The genetic signature of rapid range expansion by flying squirrels in response to contemporary climate warming

Climate is an important factor limiting species distributions. Historic climate‐change related range movements have modified the genetic diversity of species by the merging and splitting of gene pools and by the effects associated with recurrent founder events. These effects are often inferred, either from retrospective analyses of current genetic patterns or from simulations. Rarely has it been possible for the population genetic effects of range expansion to be examined with contemporaneous demographic data. We characterized the genetic signature of rapid range expansion by southern flying squirrels (Glaucomys volans) and compared these results to a stationary population of the closely related northern flying squirrel (Glaucomys sabrinus) in Ontario, Canada. Samples were taken during an approximately 200 km range expansion by G. volans (1994–2003) and genotyped at 6 (G. sabrinus) and 8 (G. volans) microsatellite loci. For G. volans, but not G. sabrinus, we found evidence of a latitudinal gradient in allele frequencies and a decrease in allelic richness along the axis of expansion. We found no evidence of isolation‐by‐distance in either species or of genetic bottlenecks in the area of G. volans expansion. These results suggest that serial founder events can cause an immediate reduction in genetic diversity following rapid range expansion with high levels of gene flow giving rise to heterogeneity within what would classically be termed panmixia. Given the pace of anthropogenic climate change, and the increasing incidence of range movements in response, this may be an important, immediate consequence of climate change.     

Density, aggregation, and body size of northern pikeminnow preying on juvenile salmonids in a large river

Predation by northern pikeminnow Ptychocheilus oregonensis on juvenile salmonids Oncorhynchus spp. occurred probably during brief feeding bouts since diets were either dominated by salmonids (>80% by weight), or contained other prey types and few salmonids (<5%). In samples where salmonids had been consumed, large rather than small predators were more likely to have captured salmonids. Transects with higher catch-per-unit of effort of predators also had higher incidences of salmonids in predator guts. Predators in two of three reservoir areas were distributed more contagiously if they had preyed recently on salmonids. Spatial and temporal patchiness of salmonid prey may be generating differences in local density, aggregation, and body size of their predators in this large river.     

Characterization of microsatellite DNA loci for the southern flying squirrel (Glaucomys volans)

Polymerase chain reaction primers for microsatellite DNA loci (one dinucleotide, four tetranucleotide and two compound) and the conditions necessary to amplify each are described for the southern flying squirrel (Glaucomys volans). These primers were tested on 22 or more individuals from a population at the Savannah River Site in South Carolina. These microsatellite primers yielded a high allelic diversity (6–22 alleles/locus), and moderate to high observed heterozygosities (0.318–0.826). Primers developed for the northern flying squirrel (Glaucomys sabrinus) were also tested for use on G. volans, with only two successful cross amplifications from the seven loci.     

A meta-analysis of forest age and structure effects on northern flying squirrel densities

Research on the impact of clearcut logging and partial harvesting practices on northern flying squirrels (Glaucomys sabrinus) has shown inconsistent and contrary results, limiting the use of this species as a management indicator species. Much of this variability in study results is due to the labor intensive nature of studying flying squirrels, resulting in small sampling sizes (average = 5.2 sites, n = 14) and high variation (CV = 0.59) across studies. We conducted a meta-analysis of relevant studies from North America to determine how forestry practices affect flying squirrel abundance. Mean effect size was −1.18 (P < 0.001; n = 14) for all studies, indicating a strong difference between control stands and those regenerating postclearcut or following partial harvesting. Our results support the association of northern flying squirrels with mature, uncut forest and their suitability as ecological indicators of these vegetation types. © 2011 The Wildlife Society.     

Effects of Logging Pattern and Intensity on Squirrel Demography

ABSTRACT We examined the effect of harvesting intensity and pattern on red squirrels (Tamiasciurus hudsonicus), northern flying squirrels (Glaucomys sabrinus), and yellow-pine chipmunks (Tamias amoenus) in mature inland Douglas-fir (Pseudotsuga menziesii glauca) forests in south-central British Columbia, Canada. We sampled squirrels 1 year before harvesting through 4 years after harvesting and estimated population parameters using open-population models. Relative to unharvested stands, each of the 3 species showed a strong response to tree removal. From 2 years to 4 years after logging, red squirrel density was 40% (SE = 7.1) lower in stands with 50% basal-area tree removal. From 1 year and up to 4 years after logging, northern flying squirrel density averaged 60% (SE = 5.2) lower in harvested treatments regardless of intensity or pattern of logging. In contrast, density of yellow-pine chipmunks increased markedly with increased logging intensity. Beginning 3 years after logging, yellow-pine chipmunk density was 734% (SE = 269) greater in stands with 50% basal-area tree removal. In the short term, harvesting intensity was a more important determinant of squirrel density than harvesting pattern. Retaining >10 m² per ha of live residual stand structure in mature inland Douglas-fir forests maintained habitat for forest-dependent species such as red squirrels and northern flying squirrels, albeit at lower densities.     

Thermal Properties of Tree Cavities During Winter in a Northern Hardwood Forest

ABSTRACT Tree cavities likely vary in their thermal quality for cavity-nesting animals, which could be especially important during winter. We conducted a winter field experiment to test whether cavities vary either in their buffering capacity or in their mean temperature according to predictable characteristics. We found that cavities buffered temperature and that there was a lag effect in temperature that appeared to be related to heating and cooling. Diameter at breast height was the most important variable influencing cavity temperature during the day, with smaller trees warming up more. During the night, diameter at breast height and tree decay class were important, such that larger, live trees cooled down less. Maintaining live trees with cavities in managed forests should be considered in addition to snag retention, because live trees appear to provide warmer structures during winter.     

A test of non‐kin social foraging in the southern flying squirrel (Glaucomys volans)

It can be challenging to understand the evolution of sociality, particularly the occurrence of co‐operation by non‐kin. Southern flying squirrels (Glaucomys volans) are an interesting example of non‐kin co‐operation because of the mutual benefits obtained by social thermoregulation during winter. Because group survival confers benefits to the entire group, flying squirrels may also follow an aggregation economy, whereby co‐operative foraging during winter is advantageous. However, the extent of such social foraging in flying squirrels is unknown. We tested for social foraging of southern flying squirrels, and also for relatedness among foraging groups. To determine the structure of foraging groups, we set up and remotely monitored feeding stations and nest cavities. All squirrels at the study site were tagged with passive integrated transponder (PIT) tags and nests and feeding stations were monitored with automated PIT‐tag recorders for a 24‐month period. Squirrels were found most often foraging alone. Squirrels that were recorded foraging together comprised unrelated individuals that were also found to share nest cavities. Squirrels were also recorded travelling farther distances between nest cavity and feeding station in the winter season than in the summer season, suggesting that, during winter, squirrels trade‐off proximity to food caches for membership in a nest group. Our data suggest that squirrels forage and cache alone in their summer home range and make solitary returns to this summer range to collect their cache during the winter months, despite exhibiting social winter nesting. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1126–1135.     

Using dynamic N‐mixture models to test cavity limitation on northern flying squirrel demographic parameters using experimental nest box supplementation

Dynamic N‐mixture models have been recently developed to estimate demographic parameters of unmarked individuals while accounting for imperfect detection. We propose an application of the Dail and Madsen ( 2011 : Biometrics, 67 , 577–587) dynamic N‐mixture model in a manipulative experiment using a before‐after control‐impact design (BACI). Specifically, we tested the hypothesis of cavity limitation of a cavity specialist species, the northern flying squirrel, using nest box supplementation on half of 56 trapping sites. Our main purpose was to evaluate the impact of an increase in cavity availability on flying squirrel population dynamics in deciduous stands in northwestern Québec with the dynamic N‐mixture model. We compared abundance estimates from this recent approach with those from classic capture–mark–recapture models and generalized linear models. We compared apparent survival estimates with those from Cormack–Jolly–Seber (CJS) models. Average recruitment rate was 6 individuals per site after 4 years. Nevertheless, we found no effect of cavity supplementation on apparent survival and recruitment rates of flying squirrels. Contrary to our expectations, initial abundance was not affected by conifer basal area (food availability) and was negatively affected by snag basal area (cavity availability). Northern flying squirrel population dynamics are not influenced by cavity availability at our deciduous sites. Consequently, we suggest that this species should not be considered an indicator of old forest attributes in our study area, especially in view of apparent wide population fluctuations across years. Abundance estimates from N‐mixture models were similar to those from capture–mark–recapture models, although the latter had greater precision. Generalized linear mixed models produced lower abundance estimates, but revealed the same relationship between abundance and snag basal area. Apparent survival estimates from N‐mixture models were higher and less precise than those from CJS models. However, N‐mixture models can be particularly useful to evaluate management effects on animal populations, especially for species that are difficult to detect in situations where individuals cannot be uniquely identified. They also allow investigating the effects of covariates at the site level, when low recapture rates would require restricting classic CMR analyses to a subset of sites with the most captures.     

Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs

Claw morphology, and claw-closing forces of four species of intertidal crabs from San Juan Island, Washington were compared and related these findings were related to prey size selection, shell breaking times and total handling times on their snail prey, Littorina sitkana Philippi. Two functional groups of crabs emerged: generalists and specialists on hard-shelled prey. The generalist, Hemigrapsus nudus (Dana), has an omnivorous diet and possesses weak claws with small, fine denticles and mechanical advantage (MA) of the claw's lever system <0.3, while the specialists, Lophopanopeus bellus (Stimpson), Cancer oregonensis (Dana) and C. productus (Randall), consume hard-shelled prey and possess large, powerful claws with broad, blunt molars and MA>0.3. The claws of the generalist, H. nudus, exhibited weaker claw closing forces (5 N) than those of similar sized specialists (>12 N). When crabs of similar weight were offered four size categories of Littorina sitkana, the generalist, Hemigrapsus nudus, exhibited a consistent preference for the smallest size categories, while the three specialists attacked all size classes offered. Hemigrapsus nudus took significantly longer (134 s) than the specialists (30–52 s) to break open a 4 mm L. sitkana. This difference in shell-breaking time between the generalist and the specialists increased with increasing prey size. The rate of successful attacks on increasingly larger L. sitkana decreased with prey size in the generalist (70% on 4 mm, 37% on 6 mm, and 0% on 8 mm snails), but remained high in the specialists (70–100%). Strength limitation of the claws is the best hypothesis to explain the avoidance of large snails by the generalist, H. nudus.