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Habitat differences of coprophilous fungi on moose dung
Mycol. Res. 106 (11): 1360–1366 (November 2002). f The British Mycological Society
1360
DOI: 10.1017/S0953756202006597 Printed in the United Kingdom.
Habitat differences of coprophilous fungi on moose dung
A˚sa NYBERG1 and Inga-Lill PERSSON2 1
Department of Ecology and Environmental Science, Umea˚ University, SE-901 87 Umea˚, Sweden. Department of Animal Ecology, Swedish University of Agricultural Sciences, SE-901 83 Umea˚, Sweden. E-mail : [email protected]
2
Received 20 September 2001; accepted 10 August 2002.
This study aimed to test whether fungal community on moose (Alces alces) dung is affected by habitat. We used dung of homogenous origin, composition, and age. Dung was placed in three different habitats in north-eastern Sweden, and was checked again after 35–36 d. Of the 26 species of fungi found, 12 were new to the region, 17 had never been observed on moose dung, and two were not previously described. We found a significant difference in species composition between the habitats, with a low number of species in the spruce forest and about a threefold increase in the pine forest and the open mire. Species diversity was negatively associated with degree of insect attack. This suggests that insects feeding either on the dung or the fungi (spores, mycelia) may be an important factor explaining the observed pattern. In order to test this hypothesis we need to run experiments excluding insects.
INTRODUCTION Many species of fungi, mosses and invertebrates are specialised to live on dung (Marino 1988, Hanski & Cambefort 1991, Dix & Webster 1995). However, most studies of coprophilous organisms have focused on fungi or beetles (Coleoptera) on domesticated animal dung in grasslands (Dickinson & Underhay 1977, Wicklow & Hirschfield 1979, Lussenhop et al. 1980). The most species-rich substrates are cattle and cervid dung (Larsen 1971, Richardson 2001). Another wellstudied substrate is rabbit dung (Angel & Wicklow 1975, Wicklow, Angel & Lussenhop 1980, Yocom & Wicklow 1980). In general, dung from wild boreal animals, and especially forest-living species such as moose Alces alces, reindeer Rangifer tarandus, and roe deer Capreolus capreolus, have been studied less. Here we focus on moose dung. A number of coprophilous fungi, mosses (especially Splachnum) and invertebrates live on moose dung (Eriksson 1992, Marino 1988), but little is known about the community composition. Neither do we know much about the influence of habitat types on community composition, although existing data indicate such differences (Lundqvist 1972, Lussenhop et al. 1980). Differences in community composition may be due to abiotic or biotic factors. Temperature and moisture are documented to affect growth rate, fruiting and species richness of coprophilous fungi (Wicklow & Moore 1974, Harrower & Nagy 1979, Kuthubutheen & Webster
1986), as well as the survival of coprophagous insect larvae (Hughes & Sands 1979). Intra- and interspecific interactions occur at the scale of the individual dung pile and have been shown to affect fungal development, as well as species composition (Ikediugwu & Webster 1970, Wicklow & Hirschfield 1979, Anson, Fisher & Kuthubutheen 1985). The outcome of these interactions can be expected to vary with habitat type. The aim of our study was to investigate the effect of habitat on coprophilous fungi developing in newly deposited, uniform moose dung. Since earlier studies frequently have shown that temperature and humidity are key factors for fungal communities, we chose three different habitats : one sunny and dry, one shady and mesic and one sunny and wet.
MATERIALS AND METHODS The study was carried out close to Bjurholm (63x 50k N, 20x 18k E) in the province of A˚ngermanland in northeast Sweden, 70 km west of Umea˚. Three sites representing common habitat types in the middle boreal forest were selected : (1) Mature pine forest (sunny and dry). The tree layer consisted of Scots pine (Pinus sylvestris), and the ground vegetation consisted of 40 % (estimated as % cover) heather (Calluna vulgaris), 40 % cowberry (Vaccinium vitis-idaea) and 20 % crowberry (Empetrum hermaphroditum). Bilberry (Vaccinium
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Table 1. List of the observed fungal species, with data on substrate preference and distribution in Sweden. New records in the A˚ngermanland province (A˚) and on moose dung (M) are denoted. – , no data found in the literature. Species
Substrate
Distribution
New records
Zygomycota Pilobolus crystallinus
D, H, R, Sq2
–a
A˚, M
Basidiomycota Coprinus sp. Sp. 1.
– –
–a –a
Ascomycota (discomycetes) Ascobolus furfuraceus A. sacchariferus Ascobolus sp. 1 Cheilymenia fimicola C. stercorea Coprotus aurorus Lasiobolus lasioboloides L. papillatus Saccobolus versicolor Thelebolus caninus T. microsporus
C, D, H, R2, He4 M, D, R5, D1, He4 – C4 D2, He4 C2 – C, D, H, R, S2, B, He4 C, D, H, R, Mu2, B, He4 Do2, B, Ca, He4 C, D, R2, B, Ca, He4
Common4 Occasional in the hemiboreal and boreal zone4 – Occasional in the temperate, hemiboreal and boreal zone4 Common4 Found in the country but frequency and distribution unknown4 – Upl8, common4 Upl1, common4 Found in the country but frequency and distribution unknown4 Common4
M A˚
Ascomycota (pyrenomycetes) Arnium caballinum Podospora myriospora Schizothecium fimicola S. vesticola Sordaria fimicola Sporormiella intermedia S. irregularis S. lageniformis S. megalospora S. minima Sporormiella sp. 1 Sporormiella sp. 2
H, C3, ReD, S5 C3 H, C3, S6 Esp. C, H3, S6 Various, H, M, C3, Ha6 C, Ha, H, S3 C, M, H, R, ReiD, RoD3 H3 C3 C, M, Ha, H, R3, S6 Various7 M7
O¨l, Upl, Mpd, Hrj, Jmt3 Bh, Srm, Upl, Vstm, Dlr, TL3 Gstr, Jmt, Vb: all over Nordic area3 Dlr, Sm, Upl6 Common in whole Scandinavia3 Dlr, Sm, Upl6 Sk–Lpl3 Sk–Lpl, common, widespread3 Sk, Bl, Sm, O¨l, Gtl, O¨g, Vg, Hl, Nrk, Srm, Upl, A˚ng, Hrj, Jmt, Nb3 Sk–TL (except Bl, Dls, Bh, Vrm)3 Sk, Bl, Sm O¨l, Gtl, Hl, Vg, Dls, Srm, Upl, Hls, Hrj, Jmt, TL3 Sk, Bl, Sm, O¨l, Gtl, Vg, Hl, Bh, Vrm, Upl, Hls, Nb3 –a –a
A˚, M A˚, M M M
A˚, M M A˚, M A˚, M M M A˚, M M
M M A˚, M A˚ A˚ A˚
Abbreviations for substrates: B, bird (Aves sp.); C, cow (Bos taurus); Ca, carnivore; D, deer (Cervidae spp.); Do, dog (Canis familiaris) ; H, horse (Equus caballus); Ha, hare (Lepus sp.); He, herbivore ; M, moose (Alces alces) ; Mu, mouse (Mus sp.); R, rabbit (Oryctolagus cuniculus) ; ReD, red deer (Cervus elaphus) ; ReiD, reindeer (Rangifer tarandus) ; RoD, roe deer (Capreolus capreolus) ; S, sheep (Ovis aries); and Sq, squirrel (Scuridae spp.). Abbreviations for Swedish provinces: Bohusla¨n (Bl), Dalarna (Dlr), Dalsland (Dls), Gotland (Gtl), Ga¨strikland (Gstr), Halland (Hl), Ha¨lsingland (Hls), Ha¨rjedalen (Hrj), Ja¨mtland (Jmt), Lappland (Lpl), Medelpad (Mpd), Norrbotten (Nb), Na¨rke (Nrk), Ska˚ne (Sk), Sma˚land (Sm), So¨rmland (Srm), Torne Lappmark (TL) Uppland (Upl), Va¨rmland (Vrm), Va¨stergo¨tland (Vg), Va¨stmanland (Vstm), Va¨sterbotten (Vb), A˚ngermanland (A˚ng), O¨land (O¨l), and O¨stergo¨tland (O¨g). 1 5 Brummelen (1967). Lundqvist (1972). 2 6 Ellis & Ellis (1998). Lundqvist (1997). 3 7 Eriksson (1992). Nils Lundqvist (pers. comm.). 4 8 Hansen & Knudsen (2000). Lundqvist & Ryman (1976).
myrtillus) occurred sparsely. The bottom layer consisted of 70 % lichens (mainly Cladonia spp.) and 30% mosses. (2) Mature spruce-pine forest (hereafter referred to as spruce forest, shady and mesic). The tree layer consisted of 70% Scots pine, 30 % Norway spruce (Picea abies) and some small birches (Betula pubescens), aspen (Populus tremula) and rowan (Sorbus aucuparia). The ground vegetation consisted of 80% bilberry and 20 % cowberry. The herbs Maianthemum bifolium and Linnaea borealis also occurred sparsely. The bottom layer consisted of 80% mosses, 10% lichens, and 10% barren ground (stones). (3) Mire (sunny and wet). The tree layer consisted of 90 % Scots pine and 10 % small birches. The ground vegetation consisted of 50% Eriophorum vaginatum and Carex globularis, 20 % heather, 10 % crowberry, 10% bog whortleberry (Vaccinium uliginosum), 5 % cloudberry (Rubus chamaemorus) and 5 %
dwarf birch (Betula nana). Bilberry, cranberry (Vaccinium oxycoccus) and Andromeda polifolia occurred sparsely. The bottom layer consisted of 90 % mosses (mainly Sphagnum spp.) and 10% lichens (mainly Cladonia spp.). 113 dung piles from six captive moose calves (2–2.5 months old) was collected at a nearby moose farm during the first week of August 2000. The calves were kept in a natural pasture and fed the same diet. About 80 % (volume) of their diet consisted of natural summer food for moose (leaves from deciduous trees, grasses and herbs), and about 20% supplemental food (Ren Forbas, Fori Foderringen Handelsbolag, Holmsund). The consistency of the moose dung resembled dung from domestic cattle, which is common for moose in summer (Schwartz & Renecker 1998). To avoid biases in the results due to decomposition processes that
Habitat differences of coprophilous organisms
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Table 2. Frequency of occurrence of each species recorded on moose dung in three habitat types in northern Sweden. n=15 in all habitats.
100
Pine forest
Spruce forest
Mire
Zygomycota Pilobolus crystallinus
1
0
4
Basidiomycota Coprinus sp. Sp. 1
2 0
1 0
4 1
Ascomycota (discomycetes) Ascobolus furfuraceus A. sacchariferus Ascobolus sp. 1 Cheilymenia fimicola C. stercorea Coprotus aurorus Lasiobolus lasioboloides L. papillatus Saccobolus versicolor Thelebolus caninus T. microsporus
1 5 8 2 4 0 1 14 0 3 3
0 3 1 0 3 1 0 5 0 0 0
2 8 5 1 7 0 0 15 3 2 2
Ascomycota (pyrenomycetes) Arnium caballinum Podospora myriospora Schizothecium fimicola S. vesticola Sordaria fimicola Sporormiella intermedia S. irregularis S. lageniformis S. megalospora S. minima Sporormiella sp. 1 Sporormiella sp. 2
0 3 8 2 1 1 2 0 1 0 10 2
1 2 3 0 0 0 0 1 0 0 8 0
1 6 14 1 2 0 1 1 0 1 12 0
F requency (%)
Species
Mire
80
Habitat type
Pine forest Spruce forest
60
40
20
have started before collection, we aimed to collect the dung and place the groups in the selected habitats as soon as possible. No dung was older than 24 h, and the groups were laid out 0.5– 4 h after collection. The experiment used even-aged dung collected from moose with the same diet and thus basically the same inoculum of species. Variables that could have biased the comparisons of dung among habitat types were thus eliminated. The dung was placed in four line transects per habitat type, pine forest (n=38 dung samples), spruce forest (n=38) and mire (n=37). The dung piles were placed on insect nets, marked with a stick and numbered. The distance between each transect and each dung pile was 10 m, and the distance between the different study sites was 10–40 km. Data were sampled at three separate occasions during August and September 2000 (hereafter referred to as 1, 2, and 3, respectively). Sampling (1) was performed at 9–10 d, (2) at 27–28 d, and (3) at 35–36 d after the dung was set out. (1) and (2). Water content was determined at two occasions and the mean value was used in the analyses. The water content of the dung was also used as a measurement of habitat moisture. One subsample per
0
0
3
6
9 12 15 Ranked species
18
21
Fig. 1. The distribution of ranked fungal species found on moose dung in northern Sweden for the three habitat types : pine forest, spruce forest and mire (n=15 for all habitats).
dung sample was taken using a thin spatula and a teaspoon to obtain a sample with material from all layers from the top to the bottom of the group equally represented. Samples were taken from all habitats on the same day under stable weather conditions and were kept in closed test tubes. The fresh weight of the samples were determined in the laboratory (1–6 h after sampling) to 0.1 mg using a Mettler AE 166 scale. The samples were then air dried at room temperature to constant weight, placed in a dessicator for 4–5 h and weighed again to obtain the dry weight. (1) The number of holes visible on the surface of the dung samples, which could be attributed to insect larvae, was counted on all dung samples (n=113) and used as an estimate of insect attack. The number of Diptera, Coleoptera and other invertebrates visible on the surface of the dung was also counted, but was insufficient for statistical analyses. Diptera and Coleoptera larvae seemed to be most common, though. (2) The percent cover of discomycetes was visually estimated. We excluded other ascomycetes because they were more difficult to detect. Also, the number of fruit bodies of basidiomycetes per dung sample was counted, but only a few were found and there was no significant difference among habitats. The percent cover of mosses was visually estimated. No vascular plants were observed to colonise the dung. All dung piles were sampled at this time (n=113). (3) The number of species of fungi was determined by taking samples from the surface of the dung. Fifteen samples from each habitat were analysed, chosen randomly among dung piles from all transects (n=45 dung samples). The samples were kept cold during the species determination in the laboratory, which was made with a stereomicroscope (Zeiss KL2500LCD) and a microscope (Zeiss Axioskop2). The fungi were mounted in glycerol. Voucher specimens are preserved in the herbarium of Umea˚ University UME.
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Table 3. Pairwise comparisons of water content (mean value of the two samplings), species richness, discomycete cover, insect damage and moss cover among three habitat types x2, D.F. and P values are presented for Kruskal–Wallis tests, Z and P values are presented for Wilcoxon tests. Spearman’s Rank Correlation (rs) and P values are presented for correlations between parameters. Bold values indicate statistical significance. x2
D.F.
Water content Pine forest–Mire Spruce forest–Pine forest Spruce forest–Mire
57.37
2
No. of species of fungi Pine forest–Spruce forest Mire–Spruce forest Mire–Pine forest
20.55
Discomycete cover Pine forest–Spruce forest Mire–Spruce forest Mire–Pine forest
16.14
No. of insect holes Pine forest–Mire Spruce forest–Pine forest Spruce forest–Mire
19.12
Cover of mosses Pine forest–Spruce forest Mire–Pine forest Mire–Spruce forest
39.82
Correlations Water content–Moss cover Water content–Discomycete cover Water content–No. of insect holes Water content–No. of fungal species Moss cover–Discomycete cover No. of insect holes–Discomycete cover No. of insect holes–Moss cover Discomycete cover–No. of fungal species No. of fungal species–Moss cover No. of fungal species–No. of insect holes
The data were analysed statistically using the SAS system for Windows (version 6.12). The non-parametric Kruskal Wallis test, Wilcoxon test (for two samples), and the Spearman’s Rank Correlation test, were used to test for habitat differences and correlations.
RESULTS We found 26 species of fungi, representing 14 different genera (Table 1). Amongst these there was one zygomycete and two basidiomycete species ; the remaining 23 species were ascomycetes, represented by 11 discomycetes and 12 pyrenomycetes. Two undescribed Sporormiella species were observed, both related to S. australis and have similar fruit bodies, but differ in spore characters. Sporormiella sp. 1 has been found on various substrates, while Sporormiella sp. 2 has only been found on moose dung (Nils Lundqvist pers. comm.). Twelve of the 26 species found were new to the province of A˚ngermanland, and 17 have not been previously reported from moose dung. Twenty of the fungal species were found in the pine forest, 11 in the spruce forest and 21 on the mire (Table 2). Eight of the species were only observed in one habitat ; four in the pine
Z
rs
P
4.59 4.67 6.51
<0.0001 <0.0001 <0.0001 <0.0001
3.25 3.94 2.25
<0.0001 0.0012 <0.0001 0.0244
2.38 3.91 1.89
0.0003 0.0175 <0.0001 0.0590
1.66 2.69 4.27
<0.0001 0.0961 0.0071 <0.0001
5.74 0.88 6.00
<0.0001 <0.0001 0.3784 <0.0001
2
2
2
2
x0.27 x0.40 0.45 x0.48 0.29 x0.14 x0.27 0.58 0.51 x0.24
0.0045 <0.0001 <0.0001 0.0009 0.0020 0.1301 0.0042 <0.0001 0.0003 0.1072
forest, three on the mire, and one in the spruce forest (Table 2). Eight species occurred only in the pine forest and the mire, and two species were found only in the spruce forest and the mire. Eight species were found in all three habitats. The relative number of dung piles occupied by the various species showed a unimodal distribution in all three habitats (Fig. 1). Most of the species were only found on one or a few dung piles. Six species in the pine forest, five in the spruce forest, and seven on the mire, were found in 10 % or less of the samples. The most common species, all habitats pooled, was Lasiobolus papillatus, which reached a frequency of 76 %; this was the most common species on the mire (frequency 100 %) and the pine forest (frequency 93 %). Sporormiella sp. 1 was the most common species (53 % of the samples) in the spruce forest. The average water content of the samples differed significantly among habitat types (Table 3). It was significantly higher in the spruce forest than in the pine forest and on the mire on both sampling occasions (Fig. 2a). It was also significantly higher in the pine forest than on the mire. We found significant negative correlations between water content and fungal species richness, cover of discomycetes, and moss cover, whereas it was a significant positive correlation between water
Habitat differences of coprophilous organisms
Water content/total weight (%)
(a)
45 b
40 35
Sampling 1 Sampling 2
a
30
e
25 20 15
c
d f
10 5 0
No. of fungal species
(b)
7 6
c a
5 4 3
b
2 1 0
Discomycete cover (%)
(c)
14
a
DISCUSSION
8 6 b
4 2 0
Moss cover (%)
(d)
45 40 35 30
a a
25 20 15 10 5 0
b
7
b
(e)
No. of insect holes
6 5 4
a
3 a
2 1 0
content and the number of insect holes (Table 3). A negative correlation, although not significant, was found between fungal species richness and the number of holes and between the cover of discomycetes and number of holes. The fungal species richness, the percent cover of discomycetes, and the percent cover of mosses, differed significantly among habitats (Fig. 2b, c, d) and were significantly higher in the pine forest and on the mire than in the spruce forest. The species richness was also significantly higher on the mire than in the pine forest, and the discomycete cover and the moss cover showed the same trend, although this was not statistically significant. The number of insect holes per dung pile differed significantly among habitat types (Fig. 2e), and was significantly higher in the spruce forest than in the pine forest and on the mire. We also found a significant negative correlation between number of holes and moss cover (Table 3). There were significant, positive correlations between the cover of discomycetes and fungal species richness, between cover of discomycetes and moss cover, and between fungal species richness and moss cover.
a
12 10
1364
Pine forest
Spruce forest
Our data indicates that the fungal community developing on moose dung is species-rich, but poorly studied so far. In spite of the limited sample size and the use of a homogenous substrate, we found 31 % (9 of 29) of the pyrenomycetes reported on moose dung in Sweden (Eriksson 1992). Twelve of the 26 species have never been reported from the region, 17 have never been reported on moose dung (Table 1), and two species appear to be undescribed. The number of species found appears to be rather high considering both the limitations listed above and that we only examined the samples once. The most comprehensive studies of fungi on cervid dung we can use for comparisons are based on incubated dung samples, examined over a longer time period (Larsen 1971, Richardson 2001). Larsen (1971) found 36 species (on dung of Dama dama, n=10), while Richardson (2001) reported 108 species on deer dung (mean 10.9 spp. samplex1, n=54), after collecting and incubating dung from all over the world over 5.5 yr. Most of the species in our study occurred in low frequency, whereas a small number of species made up the majority of the community. This pattern agrees with Richardson’s (2001) study, but the most abundant species in our study occurred at higher frequencies. This is probably due to the homogenous substrate with a homogenous inoculum, and because our sampling was limited in both space and time.
Mire
Habitat type
Fig. 2. The parameters measured on moose dung in three habitat types in northern Sweden : Water content (a), number of fungal species (b), percent cover of discomycetes (c), percent cover of mosses (d) and number of insect holes on the surface (e).
Mean values and standard errors are presented. Different letters above the bars indicate that they are significantly different from each other. n=15 in chart b. n=38 ( pine forest and spruce forest), and n=37 (mire) in charts a, c, d and e.
A˚sa Nyberg and Inga-Lill Persson Our results show significant differences among habitat types in the occurrence and species richness of coprophilous organisms developing on summer dung of moose. The spruce forest contributed most to the observed differences, but differences between the pine forest and the mire were also evident. As we used uniform dung, assumed to have the same inoculum of species, our data clearly demonstrate that habitat plays an important role in final species composition. This accords with previous studies, which have suggested that communities of coprophilous organisms differ between habitats (Lussenhop et al. 1980, Yocom & Wicklow 1980, Marino 1991a, b). These patterns were opposite to what we expected concerning the development of dung fungi. Fungi are mostly associated with moist habitats, and experiments in vitro have documented higher occurrences of coprophilous fungi when provided with free water (Kuthubutheen & Webster 1986). The dung in the spruce forest had a higher water content than that in the pine forest and on the mire, indicating a moister habitat, probably as a result of more shading from tree crowns. In spite of that, we found the lowest number of fungal species (both total and mean number per dung pile), and fungal cover in the spruce forest. There was a highly significant negative correlation between water content and the number of species of fungi, as well as cover of fungi. Contrary to this, there was a highly positive correlation between water content and number of insect holes. We also found a negative correlation, although not significant, between the number of insect holes and number of fungal species. The lack of significance might be due to differences in the insect species composition among dung piles. Different insect groups might have different impacts on the fungal community. We did not examine the insect fauna, but have the impression that there were differences between dung piles within habitat types. We suggest that the low number of species and percentage cover of fungi on the dung in the spruce forest results from negative effects of more insects in that habitat. Coprophagous insects feed on plant debris and graze on fungal mycelium, spores, and fruit bodies in the dung (Dickinson & Underhay 1977, Lussenhop et al. 1980, Wicklow & Yocom 1982, Stevenson & Dindal 1987, Dix & Webster 1995). Lussenhop et al. (1980) found that coprophagous insects could decrease hyphal density in cattle dung, and Wicklow & Yocom (1982) demonstrated that the number of fungal fruit bodies on rabbit dung incubated with insects declined with increasing insect density. Thus, the explanation for the pattern we observed could be invertebrate feeding on the substrate, feeding on the fungi (mycelia and spores), or a combination of both. The dung in the spruce forest also seemed considerably more disintegrated than that in the pine forest and on the mire, probably as a result of the heavier load of insect larvae. Feeding by coprophagous insects, especially larval dung beetles, can contribute to the crumbling and disruption of dung (Lussenhop et al. 1980, Stevenson &
1365 Dindal 1987). An alternative explanation thus might be that the dung in the spruce forest offered a rather unstable substrate for fungi and prevented their germination or development. The positive correlation between moss cover and fungal species richness, as well as fungal cover, indicates that competitive interactions between mosses and fungi are of minor importance for the community composition. In order to test whether the observed habitat differences are due to insect interaction or not, we need to run experiments excluding insects. This can be done either by treating dung with insecticides or covering it with insect nets. Since different insect species might differ in feeding preferences, we also need data on the insect fauna involved. Inoculations of fungi and insects may be used to further reveal the outcome of these interactions. ACKNOWLEDGEMENTS We thank Christer Johansson for allowing us to collect moose dung at the moose farm in Bjurholm. We are also grateful to Kjell Danell, Lars Ericson, Roger Bergstro¨m, Mats Wedin, and two anonymous reviewers for helpful comments on the manuscript. Special thanks to Nils Lundqvist for help with species identification, and valuable comments on many of the fungal species. This study was financed by the Swedish Council for Forestry and Agricultural Research, the Swedish Environmental Protection Agency, and the Kempe Foundation.
REFERENCES Angel, K. & Wicklow, D. T. (1975) Relationships between coprophilous fungi and fecal substrates in a Colorado grassland. Mycologia 67: 63–74. Anson, A. E., Fisher, P. J. & Kuthubutheen, A. J. (1985) Interactions between Pilobolus crystallinus and Pseudomonas paucimobilis isolated from rabbit dung. Transactions of the British Mycological Society 85: 161–164. Dickinson, C. H. & Underhay, V. H. S. (1977) Growth of fungi in cattle dung. Transactions of the British Mycological Society 69: 473– 477. Dix, N. J. & Webster, J. (1995) Fungal Ecology. Chapman & Hall, London. Ellis, M. B. & Ellis, J. P. (1998) Microfungi on Miscellaneous Substrates. 2nd edn. Richmond Publishing Slough. Eriksson, O. E. (1992). The Non-lichenized Pyrenomycetes of Sweden. Btj tryck, Lund. Hansen, L. & Knudsen, H. (eds) (2000) Nordic Macromycetes. Vol. 1. Ascomycetes. Helsinki University Printing House, Helsinki. Hanski, I. & Cambefort, Y. (eds) (1991) Dung Beetle Ecology. Princeton University Press, Princeton, NJ. Harrower, K. M. & Nagy, L. A. (1979) Effects of nutrients and water stress on growth and sporulation of coprophilous fungi. Transactions of the British Mycological Society 72: 459– 462. Hughes, R. D. & Sands, P. (1979) Modelling bushfly populations. Journal of applied Ecology 16: 117–139. Ikediugwu, F. E. O. & Webster, J. (1970) Antagonism between Coprinus heptemerus and other coprophilous fungi. Transactions of the British Mycological Society 54: 181–204. Kuthubutheen, A. J. & Webster, J. (1986) Water availability and the coprophilous fungus succession. Transactions of the British Mycological Society 86: 63–76. Larsen, K. (1971) Danish endocoprophilous fungi, and their sequence of occurrence. Botanisk Tidsskrift 66 : 1–32. Lundqvist, N. (1972) Nordic Sordariaceae s.lat. Symbolae Botanicae Upsalienses 20 (1) : 1–374.
Habitat differences of coprophilous organisms Lundqvist, N. (1997) Fungi fimicolae exsiccati. Fasc. 4–5 (Nos 76–125). Thunbergia 25: 1–29. Lundqvist, N. & Ryman, S. (1976) Artlista fra˚n 2 :a nordiska mykologiska kongressen i Garpenberg, Dalarna, 28.8.–1.9.1974. Friesia 11: 138–142. [In Swedish]. Lussenhop, J., Kumar, R., Wicklow, D. T. & Lloyd, J. E. (1980) Insect effect on bacteria and fungi in cattle dung. Oikos 34: 54–58. Marino, P. C. (1988) Coexistance on divided habitats: mosses in the family Splachnaceae. Annales Zoologici Fennici 25: 89–98. Marino, P. C. (1991a) Dispersal and coexistance of mosses (Splachnaceae) in patchy habitats. Journal of Ecology 79 : 1047–1060. Marino, P. C. (1991b) Competition between mosses (Splachnaceae) in patchy habitats. Journal of Ecology 79: 1031–1046. Richardson, M. J. (2001) Diversity and occurrence of coprophilous fungi. Mycological Research 105: 387– 402. Schwartz, C. C. & Renecker, L. A. (1998) Nutrition and energetics. In Ecology and Management of the North American Moose. (A. W. Franzmann & C. C. Schwartz, eds): 441– 478. Smithsonian Institution Press, Washington, DC. Stevenson, B. G. & Dindal, D. L. (1987) Functional ecology of coprophagous insects: a review. Pedobiologia 30: 285–298.
1366 van Brummelen, J. (1967) A world-monograph of the genera Ascobolus and Saccobolus (Ascomycetes, Pezizales). Persoonia, Suppl. 1: 1–260. Wicklow, D. T., Angel, K. & Lussenhop, J. (1980) Fungal community expression in lagomorph versus ruminant feces. Mycologia 72: 1015–1021. Wicklow, D. T. & Hirschfield, B. J. (1979) Evidence of a competitive hierarchy among coprophilous fungal populations. Canadian Journal of Microbiology 25 : 855–858. Wicklow, D. T. & Moore, V. (1974) Effect of incubation temperature on the coprophilous fungal succession. Transactions of the British Mycological Society 62: 411– 415. Wicklow, D. T. & Yocom, D. H. (1982) Effect of larval grazing by Lycoriella mali (Diptera:Sciaridae) on species abundance of coprophilous fungi. Transactions of the British Mycological Society 78: 29–32. Yocom, D. H. & Wicklow, D. T. (1980) Community differentiation along a dune succession: an experimental approach with coprophilous fungi. Ecology 61: 868–880.
Corresponding Editor: D. J. Lodge
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DOI: 10.1017/S0953756202006597 Printed in the United Kingdom.
Habitat differences of coprophilous fungi on moose dung
A˚sa NYBERG1 and Inga-Lill PERSSON2 1
Department of Ecology and Environmental Science, Umea˚ University, SE-901 87 Umea˚, Sweden. Department of Animal Ecology, Swedish University of Agricultural Sciences, SE-901 83 Umea˚, Sweden. E-mail : [email protected]
2
Received 20 September 2001; accepted 10 August 2002.
This study aimed to test whether fungal community on moose (Alces alces) dung is affected by habitat. We used dung of homogenous origin, composition, and age. Dung was placed in three different habitats in north-eastern Sweden, and was checked again after 35–36 d. Of the 26 species of fungi found, 12 were new to the region, 17 had never been observed on moose dung, and two were not previously described. We found a significant difference in species composition between the habitats, with a low number of species in the spruce forest and about a threefold increase in the pine forest and the open mire. Species diversity was negatively associated with degree of insect attack. This suggests that insects feeding either on the dung or the fungi (spores, mycelia) may be an important factor explaining the observed pattern. In order to test this hypothesis we need to run experiments excluding insects.
INTRODUCTION Many species of fungi, mosses and invertebrates are specialised to live on dung (Marino 1988, Hanski & Cambefort 1991, Dix & Webster 1995). However, most studies of coprophilous organisms have focused on fungi or beetles (Coleoptera) on domesticated animal dung in grasslands (Dickinson & Underhay 1977, Wicklow & Hirschfield 1979, Lussenhop et al. 1980). The most species-rich substrates are cattle and cervid dung (Larsen 1971, Richardson 2001). Another wellstudied substrate is rabbit dung (Angel & Wicklow 1975, Wicklow, Angel & Lussenhop 1980, Yocom & Wicklow 1980). In general, dung from wild boreal animals, and especially forest-living species such as moose Alces alces, reindeer Rangifer tarandus, and roe deer Capreolus capreolus, have been studied less. Here we focus on moose dung. A number of coprophilous fungi, mosses (especially Splachnum) and invertebrates live on moose dung (Eriksson 1992, Marino 1988), but little is known about the community composition. Neither do we know much about the influence of habitat types on community composition, although existing data indicate such differences (Lundqvist 1972, Lussenhop et al. 1980). Differences in community composition may be due to abiotic or biotic factors. Temperature and moisture are documented to affect growth rate, fruiting and species richness of coprophilous fungi (Wicklow & Moore 1974, Harrower & Nagy 1979, Kuthubutheen & Webster
1986), as well as the survival of coprophagous insect larvae (Hughes & Sands 1979). Intra- and interspecific interactions occur at the scale of the individual dung pile and have been shown to affect fungal development, as well as species composition (Ikediugwu & Webster 1970, Wicklow & Hirschfield 1979, Anson, Fisher & Kuthubutheen 1985). The outcome of these interactions can be expected to vary with habitat type. The aim of our study was to investigate the effect of habitat on coprophilous fungi developing in newly deposited, uniform moose dung. Since earlier studies frequently have shown that temperature and humidity are key factors for fungal communities, we chose three different habitats : one sunny and dry, one shady and mesic and one sunny and wet.
MATERIALS AND METHODS The study was carried out close to Bjurholm (63x 50k N, 20x 18k E) in the province of A˚ngermanland in northeast Sweden, 70 km west of Umea˚. Three sites representing common habitat types in the middle boreal forest were selected : (1) Mature pine forest (sunny and dry). The tree layer consisted of Scots pine (Pinus sylvestris), and the ground vegetation consisted of 40 % (estimated as % cover) heather (Calluna vulgaris), 40 % cowberry (Vaccinium vitis-idaea) and 20 % crowberry (Empetrum hermaphroditum). Bilberry (Vaccinium
A˚sa Nyberg and Inga-Lill Persson
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Table 1. List of the observed fungal species, with data on substrate preference and distribution in Sweden. New records in the A˚ngermanland province (A˚) and on moose dung (M) are denoted. – , no data found in the literature. Species
Substrate
Distribution
New records
Zygomycota Pilobolus crystallinus
D, H, R, Sq2
–a
A˚, M
Basidiomycota Coprinus sp. Sp. 1.
– –
–a –a
Ascomycota (discomycetes) Ascobolus furfuraceus A. sacchariferus Ascobolus sp. 1 Cheilymenia fimicola C. stercorea Coprotus aurorus Lasiobolus lasioboloides L. papillatus Saccobolus versicolor Thelebolus caninus T. microsporus
C, D, H, R2, He4 M, D, R5, D1, He4 – C4 D2, He4 C2 – C, D, H, R, S2, B, He4 C, D, H, R, Mu2, B, He4 Do2, B, Ca, He4 C, D, R2, B, Ca, He4
Common4 Occasional in the hemiboreal and boreal zone4 – Occasional in the temperate, hemiboreal and boreal zone4 Common4 Found in the country but frequency and distribution unknown4 – Upl8, common4 Upl1, common4 Found in the country but frequency and distribution unknown4 Common4
M A˚
Ascomycota (pyrenomycetes) Arnium caballinum Podospora myriospora Schizothecium fimicola S. vesticola Sordaria fimicola Sporormiella intermedia S. irregularis S. lageniformis S. megalospora S. minima Sporormiella sp. 1 Sporormiella sp. 2
H, C3, ReD, S5 C3 H, C3, S6 Esp. C, H3, S6 Various, H, M, C3, Ha6 C, Ha, H, S3 C, M, H, R, ReiD, RoD3 H3 C3 C, M, Ha, H, R3, S6 Various7 M7
O¨l, Upl, Mpd, Hrj, Jmt3 Bh, Srm, Upl, Vstm, Dlr, TL3 Gstr, Jmt, Vb: all over Nordic area3 Dlr, Sm, Upl6 Common in whole Scandinavia3 Dlr, Sm, Upl6 Sk–Lpl3 Sk–Lpl, common, widespread3 Sk, Bl, Sm, O¨l, Gtl, O¨g, Vg, Hl, Nrk, Srm, Upl, A˚ng, Hrj, Jmt, Nb3 Sk–TL (except Bl, Dls, Bh, Vrm)3 Sk, Bl, Sm O¨l, Gtl, Hl, Vg, Dls, Srm, Upl, Hls, Hrj, Jmt, TL3 Sk, Bl, Sm, O¨l, Gtl, Vg, Hl, Bh, Vrm, Upl, Hls, Nb3 –a –a
A˚, M A˚, M M M
A˚, M M A˚, M A˚, M M M A˚, M M
M M A˚, M A˚ A˚ A˚
Abbreviations for substrates: B, bird (Aves sp.); C, cow (Bos taurus); Ca, carnivore; D, deer (Cervidae spp.); Do, dog (Canis familiaris) ; H, horse (Equus caballus); Ha, hare (Lepus sp.); He, herbivore ; M, moose (Alces alces) ; Mu, mouse (Mus sp.); R, rabbit (Oryctolagus cuniculus) ; ReD, red deer (Cervus elaphus) ; ReiD, reindeer (Rangifer tarandus) ; RoD, roe deer (Capreolus capreolus) ; S, sheep (Ovis aries); and Sq, squirrel (Scuridae spp.). Abbreviations for Swedish provinces: Bohusla¨n (Bl), Dalarna (Dlr), Dalsland (Dls), Gotland (Gtl), Ga¨strikland (Gstr), Halland (Hl), Ha¨lsingland (Hls), Ha¨rjedalen (Hrj), Ja¨mtland (Jmt), Lappland (Lpl), Medelpad (Mpd), Norrbotten (Nb), Na¨rke (Nrk), Ska˚ne (Sk), Sma˚land (Sm), So¨rmland (Srm), Torne Lappmark (TL) Uppland (Upl), Va¨rmland (Vrm), Va¨stergo¨tland (Vg), Va¨stmanland (Vstm), Va¨sterbotten (Vb), A˚ngermanland (A˚ng), O¨land (O¨l), and O¨stergo¨tland (O¨g). 1 5 Brummelen (1967). Lundqvist (1972). 2 6 Ellis & Ellis (1998). Lundqvist (1997). 3 7 Eriksson (1992). Nils Lundqvist (pers. comm.). 4 8 Hansen & Knudsen (2000). Lundqvist & Ryman (1976).
myrtillus) occurred sparsely. The bottom layer consisted of 70 % lichens (mainly Cladonia spp.) and 30% mosses. (2) Mature spruce-pine forest (hereafter referred to as spruce forest, shady and mesic). The tree layer consisted of 70% Scots pine, 30 % Norway spruce (Picea abies) and some small birches (Betula pubescens), aspen (Populus tremula) and rowan (Sorbus aucuparia). The ground vegetation consisted of 80% bilberry and 20 % cowberry. The herbs Maianthemum bifolium and Linnaea borealis also occurred sparsely. The bottom layer consisted of 80% mosses, 10% lichens, and 10% barren ground (stones). (3) Mire (sunny and wet). The tree layer consisted of 90 % Scots pine and 10 % small birches. The ground vegetation consisted of 50% Eriophorum vaginatum and Carex globularis, 20 % heather, 10 % crowberry, 10% bog whortleberry (Vaccinium uliginosum), 5 % cloudberry (Rubus chamaemorus) and 5 %
dwarf birch (Betula nana). Bilberry, cranberry (Vaccinium oxycoccus) and Andromeda polifolia occurred sparsely. The bottom layer consisted of 90 % mosses (mainly Sphagnum spp.) and 10% lichens (mainly Cladonia spp.). 113 dung piles from six captive moose calves (2–2.5 months old) was collected at a nearby moose farm during the first week of August 2000. The calves were kept in a natural pasture and fed the same diet. About 80 % (volume) of their diet consisted of natural summer food for moose (leaves from deciduous trees, grasses and herbs), and about 20% supplemental food (Ren Forbas, Fori Foderringen Handelsbolag, Holmsund). The consistency of the moose dung resembled dung from domestic cattle, which is common for moose in summer (Schwartz & Renecker 1998). To avoid biases in the results due to decomposition processes that
Habitat differences of coprophilous organisms
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Table 2. Frequency of occurrence of each species recorded on moose dung in three habitat types in northern Sweden. n=15 in all habitats.
100
Pine forest
Spruce forest
Mire
Zygomycota Pilobolus crystallinus
1
0
4
Basidiomycota Coprinus sp. Sp. 1
2 0
1 0
4 1
Ascomycota (discomycetes) Ascobolus furfuraceus A. sacchariferus Ascobolus sp. 1 Cheilymenia fimicola C. stercorea Coprotus aurorus Lasiobolus lasioboloides L. papillatus Saccobolus versicolor Thelebolus caninus T. microsporus
1 5 8 2 4 0 1 14 0 3 3
0 3 1 0 3 1 0 5 0 0 0
2 8 5 1 7 0 0 15 3 2 2
Ascomycota (pyrenomycetes) Arnium caballinum Podospora myriospora Schizothecium fimicola S. vesticola Sordaria fimicola Sporormiella intermedia S. irregularis S. lageniformis S. megalospora S. minima Sporormiella sp. 1 Sporormiella sp. 2
0 3 8 2 1 1 2 0 1 0 10 2
1 2 3 0 0 0 0 1 0 0 8 0
1 6 14 1 2 0 1 1 0 1 12 0
F requency (%)
Species
Mire
80
Habitat type
Pine forest Spruce forest
60
40
20
have started before collection, we aimed to collect the dung and place the groups in the selected habitats as soon as possible. No dung was older than 24 h, and the groups were laid out 0.5– 4 h after collection. The experiment used even-aged dung collected from moose with the same diet and thus basically the same inoculum of species. Variables that could have biased the comparisons of dung among habitat types were thus eliminated. The dung was placed in four line transects per habitat type, pine forest (n=38 dung samples), spruce forest (n=38) and mire (n=37). The dung piles were placed on insect nets, marked with a stick and numbered. The distance between each transect and each dung pile was 10 m, and the distance between the different study sites was 10–40 km. Data were sampled at three separate occasions during August and September 2000 (hereafter referred to as 1, 2, and 3, respectively). Sampling (1) was performed at 9–10 d, (2) at 27–28 d, and (3) at 35–36 d after the dung was set out. (1) and (2). Water content was determined at two occasions and the mean value was used in the analyses. The water content of the dung was also used as a measurement of habitat moisture. One subsample per
0
0
3
6
9 12 15 Ranked species
18
21
Fig. 1. The distribution of ranked fungal species found on moose dung in northern Sweden for the three habitat types : pine forest, spruce forest and mire (n=15 for all habitats).
dung sample was taken using a thin spatula and a teaspoon to obtain a sample with material from all layers from the top to the bottom of the group equally represented. Samples were taken from all habitats on the same day under stable weather conditions and were kept in closed test tubes. The fresh weight of the samples were determined in the laboratory (1–6 h after sampling) to 0.1 mg using a Mettler AE 166 scale. The samples were then air dried at room temperature to constant weight, placed in a dessicator for 4–5 h and weighed again to obtain the dry weight. (1) The number of holes visible on the surface of the dung samples, which could be attributed to insect larvae, was counted on all dung samples (n=113) and used as an estimate of insect attack. The number of Diptera, Coleoptera and other invertebrates visible on the surface of the dung was also counted, but was insufficient for statistical analyses. Diptera and Coleoptera larvae seemed to be most common, though. (2) The percent cover of discomycetes was visually estimated. We excluded other ascomycetes because they were more difficult to detect. Also, the number of fruit bodies of basidiomycetes per dung sample was counted, but only a few were found and there was no significant difference among habitats. The percent cover of mosses was visually estimated. No vascular plants were observed to colonise the dung. All dung piles were sampled at this time (n=113). (3) The number of species of fungi was determined by taking samples from the surface of the dung. Fifteen samples from each habitat were analysed, chosen randomly among dung piles from all transects (n=45 dung samples). The samples were kept cold during the species determination in the laboratory, which was made with a stereomicroscope (Zeiss KL2500LCD) and a microscope (Zeiss Axioskop2). The fungi were mounted in glycerol. Voucher specimens are preserved in the herbarium of Umea˚ University UME.
A˚sa Nyberg and Inga-Lill Persson
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Table 3. Pairwise comparisons of water content (mean value of the two samplings), species richness, discomycete cover, insect damage and moss cover among three habitat types x2, D.F. and P values are presented for Kruskal–Wallis tests, Z and P values are presented for Wilcoxon tests. Spearman’s Rank Correlation (rs) and P values are presented for correlations between parameters. Bold values indicate statistical significance. x2
D.F.
Water content Pine forest–Mire Spruce forest–Pine forest Spruce forest–Mire
57.37
2
No. of species of fungi Pine forest–Spruce forest Mire–Spruce forest Mire–Pine forest
20.55
Discomycete cover Pine forest–Spruce forest Mire–Spruce forest Mire–Pine forest
16.14
No. of insect holes Pine forest–Mire Spruce forest–Pine forest Spruce forest–Mire
19.12
Cover of mosses Pine forest–Spruce forest Mire–Pine forest Mire–Spruce forest
39.82
Correlations Water content–Moss cover Water content–Discomycete cover Water content–No. of insect holes Water content–No. of fungal species Moss cover–Discomycete cover No. of insect holes–Discomycete cover No. of insect holes–Moss cover Discomycete cover–No. of fungal species No. of fungal species–Moss cover No. of fungal species–No. of insect holes
The data were analysed statistically using the SAS system for Windows (version 6.12). The non-parametric Kruskal Wallis test, Wilcoxon test (for two samples), and the Spearman’s Rank Correlation test, were used to test for habitat differences and correlations.
RESULTS We found 26 species of fungi, representing 14 different genera (Table 1). Amongst these there was one zygomycete and two basidiomycete species ; the remaining 23 species were ascomycetes, represented by 11 discomycetes and 12 pyrenomycetes. Two undescribed Sporormiella species were observed, both related to S. australis and have similar fruit bodies, but differ in spore characters. Sporormiella sp. 1 has been found on various substrates, while Sporormiella sp. 2 has only been found on moose dung (Nils Lundqvist pers. comm.). Twelve of the 26 species found were new to the province of A˚ngermanland, and 17 have not been previously reported from moose dung. Twenty of the fungal species were found in the pine forest, 11 in the spruce forest and 21 on the mire (Table 2). Eight of the species were only observed in one habitat ; four in the pine
Z
rs
P
4.59 4.67 6.51
<0.0001 <0.0001 <0.0001 <0.0001
3.25 3.94 2.25
<0.0001 0.0012 <0.0001 0.0244
2.38 3.91 1.89
0.0003 0.0175 <0.0001 0.0590
1.66 2.69 4.27
<0.0001 0.0961 0.0071 <0.0001
5.74 0.88 6.00
<0.0001 <0.0001 0.3784 <0.0001
2
2
2
2
x0.27 x0.40 0.45 x0.48 0.29 x0.14 x0.27 0.58 0.51 x0.24
0.0045 <0.0001 <0.0001 0.0009 0.0020 0.1301 0.0042 <0.0001 0.0003 0.1072
forest, three on the mire, and one in the spruce forest (Table 2). Eight species occurred only in the pine forest and the mire, and two species were found only in the spruce forest and the mire. Eight species were found in all three habitats. The relative number of dung piles occupied by the various species showed a unimodal distribution in all three habitats (Fig. 1). Most of the species were only found on one or a few dung piles. Six species in the pine forest, five in the spruce forest, and seven on the mire, were found in 10 % or less of the samples. The most common species, all habitats pooled, was Lasiobolus papillatus, which reached a frequency of 76 %; this was the most common species on the mire (frequency 100 %) and the pine forest (frequency 93 %). Sporormiella sp. 1 was the most common species (53 % of the samples) in the spruce forest. The average water content of the samples differed significantly among habitat types (Table 3). It was significantly higher in the spruce forest than in the pine forest and on the mire on both sampling occasions (Fig. 2a). It was also significantly higher in the pine forest than on the mire. We found significant negative correlations between water content and fungal species richness, cover of discomycetes, and moss cover, whereas it was a significant positive correlation between water
Habitat differences of coprophilous organisms
Water content/total weight (%)
(a)
45 b
40 35
Sampling 1 Sampling 2
a
30
e
25 20 15
c
d f
10 5 0
No. of fungal species
(b)
7 6
c a
5 4 3
b
2 1 0
Discomycete cover (%)
(c)
14
a
DISCUSSION
8 6 b
4 2 0
Moss cover (%)
(d)
45 40 35 30
a a
25 20 15 10 5 0
b
7
b
(e)
No. of insect holes
6 5 4
a
3 a
2 1 0
content and the number of insect holes (Table 3). A negative correlation, although not significant, was found between fungal species richness and the number of holes and between the cover of discomycetes and number of holes. The fungal species richness, the percent cover of discomycetes, and the percent cover of mosses, differed significantly among habitats (Fig. 2b, c, d) and were significantly higher in the pine forest and on the mire than in the spruce forest. The species richness was also significantly higher on the mire than in the pine forest, and the discomycete cover and the moss cover showed the same trend, although this was not statistically significant. The number of insect holes per dung pile differed significantly among habitat types (Fig. 2e), and was significantly higher in the spruce forest than in the pine forest and on the mire. We also found a significant negative correlation between number of holes and moss cover (Table 3). There were significant, positive correlations between the cover of discomycetes and fungal species richness, between cover of discomycetes and moss cover, and between fungal species richness and moss cover.
a
12 10
1364
Pine forest
Spruce forest
Our data indicates that the fungal community developing on moose dung is species-rich, but poorly studied so far. In spite of the limited sample size and the use of a homogenous substrate, we found 31 % (9 of 29) of the pyrenomycetes reported on moose dung in Sweden (Eriksson 1992). Twelve of the 26 species have never been reported from the region, 17 have never been reported on moose dung (Table 1), and two species appear to be undescribed. The number of species found appears to be rather high considering both the limitations listed above and that we only examined the samples once. The most comprehensive studies of fungi on cervid dung we can use for comparisons are based on incubated dung samples, examined over a longer time period (Larsen 1971, Richardson 2001). Larsen (1971) found 36 species (on dung of Dama dama, n=10), while Richardson (2001) reported 108 species on deer dung (mean 10.9 spp. samplex1, n=54), after collecting and incubating dung from all over the world over 5.5 yr. Most of the species in our study occurred in low frequency, whereas a small number of species made up the majority of the community. This pattern agrees with Richardson’s (2001) study, but the most abundant species in our study occurred at higher frequencies. This is probably due to the homogenous substrate with a homogenous inoculum, and because our sampling was limited in both space and time.
Mire
Habitat type
Fig. 2. The parameters measured on moose dung in three habitat types in northern Sweden : Water content (a), number of fungal species (b), percent cover of discomycetes (c), percent cover of mosses (d) and number of insect holes on the surface (e).
Mean values and standard errors are presented. Different letters above the bars indicate that they are significantly different from each other. n=15 in chart b. n=38 ( pine forest and spruce forest), and n=37 (mire) in charts a, c, d and e.
A˚sa Nyberg and Inga-Lill Persson Our results show significant differences among habitat types in the occurrence and species richness of coprophilous organisms developing on summer dung of moose. The spruce forest contributed most to the observed differences, but differences between the pine forest and the mire were also evident. As we used uniform dung, assumed to have the same inoculum of species, our data clearly demonstrate that habitat plays an important role in final species composition. This accords with previous studies, which have suggested that communities of coprophilous organisms differ between habitats (Lussenhop et al. 1980, Yocom & Wicklow 1980, Marino 1991a, b). These patterns were opposite to what we expected concerning the development of dung fungi. Fungi are mostly associated with moist habitats, and experiments in vitro have documented higher occurrences of coprophilous fungi when provided with free water (Kuthubutheen & Webster 1986). The dung in the spruce forest had a higher water content than that in the pine forest and on the mire, indicating a moister habitat, probably as a result of more shading from tree crowns. In spite of that, we found the lowest number of fungal species (both total and mean number per dung pile), and fungal cover in the spruce forest. There was a highly significant negative correlation between water content and the number of species of fungi, as well as cover of fungi. Contrary to this, there was a highly positive correlation between water content and number of insect holes. We also found a negative correlation, although not significant, between the number of insect holes and number of fungal species. The lack of significance might be due to differences in the insect species composition among dung piles. Different insect groups might have different impacts on the fungal community. We did not examine the insect fauna, but have the impression that there were differences between dung piles within habitat types. We suggest that the low number of species and percentage cover of fungi on the dung in the spruce forest results from negative effects of more insects in that habitat. Coprophagous insects feed on plant debris and graze on fungal mycelium, spores, and fruit bodies in the dung (Dickinson & Underhay 1977, Lussenhop et al. 1980, Wicklow & Yocom 1982, Stevenson & Dindal 1987, Dix & Webster 1995). Lussenhop et al. (1980) found that coprophagous insects could decrease hyphal density in cattle dung, and Wicklow & Yocom (1982) demonstrated that the number of fungal fruit bodies on rabbit dung incubated with insects declined with increasing insect density. Thus, the explanation for the pattern we observed could be invertebrate feeding on the substrate, feeding on the fungi (mycelia and spores), or a combination of both. The dung in the spruce forest also seemed considerably more disintegrated than that in the pine forest and on the mire, probably as a result of the heavier load of insect larvae. Feeding by coprophagous insects, especially larval dung beetles, can contribute to the crumbling and disruption of dung (Lussenhop et al. 1980, Stevenson &
1365 Dindal 1987). An alternative explanation thus might be that the dung in the spruce forest offered a rather unstable substrate for fungi and prevented their germination or development. The positive correlation between moss cover and fungal species richness, as well as fungal cover, indicates that competitive interactions between mosses and fungi are of minor importance for the community composition. In order to test whether the observed habitat differences are due to insect interaction or not, we need to run experiments excluding insects. This can be done either by treating dung with insecticides or covering it with insect nets. Since different insect species might differ in feeding preferences, we also need data on the insect fauna involved. Inoculations of fungi and insects may be used to further reveal the outcome of these interactions. ACKNOWLEDGEMENTS We thank Christer Johansson for allowing us to collect moose dung at the moose farm in Bjurholm. We are also grateful to Kjell Danell, Lars Ericson, Roger Bergstro¨m, Mats Wedin, and two anonymous reviewers for helpful comments on the manuscript. Special thanks to Nils Lundqvist for help with species identification, and valuable comments on many of the fungal species. This study was financed by the Swedish Council for Forestry and Agricultural Research, the Swedish Environmental Protection Agency, and the Kempe Foundation.
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