This study was done on edible, inedible and poisonous macrofungi collected around the Balikesir-Manisa highway from two different areas (roadside and background area) in 1998-1999. Cu, Zn, Fe, Mn, Co, Cd, Ni and Pb contents were determined by atomic absorption spectrophotometer in 256 samples belonging to 24 macrofungi species.
Turk J Bot 27 (2003) 45-56 © TÜB‹TAK Research Note Heavy Metal Levels in Some Macrofungi Fadime YILMAZ MuÔla University, Ula Ali Koỗman Vocational High School, Program of Fungi, 48640 Ula, MuÔla - TURKEY Mustafa IfiILOLU MuÔla University, Faculty of Science and Arts, Department of Biology, 48000 MuÔla - TURKEY Melek MERD‹VAN Dicle University, Faculty of Science and Arts, Department of Chemistry, 21000 Diyarbak›r - TURKEY Received: 23.05.2001 Accepted: 29.04.2002 Abstract: This study was done on edible, inedible and poisonous macrofungi collected around the Bal›kesir-Manisa highway from two different areas (roadside and background area) in 1998-1999 Cu, Zn, Fe, Mn, Co, Cd, Ni and Pb contents were determined by atomic absorption spectrophotometer in 256 samples belonging to 24 macrofungi species The habitat, edibility and distribution of the taxa in the families were listed According to mean dry weight (DW), Mn, Co and Cd contents were high in Omphalotus olearius (DC.: Fr.) Fr., which is a poisonous macrofungus species compared to the others; however, Fe levels were also extremely high The lowest Cu, Mn and Fe contents were found in Laetiporus sulphureus (Bull.: Fr.) Murr., which is an edible macrofungus The highest Pb and Zn contents were determined in Lycoperdon perlatum Pers as 6.5 mg/kg and 274 mg/kg respectively The contents of Ni and Cd seemed to be lower the near road Key Words: Heavy metals, macrofungi, Turkey Baz Makrofunguslarda AÔr Metal Seviyeleri ệzet: Bu ỗalflma 1998-1999 yllarnda, Balkesir-Manisa karayolu ỗevresinde, iki farkl› alandan toplanan (yol kenar› ve yola uzak alan), yenen, yenmeyen ve zehirli makrofunguslar üzerinde yap›lm›flt›r 24 makrofungus türüne ait 256 örnekte Cu, Zn, Fe, Mn, Co, Cd, Ni ve Pb iỗerikleri atomik absorpsiyon spektrofotometresiyle tespit edilmifltir Taksonlarn familyalar iỗinde daÔlfl, yenilebilirlikleri ve habitatlar liste halinde verilmifltir Ortalama kuru aÔrlklarna (DW) gửre, zehirli bir mantar tỹrỹ olan Omphalotus olearius (DC.: Fr.) Fr.de Mn, Co ve Cd iỗerikleri diÔer tỹrlerle karfllafltrldÔnda yỹksek, Fe de ise aflr yỹksek bulunmufltur En dỹflỹk Cu, Mn, Fe iỗerikleri yenebilen bir makrofungus olan Laetiporus sulphureus (Bull.: Fr.) Murr.da bulunmufltur En yỹksek Pb ve Zn iỗerikleri Lycoperdon perlatum Pers.’de s›ras›yla 6.5 mg/kg ve 274 mg/kg olarak tespit edilmifltir Ni ve Cd iỗeriklerinin yola yakn alanda daha dỹflỹk olduÔu gửzlenmifltir Anahtar Sửzcỹkler: AÔr metaller, makrofunguslar, Tỹrkiye Introduction Compared to green plants, mushrooms can build up large concentrations of some heavy metals (Stijve & Roschnic, 1974; Kuusi et al., 1981) An important factor is the absorption of these elements in the body after ingestion It has been suggested that little or none of the Cd present in fungi is absorbed during passage through the intestinal tract (Schellman et al., 1980) However, other studies indicate that Cd uptake may be fairly high (Gast et al., 1988; Vetter, 1994; Melgar et al., 1998) The fact is that the accumulation of metals by fungi has been shown primarily by the high Cd levels found in the Agaricus L.: Fr genus (Kuusi et al., 1981) It was determined that some macrofungi have the ability to accumulate heavy metals such as Cd (Stijve & Besson, 1976; Schmitt & Meisch, 1985; Jorhem & Sundström, 1995; Kalac et al., 1996) The description of the contents and factors influencing the accumulation of heavy metals in various macrofungi has been the target of many studies in recent years (Kojo & Lodenius, 1989; Falandysz & Chwir, 1997; Melgar et al., 1998; Garcia et al., 1998; Sesli & Tüzen, 1999; Falandysz et al., 2000; Demirbafl, 2001) The concentrations of Al, Cd and Pb in 17 edible, inedible and poisonous species of mushrooms were determined in the eastern part of Slovenia by Mandic et al (1992) According to their results, although the mean content of Cd in edible mushrooms was lower than it was in inedible, poisonous and deadly poisonous mushrooms, the mean content of lead in edible mushrooms was higher than it was in inedible mushrooms (Mandic et al., 1992) 45 Heavy Metal Levels in Some Macrofungi The concentrations of Pb in 95 samples of 13 species (seven mycorrhizals and six saprophites) collected from two different areas (polluted and unpolluted) in NW Spain were determined by Garcia et al (1998) The following factors were considered; species and ecology, as well as morphological portion and traffic pollution The average lead concentration of the samples was ppm dry weight Saprophite species presented higher levels than mycorrhizal ones Coprinus comatus (Müll.: Fr.) S.F.Gray reached the maximum mean concentration of 2.06 and 2.79 ppm of dry weight in the hymenophore and the rest of the fruit body The morphological portion statistically did not show a significant difference between the two portions (Garcia et al., 1998) This species, as other researchers have indicated, can be considered a bioindicator for lead contamination (Quinche, 1992) The highest Pb levels found in samples collected near roads were 2.35 mg/kg for the species Agaricus bitorquis (Quél.) Sacc and 7.00 mg/kg for Hypholoma fasciculare (Huds.: Fr.) Kummer The highest mean concentration of Cu was 51.0 mg/kg for Tricholoma terreum (Schaeff.: Fr.) Kummer and the highest mean Mn concentration was 35.9 mg/kg for Laccaria laccata (Scop.: Fr.) Bk & Br (Tüzen et al., 1998) Hg, Pb, Cd, Fe, Cu, Mn, Zn, Co and As contents were determined spectrometrically in the fruiting bodies of 109 wild and two cultivated macrofungi specimens by Sesli & Tüzen (1999) The macrofungi specimens were collected from the East Black Sea region of Turkey According to this study, no difference between sapropytic and mycorrhizal forming species was observed Trace element concentrations were highest in the macrofungi of the family Tricholomataceae The highest Pb content was 5.64 µg/g dry weight found in Hypholoma fasciculare collected from a roadside (Sesli & Tüzen, 1999) Seventeen different species of wild mushrooms growing in the East Black Sea region and one cultivated mushroom were analysed spectrometrically for trace element (Pb, Cd, Hg, Cu, Mn and Zn) levels by Demirbafl According to the results, the highest mean Pb level was 6.88 mg/kg for the species Hypholoma fasciculare collected from a roadside (Demirbafl, 2001) Turkey has a very rich flora of mushrooms because it possesses favourable environmental conditions for the growth of edible, inedible and poisonous macrofungi However, the Turkish public rarely consumes wild edible 46 macrofungi In many European countries fungi collection is very popular though the amount collected is quite insignificant (Jorhem & Sundström, 1995) The purpose of this study was to determine the contents of eight heavy metals in 24 macrofungi collected from roadside and background areas The other aim was to compare the toxicity of heavy metals, the habitat and edibility of species and traffic pollution Materials and Methods The macrofungi samples were collected from a roadside ecosystem (Bal›kesir-Manisa highway) between autumn 1998 and summer 1999 The study area (Figure 1) includes forest and lawns that have been exposed to pollutants from automobile traffic for many years The samples were classified and evaluated in two categories: roadside and background area The sampling was done between and 200 m from the road (roadside) and more than 200 m (as background area) Metal levels in 256 samples from 24 species of edible, inedible and poisonous mushrooms were analysed To identify the specimens, the habitat and morphological characteristics of the macrofungi found in the localities were recorded and photographed The macrofungus specimens were then brought to the laboratory and their spore prints were extracted and measured Specimens were identified by reference books (Moser, 1983; Breitanbach & Kranzlin, 1984) The samples were cleaned without washing, cut and dried at 40 ºC in an oven for 4.9-6.9 M ± SD MM M ± SD MM 47 ± 44-70 24 ± 10 17-39 88 ± 82-91 83 ± 73-88 12 ± 6.8 8.0-19 29 ± 22-33 493 ± 23 466-510 412 ± 12 401-425 2.3 ± 0.6 1.9-3.1 3.2 ± 0.9 2.0-4.0 0.39 ± 0.23 0.27-0.71 0.50 ± 0.19 0.33-0.74 3.8 ± 1.9 1.7-5.8 15 ± 13-19 3.0 ± 0.1 2.8-3.0 3.3 ± 0.5 3.0-4.0 M ± SD MM M ± SD MM 73 ± 66-82 75 ± 67-83 57 ± 12 49-72 67 ± 16 49-78 9.6 ± 3.7 7.8-15 14 ± 10-21 244 ± 12 223-265 698 ± 79 621-780 1.5 ± 0.7 0.65-2.0 3.0 ± 0.4 2.6-3.2 0.31 ± 0.46 0.16-0.75 0.84 ± 0.53 0.23-1.2 3.2 ± 0.9 2.2-4.0 2.8 ± 1.4 1.2-3.6 2.7 ± 0.8 1.8-3.4 4.1 ± 0.4 3.6-4.4 M ± SD MM M ± SD MM 58 ± 53-66 57 ± 10 45-64 82 ± 16 89-95 72 ± 10 62-86 12 ± 7.6-19 18 ± 69 12-29 238 ± 44 196-284 382 ± 10 372-393 2.2 ± 1.5 0.57-3.3 2.0 ± 0.6 1.3-2.5 1.4 ± 0.5 1.1-2.0 1.9 ± 0.5 1.2-2.4 3.6 ± 1.3 2.2-4.7 4.0 ± 0.9 2.8-4.6 2.4 ± 0.5 1.8-2.8 5.2 ± 1.9 3.0-7.2 R(5) B(3) 18 A subperonatus R(4) B(4) 19 H fasciculare R(5) B(7) 20 H sinapizans R(5) B(5) 21 Inocybe geophylla var violacea R(8) B(10) 22 L deliciosus R(5) B(5) 23 R delica R(4) B(4) 24 R foetens R(5) B(5) R: Roadside, B: Background area 50 Value F YILMAZ, M IfiILO⁄LU, M MERD‹VAN Species Co-Ni Cd-Co Mn-Co Pb-Ni Cd-Ni Cu-Ni 0.70b 0.75b 0.73b Table Significant correlations (r) between metal pairs in mushrooms r R luteolus L sulphureus S bellinii H hedrychii T batschii T stans A placomyces A subperonatus H sinapizans Species 0.87c 0.60a 0.50a 0.79c 0.86c 0.73a 0.78c 0.90d 0.85c 0.81c 0.79c 0.90d 0.82c 0.87d 0.64a 0.74b 0.78c Zn-Pb Fe-Zn Cu-Zn 0.76b Cd-Pb Mn-Ni Zn-Co r R luteolus L perlatum L sulphureus S bellinii T batschii T stans A placomyces A subperonatus H sinapizans Species 0.73a 0.71b 0.72b 0.79c 0.75b 0.60a 0.83d 0.62b 0.79b 0.71a 0.54a 0.77b Cu-Co Cu-Ni Co-Ni 0.77c 0.75b 0.75b 0.78b Cu-Cd Zn-Mn Co-Pb r O olearius L laccata M oreades T auratum T terreum L pudicus H fasciculare L deliciosus R delica R foetens Species 0.78c 0.77b 0.77c 0.80d 0.82d 0.67a 0.73b 0.79c 0.82d 0.80d 0.78b 0.81b Cd-Co Mn-Pb Mn-Ni Cd-Ni Zn-Cd Cu-Pb r T terreum L pudicus H fasciculare R delica R foetens 0.82c 0.60a 0.62a 0.73b 0.79b 0.74a 0.82c 0.74b 0.66a 0.78b 0.69a a: P < 0.10, b: P < 0.05, c: P < 0.02, d: P < 0.01 51 Heavy Metal Levels in Some Macrofungi were analysed and the results are given in Table In this table, the number of samples (n), mean concentrations and standard deviations (M ± SD), and minimummaximum (MM) levels are indicated for both groups The significant linear correlations found for metal concentrations in mushrooms from the roadside are indicated in Table Cu concentrations ranged from to 239 mg/kg for samples from the roadside and from 4.96 to 280 mg/kg for samples from the background area The highest mean level was found in Marasmius oreades (Bolt.: Fr.) Fr from the background area and the lowest mean levels for both areas in Laetiporus sulphureus The variation within the two studied areas was fairly low except for Marasmius oreades and Tricholoma auratum (Fr.) Gill (Figure 2) Concentration of Cu (mg/kg DW) Zn content in mushrooms ranged from 24 to 331 mg/kg for samples from the roadside and from 15 to 427 mg/kg for background area samples The highest Zn contents were found in Lycoperdon perlatum for roadside Tricholoma terreum for background areas The lowest zinc content was found in Omphalotus olearius for both areas Poisonous mushrooms were generally higher in zinc content in background areas (Figure 3) The correlation between Zn and Pb was significant in Laetiporus sulphureus (P < 0.02) The minimum and maximum concentrations of Mn in collected samples ranged from 3.7 to 42 mg/kg for roadside and from 3.8 to 42 mg/kg for background areas The highest mean concentrations were found in Omphalotus olearius for roadside areas and Agaricus subperonatus (Lge.) Sing The lowest mean concentrations were found in Laetiporus sulphureus for both areas The Mn content of edible mushrooms was higher in background areas (Figure 4) The correlation between Mn and Co was significant in L sulphureus (P < 0.02) In this study, it was found that the trace metal concentrations were statistically significant lowest in L sulphureus, which is edible Its habitat is on the living and dead wood of broadleaf trees Fungal species growing on wood contain, in general, lower concentrations of heavy metals than fungi growing on soil (Mutsch et al., 1979) 300 Figure Comparison of mean concentrations of Cu (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas Figure Comparison of mean concentrations of Zn (mg/kg dry weight) in 24 in species of mushrooms from roadside and background areas 250 200 150 100 50 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Concentration of Zn (mg/kg DW) Roadside Background 300 250 200 150 100 50 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Near road 52 Background F YILMAZ, M IfiILO⁄LU, M MERD‹VAN Concentration of Mn (mg/kg DW) 40 Figure Comparison of mean concentrations of Mn (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas Figure Comparison of mean concentrations of Fe (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas 35 30 25 20 15 10 5 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Concentration of Fe (mg/kg DW) Roadside Background 1000 900 800 700 600 500 400 300 200 100 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Roadside Background The Fe contents of mushrooms ranged from 162 to 9685 mg/kg for roadside and from 88 to 1711 mg/kg for background areas The highest concentration of Fe was found in Omphalotus olearius, with a mean of 9518 mg/kg (roadside) and 1544 mg/kg (background area) Concentrations of Fe in the other species were very low (Figure 5) The values of Co concentrations in samples ranged from 0.55 to 5.8 mg/kg for roadside and from 0.67 to 5.3 mg/kg for background areas Relatively high concentrations were found in Omphalotus olearius for roadside but Lepiota alba (Bres.) Sacc., Lycoperdon perlatum, Lactarius deliciosus Fr and Russula delica Fr for background areas (Figure 6) Cadmium concentrations ranged from 0.08 to 3.7 mg/kg for samples from roadside and from 0.22 to 4.9 mg/kg for samples from background areas The highest mean concentration was determined in Omphalotus olearius to be 3.9 mg/kg for background areas The ability to accumulate cadmium appeared highest for Hebeloma sinapizans (Paulet: Fr.) Gill in roadside areas (Figure 7) The level of samples from the background area were found statistically significant higher than the other area The correlation between Cd and Ni was significant in H sinapizans (P < 0.01) There were also significant correlations between Cd and Ni for Hypholoma fasciculare and Cd and Co for Tricholoma terreum (P < 0.02) Omphalotus olearius is a wood-decaying poisonous macrofungus Its habitat is on the roots or at the base of certain trees like Pinus sp and Olea sp Wood decaying fungi take up heavy metals absorption from the substrate Literature data indicate that heavy metal content decreases from the soil through the roots to the stems (Salt et al., 1995) Very high concentrations of cadmium have been found in the genus Agaricus (Lodenius et al., 1981; Schmitt & Meisch, 1985; Quinche, 1987; Kojo & Lodenius, 1989; Vetter, 1994) Tyler (1980) also found no correlation 53 Concentration of Co (mg/kg DW) Heavy Metal Levels in Some Macrofungi Figure Comparison of mean concentrations of Co (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas Figure Comparison of mean concentrations of Cd (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas Concentration of Cd (mg/kg DW) 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Roadside Background 4.5 3.5 2.5 1.5 0.5 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Roadside Background between the cadmium contents of mushrooms and that of the soil or substrate Because it has been suggested that Cd could be a growth stimulation factor, this phenomenon proved to be of taxonomical value and was not the result of environmental contamination with Cd from the soil (Tyler, 1980) Traffic pollution was not a significant factor for cadmium accumulation in fungi (Melgar et al., 1998) were found in Tricholoma terreum, Lepiota alba, Lactarius deliciosus, Agaricus placomyces Peck and Inocybe geophylla (Sow.: Fr.) Kumm var violacea Pat for samples from background areas The Ni level of samples from background areas was relatively higher (Figure 8) The correlation between Co and Ni was significant in Lactarius deliciosus, Tricholoma batschii Gulden and T terreum (P < 0.01) In this study, Cd contents were higher in Omphalotus olearius, Lycoperdon perlatum, Hebeloma sinapizans, Clitocybe dealbata (Sow.: Fr.) Kummer and Russula foetens Fr than in Agaricus species and the traffic pollution factor did not show significant differences High Cd concentrations were probably not caused by pollution but by species-dependent factors, so we agree with the opinion of other authors Lead concentrations in the samples ranged from 1.1 to 7.9 mg/kg for roadside and from 0.57 to mg/kg for background areas We found the highest concentrations of lead in Laccaria laccata, Marasmius oreades, Lycoperdon perlatum and Lepiota alba Mean concentrations for Omphalotus olearius, Laccaria laccata, Tricholoma stans (Fr.) Sacc., T auratum and T batschii were higher in roadside areas (Figure 9) The correlation between Co and Pb was significant in Lactarius deliciosus and Tricholoma terreum The correlation between Pb-Ni as well as Cd and Pb were significant for Agaricus placomyces and Tricholoma stans respectively (P < 0.01) The minimum and maximum values of Ni in samples ranged from 0.89 to 8.7 mg/kg for roadside areas and from 0.87 to 19 mg/kg for background areas Statistically significant highest mean concentrations of Ni 54 Concentration of Ni (mg/kg DW) F YILMAZ, M IfiILO⁄LU, M MERD‹VAN 16 Figure Comparison of mean concentrations of Ni (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas Figure Comparison of mean concentrations of Pb (mg/kg dry weight) in 24 species of mushrooms from roadside and background areas 14 12 10 2 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Species number Concentration of Pb (mg/kg DW) Roadside Background 1 10 11 12 13 14 15 16 18 19 20 21 22 23 24 Species number Roadside Background Marasmius oreades and Lacccaria laccata are saprophite edible mushrooms They live in grassy forests, on forest paths, in gardens and in parks The lead content of saprophite mushrooms were higher than those of mycorrhizal species The fruit bodies of mushrooms accumulate remarkably high concentrations of lead, especially in the vicinity of highways or other lead sources Our results agree with the data of other authors (Laaksovirta & Alakuijaka, 1978; Mornand, 1990; Jorhem & Sundström, 1995) Mushrooms can be used as bioindicators for lead soil pollution (Lodenius et al., 1981; Quinche, 1987) Other studies indicate that several species of Lycoperdaceae have a capacity for the bioaccumulation of Pb In this study, the Pb content of Lycoperdon perlatum agree with other authors (Tyler, 1980; Jorhem & Sundström, 1995) The highest Pb concentrations in studies by Sesli & Tüzen (1999) and Tüzen et al (1998) were found in collected roadside mushrooms belonging to the family Tricholomataceae Our study agreed with other studies (Sesli & Tüzen, 1998; Tüzen et al., 1998) In relation to the pollution source near main roads, Jorhem & Sundström (1995) concluded that lead was derived mainly from the contaminated roadside soil rather than from atmospheric deposition The exposure time for many mushrooms is very short, which makes the deposition of Pb from vehicle exhausts a small problem that is continuing to decrease as the use of leaded petrol is phased out (Jorhem & Sundström, 1995) The occurrence and distribution of different toxic components in certain mushrooms is not only a mycological theoretical problem, but also has practical environmental and toxicological aspects (Vetter, 1994) According to FAO/WHO (1989, 1993) acceptable weekly intakes of cadmium and lead for adults are 0.42-0.49 and 1.5-1.75 mg, respectively The Pb and Cd levels in all studied species from both areas can be considered to be high and mushrooms from these sites should not be consumed In this study, the metal contents of macrofungi collected from two different areas were determined to be statistically different Element content differed according to edibility, habitat and collection areas but no 55 Heavy Metal Levels in Some Macrofungi relationship was observed among those factors In this study element concentrations were primarily speciesdependent It was, therefore, rather difficult to determine the effect of environmental factors on the concentrations of elements Similar studies which include the analysis of various elements on a group of macrofungi species should be performed in order to explain the effect of environmental factors References Breitanbach J, Kranzlin F (1984) Fungi of Switzerland Vol 2-3 Lucerne: Verlag Mycologia Demirbafl A (2001) Levels of trace elements in the fruiting bodies of mushrooms growing in the East Black Sea region Energy Education Science & Technology 7(2): 67-81 Falandysz J, Chwir A (1997) The concentrations and 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