Introduction Numerous Species of Small Mammals Feed on Hypogeous Sporocarps of Mycorrhizal Fungi
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Cynthia J. Zabel and Jeffrey R. Waters, U.S. Forest Service, Pacific Southwest Research Station, 1700 Bayview Drive, Arcata, California 95521 introduction Numerous species of small mammals feed on of the 155 flying squirrel fecal samples exam- hypogeous sporocarps of mycorrhizal fungi (here- ined, and flying squirrel density was correlated after referred to as “truffles”) in temperate and with frequency of hypogeous sporocarps across tropical forests throughout the world (e.g., Tevis the 12 stands in which we sampled. Lichens, 1953, Fogel and Trappe 1978, Maser et al. 1978, unknown vegetative matter, spores from epigeous Taylor 1992, Johnson 1994, Janos et al. 1995). fungi, pollen from conifer staminate cones, in- Some species, such as the northern flying squir- sect parts, and seed parts were also observed in rel (Glaucomys sabrinus), California red-backed fecal samples. In another study, we found signif- vole (Clethrionomys californicus) (Ure and Ma- icant association between thinning level (heavily ser 1982), and various species within the marsu- thinned, moderately thinned, and unthinned) and pial family Potoridae (Taylor 1992, Claridge and frequencies of the 5 most common truffle gen- Cork 1994, Johnson 1994) are highly mycopha- era, suggesting that thinning led to changes in gous and feed on truffles as one of their primary the composition of truffle species (Waters et al. food sources. Although sporocarps are consumed, 1994). We also found significant association be- spores are viable after passage through small tween stand age (old-growth and mature stands mammal digestive tracts (Trappe and Maser 1977, Cork and Kenagy 1989, Claridge et al. 1992), and that originated after wildfire) and frequencies of Cork and Kenagy (1989) showed that passage truffle species, suggesting that disturbance had through the digestive tract of a species of ground long-lasting effects on the composition of truffle squirrel enhanced spore germination. Because species (Waters et al. In Press). Other studies most species of fungi that produce hypogeous spo- have also shown that composition of hypogeous rocarps eaten by small mammals are thought to sporocarps varied among stands with different be mycorrhizal, mycophagous small mammals management or natural disturbance histories (Vogt contribute to the maintenance of mycorrhizal sym- et al. 1981, Luoma et al. 1991, North et al. In bioses (Trappe and Maser 1977, Maser et al. 1978). Press). Because forest management alters spe- In a previous study we evaluated associations cies composition of fungal sporocarps, we wanted between northern flying squirrel density and for- to know whether palatability varied among spo- est structure in fir (Abies spp.) stands in the Lassen rocarps of different fungal species for a common, National Forest in northeastern California (Wa- mycophagous small mammal. We designed this ters and Zabel 1995). We found truffles in each study to determine whether northern flying squir- Northwest Science, Vol. 71, No. 2, 1997 103 0 1997 by the Northwest Scientific Association. All rights reserved. rels preferred sporocarps of certain fungal spe- tain Experimental Forest. Fir (A. concolor and cies over others, and secondarily to compare pref- A. magnifica) seeds were obtained from a U.S. erences of flying squirrels between fungal spo- Forest Service nursery in Placerville, California. rocarps and other naturally occurring food types. We used sporocarps of 5 species of fungi that were found in sufficient quantities at the time of sam- Methods pling (14-16 August 1994). Sporocarps were found by raking through the organic layers and upper Flying squirrels were trapped 4-5 August 1994 mineral soil in 4-m2 circular plots (I. 13-m radius) in 2 old-growth (>200 years) fir stands in Swain Mountain Experimental Forest, located in Lassen randomly located throughout forest stands. The National Forest in northeastern California. Only 5 species were Gautieria monticola, Alpova males were kept for the experiments to control trappei, Gymnomyces abietis, Endoptychum for possible sex effects in food preferences (e.g., depressum,and Arcangeliella lactarioides. the sensory acuity of females may vary accord- Gautieria monticola, Alpova trappei, and ing to reproductive status). Squirrels were trans- Gymnomyces abietis are truffle species; sporo- ported to Humboldt State University in Arcata, carps lack gills and a stipe and are found below California, where they were housed individually ground. Endoptychum depressum and in 1.0x 1.0x1.5-m outdoor cages. Cafeteria-style Arcangeliella Zactarioides are secotioid fungal experiments were conducted in 2 1.2x 1.2x 1.0-m species, which are considered evolutionary inter- cages that had wooden frames and l-cm hard- mediates between fungi that produce epigeous ware cloth sides.Lids were made of clear sporocarps and truffles and have morphological plexiglass. A wooden tray served as the floor of and fruiting characteristics of both groups; spo- each cage. Trays were filled to a depth of 6-7 cm rocarps have convoluted gills that are covered by with peat moss. The 2 cages were located in sepa- a veil, a reduced stipe, and are found both at the rate indoor rooms that lacked windows. ground surface and below ground. The 2 lichens were Letharia vulpina and Bryoriafremontii, which Squirrels were allowed to acclimate to cap- were 2 of the most common epiphytic lichens tivity for 2 weeks before experiments began. within Swain Mountain Experimental Forest. During the acclimation period, squirrels were fed Fungal sporocarps and lichens were kept in a re- samples of the food types used during the experi- frigerator until used in the preference tests. ments for approximately 30 minutes each night while in the test cage. Beginning the day before Size of food samples was standardized across the experiments began, animals were maintained foods and tests; samples were 2-3 cm in diam- on a reduced diet of rat chow, apples, and water. eter. All food samples were weighed before and They were weighed daily to ensure that their weight after each test to determine proportion of food did not drop below 90% of their capture weight. eaten. Each food sample was placed in a ran- domly assigned grid cell across the tray of the Experiments began shortly after sunset when feeding cage before the squirrel entered the cage. squirrels were moved from their outdoor cages Truffles were buried 2-3 cm, and all other samples into the test rooms, which were each illuminated with a red light. Order of testing and test room were placed on top of the peat moss. Fir seeds were placed in a petri dish 4 cm in diameter that were randomly determined each night. Flying squirrels entered the center of the cage through a was buried so it was level with the peat moss. plastic tube (8 cm in diameter). An observer re- The peat moss was thoroughly mixed with a rake corded behavioral observations with a tape re- after each experiment and was changed nightly. corder from a blind 1 m from the test cage. Seven squirrels were tested for 45 minutes each night Data Analysis for 4 consecutive nights (17-20 August 1994). We compared 3 measures of food preference: ( 1) Preferences of flying squirrels were compared proportion of food eaten, (2) number of tests in among 3 types of food that are available to flying which food was at least partially eaten, and (3) squirrels in the Lassen National Forest: fungal rank order food was first eaten. Any food types sporocarps, epiphytic lichens, and fir seeds. Fungal not eaten were ranked last. We used the Spearman sporocarps and lichens were collected in old- rank correlation coefficient for each of the 3 growth and mature stands within Swain Moun- pair-wise comparisons of these measures as an index 104 Zabel and Waters The 3 truffle species were consumed more than dietary studies, which have not found conifer seeds the 2 secotioid species, which is consistent with to be common in the diets of northern flying squir- results of other studies that showed hypogeous rels. Brink and Dean (1966) found that red squirrels sporocarps were more common in the diets of (Tamiasciurus hudsonicus) in Alaska could main- mycophagous small mammals than were epigeous tain weight on a diet of white spruce (Picea glauca) sporocarps (Maser et al. 1978,1986, Ure and Maser cones, but northern flying squirrels could not. In 1982, Maser et al. 1985, Maser and Maser 1987, our study, fir seeds were not presented on the cone Taylor 1992). Our results are also consistent with as they would be found under natural conditions. 3 studies that found that spores of Gautieria and Because the squirrels did not have to extract seeds the Rhizopogon group, which includes the genus from the cone, however, the energetic value of Alpova (Castellano et al. 1989), were the most the seeds was theoretically greater than the ener- common truffle spores identified in northern fly- getic value of fir seeds under natural conditions. ing squirrel stomachs and fecal pellets in Oregon We showed that preference varied significantly and California (Maser et al. 1985, Maser et al. among the 8 foods tested, but we do not know 1986, Hall 1991). Hall (1991), whose study was how the nutritional and energetic values of these conducted in the northern Sierra Nevada not far foods varied. Cork and Kenagy (1989) found that from our study area, found that Gautieria spores the nutritional value of 1 species of truffle were found in 87% of 107 flying squirrel fecal (Elaphomyces granulatus) was low for the ground pellets and stomachs examined, the Rhizopogon squirrel Spermophilus saturatus because digest- group in 81%, and the Martellia group, which ibility of the sporocarps was low. They hypoth- includes the genus Gymnomyces (Castellano et esized that truffles in general have relatively low al. 1989), in 17%. Maser et al. (1985) also found nutritional value for small mammals but are com- that the Martellia group was less common than monly consumed because truffles are seasonally Gautieria and the Rhizopogon group, and Maser abundant and highly detectable due to the strong et al.