Publications in refereed journals:

(* = student, + = post-doc)

Hibernation requires balancing energy and water demands over several months. Many studies have noted the importance of fat for hibernation energy budgets, but protein catabolism in hibernation has received less attention, and whole-animal changes in lean mass have not previously been considered. We used quantitative magnetic resonance body composition analysis to measure deposition of fat and lean mass of cave myotis (Myotis velifer) during the prehibernation period and decreases in fat and leanmass of Townsend’s big-eared bats (Corynorhinus townsendii) during hibernation. For cave myotis, lean mass represented 25% and 38%(female and male, respectively) of prehibernation mass gain. In hibernating Townsend’s big-eared bats, lean mass decrease was similar for females and males.We used values for Townsend’s bigeared bats to explore the functional implications of leanmass change for water and energy budgets. Lean mass accounted for a substantial proportion of mass change during hibernation (female: 18%,male: 35%), and although not accounting for a large proportion of the energy budget (female: 3%,male: 7%), leanmass catabolism represented an important contribution to water production (female:14%, male: 29%). Although most mammals cannot rely on protein catabolism for metabolic water production because of the water cost of excreting urea, we propose a variation of the protein-for-water strategy whereby hibernators could temporally compartmentalize the benefits of protein catabolism to periods of torpor and the water cost to periodic arousals when free drinking water is typically available. Combined, our analyses demonstrate the importance of considering changes in lean mass during hibernation.

Climate change and disease are threats to biodiversity that may compound and interact with one another in ways that are difficult to predict. White-nose syndrome (WNS), caused by a cold-loving fungus (Pseudogymnoascus destructans), has had devastating impacts on North American hibernating bats, and impact severity has been linked to hibernaculum microclimate conditions. As WNS spreads across the continent and climate conditions change, anticipating these stressors’ combined impacts may improve conservation outcomes for bats. We build on the recent development of winter species distribution models for five North American bat species, which used a hybrid correlative-mechanistic approach to integrate spatially explicit winter survivorship estimates from a bioenergetic model of hibernation physiology. We apply this bioenergetic model given the presence of P. destructans, including parameters capturing its climate-dependent growth as well as its climate-dependent effects on host physiology, under both current climate conditions and scenarios of future climate change. We then update species distribution models with the resulting survivorship estimates to predict changes in winter hibernacula suitability under future conditions. Exposure to P. destructans is generally projected to decrease bats’ winter occurrence probability, but in many areas, changes in climate are projected to lessen the detrimental impacts of WNS. This rescue effect is not predicted for all species or geographies and may arrive too late to benefit many hibernacula. However, our findings offer hope that proactive conservation strategies to minimize other sources of mortality could allow bat populations exposed to P. destructans to persist long enough for conditions to improve.

In multihost disease systems, differences in mortality between species may reflect variation in host physiology, morphology, and behavior. In systems where the pathogen can persist in the environment, microclimate conditions, and the adaptation of the host to these conditions, may also impact mortality. White‐nose syndrome (WNS) is an emerging disease of hibernating bats caused by an environmentally persistent fungus, Pseudogymnoascus destructans. We assessed the effects of body mass, torpid metabolic rate, evaporative water loss, and hibernaculum temperature and water vapor deficit on predicted overwinter survival of bats infected by P. destructans. We used a hibernation energetics model in an individual‐based model framework to predict the probability of survival of nine bat species at eight sampling sites across North America. The model predicts time until fat exhaustion as a function of species‐specific host characteristics, hibernaculum microclimate, and fungal growth. We found host body mass and hibernaculum water vapor deficit explained over half of the variation in survival with WNS across species. As previous work on the interplay between host and pathogen physiology and the environment has focused on species with narrow microclimate preferences, our view on this relationship is limited. Our results highlight some key predictors of interspecific survival among western bat species and provide a framework to assess impacts of WNS as the fungus continues to spread into western North America.

Hibernation consists of extended durations of torpor interrupted by periodic arousals. The ‘dehydration hypothesis’ proposes that hibernating mammals arouse to replenish water lost through evaporation during torpor. Arousals are energetically expensive, and increased arousal frequency can alter survival throughout hibernation. Yet we lack a means to assess the effect of evaporative water loss (EWL), determined by animal physiology and hibernation microclimate, on torpor bout duration and subsequent survival. White-nose syndrome (WNS), a devastating disease impacting hibernating bats, causes increased frequency of arousals during hibernation and EWL has been hypothesized to contribute to this increased arousal frequency. WNS is caused by a fungus, which grows well in humid hibernaculum environments and damages wing tissue important for water conservation. Here, we integrated the effect of EWL on torpor expression in a hibernation energetics model, including the effects of fungal infection, to determine the link between EWL and survival. We collected field data for Myotis lucifugus, a species that experiences high mortality from WNS, to gather parameters for the model. In saturating conditions, we predicted healthy bats experience minimal mortality. Infected bats, however, suffer high fungal growth in highly saturated environments, leading to exhaustion of fat stores before spring. Our results suggest that host adaptation to humid environments leads to increased arousal frequency from infection, which drives mortality across hibernaculum conditions. Our modified hibernation model provides a tool to assess the interplay between host physiology, hibernaculum microclimate, and diseases such as WNS on winter survival.

The importance of cave microclimate is particularly relevant at temperate latitudes where bats make seasonal use of caves for hibernation. A recent review synthesized current understanding of cave climatology, exploring the qualitative relationship between cave and surface climate with implications for hibernaculum suitability. However, a more quantitative understanding of the conditions in which bats hibernate and how they may promote or mediate WNS impacts is required. We compiled subterranean temperatures from caves and mines across the western United States and Canada to (1) quantify the hypothesized relationship between mean annual surface temperature (MAST) and subterranean temperaturand how it is influenced by measurable site attributes, and (2) use readily available gridded data to predict and continuously map the range of temperatures that may be available in caves and mines. We suggest that our model predictions should serve as hypotheses to be further tested and refined as additional data become available.

Species with broad geographic ranges may experience varied environmental conditions throughout their range leading to local adaptation. Variation among populations reflects potential adaptability or plasticity, with implications for populations impacted by disease, climate change, and other anthropogenic influences. However, behavior may counteract divergent selection among populations. We studied intraspecific variation in hibernation physiology of Myotis lucifugus (little brown myotis) and Corynorhinus townsendii (Townsend’s big-eared bat), two species of bats with large geographic ranges. We studied M. lucifugus at three hibernacula which spanned a latitudinal gradient of 1500 km, and C. townsendii from 6 hibernacula spread across 1200 km latitude and 1200 km longitude. We found no difference in torpid metabolic rate among populations of either species, nor was there a difference in the effect of ambient temperature among sites. Evaporative water loss was similar among populations of both species, with the exception of one C. townsendii pairwise site difference and one M. lucifugus site that differed from the others. We suggest the general lack of geographic variation is a consequence of behavioral microhabitat selection. As volant animals, bats can travel relatively long distances in search of preferred microclimates for hibernation. Despite dramatic macroclimate differences among populations, hibernating bats are able to find preferred microclimate conditions within their range, resulting in similar selection pressures among populations spread across wide geographic ranges.

The fungal pathogen Pseudogymnoascus destructans and resultant white-nose syndrome (WNS) continues to advance across North America, infecting new bat hibernacula. Western North America hosts the highest bat diversity in the United States and Canada, yet little is known about hibernacula and hibernation behaviour in this region. An improved understanding of the distribution of suitable hibernacula is critical for land managers to anticipate conservation needs of WNS-susceptible species in currently uninfected regions. We estimated suitability of potential winter hibernaculum sites across five bat species' ranges. We estimated winter survival capacity from a mechanistic survivorship model based on bat bioenergetics and climate conditions. We then used boosted regression trees to relate these estimates, along with key landscape attributes, to bat occurrence data in a hybrid correlative-mechanistic approach. Winter survival capacity, topography, land cover and access to subterranean features were important predictors of winter hibernaculum selection, but the shape and relative importance of these relationships varied amongst species. This suggests that the occurrence of bat hibernacula can, in part, be predicted from readily mapped above-ground features, not just below-ground characteristics for which spatial data are lacking. Furthermore, our mechanistic estimate of winter survivorship was, on average, the third strongest predictor of winter occurrence probability across focal species. Winter distributions of North American bat species were driven by their physiological capacity to survive winter conditions and duration in a given location, as well as selection for topographic and other landscape features but in species-specific ways. The influence of winter survivorship on several species' distributions, the underlying influence of climate conditions on winter survivorship and the anticipated influence of WNS on bats' hibernation physiology and survivorship together suggest that North American bat distributions may undergo future shifts as these species are exposed not only to WNS but also to climate change.

Hibernation consists of alternating phases of extended periods of torpor (low body temperature, low metabolic rate), and energetically costly periodic arousals to normal body temperature. Arousals consist of multiple phases: warming, euthermia, and cooling. Although cooling to torpid body temperature is an important phase of the torpor-arousal cycle, it is often overlooked in energetic models. When included, cooling cost is assumed to be 67% of warming cost, an assumption originally derived from a single study that measured cooling cost in ground squirrels. We derived a model of cooling cost from first principles and validated the model with empirical energetic measurements. We compared the assumed 67% proportional cooling cost with our model-predicted cooling cost for 53 hibernating mammals. Our results indicate that using 67% of warming cost only adequately represents cooling cost in ground squirrel-sized mammals. Our model allows for the generalization of energetic costs for multiple species using species-specific physiological and morphometric parameters, and for predictions over variable environmental conditions.

White-nose syndrome (WNS) has decimated hibernating bat populations across eastern and central North America for over a decade. Disease severity is driven by the interaction between bat characteristics, the cold-loving fungal agent, and the hibernation environment. While we further improve hibernation energetics models, we have yet to examine how spatial heterogeneity in host traits is linked to survival in this disease system. Here, we develop predictive spatial models of body mass for the little brown myotis (Myotis lucifugus) and reassess previous definitions of the duration of hibernation of this species. Using data from published literature, public databases, local experts, and our own fieldwork, we fit a series of generalized linear models with hypothesized abiotic drivers to create distribution-wide predictions of prehibernation body fat and hibernation duration. Our results provide improved estimations of hibernation duration and identify a scaling relationship between body mass and body fat; this relationship allows for the first continuous estimates of prehibernation body mass and fat across the species' distribution. We used these results to inform a hibernation energetic model to create spatially varying fat use estimates for M. lucifugus. These results predict WNS mortality of M. lucifugus populations in western North America may be comparable to the substantial die-off observed in eastern and central populations.

Hibernation is widespread among mammals in a variety of environmental contexts. However, few experimental studies consider interspecific comparisons, which may provide insight into general patterns of hibernation strategies. We studied 13 species of free-living bats, including populations spread over thousands of kilometers and diverse habitats. We measured torpid metabolic rate (TMR) and evaporative water loss (two key parameters for understanding hibernation energetics) across a range of temperatures. There was no difference in minimum TMR among species (i.e., all species achieved similarly low torpid metabolic rate) but the temperature associated with minimum TMR varied among species. The minimum defended temperature (temperature below which TMR increased) varied from 8 °C to < 2 °C among species. Conversely, evaporative water loss varied among species, with species clustered in two groups representing high and low evaporative water loss. Notably, species that have suffered population declines due to white-nose syndrome fall in the high evaporative water loss group and less affected species in the low evaporative water loss group. Documenting general patterns of physiological diversity, and associated ecological implications, contributes to broader understanding of biodiversity, and may help predict which species are at greater risk of environmental and anthropogenic stressors.

We describe the first reported case of diphallia in a Corynorhinus townsendii captured during fall swarming at a hibernaculum in northern Utah, USA. Upon examination, we determined that one phallus was functional, as evidenced by production of urine, while the secondary phallus appeared to be overgrown with skin. A review of the medical literature relevant to diphallia suggests that this is a case of pseudodiphallia with a bifid shaft. We hypothesize that this morphological deformity likely has a low impact on the survival of this individual but may act as a physical barrier to copulation. To our knowledge, this is the first reported case of diphallia in bats.

Non-peer reviewed publications: