors could influence the metal
concentrations and the bioconcentration factors (BCF, or the rela-
tionship between the metal concentration in mushrooms and the
metal concentration in the underlying soil where mushrooms
grow) because higher fungi are able to bioconcentrate (BCF > 1)
or exclude (BCF < 1) specific metal ions. BCF were calculated as
the relationship between the Cr concentration in the mushroom
and the Cr concentration in the soil in which the mushroom grew.
3.1. Species and ecology
The chromium concentrations in the hymenophore (H) and in
the rest of the fruiting bodies (RFB) of mushrooms are summarised
in Table 1. The mean Cr concentration in the 22 species of wild edi-
ble fungi tested was 3.1 mg/kg dry weight (3.0 in H and 3.2 in RFB).
With respect to the species, the highest mean chromium concen-
trations (mg/kg dw) of 5.8, 5.4 and 5.2 were found in Lycoperdon
utriforme, Coprinus comatus and Agaricus campestris, respectively,
whereas the lowest concentrations were found in Tricholoma port-
entosum (0.88) and Cantharellus cibarius (0.72).
Although the ANOVA indicated significant differences between
species, the Scheffé post hoc tests revealed that significant differ-
ences existed only between the values of C. cibarius and T. porten-
tosum with respect to A. campestris and C. comatus and not between
other species.
Muñoz et al. (2006) studied Cr concentrations at the subcellular
level in the cultivated mushrooms Agaricus bisporus and Pleurotus
ostreatus, and they reported concentrations in ranges previously re-
ported by other authors. In this study, the global mean concentra-
tion for all the species was 3.1 mg/kg dw; this value is
substantially lower than that reported in studies conducted in Tur-
key, which ranged from 3.94 ± 0.5 to 84.5 ± 11 mg/kg. In addition,
the highest and lowest Cr concentrations were observed for Phelli-
nus igniarius and Collybia marasmioides, respectively (Dogan et al.,
2006), and a concentration of 73.8 mg/kg dw was found for Gymn-
opus dryophilus. However, the Cr levels in other mushrooms were
between 1.95 and 38.60 mg/kg dw: 5.24 ± 0.33 in Hydnum repan-
251
dum, 4.24 ± 0.01 in Lactarius deliciosus, 38.60 ± 0.38 in C. comatus
and 15.84 ± 0.1 in Lepista nuda (Yamac et al., 2007). In contrast,
our value is higher than that found by authors who studied several
metals in samples collected in Chernobyl, including chromium
(0.048 mg/kg) (Zaichick, 2002). Other authors, such as Mendil
et al. (2004), obtained results similar to ours, where the average
chromium concentration was 1.2–4.2 mg/kg dw; the lowest and
highest chromium values were observed in Boletus badius
(1.2 ± 0.1 mg/kg), L. deliciosus (1.2 ± 0.1 mg/kg) and Polyporus (sp.)
(4.2 ± 0.4 mg/kg), and the minimum and maximum values of Cr
were obtained for P. ostreatus (1.3 ± 0.1 mg/kg) and Marasmius ore-
ades (24.3 ± 2.2 mg/kg). In contrast, the Cr concentrations were
10.4 ± 0.9 mg/kg for L. nuda and 1.9 ± 0.1 mg/kg for B. badius (Isildak
et al., 2004). Chromium is a minor chemical element in Paxillus invo-
lutus, and its mean concentration varies between 0.18 ± 0.05 mg/kg
and 1.8 ± 0.3 mg/kg in the caps and between <0.1 and 1.4 ± 0.6 mg/
kg dw in the stipes. Chromium is bio-excluded by P. involutus (Brzo-
stowski et al., 2011).
Highlighting the chromium content in some species, such as
H. repandum, Demirbasß (2001) found a concentration of 1.68 mg/
kg dw, which is lower than that of the current study (2.4 mg/kg
dw); they reported similar results for other species, such as Agaricus
silvicola (0.75 ± 0.14 mg/kg dw), Amanita rubescens (0.71 ± 0.13 mg/
kg dw) and Russula cyanoxantha (1.66 ± 0.21 mg/kg dw), which also
contained chromium concentrations lower than those obtained in
the present study for the same species (3.9 mg/kg dw, 3.05 mg/
kg dw and 2.8 mg/kg dw, respectively). In addition, the species
Xerocomus badius (B. badius), which was reported to contain Cr levels
<1000 mg/kg dw (Kojta et al., 2012), which are lower than the chro-
mium levels found in this study. Gucia et al. (2012b) found Cr con-
centrations of less than 1 mg/kg dw in the caps of Macrolepiota
procera, samples collected at different sites over a period of a few
years. Falandysz et al. (2012c) reported Cr concentrations of a few
micrograms per gram dry weight for C. cibarius, whereas the Cr con-
centration in C. cibarius in our study was slightly greater (0.73 mg/
kg dw).
Finally, a study conducted in South Africa highlights the differ-
ences between species because the detected chromium level in
A. bisporus mushrooms was 0.24 mg/kg, but Agaricus xanthoderma
and Rhizina undulata contained Cr concentrations that were 6
and 15 times greater, respectively (Jonnalagadda et al., 2006).
The mean chromium concentrations according to ecology were
2.8 mg/kg dw for the mycorrhizal species, 2.7 mg/kg dw for the lig-
nicolous saprophytic species and 3.7 mg/kg dw for the terrestrial
saprophytic species. The ANOVA indicated significant differences
according to ecological groups, and Scheffé post hoc tests showed
that a significant difference existed between the mycorrhizal and
terrestrial saprophytic species (p < 0.001).
According to ecological factors (Fig. 1), the highest concentra-
tions were observed in terrestrial saprophytic species, with statisti-
cally significant differences (p < 0.001) in relation to the
concentrations in mycorrhizal species.
In general, BCF values of terrestrial saprophytic species and
mycorrhizal species were similar (0.22 and 0.21, respectively),
with L. deliciosus showing the highest BCF (greater than 0.42) and
C. cibarius exhibiting the lowest value (0.04).
In other studies that assessed ecological factors (Figueiredo
et al., 2007), the total Cr concentrations in the mushroom cap sam-
ples ranged from 0.02 to 13.84 mg/kg dw, and no differences were
found between mycorrhizal and saprophytic mushrooms
(1.49 ± 1.41 versus 0.20 ± 0.16 mg/kg dw).
3.2. Morphological parts
The mean chromium concentrations in the species studied
according to morphological parts were 3.0 and 3.2 mg/kg dw for
252 M.A. García et al. / Food and Chemical Toxicology 58 (2013) 249–254
the hymenophore and for the rest of the fruiting body, respectively.
The highest mean chromium levels of 3.5 and 8.0, 4.5 and 6.2, and
6.2 and 4.3 mg/kg dw were found in L. utriforme, C. comatus and
A. campestris in H and RFB, respectively, whereas the lowest levels
were found in T. portentosum (0.97 mg/kg dw in H and 0.80 mg/
kg dw in RFB) and C. cibarius (0.67 mg/kg dw in H and 0.78 mg/
kg dw in RFB). There were no statistically significant differences
between the two morphological parts. These results with respect
to chromium, in contrast to other metals that demonstrate in-
creased accumulation in the hymenophore, were most likely
caused by the biological activity of proteins contained in the H to-
ward the RFB (Chang and Chan, 1973).
In studies on Parasol mushroom (M. procera), Jarzyńska et al.
(2011) reported Cr levels of 0.31 and 0.61 mg/kg dw in caps and
stipes, respectively. Falandysz et al. (2008) also reported similar
Cr levels in caps and stalks; the Cr levels were found to depend
on the sampling site and were always less than 1 mg/kg dw,
although these concentrations were still less than those obtained
in the present work for the same species (2.6 mg/kg dw). For Lecc-
inum scabrum, our Cr medium values (H: 2.6 mg/kg dw, RFB:
3.1 mg/kg dw) were also greater than those reported by Falandysz
et al. (2007) in caps (<0.5 mg/kg dw). Moreover, in Leccinum grise-
um, the caps contained more Cr than did the stipes (Jarzyńska and
Falandysz, 2012a); in contrast, the stipes of the species Leccinum
duriusculum contained a greater Cr concentration than did the caps
(Jarzyńska and Falandysz, 2012b).
The overall mean chromium ratio of H/RFB obtained in the sam-
ples analysed was 0.88.
3.3. Soil factors
The mycelia of higher fungi, especially mushrooms spread over
large areas (several square meters) and their close association with
soil and dead organic matter and/or their symbiotic association
with plant roots, offer conditions for intensive exchange with sub-
Fig. 1. Mean levels of chromium in the studied mushroom species in relation to the
ecology and the morphological part.
strates (Turnau et al., 2001; Falandysz et al., 2012c). The concentra-
tions of heavy metals in many fungi correlate with the metal
concentration in the soil in which they grow (Chang and Chan,
1973); examples include the Hg, Cu and Zn concentrations in dif-
ferent species (Alonso et al., 2003; Melgar et al., 2009) and the con-
centrations of several metals in the species Suillus grevillei and L.
duriusculum (Chudzyński and Falandysz, 2008; Jarzyńska and
Falandysz, 2012b).
The uptake and presence of heavy metals by fungi depend on
other factors, such as the pH, the temperature, the ratio between
the initial metal-ion concentration and that of the initial biomass,
and the presence of various ligands and competitive metal ions in
solution (Campos et al., 2009).
Because the heavy-metal concentrations in mushrooms are
weakly affected by the pH and the organic matter content of the
substrate, we investigated the relationship between the uptake of
chromium in mushrooms and the soil characteristics. According
to the soil characteristics and possible pollution sources, three
zone groups were established: urban, traffic, and pastureland
areas. In general, the soil pH was acidic; the highest pH (7.0, neu-
tral) was observed in Lugo’s city centre (an urban area). In traffic
areas, a pH of 5.0 was observed, and the lowest value (pH 4.0)
was observed in the pastureland zone. Our results showed that
the absorption of metals was not affected by pH, possibly because
all of the pH values were acidic and, according to literature data, in
a narrow range (Gast et al., 1988; Falandysz et al., 2012c). With re-
spect to the content of organic matter, the highest content
(14–16%) was found in pastureland soil, and urban and traffic areas
showed similar levels (7–10%). These values did not affect the me-
tal uptake.
With regard to the sampling areas, the mean chromium concen-
tration in soil was 26.0 mg/kg dw, and the lowest concentration
was observed in the pastureland area (Fig. 2). The ANOVA (Table 2)
showed significant differences (p < 0.001) between urban
(42.9 mg/kg dw) and pastureland zones (24.6 mg/kg dw).
The mean BCF value was 0.21, and all species presented BCF less
than 0.5. These values indicate the bio-exclusion of the mushrooms
studied with regard to soil chromium concentration and are in
agreement with Kalač and Svoboda (2000) for the species Agaricus
spp., M. procera and L. deliciosus; with Malinowska et al. (2004) for
X. badius; with Figueiredo et al. (2007) for several species (Agaricus,
Amanita, Lactarius, etc.); and with Chudzyński and Falandysz
(2008) for S. grevillei. This behaviour was similar to that of lead
(García et al., 2009) and in contraposition to the bioaccumulative
character of mercury (Falandysz and Bielawski, 2007; Melgar
et al., 2009).
According to the results in Tables 2 and 3, the Pearson correla-
tions showed a statistically significant (p 6 0.001) difference be-
tween the chromium concentrations in soil and mushrooms and
also with the BCF (p < 0.001). The relationship between the Cr con-
centrations in soil and those in the fruiting bodies was significantly
positive, whereas the relationship between BCF and the Cr concen-
Fig. 2. Mean levels of chromium in soils in different areas of study.
 M.A. García et al. / Food and Chemical Toxicology 58 (2013) 249–254 253

Table 2 According to our results on the total chromium, the consump-

Pearson correlations to determine the significant differences in Cr levels between the tion of tested mushrooms harvested from the areas investigated
total metal content in the underlying soil and the fruiting bodies in all of the samples
(n = 159).
therefore poses no toxicological risk to human health due to chro-
mium content, corroborating this statement the results obtained
Correlation Total Terrestrial Mycorrhizal by Figueiredo et al. (2007), who demonstrated that the most toxic
species saprophytic species
species
Cr form (CrVI) contributes to the total Cr with a low percentage
(about 11%). Although the knowledge of mushrooms nutritional
Cr soil – Cr Pearson 0.189** 0.217 0.122
fruiting- coef.
value and their information on the bioavailability of its compo-
bodies nents are limited, they are a nutritional requirement for diet (Ka-
Significance 0.001 0.016 0.089 lač, 2009).
**
Significant correlation, p 6 0.001.
Conflict of Interest

The authors declare that there are no conflicts of interest.

Table 3
Pearson correlations to determine the significant differences in Cr levels between the
total metal content in the soil and the BCF. Acknowledgement
Correlation Total species Cr soil
This work was financially supported by Xunta de Galicia
Cr soil – Cr BCF Pearson coef. 0.441** 0.577**
Significance 0.000 0.000
(INCITE08PXB261087PR).
**
Significant correlation, p < 0.001.
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