Mar 11, 2011 - B content was the highest in Coprinus micaceus (46.93 mg/ kg), the lowest in .... Coprinus comatus (O.F. Müll.) Gray. 195.3. 9.959. 1.315. 4.569.
Trace Elements and Electrolytes, Vol. 28 – No. 4/2011 (242-248)
Original ©2011 Dustri-Verlag Dr. K. Feistle ISSN 0946-2104 DOI 10.5414/TEX01198 e-pub: October 1, 2011
Concentrations of trace elements aluminum, boron, cobalt and tin in various wild edible mushroom species from Buyuk Menderes River Basin of Turkey by ICP-OES N. Durkan1, I. Ugulu2, M.C. Unver3, Y. Dogan2 and S. Baslar2 of Education, Pamukkale University, Denizli, 2Buca Faculty of Education, Dokuz Eylul University, Buca-Izmir, and 3Faculty of Education, Artvin Çoruh University, Artvin, Turkey
1Faculty
Key words trace element – edible mushrooms – ICP-OES – Turkey
Abstract. Objective: The investigation of the scale of environmental pollution is a major step towards preventing environmental pollution. Biomonitoring within an ecological programme involves the systematic use of living beings for obtaining quantitative information on changes in the environment, often due to anthropogenic activities. Material and methods: Trace metal levels in thirty-four different wild-growing edible mushroom species from Buyuk Menderes River Basin, West Anatolia, Turkey were determined by inductively coupled plasma optical emission spectroscopy (ICP-OES; Perkin Elmer, Optima 7000 DV). Results: The contents of trace elements in the mushroom samples were found in the ranges, 53.96 – 3308, 0.229 – 46.93, 0.005 – 2.224 and 2.809 – 4.711 mg/kg for aluminum, boron, cobalt and tin, respectively. Al content was the highest in Pleurotus ostreatus (3308 mg/kg), and the lowest in Laetiporus sulphureus (53.96 mg/kg). B content was the highest in Coprinus micaceus (46.93 mg/ kg), the lowest in Oudemansiella radicata (0.229 mg/kg). It was determined that Co content was the highest in Clavulina cristata (2.224 mg/kg), whereas the lowest in Agaricus bitorquis (0.005 mg/kg). In terms of Sn content, Agaricus campestris (4.711 mg/kg) was the highest, and Suillus bellinii (2.809 mg/kg) was the lowest. Conclusion: Results could be explained by the fact that there are no industrial activites that emit these metals.
Accepted for publication March 11, 2011
Introduction
Correspondence to Y. Dogan, PhD Buca Faculty of Education, Dokuz Eylul University, 35150, Buca-Izmir, Turkey yunus.dogan@ deu.edu.tr
Heavy metal pollution resulting from anthropogenic activities has become one of the most important environmental problems of present times [1, 2]. It is responsible for a number of environmental problems and risks to human health, such as decreased soil microbial activity and fertility, and yield losses [3].
The vast majority of ecosystems are contaminated with heavy metals deriving from urban activities (vehicle exhausts, municipal sewage sludge and waste incinerators), agricultural practices (fertilizers and pesticides application) and industrial processing (energy production, metalliferous mining, smelting industry, printing factories and tanneries) [4, 5, 6, 7]. The investigation of the scale of environmental pollution is a major step towards preventing environmental pollution. Chemical analysis is one of the methods for this purpose. However, analysts search for quicker, more specific and less costly methods, including bioindicatory systems, because of high costs of complex chemical analyses, and complicated and time-consuming procedures of sample preparation. The utilization of biological material, when combined with analytical techniques, allows improvement of the sensitivity and accuracy of traditional chemical methods [8]. The biological methods operated in environmental analysis may be divided into two groups; bioanalytics (the use of biological matter for environmental analyses; biosensors, biotests) and biomonitoring (the use of biota in classical chemical analysis – early warning system; bioindicators) [9]. Biomonitoring within an ecological programme involves the systematic use of living beings for obtaining quantitative information on changes in the environment, often due to anthropogenic activities [10]. Biological monitoring has various advantages and is the most significant one in study of sublethal levels of bioaccumulated contaminants within the tissues of organisms, which represent the net amount of pollutants integrated over a period of time [11].
Trace elements in various wild edible mushroom species from Buyuk Menderes River Basin
243
Figure 1. Map of the study area.
Determination of chemical compounds of living beings is one of the most frequently used methods to monitor air and soil pollution. Various living beings have been used as bioindicators: mushrooms [12, 13, 14]; mosses [1, 15, 16]; lichens [17; 18; 19]; agricultural crops and ornamental plants [20] and coniferous trees [21, 22, 23, 24, 25]. Mushrooms are known to uptake and accumulate some polluted toxic and essential elements in high concentrations [13]. Heavy metal concentrations in mushroom are considerably higher than those in agricultural crop plants, vegetables and fruits [26]. For this reason, many studies have focused considerable attention on the accumulation of heavy metals in some mushroom species from Turkey [12, 13, 14, 27, 28, 29, 30, 31, 32]. The aim of this study is to investigate concentrations of the trace elements aluminum, boron, cobalt and tin in various wild edible mushrooms from Buyuk Menderes River Basin, one of the major basins of West Anatolia.
Materials and methods Study area The research area, Buyuk Menderes River Basin, is located in the Southwestern Anatolian part of Turkey. It is a large area, which covers 3.5% of Turkey. It cuts through
the Aegean Region to the Aegean Sea, gathering agricultural and urban wastes from many arms of the Buyuk Menderes River (Figure 1).
Study materials Samples were collected from stations chosen as research areas during spring and autumn seasons in 2007 – 2009. During the process of collection, macrofungus samples were assigned a number in the field notebook and their morphological features (cap, lamel, stem, flesh, taste, smell, color change when squashed, dimensions), place of collection and growth characteristics were noted down. Photographs were taken to display each species’ characteristics. Enough samples of the recorded species were collected for identification and analysis and placed in polyetilene bags with their numbers. All the polyetilene bags were washed with 5% nitric acid and distilled water and dried in room temperature before use. Morphological features, spore dimensions and place of growth were taken into account and the mushrooms were identified according to Szemere [33], Michael and Hennig [34], Kreisel [35], Flammer [36], Phillips [37], Moser [38], Breitenbach and Kranzlin [39], Bresinsky and Besl [40], Pacioni [41], Courtecuisse and Duhem [42].
244
Durkan, Ugulu, Unver et al.
Table 1. Trace metal concentrations (as mg/kg) in analyzed mushroom species in the study area. Mushroom species
Al
B
Co
Sn
308.2
0.615
1.204
4.479
2. Agaricus bitorquis (Quél.) Sacc.
2083
0.773
0.005
4.158
3. Agaricus campestris L.
111.4
1.411
1.381
4.711
4. Agaricus essettei Bon.
620.7
3.767
0.714
4.111
5. Agrocybe aegerita (V. Brig.) Singer
261.3
11.08
1.242
4.105
6. Armillaria mellea (Vahl) P. Kumm.
192.9
3.018
1.173
3.803
7. Armillaria tabescens (Scop.) Emel
123.7
7.011
1.401
4.331
8. Clavulina cinerea (Bull.) J. Schröt.
914.1
2.928
0.883
4.356
9. Clavulina cristata (Holmsk.) J. Schröt.
971.4
0.688
2.224
3.472
10. Coprinus atramentarius (Bull.) Fr.
428.6
1.010
1.096
4.156
11. Coprinus comatus (O.F. Müll.) Gray
195.3
9.959
1.315
4.569
12. Coprinus micaceus (Bull.) Fr.
518.0
46.93
0.112
3.744
13. Ganoderma applanatum (Pers.) Pat.
744.8
0.383
0.744
3.531
14. Ganoderma lucidum (Curtis) P. Karst.
1828
0.362
0.332
3.647
15. Helvella leucopus Pers.
1865
0.939
0.088
3.978
16. Laccaria amethystea (Bull.) Murrill
235.1
3.887
1.225
3.864
17. Laccaria laccata (Scop.) Fr.
633.1
3.866
1.118
4.403
18. Laetiporus sulphureus (Bull.) Murrill
53.96
16.40
1.136
4.525
19. Lentinus tigrinus (Bull.) Fr.
227.5
3.649
1.182
2.928
20. Lentinus torulosus (Pers.) Lloyd
513.4
3.661
1.043
4.345
21. Lepista nuda (Bull.) Cooke
102.2
0.419
1.417
4.098
22. Leucoagaricus leucothites (Vittad.) M.M. Moser ex Bon
339.4
5.102
1.139
4.006
23. Lycoperdon molle Pers.
2199
1.565
1.412
4.512
24. Lycoperdon perlatum Pers.
106.6
6.835
1.390
3.821
25. Morchella conica Pers.
782.3
0.343
0.913
3.999
26. Oudemansiella radicata (Relhan) Singer
230.3
0.229
1.037
4.065
27. Pleurotus ostreatus (Jacq.) P. Kumm.
3308
2.547
0.076
3.523
28. Polyporus squamosus (Huds.) Fr.
122.5
1.416
1.373
4.061
29. Psathyrella hydrophilla (Fr.) Maire
3215
5.537
0.668
4.385
30. Rhizopogon luteolus Fr.
1773
0.414
0.349
4.019
31. Rhizopogon roseolus (Corda) Th. Fr.
1053
2.958
1.008
4.139
32. Suillus bellinii (Inz.) Watling
323.7
17.95
1.187
2.809
33. Suillus bovinus (Pers.) Roussel
482.5
1.873
0.419
4.349
34. Xerocomus chrysenteron (Bull.) Quél.
1853
10.54
1.328
3.839
1. Agaricus bisporus (J.E. Lange) Pilat
Analysis process The macrofungal samples for this research were collected from some localities of the research area in spring and summer periods from the years 2007 to 2009. They were dried at 50 °C for 48 hours. The dried samples were kept in polyethylene bags until analysis. After the drying process, 25 ml nitric acid was added on to a 2 g dried sample. It was heated slowly in a heater for 30 minutes and was left to get cold. Then 15 ml perchloric acid was added and was boiled for about 1 hour until it became colorless in a magnetic heater. After it got cold, 50 ml deionized water was added. The samples were kept in polyethyl-
ene bottles at 4 °C in a fridge until analyzing stage [43]. Teflon wares and Suprapur Merc chemicals were used in analyses. Amounts of aluminum, boron, cobalt and tin were measured from some mushrooms collected from Buyuk Menderes River Basin. The analyses of these elements in macrofungi were done by inductively coupled plasma optical emission spectroscopy (ICPOES; Perkin Elmer, Optima 7000 DV).
Results and discussion The concentrations of the trace elements aluminum, boron, cobalt and tin (mg/kg, dry
Trace elements in various wild edible mushroom species from Buyuk Menderes River Basin
245
Table 2. Daily metal intakes by a normal, 60 kg consumer in mg/serving for mushrooms of Buyuk Menderes River Basin Al
B
Co
Sn
Agaricus bisporus (J.E. Lange) Pilat
Mushroom Species
9.246
0.018
0.036
0.134
Agaricus bitorquis (Quél.) Sacc.
62.49
0.023
0.001
0.124
Agaricus campestris L.
3.342
0.042
0.041
0.141
Agaricus essettei Bon.
2.069
0.113
0.021
0.123
Agrocybe aegerita (V. Brig.) Singer
7.839
0.332
0.037
0.123
Armillaria mellea (Vahl) P. Kumm.
5.787
0.090
0.035
0.114
Armillaria tabescens (Scop.) Emel
3.711
0.210
0.042
0.129
Clavulina cinerea (Bull.) J. Schröt.
27.42
0.087
0.026
0.130
Clavulina cristata (Holmsk.) J. Schröt.
29.14
0.020
0.066
0.104
Coprinus atramentarius (Bull.) Fr.
12.85
0.030
0.032
0.124
Coprinus comatus (O.F. Müll.) Gray
5.859
0.298
0.039
0.137
Coprinus micaceus (Bull.) Fr.
15.54
1.407
0.003
0.112
Ganoderma applanatum (Pers.) Pat.
22.34
0.011
0.022
0.105
Ganoderma lucidum (Curtis) P. Karst.
54.84
0.010
0.009
0.109
Helvella leucopus Pers.
55.95
0.028
0.002
0.119
Laccaria amethystea (Bull.) Murrill
7.053
0.116
0.036
0.115
Laccaria laccata (Scop.) Fr.
18.99
0.115
0.033
0.132
Laetiporus sulphureus (Bull.) Murrill
1.618
0.492
0.034
0.135
Lentinus tigrinus (Bull.) Fr.
6.825
0.109
0.003
0.087
Lentinus torulosus (Pers.) Lloyd
15.40
0.109
0.031
0.130
Lepista nuda (Bull.) Cooke
3.066
0.012
0.042
0.122
Leucoagaricus leucothites (Vittad.) M.M. Moser ex Bon
10.18
0.153
0.034
0.120
Lycoperdon molle Pers.
65.97
0.046
0.042
0.135
Lycoperdon perlatum Pers.
3.198
0.205
0.041
0.114
Morchella conica Pers.
23.46
0.010
0.027
0.119
Oudemansiella radicata (Relhan) Singer
6.909
0.006
0.031
0.121
Pleurotus ostreatus (Jacq.) P. Kumm.
99.24
0.076
0.002
0.105
Polyporus squamosus (Huds.) Fr.
3.675
0.042
0.041
0.121
Psathyrella hydrophilla (Fr.) Maire
96.45
0.166
0.020
0.131
Rhizopogon luteolus Fr.
53.19
0.012
0.010
0.120
Rhizopogon roseolus (Corda) Th. Fr.
31.59
0.088
0.030
0.124
Suillus bellinii (Inz.) Watling
9.711
0.538
0.035
0.084
Suillus bovinus (Pers.) Roussel
14.47
0.056
0.012
0.130
Xerocomus chrysenteron (Bull.) Quél.
55.59
0.316
0.039
0.115
weight) in mushroom samples from different areas of Buyuk Menderes River Basin are given in Table 1. The mushroom species used as biomonitor to investigate the levels of the trace elements were sampled with 34 different species. The levels of elements were determined by ICP-OES. As a result of experiments carried out, the following mean concentrations were determined: The contents of Al, B, Co and Sn (mg/kg, dry weight) ranged from 53.96 to 3308, 0.229 to 46.93, 0.005 to 2.224 and 2.809 to 4.711, respectively (Table 1). In biological monitoring, by using different types of vegetation, the levels of atmo-
spheric trace metallic concentrations have been successfully monitored. In this direction, the aggregation of investigated trace elements in mushrooms collected from the different areas of Buyuk Menderes River Basin was presented in Table 1. From the table it can be seen that Al content was the highest in Pleurotus ostreatus (3,308 mg/kg), and the lowest in Laetiporus sulphureus (53.96 mg/ kg). B content was the highest in Coprinus micaceus (46.93 mg/kg), the lowest in Oudemansiella radicata (0.229 mg/kg). It was determined that Co content was the highest in Clavulina cristata (2.224 mg/kg), whereas the lowest in Agaricus bitorquis (0.005 mg/
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Durkan, Ugulu, Unver et al.
kg). In terms of Sn content, Agaricus campestris (4.711 mg/kg) was the highest, and Suillus bellinii (2.809 mg/kg) was the lowest. Arce et al. [44] determined mean Al content as 1,230 mg/kg in their study with mushroom species Suillus granulatus while Bibak et al. [45] determined Al amount in plant structure to change between 49 and 1,230 mg/kg in their analyses. When our results are evaluated, it is seen that mean Al amounts are in line with literature cited, with the exception of high content in Pleurotus ostreatus. In the study with less content, Sesli et al. [32] found Al content in various mushroom species of Black Sea region to be between 4.8 and 42.7 mg/kg. The minimum and maximum boron levels were 0.229 mg/kg in Oudemansiella radicata and 46.93 mg/kg in Coprinus micaceus, respectively. In connection with the accumulation of boron, the content of Marasmius wynnei mushroom was determined to be between 5 and 15 mg/kg by Vetter [46]. When this value range is compared with our study, it is seen that the results we obtained are within a larger range. In addition, the boron content results of our study were compared with those of Bibak et al. [45]. They found boron content in onions to be between 340 – 3,800 mg/kg. This result shows that boron content in mushrooms is low compared to plants. Cobalt concentrations in mushrooms are usually in the order of tens, maximally a few mg per kilogram of dry matter [27, 28, 29, 30, 47, 48]. In this study, cobalt was shown to be at the minimum and maximum value of 0.005 and 2.224 mg/kg dry matter, respectively. These values are in line with values in literature. However, an extraordinarily high value of 148 mg/kg dry matter was found by Michelot et al. [49] in Calocera viscosa. Mean cobalt content in mushrooms is comparable to foodstuffs, such as cereals, potato and fruit, ranging from 0.01 to 0.1 mg/kg fresh matter [50]. Similar range was determined by Shiraishi [51]. Tin values in mushroom samples have been reported to be in the ranges: 48.73 – 301.70 mg/kg [52]. In this study, the lower tin content found was 2.809 mg/kg in Suillus bellinii. The higher tin content found was 4.711 mg/kg in Agaricus campestris. Our tin levels were found to be lower than those reported in the literature.
According to the EU Scientific Committee for Food Adult Weight parameter, 60 kg of body weight was used for intake calculations as the weight of an average consumer [53]. In addition, for intake calculations, usually a 300 g portion of fresh mushrooms per meal is assumed, which contains 30 g of dry matter [54, 55]. The metal intakes by a normal (60 kg) consumer in mg/serving for edible mushrooms are presented in Table 2. It is known that high metal levels have been observed in mushrooms growing in heavily contaminated areas, such as those in the close vicinity of highways with heavy traffic [56], emission areas of metal smelters [57], domestic heating and long-range transport [58, 59]. When studies of Durkan et al. [12, 13, 14] are evaluated, it was seen that especially in the contents of Cr, Mn, Fe, Ni, Pb trace elements are high in the study area. This could be due to the factories on Büyük Menderes River, heavy traffic and partly emissions from metal smelters in the area. In the present study, the samples collected in Buyuk Menderes River Basin, showed the normal or lower aluminum, boron, cobalt and tin levels. This could be explained by the fact that there are no industrial activites that emit these metals. As a result, as reviewed by Wondratschek and Roder [60], no mushroom species can be considered as a precise indicator of environmental pollution with heavy metals. But it can be useful for distinguishing between polluted and unpolluted areas.
References [1]
[2]
[3]
[4]
[5]
Uyar G, Avcil E, Oren M, Karaca F, Oncel MS. De ter mination of heavy metal pollution in Zonguldak (Turkey) by Moss analysis (Hypnum cupressiforme). Environ Eng Sci. 2009; 26: 183194. Yildiz D, Kula I, Ay G, Baslar S, Dogan Y. Deter mination of trace elements in plants of Mt. Bozdag, Izmir, Turkey. Arch Biol Sci. 2010; 62: 731-738. Yilmaz K, Akinci IE, Akinci S. Effect of lead ac cumulation on growth and mineral composition of eggplant seedlings (Solanum melongena). New Zeal J Crop Hort. 2009; 37: 189-199. Baslar S, Dogan Y, Yenil N, Karagoz S, Bag H. Trace element biomonitoring by leaves of Populus nigra L. from Western Anatolia, Turkey. J Environ Biol. 2005; 26: 665-668. Baslar S, Kula I, Dogan Y, Yildiz D, Ay G. A Study of Trace Element Contents in Plants Growing at
Trace elements in various wild edible mushroom species from Buyuk Menderes River Basin
[6] [7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
Honaz Dagi-Denizli, Turkey. Ekoloji. 2009a; 18: 1-7. Kacalkova L, Tlustos P, Szakova J. Phytoextraction of cadmium, copper, zinc and mercury by selected plants. Plant Soil Environ. 2009; 55: 295-304. Kula I, Yildiz D, Dogan Y, Ay G, Baslar S. Trace Element Contents in Plants Growing at Mt. Akdag, Denizli. Biotechnol Biotec Eq. 2010; 24: 1587-1591. Gadzala-Kopciuch R, Berecka B, Bartoszewicz J, Buszewski B. Some considerations about bio indicators in environmental monitoring. Pol J Environ Stud. 2004; 13: 453-462. Markert B, Oehlmann J, Roth M. General aspects of heavy metal monitoring by plants and animals. In: Subramanian, KS, Iyengar, GV (eds), En vironmental biomonitoring, exposure assessment and specimen Banking. ACS Symp. Ser. 1997; 654. p.19-29. Calzoni GL, Antognoni F, Pari E, Fonti P, Gnes A, Speranza A. Active biomonitoring of heavy metal pollution using Rosa rugosa plants. Environ Pollut. 2007; 149: 239-245. Kumar NJI, Soni H, Kumar RN. Evaluation of Biomonitoring approach to study lake con tamination by accumulation of trace elements in selected aquatic macrophytes: A case study of Kanewal Community Reserve, Gujarat, India. Appl Ecol Environ Res. 2008; 6: 65-76. Durkan N, Isiloglu M, Kabar K, Dogan Y. Heavy metal levels in some macrofungi from Buyuk Menderes River Basin. Natura Montenegrina. 2008; 7: 465-473. Durkan N, Dogan Y, Unver MC, Isiloglu M, Kabar K. Levels of trace metals in some macro fungi from Buyuk Menderes River Basin. Natura Montenegrina. 2010a; 9: 753-759. Durkan N, Isiloglu M, Kabar K, Dogan Y. Trace element contents in some macrofungi from Buyuk Menderes River Basin. The Egyptian Journal of Experimental Biology. 2010b; 6: 1-4. Makinen A. Use of Hylocomium splendens for regional and local heavy metal monitoring around a coal-fried power plant in southern Finland. Symp Biol Hungurica. 1987; 35: 777- 794. Ruhling A, Rasmussen L, Pilegaard K, Makinen A, Steinnes E. Survey of atmospheric heavy metal deposition in the Nordic countries in 1985 – monitored by moss analyses. Nord. 1987; 21: 1-10. Loppi S, Giomerelli B, Bargagli R. Lichens and mosses as biomonitors of trace elements in a geo thermal area (Mt. Amiata, central Italy). Crypto gam, Mycol. 1999; 20: 119-126. Szczepaniak K, Biziuk M. Aspects of the bio monitoring studies using mosses and lichens as indicators of metal pollution. Environ Res. 2003; 93: 221-230. Ng O-H, Tan BC, Obbard JP. Lichens as bioin dicators of atmospheric heavy metal pollution in Singapore. Environ Monit Assess. 2006; 123: 6374. Warteresiewicz M. Oddzialywanie zanieczyszenia powietrza dwutlenkiem siarki na wybrane gatunki roslin w rejonie Gornoslaskiego Okregu przemys lowego. Arch Ochr Sr. 1979; 1: 95-166. Baslar S, Dogan Y, Bag H, Elci A. Trace element biomonitoring by needles of Pinus brutia from
[22]
[23]
[24]
[25]
[26] [27] [28]
[29]
[30]
[31]
[32]
[33] [34] [35] [36] [37] [38] [39] [40] [41]
247
Western Anatolia. Fresen Environ Bull. 2003; 12: 450-453. Baslar S, Dogan Y, Durkan N, Bag H. Bio monitoring of zinc and manganese in bark of Turkish red pine of Western Anatolia. J Environ Biol. 2009; 30 (Suppl): 831-834. Kaya G, Yaman M. Trace metal concentrations in cupressaceae leaves as biomonitors of environ mental pollution. Trace Elem Electroly. 2008; 25: 156-164. Dogan Y, Durkan N, Baslar S. Trace element pol lution biomonitoring using the bark of Pinus brutia (Turkish red pine) in the Western Anatolian part of Turkey. Trace Elem Electroly. 2007; 24: 146-150. Dogan Y, Ugulu I, Baslar S. Turkish Red Pine as a biomonitor: A comperative study of the accu mulation of trace elements in needles and barks. Ekoloji. 2010; 19: 88-96. Manzi P, Aguzzi A, Pizzoferrato L. Nutritional value of mushrooms widely consumed in Italy. Food Chem. 2001; 73: 321-325. Demirbas A. Concentrations of 21 metal in 18 species of mushrooms growing in the East Black Sea region. Food Chem. 2001; 75: 453-457. Tuzen M. Determination of heavy metals in soil, mushrooms and plant samples by atomic absorp tion spectrometry. Microchem J. 2003; 74: 289297. Mendil D, Uluozlu OD, Hasdemir E, Caglar A. Determination of trace elements on some wild edible mushrooms samples from Kastamonu, Turkey. Food Chem. 2004; 88: 281-285. Yesil OF, Yildiz A, Yavuz O. Level of heavy metals in some edible and poisonous macrofungi from Batman of South East Anatolia, Turkey. J Environ Biol. 2004; 25: 263-268. Isildak O, Turkekul I, Elmastas M, Aboul-Enein HY. Bioaccumulation of heavy metals in some wild-grown edible mushrooms. Anal Lett. 2007; 40: 1099-1116. Sesli E, Tuzen M, Soylak ME. Evaluation of trace metal contents of some wild edible mushrooms from Black sea region, Turkey. J Hazard Mater. 2008; 160: 462-467. Szemere L. Die unterirdischen Pilze des Karpaten beckens. Budapest: Akademia Kiado; 1965. Michael E, Hennig B. Handbuch for Pilzfreunde, Blatterpilze Dunkelblatter. Heidelberg: Vierter Band - Quelle & Meyer; 1969. Kreisel H. Grundzüge eines natürlichen Systems der Pilze. Stuttgart: Verlag Von J. Cramer; 1969. Flammer R. Differentialdiagnose dir Pliz Ver giftungen Gustav Fischer Verlag, Stuttgart- New York. 1980. Phillips R. Mushrooms and other fungi of Great Britain and Europa. London: Pan Boks Ltd.; 1981. Moser M. Keys to agarics and boleti (polyporales, boletales, agaricales, russulales). London: Roger Phillips; 1983. Breitenbach J, Kranzlin F. Fungi of Switzerland, Vol. 2, 3, 4. Luzern: Verlag Mycologia; 19861991. Bresinsky A, Besl H. Giftpilze, Werlagsgesellschaft mbH – Stuttgart. 1985. Pacioni G. Mushrooms and toadstools. London: MacDonald. & Co. Ltd.; 1985.
Durkan, Ugulu, Unver et al. [42] Courtecuisse R, Duhem B. Guide des champignons de France et d’Europe. Paris: Delachaux et Niestlé; 1994. [43] Haswell SJ. Atomic absorption spectrometry. New York: Elsevier; 1991. [44] Arce S, Cerutti S, Olsina R, Gomez MR, Martínez LD. Trace element profile of a wild edible mushroom (Suillus granulatus). J AOAC Int. 2008; 91: 853857. [45] Bibak A, Behrens A, Sturup S, Knudsen L, Gundersen V. Concentrations of 63 major and trace elements in Danish agricultural crops measured by in ductively coupled plasma mass spectrometry. 1. Onion (Allium cepa Hysam). J Agric Food Chem. 1998; 46: 3139-3145. [46] Vetter J. Boron content of edible mushrooms of Hungary. Z Lebensm Unters Forsch. 1995; 201: 524-527. [47] Isiloglu M, Yilmaz F, Merdivan M. Concentrations of trace elements in wild edible mushrooms. Food Chem. 2001; 73: 169-175. [48] Soylak M, Saracoglu S, Tuzen M, Mendil D. Determination of trace metals in mushroom samples from Kayseri, Turkey. Food Chem. 2005; 92: 649-652. [49] Michelot D, Siobud E, Doré JC, Viel C, Poirier F. Update on metal content profiles in mushrooms-toxicological implications and tentative approach to the mechanisms of bioaccumulation. Toxicon. 1998; 36: 1997-2012. [50] Weigert P. Metal loads of food of vegetable origin including mushrooms. In: Merian E (ed), Metals and their compounds in the environment. Wein heim: VCH; 1991. p: 449-468. [51] Shiraishi K. Determination of eighteen elements and 40K in eighteen food categories by Japanese subjects. J Radioanal Nucl Chem. 2005; 266: 61-69. [52] Elekes CC, Busuioc G, Ionita G. The bioaccumu lation of some heavy metals in the fruiting body of wild growing mushrooms. Not Bot Hort Agrobot. 2010; 38: 147-151. [53] Chen XH, Zhou HB, Qiu GZ. Analysis of several heavy metals in wild edible mushrooms from regions of China. Bull Environ Contam Toxicol. 2009; 83: 280-285. [54] Kalac P, Svoboda L. A review of trace element concentrations in edible mushrooms. Food Chem. 2000; 69: 273-281. [55] Svoboda L, Zimmermannová K, Kalac P. Con centrations of mercury, cadmium, lead and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. Sci Total Environ. 2000; 246: 61-67. [56] García MA, Alonso J, Fernández MI, Melgar MJ. Lead content in edible wild mushrooms in northwest Spain as indicator of environmental contamina tion. Arch Environ Contam Toxicol. 1998; 34: 330-335. [57] Lepsová A, Mejstrík V. Accumulation of trace elements in the fruiting bodies of macrofungi in the Krusné Hory Mountains Czechoslovakia. Sci Total Environ. 1988; 76: 117-128. [58] Grigalaviciene I, Rutkoviene V, Marozas V. The accumulation of heavy metals Pb, Cu and Cd at roadside forest soil. Pol J Environ Stud. 2005; 14: 109-115. [59] Viard B, Pihan F, Promeyrat S, Pihan JC. Integrated assessment of heavy metal (Pb, Zn, Cd) highway
248 pollution: bioaccumulation in soil, Graminaceae and land snails. Chemosphere. 2004; 55: 1349-1359. [60] Wondratschek I, Roder U. Monitoring of heavy metals in soils by higher fungi. In: Markert B (ed). Plants as biomonitors. Indicators for heavy metals in the terrestrial environment. Weinheim: VCH; 1993. p. 345-363.
