Changes in hibernating tricolored bat (Perimyotis subflavus) roosting behavior in response to white‐nose syndrome

Understanding animals'' behavioral and physiological responses to pathogenic diseases is critical for management and conservation. One such disease, white‐nose syndrome (WNS), has greatly affected bat populations throughout eastern North America leading to significant population declines in several species. Although tricolored bat (Perimyotis subflavus) populations have experienced significant declines, little research has been conducted on their responses to the disease, particularly in the southeastern United States. Our objective was to document changes in tricolored bat roost site use after the appearance of WNS in a hibernaculum in the southeastern U.S. and relate these to microsite temperatures, ambient conditions, and population trends. We censused a tricolored bat hibernaculum in northwestern South Carolina, USA, once each year between February 26 and March 2, 2014–2021, and recorded species, section of the tunnel, distance from the entrance, and wall temperature next to each bat. The number of tricolored bats in the hibernaculum dropped by 90.3% during the first 3 years after the arrival of WNS. However, numbers stabilized and slightly increased from 2018 to 2021. Prior to the arrival of WNS, 95.6% of tricolored bats roosted in the back portion of the tunnel that was the warmest. After the arrival of WNS, we observed a significant increase in the proportion of bats using the front, colder portions of the tunnel, particularly during the period of population stabilization and increase. Roost temperatures of bats were also positively associated with February external temperatures. Our results suggest that greater use of the colder sections of the tunnel by tricolored bats could have led to increased survival due to slower growth rates of the fungus that causes WNS in colder temperatures or decreased energetic costs associated with colder hibernation temperatures. Thus, management actions that provide cold hibernacula may be an option for long‐term management of hibernacula, particularly in southern regions.     

The Potential Impact of White-Nose Syndrome on the Conservation Status of North American Bats

White-Nose syndrome (WNS) is an emergent infectious disease that has already killed around six million bats in North America and has spread over two thousand kilometers from its epicenter. However, only a few studies on the possible impacts of the fungus on bat hosts were conducted, particularly concerning its implications for bat conservation. We predicted the consequences of WNS spread by generating a map with potential areas for its occurrence based on environmental conditions in sites where the disease already occurs, and overlaid it with the geographic distribution of all hibernating bats in North America. We assumed that all intersection localities would negatively affect local bat populations and reassessed their conservation status based on their potential population decline. Our results suggest that WNS will not spread widely throughout North America, being mostly restricted to the east and southeast regions. In contrast, our most pessimistic scenario of population decline indicated that the disease would threaten 32% of the bat species. Our results could help further conservation plans to preserve bat diversity in North America.     

Anticipating white‐nose syndrome in the Southern Hemisphere: Widespread conditions favourable to Pseudogymnoascus destructans pose a serious risk to Australia's bat fauna

There is a serious concern that white‐nose syndrome (WNS), a fungal disease causing severe population declines in North American bats, could soon threaten bats on the Australian continent. Despite an ‘almost certain' risk of incursion within the next ten years, and high virulence in naïve bat populations, we remain uncertain about the vulnerability of Australian bats to WNS. In this study, we intersected occurrences for the 27 cave roosting bat species in Australia with interpolated data on mean annual surface temperature, which provides a proxy for thermal conditions within a cave and hence its suitability for growth by the fungal pathogen Pseudogymnoascus destructans. Our analysis identifies favourable roost thermal conditions within 30–100% of the ranges of eight bat species across south‐eastern Australia, including for seven species already listed as threatened with extinction. These results demonstrate the potential for widespread exposure to P. destructans and suggest that WNS could pose a serious risk to the conservation of Australia's bat fauna. The impacts of exposure to P. destructans will depend, however, on the sensitivity of bats to developing WNS, and a more comprehensive vulnerability assessment is currently prevented by a lack of information on the hibernation biology of Australian bats. Thus, given the clear potential for widespread exposure of Australia's bats to P. destructans demonstrated by our study, two specific policy actions seem justified: (i) urgent implementation of border controls that identify and decontaminate cave‐associated fomites and (ii) dedicated funding to enable research on key aspects of bat winter behaviour and hibernation physiology. Further, as accidental translocation of this fungus could also pose a risk to other naïve bat faunas in cooler regions of southern Africa and South America, we argue that a proactive, globally coordinated approach is required to understand and mitigate the potential impacts of WNS spreading to Southern Hemisphere bats.     

Major histocompatibility complex variation is similar in little brown bats before and after white‐nose syndrome outbreak

White‐nose syndrome (WNS), caused by the fungal pathogen Pseudogymnoascus destructans (Pd), has driven alarming declines in North American hibernating bats, such as little brown bat (Myotis lucifugus). During hibernation, infected little brown bats are able to initiate anti‐Pd immune responses, indicating pathogen‐mediated selection on the major histocompatibility complex (MHC) genes. However, such immune responses may not be protective as they interrupt torpor, elevate energy costs, and potentially lead to higher mortality rates. To assess whether WNS drives selection on MHC genes, we compared the MHC DRB gene in little brown bats pre‐ (Wisconsin) and post‐ (Michigan, New York, Vermont, and Pennsylvania) WNS (detection spanning 2014–2015). We genotyped 131 individuals and found 45 nucleotide alleles (27 amino acid alleles) indicating a maximum of 3 loci (1–5 alleles per individual). We observed high allelic admixture and a lack of genetic differentiation both among sampling sites and between pre‐ and post‐WNS populations, indicating no signal of selection on MHC genes. However, post‐WNS populations exhibited decreased allelic richness, reflecting effects from bottleneck and drift following rapid population declines. We propose that mechanisms other than adaptive immunity are more likely driving current persistence of little brown bats in affected regions.     

Long‐term changes in bat activity in Quebec suggest climatic responses and summer niche partitioning associated with white‐nose syndrome

In North America, the greatest and most sudden threat to hibernating bats is white‐nose syndrome (WNS), which has caused massive declines in populations since 2006. Other determinants of bat dynamics, such as the climate, and the effect of reduction in the number of individuals sharing foraging space and summer roosting habitat may have an effect on population dynamics. We analyzed transect acoustic bat surveys conducted with ultrasonic detectors in 16 regions in Quebec, Canada, between 2000 and 2015. We used piecewise regression to describe changes in activity over time for each species and a meta‐analytic approach to measure its association with the North Atlantic Oscillation (NAO). As expected, mouse‐eared bat (Myotis spp.) activity sharply declined after the onset of WNS, down by 79% after 3 years. In contrast, big brown/silver‐haired bat activity increased over the same period, possibly due to a release of competition. Hoary bats and red bats remained present, although their activity did not increase. Myotis activity was positively correlated with a one‐year lag to the NAO index, associated with cold conditions in winter, but warm autumns. Big brown/silver‐haired and hoary bats were also more active during NAO‐positive years but without a lag. We conclude that combinations of threats may create rapid shifts in community compositions and that a more balanced research agenda that integrates a wider range of threats would help better understand and manage those changes.     

Long‐term changes in occurrence,relative abundance,and reproductive fitness of bat species in relation to arrival of White‐nose Syndrome in West Virginia,USA

White‐nose syndrome (WNS) is a disease caused by the fungus Pseudogymnoascus destructans which has resulted in the deaths of millions of bats across eastern North America. To date, hibernacula counts have been the predominant means of tracking the spread and impact of this disease on bat populations. However, an understanding of the impacts of WNS on demographic parameters outside the winter season is critical to conservation and recovery of bat populations impacted by this disease. We used long‐term monitoring data to examine WNS‐related impacts to summer populations in West Virginia, where WNS has been documented since 2009. Using capture data from 290 mist‐net sites surveyed from 2003 to 2019 on the Monongahela National Forest, we estimated temporal patterns in presence and relative abundance for each bat species. For species that exhibited a population‐level response to WNS, we investigated post‐WNS changes in adult female reproductive state and body mass. Myotis lucifugus (little brown bat), M. septentrionalis (northern long‐eared bat), and Perimyotis subflavus (tri‐colored bat) all showed significant decreases in presence and relative abundance during and following the introduction of WNS, while Eptesicus fuscus (big brown bat) and Lasiurus borealis (eastern red bat) responded positively during the WNS invasion. Probability of being reproductively active was not significantly different for any species, though a shift to earlier reproduction was estimated for E. fuscus and M. septentrionalis. For some species, body mass appeared to be influenced by the WNS invasion, but the response differed by species and reproductive state. Results suggest that continued long‐term monitoring studies, additional research into impacts of this disease on the fitness of WNS survivors, and a focus on providing optimal nonwintering habitat may be valuable strategies for assessing and promoting recovery of WNS‐affected bat populations.     

Disease‐related population declines in bats demonstrate non‐exchangeability in generalist predators

The extent to which persisting species may fill the functional role of extirpated or declining species has profound implications for the structure of biological communities and ecosystem functioning. In North America, arthropodivorous bats are threatened on a continent‐wide scale by the spread of white‐nose syndrome (WNS), a disease caused by the fungus Pseudogymnoascus destructans. We tested whether bat species that display lower mortality from this disease can partially fill the functional role of other bat species experiencing population declines. Specifically, we performed high‐throughput amplicon sequencing of guano from two generalist predators: the little brown bat (Myotis lucifugus) and big brown bat (Eptesicus fuscus). We then compared changes in prey consumption before versus after population declines related to WNS. Dietary niches contracted for both species after large and abrupt declines in little brown bats and smaller declines in big brown bats, but interspecific dietary overlap did not change. Furthermore, the incidence and taxonomic richness of agricultural pest taxa detected in diet samples decreased following bat population declines. Our results suggest that persisting generalist predators do not necessarily expand their dietary niches following population declines in other predators, providing further evidence that the functional roles of different generalist predators are ecologically distinct.     

Genetic structure of winter populations of the endangered Indiana bat (<Emphasis Type="Italic">Myotis sodalis</Emphasis>) prior to the white nose syndrome epidemic: implications for the risk of disease spread

The spread of white nose syndrome raises serious concerns about the long-term viability of affected bat species. Here we examine the geographic distribution of genetic variation, levels of population connectivity that may influence the spatial spread of WNS, and the likelihood that recent population declines in regions affected by WNS have led to the loss of unique genetic variation for the endangered Indiana bat (Myotis sodalis). We amplified a fragment of the mitochondrial control region for 375 individuals and genotyped 445 individuals at 10 microsatellite loci from 18 sampling sites distributed across the majority of the species’ range. Analysis of mitochondrial DNA indicated the presence of at least five distinct matrilineal clusters, with the most pronounced differences between northeastern sites and those in the rest of the range. The majority of individuals in the Ozark-Central, Midwest, and Appalachian recovery units fell into a single cluster. Significant differentiation also was observed between one Appalachian and one Midwestern site and the majority of other sites. However, using nuclear microsatellites we observed the absence of differentiation and widespread gene flow among all hibernacula, suggesting the occurrence of extensive gene flow through dispersal and mating. The absence of genetically distinct populations within the range of Indiana bats indicates a lack of barriers to WNS transmission, and it is unlikely that significant portions of the hibernating population of Indiana bats will remain disease free into the future. Further, while matrilineal gene flow was restricted among some sites and regions, we found no genetic evidence to support the division of Indiana bats into separate recovery units.     

Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome

White-nose syndrome (WNS) has caused alarming declines of North American bat populations in the 5 years since its discovery. Affected bats appear to starve during hibernation, possibly because of disruption of normal cycles of torpor and arousal. The importance of hydration state and evaporative water loss (EWL) for influencing the duration of torpor bouts in hibernating mammals recently led to "the dehydration hypothesis," that cutaneous infection of the wing membranes of bats with the fungus Geomyces destructans causes dehydration which in turn, increases arousal frequency during hibernation. This hypothesis predicts that uninfected individuals of species most susceptible to WNS, like little brown bats (Myotis lucifugus), exhibit high rates of EWL compared to less susceptible species. We tested the feasibility of this prediction using data from the literature and new data quantifying EWL in Natterer's bats (Myotis nattereri), a species that is, like other European bats, sympatric with G. destructans but does not appear to suffer significant mortality from WNS. We found that little brown bats exhibited significantly higher rates of normothermic EWL than did other bat species for which comparable EWL data are available. We also found that Natterer's bats exhibited significantly lower rates of EWL, in both wet and dry air, compared with values predicted for little brown bats exposed to identical relative humidity (RH). We used a population model to show that the increase in EWL required to cause the pattern of mortality observed for WNS-affected little brown bats was small, equivalent to a solitary bat hibernating exposed to RH of ～95%, or clusters hibernating in ～87% RH, as opposed to typical near-saturation conditions. Both of these results suggest the dehydration hypothesis is plausible and worth pursuing as a possible explanation for mortality of bats from WNS.     

White-nose syndrome: is this emerging disease a threat to European bats?

White-nose syndrome (WNS) is a newly emergent disease that potentially threatens all temperate bat species. A recently identified fungus, Geomyces destructans, is the most likely causative agent of this disease. Until 2009, WNS and G. destructans were exclusively known from North America, but recent studies have confirmed this fungus is also present in Europe. We assembled an international WNS consortium of 67 scientists from 29 countries and identified the most important research and conservation priorities to assess the risk of WNS to European bats. Here, we review what is known about WNS and G. destructans and detail the conservation and research recommendations aimed at understanding and containing this emerging infectious disease.     

West nile virus antibodies in bats from New Jersey and New York

Eighty-three serum samples were obtained from big brown (Eptesicus fuscus), little brown (Myotis lucifugus), and northern long-eared (Myotis septentriotalis) bats (Chiroptera: Vespertilionidae), from New Jersey and New York (USA) between July and October 2002. Samples were analyzed for neutralizing antibodies to West Nile virus (WNV) and St. Louis encephalitis (SLE) virus. One little brown bat and one northern long-eared bat tested positive for WNV neutralizing antibodies. No bats had antibodies to SLE virus. This was the first large-scale investigation of WNV infection in bats in New Jersey. Additional work is needed to determine the effects of WNV on bat populations.     

Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

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.     

Seasonal variation in age,sex, and reproductive status of Mexican free-tailed bats

In North America, Mexican free-tailed bats (Tadarida brasiliensis mexicana) consume vast numbers of insects contributing to the economic well-being of society. Mexican free-tailed bats have declined due to historic guano mining, roost destruction, and bioaccumulation of organochlorine pesticides. Long-distance migrations and dense congregations at roosts exacerbate these declines. Wind energy development further threatens bat communities worldwide and presents emerging challenges to bat conservation. Effective mitigation of bat mortality at wind energy facilities requires baseline data on the biology of affected populations. We collected data on age, sex, and reproductive condition of Mexican free-tailed bats at a cave roost in eastern Nevada located 6 km from a 152-MW industrial wind energy facility. Over 5 years, we captured 46,353 Mexican free-tailed bats. Although just over half of the caught individuals were nonreproductive adult males (53.6%), 826 pregnant, 892 lactating, 10,101 post-lactating, and 4327 nonreproductive adult females were captured. Juveniles comprised 11.5% of captures. Female reproductive phenology was delayed relative to conspecific roosts at lower latitudes, likely due to cooler temperatures. Roost use by reproductive females and juvenile bats demonstrates this site is a maternity roost, with significant ecological and conservation value. To our knowledge, no other industrial scale wind energy facilities exist in such proximity to a heavily used bat roost in North America. Given the susceptibility of Mexican free-tailed bats to wind turbine mortality and the proximity of this roost to a wind energy facility, these data provide a foundation from which differential impacts on demographic groups can be assessed.     

Population genetic structure of a common host predicts the spread of white‐nose syndrome,an emerging infectious disease in bats

Landscape complexity influences patterns of animal dispersal, which in turn may affect both gene flow and the spread of pathogens. White‐nose syndrome (WNS) is an introduced fungal disease that has spread rapidly throughout eastern North America, causing massive mortality in bat populations. We tested for a relationship between the population genetic structure of the most common host, the little brown myotis (Myotis lucifugus), and the geographic spread of WNS to date by evaluating logistic regression models of WNS risk among hibernating colonies in eastern North America. We hypothesized that risk of WNS to susceptible host colonies should increase with both geographic proximity and genetic similarity, reflecting historical connectivity, to infected colonies. Consistent with this hypothesis, inclusion of genetic distance between infected and susceptible colonies significantly improved models of disease spread, capturing heterogeneity in the spatial expansion of WNS despite low levels of genetic differentiation among eastern populations. Expanding our genetic analysis to the continental range of little brown myotis reveals strongly contrasting patterns of population structure between eastern and western North America. Genetic structure increases markedly moving westward into the northern Great Plains, beyond the current distribution of WNS. In western North America, genetic differentiation of geographically proximate populations often exceeds levels observed across the entire eastern region, suggesting infrequent and/or locally restricted dispersal, and thus relatively limited opportunities for pathogen introduction in western North America. Taken together, our analyses suggest a possibly slower future rate of spread of the WNS pathogen, at least as mediated by little brown myotis.     

Larger trees may support larger Indiana bat maternity colonies in a dynamic landscape

Indiana bats (Myotis sodalis), federally listed as endangered, are of management concern in eastern North America. While researchers quantified the habitat affinities of the species throughout the range, few studies have occurred in regions where populations are at high risk for wind energy development and changing climes. Central Illinois, USA, is a dynamic landscape where forest area has been increasing in recent decades (on public and private land) because of changing farming practices and increased habitat protections. The increasing availability of large diameter trees, increasing forest biomass, and changing forest compositions have the potential to influence Indiana bat roost habitat preferences. We assessed Indiana bat maternity roost selection at the tree and forest plot scale to characterize patterns of use in this region from 2017–2018. We predicted that large trees on the landscape would support large colonies of Indiana bats. We located bats in multiple species of trees including elm (Ulmus spp.), cottonwood (Populus deltoides), and shagbark hickory (Carya ovata). We documented larger maternity colonies sharing roosts than in previous studies from the 1980s in the same region. We suggest managers and regulatory agencies monitor Indiana bats in dynamic landscapes such as those with changing forest composition and biomass.     

Direct Detection of Fungal Siderophores on Bats with White-Nose Syndrome via Fluorescence Microscopy-Guided Ambient Ionization Mass Spectrometry

White-nose syndrome (WNS) caused by the pathogenic fungus Pseudogymnoascus destructans is decimating the populations of several hibernating North American bat species. Little is known about the molecular interplay between pathogen and host in this disease. Fluorescence microscopy ambient ionization mass spectrometry was used to generate metabolic profiles from the wings of both healthy and diseased bats of the genus Myotis. Fungal siderophores, molecules that scavenge iron from the environment, were detected on the wings of bats with WNS, but not on healthy bats. This work is among the first examples in which microbial molecules are directly detected from an infected host and highlights the ability of atmospheric ionization methodologies to provide direct molecular insight into infection.     

Effects of Hierarchical Roost Removal on Northern Long-Eared Bat (Myotis septentrionalis) Maternity Colonies

Forest roosting bats use a variety of ephemeral roosts such as snags and declining live trees. Although conservation of summer maternity habitat is considered critical for forest-roosting bats, bat response to roost loss still is poorly understood. To address this, we monitored 3 northern long-eared bat (Myotis septentrionalis) maternity colonies on Fort Knox Military Reservation, Kentucky, USA, before and after targeted roost removal during the dormant season when bats were hibernating in caves. We used 2 treatments: removal of a single highly used (primary) roost and removal of 24% of less used (secondary) roosts, and an un-manipulated control. Neither treatment altered the number of roosts used by individual bats, but secondary roost removal doubled the distances moved between sequentially used roosts. However, overall space use by and location of colonies was similar pre- and post-treatment. Patterns of roost use before and after removal treatments also were similar but bats maintained closer social connections after our treatments. Roost height, diameter at breast height, percent canopy openness, and roost species composition were similar pre- and post-treatment. We detected differences in the distribution of roosts among decay stages and crown classes pre- and post-roost removal, but this may have been a result of temperature differences between treatment years. Our results suggest that loss of a primary roost or ≤ 20% of secondary roosts in the dormant season may not cause northern long-eared bats to abandon roosting areas or substantially alter some roosting behaviors in the following active season when tree-roosts are used. Critically, tolerance limits to roost loss may be dependent upon local forest conditions, and continued research on this topic will be necessary for conservation of the northern long-eared bat across its range.     

Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white‐nose syndrome

White‐nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans (Pd) that affects bats during hibernation. Although millions of bats have died from WNS in North America, mass mortality has not been observed among European bats infected by the fungus, leading to the suggestion that bats in Europe are immune. We tested the hypothesis that an antibody‐mediated immune response can provide protection against WNS by quantifying antibodies reactive to Pd in blood samples from seven species of free‐ranging bats in North America and two free‐ranging species in Europe. We also quantified antibodies in blood samples from little brown myotis (Myotis lucifugus) that were part of a captive colony that we injected with live Pd spores mixed with adjuvant, as well as individuals surviving a captive Pd infection trial. Seroprevalence of antibodies against Pd, as well as antibody titers, was greater among little brown myotis than among four other species of cave‐hibernating bats in North America, including species with markedly lower WNS mortality rates. Among little brown myotis, the greatest titers occurred in populations occupying regions with longer histories of WNS, where bats lacked secondary symptoms of WNS. We detected antibodies cross‐reactive with Pd among little brown myotis naïve to the fungus. We observed high titers among captive little brown myotis injected with Pd. We did not detect antibodies against Pd in Pd‐infected European bats during winter, and titers during the active season were lower than among little brown myotis. These results show that antibody‐mediated immunity cannot explain survival of European bats infected with Pd and that little brown myotis respond differently to Pd than species with higher WNS survival rates. Although it appears that some species of bats in North America may be developing resistance to WNS, an antibody‐mediated immune response does not provide an explanation for these remnant populations.     

Distribution and underground habitats of cave-dwelling bats in China

To understand the distribution and relative abundance of cave-dwelling bats and to identify those sites that would be important for conservation of bat species, 25 underground sites that had not been previously surveyed were investigated in this 3-year study (from December 2003 to April 2006) in Funiu Mountain of Henan province, China. Approximately 80 000 bats were recorded, representing 12 species. The most abundant species were Rhinolophus affini s, Miniopterus schreibersi and Hipposideros pratti . The roosts were evaluated for their conservation importance. The most important sites in the area are Yunhua and Nanzhao caves, which serve as hibernaculums and nursery roosts to c . 13 740 and 11 803 bats, respectively, representing seven species. By means of cluster and correspondence analysis, the distribution of bat species was different between the two sides of the mountain and was highly dependent on the size of the cave. The underground sites in the south region hosted c . 80% of the total bats, representing 11 species. The sites in the north region hosted 20% of the total bats, representing seven species. Presently, none of the caves in the region has adequate protection and some bat populations are under serious threat. Many large caves that contained large bat populations and several species of concern had been developed as tourist sites, and so some advice on protecting the most important local habitats was sought based on the assessment of the conservation status of underground sites. This paper presents basic data concerning the distribution of cave-dwelling bats and the patterns of cave use on Funiu Mountain. The data will help local governments and policy-makers develop suitable strategies to promote local tourisms while protecting important habitats of animal species.     

Declines in summer bat activity in central New England 4 years following the initial detection of white-nose syndrome

White-nose syndrome (WNS) was first reported in a hibernating bat population in central New York State in February 2006. Since 2006, WNS has been reported from bat hibernacula across much of eastern United States and adjacent Canada and has been associated with a dramatic decline in the populations of hibernating bats in the northeastern U.S. We are only beginning to discover how these declines are manifest in changes in summer bat abundance and activity at local scales. A 3-year (2004–2006) acoustic survey showed that the forested watershed of the Quabbin Reservoir in central Massachusetts supported an abundant and species-rich summer bat community. In 2010, 4-years following the initial occurrence of WNS, a re-survey of the same habitats and sites found a 72% reduction in bat activity on the watershed. This is the identical rate of decline reported from cave hibernacula surveys (73%). This decline in summer activity levels is most likely a consequence of WNS-caused mortality. The impacts of population losses of this magnitude of a once widespread and abundant taxa are unknown but are presumed to be ecologically significant.