Food Additives and Contaminants , 2001, Vol. 18, No.

6, 503 513

ICP/ MS and ICP/ AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland
Jerzy Falandysz{*, Katarzyna Szymczyk{{ , Hideki Ichihashi{, Leszek Bielawski{, Magdalena Gucia{, Aneta Frankowska{ and Shin-Ichi Yamasaki}
{ Department of Environmental Chemistry and Ecotoxicology, University of Gdan sk, 18 Sobieskiego Str., PL 80-952 Gdan sk, Poland; { National Research Institute of Fisheries and Environment of Inland Sea, Division of Environment Conservation, Hydrochemistry Section, Maruishi 2-17-5, Ohno-cho, Hiroshima, 739-0452, Japan; } Faculty of Agriculture, Tohoku University, Sendai, Japan

(Received 13 June 2000; revised 27 November 2000; accepted 4 December 2000)

Thirty-eight elements, including toxic cadmium, lead, mercury, silver and thallium, were determined in 18 species of wild edible mushrooms collected from several sites in Pomorskie Voivodeship in northern Poland in 1994. Elements were determined by double focused high resolution inductively coupled plasma mass spectrometry (HR-ICP-MS) and inductively coupled plasma atomic emission spectroscopy (ICP-AES), after wet digestion of the dried samples with concentrated nitric acid in closed PTFE vessels using a microwave oven. K, P and Mg were present at levels of mg/g dry matter; Na, Zn, Ca, Fe, Cu, Mn, Rb, Ag, Cd, Hg, Pb, Cs, Sr, Al and Si were present at mg/g levels, while Tl, In, Bi, Th, U, Ce, Pr, Nd, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, La, Lu and Ba were present at ng/g levels. Keywords : elements, heavy metals, toxic metals, HRICP-MS, ICP-AES, mushrooms, fungi, food

utilized world-wide and which need a full evaluation of their elemental composition, taking into account their essentiality, non-essentiality and toxicity. Because of ecological and genetic but poorly known factors, the fruiting bodies of higher mushrooms are often relatively rich in mineral constituents (Schmitt et al. 1977, Varo et al. 1980, Vetter 1990). The content of the highly toxic elements such as mercury, cadmium and lead in many wild edible mushroom species collected from background (unpolluted) sites is frequently much higher than that in other plant food items (Quinche 1987, Vetter 1993). In the case of wild edible species collected from sites close to sources of pollution with various metallic elements (city lawns and parks, roadside areas, and industrial sites, etc.), concentrations of both toxic and essential elements are usually elevated (Kuusi et al. 1981, Leps ova and Kral 1988, Kalac et al. 1996, Garcia et al. 1998), thus the mushrooms are un t for human consumption. Also, if grown in contaminated substrate, cultivated mushrooms can e ectively take up and bioacummulate toxic elements at great concentrations in their fruiting bodies (Bressa et al. 1988, Falandysz et al. 1994a). Some mushroom species are described as hyper-accumulators of certain elements. The Variegated Bolete (Suillus variegatus (Swartz: Fr.) O. Kuntze) is known for accumulating very high levels of iron and Fly Agaric (Amanita muscaria (L. ex Fr.) Hooker) is known to accumulate vanadium, which is present as an organovanadiu m compound called amavadin (Kneifel and Bayer 1973). Because of the ephemeral existence of the fruiting bodies of higher mushrooms, the substrate colonized by the mycelium usually is the only source of absorbed, translocated and accumulated elements while in areas with high air pollution external contamination with adsorbed mineral particulate matter at the surface can have also some in uence. There are several environmental or species-dependent physiological factors which determine the metallic and metalloid element content of the fruiting bodies (Mejstrik and Leps ova 1993, Wondratschek and Roder 1993). In the case of mycorrhizal mushrooms an e ective

Introduction
The world of fungi represents a diverse group of organisms and is extremely rich in species diversity. There are plenty of wild edible mushrooms which are
* To whom correspondence should be addressed. e-mail: jfalandy@ chemik.chem.univ.gda.pl { Present address: University of Warmia and Mazury, Olsztyn, Poland.

Food Additives and Contaminant s ISSN 0265 203X print/ISSN 1464 5122 online # 2001 Taylor & Francis Ltd http://www.tandf.co.uk/journals DOI: 10.1080/0265203001002762 4

504

J. Falandysz et al.

`absorbing device is the mycelium which has a dense interlacement of hyphae, characterized by a large surface (high surface to volume ratio) and growths up to 50 cm deep in soil which can cover an area up to 100 m2 (Mutsch et al. 1979); sometimes this mycelium has a life span of more than 100 years. Cadmium is known to promote the growth of mycelium of Agaricus abruptibulbu s (Peck) Kau mann (Meisch et al. 1981) under laboratory conditions. In a study by Turnau (1991), cadmium dust (3.02% CdO, 1.75% ZnO, 4.07% PbO, 21.83% Al2 O3 , 5.65% CaO and 45.5% SiO2 ) added at a low rate (up to 100 mg/l) to substrate medium stimulated the mycelium growth of Armillaria lutea Gillet and Auriscalpiu m vulgare S. F. Gray under laboratory conditions. Under eld conditions an increased dosage of the aforementioned mineral dust to the plots in a pino-quercetum forest resulted in increased yield of some species of higher mushrooms. The bioavailabilit y of many mineral constituents of the higher mushrooms when ingested by man as well as the impact of di erent cooking methods or similar processes on the elemental content of the nal food products or dish remains open to question. Collection and consumption of wild edible mushrooms has a long tradition in Poland and even today is extremely popular both among villagers and citizens.

Slippery Jack (Suillus luteus (L.) S.F. Gray), European Cow Bolete (Suillus bovinus (L.) O. Kuntze), Variegated Bolete (Suillus variegatus (Swartz: Fr.) O. Kuntze), Bay Bolete (Xerocomus badius (Fr.) Kuhn. ex Gilb.), Red-cracking Bolete (Xerecomus chrysenteron (Bull.) Quel.), King Bolete or Cep (Boletus edulis Bull.: Fr.), Orange Birch Bolete (Leccinum versipelle (Fr.) Snell), Hard Bolete (Leccinum griseum (Quel.) Sing.), Brown Birch Scaber Stalk (Leccinum scabrum (Bull.: Fr.) S.F. Gray), Amethyst Deceiver (Laccaria amethistina (Bolt.) Murr.), Blue Legs (Lepista saeva (Fr.) P.D. Orton), Sandy Knight-cap (Tricholoma avovirens (Pers.: Fr.) Lund. et Nannf.), Honey Mushroom (Armillariella mellea (Vahl.: Fr.) P. Karts.), Meadow Mushroom (Agaricus campestris L.), Parasol Mushroom (Macrolepiota procera (Scop.: Fr.) Sing.) and Sa Milk Cap (Lactarius deliciosus (L.) S.F. ron Gray) were collected for examination.

Analysis
Individual specimens of the fruiting bodies were cleaned-up for substrate debris with a plastic knife, cut into small pieces if necessary and air-dried for several days. After that the samples were further dried in an oven at 408C for 48 h, pooled, if necessary, and then pulverized in the agate mortar. Dried and pulverized mushroom samples (the caps) were digested in closed vessels made of polytetra uoroethylene (PTFE) in an Automatic Microwave Digestion System (MLS 1200) using concentrated nitric acid (5 ml). All reagents used were of analytical grade. Nitric acid used for the preparation of nal solution for HR-ICP-MS was of super analytical grade (Kanto Chemical Co. Inc., Elgrade 1.38, Japan). Double distilled water was used to prepare solutions. The analysis was performed in ultra clean conditions (laboratory class 100, clean cabin class 1000). Indium (100 pg In/cm3 ) was the internal standard used. Inductively Coupled Plasma Atomic Emission Spectrometry (ICP-AES; Maxim-III, Applied Research Laboratories, Switzerland) was used for the determination of Al, Ca, K, Mg, Na, P and Si, and Double-focused High Resolution Inductively Coupled Plasma Mass Spectrometry (ICP-HR-MS; PlasmaTrace, VG Elemental, Great Britain) with an ultrasonic nebulizer (USN, Applied Research Laboratories, Switzerland) was used for the determination of the other 30 elements. Indium was used as

Materials and methods

The fruiting bodies of 18 species of wild edible mushrooms were collected at the sites: Buszkowy Gorne, _ Debki, Zarnowiec and ubiana (Pomorskie Voievodeship) in the northern part of Poland in 1994. Eighteen species were examined for `major elements (table 1) and six species were arbitrarily selected for analysis of `minor elements (table 2).

Sampling
The mushroom samples collected in this study originated from areas away from any possible point source of pollution and were considered as unpolluted and represent background sites. Common Chantharelle or Chantharelle (Cantharellus cibarius Fr.), Horn of Plenty (Craterellus cornucopioide s (L.) Pers.),

Elemental analysis of edible wild mushrooms

505

internal standard (100 pg/ml), and the indium content in mushrooms was quanti ed using instrumental neutron activation analysis (Tokai-muru, Japan). Details of the analytical procedure used are given elsewhere (Falandysz et al. 1998). The analytical method used was validated using the National Bureau of Standards Certi ed Reference Materials (NBS CRM) such as: Apple leaves (1515), Peach leaves (1547), Citrus leaves (1572), Tomato leaves (1573) and Pine needles (1575). Also National Institute for Environmental Sciences (NIES) Primary Standards (Japan) such as Rice our (10a), Rice our (10c) and Rice grass (281) were used (Yamasaki et al. 1991, Yoshida et al. 1992, Shimamura et al. 1995). In day-by-day laboratory runs with every set of ten real mushroom samples, one sample of the certi ed reference material was digested and quanti ed together with one blank. For blank samples no major interferences were found. Discrepancies between certi ed values and concentrations quanti ed were below 5% , and the coe cient of variation for single measurements was below 10% .

their study on mushrooms collected in the southeastern part of the Jotunheimen mountain area in Norway, Bakken and Olsen (1990) reported potassium concentrations in the range between 25 and 41 mg/g dry matter, which is very similar to that in our study, nevertheless, however, di erent species were examined. The caps of Sandy Knight-cap (T. avovirens) in our study (table 1) showed the greatest concentrations of potassium, 47 83 mg/g dry matter. The concentrations of potassium in di erent anatomical parts of the wild mushrooms gathered in Austria and examined by Hedrich (1988) ranged from 6.0 to 82 mg/g dry matter. Whole fruiting bodies of Common Chantharelle (C. cibarius) in this study contained potassium in concentrations of 56 2 (54 58) mg/g, and of 49 in Austria and 45 (43 48) mg/g dry matter in Finland, while King Bolete (B. edulis) contained 34 5, 30 and 25 (24 26) mg/g dry matter, respectively (Varo et al. 1980, Hedrich 1988). Concentrations of phosphorus varied and seemed to be species-dependent with the smallest concentrations of 1.2 mg/g dry matter in Variegated Bolete (S. variegatus) and of 2.3 0.6 mg/g in Horn of Plenty (C. cornucopioides) and highest in Meadow Mushroom (A. campestris) with 20 mg/g dry matter. Whole fruiting bodies of Common Chantharelle (C. cibarius) and the caps of King Bolete (B. edulis) contained phosphorus at concentrations of 5.7 0.6 and 10 2 mg/g (table 1), while in the same species analysed in Finland concentrations were 5.0 (4.1 5.6) and 4.3 (4.1 4.6) mg/g, and in Hungary 4.6 and 5.5 (4.5 6.4) mg/g dry matter, respectively (Varo et al. 1980, Vetter 1990). Magnesium was found at similar concentrations in nearly all of the mushroom species sampled in this study and the range was from 0.6 to 2.5 mg/g dry matter. Similar magnesium concentrations were reported in mushrooms investigated by Bakken and Olsen (1990), and the values in those species ranged between 0.78 and 1.2 mg/g dry matter. In studies by Varo et al. (1980) and Hedrich (1988) magnesium was quanti ed in Common Chantharelle (C. cibarius) and King Bolete (B. edulis) at concentrations of 1.0 (0.9 1.1) and 0.62 (0.59 0.66) in Finland, and 1.3 and 0.74 mg/g dry matter (stalk and cap without the tubes) in Austria, respectively, while the results of our study showed 1.2 0.1 and 1.1 0.1 mg/g dry matter (table 1). Sodium and calcium are much less abundant in higher mushrooms than potassium or phosphorus (table 1). Several species are relatively rich in sodium, namely

Results and discussion

The available data on mineral element composition of wild edible mushrooms gathered from the territory of Poland and also of cultivated Champignon (Agaricus bisporus) and Common Oyster (Pleurotus ostreatus) relate to 22 elements and ve radionuclides (Falandysz and Frankowska 2000). In this paper we present data on the concentrations of up to 38 elements in edible mushrooms of Poland, including those examined earlier. Mean concentrations of K, P, Mg, Na, Zn, Ca, Fe, Cu and Mn in the caps or whole fruiting bodies of 18 species of mushrooms, and of Rb, Ag, Cd, Hg, Pb, Cs, Sr, Tl, In, Bi, Th, U, Ce, Pr, Nd, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, La and Lu in six species are presented in tables 1 and 2, respectively, where samples numbers (n), standard deviations and ranges of concentrations are also indicated. A few data on the concentrations of Al, Ba, and Si in the caps of a small number of mushroom species are cited in the text. Potassium was the most abundant amongst the elements quanti ed and the range of the mean values was between 26 5 and 70 20 mg/g dry matter. In

506

Table 1.
n 3a;b 56 2 54 58 50 4 46 53 39 4 35 43 26 5 22 32 35 5 31 41 43 2 41 45 43 3 41 46 34 5 27 39 27 8.3 1.5 7.0 10. 9.3 0.6 9.0 10. 10 2 8.0 12. 9.0 1.2 0. 1.2 1.2 1.3 0.1 1.2 1.4 1.1 0.1 1.0 1.2 1.0 0.1 1.0 1.1 1.1 0.1 1.0 1.2 1.3 6.7 0.6 6.0 7.0 0.93 0.12 0.80 1.0 8.7 1.5 7.0 10. 1.2 0.1 1.1 1.3 55 22 42 81 920 250 730 1200 40 10 30 50 470 70 400 540 70 2.3 0.6 2.0 3.0 0.7 0.1 0.6 0.8 53 15 40 70 100 15 90 120 160 30 130 190 87 15 70 100 150 10 140 160 180 90 120 280 80 10 70 90 180 78 120 290 NA 290 110 150 420 240 5.7 0.6 5.0 6.0 1.2 0.1 1.1 1.2 83 51 40 140 100 10 90 110 K (mg/g) P (mg/g) Mg (mg/g) Na (mg/g) Zn (mg/g) Ca (mg/g) 340 130 190 430 560 69 510 640 60 12 46 69 94 55 31 130 98 24 71 120 30 13 19 44 18 10 9.0 28. 39 20 11 55 25

Concentrations of elements in dried fruiting bodies of selected wild edible mushrooms from northern Poland.
Fe (mg/g) 140 40 100 180 260 210 80 490 NA Cu (mg/g) NA Mn (mg/g) 30 9 22 40 26 56 19 35 71 27 5 22 30 53 15 40 70 3600 510 3300 4100 33 6 30 40 NA NA 14 7 6.4 19. NA

Species, site and year

Common Chantharelle Cantharellus cibarius Buszkowy Gorne, 1994 3a;b

Horn of Plenty Craterellus cornucopioides Buszkowy Gorne, 1994 3

J. Falandysz et al.

Slippery Jack Suillus luteus Buszkowy Gorne, 1994 3

European Cow Bolete Suillus bovinus Debki, 1994 3

Variegated Bolete Suillus variegatus Debki, 1994 3

34

14 2 13 16 82 10 75 89 NA 16 12 8.3 29. NA

Bay Bolete Xerocomus badius Buszkowy Gorne, 1994 3

Red-cracking Bolete Xerecomus chrysenteron Debki, 1994 4

King Bolete Boletus edulis Buszkowy Gorne, 1994 1

50 18 30 70 NA

62 10 50 74 84

9.6 2.9 5.7 12. NA

Orange Birch Bolete Leccinum versipelle Buszkowy Gorne, 1994

Hard Bolete Leccinum griseum _ Zarnowiec, 1994 3 40 3 38 43 51 7 46 59 54 50 57 70 20 47 83 53 2 51 55 59 42 76 28 3 25 31 33 7 27 41 8.3 1.5 7.0 10. 1.2 0.2 1.1 1.4 490 50 920 12 1 12 13 1.4 0. 1.4 1.4 69 46 39 120 90 10 80 100 180 57 120 230 20 15 25 2.3 2.0 2.5 NA 210 140 280 9.0 0.9 8.0 10. 1.5 0.2 1.3 1.7 70 36 35 120 75 22 50 110 78 13 61 100 50 56 60 60 50 70 590 580 220 1300 8.3 1.2 7.0 9.0 1.4 0.1 1.3 1.5 60 14 44 70 460 25 430 480 150 25 130 180 43 6 40 50 120 42 80 200 NA 25 23 27 2.1 1.9 2.3 170 110 240 150 140 160 55 50 60 90 80 100 6.7 0.6 6.0 7.0 1.3 0.1 1.2 1.4 360 80 160 520 110 40 70 150 46 18 30 65 83 15 70 100 75 28 45 100 120 120 120 55 16 40 72 NA 7.7 0.6 7.0 8.0 1.2 0.1 1.1 1.4 290 180 180 500 220 60 160 280 71 11 62 84 20 14 10 30 NA 12 6 7.8 17. 34 8 28 44 88 70 110 36 6 31 42 19 3 16 23 240 180 300 80 10 70 90 50 44 20 100 130 39 83 160 NA 16

40 0 40 40

7.3 4.6 2.0 10.

1.2 0. 1.2 1.2

830 510 280 1300

150 29 130 180

38 12 28 51

30 30 30

NA

Brown Birch Scaber Stalk Leccinum scabrum Buszkowy Gorne, 1994 3a;b

Amethyst Deceiver Laccaria amethistina Buszkowy Gorne, 1994 2

Blue Legs Lepista saeva Buszkowy Gorne, 1994 3

Sandy Knight-cap Tricholoma avovirens Buszkowy Gorne, 1994 6

Honey Mushroom Armillariella mellea Buszkowy Gorne, 1994 2

Meadow Mushroom Agaricus campestris Buszkowy Gorne, 1994 3

Parasol Mushroom Macrolepiota procera Buszkowy Gorne, 1994 3

14

Sa Milk Cap ron Lactarius deliciosus County of ubiana, 1994

10 5 5.0 15.

Elemental analysis of edible wild mushrooms

Whole fruiting bodies were analysed, otherwise only the caps. Number of pooled samples (number of individuals per sample was 5 for L. amethistina and 10 for C. cornucopioides and C. cibarius). NA, not analysed.

507

508

Table 2.

Elements in dried fruiting bodies of selected wild edible mushrooms from northern Poland.

Element 880 130 730 970 0.22 0.08 0.13 0.27 0.57 0.36 0.28 0.97 0.26 0.02 0.25 0.28 0.54 0.31 0.25 0.87 3.1 0.8 2.2 3.8 0.41 0.25 0.12 0.60 43 39 20 88 2.2 0.4 1.7 2.4 1.6 0.8 0.80 2.4 5.9 6.7 1.7 14. 2.7 2.6 0.80 5.6 1.1 1.1 0.36 2.7 0.23 0.12 0.06 0.33 27 12 16 44 3.2 1.2 1.6 4.6 1.2 0.6 0.8 1.9 4.0 2.3 1.6 6.5 9.7 1.2 8.2 11. 1.2 0.8 0.25 2.2 5.5 1.9 3.9 8.2 12 3 8.5 14. 0.68 0.21 0.44 0.83 0.19 0.08 0.11 0.27 1.2 0.9 0.61 2.2 0.79 0.40 0.34 1.1 1.6 0.7 0.83 2.3 59 42 23 110 2.7 0.8 2.0 3.5 2.6 0.8 1.7 3.3 9.9 3.4 6.0 12. 4.0 1.2 2.7 5.0 22 7 13 29 0.26 0.10 0.19 0.38 240 45 190 280 610 470 290 1300 290 120 170 410

Slippery Jack (Suillus luteus) n 3

European Cow Bolete (Suillus bovinus) n 3

King Bolete (Boletus edulis) n 4

Amethyst Deceiver (Laccaria amethystina) a n 3 5

Sandy Knight-cap (Tricholoma avovirens) n 3 2000 680 1200 2500 3.5 0.4 3.2 4.0 1.5 0.2 1.4 1.8 0.94 0.74 0.09 1.4 0.67 0.58 0.07 1.2 9.5 2.6 6.5 11. 0.85 0.22 0.68 1.1 100 85 6.0 170. 5.9 2.2 3.5 7.8 2.3 3.7 3.6 0.80 7.8 2.1 0.4 1.8 2.3

Honey Mushroom (Armillariella mellea) a n 6 10 66 17 53 100 0.87 0.43 0.41 1.4 10 5 6.4 20. 0.20 0.03 0.16 0.25 0.80 0.83 0.24 2.4 0.952 0.012 0.040 0.070 0.39 0.16 0.25 0.61 15 3 11 20 2.4 0.5 1.8 2.8 1.5 0.6 0.90 2.4 25 25 4.7 75. 5.9 5.6 1.8 17.

Rb (mg/g)

Ag

0.89 0.55 0.44 1.5

J. Falandysz et al.

Cd

0.56 0.16 0.38 0.67

Hg 1.3 0.2 1.1 1.5 20 5 15 24

0-34 0.05 0.29 0.38

Pb

Cs

Sr 63 75 19 150 2.5 1.0 1.9 3.7

0.23 0.06 0.16 0.28

Tl (ng/g)

In

Bi 2.1 0.9 1.3 3.0

0.93 0.49 0.60 1.5

Th

1.1 0.5 0.701.4

Ce 1.7 0.6 1.0 2.0 6.7 2.3 4.0 8.0 2.0 1.0 1.0 3.0 0.80 0.80 0.80 6.2 6.5 1.7 14. 0.80 0.80 0.80 3.8 3.7 1.6 8.1 3.2 2.8 2.8 0.80 4.8 0.80 4.1 3.5 1.6 6.5 19 23 5.0 46. 0.80 NA 27 14 16 47 2.2 1.2 0.80 3.7 0.90 0.90 1.1 0.6 0.70 1.7 21 5 15 25 1.2 0.70 1.7 2.9 1.5 1.7 4.6 1.5 0.6 0.90 2.0 1.5 1.2 0.802.8 1.7 3.7 2.5 2.4 7.4 3.5 1.5 2.5 5.2 1.3 0.6 0.80 1.9 0.80 0.10 0.70 0.90 0.83 0.06 0.80 0.90 4.6 1.6 3.5 6.5 0.80 1.9 1.2 0.80 3.1 0.80 1.7 1.3 0.80 2.6 11 5 7.0 16. 0.85 0.80 0.90 8.1 3.5 4.7 12. 5.0 3.0 2.6 4.0 2.8 1.7 0.80 4.0 1.9 0.6 1.6 2.8 1.6 0.2 1.3 1.7 1.6 0.90 2.3 5.0 5.2 2.0 11. 7.3 4.2 4.0 12. 4.0 1.0 3.0 5.0 4.7 4.6 2.0 10. 20 22 5.0 45. 23 12 14 40 14 9 7.0 24. 10 4 8.0 14. 67 62 10 180 14 11 3.0 33. 2.2 1.6 0.90 5.3 9.5 11.0 1.6 31. 1.6 1.1 0.60 3.6 9.9 5.3 1.2 17. 1.6 0.8 0.60 2.4 4.5 2.7 1.2 8.9 0.80 0.14 0.600.90 3.4 3.3 0.60 8.0 70 58 11 180 1.2 0.80 1.8 5.0 6.1 1.0 12. 6.5 39 3.0 12. 58 4 54 61 19 16 1.0 31. 17 14 2.0 43.

9.3 4.7 4.0 13.

42 56 7.0 110.

56 25 33 92

46 12 33 55

21 12 11 35

160 140 22 400

Pr

Nd

Sm

Eu 1.4 0.8 0.70 2.2 NA 1.1 0.5 0.70 1.4 0.70

0.67 0.06 0.60 0.70

Gd

Tb

Dy

Ho

Er 0.70 0.70 5.3 2.5 3.08.0 0.70

0.65 0.07 0.60 0.70

Tm

Yb

Elemental analysis of edible wild mushrooms

La

Lu

Number of pooled samples and number of specimens per sample. NA, not analysed.

509

510

J. Falandysz et al.

European Cow Bolete (S. bovinus) with 920 250 mg/g dry matter and Hard Bolete (L. griseum; L. duriusculum) with 830 510 mg/kg, whereas many others contain below 500 mg/g or much less. The four elements zinc, iron, copper and manganese are essential in human nutrition and were quanti ed in wild edible mushrooms; zinc was found to be the most abundant. Sandy Knight-cap (T. avovirens) with 460 25 mg/g and King Bolete (B. edulis) (290 110 mg/g) and Brown Birch Scaber Stalk (Common Scaber Stalk; L. scabrum), (220 60 mg/g) were richer in zinc than the other species (table 1). In the case of iron, Variegated Bolete (S. variegatus) contained the highest concentration, 3600 510 mg/g dry matter. The Variegated Bolete samples originated from a pine forest at the Debki site near the beach of the Baltic south coast. The same species collected from the background sites in the Augustowska Forest in north-eastern Poland in 1998 contained iron in the caps in concentrations of 1900 790 mg/g dry matter (Falandysz et al. 2000), while in a study conducted in Austria by Mutsch et al. (1979) 1700 mg Fe/g dry matter was found. It is interesting to note that iron-rich Variegated Bolete and Horn of Plenty (C. cornucopioide s) had a low phosphorus content and vice versa for the others species investigated (table 1). Copper concentrations varied depending on the mushroom species, with a range from 27 5 mg/g in the caps of Slippery Jack (S. luteus) to 240 mg/g in Meadow Mushroom (A. campestris). The King Bolete (B. edulis) in its caps contained copper concentrations of 62 10 mg/g (table 1). Studies by other authors have found that the concentrations of copper in whole fruiting bodies of King Bolete gathered at unpolluted sites were: 23 51 mg/g (Tyler 1980), 21 (20 21) mg/g (Varo et al. 1980), and 23 mg/g in stalk and cap without tubes, and 58 mg/g dry matter in tubes (Hedrich 1988). On the other hand the fruiting bodies of King Bolete collected in the vicinity of a lead smelter and a copper smelter in Bohemia contained greater concentrations of copper when compared with those originating from an unpolluted site, i.e. 52 35, 66 24 and 27 16 mg/g, respectively (Kalac et al. 1991, 1996). As mentioned earlier, the fruiting bodies of King Bolete were gathered from the site far away from any point source of pollution. The concentrations of copper in King Bolete in this study are elevated when compared with those found in specimens collected

from the background sites elsewhere (Varo et al. 1980, Hedrich 1988, Kalac et al. 1991, 1996), and are similar to those reported in specimens taken in the vicinity of a lead smelter and a copper smelter mentioned above. As regards manganese, Blue Legs (L. saeva) contained the greatest concentration with 88 mg/g (70 110) followed by Horn of Plenty (C. cornucopioide s) with 56 19 mg/g dry matter. Other species contained smaller concentrations (table 1). In studies by Schmitt et al. (1977), Mutsch et al. (1979), Varo et al. (1980) and Hedrich (1988), the concentrations of manganese reported in King Bolete (B. edulis) were similar, 27, 6 12, 16 (14 17) and 13 mg/g dry matter repectively, and in Common Chantharelle (C. cibarius) concentrations were 30, 21 59, 28 (25 32) and 50 mg/g dry matter respectively, while in this study they were 9.6 2.9 and 30 9 in mg/g dry matter respectively for the two species. Rubidium is one of the most abundant of the elements studied (table 2), and frequently is even more abundant than sodium, zinc, calcium, iron, copper or manganese (table 1). The concentrations of rubidium in ve species of the soil mushrooms described in table 2 are one or two orders of magnitude greater than of wood-decomposing species such as Honey Mushroom (A. mellea). The data on the concentrations of rubidium in the caps of ve species of the soil mushrooms in this study are similar to the values presented by Bakken and Olsen (1990). These authors found that in whole fruiting bodies of ten other species of soil mushrooms collected in Norway the rubidium concentration varied between 120 and 290 mg/g dry matter, while Varo et al. (1980) quanti ed this element in ve species of wild soil mushrooms and found values in the range between 130 and 890 mg/g dry matter, while in inedible False Morel (Gyromitra esculenta (Pers.: Fr.) Fr.) the amount ranged from 300 to 350 mg/g dry matter. There are plenty of data available in the scienti c literature on the concentrations of toxic lead, cadmium and mercury, and much less information on toxic silver or thallium in various species of wild edible mushrooms from many areas of the world. Lead was present in relatively small concentrations in all six species investigated, i.e. between 0.54 0.31 and 1.3 0.2 mg/g dry matter (total range from 0.07 to 2.4 mg/g). These values of lead content are similar to those quanti ed in the same species collected from background sites elsewhere in Europe (Seeger 1976, Varo et al. 1980, Lodenius et al. 1981). In the case

Elemental analysis of edible wild mushrooms

511

of cadmium and mercury the caps of King Bolete (B. edulis) contained greater concentrations than other species (table 2). Nevertheless, the concentrations noted in this study are within the range of the values reported for the same species from unpolluted sites in Germany (Seeger 1976), Bohemia (Kalac et al. 1991, 1996), Hungary (Vetter 1997) or Finland (Lodenius et al. 1981). Silver concentration was greatest in the caps of King Bolete, i.e. 22 7 mg/g, while it was present at levels <4.0 mg/g dry matter in other species of mushrooms (table 2). The concentrations of silver in the caps of King Bolete are somewhat greater than usually reported for this species by other authors but are similar for the Honey Mushroom (A. mellea) as reviewed by Falandysz et al. (1994b). The thallium content of higher wild mushrooms was extensively studied by Seeger and Gross (1981) but due to the low detection limit of 250 ng/g dry matter it remained undetected in most of the samples examined by these authors. In this study thallium was quanti ed in all samples and the soil mushrooms showed greater concentrations than those growing on wood, i.e. the Honey Mushroom (A. mellea), with values of from 27 12 to 100 85 and 15 3 ng/g, respectively, and the smallest concentration quanti ed was 6.0 ng/g dry matter. Also all ten species of mushrooms examined by Bakken and Olsen (1990) contained detectable amounts of thallium, and two of them, namely Tricholoma album with 1700 ng/g and Silver Violet Cort (Cortinarius alboviolaceu s (Fr.) Fr.) with 850 ng/g dry matter were especially rich in thallium. Concentrations of bismuth were in the range between 0.60 and 3.3 ng/g dry matter, which is of the same order of magnitude as reported in higher plants (Kabata-Pendias and Pendias 1999). Apart from the data given in table 2 strontium was also quanti ed in a few other species, and the concentrations were of 1.4 mg/g dry matter in Horn of Plenty (C. cornucopioides) (n 1); 3.5 mg/g in Sa ron Milk Cap (L. deliciosus) (n 1) and 1.0 mg/g in Blue Legs (L. saeva) (n 20). Aluminium, barium and silicon were quanti ed only in a few samples. The concentrations of aluminium were 140 mg/g dry matter in Common Chantharelle (C. cibarius), and 140 mg/g in Honey Mushroom (A. mellea) and 330 mg/g in Horn of Plenty (C. cornucopipides) (n 1); and of silicon were of 120 mg/g in Sandy Knight-cap (T. avovirens) and 250 mg/g dry matter in Amethyst Deceiver (L. amethystina) (n 1). Those two elements were also quanti ed in several species of higher mushrooms in Finland by Varo et al.

(1980), and barium in samples from Norway by Bakken and Olsen (1990). Common Chantharelle and King Bolete collected in Finland contained 140 (100 230) and 72 (18 130) mg/g of aluminium, and 300 (200 500) and 360 mg/g dry matter of silicon. The concentrations of barium measured in this study were 0.40 0.05 (0.35 0.45) mg/g dry matter in Slippery Jack (S. luteus) and 0.33 0.25 (0.14 0.61) mg/g dry matter in European Cow Bolete (S. bovinus), which is somewhat lower than noted in wild mushrooms in Norway. The Silver Violet Cort (C. alboviolaceus) with 3.2 mg Ba/g dry matter seemed to be especially rich in this element amongst all the species examined to date. In some other mushrooms, concentrations of barium were between 0.39 and 1.3 mg/g (Bakken and Olsen 1990). Both as a result of this study and from analysing data available from the scienti c literature, it is evident that numerous species of wild edible mushrooms gathered at the background sites away from the anthropogenic sources of the environmental pollution are relatively rich in various elements when compared with other plant food, and specimens that have been grown in polluted soil/substrate can be extraordinarily rich at least in toxic lead, cadmium and/or mercury. The availabilit y to man of many elements contained in mushrooms when consumed remains an open question and has been discussed by some authors (Jorhem and Sundstrom 1995). Apparently, when estimating the intake rates by man of toxic elements found at high concentrations in edible mushrooms ADI (Acceptable Daily Intake) values can be exceeded and thus this suggests a need for establishing species/site/element speci c consumption levels to protect human health. Nevertheless, most of the assessments (Jorhem and Sundstrom 1995) frequently refer to raw mushrooms and the impact of cooking/ processing procedures can lead to leaching and loss of some constituents and probably also of important metallic elements, metalloids and radionuclides. The parboiling and boiling of Sandy Knight-cap (T. avovirens), Bolete (Boletus luridus), Bay Bolete (X. badius) and Yellow-cracking Bolete (X. subtomentosus) lead to up to 85% loss of the radiocaesium content in the nal product (Skibniewska and Smoczynski 1999). The metallic elements such as copper, zinc, lead, cadmium and mercury are amongst those elements of which the concentrations in many kinds of foodstu are limited by law in Poland but there is no s speci c limit for edible higher mushrooms. The toler-

512

J. Falandysz et al.
ferent phorophite substrates (in Polish). Bromatologia i Chemia Toksykologiczna, 31, 401 409.

ance limit set for fresh vegetables and dried plant food items (>50% dry matter) is 4 and 20 mg/g for copper, 10 and 50 mg/g for zinc, 0.05 and 0.10 mg/g for cadmium, 0.3 and 1.0 mg/g for lead and 0.02 and 0.03 mg/g for mercury (Monitor Polski 1993). The contents of the essential elements copper and zinc in all samples of dried mushrooms in this study exceeds the legal tolerance limit set for dried food and when considering the concentrations on a fresh weight basis (moisture content of 90% , on average), the same limit applies to most of the samples (table 1). As regards the toxic elements cadmium, mercury and lead the concentrations of these elements in the caps of the higher mushrooms in this study (table 2) frequently were too high when compared with the tolerance limits set for dried foodstu and, with the exception s of lead, the limit for fresh vegetables.

Falandysz, J., Klawikowska, K., Szymanowska, B., Bielawski, L., Danisiewicz, D., Frankowska, A., and Brzostowski, A., 2000, Trace elements in selected species of mushrooms from
the area of Augustowska Forest (in Polish). Proceedings of IX Poznan skiego Konwersatorium Analitycznego (Poland: Poznan), p. 83. Garcia, M. A., Alonso, J., Fernandez, M. I., and Melgar, M. J., 1998, Lead content in edible wild mushrooms in Northwest Spain as indicator of environmental contamination. Archives of Environmental Contaminatio n and Toxicology, 34, 330 335. Hedrich, E., 1988, Short-time activation analysis of some Austrian mushrooms. Journa l of Trace and Microprobe Techniques, 6, 583 602. Jorhem, L., and Sundstrom, B., 1995, Levels of trace elements in edible fungi. Zeitschrift fur Lebensmittel Untersuchung und Forschung, 201, 311 316. Kabata-Pendias, A., and Pendias, H., 1999, Biogeochemistry of Trace Elements (in Polish) (Warszawa: Wydawnictwo Naukowe PWN). KalaC, P., Burda, J., and StaSkova, I., 1991, Concentrations of lead, cadmium, mercury and copper in mushrooms in the vicinity of a lead smelter. Science of the Total Environment, 105, 109 119. KalaC, P., Niznanska, M., Bevilaqua, D., and Stakova, I., 1996, Concentrations of mercury, copper, cadmium and lead in fruiting bodies of edible mushrooms in the vicinity of a mercury smelter and a copper smelter. Science of the Total Environment, 177, 251 258. Kneifel, H., and Bayer, E., 1973, Strukturermittlung der Vanadiumverbinung des Fliegenpilzes. Angewandte Chemie, 85, 542 543. Kuusi, T., Laaksovirta, K., Liukkonen-Lilja, H., Lodenius, M., and Piepponen, S., 1981, Lead, cadmium, and mercury contents of fungi in the Helsinki area and in unpolluted control areas. Zeitschrift fur Lebensmittel Untersuchung und Forschung, 173, 261 267. LepSova, A., and Kral, R., 1988, Lead and cadmium in fruiting bodies of macrofungi in the vicinity of a lead smelter. Science of the Total Environment, 76, 129 138. Lodenius, M., and Herranen, M., 1981, In uence of a chlor-alkali plant on the mercury contents of fungi. Chemosphere, 10, 313 318. Lodenius, M., Kuusi, T., Laaksovirta, K., Liukkonen-Lilja, H., and Piepponen, S., 1981, Lead, cadmium and mercury contents of fungi in Mikkeli, SE Finland. Annales Botanicae Fennci, 18, 183 186. Meisch, H-U., Scholl, A-R., and Schmitt, J. A., 1981, Cadmium as a growth factor for the mushroom Agaricus abruptibulbu s (Peck) Kau mann (in German). Zeitschrift fur Naturforschun g, 36c, 765 771. Mejstrik, V., and LepSova, A., 1993, Applicability of fungi to the monitoring of environmental pollution by heavy metals. Plants as biomonitors. Indicators for Heavy Metals in the Terrestrial Environment, edited by B. Markert (Veinheim: VCH Verlagsgesellschaft), pp. 365 378. Monitor Polski, 1993, No. 22, May 11, position 233. Mutsch, F., Horak, O., and Kinzel, H., 1979, Trace elements in higher fungi (in German). Zeitschrift fur P anzenphysiologi e, 94, 1 10. Quinche, J-P., 1987, Le cadmium, un element present en traces dans les sols, les plantes et les champignons. Revue Suisse Agriculturae, 19, 71 77. Schmitt, J. A., Meisch, H.-U., and Reinle, W., 1977, Heavy metals in higher fungi, II Manganese and iron (in German). Zeitschrift fur Naturforschun g, 32c, 712 723.

Acknowledgements
The authors would like to thank to Dr K. Kannan (National Food Safety & Toxicology Center, Michigan State University, East Lansing, Michigan, USA) for critical reading of the manuscript and nancial support from the Polish State Committee of Scienti c Research (KBN) under Grant Nos 1254/ P04/2000/19 and DS/8250-4-0092-01 and under the Scienti c and Technological Cooperation Joint Project between Poland and Japan.

References
Bakken, L. R., and Olsen, R. A., 1990, Accumulation of radiocaesim Bressa, G., Cima, L., and Costa, P., 1988, Bioaccumulation of Hg
in the mushroom Pleurotus ostreatus. Ecotoxicology and Environmental Safety, 16, 85 89. Falandysz, J., and Frankowska, A., 2000, Bioaccumulation of elements and radionuclides by macrofungi: review for the territory of Poland (in Polish). Roczniki Panstwowego Zakladu Higieny, 51, 321 344. Falandysz, J., Bona, H., and Danisiewicz, D., 1994a, Silver uptake by Agaricus bisporus from an arti cially enriched substrate. Zeitschrift fur Lebensmittel Untersuchung und Forschung, 199, 225 228. Falandysz, J., Bona, H., and Danisiewicz, D., 1994b, Silver content of higher mushrooms (in Polish). Bromatologia i Chemia Toksykologiczna, 27, 211 225. Falandysz, J., Ichihashi, H., Piszczek, M., and Yamasaki, S., 1998, Elements in lichen Hypogymnia physode s overgroving difin fungi. Canadia n Journa l of Microbiology, 36, 704 710.

Elemental analysis of edible wild mushrooms

513

Seeger, R., 1976, Mercury content of mushrooms (in German).

Zeitschrift fur Lebensmittel Untersuchung und Forschung, 160, 303 312. Seeger, R., 1978, Cadmium in mushrooms (in German). Zeitschrift fur Lebensmittel Untersuchung und Forschung, 166, 23 34. Seeger, R., and Gross, M., 1981, Thallium in higher fungi (in German). Zeitschrift fur Lebensmittel Untersuchung und Forschung, 173, 9 15.

Varo, P., Lahelma, O., Nuurtamo, M., Saari, E., and Koivistoinen, P., 1980, Mineral element composition of
Finnish foods. VII. Potato, vegetables, fruits, berries, nuts and mushrooms. Acta Agriculturae Scandinavica, Supplement, 22, 89 113. Vetter, J., 1990, Mineral element content of edible and poisonous macrofungi. Acta Alimentaria, 19, 27 40. Vetter, J., 1993, Toxic elements in certain higher fungi. Food Chemistry, 48, 207 208. Wondratschek, I., and Roder, U., 1993, Monitoring of heavy metals in soils by higher fungi. Plants as Biomonitors. Indicators for Heavy Metals in the Terrestrial Environment, edited by B. Markert (Veinheim: VCH Verlagsgesellschaft), pp. 345 363. Yamasaki, S., Tsumura, A., and Cai, D., 1991, Microwave dissolution and ICP-MS for the determination of trace and ultra-trace elements in plant tissue. Applications of Plasma Source Mass Spectrometry, edited by G. Holland and A. M. Eaton (Cambridge: The Royal Society of Chemistry), pp. 110 118. Yoshida, T., Yamasaki, S., and Tsumura, A., 1992, Determination of trace and ultra-trace elements in 32 international geostandards by ICP-MS. Journal of Mining, Petrology and Economic Geology, 87, 107 122.

Shimamura, T., Iwashita, M., Takaku, Y., Akabane, I., Tsumura, A., and Yamasaki, S., 1995, Determination of the trace
elements in a Mizuho ice core sample by a combination of conventional and high resolution inductively coupled plasma mass spectrometry. Proceedings of the NIPR Symposium on Polar Meteorology and Glaciology, 9, 33 44. Skibniewska, K., and Smoczynski, S., 1999, In uence of cooking on radiocaesium contamination of edible mushrooms (in Polish). Roczniki Panstwowego Zakladu Higieny, 50, 157 161. Turnau, K., 1991, The in uence of cadmium dust on fungi in a pinoqercetum forest. Ekologia Polska, 39, 39 57. Tyler, G., 1980, Metals in sporophores of Basidiomycetes. Transactions of the British Mycological Society, 74, 41 49.