COULD WHITE-NOSE SYNDROME MANIFEST DIFFERENTLY IN MYOTIS LUCIFUGUS IN WESTERN VERSUS EASTERN REGIONS OF NORTH AMERICA? A REVIEW OF FACTORS.

White-nose syndrome (WNS) has notably affected the abundance of Myotis lucifugus (little brown myotis) in North America. Thus far, substantial mortality has been restricted to the eastern part of the continent where the cause of WNS, the invasive fungus Pseudogymnoascus destructans, has infected bats since 2006. To date, the state of Washington is the only area in the Western US or Canada (the Rocky Mountains and further west in North America) with confirmed cases of WNS in bats, and there the disease has spread more slowly than it did in Eastern North America. Here, we review differences between M. lucifugus in western and eastern parts of the continent that may affect transmission, spread, and severity of WNS in the West and highlight important gaps in knowledge. We explore the hypothesis that western M. lucifugus may respond differently to WNS on the basis of different hibernation strategies, habitat use, and greater genetic structure. To document the effect of WNS on M. lucifugus in the West most effectively, we recommend focusing on maternity roosts for strategic disease surveillance and monitoring abundance. We further recommend continuing the challenging work of identifying hibernation and swarming sites to better understand the microclimates, microbial communities, and role in disease transmission of these sites, as well as the ecology and hibernation physiology of bats in noncavernous hibernacula.

Once upon a time in Mexico: Holocene biogeography of the spotted bat (Euderma maculatum).

Holocene-era range expansions are relevant to understanding how a species might respond to the warming and drying climates of today. The harsh conditions of North American deserts have phylogenetically structured desert bat communities but differences in flight capabilities are expected to affect their ability to compete, locate, and use habitat in the face of modern climate change. A highly vagile but data-deficient bat species, the spotted bat (Euderma maculatum), is thought to have expanded its range from central Mexico to western Canada during the Holocene. With specimens spanning this latitudinal extent, we examined historical demography, and used ecological niche modeling (ENM) and phylogeography (mitochondrial DNA), to investigate historic biogeography from the rear to leading edges of the species' range. The ENM supported the notion that Mexico was largely the Pleistocene-era range, whereas haplotype pattern and Skyline plots indicated that populations expanded from the southwestern US throughout the Holocene. This era provided substantial gains in suitable climate space and likely facilitated access to roosting habitat throughout the US Intermountain West. Incongruent phylogenies among different methods prevented a precise understanding of colonization history. However, isolation at the southern-most margin of the range suggests a population was left behind in Mexico as climate space contracted and are currently of unknown status. The species appears historically suited to follow shifts in climate space but differences in flight behaviors between leading edge and core-range haplogroups suggest range expansions could be influenced by differences in habitat quality or climate (e.g., drought). Although its vagility could facilitate response to environmental change and thereby avoid extinction, anthropogenic pressures at the core range could still threaten the ability for beneficial alleles to expand into the leading edge.

Microbial isolates with Anti-Pseudogymnoascus destructans activities from Western Canadian bat wings.

Pseudogymnoascus destructans (Pd) is the causative agent of white-nose syndrome, which has resulted in the death of millions of bats in North America (NA) since 2006. Based on mortalities in eastern NA, the westward spread of infections likely poses a significant threat to western NA bats. To help prevent/reduce Pd infections in bats in western NA, we isolated bacteria from the wings of wild bats and screened for inhibitory activity against Pd. In total, we obtained 1,362 bacterial isolates from 265 wild bats of 13 species in western Canada. Among the 1,362 isolates, 96 showed inhibitory activity against Pd based on a coculture assay. The inhibitory activities varied widely among these isolates, ranging from slowing fungal growth to complete inhibition. Interestingly, host bats containing isolates with anti-Pd activities were widely distributed, with no apparent geographic or species-specific pattern. However, characteristics of roosting sites and host demography showed significant associations with the isolation of anti-Pd bacteria. Specifically, anthropogenic roosts and swabs from young males had higher frequencies of anti-Pd bacteria than those from natural roosts and those from other sex and age-groups, respectively. These anti-Pd bacteria could be potentially used to help mitigate the impact of WNS. Field trials using these as well as additional microbes from future screenings are needed in order to determine their effectiveness for the prevention and treatment against WNS.

Similar hibernation physiology in bats across broad geographic ranges.

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.

Interspecific variation in evaporative water loss and temperature response, but not metabolic rate, among hibernating bats.

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.

What is winter? Modeling spatial variation in bat host traits and hibernation and their implications for overwintering energetics.

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.

Body mass and hibernation microclimate may predict bat susceptibility to white-nose syndrome.

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 fit a linear model to determine relationships with each variable and predicted survival and semipartial correlation coefficients to determine the major drivers in variation in bat survival. 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.

NABat: A top-down, bottom-up solution to collaborative continental-scale monitoring.

Collaborative monitoring over broad scales and levels of ecological organization can inform conservation efforts necessary to address the contemporary biodiversity crisis. An important challenge to collaborative monitoring is motivating local engagement with enough buy-in from stakeholders while providing adequate top-down direction for scientific rigor, quality control, and coordination. Collaborative monitoring must reconcile this inherent tension between top-down control and bottom-up engagement. Highly mobile and cryptic taxa, such as bats, present a particularly acute challenge. Given their scale of movement, complex life histories, and rapidly expanding threats, understanding population trends of bats requires coordinated broad-scale collaborative monitoring. The North American Bat Monitoring Program (NABat) reconciles top-down, bottom-up tension with a hierarchical master sample survey design, integrated data analysis, dynamic data curation, regional monitoring hubs, and knowledge delivery through web-based infrastructure. NABat supports collaborative monitoring across spatial and organizational scales and the full annual lifecycle of bats.