Heavy Metal Contents in Some Macrofungi Collected in the Northwestern Part of Turkey
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1 Arch. Environ. Contam. Toxicol. 41, 1 7 (2001) DOI: /s ARCHIVES OF Environmental Contamination and Toxicology 2001 Springer-Verlag New York Inc. Heavy Metal Contents in Some Macrofungi Collected in the Northwestern Part of Turkey M. Işiloğlu, 1 M. Merdivan, 2 F. Yilmaz 3 1 Department of Biology, Muğla University, 48000, Muğla, Turkey 2 Department of Chemistry, Dicle University, Diyarbakır, Turkey 3 Department of Mushroom, Ula Technical High School, Muğla University, 48640, Ula-Muğla, Turkey Received: 15 November 2000/Accepted: 1 February 2001 Abstract. Eight metal contents were determined in wild growing macrofungi collected from two different areas in Balikesir and Akhisar (NW Turkey). The analysis has been done by atomic absorption spectrophotometry in 179 samples of 16 species. Pb was accumulated extensively by G. sessile and L. cinerascens in both areas. Concentration of Cd was significantly high in A. pseudopratensis from background area and M. excissa from near road area. The high concentrations of Fe and Zn were found in M. ramealis and L. cinerascens for both areas. The mean concentration of Cu was high in V. pratense from background area and C. butyracea var. butyracea from near road area. The highest mean concentrations of Co and Mn for both areas were seen in G. sessile and M. excissa, respectively. A high Ni concentration was found in G. sessile and H. hypothejus from background area. We found no considerably significant differences in the concentrations of all studied elements between two areas. Correspondence to: F. Yilmaz; fyilmaz@mu.edu.tr Many investigations have dealt with the metal contents of cultivated mushrooms and in wild-growing mushrooms as well. Compared to green plants, mushrooms can uptake and accumulate considerable amounts of some heavy metals, such as Cd, Hg, and Pb (Kalac et al. 1991, 1996; Vetter 1994; Kojo et al. 1989; Falandysz and Chwir 1997; Kalac and Slapetova 1997). The factors governing the accumulation of metals in mushrooms are not well known. The principal factors influencing the accumulation of heavy metals in macrofungi are environmental factors (metal concentration in the soil, ph, contamination by atmospheric deposition) and fungal factors (fungal structure, morphological portion, development of mycelium and fruit bodies, biochemical composition, decomposition activity). The concentrations of Cd seem to be primarily dependent on the fungal factors, basically of the species and the biochemical composition (Melgar et al. 1998). Pb is more uniformly distributed among different species than Cd and Hg (Lodenius et al. 1981; Zurera-Cosana et al. 1987; Jorhem and Sundström 1995) and is accumulated remarkably at high concentrations on the fruit bodies of mushrooms, especially in the vicinity of highways or other lead sources (Jorhem and Sundström 1995; Laaksovirta and Alakuijala 1978; Liukkonen-Lilja et al. 1983). To what extent metals accumulate in mushrooms and in which species is not very well documented. There are, however, several indications in the literature that a number of species can contain fairly high levels of different metals (Jorhem and Sundström 1995; Yoshida and Muramatsu 1997; Sesli and Tüzen 1999; Gast et al. 1988; Gabriel et al. 1997). Wild-growing mushrooms are a delicacy in many countries, but in Turkey macrofungi collection is not very popular. Some people, however, collect fungi in such quantities that they can make a contribution to food intake, mostly in the autumn. The purpose of the present work was to evaluate the occurrence of eight metals in several species of macrofungi, whether consumed by the public or not, collected from Balikesir and Akhisar (northwest region of Turkey) in relation to some factors: species, the influence of traffic pollution, and the role of mushrooms as bioindicators. Also, this article attempts to broaden the investigated species of mushrooms on this subject. Materials and Methods The study was carried out in northwestern region of Turkey in autumn 1998 and winter The areas of the study (Figure 1) included pasturelands, forests, and vicinity to road subject to heavy traffic. The samples belonging to same species were collected from two different parts along 50 km of highway; near highway (0 50 m) and away from highway (more than 200 m). A great number of samples were collected from the vicinity of Değirmenboğazi, Susurluk country, and Demirtas village, which possess favorable environmental conditions for the growth of mushrooms. The habitat and morphological characteristics of the macrofungi found in the localities were recorded and photographed for diagnosis. The macrofungi specimens were then carried to the laboratory. A spore print was made to determine the color of the spores, and the spores were then used to determine the measurements. Finally, each species was identified using the reference books (Moser 1983; Breitanbach-
2 2 M. Işiloğlu et al. Fig. 1. The map of the sampling area and indication of the sampling site Kranzlin 1984). The family and species of investigated macrofungi were given in details with their edibility in Table 1. In all, a total of 179 samples were analyzed, presenting 16 different macrofungi species. Collected fresh samples were previously freed from foreign matter. Damaged or soiled parts were trimmed off with a plastic knife, and smaller particles were removed with a fine brush. Samples were air-dried for several days and then dried in an oven at 40 C for 48 h. Aliquots of g homogenized dry mushrooms were placed in a porcelain crucible and ashed in an oven at C for h. Ashed material was dissolved in 2 ml concentrated HNO 3, evaporated to dryness, heated again to 450 C for 3 h, dissolved in 1 ml concentrated H 2 SO 4 and 2 ml concentrated HNO 3, and diluted with distilled water up to 25 ml. The analysis was conducted in duplicate. The metals were determined by atomic absorption spectrophotometry (AAS) Pb, Cd, Ni, and Co were analyzed by graphite furnace AAS using Perkin Elmer SIM AA 600 model with Zeeman background correction. Zn, Cu, Fe, and Mn were determined by flame AAS, using Pye Unicam 929 with deuterium background correction. The wavelengths used were: Pb nm, Cd nm, Ni nm, Co nm, Zn nm, Cu nm, Mn nm, and Fe nm.
3 Heavy Metals in Macrofungi 3 Table 1. The families and edibility of macrofungi species Family and Species of Macrofungi Lycoperdaceae Corda Vascellum pratense (pers.) Kreisel Geastraceae Corda Geastrum sessile (Sow.) Pouz. Bolataceae R. Maire Suillus collinitus (Fr.) O. Kuntze Gomphideaceae R. Maire Chroogomphus rutilus (Schff.:Fr.) O.K. Miller Hygrophoraceae Roze ex Mre. Hygrophorus hypothejus (Fr.:Fr.) Fr. Tricholomataceae Roze ex Overem Collybia butyracea (Fr.:Fr.) Kumm. var. asema Fr. Collybia butyracea (Bull.:Fr.) Kumm. var. butyracea Fr. Marasmius ramealis (Bull.:Fr.) Sing. Melanoleuca excissa (Fr.) Sing. Lepiotaceae Roze Lepiota clypeolaria (Bull.:Fr.) Kummer Lepiota ignivolvata Bousset-Joss. Leucoagaricus cinerascens Quél. Leucoagaricus macrorhizus (Locq.) Sing. Agaricaceae Cohn. Agaricus pseudopratensis Bohus Russulaceae Roze Lactarius porninsis Roll Russula vinosa Lindbl. Edibility Edible (only when young) Edible (not recommended) Edible A certified reference material consisting of green algae (MBH, reference materials) was developed for survey and analyzed together with the samples. Differences between certified and experimentally found concentrations were up to 3 5% for Cu, Zn, Fe, and Mn and up to 3 7% for Pb, Cd, Ni, and Co. Detection limits were calculated as three times the standard deviation of a large number of blanks that were taken through the entire analytical procedure. Detection limits for each elements were, g/l for Mn, g/l for Cd, g/l for Cu, g/l for Co, g/l for Zn, g/l for Fe, and g/l for Pb. Correlation between concentrations of metals was tested by regression analysis. Results and Discussion Sixteen species of wild macrofungi were collected. Total number of samples from vicinity of road was 96 and from background was 83. Statistical treatment of data by t test confirmed significant differences in only Ni content between both groups at the probability levels of 95%. Metal concentrations in the macrofungus species, when at least three samples were analyzed, are given in Table 2. In this table, number of samples (n), mean concentrations, and standard deviations are indicated for both groups. The correlation coefficients were calculated for all pairs of metals in all investigated species having at least three samples. The significant linear correlations found among metal concentrations in mushrooms from the near road area are indicated in Table 3. Cu concentrations ranged from 6.6 to 115 mg/kg (near road) and from 8.7 to 120 mg/kg (background). The Cu concentrations were higher in G. sessile, C. butyracea var. butyracea C. butyracea var. asema, and L. macrorhizus for near road area and V. pratense for background area. The low copper content was found in H. hypothejus and C. rutilus for both areas. The differences seem to be insignificant in other species. Concentration of Cu in mushrooms is notably higher than in higher plants (Kalac et al. 1991). It is not yet clear whether or not high Cu concentrations can be nutritive source. Content of Zn in mushrooms ranged from 5.8 to 370 mg/kg (near road) and from 15 to 460 mg/kg (background). The lowest mean level was found in C. rutilus from both areas and the highest in L. cinerascens. The variation within two studied areas was fairly low except for H. hypothejus. Mushrooms are known as Zn accumulators. Zn is widespread among living organisms due to its biological significance. Content of Fe in mushrooms ranged from 150 to 3,450 mg/kg (near road area) and from 170 to 3,900 mg/kg (background area). The highest concentration of Fe by far was found in M. ramealis, with means of 3,000 mg/kg (near road area) and 3,750 mg/kg (background area). The next highest level was found in G. sessile, with means of 1,200 mg/kg and 2,700 mg/kg for samples from near road and from background area, respectively. The lowest concentrations, 160 and 190 mg/kg, were found in L. ignivolvata from both areas. Thus, the lowest and highest concentrations differ by a factor of about 20 for both areas. Minimum and maximum concentrations of Mn in collected samples were 5.7 and 50 mg/kg (near road areas) and 3.5 and 70 mg/kg (background area). The highest mean concentrations were found in M. excissa for samples from both areas. The next highest content of Mn was found in C. butyracea var. butyracea, H. hypothejus, and C. rutilus for samples from a concentration area. The mean concentration for most species was in
4 4 M. Işiloğlu et al. Table 2. Metal content in individual macrofungi species (mg/kg, dry weight); data are represented as means and standard deviations Family and Species Area Value Element Cu Zn Mn Fe Co Cd Ni Pb Lycoperdaceae V. pratense NR(7) Mean SD B (7) Mean SD Geastraceae G. sessile NR(8) Mean , SD B(8) Mean , SD Bolataceae S. collinitus NR(6) Mean SD B(3) Mean SD Gomphidiaceae C. rutilus NR(3) Mean SD B(3) Mean , SD Hygrophoraceae H. hypothejus NR(7) Mean SD B(5) Mean , SD Tricholomataceae C. butyracea var. NR(7) Mean asema SD B(7) Mean SD C. butyracea var. NR(7) Mean butyracea SD B(7) Mean SD M. ramealis NR(9) Mean , SD B(6) Mean , SD M. excissa NR(6) Mean SD B(6) Mean SD Lepiotaceae L. clypeolaria NR(6) Mean SD B(5) Mean , SD L. ignivolvata NR(6) Mean SD B(4) Mean SD L. cinerascens NR(4) Mean SD B(3) Mean SD L. macrorhizus NR(7) Mean SD B(6) Mean SD
5 Heavy Metals in Macrofungi 5 Table 2. Family and Species Area Value Cu Zn Mn Fe Co Cd Ni Pb Agaricaceae A. pseudopratensis NR(4) Mean SD B(5) Mean SD Russulaceae L. porninsis NR(4) Mean SD B(3) Mean SD R. vinosa NR(5) Mean SD B(5) Mean SD NR: Near road area, B: Background area. Element Table 3. Significant correlations (r) between metal pairs in mushrooms Species Cd Pb Cd Co Cd Ni Cu Co Cu Pb Cu Ni H. hypothejus 0.59 a 0.62 b 0.61 b 0.57 b S. collinitus 0.70 b 0.74 a L. clypeolaria 0.63 b 0.66 b Mn Co Mn Pb Mn Ni Cu Mn Zn Mn Cu Zn S. collinitus 0.70 b 0.65 b 0.68 b M. excissa 0.68 a 0.60 b 0.55 c M. ramealis 0.57 a R. vinosa 0.64 b L. clypeolaria 0.64 b a p b p c p the range of mg/kg. There was a positive correlation between Cu and Mn for M. excissa, which accumulated high amounts of Cu. The correlation between Zn and Mn was strong in S. collinitus and M. ramealis. The values of Co concentrations in samples were ranged from 0.56 to 5.8 mg/kg (near road area) and from 0.55 to 7.0 mg/kg (background area). The Co content in all species was generally low. Relatively high concentrations were found in G. sessile and V. pratense 3.8 and 3.6 mg/kg and 5.7 and 4.3 mg/kg for near road and background area, respectively. The variation within species was also low, but the level of samples from background area was relatively higher than for the other area. Significant linear correlations between concentrations of Cu and Co were only found for H. hypothejus and L. clypeolaria and those between Mn and Co were found for S. collinitus and M. excissa. Minimum and maximum values of Ni in samples were 1.3 and 11 mg/kg for samples from near road area and 1.4 and 18 mg/kg for samples from background area. Thus, the lowest and the highest concentrations differ by a factor of 12. The considerably highest mean concentrations of Ni in H. hypothejus, M. excissa, G. sessile, C. butyracea var. butyracea, and C. rutilus for samples from background area were found. The mean concentrations of other species were in the range of 3 6 mg/kg. The positive significant correlation between Cu and Ni was only seen in L. clypeolaria, and those between Mn and Ni was only seen in M. excissa. The high Ni concentration was seen in studies by Jorhem and Sundström (1995), Anderson et al. (1982), and Vetter (1994) as in this study. It can be concluded that Ni in macrofungi varies widely in different studies (Jorhem and Sunderström 1995). Cd concentrations were ranged from 0.10 to 4.0 mg/kg for samples from near road area and from 0.15 to 8.0 mg/kg for samples from background area. A. pseudopratensis had the highest mean concentrations of accumulated Cd: 3.2 and 6.2 mg/kg for near road and background areas (respectively); then, M. excissa showed the highest mean value of Cd with concentrations of 3.7 and 1.2 mg/kg for samples from near road and background area, respectively. The lowest mean concentrations were observed in the species C. rutilus, S. collinitus, and H. hypothejus with values less than 0.42 mg/kg for near road and background area. There was a significant correlation between
6 6 M. Işiloğlu et al. Cd and Ni in S. collinitus, which accumulated these moderately. Brunnert and Zadrazil (1985) concluded from experimental uptake studies that Cd and Zn compete for being resorbed by the fruiting bodies. However, Seeger (1982) concluded from other work that there is no correlation between Cd and Zn contents in wild-growing mushrooms; our data also do not provide such a correlation. These contradictory findings illustrate that a relationship with environmental parameters can exist without being found in field studies due to too many interfering factors. Very high concentrations of Cd have been found in the genus Agaricus as in our study (Vetter 1994; Kojo and Lodenius 1989; Lodenius et al. 1981; Schmitt and Meisch 1985; Quinche 1987). Tyler (1980) also found no correlation between the Cd 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 (Schmitt and Meisch 1985). Traffic pollution did not show statistically significant differences. The mean values, with the exceptions of A. pseudopratensis, M. excissa, and C. butyracea var. butyracea, were similar for near road and inner-part areas. Lodenius et al. (1981) noticed that high Cd concentrations were only found in the Agaricus samples, and they were probably not caused by pollution by species-dependent factors. Values of Pb concentrations in samples ranged from 1.3 to 14 (near road area) and from 0.75 to 10 (background area). We found the highest concentrations of lead in L. cinerascens from near road area and in G. sessile from background area. The variation within the studied areas was not significantly high, except for L. cinerascens and M. ramealis. Traffic pollution is important, mainly in the samples collected in near road area, having high automobile traffic, which generally showed maximum levels. The results may agree with the opinion of other authors (Lodenius et al. 1981; Zurera- Cosana et al. 1987; Kalac et al. 1989) who considered that the Pb content in mushrooms was influenced by the deposition of Pb emitted from car exhaust. The correlation between Cd Pb and Cu Pb was evident in H. hypothejus and also for S. collinitus between Cu Pb. In relation to the pollution source (main roads), Jorhem and Sundström (1995) concluded that lead was derived mainly from the contaminated roadside soil rather than from atmospheric deposition. Conclusion In this study, the metal contents of macrofungi collected from two different areas are not considerably different except for Pb. The effects of traffic pollution were seen mostly in Pb contents of mushrooms. The contents of cadmium and lead in mushrooms can be considered as high when compared with the acceptable values of Cd and Pb by FAO/ WHO (1989, 1993). The occurrence and distribution of different toxic components in certain mushrooms not only is a mycological theoretical problem but also has toxicological practical aspects. Therefore, the investigation of the biological mechanisms of uptake and accumulation could play an important role in the future. References Breitanbach J, Kranzlin F (1984) Fungi of Switzerland, vol 2 3. Verlag Mycologia, Lucerne Brunnert H, Zadrazil F (1985) The influence of zinc on the translocation of cadmium and mercury in the fungus Agrocybe aegerita. Angew Botanik 59: Falandysz J, Chwir A (1997) The concentrations and bioconcentrations factors for mercury in mushrooms from the Mierzeja Wislana sand-bar, Northern Poland. Sci Total Environ 203: FAO/WHO (1989) Evaluation of certain food additives and contaminants, 33. Report of the Joint FAO/WHO, WHO Technical Report Series 776, Geneva FAO/WHO (1993) Evaluation of certain food additives and contaminants. WHO Technical Report Series 837, Geneva Gabriel J, Baldrian P, Rychlovsky P, Krenzelok M (1997) Heavy metal content in wood-decaying fungi, collected in Prague and in the national park Sumava in the Czech Republic. Bull Environ Contam Toxicol 59: Gast CH, Jansen E, Bierling J, Haanstra L (1988) Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 17(4): Jorhem L, Sundström B (1995) Levels of some trace elements in edible fungi. Z Lebensm Unters Forsch 201: Kalac P, Slapetova M (1997) Mercury contents in fruiting bodies of wild growing edible mushrooms Potrav Vedy 15(6): Kalac P, Wittingerova M, Staskova I, Simak M, Bastl J (1989) Contents of mercury, lead and cadmium in mushrooms. Cs Hyg 34: Kalac P, Burda J, Staskova I (1991) Concentrations of lead, cadmium, mercury, and copper in mushrooms in the vicinity of a lead smelter. Sci Total Environ 105: Kalac P, Niznanska M, Bevilaqua D, Staskova 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. Sci Total Environ 177: Kojo MR, Lodenius M (1989) Cadmium and mercury in macrofungi. Mechanisms of transport and accumulation. Angew Botanik 63: Laaksovirta K, Alakuijala P (1978) Lead, cadmium and zinc contents of fungi in the parts of Helsinki Ann Bot Fennici 15: Liukkonen-Lilja H, Kuusi T, Laaksovirta K, Lodenius M, Piepponen S (1983) The effects of lead processing works on the lead, cadmium and mercury contents of fungi. Z Lebensm Unters Forsch 176: Lodenius M, Kuusi T, Laaksovirta K, Lilja HL, Piepponen S (1981) Lead, cadmium and mercury contents of fungi in Mikkeli, SE Finland. Ann Bot Fennici 18: Melgar MJ, Alonso J, Perez-Lopez M, Garcia MA (1998) Influence of some factors in toxicity and accumulation of cadmium from edible wild macrofungi in NW Spain. J Environ Sci Health B33(4): Moser M (1983) Keys to agarics and boleti. Gustav Fischer Verlag, London Quinche JP (1987) Le cadmium un element present en traces dans les sols, les plantes et les champignons. Rev Suisse Agric 19:71 77
7 Heavy Metals in Macrofungi 7 Schmitt JA, Meisch HU (1985) Cadmium in mushrooms-distribution, growth effects and binding. Trace Elem Med 2: Seeger R (1982) Toxische schwermetalle in Pilzen. Dtsch Apoth Z 122: Sesli E, Tüzen M (1999) Levels of trace elements in the fruiting bodies of macrofungi growing in the East Black Sea region of Turkey. Food Chem 65: Tyler G (1980) Metals in sporophores of basidiomycetes. Trans Br Mycol Soc 74:41 49 Vetter J (1994) Data on arsenic and cadmium contents of some common mushrooms. Toxicol 32:11 15 Yoshida S, Muramatsu Y (1997) Determination of major and trace elements in mushroom, plant and soil samples collected from Japanese forests. Int J Environ Anal Chem 67(1 4): Zurera-Cosano G, Rincon-Leon F, Pozo-Lora R (1987) Lead and cadmium content of some edible mushrooms. J Food Qual 10:
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