Great Basin Naturalist

Volume 48 Number 3 Article 8

7-31-1988

Interactions among , mycorrhizal fungi, and coniferous forests in Oregon

Chris Maser U.S. Department of Interior, Bureau of Land Management, Corvallis, Oregon

Zane Maser Oregon State University, Corvallis

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Recommended Citation Maser, Chris and Maser, Zane (1988) "Interactions among squirrels, mycorrhizal fungi, and coniferous forests in Oregon," Great Basin Naturalist: Vol. 48 : No. 3 , Article 8. Available at: https://scholarsarchive.byu.edu/gbn/vol48/iss3/8

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. INTERACTIONS AMONG SQUIRRELS, MYCORRHIZAL FUNGI, AND CONIFEROUS FORESTS IN OREGON

Chris Maser' and Zane Maser^

Abstract —We examined the mycophagy (ingestion of fungi) of squirrels of five genera and eight species in the coniferous forests of Oregon. Data from 644 dietary samples demonstrated that scjuirrels of all eight species are mycophagous and eat the belowground fruiting bodies of at least 26 genera of mycorrhizal fungi. Four species are primarily arboreal and active throughout the year; the other four are primarily terrestrial and hibernate during winter. Of the squirrels examined, only the northern flying [Glaucomys sahrinus [Shaw]) is nocturnal and almost exclusively a fungivore. The flying squirrel is used to illustrate the dynamics of all the squirrels in association with hypogeous mycorrhizal fungi, nitrogen-fixing bacteria, yeast, and coniferous trees in Oregon forests because we have studied it the most. Squirrels may prove to be vital links among different processes within temperate coniferous forests.

Although early studies of small- Other studies of the northern flying squirrel food habits included a few papers dealing with (Maser et al. 1985, 1986), the' yellow-pine mycorrhizal fungi (e.g., Bakerspigel 1956, { amoenus [J. A. Allen]) 1958, Dowding 1955, Hamilton 1941, Tevis (Maser and Maser 1987), and the Siskiyou 1952, 1953, Whitaker 1962, Williams and chipmunk {Eutamias siskiyou A.H. Howell) Finney 1964), the first interdisciplinary stud- (Mclntire 1980) are based on 524 samples. So, ies to examine the role of small as for all practical purposes, this paper is based dispersal agents for spores of mycorrhizal on data from 644 squirrels in Oregon forests. fungi are recent (Kotter and Farentinos 1984a, 1984b, Maser, Trappe, and Nussbaum Study Area 1978, Maser, Trappe, and Ure 1978, Trappe and Maser 1976, 1977, Ure and Maser 1982). Squirrels from five physiographic provinces The first extensive literature review of small- were studied: Coast Range, Klamath Moun- mammal mycophagy was published in 1978 tains, Western Cascades, High Cascades, and (Fogel and Trappe 1978). Symbioses between Blue Mountains (Fig. 1). They were taken small-mammal and mycorrhizal fungus have from five forest types within these areas: (1)

also been documented recently in Europe western hemlock (Tsu^a heterophylla [Raf ] (Blaschke and Baumler 1986, Durrieu et al. Sarg.) zone, which encompasses most of the 1984, Froidevaux 1981). Only now are re- Coast Range and Western Cascades provinces searchers beginning to understand the impor- of western Oregon; (2) mixed-conifer and tance of nitrogen-fixing bacteria in the symbi- mixed-evergreen zone of the Klamath Moun- otic relation of small-mammal, mycorrhizal tains province of extreme southwestern Ore- fungus, coniferous tree mutualism (Ei ct al. gon; (3) subalpine forest—Pacific silver fir 1986). {Abies amahilis [Dougl.] Forbes), subalpine

In this paper we present data on the fungal fir (A. lasiocarpa [Hook.] Nutt.), and moun- diet of squirrels of four genera and six species tain hemlock (i. incrtcnsiana [Bong.] Carr.) from the coniferous forests of Oregon, and we zone—along the crest of the High Cascades; examine potential interactions among five (4) ponderosa pine {Pititis pondcrosa Dougl. genera of eight species of mycophagous s(juir- ex Loud.) zone on the east slope of the High rels and the coniferous forests of Oregon. C'ascades; and (5) grand fir (A. grandis

In addition to giving new data on the 118 [ Dougl. ] Lindl. ) and Douglas-fir (Pseudotsuga squirrels, this paper is intended as a synthesis mcuzicsii [Mirb.] Franco) zone of the Blue of the potential ecological roles s(juirrels play Mountains pro\ ince in extreme northeastern in coniferous forests of the Pacific Northwest. Oregon (Franklin and Dyrness 1973).

'U.S. Departrnt-nt of the Interior, Bureau of I-and ManaRement, .1200 Jefferson Way, Corvallis. Oregon 97.T}1 (I'SA). ^Department of Fore.st Science. Oregon State University. Corvallis. Oregon 97331 (USA).

358 July 1988 Maser, Maser: Squirrels and Mycorrhizal Fungi 359

Fig. 1. Physiographic and geological provinces of Oregon (after Franklin and Dyrness 1973): 1 = Coast Range, 2 Klamath Mountains, 3 = Willamette Valley, 4 = Western Cascades, 5 = High Cascades, 6 = Blue Mountains, 7 Columbia Basin, 8 = High Lava Plains, 9 = Basin and Range, and 10 = Owyhee Upland.

Methods and Materials spores. Fungal taxa were identified by use of a

spore key (Trappe et al. , in press). Percentage One hundred and two squirrels of four gen- of volume of each fungal taxon in each stomach era and six species were either dead-trapped was estimated visually and recorded for each or shot and quick-frozen in the field for later slide. analysis. Stomachs were excised in the labora- tory and preserved in vials of 10% formalin. Results Stomach contents were examined micro- scopically at 100, 400, and lOOOX magnifica- Twenty-six genera of hypogeous (below- tion. For fungal analysis, each vial was shaken ground fruiting) mycorrhizal fungi were iden- vigorously and opened. Narrow, parallel- tified from the stomachs of the 118 squirrels

sided forceps were plunged to the bottom, (Table 1). Rhizopogon was the dominant closed, and withdrawn. The captured mate- genus in all squirrel diets, followed by Gau- rial was placed on a microscope slide, mixed tieria. These two genera were the only ones with a drop of Melzer's reagent, and enclosed eaten by all eight species of squirrels. Hy-

under a 22 x 40-mm cover slip. (See Trappe rnenogaster was third, although it was con- et al., in press, for details of methods.) The sumed by only three species of squirrels. Hys- slide was systematically moved over the en- terangimn, not eaten in great abundance, was tire area of the cover slip to examine fungal found in four of the eight species of squirrels. 360 Great Basin Naturalist Vol. 48, No. 3

Table 1. The occurrence of spores of 26 fungal taxa in the stomachs of 118 squirrels (Sciuridae) from a range of forest types in Oregon. Percent volume by stomach contents and percent frequency (in parentheses) of fungal taxa; n = number of individuals sampled. July 1988 Maser, Maser: Squirrels and Mycorrhizal Fungi 361 in a single Douglas squirrel included Leuco- hyphae extend into the soil and serve as exten- gaster, Leucophelps, Hymenogaster, Hys- sions of the root systems of the hosts and are terangium, and Melanogaster. The most fun- both physiologically and geometrically more gal genera from one Douglas squirrel stomach effective for nutrient absorption than are the was seven. Although Rhizopogon ranged from roots themselves (Maser, Trappe, and Nuss- to 100% of the stomach contents of the red baum 1978, Trappe 1981, Trappe and Fogel squirrel (T. hudsonicus [Erxleben]), Gau- 1977, Trappe and Maser 1977). Both ectomy- tieria ranged from to 20%. The only other corrhizal and endomycorrhizal fungi serve hypogeous fungus that accounted for more similar purposes, but the fungi usually occur than 10% of stomach contents was Hymeno- on different host plants. gaster; it accounted for 80% in one stomach. When ectomycorrhizal fungi are predomi- The most fungal genera from one red squirrel nant in the fungal diet of small mammals, they stomach was four. are also predominant in the habitat, such as Rhizopogon ranged from to 71% of the coniferous forests. There, they are mostly As- stomach contents from western gray squirrels comycetes and Basidiomycetes associated {Sciurus griseus Ord), and Gautieria ranged with Pinaceae, Fagaceae, Salicaceae, Betu- from to 70%. The only other hypogeous laceae, and a few other plant families (Fogel fungi that accounted for 10% or more of a and Trappe 1978, Maser, Trappe, and Nuss- western gray squirrel's stomach contents were baum 1978, Trappe and Maser 1977). Tuber and Leucogaster. The most fungal gen- The Endogonaceae (Zygomycetes) include era from one stomach was five. saprophytic, ectomycorrhizal, and vesicular- arbuscular (VA) endomycorrhizal species. Discussion Vesicular-arbuscular mycorrhizae are formed by Endogonaceae with most higher plants The following is a synthesis of how we think that are not ectomycorrhizal, including the some of the forest puzzle fits together. The Cupressaceae, Taxodiaceae, Aceraceae, and whole is far greater than the sum of its parts; most herbaceous plants. Most plants on this view may help in understanding that sim- stream banks, meadows, and prairies, and in plification of forest diversity may have nega- early stages of forest succession, in forest un- tive effects that go beyond our expectations or derstories, or in forests containing VA-mycor- knowledge. rhizal tree species have VA-mycorrhizal En- dogonaceae associated with their roots The Hypogeous Fungi (Maser, Trappe, and Nussbaum 1978, Miller The term mycorrhiza, literally meaning 1979, Reece and Bonham 1978, Trappe 1981, "fungus-root," denotes the symbiotic relation Wilhams and Aldon 1976). between certain fungi and plant roots. Fungi Fungal-Forest Relations that produce hypogeous sporocarps (below- ground fruiting bodies) are probably all my- Sporocarps of hypogeous fungi may be corrhizal (Miller 1983, Trappe and Maser available year-round, in the Oregon Coast 1977). Woody plants in the Pinaceae (pine, Range for example, although their abundance Pinus; fir, Abies; spruce, Picea; larch, Larix; varies seasonally and always decreases in win- Douglas-fir, Pseudotsuga; hemlock, Tsuga), ter (Hunt and Trappe, in press) (Fig. 2). Num- Fagaceae (oak, Quercus), and Betulaceae bers of species and biomass of hypogeous (birch, Betula; alder, Alnus) especially de- fungi differ among stands that have the same pend on mycorrhiza-forming fungi for nutri- species of trees. For example, 30 species ent uptake, a phenomenon traceable back of Basidiomycetes and Ascomycetes, with some 400 million years to the earliest known monthly biomass averaging 2.09 kg/ha, were fossils of plant rooting structures (Harley and recorded for a north-facing stand of Douglas- Smith 1983, Marks and Kozlowski 1973, fir in the central Oregon Coast Range. Fifteen Pirozynski and Malloch 1975). species, with monthly biomass averaging 1.20 Mycorrhizal fungi absorb nutrients and wa- kg/ha, were present on a nearby south-facing ter from soil and translocate them to a host slope (Fogel and Hunt 1979, Hunt and plant. The host provides sugars through pho- Trappe, in press). tosynthesis to the mycorrhizal fungi. Fungal Production of sporocarps fluctuates widely 362 Great Basin Naturalist Vol. 48, No. 3

cvj E CO

MONTH (1980-1982)

Fig. 2. Monthly production of hypogeou.s sporocarps in an Oregon Coast Range Douglas-fir stand (after Hunt and Trappe, in press).

Rhizopogon \ ww\\\\\w\\\\\\\\\\\\\\\\ Gautieria

Hymenogaster n\\\\\\\\\\\\\\\\\\\\\\\\- \\\\\\\\\W Hysterangium

Tuber Genea Truncocolumella

1^ M M N

Fig. 3. Seasonal occurrence of selected genera of hypogeous fungi in the Oregon C^oa.st Range (adapted from Hunt and Trappe, in press).

over short periods in a given stand. Peaks in for a given genus or species varies with year, hiomass frequently result from "blooms" of stand structure, and weather conditions. one species, such as a large crop o{ Gauticrki Many hypogeous Ascomycetes (true truffles, monticola Harkn. that comprised 89% of the such as Ccopora sp. and Genca sp.) fruit more total sporocaqo biomass in October 1980 abundantly in winter and spring than in sum-

(Hunt and Trappe, in press). Most genera of mer and fall. Of the hypogeous Basidio- hypogeous fungi fruit seasonally and can pre- mycetes (false truffles), the genus Rliiz()j)o^on

dictably be found during certain months fruits primariK' in summer and fall, but a few (Fig. 3). species, such as R. vinicolor \.H. Smith, fruit Fruiting patterns are relatively consistent, throughout the year. F'ruiting of Truncocol-

although length of the annual fruiting period umella citrina Zeller is invariablv restricted to July 1988 Maser, Maser: Squirrels and Mycorrhizal Fungi 363

Table 2. General distribution of mycophagous squirrels in Oregon by physiographic province and forest type.

Taxa of squirrels

Physiographic province Northern Douglas Red Western Yellow- Townsend Siskiyou Mantled Forest type flying squirrel squirrel gray pine chipmunk chipmunk ground squirrel squirrel chipmunk squirrel Coast range Western hemlock zone Klamath Mountains Mixed-conifer and mixed-evergreen zone Western Cascades Western hemlock zone High-Cascades (crest)

Pacific silver fir,

subalpine fir, and mountain hemlock zone High Cascades (east flank) Ponderosa pine zone Blue Mountains Grand fir and Douglas-fir zone

'The Townsend chipmunk and the Siskiyou chipmunk are separated in the Klamath Mountains Province by habitat. The Townsend chipmunk is associated primarily with the mixed-conifer forest type; the Siskiyou chipmunk is associated primarily with the mixed-evergreen forest type.

"The yellow-pine chipmunk and the Townsend chipmunk are separated along the crest of the High Cascades Province by habitat. The yellow-pine chipmunk is largely confined to the lodgepole pine {Pinus contorta) forest type that extends down the east flank of the High Cascades Province into the Ponderosa Pine Zone. The Townsend chipmunk occurs primarily in the Pacific silver fir-subalpine fir-mountain hemlock forest that extends down the west flank of the High Cascades Province to the Western hemlock zone of the Western Cascades Province.

The Douglas squirrel and the red squirrel both occur in the Blue Mountains Province. Their separation, in the extreme northeastern part of the province, is apparently the result of dominant tree species. The red squirrel is closely associated with lodgepole pine, which dominates much of the northeastern Blue Mountains Province. The Douglas squirrel occurs throughout the rest of the forested areas in Oregon, which are dominated by conifers other than lodgepole pine (Hatton and Hoffmann 1979).

September through December in the Pacific The Squirrels Northwest. In contrast, the two most abun- Five genera and eight species of squirrels dant species of Hysterangium in the Coast were collected in the study area: (1) northern Range (//. coriaceum Hesse and H. crassurn flying scjuirrel, (2) Douglas squirrel, (3) red [Tul. & Tul. ] Knapp) commonly fruit through- squirrel, (4) western gray squirrel, (5) yellow- out the year (Hunt and Trappe, in press). pine chipmunk, (6) Townsend chipmunk, (7) Seasonal abundance of hypogeous fungi gen- Siskiyou chipmunk, and (8) mantled ground erally follows changes in temperature and squirrel. These squirrels do not occur simulta- precipitation (Fogel 1976). neously in either a given physiographic prov- Several species of hypogeous fungi, includ- ince or a given forest type (Table 2). ing Rhizopogon vinicolor, R. truncatus Lin- The squirrels are separated in habitat use in der, and Gautieria monticola, are known to three basic ways. First, if habitat use is very fruit in or adjacent to large, well-decomposed, similar, the squirrels occur in different forest woody debris. Thus, stands that have substan- types, such as the Townsend chipmunk in tial amounts of large, rotting wood may en- mixed conifer and the Siskiyou chipmunk in hance the fruiting of some species. Further, (Table if habitat the seasonal fruiting period may be extended mixed evergreen 2). Second, is very similar in site, the squirrels are by proximity of fungi to large, fallen, rotting use one trees because of the high water content such separated by time of activity, such as noctur- trees retain through dry periods (Maser and nal for the northern flying squirrel and diurnal Trappe 1984). Production of hypogeous spor- for the Douglas squirrel (Table 3). Third, if ocarps throughout the year provides a re- squirrels are in the same area and are active at markably reliable nutrient base for small the same time, they use the habitat differ- mammals, even though most species of hypo- ently, such as the yellow-pine chipmunk that geous fungi fruit only part of the year and total climbs into shrubs and trees and the mantled annual abundance differs substantially from ground squirrel that does not (Table 3). year to year. Some species, such as the Siskiyou chipmunk, 364 Great Basin Naturalist Vol. 48, No. 3

Table 3. General behavior patterns of mycophagous squirrels in Oregon.

Taxa of squirrel

Behavior Northern Douglas Red Western Yellow- Townsend Siskiyou Mantled Source flying squirrel squirrel gray pine chipmunk chipmunk ground squirrel squirrel chipmunk squirrel

Reproduction and nesting In canopy x x x x Brand 1974, Broadbooks 1974, Occasionally 19.58, above ground x x Huestis 19.51,

and low in Maser et al. 1981, trees Shaw 1944

On or below ground x x x x

Diet Mycorrhizal xxxxx xxx Bailey 1936, fungi Broadbooks 1958, Gordon 1943, Maser and Maser Lichens 1987, Maser etal. 1978, 1981, 1985, 1986, Nonfungal Mclntire 1980, foods 1984, Stienecker and Browning 1970, Tevis 1952, 1953

Time OF ACTIVITY Nocturnal Bailey 1936, Maser etal. 1981 Diurnal

Climbs Into trees Bailey 1936, Maser etal. 1981, Shrubs and Mclntire 1980, trees 1984

Neither shrubs nor trees

Hibernates No Bailev 1936, Yes Maser etal. 1981

further divide the habitat by sex; female.s of the flying squirrel is nocturnal, and the Dou- thi.s species are more closely associated with glas squirrel and red squirrel arc diurnal

trees and large, fallen woody material (logs) (Table 3). The diurnal squirrels, however, do

than are males because females keep their not overlap iu habitat use (Table 2). These young in and around such protective cover. scjuirrels are primarily inhabitants of conifer- Such differences in habitat use carry over to ous forests. The western gray squirrel, on the food habits (Mclntire 1980). other hand, may be associated with the flying s(juirrel and tiie Douglas s(juirrel, but usually Behavior among Squirrels in mi.xed forests, such as the ecotone between The northern flying squirrel occurs through- oak woodlands and coniferous forest. The

out coniferous forests of Oregon (Table 2). western gray scjuirrel, although diurnal, is Where the flying s(juirrel and either the Dou- largely separated from the Douglas s(}uirrel glas squirrel or red squirrel occupy the same by habitat and food habits other than my- area, they are separated by activity period; cophagy. July 1988 Maser, Maser: Squirrels and Mycorrhizal Fungi 365

The above squirrels are primarily arboreal. phyll-lacking mycorrhizal fungi, which gener- The and mantled ground squirrel ally are not competent saprophytes. The fun- are mainly terrestrial, and both are diurnal gus absorbs minerals, other nutrients, and (Table 3). Where the yellow-pine chipmunk water from the soil and translocates them into and Townsend chipmunk come together, the host. Further, nitrogen-fixing bacteria they are separated by habitat (Maser, unpub- (Azospirillum sp.) that occur inside the my- lished data) (Table 2) or by the use of vege- corrhiza use a fungal "extract" as food and in tative cover, or both (Meredith 1972). The turn fix atmospheric nitrogen (Li and Castel- Townsend chipmunk and Siskiyou chipmunk lano 1985). The available nitrogen may be also use different habitats where they occur used by both the fungus and the host tree. In effect, together (Table 2). The mantled ground squir- mycorrhiza-forming fungi serve as highly efficient extensions of rel may overlap in habitat use with all species the host root system. Many of the fungi also of chipmunks but is different enough in tem- produce growth regulators perament that serious overt aggression does that induce production of new root tips and increase the useful life not appear to be a problem (Broadbooks 1958, span of the host roots. At the same time, host plants Gordon 1943). prevent mycorrhizal fungi from damaging Of all the squirrels we studied, only the the roots. Mycorrhizal colonization enhances northern flying squirrel is nocturnal and a resistance to attack by pathogens. Some my- strict fungivore (Table 3). The other seven corrhizal fungi produce compounds that pre- species are diurnal and opportunistic fungi- vent pathogens from contacting the root sys- vores. Where they are sympatric, their di- tem (Harley and Smith 1983, Marks and ets—other than fungi—differ. Kozlowski 1973, Trappe and Maser 1977). The squirrels that are primarily arboreal are Basidiomycetes and Ascomycetes that pro- active all year, but those that are primarily duce hypogeous sporocarps are all presumed terrestrial hibernate (Table 3). The chip- to be mycorrhizal (Miller 1983, Trappe and munks apparently store food, such as seeds, in Maser 1977). their nests for winter sustenance (Broadbooks 1958, Stebbins and Orich 1977); whereas the The Sporocarp Connection mantled ground squirrel accumulates much Sporocarps are the initial link between hy- body fat in preparation for hibernation (Blake pogeous mycorrhizal fungi and the flying 1972, Yousef and Bradley 1971). squirrel. Flying squirrels nest and reproduce Squirrel-Forest Relations in the tree canopy and come to the ground where they dig and eat hypogeous sporocarps. We will use the northern flying squirrel to As a sporocarp matures, it produces a strong illustrate the squirrels we studied because we odor that attracts the foraging squirrel (Maser, know the most about the flying squirrel and Trappe, and Nussbaum 1978, Trappe and because the other squirrels serve similar eco- Maser 1977). (The odors are strong enough logical functions in the forest. that we can detect many of them.) Evidence of The most obvious northern flying squirrel- a squirrel's foraging remains in the form of forest relations are those that occur on the shallow pits in the forest soil and occasional surface of the ground, such as foraging. Even partially eaten sporocarps. their nesting and reproductive behavior re- Sporocarps of hypogeous fungi contain nu- mains relatively obscure because of nocturnal trients necessary for small mycophagists (Fo- habits. As we probe the secrets of the flying gel and Trappe 1978, Gronwall and Pehrson squirrel, however, at least four intercon- 1984, Sanders 1984). In addition to having nected cycles emerge that unite the above- nutritional value, sporocarps contain water, ground and belowground parts of the forest. fungal spores, nitrogen-fixing bacteria, and

yeast (Li and Castellano 1985, Li et al. 1986, The Fungal Connection Maser, Trappe, and Nussbaum 1978, Maser Fungal hyphae penetrate the tiny, non- et al. 1985). woody rootlets of the host plant to form a The Squirrel Connection balanced, harmless mycorrhizal symbiosis with the roots. The host plant provides simple Most nutrients required by vascular plants sugars and other metabolites to the chloro- are absorbed from soil via mycorrhizal fiingi. 366 Great Basin Naturalist Vol. 48, No. 3

These fungi therefore clearly play a vital role where they fall. In the forest canopy, the pel- in nutrient cycling, productivity, and plant lets might remain and disintegrate in the tree succession. As forest succession advances, tops. Or a pellet could drop to a fallen, rotting mycophagous squirrels have different fungi tree and inoculate the wood (Maser and available as food in differing relative abun- Trappe 1984). On the ground, a squirrel dances, and the squirrels' defecation of viable might defecate on a disturbed area of the spores may help pace successional advance- forest floor where a pellet could land near a conifer rootlet ment. Spore dispersal is thus an integral part feeder that may become inocu- of the fungal cycle. lated with the mycorrhizal fungus when spores When flying squirrels eat sporocarps, they germinate (Fries 1982). If environmen- consume fungal tissue containing nutrients, tal conditions are suitable and root tips are available water, viable fungal spores, nitrogen-fixing for colonization, a new fungal colony may be established. Otherwise, hyphae of bacteria, and yeast. Pieces of sporocarp move germinated spores may fuse with an existing to the stomach where fungal tissue is di- fungal thallus and thereby contribute new ge- gested, then through the small intestine netic material (Trappe and Molina 1986). where absorption takes place, then to the ce- The northern flying squirrel exerts a dy- cum. The cecum is like an eddy along a swift namic, functionally diverse influence within stream; it concentrates, mixes, and retains the forest. The complex of effects ranges fungal spores, nitrogen-fixing bacteria, and through the crown of the tree, down to the yeast (Li et al. 1986, Maser and Maser, un- soil surface, and into the soil mantle where, published data). Captive deer mice {Per- through mycorrhizal fungi, nutrients are con- omyscus maniculatus [Wagner]) retained fun- ducted through the roots and into the trunk gal spores in the cecum for more than a month and crown of the tree (Fig. 4). after ingestion (Maser and Maser, unpub- lished data). In the colon, undigested materi- Conclusions als, including cecal contents, are formed into excretory pellets containing viable fungal The world is losing both species and habitats spores, nitrogen-fixing bacteria, and yeast (Li because people are not sensitive to how and et al. 1986). The fecal pellet therefore recon- why they are functionally interconnected. For nects the squirrel to the fungus. maximum information to be derived from the remaining, intact systems, well-planned in- The Pellet Connection terdisciplinary studies are needed. As empha-

A fecal pellet is more than a package ofwaste sized by Rausch (1985), we must understand

products; it is a "pill " of symbionts dispensed the organism and habitat in context with each into the forest. Each fecal pellet contains four other if we are to understand the organism, or

components of potential importance to the its function within its habitat. If we do not

forest: (1) spores of hypogeous mycorrhizal understand the organism and its function

fungi, (2) yeast, (3) nitrogen-fixing bacteria, within its habitat, how can we understand the and (4) the complete nutrient component for results of unexpected changes in the habitat

nitrogen-fixing bacteria. when the organism is removed? For example, The spores of the mycorrhizal fungi are vi- forest , such as the scjuirrels in our able (Kotter and Farentinos 1984b, Trappe study, cat hypogeous mycorrhizal fungi that and Maser 1976). Spores of some mycorrhizal- are obligatory symbionts with coniferous forming fungi are stimulated in germination trees. This seems to be a widespread phe-

by extractives from other fungi, such as veast nomenon in temperate forests. If the potential (Fries 1966, Oort 1974). importance of such interconnected ecological

Each fecal pellet also contains the entire processes is not appreciated, what might the nutrient requirement for Azospirillum sp. effects be of forest simplification through loss The yeast, as a part of the nutrient base, has of organisms and iiabitats that may severely some ability to stimulate both growth a>id impair ecological processes?

nitrogen-fixation in AzospiriUwn sp. (Li et al. The focus of biological research has recently 1986). Abundant yeast propagules may also shifted from the autecology of species to com- stimulate spore germination. munity ecology, but neither approach cap- The fate of fecal pellets varies, depending on tures the functional dynamics of a species in July 1988 Maser, Maser: Squirrels and Mycorrhizal Fungi 367

Squirrels rest and reproduce in trees

Fungi accumulate nutrients Squirrels feed on and produce sporocarps hypogeous sporocarps

Fungi obtain carbohydrates Fecal pellets containing from trees and return nutrients fungal spores, N-fixing which are distributed bacteria, and yeast are throughout the tree deposited on forest floor

Spores germinate and establish new fungal colonies or add genetic material to existing colonies

Fig. 4. Major components of flying squirrel-fungus-tree mutualism.

concert with the ecosystem. Data for this ment of Forest Management, Oregon State paper, for example, have been derived University, Corvallis) read and improved this through cooperative efforts of biologists, my- paper. Sheila Till typed the various drafts. We cologists, and microbiologists. Such a team appreciate the help. approach is essential to understanding the This paper represents a partial contribution vast array of interactions that are part of (No. 33) of the project entitled "The Fallen ecosystem processes. Tree—an Extension of the Live Tree. The project is cooperative among the U.S. De- Acknowledgments partment of the Interior, Bureau of Land Management; U.S. Department of Agricul- D. K. Grayson (Department of Anthro- ture, Forest Service, Pacific Northwest pology and Burke Museum, University of Research Station; Oregon State University, Washington, Seattle), G. Hunt (Balco Refor- Department of Forest Science; U.S. Depart- estation Centre, Kamloops, B.C.) M. L. John- ment of Agriculture, Agricultural Research son (Burke Museum, University of Washing- Service; and Oregon Department of Fish and

ton, Seattle), and J. C. Tappeiner (Depart- Wildlife. 368 Great Basin Naturalist Vol. 48, No. 3

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