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Background: Bats of the genus Lasiurus occur throughout the Americas and have diversified into at least 20 species among three subgenera. The hoary bat ( Lasiurus cinereus ) is highly migratory and ranges farther across North America than any other wild mammal. Despite the ecological importance of this species as a major insect predator, and the particular susceptibility of lasiurine bats to wind turbine strikes, our understanding of hoary bat ecology, physiology, and behavior remains poor., Methods: To better understand adaptive evolution in this lineage, we used whole-genome sequencing to identify protein-coding sequence and explore signatures of positive selection. Gene models were predicted with Maker and compared to seven well-annotated and phylogenetically representative species. Evolutionary rate analysis was performed with PAML., Results: Of 9,447 single-copy orthologous groups that met evaluation criteria, 150 genes had a significant excess of nonsynonymous substitutions along the L. cinereus branch ( P < 0.001 after manual review of alignments). Selected genes as a group had biased expression, most strongly in thymus tissue. We identified 23 selected genes with reported immune functions as well as a divergent paralog of Steep1 within suborder Yangochiroptera. Seventeen genes had roles in lipid and glucose metabolic pathways, partially overlapping with 15 mitochondrion-associated genes; these adaptations may reflect the metabolic challenges of hibernation, long-distance migration, and seasonal variation in prey abundance. The genomic distribution of positively selected genes differed significantly from background expectation by discrete Kolmogorov-Smirnov test ( P < 0.001). Remarkably, the top three physical clusters all coincided with islands of conserved synteny predating Mammalia, the largest of which shares synteny with the human cat-eye critical region (CECR) on 22q11. This observation coupled with the expansion of a novel Tbx1 -like gene family may indicate evolutionary innovation during pharyngeal arch development: both the CECR and Tbx1 cause dosage-dependent congenital abnormalities in thymus, heart, and head, and craniodysmorphy is associated with human orthologs of other positively selected genes as well., Competing Interests: The authors declare that they have no competing interests., (© 2022 Cornman and Cryan.)

Wind energy producers need deployable devices for wind turbines that prevent bat fatalities. Based on the speculation that bats approach turbines after visually mistaking them for trees, we tested a potential light-based deterrence method. It is likely that the affected bats see ultraviolet (UV) light at low intensities. Here, we present the results of a multi-month experiment to cast dim, flickering UV light across wind turbine surfaces at night. Our objectives were to refine and test a practical system for dimly UV-illuminating turbines while testing whether the experimental UV treatment influenced the activity of bats, birds, and insects. We mounted upward-facing UV light arrays on turbines and used thermal-imaging cameras to quantify the presence and activity of night-flying animals. The results demonstrated that the turbines can be lit to the highest reaches of the blades with "invisible" UV light, and the animal responses to such experimental treatment can be concurrently monitored. The UV treatment did not significantly change nighttime bat, insect, or bird activity at the wind turbine. Our findings show how observing flying animals with thermal cameras at night can help test emerging technologies intended to variably affect their behaviors around wind turbines.

Background: Hoary bats ( Lasiurus cinereus ) are among the bat species most commonly killed by wind turbine strikes in the midwestern United States. The impact of this mortality on species census size is not understood, due in part to the difficulty of estimating population size for this highly migratory and elusive species. Genetic effective population size (Ne) could provide an index of changing census population size if other factors affecting Ne are stable., Methods: We used the NeEstimator package to derive effective breeding population size (Nb) estimates for two temporally spaced cohorts: 93 hoary bats collected in 2009-2010 and an additional 93 collected in 2017-2018. We sequenced restriction-site associated polymorphisms and generated a de novo genome assembly to guide the removal of sex-linked and multi-copy loci, as well as identify physically linked markers., Results: Analysis of the reference genome with psmc suggested at least a doubling of Ne in the last 100,000 years, likely exceeding Ne = 10,000 in the Holocene. Allele and genotype frequency analyses confirmed that the two cohorts were comparable, although some samples had unusually high or low observed heterozygosities. Additionally, the older cohort had lower mean coverage and greater variability in coverage, and batch effects of sampling locality were observed that were consistent with sample degradation. We therefore excluded samples with low coverage or outlier heterozygosity, as well as loci with sequence coverage far from the mode value, from the final data set. Prior to excluding these outliers, contemporary Nb estimates were significantly higher in the more recent cohort, but this finding was driven by high values for the 2018 sample year and low values for all other years. In the reduced data set, Nb did not differ significantly between cohorts. We found base substitutions to be strongly biased toward cytosine to thymine or the complement, and further partitioning loci by substitution type had a strong effect on Nb estimates. Minor allele frequency and base quality bias thresholds also had strong effects on Nb estimates. Instability of Nb with respect to common data filtering parameters and empirically identified factors prevented robust comparison of the two cohorts. Given that confidence intervals frequently included infinity as the stringency of data filtering increased, contemporary trends in Nb of North American hoary bats may not be tractable with the linkage disequilibrium method, at least using the protocol employed here., Competing Interests: The authors declare there are no competing interests., (©2021 Cornman et al.)

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., Competing Interests: We declare no competing interests., (Published 2021. This article is a U.S. Government work and is in the public domain in the USA. Ecology and Evolution published by John Wiley & Sons Ltd.)

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., Competing Interests: The authors have declared that no competing interests exist.

Bats vocalize during flight as part of the sensory modality called echolocation, but very little is known about whether flying bats consistently call. Occasional vocal silence during flight when bats approach prey or conspecifics has been documented for relatively few species and situations. Bats flying alone in clutter-free airspace are not known to forgo vocalization, yet prior observations suggested possible silent behavior in certain, unexpected situations. Determining when, why, and where silent behavior occurs in bats will help evaluate major assumptions of a primary monitoring method for bats used in ecological research, management, and conservation. In this study, we recorded flight activity of Hawaiian hoary bats ( Lasiurus cinereus semotus ) under seminatural conditions using both thermal video cameras and acoustic detectors. Simultaneous video and audio recordings from 20 nights of observation at 10 sites were analyzed for correspondence between detection methods, with a focus on video observations in three distance categories for which accompanying vocalizations were detected. Comparison of video and audio detections revealed that a high proportion of Hawaiian hoary bats "seen" on video were not simultaneously "heard." On average, only about one in three visual detections within a night had an accompanying call detection, but this varied greatly among nights. Bats flying on curved flight paths and individuals nearer the cameras were more likely to be detected by both methods. Feeding and social calls were detected, but no clear pattern emerged from the small number of observations involving closely interacting bats. These results may indicate that flying Hawaiian hoary bats often forgo echolocation, or do not always vocalize in a way that is detectable with common sampling and monitoring methods. Possible reasons for the low correspondence between visual and acoustic detections range from methodological to biological and include a number of biases associated with the propagation and detection of sound, cryptic foraging strategies, or conspecific presence. Silent flight behavior may be more prevalent in echolocating bats than previously appreciated, has profound implications for ecological research, and deserves further characterization and study.

Understanding of migration in small bats has been constrained by limitations of techniques that were labor-intensive, provided coarse levels of resolution, or were limited to population-level inferences. Knowledge of movements and behaviors of individual bats have been unknowable because of limitations in size of tracking devices and methods to attach them for long periods. We used sutures to attach miniature global positioning system (GPS) tags and data loggers that recorded light levels, activity, and temperature to male hoary bats (Lasiurus cinereus). Results from recovered GPS tags illustrated profound differences among movement patterns by individuals, including one that completed a >1000 km round-trip journey during October 2014. Data loggers allowed us to record sub-hourly patterns of activity and torpor use, in one case over a period of 224 days that spanned an entire winter. In this latter bat, we documented 5 torpor bouts that lasted ≥16 days and a flightless period that lasted 40 nights. These first uses of miniature tags on small bats allowed us to discover that male hoary bats can make multi-directional movements during the migratory season and sometimes hibernate for an entire winter.

Solar power towers produce electrical energy from sunlight at an industrial scale. Little is known about the effects of this technology on flying animals and few methods exist for automatically detecting or observing wildlife at solar towers and other tall anthropogenic structures. Smoking objects are sometimes observed co-occurring with reflected, concentrated light ("solar flux") in the airspace around solar towers, but the identity and origins of such objects can be difficult to determine. In this observational pilot study at the world's largest solar tower facility, we assessed the efficacy of using radar, surveillance video, and insect trapping to detect and observe animals flying near the towers. During site visits in May and September 2014, we monitored the airspace surrounding towers and observed insects, birds, and bats under a variety of environmental and operational conditions. We detected and broadly differentiated animals or objects moving through the airspace generally using radar and near solar towers using several video imaging methods. Video revealed what appeared to be mostly small insects burning in the solar flux. Also, we occasionally detected birds flying in the solar flux but could not accurately identify birds to species or the types of insects and small objects composing the vast majority of smoking targets. Insect trapping on the ground was somewhat effective at sampling smaller insects around the tower, and presence and abundance of insects in the traps generally trended with radar and video observations. Traps did not tend to sample the larger insects we sometimes observed flying in the solar flux or found dead on the ground beneath the towers. Some of the methods we tested (e.g., video surveillance) could be further assessed and potentially used to automatically detect and observe flying animals in the vicinity of solar towers to advance understanding about their effects on wildlife.

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 the year 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 on 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 the year 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.

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.

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.

Determining the detailed movements of individual animals often requires them to carry tracking devices, but tracking broad-scale movement of small bats (<30 g) has been limited by transmitter technology and long-term attachment methods. This limitation inhibits our understanding of bat dispersal and migration, particularly in the context of emerging conservation issues such as fatalities at wind turbines and diseases. We tested a novel method of attaching lightweight global positioning system (GPS) tags and geolocating data loggers to small bats. We used monofilament, synthetic, absorbable sutures to secure GPS tags and data loggers to the skin of anesthetized big brown bats (Eptesicus fuscus) in Colorado and hoary bats (Lasiurus cinereus) in California. GPS tags and data loggers were sutured to 17 bats in this study. Three tagged bats were recaptured 7 months after initial deployment, with tags still attached; none of these bats showed ill effects from the tag. No severe injuries were apparent upon recapture of 6 additional bats that carried tags up to 26 days after attachment; however, one of the bats exhibited skin chafing. Use of absorbable sutures to affix small tracking devices seems to be a safe, effective method for studying movements of bats over multiple months, although additional testing is warranted. This new attachment method has the potential to quickly advance our understanding of small bats, particularly as more sophisticated miniature tracking devices (e.g., satellite tags) become available.

Background: The physiological effects of white-nose syndrome (WNS) in hibernating bats and ultimate causes of mortality from infection with Pseudogymnoascus (formerly Geomyces) destructans are not fully understood. Increased frequency of arousal from torpor described among hibernating bats with late-stage WNS is thought to accelerate depletion of fat reserves, but the physiological mechanisms that lead to these alterations in hibernation behavior have not been elucidated. We used the doubly labeled water (DLW) method and clinical chemistry to evaluate energy use, body composition changes, and blood chemistry perturbations in hibernating little brown bats (Myotis lucifugus) experimentally infected with P. destructans to better understand the physiological processes that underlie mortality from WNS., Results: These data indicated that fat energy utilization, as demonstrated by changes in body composition, was two-fold higher for bats with WNS compared to negative controls. These differences were apparent in early stages of infection when torpor-arousal patterns were equivalent between infected and non-infected animals, suggesting that P. destructans has complex physiological impacts on its host prior to onset of clinical signs indicative of late-stage infections. Additionally, bats with mild to moderate skin lesions associated with early-stage WNS demonstrated a chronic respiratory acidosis characterized by significantly elevated dissolved carbon dioxide, acidemia, and elevated bicarbonate. Potassium concentrations were also significantly higher among infected bats, but sodium, chloride, and other hydration parameters were equivalent to controls., Conclusions: Integrating these novel findings on the physiological changes that occur in early-stage WNS with those previously documented in late-stage infections, we propose a multi-stage disease progression model that mechanistically describes the pathologic and physiologic effects underlying mortality of WNS in hibernating bats. This model identifies testable hypotheses for better understanding this disease, knowledge that will be critical for defining effective disease mitigation strategies aimed at reducing morbidity and mortality that results from WNS.

Wind turbines are causing unprecedented numbers of bat fatalities. Many fatalities involve tree-roosting bats, but reasons for this higher susceptibility remain unknown. To better understand behaviors associated with risk, we monitored bats at three experimentally manipulated wind turbines in Indiana, United States, from July 29 to October 1, 2012, using thermal cameras and other methods. We observed bats on 993 occasions and saw many behaviors, including close approaches, flight loops and dives, hovering, and chases. Most bats altered course toward turbines during observation. Based on these new observations, we tested the hypotheses that wind speed and blade rotation speed influenced the way that bats interacted with turbines. We found that bats were detected more frequently at lower wind speeds and typically approached turbines on the leeward (downwind) side. The proportion of leeward approaches increased with wind speed when blades were prevented from turning, yet decreased when blades could turn. Bats were observed more frequently at turbines on moonlit nights. Taken together, these observations suggest that bats may orient toward turbines by sensing air currents and using vision, and that air turbulence caused by fast-moving blades creates conditions that are less attractive to bats passing in close proximity. Tree bats may respond to streams of air flowing downwind from trees at night while searching for roosts, conspecifics, and nocturnal insect prey that could accumulate in such flows. Fatalities of tree bats at turbines may be the consequence of behaviors that evolved to provide selective advantages when elicited by tall trees, but are now maladaptive when elicited by wind turbines.

Long-distance migration evolved independently in bats and unique migration behaviors are likely, but because of their cryptic lifestyles, many details remain unknown. North American hoary bats (Lasiurus cinereus cinereus) roost in trees year-round and probably migrate farther than any other bats, yet we still lack basic information about their migration patterns and wintering locations or strategies. This information is needed to better understand unprecedented fatality of hoary bats at wind turbines during autumn migration and to determine whether the species could be susceptible to an emerging disease affecting hibernating bats. Our aim was to infer probable seasonal movements of individual hoary bats to better understand their migration and seasonal distribution in North America. We analyzed the stable isotope values of non-exchangeable hydrogen in the keratin of bat hair and combined isotopic results with prior distributional information to derive relative probability density surfaces for the geographic origins of individuals. We then mapped probable directions and distances of seasonal movement. Results indicate that hoary bats summer across broad areas. In addition to assumed latitudinal migration, we uncovered evidence of longitudinal movement by hoary bats from inland summering grounds to coastal regions during autumn and winter. Coastal regions with nonfreezing temperatures may be important wintering areas for hoary bats. Hoary bats migrating through any particular area, such as a wind turbine facility in autumn, are likely to have originated from a broad expanse of summering grounds from which they have traveled in no recognizable order. Better characterizing migration patterns and wintering behaviors of hoary bats sheds light on the evolution of migration and provides context for conserving these migrants.

Bats are sources of high viral diversity and high-profile zoonotic viruses worldwide. Although apparently not pathogenic in their reservoir hosts, some viruses from bats severely affect other mammals, including humans. Examples include severe acute respiratory syndrome coronaviruses, Ebola and Marburg viruses, and Nipah and Hendra viruses. Factors underlying high viral diversity in bats are the subject of speculation. We hypothesize that flight, a factor common to all bats but to no other mammals, provides an intensive selective force for coexistence with viral parasites through a daily cycle that elevates metabolism and body temperature analogous to the febrile response in other mammals. On an evolutionary scale, this host-virus interaction might have resulted in the large diversity of zoonotic viruses in bats, possibly through bat viruses adapting to be more tolerant of the fever response and less virulent to their natural hosts.

White-nose syndrome is devastating North American bat populations but we lack basic information on disease mechanisms. Altered blood physiology owing to epidermal invasion by the fungal pathogen Geomyces destructans (Gd) has been hypothesized as a cause of disrupted torpor patterns of affected hibernating bats, leading to mortality. Here, we present data on blood electrolyte concentration, haematology and acid-base balance of hibernating little brown bats, Myotis lucifugus, following experimental inoculation with Gd. Compared with controls, infected bats showed electrolyte depletion (i.e. lower plasma sodium), changes in haematology (i.e. increased haematocrit and decreased glucose) and disrupted acid-base balance (i.e. lower CO2 partial pressure and bicarbonate). These findings indicate hypotonic dehydration, hypovolaemia and metabolic acidosis. We propose a mechanistic model linking tissue damage to altered homeostasis and morbidity/mortality.

The emerging wildlife disease white-nose syndrome is causing widespread mortality in hibernating North American bats. White-nose syndrome occurs when the fungus Geomyces destructans infects the living skin of bats during hibernation, but links between infection and mortality are underexplored. We analyzed blood from hibernating bats and compared blood electrolyte levels to wing damage caused by the fungus. Sodium and chloride tended to decrease as wing damage increased in severity. Depletion of these electrolytes suggests that infected bats may become hypotonically dehydrated during winter. Although bats regularly arouse from hibernation to drink during winter, water available in hibernacula may not contain sufficient electrolytes to offset winter losses caused by disease. Damage to bat wings from G. destructans may cause life-threatening electrolyte imbalances.

Bats are hosts to a range of zoonotic and potentially zoonotic pathogens. Human activities that increase exposure to bats will likely increase the opportunity for infections to spill over in the future. Ecological drivers of pathogen spillover and emergence in novel hosts, including humans, involve a complex mixture of processes, and understanding these complexities may aid in predicting spillover. In particular, only once the pathogen and host ecologies are known can the impacts of anthropogenic changes be fully appreciated. Cross-disciplinary approaches are required to understand how host and pathogen ecology interact. Bats differ from other sylvatic disease reservoirs because of their unique and diverse lifestyles, including their ability to fly, often highly gregarious social structures, long lifespans and low fecundity rates. We highlight how these traits may affect infection dynamics and how both host and pathogen traits may interact to affect infection dynamics. We identify key questions relating to the ecology of infectious diseases in bats and propose that a combination of field and laboratory studies are needed to create data-driven mechanistic models to elucidate those aspects of bat ecology that are most critical to the dynamics of emerging bat viruses. If commonalities can be found, then predicting the dynamics of newly emerging diseases may be possible. This modelling approach will be particularly important in scenarios when population surveillance data are unavailable and when it is unclear which aspects of host ecology are driving infection dynamics., (© 2012 Blackwell Verlag GmbH.)

Bats are the natural reservoirs of a number of high-impact viral zoonoses. We present a quantitative analysis to address the hypothesis that bats are unique in their propensity to host zoonotic viruses based on a comparison with rodents, another important host order. We found that bats indeed host more zoonotic viruses per species than rodents, and we identified life-history and ecological factors that promote zoonotic viral richness. More zoonotic viruses are hosted by species whose distributions overlap with a greater number of other species in the same taxonomic order (sympatry). Specifically in bats, there was evidence for increased zoonotic viral richness in species with smaller litters (one young), greater longevity and more litters per year. Furthermore, our results point to a new hypothesis to explain in part why bats host more zoonotic viruses per species: the stronger effect of sympatry in bats and more viruses shared between bat species suggests that interspecific transmission is more prevalent among bats than among rodents. Although bats host more zoonotic viruses per species, the total number of zoonotic viruses identified in bats (61) was lower than in rodents (68), a result of there being approximately twice the number of rodent species as bat species. Therefore, rodents should still be a serious concern as reservoirs of emerging viruses. These findings shed light on disease emergence and perpetuation mechanisms and may help lead to a predictive framework for identifying future emerging infectious virus reservoirs.

White-nose syndrome (WNS) is an emerging disease of hibernating bats associated with cutaneous infection by the fungus Geomyces destructans (Gd), and responsible for devastating declines of bat populations in eastern North America. Affected bats appear emaciated and one hypothesis is that they spend too much time out of torpor during hibernation, depleting vital fat reserves required to survive the winter. The fungus has also been found at low levels on bats throughout Europe but without mass mortality. This finding suggests that Gd is either native to both continents but has been rendered more pathogenic in North America by mutation or environmental change, or that it recently arrived in North America as an invader from Europe. Thus, a causal link between Gd and mortality has not been established and the reason for its high pathogenicity in North America is unknown. Here we show that experimental inoculation with either North American or European isolates of Gd causes WNS and mortality in the North American bat, Myotis lucifugus. In contrast to control bats, individuals inoculated with either isolate of Gd developed cutaneous infections diagnostic of WNS, exhibited a progressive increase in the frequency of arousals from torpor during hibernation, and were emaciated after 3-4 mo. Our results demonstrate that altered torpor-arousal cycles underlie mortality from WNS and provide direct evidence that Gd is a novel pathogen to North America from Europe.

Understanding animal mating systems is an important component of their conservation, yet the precise mating times for many species of bats are unknown. The aim of this study was to better understand the details and timing of reproductive events in species of bats that die most frequently at wind turbines in North America, because such information can help inform conservation strategies. We examined the reproductive anatomy of hoary bats (Lasiurus cinereus), eastern red bats (L. borealis), and silver-haired bats (Lasionycteris noctivagans) found dead beneath industrial-scale wind turbines to learn more about when they mate. We evaluated 103 L. cinereus, 18 L. borealis, and 47 Ln. noctivagans from wind energy facilities in the United States and Canada. Histological analysis revealed that most male L. cinereus and L. borealis, as well as over half the Ln. noctivagans examined had sperm in the caudae epididymides by late August, indicating readiness to mate. Testes regression in male hoary bats coincided with enlargement of seminal vesicles and apparent growth of keratinized spines on the glans penis. Seasonality of these processes also suggests that mating could occur during August in L. cinereus. Spermatozoa were found in the uterus of an adult female hoary bat collected in September, but not in any other females. Ovaries of all females sampled had growing secondary or tertiary follicles, indicating sexual maturity even in first-year females. Lasiurus cinereus, L. borealis, and Ln. noctivagans are the only North American temperate bats in which most first-year young of both sexes are known to sexually mature in their first autumn. Our findings provide the first detailed information published on the seasonal timing of mating readiness in these species most affected by wind turbines.

White-nose syndrome (WNS) has caused recent catastrophic declines among multiple species of bats in eastern North America. The disease's name derives from a visually apparent white growth of the newly discovered fungus Geomyces destructans on the skin (including the muzzle) of hibernating bats. Colonization of skin by this fungus is associated with characteristic cutaneous lesions that are the only consistent pathological finding related to WNS. However, the role of G. destructans in WNS remains controversial because evidence to implicate the fungus as the primary cause of this disease is lacking. The debate is fuelled, in part, by the assumption that fungal infections in mammals are most commonly associated with immune system dysfunction. Additionally, the recent discovery that G. destructans commonly colonizes the skin of bats of Europe, where no unusual bat mortality events have been reported, has generated further speculation that the fungus is an opportunistic pathogen and that other unidentified factors are the primary cause of WNS. Here we demonstrate that exposure of healthy little brown bats (Myotis lucifugus) to pure cultures of G. destructans causes WNS. Live G. destructans was subsequently cultured from diseased bats, successfully fulfilling established criteria for the determination of G. destructans as a primary pathogen. We also confirmed that WNS can be transmitted from infected bats to healthy bats through direct contact. Our results provide the first direct evidence that G. destructans is the causal agent of WNS and that the recent emergence of WNS in North America may represent translocation of the fungus to a region with a naive population of animals. Demonstration of causality is an instrumental step in elucidating the pathogenesis and epidemiology of WNS and in guiding management actions to preserve bat populations against the novel threat posed by this devastating infectious disease.

Bats are reservoirs for many different coronaviruses (CoVs) as well as many other important zoonotic viruses. We sampled feces and/or anal swabs of 1,044 insectivorous bats of 2 families and 17 species from 21 different locations within Colorado from 2007 to 2009. We detected alphacoronavirus RNA in bats of 4 species: big brown bats (Eptesicus fuscus), 10% prevalence; long-legged bats (Myotis volans), 8% prevalence; little brown bats (Myotis lucifugus), 3% prevalence; and western long-eared bats (Myotis evotis), 2% prevalence. Overall, juvenile bats were twice as likely to be positive for CoV RNA as adult bats. At two of the rural sampling sites, CoV RNAs were detected in big brown and long-legged bats during the three sequential summers of this study. CoV RNA was detected in big brown bats in all five of the urban maternity roosts sampled throughout each of the periods tested. Individually tagged big brown bats that were positive for CoV RNA and later sampled again all became CoV RNA negative. Nucleotide sequences in the RdRp gene fell into 3 main clusters, all distinct from those of Old World bats. Similar nucleotide sequences were found in amplicons from gene 1b and the spike gene in both a big-brown and a long-legged bat, indicating that a CoV may be capable of infecting bats of different genera. These data suggest that ongoing evolution of CoVs in bats creates the possibility of a continued threat for emergence into hosts of other species. Alphacoronavirus RNA was detected at a high prevalence in big brown bats in roosts in close proximity to human habitations (10%) and known to have direct contact with people (19%), suggesting that significant potential opportunities exist for cross-species transmission of these viruses. Further CoV surveillance studies in bats throughout the Americas are warranted.

White-nose syndrome (WNS) is causing unprecedented declines in several species of North American bats. The characteristic lesions of WNS are caused by the fungus Geomyces destructans, which erodes and replaces the living skin of bats while they hibernate. It is unknown how this infection kills the bats. We review here the unique physiological importance of wings to hibernating bats in relation to the damage caused by G. destructans and propose that mortality is caused by catastrophic disruption of wing-dependent physiological functions. Mechanisms of disease associated with G. destructans seem specific to hibernating bats and are most analogous to disease caused by chytrid fungus in amphibians.

This study quantifies sex differences in thermoregulation and water loss of a small (20-35 g) insectivorous heterothermic mammal, the hoary bat Lasiurus cinereus, during its spring migration. We measured body temperature, metabolic rate and evaporative water loss, and calculated wet thermal conductance, for bats exposed to air temperatures ranging from 0 to 40 degrees C for periods of 2-5 h. Pregnant females maintained normothermic body temperatures (35.7+/-0.7 degrees C; mean +/- S.E.M.) independent of air temperature. In contrast, males became torpid during the majority (68%) of exposures to air temperatures <25 degrees C. The thermal neutral zone (TNZ) ranged between approximately 30 degrees C and 34 degrees C in both sexes and, within the TNZ, females had lower mass-specific metabolic rates (6.1+/-0.2 mW g(-1)) than males (9.0+/-0.9 mW g(-1)). Wet thermal conductance values in torpid bats (0.7+/-0.5 mW g(-1) deg.(-1)) were lower than those of normothermic individuals (1.1+/-0.3 mW g(-1) deg.(-1)). Mass-specific rates of evaporative water loss in males were consistently higher than in females at most air temperatures and rates of water loss in torpid bats were 63+/-6% of normothermic values. These results suggest that male and pregnant female L. cinereus employ different thermoregulatory strategies during their spring migration. Females defend normothermic body temperatures, presumably to expedite embryonic growth, while males use torpor, presumably to minimize energy and water deficits. These variable thermoregulatory strategies may reflect continental differences in the summer distribution of the sexes.