The northern flying squirrel: a mycophagist in southwestern Oregonl

CHRIS MASER U.S. Department of the lnterior, Bureau of Land Management, Forestry Sciences Laboratory, 3200 Jefferson Way,

Corvallis, OR, U.S.A. 97331

ZANE MASER Department of Forest Science, Oregon State University, Corvallis, OR, U.S.A. 97331

JOSEPH W. WITT U.S. Department of the lnterior, Bureau of Land Management, 777 NW Garden Valley Boulevard,

Roseburg, OR, U.S.A. 97470

A N D

GARY HUNT^ Department of Forest Science, Oregon State University, Corvallis, OR, U .S.A . 97331

Received January 16, 1986

MASER, C. , Z. MASER, J. W. WITT, and G. HUNT. 1986. The northern flying squirrel: a mycophagist in southwestern Oregon. Can. J. Zool. 64: 2086-2089.

Fecal samples were collected over 27 months from the northern flying squirrel (Gluucomys subrinus (Shaw)), a mycophagist in the Pacific Northwest portion of its range. Nine genera of hypogeous Basidiomycetes, 10 of hypogeous Ascomycetes, and 1 of hypogeous Zygomycetes were identified from fecal samples (hypogeous fungi fruit underground). The squirrel food habits generally paralleled the seasonal availability of the hypogeous fungi, but with notable exceptions. Our data demonstrate the functional diversity an individual species lends to its habitat when viewed in a functional context.

MASER, C. , Z. MASER, J. W. WITT et G. HUNT. 1986. The northern flying squirrel: a mycophagist in southwestern Oregon. Can. J. Zool. 64: 2086-2089.

Les feces d'un kcureuil mycetophage, le Grand Polatou~he (Glaucomys sabrinus (Shaw)), ont kte recueillies durant 27 mois dans une partie de son aire de rkpartition, le nord-ouest des Etats-Unis. Neuf genres de Basidiomycetes hypogks, 10 d'Ascomycetes hypogks et 1 genre de Zygomycete hypoge ont kt6 retrouves dans les feces (champignons hypoges = a fructifications souterraines). Les habitudes alimentaires de cet kcureuil suivent ordinairement la disponibilite saisonnikre des champignons hypogks, mais il y a des exceptions marqukes. Nos rksultats mettent en evidence la diversite fonctionnelle qu'une espece prete a son habitat dans un, contexte fonctionnel .

[Traduit par la revue]

Introduction (90 to 100% of stomach volume) of flying squirrels in northern

The northern flying squirrel (Glaucomys sabrinus (Shaw)) exemplifies the rodent-habitat relations we are finding with a number of species (Maser et al. 1981; Wells-Gosling and Heaney 1984). Recent food-habit studies have begun to reveal the complex functional roles of these mammals within the temperate coniferous forest (Maser, Maser, and Trappe 1985; Li et al. 1986). In this study we document seasonal patterns of squirrel consumption of fungal fruiting bodies and relate our findings to previously established patterns of fruiting in hypo- geous fungi (G. Hunt and J. M. Trappe, manuscript submitted for publication3).

In the Pacific Northwest the northern flying squirrel is primarily a mycophagist (Maser, Maser, and Trappe 1985; Maser, Mowrey et al. 1985; McKeever 1960). Hypogeous fungi (fruiting underground) and epiphytic lichens are the major foods

'paper No. FRL-2086 of the Forest Research Laboratory, Oregon State University, Corvallis, OR, U.S.A. 9733 1 . Mention of a product or trademark by name does not constitute endorsement by Oregon State University.

'present address: Balco Reforestation Centre, R.R. 3, Kamloops, B.C., Canada V2C 5K1.

3 ~ u n t , G. , and J. M. Trappe. Seasonal hypogeous sporocarp production in a western Oregon Douglas-fir stand. Manuscript sub- mitted for publication.

Oregon. In northeastern Oregon, for example, hypogeous fungi are the principal food from July to December; from December through June, the lichen Bryoria fremontii (Tuck.) Brodo & Hawks is not only the squirrel's predominant food but also its sole nesting material (Maser, Maser, and Trappe 1985).

Study area The study area, 34 km northwest of Roseburg, Douglas Co.,

Oregon, lies generally within the western hemlock (Tsuga heterophylla (Raf.) Sarg.) zone of the Coast Ranges physiographic province (Franklin and Dyrness 1973). (References to the "Coast Ranges" refer to the central and northern Coast Ranges of Oregon.) The site has an average slope of 30% with a southern aspect; elevation ranges from 20 1 to 316 m. The overstory was old-growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) - western hemlock - western red cedar (Thuja plicata Donn); the understory was dominated by Pacific rhododendron (Rhododendron macrophyllum D. Don) - Oregon grape (Berberis nervosa Pursh). Old-growth Douglas-fir ranged from 87 to 103 cm in diameter at breast height (DBH).

Methods Northern flying squirrels were captured in Tomahawk live traps (No.

201) fastened about 1.5 m above the ground to trunks of trees greater than 39 cm DBH. Traps were examined daily. Each squirrel was ear-tagged, placed in a cloth sack for 5 min to allow it to defecate, and released. Fecal pellets deposited in the sack were collected and

Pnnted In Canada Impr~me au Canada

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

Uni

vers

ity o

f Sy

dney

on

03/1

0/13

For

pers

onal

use

onl

y.

TA

BL

E 1.

Rel

ativ

e fr

eque

ncy,

by

mon

ths,

of

fung

al ta

xa u

sed

as f

ood

by n

orth

ern

flyi

ng s

quir

rels

(m

ales

and

fem

ales

com

bine

d; N

= n

umbe

r of

squ

irre

ls)

Jan.

Fe

b.

Mar

. A

pr .

May

Ju

ne

July

A

ug .

Sep

t.

Oct

. N

ov.

Dec

. T

otal

(N

=1

4)

(N=

9)

(N=

12

) (N

=1

1)

(N=

13

) (N

=8

) (N

=1

7)

(N=

10

) (N

=2

9)

(N=

15

) (N

=1

4)

(N=

10

) (N

=1

62

)

Bas

idio

myc

etes

(hy

poge

ous)

R

hizo

pogo

na

86

Gau

tieri

a 2

1 H

ymen

ogas

ter

86

Mel

anog

aste

r 2

1 O

ctav

iani

na

0 R

adiig

era

0 H

yste

rang

ium

50

L

euco

gast

er

14

Leu

coph

leps

29

Asc

omyc

etes

(hy

poge

ous)

E

laph

omyc

es

100

Bal

sam

ia

0 G

eopo

ra

9 3

Pic

oa

7 G

anab

ea

0 G

enea

2

1 H

ydno

tr-y

a 0

Pez

iza

7 C

hoir

omyc

es

0 T

uber

7

Zyg

omyc

etes

(hy

poge

ous)

G

lom

us

7

Uni

dent

ifie

d ep

igeo

us s

pore

s 7

Oth

er

unid

entif

ied

spor

es

64

Lic

hens

64

"May

als

o in

clud

e T

runr

orol

umel

la i

n fa

ll sa

mpl

es. C

an. J

. Zoo

l. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

nive

rsity

of

Sydn

ey o

n 03

/10/

13Fo

r pe

rson

al u

se o

nly.

2088 CAN. J. ZOOL. VOL. 64, 1986

preserved in vials of 10% formalin. Fecal samples were collected from squirrels only at first capture during each trapping period, because samples collected at subsequent captures might have been contami- nated by ingested bait.

The study was conducted from December 1982 through February 1985. We considered 10 samples per month as an adequate representa- tion of food habits. Twenty-seven months were needed to get 10 samples per month for 10 months; we still had only 9 samples in February and 8 samples in June.

In the laboratory, a portion of a fecal pellet was placed on a microscope slide with smooth-surfaced forceps; serrated forceps may contaminate subsequent samples. Fecal matter was macerated and a drop of Melzer's reagent (I, KI, and chloral hydrate) was added. For each squirrel, one slide of feces was examined with bright-field microscopy at 100,400, and 1000 X magnification. Hypogeous fungal taxa were identified with a spore key (Trappe et al. 1986). Not all hypogeous fungal genera can be distinguished by spore morphology. For example, spores of Rhizopogon, Alpova, and Truncocolumella are too similar to separate. Alpova probably is rare at our site. Trunco- columella fruits only from October to December; spores recorded as Rhizopogon at our site may include Truncocolumella in autumn samples. Occurrence of spores from epigeous fungi (fruiting above ground) and lichens, although not identified to taxon, were recorded for comparison with occurrence of hypogeous fungal taxa.

Relative frequency of occurrence (the percentage of total animals with spores from a fungal taxon) for each fungal taxon was calculated. Percent volume of each taxon was not estimated because most fungal tissue had been digested; all that remained of fungi in the feces were the spores. Student's t-tests were used to determine if differences in relative frequency were significant; P < 0.05 was accepted as the level of significance.

Results Ninety-two ear-tagged squirrels were captured and sampled

162 times; 15 individuals accounted for 70 samples. Nine genera of hypogeous Basidiomycetes, 10 genera of hypogeous Ascomycetes, and 1 genus of hypogeous Zygomycetes were identified from fecal samples. Samples from most months contained spores not identifiable to genus.

Seasonal occurrence of genera varied substantially through- out the study (Table 1). For example, five genera occurred in samples from all months, whereas four genera were present in samples from only 1 or 2 months. Total relative frequency was comparatively high (greater than 80%) for Rhizopogon and Geopora and below 10% for eight genera.

Relative frequency of Geopora and Genea was significantly higher during winter and spring (December to June) than during summer and fall (July to November). Hymenogaster occurred more often between January and June than between July and December. In contrast, relative frequency of Hysterangium and Rhizopogon did not change significantly by season throughout the year. Combined relative frequency for eight selected genera (taxa occurring in 40% or more of animals sampled) ranged from 31% in March to 89% in June (Fig. 1). No significant differences in relative frequency of consumption were found between males (captured 85 times) and females (captured 77 times).

Discussion In general, the frequencies with which specific fungal taxa

were consumed reflected seasonal availability of those genera, as documented previously by sporocarp collections (G. Hunt and J. M. Trappe, see footnote 3). Notable exceptions occurred, however.

Consumption of the eight taxa that composed 40% of the squirrel diet was unexpectedly low in March and April, when

MONTHS

FIG. 1. Combined relative frequency by month of eight fungal taxa composing 40% or more of the total annual frequency of the northern flying squirrel diet in southwestern Oregon.

abundance of hypogeous fungi generally increases (G. Hunt and J . M. Trappe, see footnote 3). Our data provide no explanation for this apparent drop in consumption of fungi in the eight taxa. The decrease in relative frequency from June to August was expected, because summer drought reduces sporocarp produc- tion. Rain in September and October and falling temperatures in November and December could account for the peak in relative frequency of consumption in the fall.

Our data indicate that Rhizopogon was consumed throughout the study, even though this genus fruits more abundantly in summer and fall (G. Hunt and J .M. Trappe, see footnote 3). Several factors may explain why consumption frequency did not always fluctuate with known fruiting patterns and abundance, in this and other instances. (i) Some taxa may be consumed selectively because they differ in palatability, odor, or both. (ii) Our sample size may have been too small to detect all significant changes in frequency of consumption; however, consumption patterns did reflect known seasonal fruiting habits for some genera. (iii) Fruiting patterns of some species in our stand may differ from those in previously studied stands because of particular conditions. For example, we have observed that several species of hypogeous fungi, including Rhizopogon vinicolor Smith, R. truncatus Smith, and Gautieria monticola Harken, fruit in or adjacent to large, well-decomposed wood debris (G. Hunt, unpublished data). Thus the fruiting of some species may be enhanced in stands with substantial amounts of large rotting wood. Such wood also retains a high water content through dry periods (Maser and Trappe 1984), which may extend the fungal fruiting season. (iv) Flying squirrels could circumvent seasonal variation in fruiting by drying and storing sporocarps for later consumption. Although we have no direct evidence for this behavior in flying squirrels, other small mammals engage in such activities (Ure and Maser 1982). The red squirrel (Tamiasciurus hudsonicus Erxleben) in northeastern Oregon caches hypogeous sporocarps in bird boxes (R. G. Anderson, personal communication), and we have found that

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

Uni

vers

ity o

f Sy

dney

on

03/1

0/13

For

pers

onal

use

onl

y.

MASER ET AL. 2089

captive deer mice (Peromyscus maniculatus (Wagner)) store hypogeous sporocarps. (v) Spores may be retained in the digestive tract for days, or even weeks, after ingestion. We have no direct evidence for this in flying squirrels, but captive deer mice in our laboratory retained fungal spores in the cecum for more than a month (unpublished data).

Mycorrhizal fungi play a vital role in nutrient cycling, productivity, and plant succession in ecosystems. They also are the primary food resource for flying squirrels in our study area and they provide a remarkably reliable nutrient base for these animals. The squirrels extract nutrients from the sporocarps (Fogel and Trappe 1978; Gronwall and Pehrson 1984; Sanders 1984) and concentrate viable fungal spores (Trappe and Maser 1976; Kotter and Farentinos 1984), nitrogen-fixing bacteria, yeast, and growth factors in their excretory pellets (Maser et al. 1978; Li and Castellano 1985; Maser, Maser, and Trappe 1985; Li et al. 1986). As they travel through the forest, they disperse the fungal spores in their droppings. When conditions are favorable, the spores germinate, either forming a new colony or fusing with and contributing new genetic material to an existing fungal thallus (Trappe and Molina 1986).

The traditional view of forest rodents has been relatively simple, but our perception is changing as we uncover the complex functional relationships in which these mammals are involved.

Acknowledgments Donald K. Grayson, Robert L. Rausch, Peter D. Weigl, and

B. J. Verts reviewed and improved the manuscript. V. Bissell typed the various drafts. We are grateful for the help. This paper represents a partial contribution (No. 16) of the project entitled "The fallen tree-an extension of the live tree." The project is cooperative among the U. S . Department of the Interior, Bureau of Land Management; U. S . Department of Agriculture, Forest Service, Pacific Northwest Forest and Range Experiment Station; Oregon State University, Department of Forest Science; U. S . Department of Agriculture, Agricultural Re- search Service; and Oregon Department of Fish and Wildlife.

FOGEL, R., and J. M. TRAPPE. 1978. Fungus consumption (myco- phagy) by small animals. Northwest Sci. 52: 1-31.

FRANKLIN, J. F., and C. T. DYRNESS. 1973. Natural vegetation of Oregon and Washington. U.S. For. Serv. Gen. Tech. Rep. PNW-8.

GRONWALL, O., and A. PEHRSON. 1984. Nutrient content in fungi as a primary food of the red-squirrel Sciurus vulgaris L. Oecologia, 64: 230-23 1.

KOTTER, M. M., and R. C. FARENTINOS. 1984. Formation of ponderosa pine ectomycorrhizae after inoculation with feces of tassel-eared squirrels. Mycologia, 76: 758-760.

LI, C. Y., and M. A. CASTELLANO. 1985. Nitrogen-fixing bacteria isolated from within sporocarps of three ectomycorrhizal fungi. In Proceedings of the 6th North American Conference on Mycorrhizae, Bend, OR, 25-29 June 1984. Edited by R. Molina. Forest Research Laboratory, Oregon State University, Corvallis, OR. p. 164.

LI, C. Y., C. MASER, Z. MASER, and B. A. CALDWELL. 1986. Nitrogen-fixing bacteria in feces of three forest rodents. Great Basin Nat. In press.

MASER, C., B. R. MATE, J. F. FRANKLIN, and C. T. DYRNESS. 198 1. Natural history of Oregon Coast mammals. U.S. For. Serv. Gen Tech. Rep. PNW- 133.

MASER, C., and J . M . TRAPPE (Technical editors). 1984. The seen and unseen world of the fallen tree. U.S. For. Serv. Gen. Tech. Rep. PNW- 164.

MASER, C., J. M. TRAPPE, and R. A. NUSSBAUM. 1978. Fungal - small mammal interrelationships with emphasis on Oregon coni- ferous forests. Ecology, 59: 799-809.

MASER, Z., C. MASER, and J. M. TRAPPE. 1985. Food habits of the northern flying squirrel (Glaucomys sabrinus) in Oregon. Can. J. Zool. 63: 1084- 1088.

MASER, Z., R. MOWREY, C. MASER, and W. YUN. 1985. Northern flying squirrel: the moonlight truffler. In Proceedings of the 6th North American Conference on Mycorrhizae, Bend, OR, 25-29 June 1984. Edited by R. Molina. Forest Research Laboratory, Oregon State University, Corvallis, OR. p. 269.

MCKEEVER, S. 1960. Food of the northern flying squirrel in north- eastern California. J. Mammal. 41: 270-271.

SANDERS, S. D. 1984. Foraging by Douglas tree squirrels (Tamias- ciurus douglasii: Rodentia) for conifer seeds and fungi. Ph .D. dissertation, University of California, Davis.

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., Z. MASER, and C. MASER. 1986. Synoptic spore key to genera of hypogeous fungi of northern temperate forests with special reference to animal mycophagy . U . S. Forest Service Pacific North- west Research Station, Portland, OR. In press.

TRAPPE, J. M., and R. MOLINA. 1986. Taxonomy and genetics of mycorrhizal fungi: their interaction and relevance. In Proceedings of the 1st European Symposium on Mycorrhizae. Edited by V. Gianinazzi-Pearson and S. Gianinazzi. Institut National de la Recherche Agronomique. In press.

URE, D. C., and C. MASER. 1982. Mycophagy of red-backed voles in Oregon and Washington. Can. J. Zool. 60: 3307-3315.

WELLS-GOSLING, N., and L. R. HEANEY. 1984. Glaucomys sabrinus. Mamm. Species, 229: 1-8.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

Uni

vers

ity o

f Sy

dney

on

03/1

0/13

For

pers

onal

use

onl

y.