Contents of Eight Trace Elements in Edible Mushrooms from a Rural Area Lubomir Svoboda, Vladislav Chrastny

Contents of eight trace elements in edible mushrooms from a rural area Lubomir Svoboda, Vladislav Chrastny

To cite this version:

Lubomir Svoboda, Vladislav Chrastny. Contents of eight trace elements in edible mushrooms from a rural area. Food Additives and Contaminants, 2007, 25 (01), pp.51-58. 10.1080/02652030701458519. hal-00577280

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For Peer Review Only

Contents of eight trace elements in edible mushrooms from a rural area

Journal: Food Additives and Contaminants

Manuscript ID: TFAC-2007-012.R1

Manuscript Type: Original Research Paper

Date Submitted by the 14-May-2007 Author:

Complete List of Authors: Svoboda, Lubomir; University of South Bohemia, Faculty of Agriculture, Studentska 13, 370 05 Ceske Budejovice, Dep. of Applied Chemistry Chrastny, Vladislav; University of South Bohemia, Faculty of Agriculture, Studentska 13, 370 05 Ceske Budejovice, Dep. of Applied Chemistry

Methods/Techniques: Metals analysis - ICP/MS

Additives/Contaminants: Trace elements, Trace elements (nutritional)

Food Types: Mushrooms

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1 2 3 4 Contents of eight trace elements in edible mushrooms from a rural area 5 6 7 LUBOMÍR SVOBODA and VLADISLAV CHRASTNÝ 8 9 10 11 Department of Applied Chemistry, Faculty of Agriculture, University of South Bohemia, 12 13 Studentská 13, 370 05 České Bud ějovice, Czech Republic, e-mail: [email protected] 14 15 16 For Peer Review Only 17 18 Abstract 19 20 21 22 Eight trace elements were determined using ICP-MS in 78 samples of fruiting bodies of 22 23 edible mushroom species. The mushrooms were collected from four sites in a rural area 24 25 unpolluted by human activities. Median values (dry matter) were as follows:- arsenic (As) 26 27 1.45 mg kg -1, barium (Ba) 1.41 mg kg -1, cobalt (Co) 0.28 mg kg -1, copper (Cu) 47.0 mg kg -1, 28 -1 -1 -1 29 rubidium (Rb) 130 mg kg , silver (Ag) 2.95 mg kg , thallium (Tl) 0.02 mg kg and 30 -1 31 vanadium (V) 0.25 mg kg . Higher trace element accumulation was observed within samples 32 of Macrolepiota procera , Macrolepiota rhacodes , Lycoperdon perlatum, Lycoperdon 33 34 gigantea and Xerocomus chrysenteron for As and Cu, and within samples of Cantharellus 35 36 cibarius and of genera Boletus and Suillus for Rb. 37 38 39 40 41 Keywords: edible mushrooms; trace elements; arsenic; heavy metals; barium; cobalt; copper; 42 43 rubidium; silver; thallium; vanadium 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Introduction 4 5 6 7 Extensive research has been carried out since the 1970´s on the occurrence of trace elements 8 9 (mainly heavy metals) in mushrooms (higher fungi, macrofungi). The research has had mainly 10 two aims: screening of mushroom fruiting bodies as bioindicators of environmental pollution 11 12 and searching for edible species accumulating high levels of some trace elements. As 13 14 detected, many wild growing species accumulate high concentrations, especially of cadmium, 15 16 mercury, lead For and copper, Peer at levels considerablyReview exceeding Only those in plants and in foods 17 18 generally (for a review see Kala č & Svoboda 2000). 19 20 21 Knowledge of the roles of trace elements in physiology of higher fungi has been limited. 22 23 Concentrations of the elements in fruiting bodies are generally species-dependent. Substrate 24 25 composition is an important factor, but great differences exist in the uptake of individual 26 metals (Tyler 1982, Gast et al. 1988, Michelot et al. 1998). 27 28 29 30 The age of the fruiting body or its size are of less importance. Some authors reported higher 31 32 metal concentrations in younger fruiting bodies. This is explained by the transport of a metal 33 34 from mycelium to the fruiting body during the start of fructification. During the following 35 increase of the fruiting body mass, the metal concentrations decrease. The proportion of metal 36 37 concentrations from atmospheric deposition seems to be of less importance due to a short 38 39 lifetime of fruiting bodies of the most of edible species, which is usually 10-14 days. In our 40 41 opinion, metal levels in fruiting bodies of wild growing mushrooms are considerably affected 42 by the age of mycelium and by the interval between the fructifications. All these factors cause 43 44 a very wide variability in the trace element concentrations within a species, commonly to one 45 46 order of magnitude. 47 48 49 Information on levels of detrimental metals and metaloids has been required for countries 50 51 with a traditionally high consumption of wild growing edible mushrooms. This study follows 52 53 our previous work (Nová čková et al. 2007), the primary aim of which was to consider the 54 55 contents of mercury, cadmium and lead in wild edible mushrooms growing in a site with 56 57 specific geological ground, namely with the occurrence of serpentines and amphiboles. No 58 significant differences were observed between the level of three studied metals in mushrooms 59 60 from the tested and background unpolluted areas. The objective of the present work was to determine the potential health risk contents of eight trace elements, including those with

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1 2 3 scarce data, in fruiting bodies of widely consumed mushroom species growing in an area 4 5 known by an increased occurrence of serpentines and amphiboles. 6 7 8 9 Materials and methods 10 11 12 Sampling 13 14 The study was carried out at four sites over an area of 0.7-2.7 ha in a rural unpolluted region 15 16 near a small townFor Moravský Peer Krumlov, south-westernReview Moravia, Only Czech Republic, about 30 km 17 18 south-west from the city of Brno. The sites were up to 15 km apart, around the nature reserve 19 “Serpentine steppe” near Mohelno, at an altitude of 230 – 460 m above sea level. Nuclear 20 21 power station Dukovany (4 x 440 MW), in operation since 1985, lies near the sites. No roads 22 23 with extensive traffic have crossed the tested area. 24 25 26 Mushrooms were collected in mixed forests with prevailing oak, beech, acacia, spruce and 27 28 pine during the period 2001 - 2003. One complete fruiting body was used as a sample. The 29 30 bodies were cleaned of all surface contamination by a stainless steel knife. No washing or cap 31 32 peeling was applied. The bodies were sliced and dried at an ambient temperature in a dust- 33 34 free room in a manner typical for mushroom preparation for culinary purposes and then 35 powdered. In total, 78 samples of 22 mushroom species were collected and analysed. 36 37 38 39 Analytical procedures 40 41 About 0.3 g of an air dried mushroom sample was wet digested with 5 ml of suprapure 42 concentrated nitric acid (Merck, Germany) in a closed Teflon ® vessel in a microwave oven 43 44 MDS 2000 (CEM Corp., USA). The digest was diluted to 25 ml with deionized water 45 46 (MILLI-Q Element, Millipore, France) and filtrated using glass microfibre filter GF/C 47 48 (Whatman, UK). 49 50 51 Each of the mushroom samples was analysed in triplicate. The determination of the metal 52 53 concentrations was performed using a mass spectrometer with inductively coupled plasma 54 55 (ICP-MS) PQExCell (VG Elemental, UK) under standard conditions with a Meinhard 56 57 concentric nebulizer. For all measurements presented, quantification was performed using an 58 aqueous multi-element standard solution Merck VI (CertiPUR, Merck, Germany). The 59 60 calibration procedure consisted of ten measurement replicates of the instrumental blank and five measurement replicates of the differently diluted standard solutions. To eliminate non-

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1 2 3 spectral interferences, internal standardisation was used. The results were within limits of 4 5 quantification for arsenic, barium, cadmium, cobalt, copper, lead, rubidium, silver, thallium 6 7 and vanadium (calculated as 10-fold of standard deviation from ten replicates of the 8 -1 9 instrumental blank solution) 10, 20, 2.5, 75, 2.5, 15, 2 and 2.5 µg kg dry matter, 10 respectively. A reference material CRM BCR No 60, Trace elements in an aquatic plant 11 12 Lagarosiphon major (Commission of the European Communities, Community Bureau of 13 14 Reference, Belgium) and epiphytic lichen Evernia prunastri (International Atomic Energy 15 16 Agency, Wienna,For Austria) Peer was used forReview the evaluation of theOnly measurement precision and 17 18 accuracy. Differences between determined and certified contents were for all analysed 19 elements below 10 %. 20 21 22 23 Statistical method 24 25 Outlying results were identified by Grubbs‘ test and were not statistically processed by 26 Student´s test. For all statistical procedures, values below the limits of quantification were 27 28 used for the calculations as halves of the limits of quantification. Differences in the element 29 30 contents among species (given in Table II) were tested by Duncan´s multiple range test with 31 32 alpha levels for critical ranges P < 0.05, using program Statistica for Windows, StatSoft, Inc., 33 34 USA. 35 36 37 38 39 Results and discussion 40 41 42 In total, 78 samples of 22 mushroom species were collected and analysed. Contents of the 43 44 individual metals are given in Table I. Element concentrations are expressed as mg kg -1 dry 45 46 matter. There exists a consensus that dry matter content of mushrooms is 10 %. 47 48 49 High values of standard deviation, even higher several times than mean values (Table II), 50 51 were caused by a highly abnormal metal content distribution. A very wide range of metal 52 53 contents within a species is quite common in mushrooms (for review see Kala č & Svoboda 54 55 2000). Such a situation is different from that in plants. Basic Statistical characteristics of the 56 57 determined trace elements for eight mushroom species with at least four five samples are 58 given in Table II. 59 60

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1 2 3 Statistical testing by Duncan´s test revealed no differences in four elements (arsenic, barium, 4 5 silver and vanadium) and limited differences in three elements (cobalt, rubidium and 6 7 thallium). Copper was the only element with three different content levels. The results of the 8 9 test are affected with wide variations of the element contents within the individual species. 10 11 12 Arsenic 13 14 High contents of metalloid arsenic (median 1.45 mg kg -1 dry matter, Table I) were found in 15 16 Macrolepiota For rhacodes , Peer M. procera , LycoperdonReview perlatum Onlyand Xerocomus chrysenteron. 17 18 Several accumulating species such as Agaricus spp. , Laccaria amethystina, L. fraterna, L. 19 laccata , Macrolepiota procera and Telephora terrestris were reported (Vetter 1989, Stijve & 20 21 Bourqui 1991, Parisis & Van Den Heede 1992, Byrne et al. 1995, Slekovec & Irgolic 1996, 22 23 Šlejkovec et al. 1997, Weeks at al. 2006). Moreover, an extreme arsenic content was found in 24 -1 25 inedible Sarcosphaera coronaria with maximum values of 2130 and 7090 mg kg dry matter 26 (Stijve et al. 1990 and Borovi čka 2004), respectively. 27 28 29 30 Food and feed plants, in contrast to marine animal organisms, contain only a very limited 31 -1 32 level of arsenic. Cereal and potatoes exhibit medium content of 0.05 mg kg fresh matter and 33 -1 34 fruits and vegetables between 0.02-0.04 mg kg fresh matter (Weigert 1991). 35 36 37 Barium 38 -1 39 The mean barium content of all analysed samples was 2.15 mg kg dry matter. As compared 40 41 with other metals, barium contents were relatively equal without a tendency of its 42 accumulation within certain genera of mushrooms. A similar situation was observed also for 43 44 cobalt and vanadium. 45 46 47 48 There is a lack of limited information on contents of barium in mushrooms. Both Vetter 49 (1989) in Agaricus spp. and Pleurotus spp. and Arguete et al. (1998) in Amanita rubescens , A. 50 51 flavorubescens and Russula pectinatoides Bakken & Olsen (1990), Vetter (1989) and Arguete 52 53 et al. (1998) found mean contents of barium in order of a maximum few mg per kilogram of 54 55 dry matter. Our results are in a good agreement with their findings. Shiraishi (2004) 56 57 performed an analysis of dietary intakes of 19 elements (including barium, cobalt, copper, and 58 rubidium) in eighteen food categories by Japanese subjects: For barium, two categories had 59 60 high concentrations: seaweeds and nuts and seeds (4.61 and 5.91 mg kg -1 fresh matter,

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1 2 3 respectively). For mushrooms, average content of 0.26 mg kg -1 fresh matter was reported 4 5 (Shiraishi 2004). 6 7 8 9 Cobalt 10 For cobalt we obtained median and maximum value of 0.28 and 3.25 mg kg -1 dry matter, 11 12 respectively. Usual contents of cobalt in mushrooms are in order of tenth, maximally a few 13 14 mg per kilogram of dry matter (Młodecki et al. 1965, Drbal & Kala č 1976, Mutsch et al. 1979, 15 16 Kala č et al. 1989,For Vetter Peer1989, Barcan Reviewet al. 1998, Sesli & TüzenOnly 1999, Siobud-Dorocant et 17 18 al. 1999, Demirba 2001, Mendil et al. 2004, Ye il et al. 2004, Tüzen 2003, Iilo ğlu et al., 19 2001, Solyak et al. 2005). An extraordinary high value of 148 mg kg -1 dry matter found 20 21 Michelot et al. (1999) in Calocera viscosa . Mean contents of cobalt in mushrooms are 22 23 comparable with foodstuffs like cereals, potatoe, and fruits, where these range from 0.01 to 24 -1 25 0.1 mg kg fresh matter (Weigert 1991). Similar range was determined by Shiraishi (2004). 26 27 28 Copper 29 -1 30 The mean copper content of all analysed samples 74.7 mg kg dry matter (Table II) was the 31 -1 32 second highest value from all analysed metals, with maximum values 451 and 502 mg kg dry 33 Xerocomus chrysenteron 34 matter found in . However, these two concentrations were identified 35 by Grubbs‘ test like the outliers. Other high levels were observed within the genera 36 37 Macrolepiota and Lycoperdon . Usual copper contents in mushrooms are in order of tens mg 38 -1 39 kg dry matter. In accumulating species like Agaricus spp., Lycoperdon spp., Macrolepiota 40 -1 41 procera and M. rhacodes the contents could be between 100-300 mg kg dry matter 42 (Wondratschek & Röder 1993, Alonso et al. 2003, Kala č & Svoboda 2000). However, higher 43 44 contents could be found in heavy polluted areas such us in the close vicinity of copper 45 46 smelters. (Svoboda et al. 2000). The average copper content in fruits and vegetables ranges 47 -1 48 between 0.6 and 1.0 mg kg fresh material (Weigert 1991), which is consistent with findings 49 of Shiraishi (2004). 50 51 52 53 Rubidium 54 -1 55 The mean rubidium content of all analysed samples 174 mg kg dry matter (Table II) have 56 -1 57 always been the highest from all analysed metals, with maximum value 3009 mg kg dry 58 matter found in Xerocomus chrysenteron . However, this extraordinary concentration was 59 60 identified by Grubbs‘ test like an outlier. Above-average contents 355 and 351 mg kg -1 dry matter of rubidium were found in two available samples of Cantharellus cibarius and in the

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1 2 3 most samples of genera Boletus and Suillus . Hedrich (1988) reported also the highest content 4 5 of rubidium in a sample of C. cibarius 911 mg kg -1 dry matter. Řanda et al. (2005) observed 6 -1 7 the extraordinary high content of 1250 mg kg dry matter in Hydnum repandum and the 8 -1 9 second highest values of 590 mg kg dry matter was also found in C. cibarius . Tyler (1980) 10 determined the highest contents of 1190 and 1070 mg kg -1 dry matter in H. repandum and C. 11 12 cibarius , respectively and a high level in all species of Lactarius and in most samples of 13 14 Amanita . Klán et al. (1988) besides high content in C. cibarius and in samples of the 15 16 Boletaceae familyFor reported Peer the highest Review level in Lactarius Only rufus . Tyler (1982) performed 17 18 stepwise regression statistics for contents of twelve metals including of rubidium in Amanita 19 rubescens and Collybia peronata and characteristics of their growing substrate. He concluded 20 21 that metal concentration, acidity and certain physical properties of the substrates in most cases 22 23 are of much less importance in regulating the uptake of metals by the two examined 24 25 mushroom species than by the vascular plants. However, there is an exception in rubidium, 26 since there is a relatively high positive correlation of its level between fruiting body and 27 28 substrate and negative correlation between pH or degree of metal ion saturation. Ko śla (1997) 29 30 mentioned the similar situation in plants, where its uptake is increasing with decreasing pH of 31 32 substrate. Shiraishi (2004) found a high concentration of rubidium in the categories of nuts 33 -1 34 and seeds, potatoes, mushrooms, meats, and seaweeds (13.0, 7.46, 7.46, 5.21 and 4.14 mg kg 35 fresh matter, respectively). 36 37 38 39 Silver 40 41 For silver, the determined contents ranged very widely from values under the limit of 42 quantification 0.015 mg kg -1 dry matter to maximum concentration 315 mg kg -1 dry matter in 43 44 a sample of Lycoperdon perlatum . We did not observe any evident ability to accumulate silver 45 46 in a certain taxonomic group like genus or family. However, in contrary to barium, cobalt and 47 48 vanadium, silver contents are highly fluctuating with a high variation within the individual 49 mushroom species. Overall RSD for silver calculated from all samples regardless of their 50 51 taxonomic species was the highest (224 %) from all eleven eight investigated metals (Table 52 53 II). Very similarly wide-ranging contents were reported by Falandysz et al. (1994a), 54 55 Arugguete (1998), Siobud-Dorocant et al. (1999) and Řanda et al. (2005). Nevertheless, it is 56 57 very difficult to perform an objective conclusion about the accumulation of silver in certain 58 mushrooms species. A higher number of samples would be thus useful for the comparison of 59 60 silver-accumulation ability of certain mushrooms species. Hedrich (1988) found a high bioaccumulation potency for silver in Agaricus augustus and Falandysz et al. (1994b) in A.

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1 2 3 campestris and A. bisporus . Byrne et al. (1979) determined the highest silver contents in 4 5 samples of Agaricus spp. and above-average levels in genera Lycoperdon and Boletus . 6 7 According to Petering & McClain (1991), silver is present in plants in the range of 0.006 to 8 -1 -1 9 0.28 mg kg . In fungi and bacteria, they reported silver content of about 29 to 210 mg kg , 10 respectively. Aquatic plants tend to concentrate silver from their environments several 11 12 hundredfold. 13 14 15 16 Thallium For Peer Review Only 17 18 A very high variance of content, similar as to that observed for silver, was also determined 19 for thallium. This observation is consistent with findings from other authors. Mean thallium 20 21 content of all analysed samples 0.045 mg kg -1 dry matter (Table II) was the lowest one among 22 23 the determined elements. Usual levels of thallium in mushrooms have been in order of 24 -1 25 hundredth or maximally a few tenth mg kg dry matter (Seeger & Gross 1981, Bakken & 26 Olsen 1990, Parisis & Van Den Heede 1992, Yoshida et al. 1996, Falandysz et al. 2001, 27 28 Řanda & Ku čera 2004). No considerable inter-species differences in thallium concentration 29 30 were observed. However, Seeger & Gross (1981) and Yoshida et al. (1996) mentioned a 31 32 somewhat higher accumulation ability of Agaricus spp. Extraordinary high values 4.79 and 33 -1 Lactarius deliciosus Suillus luteus, 34 3.48 mg kg dry matter were registered in and 35 respectively, growing near a flotation waste reservoir serving a mining and metallurgical 36 37 works (Dmowski & Badurek 2002). An absolutely maximum reported content of 5.5 mg kg -1 38 39 dry matter found Seeger & Gross (1981) in inedible Peziza badia ( Ascomycetes ). 40 -1 41 The usual mean thallium contents of cereals, fruits, and vegetables are about 0.05-0.1 mg kg 42 fresh material (Weigert 1991). 43 44 45 46 Vanadium 47 48 Toxic Amanita muscaria has been well-known vanadium accumulator since the 1930s. Koch 49 et al. (1987) and Řanda et al. (2005) confirmed high accumulation ability of A. muscaria, with 50 51 content in order of magnitude of hundreds mg kg -1 dry matter. Usual levels of vanadium in 52 53 other species are much more lower – typically in order of tenth mg per kilogram of dry matter 54 55 (Hedrich 1988, Parisis & Van Den Heede 1992, Valiulis et al. 1995, Vetter 1999). Our results 56 57 are in a good agreement with the literature data. According to Reilly (2002), levels in most 58 foods appear to be low, between 1 and 30 mg kg -1. Skimmed milk, lobster and some other sea 59 60 foods, vegetable oils, certain vegetables, and some cereals are reported among the richest food source of vanadium (Repinc et al. 2005).

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1 2 3 Petering HG, McClain CJ. 1991. Silver. In: Merian E, editor. Metals and Their Compounds in 4 5 the Environment. Weinheim: VCH., p 1191. 6 7 Řanda Z, Ku čera J. 2004. Trace elements in higher fungi (mushrooms) determined by 8 9 activation analysis. Journal of Radioanalytical and Nuclear Chemistry 259:99-107. 10 Řanda Z, Soukal L, Mizera J. 2005. Possibilities of the short-therm thermal and epithermal 11 12 neutron activation for analysis of macromycetes (mushrooms). Journal of Radioanalytical and 13 14 Nuclear Chemistry 264:67-76. 15 16 Reilly C. 2002.For Metal Contamination Peer ofReview Food: Its Significance Only for Food Quality and Human 17 rd 18 Health, 3 edition. Oxford: Blackwell Science Ltd. p181. 19 Repinc U, Benedik V, Stibilj V, 2005. Determination of vanadium in biological and 20 21 environmental samples by RNNA with emphasis on quality control. Journal of 22 23 Radioanalytical and Nuclear Chemistry 264:39-43. 24 25 Seeger R, Gross M. 1981. Thallium in higher mushrooms. Zeitschrift für Lebensmittel- 26 Untersuchung und -Forschung 173:9-15. (in German) 27 28 Sesli E, Tüzen M. 1999. Levels of trace elements in the fruiting bodies of macrofungi 29 30 growing in the East black Sea region of Turkey. Food Chemistry 65:453-460. 31 40 32 Shiraishi K. 2005. Determination of eighteen elements and K in eighteen food categories by 33 34 Japanese subjects. Journal of Radioanalytical and Nuclear Chemistry, 266:61-69. 35 Siobud-Dorocant E, Doré JC, Michelot D, Poirier F, Viel C. 1999. Multivariate analysis of 36 37 metal concentration profiles in mushrooms. SAR and QSAR in Environ. Research 10:315- 38 39 370. 40 41 Šlejkovec Z, Byrne AR, Stijve T, Goessler W, Irgolic KJ. 1997. Arsenic compounds in higher 42 fungi. Applied Organometallic Chemistry 2:673-682. 43 44 Slekovec M, Irgolic KJ. 1996. Uptake of arsenic by mushrooms from soil. Chemical 45 46 Speciation and Bioavailability 8:67-73. 47 48 Soylak M, Saraço ğlu S, Tüzen M, Mendil D. 2005. Determination of trace metals in 49 mushroom samples from Kayseri, Turkey. Food Chemistry 92:649-652. 50 51 Stijve T, Bourqui B. 1991. Arsenic in edible mushrooms. Deutsche Lebensmittel-Rundschau 52 53 87:307-310. 54 55 Stijve T, Vellinga EC, Herrmann A. 1990. Arsenic accumulation in some higher fungi. 56 57 Persoonia 14:161-166. 58 Svoboda L, Zimmermannová K, Kala č P. 2000. Concentration of mercury, cadmium, lead and 59 60 copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. Science of the Total Environment 246:61-67.

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1 2 3 Tüzen M. 2003. Determination of heavy metals in soil, mushrooms and plant samples by 4 5 atomic absorption spectrometry. Microchemical Journal J. 74:289-297. 6 7 Tyler G. 1980. Metals in sporophores of Basidiomycetes . Transactions of the British 8 9 Mycological Society 74:41-49. 10 Tyler G. 1982. Accumulation and exclusion of metals in Collybia peronata and Amanita 11 12 rubescens . Transactions of the British Mycological Society 79:239-245. 13 14 Valiulis D, Stankevi čiene D, Kvietkus K. 1995. Metal accumulation in some fungi species 15 16 growing in Lithuania.For Atmospheric Peer Physics Review 17:47-51. Only 17 18 Vetter J. 1989. Comparison of mineral elements in Agaricus and Pleurotus fruit bodies. (in 19 German). Zeitschrift für Lebensmittel-Untersuchung und -Forschung 189:346-350. 20 21 Vetter J. 1999. Vanadium content of some common edible, wild mushroom species. Acta 22 23 Alimentaria 28:39-48. 24 25 Weigert P. 1991. Metal loads of food of vegetable origin including mushrooms. In: Merian E, 26 editor. Metals and Their Compounds in the Environment. Weinheim: VCH. p 449. 27 28 Weeks CA, Croasdale M, Osborne MA, Hewitt L, Miller PF, Robb P, Baxter MJ, Warriss PD, 29 30 Knowles TG. 2006. Multi-element survey of wild edible fungi and blackberries in the UK. 31 32 Food Additives and Contaminants 23:140-147. 33 34 Wondratschek I, Röder U. 1993. Monitoring of heavy metals in soils by higher fungi. In: 35 Merkert B, editor. Plants as Biomonitors. Indicators for Heavy Metals in the Terrestrial 36 37 Environment. Weinheim: VCH. p 345. 38 39 Ye il ÖF, Yildiz A, Yavuz Ö. 2004. Level of heavy metals in some edible and poisonous 40 41 macrofungi from Batman of south east Anatolia, Turkey. Journal of Environmental Biology 42 25:263-268. 43 44 Yoshida S, Muramatsu Y, Ban-Nai T. 1996. Accumulation of radiocesium and trace elements 45 46 in mushrooms collected from Japanese forests. Mitteilungen der Österreichischen 47 48 Bodenkundlichen Gesellschaft 53:251-258. 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Table I. Content of eight analysed elements (mg kg -1 dry matter) in mushroom samples. 4 5 6 7 Species As Ba Co Cu Rb Ag Tl V 8 Cantharellus cibarius 0.48 6.68 1.22 50.4 355 ND 0.03 0.15 9 0.31 2.62 0.47 34.1 351 0.07 0.02 0.37 10 Armillaria mellea 0.01 0.20 0.02 16.2 158 2.53 ND 0.23 11 Lepista nuda 3.07 1.44 0.17 91.6 3.51 0.61 ND 0.37 12 Marasmius oreades 55.5 2.98 0.09 50.1 77.0 ND 0.03 0.67 13 2.35 5.15 1.20 104 8.14 3.51 0.02 1.16 14 15 Amanita rubescens 0.69 0.68 0.49 44.8 67.8 ND 0.01 0.11 16 For Peer 0.95 3.83Review 0.77 58.3 Only 541 11.2 0.08 0.36 17 0.70 5.55 0.45 41.1 192 0.06 0.04 0.84 18 4.76 0.26 0.05 11.3 278 6.33 0.30 0.07 19 Agaricus campestris 2.60 2.63 0.24 47.0 3.92 17.0 0.02 0.70 20 Agaricus macrosporus 2.64 1.39 0.30 91.7 21.3 23.7 0.03 0.32 21 Macrolepiota rhacodes 30.8 0.65 0.12 140 30.3 6.67 0.01 0.19 22 30.2 0.57 0.34 123 37.3 8.94 0.01 0.42 23 8.61 0.81 0.16 117 22.0 6.39 ND 0.23 24 Macrolepiota procera 2.57 0.64 0.70 203 27.2 129 0.02 0.20 25 2.07 0.73 0.41 205 9.43 1.58 0.02 0.69 26 27 2.84 0.60 0.34 226 53.0 1.71 0.02 0.11 28 4.68 3.66 8.27 238 10.5 5.39 0.02 0.52 29 1.45 2.98 0.40 188 18.4 2.02 0.01 0.25 30 4.48 2.03 0.89 269 24.3 151 0.01 0.53 31 Suillus grevillei 3.21 1.83 0.12 25.1 795 0.77 0.01 0.72 32 0.16 0.38 0.12 14.8 130 0.40 0.01 0.09 33 Suillus granulatus 0.40 0.31 0.06 37.4 318 1.67 0.03 0.33 34 1.02 10.2 1.02 60.6 248 61.2 0.01 1.66 35 Leccinum scabrum 1.21 0.64 0.15 22.0 179 2.02 0.01 0.40 36 1.44 0.55 0.09 29.6 173 0.30 0.02 0.10 37 Boletus erythropus 0.79 1.41 0.06 24.0 206 1.82 0.03 0.07 38 39 0.86 0.55 0.06 23.7 308 1.87 0.06 0.31 40 Boletus aestivalis 1.85 1.24 0.10 25.2 341 7.36 0.16 0.09 41 3.48 1.32 0.46 33.6 318 8.42 0.24 0.15 42 0.51 2.17 0.28 60.4 67.2 0.62 0.01 0.61 43 1.96 0.23 0.06 15.1 145 7.79 0.19 0.04 44 1.40 0.08 0.25 14.4 161 40.9 0.11 0.04 45 5.32 1.67 0.62 53.4 868 15.1 0.64 0.16 46 Boletus edulis 1.48 0.88 0.90 22.0 489 6.84 0.04 0.13 47 2.62 1.59 0.20 52.1 341 13.5 0.05 0.11 48 1.68 0.53 0.10 24.9 216 3.99 0.11 0.15 49 2.17 0.79 0.16 36.1 304 9.92 0.07 0.14 50 51 7.34 2.62 0.18 84.7 574 21.0 0.74 0.38 52 53 54 55 56 57 58 59 60 Table I continued

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1 2 3 4 Xerocomus badius 0.49 1.54 0.25 30.6 452 0.75 ND 0.41 5 6 0.59 4.42 0.42 51.7 102 0.70 0.01 0.71 7 0.39 2.39 0.26 53.0 316 2.24 0.20 0.09 8 0.82 0.71 0.09 32.9 294 2.06 0.09 0.08 9 0.87 0.87 0.03 61.1 344 2.25 0.02 0.09 10 0.53 3.07 0.40 65.1 510 63.6 0.09 0.11 11 Xerocomus subtomentosus 0.43 1.26 0.04 17.2 112 ND 0.03 0.08 12 0.49 0.99 0.32 31.0 152 3.44 0.04 0.12 13 0.23 0.44 0.59 24.2 42.0 2.49 0.01 0.06 14 0.53 1.72 0.11 15.1 87.3 2.52 0.02 0.33 15 0.35 1.25 0.09 18.3 104 2.50 0.02 0.39 16 For Peer Review Only 1.57 4.75 0.24 93.0 205 7.27 0.03 0.25 17 18 Xerocomus chrysenteron 24.3 21.1 3.25 451 3009 3.00 0.71 1.12 19 2.66 1.18 0.08 30.8 82.9 ND 0.02 0.09 20 1.16 1.91 0.56 69.4 81.3 3.47 0.01 0.06 21 1.87 2.16 0.53 37.3 279 7.3 0.04 0.15 22 1.75 1.14 0.24 35.8 139 0.495 0.04 0.60 23 1.12 0.53 0.13 34.5 165 0.235 0.01 0.05 24 5.09 9.17 1.04 502 160 11.9 0.02 0.68 25 Russula cyanoxantha 0.21 1.29 0.29 25.2 36.9 ND 0.01 0.09 26 0.27 2.50 0.73 39.0 33.0 0.38 ND 0.08 27 0.13 1.62 0.81 51.3 128 1.60 0.01 0.07 28 0.31 1.72 1.11 42.8 64.7 119 ND 0.09 29 30 0.28 5.58 0.65 33.0 160 0.33 0.01 1.22 31 0.20 3.10 0.66 38.3 90.6 0.36 0.02 0.72 32 0.41 5.37 1.81 53.6 148 0.53 0.01 0.83 33 Russula aeruginea 0.10 2.89 0.73 64.0 65.9 8.00 ND 0.05 34 0.22 1.15 0.69 38.9 211 0.93 0.06 0.10 35 Lycoperdon perlatum 3.02 2.86 0.21 177 11.9 151 0.02 0.27 36 2.97 1.02 0.42 132 16.9 15.6 0.01 0.14 37 3.68 3.11 0.07 108 11.3 1.94 0.01 0.39 38 3.61 1.05 0.21 202 22.1 10.2 0.01 0.45 39 27.6 0.72 0.07 220 12.9 3.18 0.02 0.50 40 4.32 2.57 0.98 53.9 25.5 5.24 0.01 0.52 41 42 1.40 1.28 0.09 23.0 237 2.95 0.02 0.65 43 6.03 6.93 0.49 310 22.7 75.0 0.01 0.39 44 Lycoperdon gigantea 4.66 0.82 0.08 41.3 1.88 10.6 0.01 0.29 45 8.14 5.02 2.09 252 11.2 315 0.02 1.07 46 Bold face type is used for marking of outlying values (Grubbs ‘ test ) 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Table II. Basic statistical characteristics of the trace element contents (mg kg -1 dry 4 5 matter) of all analysed samples. 6 7 As Ba Co Cu Rb Ag Tl V 8 n 77 77 77 76 77 77 76 77 9 x 3.35 2.15 0.45 74.7 174 14.4 0.05 0.34 10 Sx 6.19 2.02 0.52 70.6 179 32.3 0.09 0.29 11 RSD (%) 185 94.3 115 94.5 103 224 194 87.1 12 Median 1.45 1.41 0.28 47.0 130 2.95 0.02 0.25 13 x min 0.01 0.08 0.02 14.4 1.88 ND ND 0.04 14 x max 30.8 10.2 3.25 310 868 151 0.64 1.22 15 st 16 1 quartile For 0.49 0.73Peer 0.11 Review30.7 30.3 0.75Only 0.01 0.10 rd 17 3 quartile 3.07 2.86 0.62 91.7 278 8.94 0.04 0.50 18 n ... number of samples; x ... mean value; S x ... standard deviation; RSD ... relative standard deviation 19 Outlying values identified by Grubbs´ test were not used for statistical calculations. 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Table III. II. Statistical data of trace element contents (mg kg -1 dry matter) in mushroom species with at 4 least five samples. Different letters in a column mean significant difference at P < 0.05. The letters are 5 given in alphabetical order with increasing content of the metal. Outlying values identified by Grubbs´ 6 test were not used for statistical calculations 7 8 As Ba Co Cu Rb Ag Tl V 9 Macrolepiota procera (n = 6) 10 a a a,b c a a a a 11 x 3.02 1.77 0.55 221 23.8 48.6 0.01 0.38 12 Sx 1.30 1.33 0.24 29.3 16.0 71.4 0.01 0.23 13 Median 2.71 1.38 0.41 215 21.4 3.71 0.02 0.38 14 x min 1.45 0.60 0.34 188 9.43 1.58 0.01 0.11 15 x max 4.68 3.66 0.89 269 53.0 151 0.02 0.69 16 Boletus aestivalisFor (n = 6) Peer Review Only 17 x 2.42 a 1.12 a 0.29 a 33.7 a 317 b 13.4 a 0.22 b 0.18 a 18 S 1.72 0.82 0.21 19.4 290 14.3 0.22 0.22 19 x Median 1.91 1.28 0.26 29.4 239 8.10 0.17 0.12 20 21 x min 0.51 0.08 0.06 14.4 67.2 0.62 0.01 0.04 22 x max 5.32 2.17 0.62 60.4 868 40.9 0.64 0.61 23 Boletus edulis (n = 5; n = 4 for Tl) 24 x 3.06 a 1.28 a 0.31 a 44.0 a 385 b 11.0 a 0.07 a 0.18 a 25 Sx 2.44 0.85 0.33 25.6 145 6.58 0.03 0.11 26 Median 2.17 0.88 0.18 36.1 341 9.92 0.06 0.14 27 x min 1.48 0.53 0.10 22.0 216 3.99 0.04 0.11 28 x max 7.34 2.62 0.90 84.7 574 21.0 0.11 0.38 29 Xerocomus badius (n = 6) 30 a a a a b a a a 31 x 0.61 2.17 0.24 49.1 336 11.9 0.07 0.25 32 Sx 0.19 1.42 0.16 14.4 142 25.3 0.08 0.26 33 Median 0.56 1.97 0.26 52.3 330 2.15 0.06 0.10 34 x min 0.39 0.71 0.03 30.6 102 0.70 ND 0.08 35 x max 0.87 4.42 0.42 65.1 510 63.6 0.20 0.71 36 Xerocomus subtomentosus (n = 6) 37 a a a a a a a a x 0.60 1.73 0.23 33.1 117 3.04 0.02 0.21 38 39 Sx 0.49 1.54 0.21 29.9 56.0 2.37 0.01 0.14 40 Median 0.46 1.25 0.17 21.2 108 2.51 0.02 0.18 41 x min 0.23 0.44 0.04 15.1 42.0 ND 0.01 0.06 42 x max 1.57 4.75 0.59 93.0 205 7.27 0.04 0.39 43 Xerocomus chrysenteron (n = 7; n = 6 for Ba,Rb; n = 5 for Cu ) 44 x 5.42 a 2.68 a 0.83 a 41.6 a 151 a 3.77 a 0.02 a 0.39 a 45 Sx 8.43 3.23 1.12 15.8 72.5 4.40 0.01 0.41 46 Median 1.87 1.55 0.53 35.8 149 3.00 0.02 0.15 47 x min 1.12 0.53 0.08 30.8 81.3 ND 0.01 0.05 48 x max 24.3 9.17 3.25 69.4 279 11.9 0.04 1.12 49 50 Russula cyanoxantha (n=7) a a b a a a a a 51 x 0.26 3.03 0.87 40.4 94.6 17.5 0.01 0.44 52 Sx 0.09 1.78 0.48 9.91 52.2 44.9 0.01 0.48 53 Median 0.27 2.50 0.73 39.0 90.6 0.38 0.01 0.10 54 x min 0.13 1.29 0.29 25.2 33.0 ND ND 0.07 55 x max 0.41 5.58 1.81 53.6 160 119 0.02 1.22 56 Lycoperdon perlatum (n=8) 57 x 6.58 a 2.44 a 0.32 a 153 b 45.0 a 33.1 a 0.01 a 0.41 a 58 59 Sx 8.59 2.04 0.31 93.6 77.8 53.4 0.01 0.16 60 Median 3.64 1.92 0.21 155 19.5 7.69 0.01 0.42 x min 1.40 0.72 0.07 23.0 11.3 1.94 0.01 0.14 x max 27.6 6.93 0.98 310 237 151 0.02 0.65

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1 2 3 Outlying values identified by Grubbs´ test were not used for statistical calculations. 4 5 6 7 8 9 10 11 12 13 14 15 16 For Peer Review Only 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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