Mycophagy and spore dispersal by small mammals in bavarian forests

Forest Ecology and Management, 26 (1989) 237-245

237

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

Mycophagy and Spore Dispersal by Small Mammals in Bavarian Forests H. BLASCHKE 1and W. B.~UMLER 2

1Lehrstuhl [i2r Forstbotanik, and 2Lehrstuhl f~r angewandte Zoologic, Universit~tt Mi~nchen, 8000 Mi~nchen 2 (Federal Republic of Germany) (Accepted 22 April 1988)

ABSTRACT Blaschke, H. and B~iumler, W., 1989. Mycophagy and spore dispersal by small mammals in Bavarian forests. For. Ecol. Manage., 26: 237-245. Spores of hypogeous fungi found in stomach contents of mice and voles trapped in high and low-elevation forests were identified and recorded with estimates of frequency of fungal genera. The data show differences between sites in the number of fungal taxa consumed. A similar taxa frequency was noted on plots with regenerations adjacent to mature stands. Spores of Endogonaceae were found to occur more often within reforestation sites linked with qualitative changes in ground vegetation.

INTRODUCTION

A characteristic of coniferous and deciduous forests is the abundant formation of mycorrhizae and the associated hypogeous fungal sporocarps in microniches of soil humus and litter layer. The common use of these fungal fruiting bodies as food by rodents has long been documented (Froidevaux and Schw~irzel, 1977; Fogel and Trappe, 1978; Maser et al., 1978), and interdisciplinary studies conducted in the Pacific Northwest of the United States and similar investigations in Australia have provided much information on the significance of mycophagy and the dispersal of faecal pellets containing mycorrhizal spores vital to the life cycle of trees and fungi (Maser et al., 1986; Malajczuk et al., 1987 ). As shown by Maser and Trappe (1984), small mammals consuming hypogeous fungi may play an important role in terms of functional components and plant/animal interrelations in forest ecosystems. By disseminating viable spores of hypogeous mycorrhizal fungi, some forest-dwelling rodents help maintain productivity of forests (Li et al., 1986). Thus, based on inventories of the distribution (B~iumler, 1981b), nutrition, and population dynamics of small mammals in Bavaria (B~iumler and Hohenadl, 1980; B~ium0378-1127/89/$03.50

© 1989 Elsevier Science Publishers B.V.

238 ler, 1981a; Blaschke and B~iumler, 1986), the present study was undertaken to add to our knowledge of mycophagy with emphasis on food/habitat interrelationships and the potential of small, forest-dwelling rodents as primary vectors of spores of hypogeous fungi within high and low-elevation coniferous forests, mixed stands, and afforestation sites. MATERIALSAND METHODS

Study sites For food-habit studies, 238 small mammals trapped as part of an interdisciplinary project (B/iumler, 1981a; Blaschke and B/iumler, 1986) within plots in the Chiemgau Alps near Ruhpolding (altitude 800-1200 m) during 19801985 were examined. A total of 560 animals (Apodemus flavicollis (Mel.), A. syluaticus (L.), Clethrionomys glareolus (Schreb.), Microtus agrestis (L.), and Pitymys subterraneus (Sel.)) were available from subsequent studies in high and low-elevation forests (6 locations: Donau region B,D,G; Unterfranken, U,E; Ruhpolding R; see Fig. 1 ).

Methods For fungal analysis, samples of the stomach contents of mice and voles ( n = 4 2 9 in autumn 1985; n=67 in spring 1986; n=64 in autumn 1986) were

[] Wijrzbut

N

A 0 i

i Scale

M~nchen

Fig. 1. Locationsof study sites in Bavaria, 1980-1986.B, Beilngries;D, Donauraum;G, Geisenfeld; E, Ebrach; U, Unterfranken;R, Ruhpolding.

239 mounted on slides (prepared according to Maser et al., 1986), examined microscopically, and used to estimate relative number of spores of each fungal genus consumed. Fungal spores were identified to genus with synoptic spore keys (Trappe, 1982; Trappe et al., 1988) and recorded with estimates of the 'fungal taxa frequency' and 'mycophagy frequency', according to Maser et al. (1978). Because the number of trapped animals varied between species and sex in different plots and locations, pooling of data (due to limited material from different locations) as a prerequisite for computer analysis was necessary. Relative numbers of spores were calculated and expressed as percentage values of fungal genera consumed. Based on a nonparametric statistical test (Conover, 1971), differences in relative frequency were accepted at the P < 0.05 level. RESULTS In the Chiemgau Alps (Ruhpolding plots R) fungal spores were found in the stomach content of A. flavicollis (7 % by volume), C. glareolus (36% by volume) and P. subterraneus (0.1% by volume) with an average annual mycophagy frequency of 25%, 42% and 1%, respectively, during 1980-1985. In late summer and autumn however, a frequency ranging from 93-94% for both A. flavicollis and C. glareolus was recorded. The predominant spores detected in this first 5-year period were from hypogeous ascomycetes. In additional samples originating from the same location (R), we found a dietary shift in spring, with beech and maple seedlings as main components of stomach contents (B~iumler, 1986). In autumn 1986, besides unidentified spores, basidiospores encountered were Gautieria sp., Hymenogaster sp. and Octaviania sp. (Table 1 ). The fungal taxa frequency (FT) on high elevation sites ranged from 1 to 8 with a high proportion ( < 60% ) of basidiospores (Table 2). The percentages of spores of hypogeous fungi frequently identified and recorded in different plots during 1985/ 86 are presented in Table 3. Data from low-elevation forests (Jura, Donau region B, D, G and Steigerwald E) parallels the above data in many respects. Within coniferous and mixed-hardwood stands the hypogeous sporocarps of ascomycetes, basidiomycetes and zygomycetes consumed seemed to occur in abundance (Table 3 ). The distribution of fungal species varied among plots, and thus fungal taxa frequency recorded for A. flavicoUis and C. glareolus in 6 locations was also variable, as shown in Table 2. Note that the maximum frequency (range 5-6) occurred more often for C. glareolus within plots, compared with the low frequency of fungal genera (0-3) for A. flavicollis in study sites Beilngries B and Geisenfeld G. Again, the fungi consumed were mostly hypogeous ascomycetes and basidiomycetes, including a high proportion of Endogonaceae (Table 3), and reflected the existing functional dependency of the components in a

240 TABLE 1 Mycophagy frequency ( MF ) and relative numbers of spores consumed by Apodemus flavicoUis and Clethrionomys glareolus within plots in autumn 1986 Fungal genera

Ascomycotina

Choiromyces Elaphomyces Genea Tuber Basidiomycotina

Gautieria Hymenogaster Octaviania Zygomycotina

Endogone/Glomus Sclerocystis Other fungi Unidentified

A. flavicollis (n = 24)

C. glareolus (n=38)

Spores (no.)

MF (%)

Spores (no.)

MF (%)

5

55

28

77

0

0

0

0

5 1 0

55 5 0

3 9 13

23 37 21

15 0 6

33 0 22

68 7 19

85 12 33

0

0

2

1

1 1 0

5 5 0

18 12 6

50 40 15

9

11

42

65

TABLE2 Number of samples (n) and frequency of taxa (FT) of hypogeous fungi in stomach contents of

Apodemus flavicoUis and Clethrionomys glareolus recorded in 1985/86 from old (0) and planted/ naturally regenerated (P/N) stands Plot No.

10/50 22 60 70/90 110/141 142/150 220/280 270/275 1/270 15/90 13/113

Location

SchSnbrunn SchSnbrunn Beilngries Beilngries Geisenfeld Geisenfeld Ebrach Ebrach Unterfranken Donauraum Ruhpolding

Stand/Site *

P/N 0 S* P P 0 P/N O P/N P/N 0

A. flavicoUis

C. glareolus

n

FT Range

n

FT Range

28 9 0 2 31 0 0 0 15 0 3

0-6 1-4 0 0-3 0-2 0 0 0 0-3 0 1-3

76 0 2 51 136 12 26 9 25 14 14

0-6 0 4 0-5 1-6 1-3 0-1 0-1 1-4 1-5 1-8

tAll low-elevation except Ruhpolding (high). *Seedlings of oak.

241 TABLE3 Relative n u m b e r of spores of hypogeous fungi recorded 1985/1986 in stomach c o n t e n t s of Apodemus flavicoUis a n d Clethrionomys glareolus from high and low-elevation forests in different locations Plot/Location

A. flavicoUis(n=88) (%)

Z

(%)

A

(%)

B

(%)

Z

(%)

0 0 0

0 0 0

2 0 13

50 0 48

19 5 6

44 t0 46

1 23 0

1 48 0

24 20 7

55 42 54

100 0

0 0

0 0

0 0

0 0

39 61

54 92

19 4

27 6

11 1

15 2

11 2 1 0

85 56 17 0

0 0 5 0

0 0 64 0

2 2 2 0

15 44 19 0

6 4

50 24

6 12

50 70

0 1

0 6

54 53 52 2 49 32 26

56 51 67 7 32 30 27

26 3 23 2 74 69 57

27 29 30 7 47 64 58

16 20 2 20 32 6 14

17 19 3 86 21 6 15

*A

(%)

2 0 14

50 0 52

70 Beilngries 90

3 0

110 Geisenfeld 120 130 150 Donauraum, Ruhpolding Unterfranken

10 S c h S n b r u n n 40 50

C. glareolus(n=330)

B

*A = Ascomycotina, B = Basidiomycotina, Z = Zygomycotina.

TABLE 4 Relative numbers of spores recorded for Apodemus flavicoUis and Clethrionomys glareolus in aut u m n 1985 based on analysis by sex ( M e a n value M-- Males a n d F= Females combined) Fungal genera

Ascomycotina

Choiromyces Elaphomyces Genea Tuber Basidiomycotina

Hymenogaster Zygomycotina

Endogone Glomus Sclerocystis ~M/F= 14/13. 2M/F= 93/65.

C. glareolus 2 ( n = 158)

A. flavicoUis 1 ( n = 2 7 ) Mean

M

%

23

38 0 6 130 131

90 0 67 99 96

29 29 19 40 6 3

52 52 86 95 67 75

0 5 68 81 28 29 12 29

6 3

F

%

Mean

M

%

F

%

4 0 3 1 5

10 0 33 1 4

48 4 7 73 133

48 4 8 116 129

50 100 67 92 48

48 0 4 10 140

50 0 33 8 52

27 27 3 2 3 1

49 48 14 5 33 25

56 68 28 20 50 13

49 56 32 22 70 7

44 42 57 56 71 27

63 77 24 17 29 19

56 58 43 44 29 73

242 TABLE 5 Relative frequency (%) of hypogeous fungal genera in stomach contents of mice and voles recorded for all sites in 1985 Fungal genera

Class

Total* Ascomycotina Choiromyces Elaphomyces

Genea Tuber Total* Basidiomycotina

Hymenogaster Total* Zygomycotina

Endogone Glomus Sclerocystis

A. flavicollis

C. glareolus

(n=27)

(n=159)

74 0 74 15 22

82 1 30 10 65

72 1 40 10 49

22 22

53 44

42 35

63 15 41 7

55 27 36 18

48 24 29 14

All rodents

*Percentage of total animals with spores from hypogeous fungal taxa in a class. TABLE6 Frequency of fungal taxa (FT)* and relative number of spores for Apodemus sylvaticus and Microtus agrestis collected within planted/naturally regenerated ( P / N ) plots (B, D, G, low-elevation forests)

M. agrestis (n-- 12)

A. sylvaticus ( n = 5 ) Plot No.

Site

13 20 90 130

SchSnbrunn SchSnbrunn Beilngries Geisenfeld

P P P P

FT

No. of spores A B Z

Plot No.

Site

2 3 2 4

34 8 17 4

10 60 70 90 110 150

SchSnbrunn Beilngries Beilngries Beilngries Geisenfeld Geisenfeld

0 3 0 35

1 2 3 40

P N P P P N

FT

No. of spores A B Z

3 1 1 1 2 5

9 6 3 7 125 7

1 0 0 0 0 8

4 0 0 0 16 22

*A = Ascomycotina, B = Basidiomycotina, Z = Zygomycotina. tripartite association of small rodents, mycorrhizal fungi and host plants on the sites examined. Mice and voles trapped in September/October 1985 h a d a m a r k e d l y h i g h m y c o p h a g y f r e q u e n c y ( 9 3 - 9 8 % ) . O f t h e a n i m a l s e x a m i n e d , i n c l u d i n g P. subterraneus a n d A. sylvaticus, o n l y 11% c o n t a i n e d n o s p o r e s , a n d a d r a s t i c d e c r e a s e i n t h e m y c o p h a g y f r e q u e n c y ( 3 5 % ) o c c u r r e d i n s p r i n g 1986 i n l o w - e l e v a t i o n p l o t s w h e n C. glareolus h a d a l o w f u n g a l - t a x a f r e q u e n c y { 0 - 2 ).

243

Altogether, of the spores encountered 1985 and 1986, 14 species were distinguished; the identified genera are listed in Tables 4 and 5. The fungi occurring with the greatest frequency within all the plots examined included species of Genea, Tuber and Hymenogaster. The available data (relative number of spores, Table 4) clearly show a significant difference ( P < 0.05) between species and sex of A. flavicollis; males had preferentially eaten Ascomycetes, (Genea, Tuber) whereas this difference was not evident between sexes of C. glareolus in the frequency of Tuber within plots. However, we found a preference of hypogeous ascomycetes like Tuber sp. over other hypogeous taxa by both A. flavicoUis and C. glareolus (males and females combined) with pooled data from 6 locations (Table 5). A consistent feature of plantations (plots 110, 130, 150; Geisenfeld G) was a relative high number of Endogonaceae spores, but a low fungal-taxa frequency (1-3) in the stomach content of A. sylvaticus and M. agrestis (Table 6). In the samples taken from afforested plots we recorded spore numbers in a range similar to the surrounding mature stands; in plantations adjacent to mature stands, fungal taxa frequency ranged from 1 to 6, but in old-growth low-elevation forests we estimated for A. flavicoUis and C. glareolus only a range of 0-4 and 0-3, respectively (Table 2). For C. glareolus which had a maximal fungal taxa frequency of 8 in high-elevation forests with relatively high numbers of basidiospores, species of Endogonaceae forming a kind of ectomycorrhiza with conifer and angiosperm trees and vesicular-arbuscular mycorrhiza (VAM) with herbaceous plants (Gerdemann and Trappe, 1974) were mainly recorded in the afforestation plots, and in forest openings favourable for VAM host plants. DISCUSSION

The data of our preliminary studies of mycophagy in several Bavarian forest districts (Blaschke and B~iumler, 1986) show that hypogeous spores were concentrated in the digestive tracts of A. flavicoUis and C. glareolus during fall, whereas only relatively small numbers of spores were found in spring. The available data based on relative numbers of spores of asco-, basidio- and zygomycetes consumed by C. glareolus might indicate some of the specific patterns of hypogeous species community structure and of sporocarp production related to host plants in forest ecosystems (Hunt and Trappe, 1987). It is evident from the foregoing and from parallel studies in other continents (Malajczuk et al., 1987; Maser and Maser, 1987), that interrelationships are difficult to establish in complex forested ecosystems with a diversity of components, habitats, soils and climatic conditions. As a result of our food-habit study, it appears that sporocarp distribution on sites opened for regeneration were reflected by the frequency of fungal taxa and showed no difference when compared with adjacent mature stands. However, a high number of spores of

244

the Endogonaceae was evident in animals trapped on opened sites with a ground flora consisting of VAM plants. Early descriptions (Hesse, 1894) on the occurrence of truffles in soil humus already pointed to habitats of voles and microniches in accumulated organic debris suitable for the development of hypogeous sporocarps, which were eaten by small mammals. Forest habitats in opened stands containing substrates such as coarse woody debris (logs) and larger amounts of decaying bark may also create favourable conditions for the development of hypogeous fungi and ectomycorrhizae associated with fine roots (Maser and Trappe, 1984; Blaschke, 1987). One can assume that changes in habitat structure are caused by alterations of sites, which in turn leads to a change in the fungal species composition (Winterhoff and Krieglsteiner, 1984; Schmitt, 1987). Shifts in fungal populations caused by clearcutting in high-elevation forests influence the existing fauna and could account for changes in rodent population (B~iumler, 1981). Hence, a mature or old-growth forest inhabited by small mammals that feed on hypogeous fungi may serve as a source of spores of mycorrhizal fungi and might also be essential to inoculation of afforestation sites and for natural regeneration as well. However, in some denuded areas with dense grass cover, M. agrestis has been found in association with beech plantations to cause damage to tree seedlings (Jirgle, 1984). Our findings and the available data from similar studies in two continents with other types of forest ecosystems are fully compatible with the concept that mycophagy and spore dispersal are important functional factors responsible for the survival of host plants which depend on obligatory symbiotic relationships, and may also be essential in maintaining ecosystem health (Li et al., 1986). Our study provided also a preliminary database to further examine this issue with regard to habitat aspects such as spore dispersal in afforestations and natural regenerations. An extension of interdisciplinary studies is a critical need, to fully understand relationships between small mammals, mycorrhizal associations, and site characteristics. ACKNOWLEDGEMENTS

We appreciate the help of S. Hopper for microscopic examination of slides and processing the data. Dr. J. Trappe and Z. Maser (USDA Forestry Sciences Laboratory, Corvallis, Oregon) kindly provided the synoptic spore keys for families and genera of hypogeous fungi. C. Maser critically reviewed the manuscript.

245 REFERENCES B~iumler, W. 1981a. Verbreitung, Ernithrung und Populationsdynamik der RStelmaus (Clethryonomys glareolus) und der Gelbhalsmaus (Apodemus flavicoUis) in einem Waldgebiet der Bayerischen Alpen. Anz. Schtidlingskde., Pflanz. Umweltschutz, 54: 49-53. Btiumler, W., 1981b. Verbreitung von Miiusen in verschiedenen Waldgebieten Bayerns. Anz. Sch~idlingskde., Pflanz. Umweltschutz, 54: 99-104. B~iumler, W., 1986. Trtiffeln, M~iuse und Testosteron. Naturwiss. Rundsch., 39: 396-397. B~iumler, W. and Hohenadl, W., 1980. lJber den Einfluss alpiner Kleins~iuger auf die Verjiingung in einem Bergmischwald der Chiemgauer Alpen. Forstwiss. Centralbl., 99: 207-221. Blaschke, H., 1987. Vorkommen und Charakterisierung der Ektomykorrhiza-assoziation Tuber puberulum + Picea abies. Z. Mykol., 53: 283-288. Blaschke, H. and Btiumler, W., 1986. [)ber die Rolle des BiogeozSnose in Wurzelbereich von Waldb~iumen. Forstwiss. Centralbl., 105: 122-130. Conover, W.J., 1971. Practical Nonparametric Statistics. Wiley, New York, 462 pp. Fogel, R. and Trappe, J.M., 1978. Fungus consumption (mycophagy) by small animals. Northwest Sci., 52: 1-31. Froidevaux, L. and Schw~zel, C., 1977. Aspects qualitatifs et quantitatifs des champignons hypog~s truffo'fdes mycorrhiziques en for~t. Schweiz. Z. Forstwes., 128: 800-813. Gerdemann, J.M. and Trappe, J.M., 1974. The Endogonaceae in the Pacific Northwest. Mycol. Mem., 5: 1-75. Hesse, R., 1894. Die Hypog~ien Deutschlands Bd. 2, Die Tuberaceen und Elaphomyceten, Vlg. Hofstetter, Halle, 140 pp. Hunt, G.A. and Trappe, J.M., 1987. Seasonal hypogeous sporocarp production in a western Orgeon Douglas-fir stand. Can. J. Bot., 65: 438-445. Jirgle, J., 1984. Walderneuerung der Waldbes~nde im erzgebirgischen Immissionsgebiet, Luftverunreinigung - Air Pollution, XIII. Int. Meeting of Specialists in Air Pollution Damage in Forests (Symposium IUFRO S 2.09), 27 August-1 September 1984 at Most, CSSR. Forestry and Game Management Research Institute, Jilovi~t~ Strnady, CSSR, pp. 34-46. Li, C.-Y., Maser, Z. and Caldwell, B.A., 1986. Role of three rodents in forest nitrogen fixation in Western Oregon; Another aspect of mammal-mycorrhizal fungus-tree mutualism. Great Basin Nat., 46: 411-414. Malajczuk, N., Trappe, J.M. and Molina, R., 1987. Interrelationships among some ectomycorrhizal trees, hypogeous fungi and small mammals; Western Australian and northwest American parallels. Aust. J. Ecol., 12: 53-55. Maser, C. and Maser, Z., 1987. Notes on mycophagy in four species of mice in the genus Peromyscus. Great Basin Nat., 47: 308-313. Maser, C. and Trappe, J.M. (Technical Editors), 1984. The seen and unseen world of the fallen tree. U.S. For. Serv. Gen. Tech. Rep. PNW-164, 56 pp. Maser, C., Trappe, J.M. and Nussbaum, R.A., 1978. Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests. Ecology, 59: 799-8~9. Maser, C., Maser, Z., Vitt, J.W. and Hunt, G., 1986. The northern flying squirrel; a mycophagist in southwestern Oregon, Can. J. Zool., 64: 2086-2089. Schmitt, J.A., 1987. Funktion, Bedeutung und Situation der Pilze in saarllindischen W~ldern. "Pilzsterben'? Zum Rtickgang der Pilzarten und Pilzfruktifikationen im Saarland. In: H. Derbsch and J.A. Schmitt (Editors), Atlas der Pilze des Saarlandes, Teil 2; Nachweis, Okologie und Beschreibungen. Dellatina, Saarbrticken, pp. 23-78. Trappe, J.M., 1982. Synoptic keys to the genera and species of zygomycetous mycorrhizal fungi. Phytopathology, 72: 1102-1108. Trappe, J.M., Castellano, M.A., Maser, Z. and Maser, C., 1988. Synoptic spore key to genera of hypogeous fungi of northern temperate forests with special reference to animal mycophagy. Mad River Press, Eureka, Calif. Winterhoff, W. and Krieglsteiner, G.J., 1984. Gef~ihrdete Pilze in Baden-Wtirttemberg. Beih, Ver5ff, Naturschutz Landschaftspflege Bad-Wtirtt., 40: 1-120, Karlsruhe.