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Accumulation of trace elements in the fruiting bodies of macrofungi in the Krušné Hory Mountains, Czechoslovakia
The Science of the Total Environment, 76 (1988) 117 128 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
117
A C C U M U L A T I O N OF TRACE E L E M E N T S IN THE F R U I T I N G B O D I E S OF M A C R O F U N G I IN THE KRU~NI~ HORY M O U N T A I N S , CZECHOSLOVAKIA
A. LEP~OVA and V. MEJSTi~IK Institute of Landscape Ecology, Czechoslovak Academy of Sciences, Na sddkdch 702, 370 05 ~eskd Bud~jovice (Czechoslovakia)
(Received November 18th, 1987; accepted February 24th, 1988)
ABSTRACT The concentrations of some trace elements (Pb, Cd, Cu, Fe, Mn, Zn, Co, Ni) were determined in fruiting bodies of 20 fungal species from seven families (order Agaricales, Basidiomycetes) growing in the Kru~n6 Hory Mountains, Czechoslovakia, where the air pollution is characterized as moderate. Samples were collected from three stands: a spruce forest, the waterlogged margin of a peat bog, and the peat bog itself. The biomass of fruiting bodies of all macrofungi was determined simultaneously. The trace element concentrations varied among trophic groups of fungi: saprophytic species (S) and those parasitic on Sphagnum (Sph) exhibited the highest concentrations, while wood-decomposing (Wd) species displayed the lowest. Several species mycorrhizal with spruce (Ms), such as Amanita umbrinolutea, Russula ochroleuca, and Xerocomus badius, also attained higher concentrations than were found for other mycorrhizal fungi. The trace element concentrations were higher in the caps than in the stems of the fungi. The fraction of trace metals retained by the biomass of fruiting bodies of fungi with respect to annual fallout is estimated at 1%o. Factors affecting fungal uptake of trace elements are discussed.
INTRODUCTION The incidence, distribution and accumulation of trace elements in various parts of the environment have been attracting considerable attention, mainly because of their potential toxicity. Although many attempts have been made to reach a better understanding of the role of trace elements in fruiting bodies of f u n g i ( C r o n m a r c k e t al., 1975; H i n n e r i , 1975; D r b a l a n d K a l a G 1976; S e e g e r e t al., 1976; D r b a l e t al., 1975a,b; E n k e e t al., 1977, 1979; M c G r e i g h t a n d S c h r o e d e r , 1977; L a a k s o v i r t a a n d A l a k u i j a l a , 1978; O h t o n e n , 1978; S e e g e r , 1978; K u t h a n , 1979; M u t s c h e t al., 1979; T y l e r , 1980, 1982a, b; V o g t a n d E d m o n d s , 1980; L o d e n i u s , 1981; R i i h l i n g et al., 1983; T r e p t o w a n d L i s t , 1983) o u r k n o w l e d g e is s t i l l i n c o m p l e t e . T h e p r e s e n t p a p e r c o n s i d e r s t h e Pb, Cd, Cu, F e , M n , Zn, C o a n d Ni contents of different fungal species from three characteristic stands of the k r u ~ n 6 H o r y M o u n t a i n s , w h e r e t h e a i r p o l l u t i o n is m o d e r a t e ( ~ k o d a , 1980).
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118 MATERIALS AND METHODS
The study area is situated in the Kru~n~ Hory Mountains, Czechoslovakia (lat. 05°24'N, long. 12°55'E, ~1030m above sea level), in the Bo~idarsk~ Ra~elini~t~ nature reserve which consists of several peat bogs and natural spruce forests. The climate of the area is characterized by an average annual temperature of 4°C and average annual precipitation of 1150 mm; snow cover persists for 140 days of the year, with a maximum thickness of 100-150cm. Fogs are most frequent in August and September, and occur on average about 100 days per year. The directions of the dominant winds are W, NW and SW (Quitt, 1971; BSer and Veseck:~, 1975). Nutrient-poor, humic-ferric podsols cover a phyllite substrate. The Mrtv:~ Rybnlk, our study area, is a peat bog of the watershed type which originates at the points of issue of underground water (Dohnal, 1965). The most important sources of atmospheric pollution are from brown-coalfired power stations and opencast mines in the basin of the Kru~n6 Hory Mountains. The study area lies 30 km NWW of the coal-fired power station at Prun6~ov, 20 km NEE of a coal-fired power station at V~esov~i, and 25-30 km NE and N of opencast mines in the Sokolov basin. The area is not very rich in trace elements (Table 1) (~koda, 1980). Fruiting bodies of fungi were collected from three sampling sites within the study area from May to October 1975 and 1976, for biomass determination and trace metal analyses. The permanent plots, ~ 1 km WSW of Mount ~pi5~k (1116 m above sea level), were situated on a line running from north to south, 800m in length, and represented typical vegetation stands: a spruce forest (stand I), the water-logged margin of the peat bog (stand II) and the central part of the peat bog (stand III). The altitude of all sampling sites was ~ 1030 m. Stand I is covered with a plant community of the association Calamagrostidi villosa~Piceetum typicum Hartmann et J a h n 1976, and the subassociation sphagnetosum, in moist sites. The spruce forest, planted ~ 80 years ago in a natural habitat, is now 8-10m high. The substrate consists of podsolic soil typical of spruce stands. Both the height of the litter (3 cm) and the presence of raw humus are typical of these altitudes (Tables 2 and 3). The species of fungi sampled from the three sites were arranged into five trophic groups: species forming mycorrhizae with Picea abies (Ms), with Pinus mugo (Mp), wood-decomposing species (Wd), various saprophytic species (S) and those parasitic on Sphagnum (Sph). Group Ms was represented by Russula ochroleuca (Pers.) Fr., Amanita umbrinolutea S6cr., R. emetica Fr., Hygrophorus olivaceoalbus (Fr. ex Fr.) Fr., Xerocomus badius (Fr.) Kfihn. ex Gilb., and Cortinarius brunneus Fr.; group Wd was represented by Mycena alcalina (Fr.) Kummer, Gymnopilus sapineus (Fr.) Mre., Calocera viscosa (Pers. ex Fr.) Fr., Naematoloma capnoides (Fr.) Karst., and Fomitopsis pinicola (Sw. ex Fr.) Karst; and group S by Mycena galopoda (Pers. ex Fr.) Kummer, Micromphaleperforans (Hoffm. ex Fr.) Sing., Marasmius androsaceus (L. ex Fr.) Fr., and Glitocybe langei Sing. ex Hora.
12.95 33.56 35.55
T o t a l i n stand: I II III
A m o u n t of element in wet deposition over 1 y e a r (~koda, 1980)
III
II
3.98 1.75 7.22 5.75 2.88 24.93 0.66 34.89
S Wd Ms Sph Sm Ms S Mp
I
Biomass (year 1)
Trophic group
Stand
14 x 10s
79.5 110.7 76.72
56.8 4.8 17.9 45.2 3.7 61.8 9.42 67.3
Pb
Element
7.3 x 105
18.95 35.25 27.77
11.9 0.84 6.21 11.0 2.65 21.6 1.97 25.8
Cd
19.6 x 105
1351 2328 1201
818 74 459 664 81 1583 136 1065
Cu
120 x 10 ~
2631 7056 2779
1373 463 795 3981 329 2746 228 2551
Fe
887 x 105
3663 10175 4693
1132 237 2294 1993 261 7921 188 4505
Zn
The total a m o u n t of trace elements (gg/100m 2) in the b i o m a s s of f r u i t i n g bodies of fungi (g dry w e i g h t / 1 0 0 m 2)
TABLE 1
25 x 10~
400 669 627
246 47 107 248 50 371 41 586
Mn
115.5 320.0 150.2
43.4 12.2 59.9 88.2 24.8 207 7.2 143
Co
47 x 10 ~
29.0 82.3 16.9
20.1 1.1 8.7 41.0 11.4 29.9 3.4 13.5
Ni
120 TABLE 2 The soil profile of stand I Horizon
Depth (cm)
Aoo Ao
0-3 3~
A1
4-10
A2
10-16
Description of the horizon Undecomposed litter of spruce needles and herbs Slightly decomposed litter. Both horizon A00 and A0 richly interwoven with roots of herbs and species of the genus Vaccinium Black fine humus, heavily interwoven with spruce roots and blackberries in the upper part Leached podzol horizon, ash-grey in colour with occasional rock fragments (max. 5 cm); slightly interwoven with spruce roots
S t a n d II is s i t u a t e d at the w a t e r l o g g e d m a r g i n of the peat bog, with the a s s o c i a t i o n Calamagrostidi villosa~Piceetum sphagnetosum H a r t m a n n et J a h n 1967; from 1930 to 1940 the m a r g i n was d r a i n e d and planted with spruce, but now the u n t e n d e d d r a i n a g e system is o v e r g r o w n with v e g e t a t i o n and the trees are dying. The t h i c k n e s s of the peat l a y e r varies from 50 to 80cm, and the u n d e r g r o u n d w a t e r level f r e q u e n t l y r e a c h e s the soil surface; it falls to 10 cm below the soil surface in the driest m o n t h only. Typical h u m m o c k and hollow v e g e t a t i o n is well developed with species of the genus Vaccinium and Sphagnum species (S. robustum, S. fallax) respectively. M y c o r r h i z a l fungi with spruce (Ms) are the most i m p o r t a n t t r o p h i c g r o u p in this stand: Dermocybe uliginosa (Berk) Mos. D. palustris (Mos.) Mos. var. sphagneti (Orton) Mos., Russula paludosa Britz., R. emetica Fr., Lactarius rufus (Scop. ex Fr.) Fr., L. necator (Bull. em. Pers. ex Fr.) Karst., and Paxillus involutus (Batsch. ex Fr.) Fr.; S a p r o p h y t i c species (Sm), n a m e l y Naematoloma elongatipes (Peck.) Sing., are a b u n d a n t on dead parts of Sphagnum; living parts of moss are parasitized by Lyophyllum palustre (Peck.) Sing. and Galerina paludosa (Fr.) Kfihn. S t a n d I I I is in the u n d i s t u r b e d c e n t r a l p a r t of the peat bog, with the associa t i o n Vaccinio uliginosi Pinetum mughi H a r t m a n n et J a h n 1967, w h i c h is TABLE 3 pH in stands I, II and III Stand I Stand II Stand III
A004.3 Living parts of Sphagnum 1-5 cm depth Pinus mugo litter 1-4 cm depth Living parts of Sphagnum 1-4 cm depth
A0 3.8-4.4 4.2 3.8 4.1
A1 3.9-5.0 Peat 5-10 cm 4.4 Peat 5-10 cm 3.84.2
121 characterized by alternating pine-clad (Pinus mugo) sites and open sites mainly covered with cotton grass (Eriophorum vaginatum). After heavy rainfall the level of underground water reaches the soil surface; in the driest months it recedes to 50 cm below the surface. The peat layer is ~ 5 m thick. Most fungal species form mycorrhizae with pine (Mp): Russula decolorans Fr., R. paludosa Britz., R. emetica Fr., Lactarius rufus (Scop. ex Fr.) Fr., L. helvus (Fr.) Fr., Suillus flavidus (Fr. ex Fr.) Presl., S. variegatus (Schwartz ex Fr.) Kuntze, Hebeloma longicaudum (Pers. ex Fr.) Kummer, and various species of the genus Cortinarius. Saprophytic species (S) grow on various substrates, e.g. Galerina luteofulva Orton, Rhodphyllus cetratus (Fr.) Qu61. and Naematoloma udum (Pers. ex Fr.) Karst. on peat; numerous species of the genus Galerina on mosses; and Mycena galopoda (Pers. ex Fr.) Kummer and Marasmius androsaceus (L. ex Fr.) Fr. on litter. Permanent sampling plots were selected for each stand; three for stand I, one for stand II and two for stand III, all 30 × 30 m square. We sampled fungi in intervals from 7 to 14 days, and collected all fruiting bodies present in the plot. These were cleaned, placed in filter-paper bags, dried at 95-105°C and weighed so as to determine their dry matter weight. The major species (Hering, 1966), i.e. species with a weight production of fruiting bodies of at least 5%, were taken from each stand for metal analysis, the cap and the stem being treated separately; small fruiting bodies were treated as a whole. The samples were crushed in polythene bags, and 2 g of each sample was digested in HNO3 and H202. The methods used for trace element determination were stripping voltammetry (Vydra et al., 1977) for Pb, Cd and Cu, and atomic absorption spectrometry (AAS) for Mn, Fe, Zn, Ni and Co, using a Perkin Elmer model 400. The two methods have been described in detail by Guy and Chakrabarti (1977). The results were subjected to the t-test and one-way analysis of variance (Dixon and Brown, 1977). RESULTS AND DISCUSSION We identified 51 species of fungi (mainly Agaricales and Aphyllophorales) in samples from the permanent plots of the three stands. Eight species live saprophytically on various dead materials (e.g., needles, cones, leaves, moss, peat, decomposed litter, etc.), 10 species grow on dead wood (branches, stems and stumps of spruce), 20 species are considered to form ectomycorrhizae with spruce and/or pine, and two species are parasites on Sphagnum. We determined the biomass of the fruiting bodies for all stands, and evaluated the share of the main trophic groups to total biomass production (Table 4). Biomass production by fungi may be influenced by, among other factors, the concentrations of elements in the upper litter and humus horizon and by chemical processes. Lawrey (1978) found that the concentrations of trace
Galerina paludosa Strophariaceae Naematoloma capnoides N. elongatipes Russulaceae Lactarius rufus
var. s p h a g n e t i
Dermocybe palustris
Cortinariaceae Dermocybe uliginosa
Amanitaceae Amanita umbrinolutea
Family Species
0.46 0.10 0.17 0.14 0.10 0.13
l0
C S
1.48 0.74 0.62 0.24 1.33 0.54 0.44 0.21
2.66 1.83 0.66 0.03 1.89 1.26 0.28 0.04 1.30 0.98 0.92 0.46
0.65 0.55 0.24 0.13 0.16 1.85
~
Cu
2.1 4.2
sx
19.7 12.6
132 75.5 28.2
8.5 5.0
9.9 4.9 13.7
38.5 15.5 28.1 6.3 54.4 11.2 42.0 20.2 29.4 10.0 46.8 39.1
2.06 268 2.27 104
sx
2 C S 7 W
0.36 0.53 1.48 0.82 0.77 2.16
6.3 0.09 9.25 4.12 0.21 5.98
5c
2.59 2.59 2.96 2.48 2.22 6.07
C S
sx
Cd
3 C S 2 C S 5 W 2 W
2
5c
n a pb Pb
74 83
178 70 90
197 116 119 153 194 180
380 264
~c
Zn
14.1 10.2
~
32.2 20.6
12.3 13.1
19.1 29.4 17.5 15.9 48.4 17.5
45.2 22.1 21.8 22.4 122 21.8 14.1 19.8 78.8 19.~ 13.4 44.7
149 23.3
sx
Mn
3.7 5.11
2.1 9.1 4.8
8.62 40.7 18.7 12.2 10.6 0.7
4.73 2.75
sx
55.2 33.2
sx
59 48
200 123 114
25.8 28.5
32.5 66.3 56.2
170 50.6 259 204 194 100 149 73.3 165 63.8 310 63.6
135 100
5c
Fe
C o n c e n t r a t i o n s of trace e l e m e n t s (~gg ' dry wt.) in the fruiting bodies of selected fungal species
TABLE 4
0.7 0.6
7.6 0.5 8.6
Yc
Co
0.17 0.05
Sm
Wd
Sph
Ms
Ms
Ms
Trophic group
II, III Ms, Mp
0.4 0.28 ! 0.2 0.2 3.95 0.78 I! 0.53 0.2 0.6 0.1
1.2 0.1 4.3
0.33 I 0.36
sx
Stand
0.32 0.37 II 0.90 0.68 1.70 1.44 II 1.90 0.11 2.20 1.56 6.75 1.20 II
0.23 2.9 0.37 3.4
sx
5.0 4.54 16.4 6.83 65.1 28.2 5.3 1.7 12.8 5.3 3.8 0.78
8.8 1.7
5c
Ni
1.61 2.75 4.66 2.94 1.80 0.42 1.24 4.10 2.92 3.40 2.20
0.60 0.24 0.41 0.62 0.23 0.69 1.08 2.71 1.72 1.58 0.31
0.24 0.13 0.32 0.19 0.11 0.51 0.54 0.99 0.48 0.40 0.58
2.37 1.64 2.11 0.56 0.63 0.25
2.45 1.70 0.82 0.73 2.57 3.26
3 C S 2 C S 4 C S
1.22 0.46 0.22 0.01 1.00 0.99
1.84 0.63 0.13 0.84 0.52 0.49 0.07 0.37 0.14
0.11
1.61 2.17 0.83 4.59 5.78 0.75 0.67 0.51 0.53
0.57 0.71 0.51 0.97 0.33 0.14 0.97 0.57 0.49 0.56 0.41
7 W
8 W 9.24 5 W 14.3 2 W 3.63
2 C S 3 W 4 C S 6 C S 4 C S 6 C S
15.6
24.8 44.4 16.7
104 44.0 51.9 13.1 16.3 5.9 5.1 0.7 17.7 2.9 11.0 4.0
56.8
146 206 39.1
25.1 8.8 15.5 7.5 28.9 1.7 110 28.2 49.7 11.8 11.9 11.8 12.8 6.3 189 72.8 158 62.1 65.1 7.6 39.9 5.9
41.1
489 13.1 316 41.0 119 48.7 58 15.4 142 12.0 82 16.4
202 12.3 8.9 11.7 6.9 21.0 33.4
8.8 3.76 2.5 0.91 3.57 4.35 7.87
1.89
17.3 8.75 0.9
15.2 1.7 13.5 2.33 12.8 4.12 19.8 2.65 8.6 2.3 15.9 10.0 18.6 6.0 17.4 0.62 11.3 1.15 24.0 1.66 15.1 2.16
263 30.1 47.9 284 23.8 61.8 159 19.1 35.0
122 50.8 99 53.2 132 27.2 243 28.2 184 10.2 74 72.6 80 50.4 1081 114 787 129 251 25.6 172 7.8
115 111 49 36 95 175
76
30.5 10.0 39.1 17.9 14.6 69.4
62.3
4.6 6.1 0.7 0.4 7.6 5.4
4.2
20.1 10.9 12.7
0.15 0.54 1.8 0.6 0.2 0.33 0.9 1.2 0.52 0.3 0.4
Ms Mp
I, II III
0.99 I 0.33 0.94 II 0.34 0.85 III 0.12
Mp
Mp
Ms
Ms
Sph S Wd
Mp
III
II ! I
Ms
I
II, III Ms, Mp
Mp
III
1.46 0.82 I, II
8.08 2.42 5.04 3.32 1.24 0.62
0.2 1.0 2.1 0.8 0.2 0.3 0.6 1.7 1.3 0.4 0.4
2.65 0.6 1.41 0.4 0.62 1.4 0.43 1.6 8.7 0.6 5.3 0.2
1.35
10.6 9.2 0.92
0.4 1.3 0.07 25.9 1.4 0.4 37.9 12.3 10.2 20.9 2.5 2.1 16.7 2.4 2.9 32.8 1.5 1.03 33.1 0.8 0.85 30.9 2.6 1.3 14.9 1.9 0.93 23.1 6.2 5.0 23.8 18.8 9.7
833 346 345 170 470 227
55 61 89 66 51 44 68 63 50 94 73
an = n u m b e r of samples.bp = p a r t of f r u i t i n g body: C = cap, S = stem and W = whole fruiting body; o t h e r e x p l a n a t i o n s in Table 3.
S. flavidus
Suillus variegatus
Tricholomataceae Lyophyllum palustre Mycena galopoda M. alcalina Paxillaceae Paxillus involutus Boletaceae Xerocomus badius
R. paludosa
R. ochroleuca
R. emetica
L. necator Russula decolorans
L. helvus
¢.O
124
elements were higher in the litter than in needles attached to the branches. Trace element concentrations in the litter increase by processes associated with microbial decomposition. Airborne trace elements are retained in the upper soil horizon due to binding of the metals by humic substances. Therefore, the highest microbial activity is associated with litter decomposition, nutrient cycling and nitrogen fixation; mycorrhizae formation occurs in areas of elevated metal concentrations. We analysed 20 species of fungi belonging to seven families (Table 4). The trace element concentrations were highest in fungi of the family Tricholomataceae: the saprophytic species Mycena galopoda inhabiting various kinds of litter, and Lyphyllum palustre, the Sphagnum parasite; and in fungi of the family Amanitaceae; Amanita umbrinolutea, the species mycorrhizal with spruce. Galerina paludosa (fam. Cortinariaceae), Russula ochroleuca (fam. Russulaceae) and Xerocomus badius (Boletaceae) also exhibited higher trace element concentrations than other fungal species. The trophic groups of fungi (MPa, S, Wd, Sm, Sph; whole fruiting bodies) differ significantly in concentrations of all trace elements except cobalt (ANOVA, P < 0.01) (Table 5). The trace element concentrations in fungi mycorrhizal with spruce (MPa) were slightly higher than in those mycorrhizal with pine (MPm). The differences between these two trophic groups (MPa and MPm) were significant for Zn, Ni and Cu (both in caps and stems), for Fe and Pb in the caps only, and for Cd in the stems only (t-test, P < 0.05). Data on the trace elements and their quantitative evaluation suggest that the bioaccumulation of some elements is species specific (Tyler, 1980, 1982a, b). It depends on the ability of the species to extract elements from the substrate, and on the selective uptake and deposition of elements in tissues. The concentration of cadmium (and other trace elements) in plants was found to depend not only on the concentration of the metal in the soil but also on a number of soil and climatic conditions and on the physiology of the plant. The acidity of the substrate was one of the most important factors influencing cadmium uptake by the plant and the movement of cadmium through the plant. The cadmium concentration of the plant tissues increased with increasing soil acidity (Page et al., 1981). Soil acidity is becoming an important factor in certain localities (Table 3) because it is increasing as a result of acid rain. Relatively high trace element concentrations were found for fungi parasitic on moss, Lyophyllum palustre and Galerina paludosa; this was not surprising as Sphagnum is able to accumulate increased amounts of trace elements (Pucket and Burton, 1981). The physiology of mycorrhizal fungi is relatively uniform; they differ mainly in their requirements concerning the species of the host plant and perhaps in requirements concerning the stand. Mycorrhizal fungi favourably influence the uptake of phosphorus. Bolland et al. (1977) found that the presence of phosphates increased the adsorption of several microelements in the soil and thus diminished their solubility. The low phosphorus pool in the soil may be
C S W C S W W C S W W W
Ms
Sm Sph
S Wd
Mp
p
Trophic group
16 16 16 30 31 1 5 2 2 2 7 10
n
2.17 2.18 2.55 2.01 1.83 2.42 14.28 2.68 1.89 3.63 1.30 8.60
Pb
4.59 1.82 1.26 0.66 0.98 2.08
1.3 0.86 1.23 1.27 0.96
sx 1.40 0.94 0.24 0.94 0.52 1.42 2.78 0.66 0.28 0.51 0.92 2.10
2
Cd
0.75 0.03 0.35 0.53 0.46 0.75
1.22 0.75 0.24 0.58 0.42
sx 86.1 63.1 41.4 38.8 22.2 40.6 20.6 132 75.5 39.1 28.2 126
2
Cu
44.4 9.9 4.9 17.4 13.7 47.3
77.4 65.1 17.9 36.2 16.7
sx 445 318 189 145 112 181 284 176 69.6 159 70.7 246
2
Zn
23.8 19.1 17.5 19.1 48.4 44.3
409 298 58.3 86.6 52.8
sx 16.7 13.8 14.1 17.2 16.4 16.8 61.8 29.4 15.9 35.0 17.5 47.3
~
Mn
8.5 8.1 9.1 0.9 4.8 15.3
7.5 7.7 8.2 7.1 8.7
sx
107 109 115 68.3 76.4 116 345 200 123 471 114 728
2
Fe
170 32.5 66.3 267 56.2 377
68.6 116 72.4 29.1 50.8
sx
10.9 5.6 8.5 3.5 4.7 2.9 10.9 7.6 0.5 12.7 8.6 16.8
2
Co
C o n c e n t r a t i o n s of t r a c e e l e m e n t s i n f r u i t i n g b o d i e s of f u n g i of s e l e c t e d t r o p h i c g r o u p s ; for e x p l a n a t i o n s see t e x t a n d T a b l e 4
TABLE 5
9.2 1.2 0.1 0.92 4.3 11.6
22.5 6.5 6.4 4.7 7.7
sx
0.90 0.99 1.72 0.41 0.35 0.66 5.04 0.39 0.15 1.24 3.95 7.8
x
Ni
3.32 0.28 0.20 0.62 0.78 2.3
1.01 0.77 1.27 0.54 0.49
sx
126 further reduced by mycorrhizae, which contributes to the mobility of trace elements and also to their transport to the plant (Tinker, 1975). The uptake and transport of trace elements seems to differ in the various species ofmycorrhizal fungi, but reliable evidence is still lacking. According to our results, a greater amount of trace elements was bound in the fruiting bodies of mycorrhizal fungi than in those of saprophytic fungi, since mycorrhizal fungi form larger fruiting bodies and produce a greater biomass than saprophytic fungal species (Table 1). It was calculated that fruiting bodies of fungi accumulate in their biomass only ~ 1%o of the annual wet deposition (Table 1). Although wet deposition on the surface of fruiting bodies is apparently of little importance, the effect of dry deposition may be considerable, particularly in heavily polluted areas (Lep§ov~ and Kr~l, 1988). The substrate seems to be the main source of fungal uptake of trace elements. This assumption is supported by the fact that the mycelium of macrofungi develops mostly in the layer of raw humus, i.e. in the uppermost soil horizons (5-10cm), where the concentrations of trace elements are reported to be highest (Heinrichs and Mayer, 1977; Lawrey, 1978). Trace element concentrations in fungi are considerably higher than those in agricultural crop plants, vegetables and fruit (Treptow and List, 1983). This would suggest that fungi possess a very effective mechanism that enables them to take up some trace elements from the substrate more readily. This mechanism may be more effective in the parasitic and saprophytic fungi trophic groups than in the mycorrhizal fungi group. CONCLUSIONS These investigations were conducted in 1975 and 1976 in three typical stands from the Bo~idarsk6 ra§elini§t6 peat bog. We identified 26 species of saprophytic fungi growing on different substrates, 10 wood-decomposing species, two species parasitic on Sphagnum, and 21 mycorrhizal species mainly of the orders Agaricales and Aphyllophorales. Twenty of these fungal species were selected for analysis in order to determine the concentrations of trace elements (Pb, Cd, Cu, Zn, Fe, Mn, Ni and Co) in the fruiting bodies. Our results show that the concentrations of trace elements in the fruiting bodies of fungi tend to be species specific. We observed increased trace element concentrations for all fungal species. The species Amantia umbrinolutea,
Russula ochroleuca, Xerocomus badius, Lyophyllum palustre, Galerina paludosa and Mycena galopoda accumulated trace elements in higher concentrations than the remaining species. In general the concentrations were higher in the caps than in the stems of the fungi. The concentrations were found to depend on the physiology of the species, and particularly on its trophic pattern. They were highest in saprophytic species, lower in those parasitic on Sphagnum and those producing mycorrhizae with spruce and pine, and lowest in species saprophytic on wood.
127 O w i n g to t h e s h o r t life of t h e f r u i t i n g b o d i e s (7-14 days), n e i t h e r d r y n o r w e t d e p o s i t i o n o n t h e s u r f a c e of t h e c a p a p p r e c i a b l y i n f l u e n c e d t h e c o n c e n t r a t i o n s of trace e l e m e n t s in the fungi in this m o d e r a t e l y p o l l u t e d area. H i g h e r t r a c e e l e m e n t c o n c e n t r a t i o n s w e r e f o u n d for f u n g i f r o m t h e s p r u c e s t a n d (I) t h a n for t h o s e f r o m t h e o t h e r t w o s t a n d s - - t h e w a t e r l o g g e d m a r g i n of t h e p e a t b o g (II) a n d t h e p e a t b o g i t s e l f (III). D i f f e r e n c e s i n t r a c e e l e m e n t c o n c e n t r a t i o n s from one y e a r to the n e x t were n o t significant. ACKNOWLEDGEMENTS T h a n k s a r e d u e to D r R. K r ~ l a n d D r R. H a l e § for t h e i r a s s i s t a n c e i n s a m p l e a n a l y s e s , a n d D r J. Lep~ for s t a t i s t i c a l e v a l u a t i o n of t h e a n a l y t i c a l r e s u l t s . O u r t h a n k s a l s o t o M r s L. M i k o v c o v ~ a n d M. S k o ~ e p o v ~ for t h e i r t e c h n i c a l a s s i s t a n c e i n t h e t r e a t m e n t of t h e s a m p l e s , a n d p a r t i c u l a r l y to M r s H. L e t o v s k ~ for h e r h e l p i n c o l l e c t i n g s a m p l e s o f f r u i t i n g b o d i e s f r o m t h e p e r m a n e n t plots. REFERENCES B6er, W. and A. Veseck~, 1975. Podnebl a po~asi Kru~n~ch hor. ~esk~ Hydrometeorologick:~ l~stav, Praha. Bolland, M.D.A., A.M. Posner and J.P. Quirk, 1977. ZH adsorption by goethite in the absence and presence of phosphate. J. Soil. Res., 15: 27~286. Cronmarck, K., R.L. Todd and C.D. Monk, 1975. Patterns of basidiomycete nutrient accumulation in conifer and deciduous forest litter. Soil Biol. Biochem. 7: 265-268. Dixon, W.J. and M.B. Brown, 1977. BMDP-77. Biomedical Computer Programs. P-Series. University of California, Berkeley. Dohnal, J., 1965. ~eskoslovensk~i ra~elini§t~ a slatini§t~. SZN, Praha. Drbal, K. and P. Kala~, 1976. Obsah kobaltu v n~kter:~ch druzlch jedl:~ch hub. ~es. Mykol., 28: 24 26. Drbal, K. and P. KalaS, A. ~eflov~ and J. ~efl, 1975a. Obsah stopov:~ch prvku ~eleza a manganu v n~kter~ch druzich jedl:~ch hub. ~eska Mykol., 29: 110-114. Drbal, K., P. KalaS, A. ~eflov~ and ~efl, 1975b. Obsah m~di (Cu) v n~kter~ch druzich jedl~ch hub. ~eska Mykol., 29: 184-186. Enke, M., H. Matschiner and M.K. Achtzehn, 1977. Heavy metal enrichments in mushrooms. Nahrung, 21:331 334. Enke, M., M. Roschig, H. Matschiner and M.K. Achtzehn, 1979. Zur Blei-, Cadmium- und Quecksilber- Aufnahme in Kultur-champignons. Nahrung, 23:731 737. Guy, R.D. and C.L. Chakrabarti, 1977. Analytical techniques for speciation in trace metals. International Congress on Heavy Metals in the Environment. Toronoto. Heinrichs, H. and R. Mayer, 1977. Distribution and cycling of major and trace elements in two Central European forest ecosystems. J. Environ. Qual., 6: 402-407. Hering, T.F., 1966. The terricolous higher fungi of four Lake District woodlands. Trans. Br. Mycol. Soc., 42: 1-14. Hinneri, S., 1975. Mineral elements of macrofungi in oak-rich forest on Lenholm Island inner archipelago of SW Finland. Ann. Bot. Fenn., 12: 135-140. Kuthan, J., 1979. Die Auswertung des Bleigehaltes in Bronze-RShling-Boletus aureus Bull. ex Fr. entlang einer der Verkehrasandern in Bulgarien. ~eska Mykol., 33: 58-59. Lasksovirta, K. and A.P. Alakuijala, 1978. Lead, cadmium and zinc contents of fungi in the parks of Helsinki. Ann. Bot. Fenn., 15: 254-257. Lawrey, J.D., 1978. Trace metal dynamics in decomposing leaf litter in habitats variously influenced by coal strip mining. Can. J. Bot., 56: 953-962. -
-
128
Lep§ov~, A. and R. Kr~l, 1988. Lead and cadmium in fruiting bodies of macrofungi in the vicinity of a lead smelter. Sci. Total Environ., 76: 129-138. Lodenius, M., 1981. Lead, cadmium and mercury contents of fungi. Ann. Bot. Fenn., 18:183 186. McGreight, J.D. and D.B. Schroeder, 1977. Cadmium, lead and nickel content of Lycoperdon perlatum Pers. in roadside envornment. Environ. Pollut., 13: 265-268. Mutsch, F., O. Horak and H. Kinzel, 1979. Trace elements in higher fungi. Z. Pflanzenphysiol., 94: 1 10. Ohtonen, R., 1978. Mineral elements in some wild mushrooms. Karstenia, 18 Suppl: 97-99. Page, A.L., F.T. Bingham and A.C. Chang, 1981. Cadmium. In: N.W. Lepp (Ed.), Effect of Heavy Metal Pollution on Plants. Vol. 2. Applied Science Publishers, London and New York. Pucket, K.J. and M.A.S. Burton, 1981. The effect of trace elements on lower plants. In: N.W. Lepp (Ed.), Effect of Heavy Metal Pollution on Plants. Vol. 2. Applied Science Publishers, London and New York. Quitt, E., 1971. Klimatick~ oblasti ~eskoslovenska. Stud. Geogr., 16:1 74. Rfihling, A.E. B ~ t h , A. Nordgren and B. SSnderstrSm, 1983. Fungi in metal contaminated soil near the Gusum Brass, Sweden. Ambio, 13: 34-36. Seeger, R., 1978. Cadmium in Pilzen. Z. Lebensm. Unters. Forsch., 166: 23-34. Seeger, R., E. Meyer and S. Schonhut, 1976. Blei in Pilzen. Z. Lebensm. Unters. Forsch., 162:7 10. ~koda, J., 1980. V~zkum l~tkov6ho slo~enl sr~i~kov~ch vod s p~ihl~dnutlm k v:~skytu stopov~ch prvkfi. V~zkumn~ l:lstav Vodohospod~sk~, Praha. Tinker, P.B.H., 1975. Effects of vesicular-arbuscular mycorrhizas on higher plants. In: F.E. Sanders, B. Mosse and P.B.H. Tinker (Eds), Endomycorrhizas. Academic Press, London. Treptow, H. and D. List, 1983. Die Schwermetallkontamination von Obst, Gemiise und Speisepilzen in ihrer Bedeutung ffir die Ern/ihrung. Ern/ihr.-Umsch., 30: 301-303. Tyler, G., 1980. Metals in sporophores of Basidiomycetes. Trans. Br. Mycol. Soc., 74:41 49. Tyler, G., 1982a. Accumulation and exclusion of metals in Collybia peronata and Amanita rubescens. Trans. Br. Mycol. Soc., 79: 239-245. Tyler, G., 1982b. Metal accumulation by wood-decaying fungi. Chemosphere, 11: 1141-1146. Vogt, K.A. and R.L. Edmonds, 1980. Patterns of n u t r i e n t concentration in basidiocarps in Western Washington. Can. J. Bot., 58: 694~98. Vydra, F., K. ~tulik and E. Julglkovg~, 1977. Rozpou~t6cl polarografie a voltametrie. Academia, Praha.
117
A C C U M U L A T I O N OF TRACE E L E M E N T S IN THE F R U I T I N G B O D I E S OF M A C R O F U N G I IN THE KRU~NI~ HORY M O U N T A I N S , CZECHOSLOVAKIA
A. LEP~OVA and V. MEJSTi~IK Institute of Landscape Ecology, Czechoslovak Academy of Sciences, Na sddkdch 702, 370 05 ~eskd Bud~jovice (Czechoslovakia)
(Received November 18th, 1987; accepted February 24th, 1988)
ABSTRACT The concentrations of some trace elements (Pb, Cd, Cu, Fe, Mn, Zn, Co, Ni) were determined in fruiting bodies of 20 fungal species from seven families (order Agaricales, Basidiomycetes) growing in the Kru~n6 Hory Mountains, Czechoslovakia, where the air pollution is characterized as moderate. Samples were collected from three stands: a spruce forest, the waterlogged margin of a peat bog, and the peat bog itself. The biomass of fruiting bodies of all macrofungi was determined simultaneously. The trace element concentrations varied among trophic groups of fungi: saprophytic species (S) and those parasitic on Sphagnum (Sph) exhibited the highest concentrations, while wood-decomposing (Wd) species displayed the lowest. Several species mycorrhizal with spruce (Ms), such as Amanita umbrinolutea, Russula ochroleuca, and Xerocomus badius, also attained higher concentrations than were found for other mycorrhizal fungi. The trace element concentrations were higher in the caps than in the stems of the fungi. The fraction of trace metals retained by the biomass of fruiting bodies of fungi with respect to annual fallout is estimated at 1%o. Factors affecting fungal uptake of trace elements are discussed.
INTRODUCTION The incidence, distribution and accumulation of trace elements in various parts of the environment have been attracting considerable attention, mainly because of their potential toxicity. Although many attempts have been made to reach a better understanding of the role of trace elements in fruiting bodies of f u n g i ( C r o n m a r c k e t al., 1975; H i n n e r i , 1975; D r b a l a n d K a l a G 1976; S e e g e r e t al., 1976; D r b a l e t al., 1975a,b; E n k e e t al., 1977, 1979; M c G r e i g h t a n d S c h r o e d e r , 1977; L a a k s o v i r t a a n d A l a k u i j a l a , 1978; O h t o n e n , 1978; S e e g e r , 1978; K u t h a n , 1979; M u t s c h e t al., 1979; T y l e r , 1980, 1982a, b; V o g t a n d E d m o n d s , 1980; L o d e n i u s , 1981; R i i h l i n g et al., 1983; T r e p t o w a n d L i s t , 1983) o u r k n o w l e d g e is s t i l l i n c o m p l e t e . T h e p r e s e n t p a p e r c o n s i d e r s t h e Pb, Cd, Cu, F e , M n , Zn, C o a n d Ni contents of different fungal species from three characteristic stands of the k r u ~ n 6 H o r y M o u n t a i n s , w h e r e t h e a i r p o l l u t i o n is m o d e r a t e ( ~ k o d a , 1980).
0048-9697/88/$03.50
© 1988 Elsevier Science Publishers B.V.
118 MATERIALS AND METHODS
The study area is situated in the Kru~n~ Hory Mountains, Czechoslovakia (lat. 05°24'N, long. 12°55'E, ~1030m above sea level), in the Bo~idarsk~ Ra~elini~t~ nature reserve which consists of several peat bogs and natural spruce forests. The climate of the area is characterized by an average annual temperature of 4°C and average annual precipitation of 1150 mm; snow cover persists for 140 days of the year, with a maximum thickness of 100-150cm. Fogs are most frequent in August and September, and occur on average about 100 days per year. The directions of the dominant winds are W, NW and SW (Quitt, 1971; BSer and Veseck:~, 1975). Nutrient-poor, humic-ferric podsols cover a phyllite substrate. The Mrtv:~ Rybnlk, our study area, is a peat bog of the watershed type which originates at the points of issue of underground water (Dohnal, 1965). The most important sources of atmospheric pollution are from brown-coalfired power stations and opencast mines in the basin of the Kru~n6 Hory Mountains. The study area lies 30 km NWW of the coal-fired power station at Prun6~ov, 20 km NEE of a coal-fired power station at V~esov~i, and 25-30 km NE and N of opencast mines in the Sokolov basin. The area is not very rich in trace elements (Table 1) (~koda, 1980). Fruiting bodies of fungi were collected from three sampling sites within the study area from May to October 1975 and 1976, for biomass determination and trace metal analyses. The permanent plots, ~ 1 km WSW of Mount ~pi5~k (1116 m above sea level), were situated on a line running from north to south, 800m in length, and represented typical vegetation stands: a spruce forest (stand I), the water-logged margin of the peat bog (stand II) and the central part of the peat bog (stand III). The altitude of all sampling sites was ~ 1030 m. Stand I is covered with a plant community of the association Calamagrostidi villosa~Piceetum typicum Hartmann et J a h n 1976, and the subassociation sphagnetosum, in moist sites. The spruce forest, planted ~ 80 years ago in a natural habitat, is now 8-10m high. The substrate consists of podsolic soil typical of spruce stands. Both the height of the litter (3 cm) and the presence of raw humus are typical of these altitudes (Tables 2 and 3). The species of fungi sampled from the three sites were arranged into five trophic groups: species forming mycorrhizae with Picea abies (Ms), with Pinus mugo (Mp), wood-decomposing species (Wd), various saprophytic species (S) and those parasitic on Sphagnum (Sph). Group Ms was represented by Russula ochroleuca (Pers.) Fr., Amanita umbrinolutea S6cr., R. emetica Fr., Hygrophorus olivaceoalbus (Fr. ex Fr.) Fr., Xerocomus badius (Fr.) Kfihn. ex Gilb., and Cortinarius brunneus Fr.; group Wd was represented by Mycena alcalina (Fr.) Kummer, Gymnopilus sapineus (Fr.) Mre., Calocera viscosa (Pers. ex Fr.) Fr., Naematoloma capnoides (Fr.) Karst., and Fomitopsis pinicola (Sw. ex Fr.) Karst; and group S by Mycena galopoda (Pers. ex Fr.) Kummer, Micromphaleperforans (Hoffm. ex Fr.) Sing., Marasmius androsaceus (L. ex Fr.) Fr., and Glitocybe langei Sing. ex Hora.
12.95 33.56 35.55
T o t a l i n stand: I II III
A m o u n t of element in wet deposition over 1 y e a r (~koda, 1980)
III
II
3.98 1.75 7.22 5.75 2.88 24.93 0.66 34.89
S Wd Ms Sph Sm Ms S Mp
I
Biomass (year 1)
Trophic group
Stand
14 x 10s
79.5 110.7 76.72
56.8 4.8 17.9 45.2 3.7 61.8 9.42 67.3
Pb
Element
7.3 x 105
18.95 35.25 27.77
11.9 0.84 6.21 11.0 2.65 21.6 1.97 25.8
Cd
19.6 x 105
1351 2328 1201
818 74 459 664 81 1583 136 1065
Cu
120 x 10 ~
2631 7056 2779
1373 463 795 3981 329 2746 228 2551
Fe
887 x 105
3663 10175 4693
1132 237 2294 1993 261 7921 188 4505
Zn
The total a m o u n t of trace elements (gg/100m 2) in the b i o m a s s of f r u i t i n g bodies of fungi (g dry w e i g h t / 1 0 0 m 2)
TABLE 1
25 x 10~
400 669 627
246 47 107 248 50 371 41 586
Mn
115.5 320.0 150.2
43.4 12.2 59.9 88.2 24.8 207 7.2 143
Co
47 x 10 ~
29.0 82.3 16.9
20.1 1.1 8.7 41.0 11.4 29.9 3.4 13.5
Ni
120 TABLE 2 The soil profile of stand I Horizon
Depth (cm)
Aoo Ao
0-3 3~
A1
4-10
A2
10-16
Description of the horizon Undecomposed litter of spruce needles and herbs Slightly decomposed litter. Both horizon A00 and A0 richly interwoven with roots of herbs and species of the genus Vaccinium Black fine humus, heavily interwoven with spruce roots and blackberries in the upper part Leached podzol horizon, ash-grey in colour with occasional rock fragments (max. 5 cm); slightly interwoven with spruce roots
S t a n d II is s i t u a t e d at the w a t e r l o g g e d m a r g i n of the peat bog, with the a s s o c i a t i o n Calamagrostidi villosa~Piceetum sphagnetosum H a r t m a n n et J a h n 1967; from 1930 to 1940 the m a r g i n was d r a i n e d and planted with spruce, but now the u n t e n d e d d r a i n a g e system is o v e r g r o w n with v e g e t a t i o n and the trees are dying. The t h i c k n e s s of the peat l a y e r varies from 50 to 80cm, and the u n d e r g r o u n d w a t e r level f r e q u e n t l y r e a c h e s the soil surface; it falls to 10 cm below the soil surface in the driest m o n t h only. Typical h u m m o c k and hollow v e g e t a t i o n is well developed with species of the genus Vaccinium and Sphagnum species (S. robustum, S. fallax) respectively. M y c o r r h i z a l fungi with spruce (Ms) are the most i m p o r t a n t t r o p h i c g r o u p in this stand: Dermocybe uliginosa (Berk) Mos. D. palustris (Mos.) Mos. var. sphagneti (Orton) Mos., Russula paludosa Britz., R. emetica Fr., Lactarius rufus (Scop. ex Fr.) Fr., L. necator (Bull. em. Pers. ex Fr.) Karst., and Paxillus involutus (Batsch. ex Fr.) Fr.; S a p r o p h y t i c species (Sm), n a m e l y Naematoloma elongatipes (Peck.) Sing., are a b u n d a n t on dead parts of Sphagnum; living parts of moss are parasitized by Lyophyllum palustre (Peck.) Sing. and Galerina paludosa (Fr.) Kfihn. S t a n d I I I is in the u n d i s t u r b e d c e n t r a l p a r t of the peat bog, with the associa t i o n Vaccinio uliginosi Pinetum mughi H a r t m a n n et J a h n 1967, w h i c h is TABLE 3 pH in stands I, II and III Stand I Stand II Stand III
A004.3 Living parts of Sphagnum 1-5 cm depth Pinus mugo litter 1-4 cm depth Living parts of Sphagnum 1-4 cm depth
A0 3.8-4.4 4.2 3.8 4.1
A1 3.9-5.0 Peat 5-10 cm 4.4 Peat 5-10 cm 3.84.2
121 characterized by alternating pine-clad (Pinus mugo) sites and open sites mainly covered with cotton grass (Eriophorum vaginatum). After heavy rainfall the level of underground water reaches the soil surface; in the driest months it recedes to 50 cm below the surface. The peat layer is ~ 5 m thick. Most fungal species form mycorrhizae with pine (Mp): Russula decolorans Fr., R. paludosa Britz., R. emetica Fr., Lactarius rufus (Scop. ex Fr.) Fr., L. helvus (Fr.) Fr., Suillus flavidus (Fr. ex Fr.) Presl., S. variegatus (Schwartz ex Fr.) Kuntze, Hebeloma longicaudum (Pers. ex Fr.) Kummer, and various species of the genus Cortinarius. Saprophytic species (S) grow on various substrates, e.g. Galerina luteofulva Orton, Rhodphyllus cetratus (Fr.) Qu61. and Naematoloma udum (Pers. ex Fr.) Karst. on peat; numerous species of the genus Galerina on mosses; and Mycena galopoda (Pers. ex Fr.) Kummer and Marasmius androsaceus (L. ex Fr.) Fr. on litter. Permanent sampling plots were selected for each stand; three for stand I, one for stand II and two for stand III, all 30 × 30 m square. We sampled fungi in intervals from 7 to 14 days, and collected all fruiting bodies present in the plot. These were cleaned, placed in filter-paper bags, dried at 95-105°C and weighed so as to determine their dry matter weight. The major species (Hering, 1966), i.e. species with a weight production of fruiting bodies of at least 5%, were taken from each stand for metal analysis, the cap and the stem being treated separately; small fruiting bodies were treated as a whole. The samples were crushed in polythene bags, and 2 g of each sample was digested in HNO3 and H202. The methods used for trace element determination were stripping voltammetry (Vydra et al., 1977) for Pb, Cd and Cu, and atomic absorption spectrometry (AAS) for Mn, Fe, Zn, Ni and Co, using a Perkin Elmer model 400. The two methods have been described in detail by Guy and Chakrabarti (1977). The results were subjected to the t-test and one-way analysis of variance (Dixon and Brown, 1977). RESULTS AND DISCUSSION We identified 51 species of fungi (mainly Agaricales and Aphyllophorales) in samples from the permanent plots of the three stands. Eight species live saprophytically on various dead materials (e.g., needles, cones, leaves, moss, peat, decomposed litter, etc.), 10 species grow on dead wood (branches, stems and stumps of spruce), 20 species are considered to form ectomycorrhizae with spruce and/or pine, and two species are parasites on Sphagnum. We determined the biomass of the fruiting bodies for all stands, and evaluated the share of the main trophic groups to total biomass production (Table 4). Biomass production by fungi may be influenced by, among other factors, the concentrations of elements in the upper litter and humus horizon and by chemical processes. Lawrey (1978) found that the concentrations of trace
Galerina paludosa Strophariaceae Naematoloma capnoides N. elongatipes Russulaceae Lactarius rufus
var. s p h a g n e t i
Dermocybe palustris
Cortinariaceae Dermocybe uliginosa
Amanitaceae Amanita umbrinolutea
Family Species
0.46 0.10 0.17 0.14 0.10 0.13
l0
C S
1.48 0.74 0.62 0.24 1.33 0.54 0.44 0.21
2.66 1.83 0.66 0.03 1.89 1.26 0.28 0.04 1.30 0.98 0.92 0.46
0.65 0.55 0.24 0.13 0.16 1.85
~
Cu
2.1 4.2
sx
19.7 12.6
132 75.5 28.2
8.5 5.0
9.9 4.9 13.7
38.5 15.5 28.1 6.3 54.4 11.2 42.0 20.2 29.4 10.0 46.8 39.1
2.06 268 2.27 104
sx
2 C S 7 W
0.36 0.53 1.48 0.82 0.77 2.16
6.3 0.09 9.25 4.12 0.21 5.98
5c
2.59 2.59 2.96 2.48 2.22 6.07
C S
sx
Cd
3 C S 2 C S 5 W 2 W
2
5c
n a pb Pb
74 83
178 70 90
197 116 119 153 194 180
380 264
~c
Zn
14.1 10.2
~
32.2 20.6
12.3 13.1
19.1 29.4 17.5 15.9 48.4 17.5
45.2 22.1 21.8 22.4 122 21.8 14.1 19.8 78.8 19.~ 13.4 44.7
149 23.3
sx
Mn
3.7 5.11
2.1 9.1 4.8
8.62 40.7 18.7 12.2 10.6 0.7
4.73 2.75
sx
55.2 33.2
sx
59 48
200 123 114
25.8 28.5
32.5 66.3 56.2
170 50.6 259 204 194 100 149 73.3 165 63.8 310 63.6
135 100
5c
Fe
C o n c e n t r a t i o n s of trace e l e m e n t s (~gg ' dry wt.) in the fruiting bodies of selected fungal species
TABLE 4
0.7 0.6
7.6 0.5 8.6
Yc
Co
0.17 0.05
Sm
Wd
Sph
Ms
Ms
Ms
Trophic group
II, III Ms, Mp
0.4 0.28 ! 0.2 0.2 3.95 0.78 I! 0.53 0.2 0.6 0.1
1.2 0.1 4.3
0.33 I 0.36
sx
Stand
0.32 0.37 II 0.90 0.68 1.70 1.44 II 1.90 0.11 2.20 1.56 6.75 1.20 II
0.23 2.9 0.37 3.4
sx
5.0 4.54 16.4 6.83 65.1 28.2 5.3 1.7 12.8 5.3 3.8 0.78
8.8 1.7
5c
Ni
1.61 2.75 4.66 2.94 1.80 0.42 1.24 4.10 2.92 3.40 2.20
0.60 0.24 0.41 0.62 0.23 0.69 1.08 2.71 1.72 1.58 0.31
0.24 0.13 0.32 0.19 0.11 0.51 0.54 0.99 0.48 0.40 0.58
2.37 1.64 2.11 0.56 0.63 0.25
2.45 1.70 0.82 0.73 2.57 3.26
3 C S 2 C S 4 C S
1.22 0.46 0.22 0.01 1.00 0.99
1.84 0.63 0.13 0.84 0.52 0.49 0.07 0.37 0.14
0.11
1.61 2.17 0.83 4.59 5.78 0.75 0.67 0.51 0.53
0.57 0.71 0.51 0.97 0.33 0.14 0.97 0.57 0.49 0.56 0.41
7 W
8 W 9.24 5 W 14.3 2 W 3.63
2 C S 3 W 4 C S 6 C S 4 C S 6 C S
15.6
24.8 44.4 16.7
104 44.0 51.9 13.1 16.3 5.9 5.1 0.7 17.7 2.9 11.0 4.0
56.8
146 206 39.1
25.1 8.8 15.5 7.5 28.9 1.7 110 28.2 49.7 11.8 11.9 11.8 12.8 6.3 189 72.8 158 62.1 65.1 7.6 39.9 5.9
41.1
489 13.1 316 41.0 119 48.7 58 15.4 142 12.0 82 16.4
202 12.3 8.9 11.7 6.9 21.0 33.4
8.8 3.76 2.5 0.91 3.57 4.35 7.87
1.89
17.3 8.75 0.9
15.2 1.7 13.5 2.33 12.8 4.12 19.8 2.65 8.6 2.3 15.9 10.0 18.6 6.0 17.4 0.62 11.3 1.15 24.0 1.66 15.1 2.16
263 30.1 47.9 284 23.8 61.8 159 19.1 35.0
122 50.8 99 53.2 132 27.2 243 28.2 184 10.2 74 72.6 80 50.4 1081 114 787 129 251 25.6 172 7.8
115 111 49 36 95 175
76
30.5 10.0 39.1 17.9 14.6 69.4
62.3
4.6 6.1 0.7 0.4 7.6 5.4
4.2
20.1 10.9 12.7
0.15 0.54 1.8 0.6 0.2 0.33 0.9 1.2 0.52 0.3 0.4
Ms Mp
I, II III
0.99 I 0.33 0.94 II 0.34 0.85 III 0.12
Mp
Mp
Ms
Ms
Sph S Wd
Mp
III
II ! I
Ms
I
II, III Ms, Mp
Mp
III
1.46 0.82 I, II
8.08 2.42 5.04 3.32 1.24 0.62
0.2 1.0 2.1 0.8 0.2 0.3 0.6 1.7 1.3 0.4 0.4
2.65 0.6 1.41 0.4 0.62 1.4 0.43 1.6 8.7 0.6 5.3 0.2
1.35
10.6 9.2 0.92
0.4 1.3 0.07 25.9 1.4 0.4 37.9 12.3 10.2 20.9 2.5 2.1 16.7 2.4 2.9 32.8 1.5 1.03 33.1 0.8 0.85 30.9 2.6 1.3 14.9 1.9 0.93 23.1 6.2 5.0 23.8 18.8 9.7
833 346 345 170 470 227
55 61 89 66 51 44 68 63 50 94 73
an = n u m b e r of samples.bp = p a r t of f r u i t i n g body: C = cap, S = stem and W = whole fruiting body; o t h e r e x p l a n a t i o n s in Table 3.
S. flavidus
Suillus variegatus
Tricholomataceae Lyophyllum palustre Mycena galopoda M. alcalina Paxillaceae Paxillus involutus Boletaceae Xerocomus badius
R. paludosa
R. ochroleuca
R. emetica
L. necator Russula decolorans
L. helvus
¢.O
124
elements were higher in the litter than in needles attached to the branches. Trace element concentrations in the litter increase by processes associated with microbial decomposition. Airborne trace elements are retained in the upper soil horizon due to binding of the metals by humic substances. Therefore, the highest microbial activity is associated with litter decomposition, nutrient cycling and nitrogen fixation; mycorrhizae formation occurs in areas of elevated metal concentrations. We analysed 20 species of fungi belonging to seven families (Table 4). The trace element concentrations were highest in fungi of the family Tricholomataceae: the saprophytic species Mycena galopoda inhabiting various kinds of litter, and Lyphyllum palustre, the Sphagnum parasite; and in fungi of the family Amanitaceae; Amanita umbrinolutea, the species mycorrhizal with spruce. Galerina paludosa (fam. Cortinariaceae), Russula ochroleuca (fam. Russulaceae) and Xerocomus badius (Boletaceae) also exhibited higher trace element concentrations than other fungal species. The trophic groups of fungi (MPa, S, Wd, Sm, Sph; whole fruiting bodies) differ significantly in concentrations of all trace elements except cobalt (ANOVA, P < 0.01) (Table 5). The trace element concentrations in fungi mycorrhizal with spruce (MPa) were slightly higher than in those mycorrhizal with pine (MPm). The differences between these two trophic groups (MPa and MPm) were significant for Zn, Ni and Cu (both in caps and stems), for Fe and Pb in the caps only, and for Cd in the stems only (t-test, P < 0.05). Data on the trace elements and their quantitative evaluation suggest that the bioaccumulation of some elements is species specific (Tyler, 1980, 1982a, b). It depends on the ability of the species to extract elements from the substrate, and on the selective uptake and deposition of elements in tissues. The concentration of cadmium (and other trace elements) in plants was found to depend not only on the concentration of the metal in the soil but also on a number of soil and climatic conditions and on the physiology of the plant. The acidity of the substrate was one of the most important factors influencing cadmium uptake by the plant and the movement of cadmium through the plant. The cadmium concentration of the plant tissues increased with increasing soil acidity (Page et al., 1981). Soil acidity is becoming an important factor in certain localities (Table 3) because it is increasing as a result of acid rain. Relatively high trace element concentrations were found for fungi parasitic on moss, Lyophyllum palustre and Galerina paludosa; this was not surprising as Sphagnum is able to accumulate increased amounts of trace elements (Pucket and Burton, 1981). The physiology of mycorrhizal fungi is relatively uniform; they differ mainly in their requirements concerning the species of the host plant and perhaps in requirements concerning the stand. Mycorrhizal fungi favourably influence the uptake of phosphorus. Bolland et al. (1977) found that the presence of phosphates increased the adsorption of several microelements in the soil and thus diminished their solubility. The low phosphorus pool in the soil may be
C S W C S W W C S W W W
Ms
Sm Sph
S Wd
Mp
p
Trophic group
16 16 16 30 31 1 5 2 2 2 7 10
n
2.17 2.18 2.55 2.01 1.83 2.42 14.28 2.68 1.89 3.63 1.30 8.60
Pb
4.59 1.82 1.26 0.66 0.98 2.08
1.3 0.86 1.23 1.27 0.96
sx 1.40 0.94 0.24 0.94 0.52 1.42 2.78 0.66 0.28 0.51 0.92 2.10
2
Cd
0.75 0.03 0.35 0.53 0.46 0.75
1.22 0.75 0.24 0.58 0.42
sx 86.1 63.1 41.4 38.8 22.2 40.6 20.6 132 75.5 39.1 28.2 126
2
Cu
44.4 9.9 4.9 17.4 13.7 47.3
77.4 65.1 17.9 36.2 16.7
sx 445 318 189 145 112 181 284 176 69.6 159 70.7 246
2
Zn
23.8 19.1 17.5 19.1 48.4 44.3
409 298 58.3 86.6 52.8
sx 16.7 13.8 14.1 17.2 16.4 16.8 61.8 29.4 15.9 35.0 17.5 47.3
~
Mn
8.5 8.1 9.1 0.9 4.8 15.3
7.5 7.7 8.2 7.1 8.7
sx
107 109 115 68.3 76.4 116 345 200 123 471 114 728
2
Fe
170 32.5 66.3 267 56.2 377
68.6 116 72.4 29.1 50.8
sx
10.9 5.6 8.5 3.5 4.7 2.9 10.9 7.6 0.5 12.7 8.6 16.8
2
Co
C o n c e n t r a t i o n s of t r a c e e l e m e n t s i n f r u i t i n g b o d i e s of f u n g i of s e l e c t e d t r o p h i c g r o u p s ; for e x p l a n a t i o n s see t e x t a n d T a b l e 4
TABLE 5
9.2 1.2 0.1 0.92 4.3 11.6
22.5 6.5 6.4 4.7 7.7
sx
0.90 0.99 1.72 0.41 0.35 0.66 5.04 0.39 0.15 1.24 3.95 7.8
x
Ni
3.32 0.28 0.20 0.62 0.78 2.3
1.01 0.77 1.27 0.54 0.49
sx
126 further reduced by mycorrhizae, which contributes to the mobility of trace elements and also to their transport to the plant (Tinker, 1975). The uptake and transport of trace elements seems to differ in the various species ofmycorrhizal fungi, but reliable evidence is still lacking. According to our results, a greater amount of trace elements was bound in the fruiting bodies of mycorrhizal fungi than in those of saprophytic fungi, since mycorrhizal fungi form larger fruiting bodies and produce a greater biomass than saprophytic fungal species (Table 1). It was calculated that fruiting bodies of fungi accumulate in their biomass only ~ 1%o of the annual wet deposition (Table 1). Although wet deposition on the surface of fruiting bodies is apparently of little importance, the effect of dry deposition may be considerable, particularly in heavily polluted areas (Lep§ov~ and Kr~l, 1988). The substrate seems to be the main source of fungal uptake of trace elements. This assumption is supported by the fact that the mycelium of macrofungi develops mostly in the layer of raw humus, i.e. in the uppermost soil horizons (5-10cm), where the concentrations of trace elements are reported to be highest (Heinrichs and Mayer, 1977; Lawrey, 1978). Trace element concentrations in fungi are considerably higher than those in agricultural crop plants, vegetables and fruit (Treptow and List, 1983). This would suggest that fungi possess a very effective mechanism that enables them to take up some trace elements from the substrate more readily. This mechanism may be more effective in the parasitic and saprophytic fungi trophic groups than in the mycorrhizal fungi group. CONCLUSIONS These investigations were conducted in 1975 and 1976 in three typical stands from the Bo~idarsk6 ra§elini§t6 peat bog. We identified 26 species of saprophytic fungi growing on different substrates, 10 wood-decomposing species, two species parasitic on Sphagnum, and 21 mycorrhizal species mainly of the orders Agaricales and Aphyllophorales. Twenty of these fungal species were selected for analysis in order to determine the concentrations of trace elements (Pb, Cd, Cu, Zn, Fe, Mn, Ni and Co) in the fruiting bodies. Our results show that the concentrations of trace elements in the fruiting bodies of fungi tend to be species specific. We observed increased trace element concentrations for all fungal species. The species Amantia umbrinolutea,
Russula ochroleuca, Xerocomus badius, Lyophyllum palustre, Galerina paludosa and Mycena galopoda accumulated trace elements in higher concentrations than the remaining species. In general the concentrations were higher in the caps than in the stems of the fungi. The concentrations were found to depend on the physiology of the species, and particularly on its trophic pattern. They were highest in saprophytic species, lower in those parasitic on Sphagnum and those producing mycorrhizae with spruce and pine, and lowest in species saprophytic on wood.
127 O w i n g to t h e s h o r t life of t h e f r u i t i n g b o d i e s (7-14 days), n e i t h e r d r y n o r w e t d e p o s i t i o n o n t h e s u r f a c e of t h e c a p a p p r e c i a b l y i n f l u e n c e d t h e c o n c e n t r a t i o n s of trace e l e m e n t s in the fungi in this m o d e r a t e l y p o l l u t e d area. H i g h e r t r a c e e l e m e n t c o n c e n t r a t i o n s w e r e f o u n d for f u n g i f r o m t h e s p r u c e s t a n d (I) t h a n for t h o s e f r o m t h e o t h e r t w o s t a n d s - - t h e w a t e r l o g g e d m a r g i n of t h e p e a t b o g (II) a n d t h e p e a t b o g i t s e l f (III). D i f f e r e n c e s i n t r a c e e l e m e n t c o n c e n t r a t i o n s from one y e a r to the n e x t were n o t significant. ACKNOWLEDGEMENTS T h a n k s a r e d u e to D r R. K r ~ l a n d D r R. H a l e § for t h e i r a s s i s t a n c e i n s a m p l e a n a l y s e s , a n d D r J. Lep~ for s t a t i s t i c a l e v a l u a t i o n of t h e a n a l y t i c a l r e s u l t s . O u r t h a n k s a l s o t o M r s L. M i k o v c o v ~ a n d M. S k o ~ e p o v ~ for t h e i r t e c h n i c a l a s s i s t a n c e i n t h e t r e a t m e n t of t h e s a m p l e s , a n d p a r t i c u l a r l y to M r s H. L e t o v s k ~ for h e r h e l p i n c o l l e c t i n g s a m p l e s o f f r u i t i n g b o d i e s f r o m t h e p e r m a n e n t plots. REFERENCES B6er, W. and A. Veseck~, 1975. Podnebl a po~asi Kru~n~ch hor. ~esk~ Hydrometeorologick:~ l~stav, Praha. Bolland, M.D.A., A.M. Posner and J.P. Quirk, 1977. ZH adsorption by goethite in the absence and presence of phosphate. J. Soil. Res., 15: 27~286. Cronmarck, K., R.L. Todd and C.D. Monk, 1975. Patterns of basidiomycete nutrient accumulation in conifer and deciduous forest litter. Soil Biol. Biochem. 7: 265-268. Dixon, W.J. and M.B. Brown, 1977. BMDP-77. Biomedical Computer Programs. P-Series. University of California, Berkeley. Dohnal, J., 1965. ~eskoslovensk~i ra~elini§t~ a slatini§t~. SZN, Praha. Drbal, K. and P. Kala~, 1976. Obsah kobaltu v n~kter:~ch druzlch jedl:~ch hub. ~es. Mykol., 28: 24 26. Drbal, K. and P. KalaS, A. ~eflov~ and J. ~efl, 1975a. Obsah stopov:~ch prvku ~eleza a manganu v n~kter~ch druzich jedl:~ch hub. ~eska Mykol., 29: 110-114. Drbal, K., P. KalaS, A. ~eflov~ and ~efl, 1975b. Obsah m~di (Cu) v n~kter~ch druzich jedl~ch hub. ~eska Mykol., 29: 184-186. Enke, M., H. Matschiner and M.K. Achtzehn, 1977. Heavy metal enrichments in mushrooms. Nahrung, 21:331 334. Enke, M., M. Roschig, H. Matschiner and M.K. Achtzehn, 1979. Zur Blei-, Cadmium- und Quecksilber- Aufnahme in Kultur-champignons. Nahrung, 23:731 737. Guy, R.D. and C.L. Chakrabarti, 1977. Analytical techniques for speciation in trace metals. International Congress on Heavy Metals in the Environment. Toronoto. Heinrichs, H. and R. Mayer, 1977. Distribution and cycling of major and trace elements in two Central European forest ecosystems. J. Environ. Qual., 6: 402-407. Hering, T.F., 1966. The terricolous higher fungi of four Lake District woodlands. Trans. Br. Mycol. Soc., 42: 1-14. Hinneri, S., 1975. Mineral elements of macrofungi in oak-rich forest on Lenholm Island inner archipelago of SW Finland. Ann. Bot. Fenn., 12: 135-140. Kuthan, J., 1979. Die Auswertung des Bleigehaltes in Bronze-RShling-Boletus aureus Bull. ex Fr. entlang einer der Verkehrasandern in Bulgarien. ~eska Mykol., 33: 58-59. Lasksovirta, K. and A.P. Alakuijala, 1978. Lead, cadmium and zinc contents of fungi in the parks of Helsinki. Ann. Bot. Fenn., 15: 254-257. Lawrey, J.D., 1978. Trace metal dynamics in decomposing leaf litter in habitats variously influenced by coal strip mining. Can. J. Bot., 56: 953-962. -
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