Northeastern Naturalist
648
R.T. Meyer, A. Weir, and T.R. Horton
22001155 NORTHEASTERN NATURALIST 2V2(o3l). :2624,8 N–6o5. 13
Small-Mammal Consumption of Hypogeous Fungi in the
Central Adirondacks of New York
Robert T. Meyer1,*, Alexander Weir1, and Thomas R. Horton1
Abstract - Small mammals are generally known to consume and disperse subterranean
(hypogeous) fungi, but accounts for this behavior are lacking for the northeastern US. We
report on the use of these fungi by a sample of small mammals from the central Adirondack
Mountains of New York. We analyzed 57 fecal samples from Peromyscus maniculatus
(Deer Mouse), Myodes gapperi (Southern Red-backed Vole), Tamias striatus (Eastern
Chipmunk), and Blarina brevicauda (Short-tailed Shrew) to determine whether they
were consuming fungi in the central Adirondack Mountains. We found that fecal samples
from Eastern Chipmunk (n = 12), Southern Red-backed Vole (n = 14), Short-tailed Shrew
(n = 14), and Deer Mouse (n = 17) contained Glomus spp. (arbuscular mycorrhizal fungi)
spores (33.3%, 35.7%, 21.4%, and 17.6% of samples, respectively) and Russulaceae spores
(66.6%, 35.7%, 7.14% and 5.9% of samples, respectively). One sample from an Eastern
Chipmunk also contained Gautieria spores.
Introduction
Mycorrhizal fungi create connections between trees and facilitate increased water-
and mineral-uptake into tree roots (Smith and Read 2008). Hypogeous fungi,
such as truffles, typically form mycorrhizal associations, and small mammals and
invertebrates disperse their spores. There is evidence that certain mammal species
are able to detect the odor of underground fungi (Fogel and Trappe 1978). When
small mammals eat the fruiting body of the fungus, the spores move through their
digestive tract, are defecated, and then sometimes germinate to form mycorrhizal
associations in a new location (Ashkannejhad and Horton 2006, Nuñez et al. 2013,
Trappe and Maser 1976). Mycophagy, the consumption of fungi, may provide some
mammals with essential minerals and carbohydrates while facilitating the dispersal
of spores across the landscape (Fogel and Trappe 1978). Many mammals that
consume fungi have large home-ranges that span different vegetation types and
they can thus inoculate different ecological communities with spores of hypogeous
fungi (Ashkannejhad and Horton 2006, Ovaska and Herman 1986). We examined
fecal samples from several small mammals captured at a study area in the central
Adirondack Mountains of New York to document consumption of hypogeous fungi
by small mammals in this region.
1Department of Environmental and Forest Biology, State University of New York College of
Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210. *Corresponding
author - rtmeyer13@gmail.com.
Manuscript Editor: Frederick A. Servello
Northeastern Naturalist Vol. 22, No. 3
R.T. Meyer, A. Weir, and T.R. Horton
2015
649
Study Site
We chose two study sites in the Huntington Wildlife Forest of the SUNY-College
of Environmental Science and Forestry, located in the Adirondack State Park in
Newcomb, NY. The first site is a natural area that consists of 365 ha of old-growth
forest with mixed conifers and deciduous trees. The second study site, called the
Hare Area, consists of 60 ha of Picea sp. (spruce)–Abies sp. (fir)-dominated forest.
Historical, topographical, and vegetative characteristics of the study area have been
previously reported in McNulty et al. (2008).
Methods
We trapped small mammals and collected feces for analysis of fungi use during
16–19 July 2007, which is the early stage of the annual fruiting period for fungi
(July–October). We set up a 7 m x 7 m grid with trap stations spaced 20 m apart in
both areas. We used 1 small and 1 large Sherman trap at each trap station (98 traps
total). We baited traps with peanut butter, rolled oats, and paraffin (ratio of 1:4:2);
the traps were set out in the evening and checked in the morning for small mammals.
We marked captured animals by attaching an ear tag if the ear’s pinna were large
enough or with Wite-out® if the pinna were too small or absent.
We collected feces from the trap floors and placed the samples in labeled envelopes
to air dry. We then cleaned the floor of the trap with a damp cloth to remove
excess feces and prevent contamination of feces from other captured individuals;
marked animals were released on site. Feces of recaptured animals were used unless
the animal had been caught the previous night.
Once dry, the envelopes containing fecal samples were kept in a jar with Drierite
® anhydrous calcium sulfate. We pre-sampled stored spores in September 2013
to confirm that they were still identifiable after >5 y in storage, then began our
analysis. We placed 25 mg from each fecal sample into its own 0.5-dram vial with 1
mL of 15% ethanol to rehydrate the sample (Pyare and Longland 2001). We used a
clean mall probe to break apart large pellets and 3 pulses of a Vortex Genie 2 mixer
(Fisher Scientific, Bohemia, NY) to homogenize each sample. To create a slide for
microscopic analysis, we plunged a pair of smooth-sided tweezers to the bottom of
the vial, closed the tips, and withdrew the tweezers, applied the residue to a clean
slide, and air-dried the sample for ~2 minutes. To identify the spores, we made 2
covered slides for each sample—1 with 1 drop of Melzer’s reagent to determine
staining characteristics and 1 with 1 drop of 100% glycerol to compare to the spores
with Melzer’s and preserve the sample. We viewed samples under a Nikon E-800
research microscope equipped with differential interference contrast (DIC) optics
starting at 40x, frequently switching to 60x and 100x objectives to give more detail
for identification of fecal contents (Pyare and Longland 2001). We classified spores
as hypogeous if they were radially symmetrical, a characteristic of hypogeous fungi.
We examined each slide for 15 minutes to control effort per slide and identified fungal
spores to family or genus using spore keys (Castellano et al.1989, Morton and
Benny 1990).
Northeastern Naturalist
650
R.T. Meyer, A. Weir, and T.R. Horton
2015 Vol. 22, No. 3
Results
We found spores of hypogeous members of Russulaceae, Glomus spp., or
Gautieria spp. in 24 of the 57 fecal samples, with 6 samples containing more
than 1 species of fungi. Tamias striatus L. (Eastern Chipmunk, n = 12), Myodes
gapperi (Vigors) (Southern Red-backed Vole, n = 14), Blarina brevicauda
(Say) (Short-tailed Shrew, n = 14), and Peromyscus maniculatus (Wagner) (Deer
Mouse, n = 17) fecal samples contained Glomus spores in 33.3%, 35.7%, 21.4%
and 17.6% of samples, respectively, and Russulaceae spores in 66.6%, 35.7%,
7.14% and 5.9% of samples, respectively. One sample from an Eastern Chipmunk
contained both species of fungi as well as Gautieria spores. We frequently encountered
spores of other epigeous fungi in fecal samples but they were ignored
for the purposes of this study.
Discussion
All 4 small-mammal species were clearly consuming hypogeous fungi, both
Glomus and Russulaceae species, during the July sampling period, and our results
indicate that fungi are a common item in the animals’ diets. If consumption of bait
in traps influenced our results, we believe that would have caused us to underestimate
the percent occurrence of spores in feces. There were indications of greater
use of hypogeous fungi by Eastern Chipmunks and Southern Red-backed Voles
than by Short-tailed Shrews or Deer Mice, but we were unable to assess relative
use because of the small number of fecal samples and the short sampling period.
It is notable that our results from Southern Red-backed Voles are consistent with
reported use of Russulaceae fungi across the species’ range (Maser and Maser 1988,
Pastor et al. 1996).
It is also notable that spores of several hypogeous species were absent in our
samples. Much of the literature on small-mammal mycophagy involves the presence
of Endogone (Zygomycota) and Hymenogaster (Basidiomycota), and both
types of fungi have been reported as being consumed by small mammals in the
northeastern US (Hamilton 1941, Whitaker 1962). Our short sampling time and
small sample size may explain the absence of Hymenogaster, which has seasonal
fruiting habits (Castellano et al. 1989). Endogone spp., however, fruit year-round
and are common throughout the northern hemisphere (Trappe et al. 2009). Endogone’s
absence in our samples may be an artifact of the taxonomic changes to the
group since the 1970s. Some of the spores we identified as Glomus may have been
previously considered to be Endogone species.
Given our observed use of hypogeous fungi by Short-tailed Shrew, Deer Mouse,
Eastern Chipmunks, and Southern Red-backed Voles, these and other small mammals
may have important roles in the dispersal of mycorrhizal fungi in northeastern
US forests. To better understand that role, future studies should seek to determine
the relative consumption and temporal changes of fungal consumption.
Northeastern Naturalist Vol. 22, No. 3
R.T. Meyer, A. Weir, and T.R. Horton
2015
651
Acknowledgments
We would like to express our gratitude to Andrea Reinheart Perez for the collection of fecal
samples. Thank you to Stacy McNulty and Charlotte Demers for their helpful comments
on early versions of the manuscript and to the SUNY ESF Adirondack Ecological Center
for logistical support. We thank Dr. James Trappe for his contribution to spore identification
during the project.
Literature Cited
Ashkannejhad, S., and T.R. Horton. 2006. Ectomycorrhizal ecology under primary succession
on coastal sand dunes: Interactions involving Pinus contorta, suilloid fungi, and
deer. New Phytologist 169:345–354.
Castellano, M.A., J.M. Trappe, Z. Maser, and C. Maser. 1989. Key to the Spores of the Genera
of Hypogeous Fungi of North Temperate Forests with Special Reference to Animal
Mycophagy. Mad River Press, Eureka, CA. 186 pp.
Fogel, R., and J. Trappe. 1978. Fungus consumption (mycophagy) by small animals. Northwest
Science 52:1–31.
Hamilton, W.J., Jr. 1941. The food of small forest-mammals in eastern United States. Journal
of Mammalogy 22:250–263.
Maser, C., and Z. Maser. 1988. Mycophagy of red-backed voles, Clethrionomys californicus
and C. gapperi.The Great Basin Naturalist 48:269–273.
McNulty, S.A., S. Droege, and R.D. Masters. 2008. Long-term trends in breeding birds
in an old-growth Adirondack forest and the surrounding region. The Wilson Journal of
Ornithology 120:153–158.
Morton, J.B., and G.L. Benny. 1990. Revised classification of arbuscular mycorrhizal fungi
(Zygomycetes): A new order, Glomales, two new suborders, Glominae and Gigasporinae,
and two new families, Acaulosporaceae and Gigasporaceae, with an emendation of
Glomaceae. Mycotaxon 37:471–491.
Nuñez, M.A., J. Hayward, T.R. Horton, G.C. Amico, R.D. Dimarco, M.N. Barrios-Garcia,
and D. Simberloff. 2013. Exotic mammals disperse exotic fungi that promote invasion
by exotic trees. PLoS ONE 8:e66832.
Ovaska, K., and T.B. Herman. 1986. Fungal consumption by six species of small mammals
in Nova Scotia. Journal of Mammalogy 67:208–211.
Pastor, J., B. Dewey, and D.P. Christian. 1996. Carbon and nutrient mineralization and
fungal-spore composition of fecal pellets from voles in Minnesota. Ecography 19:52–61.
Pyare, S., and W.S. Longland. 2001. Patterns of ectomycorrhizal-fungi consumption by
small mammals in remnant old-growth forests of the Sierra Nevada. Journal of Mammalogy
82:681–689.
Smith, S.E., and D. Read. 2008. Mycorrhizal Symbiosis. 3rd Edition. Academic Press, New
York, NY. 800 pp.
Trappe, J.M., and C. Maser. 1976. Germination of spores of Glomus macrocarpus (Endogonaceae)
after passage through a rodent digestive tract. Mycologia 68:433–436.
Trappe, J.M., R. Molina, D.L. Luoma, E. Cázares, D. Pilz, J.E. Smith, M.A. Castellano,
S.L. Miller, and M.J. Trappe. 2009. Diversity, ecology, and conservation of truffle fungi
in forests of the Pacific Northwest. USDA Forest Service, Pacific Northwest Research
Station General Technical Report GTR-772. Portland, OR.
Whitaker, J.O., Jr. 1962. Endogone, Hymenogaster, and Melanogaster as small-mammal
foods. American Midland Naturalist 67:152–156.