Concentrations of Mercury, Cadmium, Lead and Copper in Fruiting Bodies of Edible Mushrooms in an Emission Area of a Copper Smelter and a Mercury Smelter

The Science of the Total Environment 246Ž. 2000 61᎐67

Concentrations of mercury, cadmium, lead and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter

L. Svobodaa, K. Zimmermannova´ˇb, P. Kalac a,U aDepartment of Chemistry, Faculty of Agriculture, Uniërsity of South Bohemia, 370 05 Ceskeˇ ´ˇ Budejoïce, Czech Republic bDepartment of Botany and Genetics, Faculty of Science, Uniërsity of Constantine Philosopher, 949 01 Nitra, Sloäk Republic

Received 26 July 1999; accepted 11 October 1999

Abstract

Four metals were determined by AAS techniques in 56 samples of 23 wild mushroom species collected in a heavily polluted area in eastern Slovakia in 1997 and 1998. The area has been contaminated from historical polymetallic ores mining and smelting and by emissions from a mercury smelter between 1969 and 1993 and from a copper smelter since 1951. No signiﬁcant differences in metal concentrations Ž.P-0.05 were found in four species when comparing the periods 1992᎐1993 and 1997᎐1998. Considerable contamination of most species was observed mainly for mercury and cadmium. The highest levels of mercury, up to 50 mg kgy1 dry matter, were found in Boletus reticulatus, Lycoperdon perlatum and Marasmius oreades, and of cadmium up to 20 mg kgy1 dry matter in Xerocomus chrysenteron and Lycoperdon perlatum. The latter species also had extremely high lead and copper concentrations in hundreds of milligrams per kilogram dry matter. Concentrations of mercury and copper in caps of four Boletaceae species were signiﬁcantly Ž.P-0.05 higher than those in stipes. ᮊ 2000 Elsevier Science B.V. All rights reserved.

Keywords: Edible mushrooms; Heavy metals; Mercury; Cadmium; Lead; Copper; Mercury smelter vicinity; Copper smelter vicinity

1. Introduction countries and yearly consumption may exceed 10 kg for some individuals. Fruiting bodies of many Wild mushrooms have been a very popular mushroom species accumulate considerable levels delicacy especially in some central European of mercury, cadmium, lead, and copper. The ele- ment concentrations are primarily species-depen- dent. Numerous literature data were reviewed U Corresponding author. ŽSeeger, 1982; Kalacˇ and Svoboda, 1998; Michelot

0048-9697r00r$ - see front matter ᮊ 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7Ž. 9 9 00411-8 62 L. S¨oboda et al. rThe Science of the Total En¨ironment 246() 2000 61᎐67 et al., 1998. . The reported metal concentrations In our previous studyŽ. Kalacˇ et al., 1996 we differ over very wide ranges within a mushroom were interested in mushrooms collected from an species and knowledge on factors affecting accu- area contaminated by emissions from a mercury mulation rates has been very limited. There has smelter and a copper smelter between 1990 and been a consensus that mushroom fruiting bodies 1993. Nevertheless, the mercury smelter was are not the appropriate bioindicator of environ- closed in 1993 and the copper smelter decreased mental contamination by heavy metals. However, its metal emissions during the 1990s. The aims of in heavily polluted areas the observed metal con- our present work are to compare levels of four centrations have been considerably elevated. metals in mushroom fruiting bodies in a selected

Fig. 1. Maps of study area. L. Söboda et al. rThe Science of the Total Enïronment 246() 2000 61᎐67 63 emission area in during the periods 1992᎐1993 40 and 55 tons, lead emissions decreased from and 1997᎐1998 and to survey further edible some 50 t to 20 t since 1990. mushroom species for the metal concentrations. Mercury was produced from a sulphide concen- trate in Rudnanyˇ at a composite plant since 1963 and the smelter since 1969. Annual emissions 2. Materials and methods were approximately 4 t of mercury. Both plants were closed in 1993. However, a limited release of contaminated dust from spoil heaps continues. The study was carried out in eastern Slovakia, Nevertheless, many thousands of tons of mercury near the village Kluknava situated 30 km northwest of Kosiceˇ Ž. Fig. 1a . The observed area of are estimated to have been released into the 2=2 km has been contaminated by emissions environment during seven centuries of polymetal- from the adjacent copper smelter at Krompachy lic ores mining and smelting in the region. and the mercury smelter at Rudnanyˇ 15 km apart Both smelters are situated in valleys of sub- Ž.Fig. 1b . Both smelters are located in the Slovak montane landscape covered with forests. The pre- ore-yielding mountains area, where polymetallic vailing winds are north-westerly and westerly. The ores have been exploited since the Bronze Age. observed areaŽ. Fig. 1b is formed by four forested Iron, copper, and silver were produced with a valleys with orientation from north-east to south- large development during the Middle Ages. west. Spruce Ž.Picea abies is the prevailing tree in Small-scale copper smelters have operated in coniferous and mixed forests at an altitude the Krompachy region for several centuries. The between 400 and 800 m above sea level. Exposure present smelter has been operating since 1951 of the area to metal pollution for centuries is and it has processed ore concentrates and recy- reflected in high soil contamination. Metal con- cled copper materials. Annual copper emissions centrations vary widely in the forest soils between from its stack height of 200 m have been between 0.01 and 0.32, 0.25 and 10, 15 and 2200 and 10

Table 1 Metal concentrationsŽ. mg kgy1 dry matter in four species given as 1997᎐1998r1992᎐1993 data and background mean values from several European countries

Metal Parameter Xerocomus Leccinum Leccinum Macrolepiota badius Ž.M aarufum Ž.M griseum Ž.M aprocera Ž.S a

n3r45r33r34r6 Hg x 3.95r4.77 2.41r4.85 1.92r2.36 40.6r31.3 r r r r Sx 2.38 3.62 1.25 4.30 0.33 1.53 32.1 31.0 Background 0.61bebd᎐ 0.80 5.03 , 2.91 Cd x 1.15r5.85 0.19r1.87 5.01r4.44 7.72r11.2 r r r r Sx 0.41 4.56 0.10 2.01 3.64 2.90 7.57 13.2 Background 0.89bfbc᎐ 1.0 1.82 , 1.9 Pb x 1.39r4.04 3.92r1.04 1.58r3.83 62.4r29.9 r r r r Sx 0.77 2.22 4.08 1.33 0.54 1.76 39.9 34.4 Background 1.26b ᎐᎐ 4.87bc , 7.4 Cu x 41.4r42.9 91.6r32.2 36.1r52.2 324r228 r r r r Sx 1.8 10.4 93.4 9.9 8.6 22.3 148 60.2 Background 39.8b ᎐᎐ 155bc , 200

a M, mycorrhizal species; S, saprophytic species. b BohemiaŽ. Kalacˇˇ´ et al., 1989a,b; Kalac andˇ Slapetova, 1997 . c SwedenŽ. Jorhem and Sundstrom,¨ 1995 . d HungaryŽ. Vetter and Berta, 1997 . e BavariaŽ. Seeger, 1976a . f BavariaŽ. Seeger, 1978 . 64 L. Söboda et al. rThe Science of the Total Enïronment 246() 2000 61᎐67 b b b b b b ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ 31.5 22.1, 45.550.5 21.8 47.3 45 34.5, 22.6 16.9 86.8 75.3, 54.6 52.4 58.7 31.3, 32.2 23.8 15.8, 14.2 505, 347 ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ 0.23, 13.1 5.82 1.93 2.84, 1.97 2.01 1.89, 17.2, h ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ 0.47 0.56 1.67, 7.49 7.77 1.55, 2.9 1.45, aaaa aaaa fh g aaaa gh gehee aaaa cccb geee aaaa gh gh fh g gh dccd gdd cccbd dhd gd fh g ᎐ ᎐ ᎐ ᎐ ᎐ ᎐ 0.56 0.33 0.50.678.53.0 0.2 1.4 41.9 0.9 1.0 ˇ ¨ 1 1.86 1.78 2.81, 5.7 0.66 16.5,0.33,0.58 1.359.07,9.29 0.02 0.11 0.6 1.03, 3.34 0.57, 1.12 0.913.97 0.32, 0.5 0.52 0.84 36.4, 46.1 0.2 0.35 32.1 12.7, 0.4 9.11 2.55 3.16 0.7 0.84 1.3 81.7, 85.2 24.0 40 4.19 46 1.92 2.96 0.11 1.20 1.52 y Area55.3 Background 2.39 , Area Background 6.81 Area 2.50 Background Area 6.0 Background 1.48 90.444.5 27.3 3.3 10.9 Ž. S 22.9, 2.9 16.5, 2.1 223, 145 M 0.60, 0.07 1.43, 0.29 3.13, 1.58 99.6, 38.8 Ž. Ž. M 4.79, 0.53 2.77, 5.7 1.79, M 10.5, 0.9 0.37, 0.3 1.42, 1.10, 0.9 32.2, 24.3, 35 S 33.0 1.7 9.41 0.3 28.7 1.8 263 81 120 ˇˇ´ ig h M 0.68, 0.28 0.45, M2.49, Ž. Ž. Ž. Ž. Ž. M 5.71 0.19 0.99 0.55 2.58 3.76 50.7 33.4 M 2.97 0.57 0.45 1.13 0.93 0.42 35.0 14.9 Ž. Ž. M 2.20 1.8 M 11.2 0.27 4.57 1.9 16.8 M2.15 M 0.34 19.2 2.1 Ž. Ž. Ž. Ž. M2.69 Ž. M 5.35, 11.3 0.15 1.58, 0.75 0.13 0.2 5.47, 4.46 0.24 66.5, 52.3 7.9 Ž. Ž. Ž. Ž. Ž. Ž. Ž. M0.04, Ž. Ž. M3.08 alis Ž. ¨ M4.0 M 17.6 0.62 0.34 9.0 1.12 Ž. Ž. Bavaria Seeger, 1978 . Danmark Andersen et al., 1982 . Bohemia Kalac et al., 1989a,b; Kalac and Slapetova, 1997 . Bavaria Seeger, 1976a . Finland Kuusi et al., 1981 . Sweden Jorhem and Sundstrom, 1995 . Hungary Vetter and Berta, 1997 . Austria Mutsch et al., 1979 . M, mycorrhizal species; S, saprophytic species. esca a b c d e f g h i B. aesti ¨ Ž.Ž. chrysenteron Metal concentrations mg kg dry matter in 19 mushroom species and background mean levels from several European countries Table 2 Xerocomus X. subtomentosus L. quercinum Boletus reticulatus Leccinum scabrum Hydnum repandum Russula aeruginea R. lepida R. Lactarius deliciosus L. pinicola Marasmius oreades Ramaria aurea Lycoperdon perlatum R. polychroma R. paludosa Boletellus fragilipes Species HgSuillus luteus Cantharellus cibarius Cd Pb Cu L. Söboda et al. rThe Science of the Total Enïronment 246() 2000 61᎐67 65 and 730 mg kgy1 for mercury, cadmium, lead, and tions in the periods 1992᎐1993 and 1997᎐1998 copper, respectively. were tested by t-test and regression analysis was For a sample, one to four complete fruiting used for testing of differences in metal concentra- bodies of a species were collected from a place of tions in caps and stipes. diameter up to 5 m. The prevailing nutritional strategy of the individual mushroom species Ž.Ž.saprophytic or mycorrhizal Keizer, 1998 is 3. Results and discussion given in Tables 1᎐3. Fruiting bodies were cleaned by a stainless knife from all surface contamination in a manner usual for the preparation of A possible decrease in the metal levels in fruit- mushroom for culinary purposes. No washing or ing bodies following closure of the mercury caps peeling was used. Fruiting bodies were sliced smelter in 1993 and a decrease of copper smelter and dried at ambient temperature. emissions since the start of the 1990s was tested Sample homogenization and ashing, and cad- for four mushroom species with at least three mium, lead and copper determination by atomic samples from the observed area from both periods 1992᎐1993 and 1997᎐1998. Results are given absorption spectrometry measurements, were the in Table 1. Differences of mean values tested by same as described in our previous workŽ Kalacˇ et t-test are not statistically significant at level P- al., 1996. . Mercury was determined in the homog- 0.05. However, the limited number of samples enized dried samplesŽ. 0.1᎐0.2 g using a cold- and the great variance of metal concentrations vapour AAS analyzerŽ. AMA 254, Altec Prague y1 must be taken into consideration. with a detection limit of 0.5 ng g . Mean differ- Metal concentrations in 19 mushroom species ences between duplicates were up to 5%. Blank with only one, two or three samples are given in background levels were below the detection limits Table 2. Mean values, published for mushrooms for all determined elements. The green alga collected from unpolluted or mildly polluted ar- Chlorella kessleri, P-ACHKŽ Institute of Radioe- eas of several European countries are shown for cology and Applied Nuclear Techniques, Kosice,ˇ comparison as background levels. Differences Slovakia. was used as the reference material. between experimentally determined and pub- Differences between experimentally determined lished background concentrations were not statis- and certified concentrations were up to 2% for tically tested due to the low number of samples. mercury and up to 5% for the other metals. Unfortunately, information on background levels Differences between metal mean concentra- is lacking for many species. As can be seen from

Table 3 Distribution of metals within fruiting bodies in four mycorrhizal Boletaceae species

y Species StipeŽ. mg kg1 dry matter Cap Ž relative conc., stipes1.0 . Hg Cd Pb Cu Hg Cd Pb Cu

Boletus edulis 29.1 7.50 1.53 62.7 1.84 3.20 0.55 2.09 10.3 0.89 0.78 23.0 1.83 3.89 1.17 1.98 Boletus reticulatus 17.9 2.82 1.24 72.4 1.93 3.37 0.62 0.98 20.3 9.60 1.17 71.8 1.45 2.48 1.97 2.26 13.6 1.54 0.75 51.0 1.54 5.13 2.80 1.90 23.5 0.81 0.40 27.5 1.70 2.16 0.60 2.17 Leccinum scabrum 1.32 1.23 1.94 25.4 2.86 2.08 2.04 2.69 1.95 2.73 1.09 30.7 2.19 3.85 0.83 2.15 1.56 1.49 0.46 17.1 2.08 1.82 2.13 2.06 Leccinum griseum 1.09 1.43 1.44 28.2 1.96 1.50 1.17 1.79 66 L. S¨oboda et al. rThe Science of the Total En¨ironment 246() 2000 61᎐67

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