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The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to wildlife. Here, we review the diversity and natural host range of β-CoVs in bats and examine the risk of humans inadvertently infecting free-ranging bats with SARS-CoV-2. Our review of the global distribution and host range of β-CoV evolutionary lineages suggests that 40+ species of temperate-zone North American bats could be immunologically naïve and susceptible to infection by SARS-CoV-2. We highlight an urgent need to proactively connect the wellbeing of human and wildlife health during the current pandemic and to implement new tools to continue wildlife research while avoiding potentially severe health and conservation impacts of SARS-CoV-2 "spilling back" into free-ranging bat populations.

Bat fatalities at wind energy facilities in North America are predominantly comprised of migratory, tree‐dependent species, but it is unclear why these bats are at higher risk. Factors influencing bat susceptibility to wind turbines might be revealed by temporal patterns in their behaviors around these dynamic landscape structures. In northern temperate zones, fatalities occur mostly from July through October, but whether this reflects seasonally variable behaviors, passage of migrants, or some combination of factors remains unknown. In this study, we examined video imagery spanning one year in the state of Colorado in the United States, to characterize patterns of seasonal and nightly variability in bat behavior at a wind turbine. We detected bats on 177 of 306 nights representing approximately 3,800 hr of video and > 2,000 discrete bat events. We observed bats approaching the turbine throughout the night across all months during which bats were observed. Two distinct seasonal peaks of bat activity occurred in July and September, representing 30% and 42% increases in discrete bat events from the preceding months June and August, respectively. Bats exhibited behaviors around the turbine that increased in both diversity and duration in July and September. The peaks in bat events were reflected in chasing and turbine approach behaviors. Many of the bat events involved multiple approaches to the turbine, including when bats were displaced through the air by moving blades. The seasonal and nightly patterns we observed were consistent with the possibility that wind turbines invoke investigative behaviors in bats in late summer and autumn coincident with migration and that bats may return and fly close to wind turbines even after experiencing potentially disruptive stimuli like moving blades. Our results point to the need for a deeper understanding of the seasonality, drivers, and characteristics of bat movement across spatial scales., Bat behavior driving fatalities at wind turbines remains poorly understood. Our analysis of one year of video imagery at a wind turbine in Colorado revealed seasonal peaks of bat activity that included increases in diversity and duration of behaviors that may exacerbate risk of fatality. Our results point to the need for a deeper understanding of the seasonality, drivers, and characteristics of bat movement across spatial scales.

The novel beta-coronavirus, SARS-CoV-2, may pose a threat to North American bat populations if bats are exposed to the virus through interaction with humans, if the virus can subsequently infect bats and be transmitted among them, and if the virus causes morbidity or mortality in bats Further, if SARS-CoV-2 became established in bat populations, it could possibly serve as a source for new infection in humans, domesticated animals, or other wild animals Wildlife management agencies in the United States are concerned about these potential risks and have begun to issue guidance regarding work that brings humans into contact with bats, but decision making is difficult because of the high degree of uncertainty about many of the relevant processes that could lead to virus transmission and establishment The risk assessment described in this report was undertaken to provide management agencies with an understanding of the likelihood that the various steps in the causal pathways would lead to SARS-CoV-2 infection of North American bats from people This assessment focused on the active season for bats in the temperate zone of North America (April 15 through November 15), and used Myotis lucifugus (little brown bats) as a surrogate species At the time of this work (April 2020), no empirical data about the effects of SARS-CoV-2 on North American bats were available, so a formal process of expert judgment was used to elicit estimates of the underlying parameters Twelve experts in bat ecology, epidemiology, virology, and wildlife disease from the United States, United Kingdom, and Australia participated in the elicitation A Monte Carlo simulation model was used to integrate the parameter estimates elicited from the experts and to predict the likelihood of exposure and infection in bats through a series of transmission pathways, with particular attention to capturing uncertainty in the predictions Given the current state of knowledge as expressed by the expert panel, the results of this assessment indicate that there is a non-negligible risk of transmission of SARS-CoV-2 from humans to bats For example, if a research scientist were shedding SARS-CoV-2 virus while handling bats under the field protocols used in North America prior to the COVID-19 pandemic, the risk model indicates that 50 percent (uncertainty, 15-84 percent) of those bats could be exposed to virus, and 17 percent (uncertainty, 3-51 percent) could become infected Use of personal protective equipment, especially a respirator, is expected to reduce the exposure risk The expert panel estimated that exposure risk from research scientists could be reduced 94-96 percent (uncertainty, 86-99 percent) through proper use of appropriate N95 respirators (a type of mechanical filter worn over the nose and mouth), dedicated clothing (such as Tyvek coveralls), and gloves Should any North American bats become infected with SARS-CoV-2, the expert panel estimated that there is an approximately 33-percent chance the virus could spread within a bat population This study, conducted by the U S Geological Survey in cooperation with the U S Fish and Wildlife Service, identified several critical uncertainties that could affect the estimate of risks associated with SARS-CoV-2 entering bat populations- notably, the underlying probability that a human would be shedding virus while working with bats, the likelihood of the virus replicating in bat tissue, and the likelihood of transmission of the virus within bat populations Ongoing empirical work during May-October 2020 may shed light on these issues Follow-up work is needed to better understand the probability of transmission of SARS-CoV-2 to bats from the general public;the manner in which the probabilities of exposure, infection, and transmission would differ during hibernation compared to the breeding season;and the likelihood of important effects, like morbidity and mortality in bats, the possibility of zoonosis from a North American bat reservoir, and effects of and on other wildlife

Animals often migrate to exploit seasonally ephemeral food. Three species of nectar-feeding phyllostomid bats migrate north from Mexico into deserts of the United States each spring and summer to feed on blooms of columnar cactus and century plants (Agave spp.). However, the habitat needs of these important desert pollinators are poorly understood. We followed the nighttime movements of 2 species of long-nosed bats (Leptonycteris yerbabuenae and L. nivalis) in an area of late-summer sympatry at the northern edges of their migratory ranges. We radio-tracked bats in extreme southwestern New Mexico during 22 nights over 2 summers and acquired location estimates for 31 individuals. Both species cohabitated 2 major day roosts that were 30 km apart and in different mountain ranges, and individual bats sometimes moved between the roosts. Sampling was opportunistic and limited, but there were no obvious qualitative differences in observed patterns of movement between species or years, or among sex, age, and reproductive groups. Both species were observed foraging most often in the mountain range that had a relatively higher observed density of presumed food plants (Agave palmeri); when roosting in an adjacent mountain range, bats sometimes commuted >20 km one way to forage. Contrary to evidence indicating these species partition resources farther south in Mexico, our findings suggest that L. yerbabuenae and L. nivalis seasonally share common roost and food resources during late summer in this northern area of sympatry.

Despite conservation concerns for many species of bats, factors causing mortality in bats have not been reviewed since 1970. Here, we review and qualitatively describe trends in the occurrence and apparent causes of multiple mortality events (MMEs) in bats around the world. We compiled a database of MMEs, defined as cases in which ≥ 10 dead bats were counted or estimated at a specific location within a maximum timescale of a year, and more typically within a few days or a season. We tabulated 1180 MMEs within nine categories. Prior to 2000, intentional killing by humans caused the greatest proportion of MMEs in bats. In North America and Europe, people typically killed bats because they were perceived as nuisances. Intentional killing occurred in South America for vampire bat control, in Asia and Australia for fruit depredation control, and in Africa and Asia for human food. Biotic factors, accidents, and natural abiotic factors were also important historically. Chemical contaminants were confirmed causes of MMEs in North America, Europe, and in islands. Viral and bacterial diseases ranked low as causes of MMEs in bats. Two factors led to a major shift in causes of MMEs in bats at around 2000: the global increase of industrial wind-power facilities and the outbreak of white-nose syndrome in North America. Collisions with wind turbines and white-nose syndrome are now the leading causes of reported MMEs in bats. Collectively, over half of all reported MMEs were of anthropogenic origin. The documented occurrence of MMEs in bats due to abiotic factors such as intense storms, flooding, heat waves, and drought is likely to increase in the future with climate change. Coupled with the chronic threats of roosting and foraging habitat loss, increasing mortality through MMEs is unlikely to be compensated for, given the need for high survival in the dynamics of bat populations.

Bat specimens held in natural history museum collections can provide insights into the distribution of species. However, there are several important sources of spatial error associated with natural history specimens that may influence the analysis and mapping of bat species distributions. We analyzed the importance of geographic referencing and error correction in species distribution modeling (SDM) using occurrence records of hoary bats (Lasiurus cinereus). This species is known to migrate long distances and is a species of increasing concern due to fatalities documented at wind energy facilities in North America. We used 3,215 museum occurrence records collected from 1950–2000 for hoary bats in North America. We compared SDM performance using five approaches: generalized linear models, multivariate adaptive regression splines, boosted regression trees, random forest, and maximum entropy models. We evaluated results using three SDM performance metrics (AUC, sensitivity, and specificity) and two data sets...

Conservation planning can be challenging due to the need to balance biological concerns about population viability with social concerns about the benefits biodiversity provide to society, often while operating under a limited budget. Methods and tools that help prioritize conservation actions are critical for the management of at-risk species. Here, we use a multi-attribute utility function to assess the optimal maternity roosts to conserve for maintaining the population viability and the ecosystem services of a single species, the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Mexican free-tailed bats provide ecosystem services such as insect pest-suppression in agricultural areas and recreational viewing opportunities, and may be threatened by climate change and development of wind energy. We evaluated each roost based on five attributes: the maternity roost’s contribution to population viability, the pest suppression ecosystem services to the surrounding area provided by the bats residing in the roost, the ecotourism value of the roost, the risks posed to each roost structure, and the risks posed to the population of bats residing in each roost. We compared several scenarios that prioritized these attributes differently, hypothesizing that the set of roosts with the highest rankings would vary according to the conservation scenario. Our results indicate that placing higher values on different roost attributes (e.g. population importance over ecosystem service value) altered the roost rankings. We determined that the values placed on various conservation objectives are an important determinant of habitat planning.

All 16 species of bats known to occur in western Colorado are found at Mesa Verde National Park (MVNP) in the southwestern United States. Since 1996, wildfires have burned more than 70% of MVNP (>15,000 ha), potentially altering food and roosting resources for bats. During the summers of 2006–2007, we investigated roost use by reproductive female western long-eared myotis (Myotis evotis). We located 33 bat roosts in rock crevices and 1 in a juniper snag. All but 2 of the roosts were in unburned habitat. Bats roosted alone or in small groups (≤3 individuals) and switched roosts frequently (1–7 roosts per bat, median = 1.5 roosts per bat, SE = 0.5 roosts per bat). We compared occupied roosts with randomly selected unoccupied crevices and used an information theoretic approach to determine which variables were most important in determining roost use at microhabitat and landscape scales. At the microhabitat scale, maternity roosts were higher above the ground and deeper than random, unoccupied rock c...

Modeling environment and individual bat and fungal traits predicts continental-scale differences in white-nose syndrome., White-nose syndrome is a fungal disease killing bats in eastern North America, but disease is not seen in European bats and is less severe in some North American species. We show that how bats use energy during hibernation and fungal growth rates under different environmental conditions can explain how some bats are able to survive winter with infection and others are not. Our study shows how simple but nonlinear interactions between fungal growth and bat energetics result in decreased survival times at more humid hibernation sites; however, differences between species such as body size and metabolic rates determine the impact of fungal infection on bat survival, allowing European bat species to survive, whereas North American species can experience dramatic decline.

We determined the bat fauna at Mesa Verde National Park (Mesa Verde) in 2006 and 2007, characterized bat elevational distribution and reproduction, and investigated roosting habits of selected species. We captured 1996 bats of 15 species in mist nets set over water during 120 nights of sampling and recorded echolocation calls of an additional species. The bat fauna at Mesa Verde included every species of bat known west of the Great Plains in Colorado, except the little brown bat (Myotis lucifugus). Some species showed skewed sex ratios, primarily due to a preponderance of males. Thirteen species of bats reproduced at Mesa Verde. Major differences in spring precipitation between the 2 years of our study were associated with differences in reproductive rates and, in some species, with numbers of juveniles captured. Reduced reproductive effort during spring drought will have a greater impact on bat populations with the forecasted increase in aridity in much of western North America by models of glo...

Thousands of industrial-scale wind turbines are being built across the world each year to meet the growing demand for sustainable energy. Bats of certain species are dying at wind turbines in unprecedented numbers. Species of bats consistently affected by turbines tend to be those that rely on trees as roosts and most migrate long distances. Although considerable progress has been made in recent years toward better understanding the problem, the causes of bat fatalities at turbines remain unclear. In this synthesis, we review hypothesized causes of bat fatalities at turbines. Hypotheses of cause fall into 2 general categories—proximate and ultimate. Proximate causes explain the direct means by which bats die at turbines and include collision with towers and rotating blades, and barotrauma. Ultimate causes explain why bats come close to turbines and include 3 general types: random collisions, coincidental collisions, and collisions that result from attraction of bats to turbines. The random collision hypothesis posits that interactions between bats and turbines are random events and that fatalities are representative of the bats present at a site. Coincidental hypotheses posit that certain aspects of bat distribution or behavior put them at risk of collision and include aggregation during migration and seasonal increases in flight activity associated with feeding or mating. A surprising number of attraction hypotheses suggest that bats might be attracted to turbines out of curiosity, misperception, or as potential feeding, roosting, flocking, and mating opportunities. Identifying, prioritizing, and testing hypothesized causes of bat collisions with wind turbines are vital steps toward developing practical solutions to the problem.

Hoary bats (Lasiurus cinereus) exhibit continental patterns of migration that are unique to bats, but details about their behaviors during migration are lacking. We captured 177 hoary bats in spring and early summer 2002 as individuals migrated through the Sandia Mountains of north-central New Mexico. Our results support earlier observations of asynchronous timing of migration between sexes of L. cinereus during spring, with females preceding males by ca. 1 month. We provide the first evidence that hoary bats may travel in dispersed groups, fly below the tree canopy along streams, and feed while migrating during spring. Analysis of guano revealed that diet of L. cinereus consisted mostly of moths, with more than one-half of samples identified as Noctuidae and Geometridae. We observed a late-spring decline in consumption of moths that might be related to seasonal changes in abundance of prey, differential selection of prey by bats, or sampling bias. We suspect that spring migration of L. cinereus through New Mexico temporally coincides with the seasonal abundance of moths.

Wind energy is rapidly becoming a viable source of alternative energy, but wind turbines are killing bats in many areas of North America. Most of the bats killed by turbines thus far have been migratory species that roost in trees throughout the year, and the highest fatality events appear to coincide with autumn migration. Hoary bats (Lasiurus cinereus) are highly migratory and one of the most frequently killed species at wind turbines. We analyzed a long-term data set to investigate how weather and moonlight influenced the occurrence of hoary bats at an island stopover point along their migration route. We then related our results to the problem of bat fatalities at wind turbines. We found that relatively low wind speeds, low moon illumination, and relatively high degrees of cloud cover were important predictors of bat arrivals and departures, and that low barometric pressure was an additional variable that helped predict arrivals. Slight differences in the conditions under which bats arrived and departed from the island suggest that hoary bats may be more likely to arrive on the island with passing storm fronts in autumn. These results also indicate that fatalities of hoary bats at wind turbines may be predictable events, that the species may be drawn to prominent landmarks that they see during migration, and that they regularly migrate over the ocean. Additional observations from this and other studies suggest that the problem of bat fatalities at wind turbines may be associated with flocking and autumn mating behaviors.

Despite evidence of migration in North American tree bats (genera Lasiurus and Lasionycteris), details regarding seasonal movements in these widely distributed species are few. This study attempted to clarify patterns of seasonal distribution by mapping museum occurrence records by month. Monthly changes in the distribution of records indicate seasonal movements of tree bats. Northward migration during spring by Lasiurus cinereus appears to stem from wintering grounds in California and Mexico. During summer, male L. cinereus is mainly distributed in western North America, whereas females dominate samples from eastern regions. Lasiurus borealis winters in southeastern areas and expands its range into more northern regions during warmer months. Seasonal dispersal of Lasiurus blossevillii from California is apparently limited, and it is unclear if this group mixes with others to the south and east. Lasionycteris noctivagansalso shows movement at the continental scale, although movements may differ between western and eastern groups. Museum records provide little evidence of major movement by any species between North and South America. Despite inherent biases, museum records are a viable means of investigating bat migration. words: Chiroptera, Lasionycteris noctivagans, Lasiurus blossevillii, Lasiurus borealis, Lasiurus cinereus, migration, occurrence records, seasonal distribution

Bats are among the most economically important nondomesticated mammals in the world. They are well-known pollinators and seed dispersers, but crop pest suppression is probably the most valuable ecosystem service provided by bats. Scientific literature and popular media often include reports of crop pests in the diet of bats and anecdotal or extrapolated estimates of how many insects are eaten by bats. However, quantitative estimates of the ecosystem services provided by bats in agricultural systems are rare, and the few estimates that are available are limited to a single cotton-dominated system in Texas. Despite the tremendous value for conservation and economic security of such information, surprisingly few scientific efforts have been dedicated to quantifying the economic value of bats. Here, we outline the types of information needed to better quantify the value of bats in agricultural ecosystems. Because of the complexity of the ecosystems involved, creative experimental design and innovative new methods will help advance our knowledge in this area. Experiments involving bats in agricultural systems may be needed sooner than later, before population declines associated with white-nose syndrome and wind turbines potentially render them impossible.

s of Workshop Research Presentations This section provides extended abstracts of the research presentations given on the first day and a half of the workshop. (Presenting Author’s name is in bold; full contact information for presenting authors is found in the “Contact Information” section; see “References Cited” section for full reference citations). Disclaimer – All presentations at the workshop were for informational purposes only. Neither the USGS nor the USFWS endorses any products promoted during the workshop. Primer on Radar Biology and Applications to Conservation Issues Ron Larkin, Illinois Natural History Survey, Champaign, Ill. This lecture is based primarily on two book chapters (Larkin, 2005; Diehl and Larkin, 2005). The brief summary here does not do justice to those more thorough treatments of the subject. Because bats make up an unknown and possibly appreciable part of the radar-echo-producing flying animals in many situations, and because arthropods are also often prominent, it is best to speak of radar biology rather than radar ornithology and "flying vertebrates" rather than "birds."

Understanding seasonal distribution and movement patterns of animals that migrate long distances is an essential part of monitoring and conserving their populations. Compared to migratory birds and other more conspicuous migrants, we know very little about the movement patterns of many migratory bats. Hoary bats (Lasiurus cinereus), a cryptic, wide-ranging, long-distance migrant, comprise a substantial proportion of the tens to hundreds of thousands of bat fatalities estimated to occur each year at wind turbines in North America. We created seasonally-dynamic species distribution models (SDMs) from 2,753 museum occurrence records collected over five decades in North America to better understand the seasonal geographic distributions of hoary bats. We used 5 SDM approaches: logistic regression, multivariate adaptive regression splines, boosted regression trees, random forest, and maximum entropy and consolidated outputs to generate ensemble maps. These maps represent the first formal hypotheses for sex- and season-specific hoary bat distributions. Our results suggest that North American hoary bats winter in regions with relatively long growing seasons where temperatures are moderated by proximity to oceans, and then move to the continental interior for the summer. SDMs suggested that hoary bats are most broadly distributed in autumn—the season when they are most susceptible to mortality from wind turbines; this season contains the greatest overlap between potentially suitable habitat and wind energy facilities. Comparing wind-turbine fatality data to model outputs could test many predictions, such as ‘risk from turbines is highest in habitats between hoary bat summering and wintering grounds’. Although future field studies are needed to validate the SDMs, this study generated well-justified and testable hypotheses of hoary bat migration patterns and seasonal distribution.

We appreciate the comments by Fisher and Naidoo regarding our recent effort to provide a first estimate of how much the disappearance of bats could cost the agricultural industry in the United States. Their critique focuses on the fact that variation in agricultural and ecological systems across the

The migration of animals across long distances and between multiple habitats presents a major challenge for conservation. For the migratory Mexican free-tailed bat (Tadarida brasiliensis mexicana), these challenges include identifying and protecting migratory routes and critical roosts in two countries, the United States and Mexico. Knowledge and conservation of bat migratory routes is critical in the face of increasing threats from climate change and wind turbines that might decrease migratory survival. We employ a new modeling approach for bat migration, network modeling, to simulate migratory routes between winter habitat in southern Mexico and summer breeding habitat in northern Mexico and the southwestern United States. We use the model to identify key migratory routes and the roosts of greatest conservation value to the overall population. We measure roost importance by the degree to which the overall bat population declined when the roost was removed from the model. The major migratory routes—those with the greatest number of migrants—were between winter habitat in southern Mexico and summer breeding roosts in Texas and the northern Mexican states of Sonora and Nuevo Leon. The summer breeding roosts in Texas, Sonora, and Nuevo Leon were the most important for maintaining population numbers and network structure - these are also the largest roosts. This modeling approach contributes to conservation efforts by identifying the most influential areas for bat populations, and can be used to as a tool to improve our understanding of bat migration for other species. We anticipate this approach will help direct coordination of habitat protection across borders.