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Tree Squirrel Habitat Selection and Predispersal Seed Predation in a Declining Subalpine Conifer

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Tree Squirrel Habitat Selection and Predispersal Seed Predation in a Declining Subalpine Conifer Oecologia DOI 10.1007/s00442-009-1496-5 PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Tree squirrel habitat selection and predispersal seed predation in a declining subalpine conifer Shawn T. McKinney · Carl E. Fiedler Received: 11 February 2008 / Accepted: 22 October 2009 © Springer-Verlag 2009 Abstract DiVerential responses by species to modern variables were the least important in squirrel habitat selec- perturbations in forest ecosystems may have undesirable tion. Squirrel habitat use was lower and varied more in impacts on plant-animal interactions. If such disruptions P. albicaulis-dominant forests, and predispersal cone cause declines in a plant species without corresponding predation decreased linearly with increasing P. albicaulis declines in a primary seed predator, the eVects on the plant relative abundance. In Northern Rocky Mountain sites, could be exacerbated. We examined one such interaction where P. albicaulis mortality was higher and abundance between Pinus albicaulis (whitebark pine), a bird-dispersed, lower, squirrel predation was greater than in Central Rocky subalpine forest species experiencing severe population Mountain sites. In ecosystems with reduced P. albicaulis declines in the northern part of its range, and Tamiasciurus abundance, altered interactions between the squirrel and hudsonicus (red squirrel), an eYcient conifer seed predator, pine may lead to a lower proportion of P. albicaulis con- at 20 sites in two distinct ecosystems. Hypotheses about tributing to population recruitment because of reduced seed squirrel habitat preferences were tested to determine how availability. Reducing the abundance of competing conifers changes in forest conditions inXuence habitat use and will create suboptimal squirrel habitat, thus lowering cone subsequent levels of predispersal cone predation. We per- predation in P. albicaulis and ensuring more seeds are formed habitat selection modeling and variable ranking available for avian dispersal. based on Akaike’s information criterion; compared the level and variance of habitat use between two forest types Keywords Cronartium ribicola (white pine blister rust) · (P. albicaulis dominant and mixed conifer); and modeled Forest health · Forest structure · Forest species composition · the relationship between P. albicaulis relative abundance Pinus albicaulis (whitebark pine) and predispersal cone predation. T. hudsonicus did not demonstrate strong habitat preference for P. albicaulis, and thus, declines in the pine were not met with proportional Introduction declines in squirrel habitat use. P. albicaulis habitat Human-induced changes to forest ecosystems can alter plant-animal interactions, leading to disproportionate Communicated by Jörg Ganzhorn. eVects on certain plant species. Both the loss of animal seed dispersers, whether from forest fragmentation (Cordeiro S. T. McKinney · C. E. Fiedler and Howe 2003), overhunting (Meehan et al. 2002), or College of Forestry and Conservation, invasive species (McKinney et al. 2009), and the introduc- University of Montana, Missoula, MT 59812, USA tion of animal seed predators (Christian 2001) have induced Present Address: plant declines and shifts in community composition. What S. T. McKinney (&) is not well known is how declines in plant abundance– National Park Service Inventory and Monitoring Program, without corresponding declines in animal abundance–might Sierra Nevada Network, P.O. Box 700-W, V W El Portal, CA 95318, USA a ect plant-animal interactions. Speci cally, if a plant spe- e-mail: [email protected] cies is declining but a seed predator remains intact, will the 123 Oecologia eVects on the plant be exacerbated? The issue becomes mid-summer, however, acting as seed predators and com- especially compelling when the plant in question is a peting with tree squirrels (Hutchins and Lanner 1982). foundation tree species and thus regulates population and Where squirrels outcompete nutcrackers for seeds, the evo- community dynamics, and tempers ecosystem processes lution of cone and seed traits that facilitate nutcracker seed (Ellison et al. 2005). dispersal is constrained (Siepielski and Benkman 2007). North American and Eurasian arboreal squirrels The pine is considered a foundation species of subalpine (Tamiasciurus and Sciurus genera) and members of the forest ecosystems (Ellison et al. 2005) because it: (1) regu- genus Pinus have an evolutionary relationship dating back lates snowmelt and stream Xow (Farnes 1990); (2) moder- to the late Pliocene (ca. 1.7 Ma; Hafner 1984; Axelrod ates local environments, allowing for establishment of 1986). The evolution of tree squirrel adaptations for spe- shade-tolerant conifers (Callaway 1998) and diverse under- cialized feeding on pine seeds, and Pinus cone and seed story communities; and (3) provides an important food morphologies to inhibit seed predation, is well documented source for many birds and mammals, including grizzly (Smith 1970; Elliott 1974; Benkman et al. 1984). Arboreal bears (Ursus arctos) that poach cones from squirrel mid- squirrels can exert signiWcant ecological and evolutionary dens (Mattson et al. 1991). eVects on seeds, tree population dynamics, and forest struc- P. albicaulis is faced with multiple challenges to its ture by directly inXuencing seed fate (Steele et al. 2005). long-term persistence, including the exotic fungal patho- Despite this predation pressure, the distribution of Pinus gen, Cronartium ribicola, which causes white pine blister has generally been increasing in both North America and rust (HoV et al. 1980), mountain pine beetle (Dendroctonus Eurasia (Axelrod 1986; Willis et al. 1998), underscoring ponderosae) upsurges (Logan and Powell 2001), and suc- the ability of pines to adapt to challenges posed by eYcient cessional replacement by shade-tolerant conifers (Arno seed predators. 1980). Fire exclusion has also prevented creation of forest Many coniferous forests are currently facing insect epi- openings favorable both to nutcracker seed-caching and demics, exotic species invasions, and altered disturbance later germination and development of shade-intolerant regimes that negatively and disproportionately aVect Pinus seedlings (Brown et al. 1994; Murray et al. 2000). Declines species. How changes in tree species composition will in P. albicaulis are occurring nearly rangewide, but are aVect interactions between Pinus seed producers and tree most severe in the Northern Rocky Mountains, where tree squirrel seed predators will likely depend on the squirrel’s mortality and blister rust infection levels reach 90% in food choices and habitat preferences. For example, North some stands (Keane et al. 1994; Kendall and Keane 2001). American arboreal squirrels selectively harvest cones from T. hudsonicus is a territorial granivore and central-place tree species with the highest cone energy content (Smith forager (Elliott 1988). Territories are maintained by a single 1968, 1970). Tree species selection based on cone energy adult that cuts conifer cones and stores them in middens content is also documented in Eurasian squirrels, with (Smith 1981). Within Rocky Mountain coniferous forests, selection apparently dependent upon forest composition mean territory sizes (no. ha¡1) reported here and in the (Lurz et al. 1995; Molinari et al. 2006). literature are similar: 0.4–1.5 in Alberta, Canada (Rusch We studied Tamiasciurus hudsonicus [North American and Reeder 1978; Larsen and Boutin 1994); 0.7–1.1 in red squirrel (Erxleben) family Sciuridae] habitat use in Wyoming and Montana, US (Mattson and Reinhart 1997; Rocky Mountain Pinus albicaulis [whitebark pine the present study); and 1.3 in Colorado, US (Gurnell 1984). (Engelmann) family Pinaceae, subgenus Strobus] forests to Squirrels favor habitat conditions that ensure a dependable understand how seed producer and seed predator relation- supply of cones and fungi (mixed conifer forests with high ships are inXuenced by diVerential Pinus mortality. The basal area), allow for adequate cone storage (cool and moist species’ geographical ranges are sympatric in the Rocky forest Xoor), and provide suitable nesting sites, and cover Mountains where both maintain a boreal aYnity. Further- from predators (closed, tall canopies; Rothwell 1979; Steele more, both species are present in late Pleistocene deposits 1998). However, suboptimal habitats that do not possess all (ca. 0.8–0.5 Ma; Kurtén and Anderson 1980; Baker 1990), of these characteristics can be temporarily used during peri- suggesting a prolonged ecological interaction. ods of population growth (Rusch and Reeder 1978). Indi- P. albicaulis occurs in nearly pure stands on the coldest viduals may disperse into suboptimal conditions, cut cones and driest sites where few other tree species can grow, and to eat in situ, and attempt to form a new territory. Strong in mixed-species stands on less severe, lower elevation sites philopatry, increased predation risk with increasing dis- (Arno and HoV 1990). Its seeds are retained in indehiscent persal distance, and lower survival contribute to transient cones (McCaughey and Schmidt 1990) and are dispersed in squirrel occurrence in suboptimal habitats (Larsen and late summer and early fall by Clark’s nutcracker (Nucifraga Boutin 1994). Thus, the relative proportion of active mid- columbiana), a coevolved mutualist with the pine (Tomback dens (indicating residence) versus cones cut and eaten in 1982). Nutcrackers consume unripe seeds in early to situ (indicating transience) can be used as an index of 123 Oecologia
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