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Ecology and impacts of white-nose syndrome on bats


The recent introduction of Pseudogymnoascus destructans (the fungal pathogen that causes white-nose syndrome in bats) from Eurasia to North America has resulted in the collapse of North American bat populations and restructured species communities. The long evolutionary history between P. destructans and bats in Eurasia makes understanding host life history essential to uncovering the ecology of P. destructans. In this Review, we combine information on pathogen and host biology to understand the patterns of P. destructans spread, seasonal transmission ecology, the pathogenesis of white-nose syndrome and the cross-scale impact from individual hosts to ecosystems. Collectively, this research highlights how early pathogen detection and quantification of host impacts has accelerated the understanding of this newly emerging infectious disease.


White-nose syndrome (WNS) is a fungal disease in bats and one of the most devastating infectious disease outbreaks in wild mammals to emerge over the past century1,2,3,4,5,6,7,8,9,10,11,12,13,14,15. WNS was first detected in 2007 by biologists who discovered an abnormal mortality event at a cave in Albany County, New York (NY), USA, while conducting routine bat population monitoring surveys16. Bats that were still alive were covered in a white fungus, which was most noticeable on their muzzles, ears and wings, thus leading to the disease being named WNS17,18. Following this discovery, inspection of nearby hibernation sites (hibernacula) led to similar findings and further examination of photos collected from previous winter surveys revealed that bats at another nearby site had visible signs of infection with the fungus in the winter of 2005–2006. Thus, the earliest evidence of this disease in North America is on 16 February 2006 in Howes Cave, NY17. Histological examination of dead and dying bats later identified the likely causative agent as Geomyces destructans19, a novel fungus that was unknown to science before its discovery in North America17. Based on DNA sequence data from other Geomyces spp. and related fungi, G. destructans was reclassified as Pseudogymnoascus destructans16,17,20 in 2013.

P. destructans is a multi-host psychrophilic ascomycete20 in the order Onygenales, which contains many other pathogenic and environmentally resilient fungi. Molecular evidence suggests that P. destructans has evolved with Eurasian bat communities, with which it has coexisted for millenia21,22, to become a specialist pathogen that relies primarily on living bat tissue for growth and replication22,23,24. The investment in parasitic traits has led to physiological and ecological trade-offs22,23,24,25,26, which make P. destructans both reliant on but also well adapted to infecting the epidermal tissue of hibernating bats during the winter26,27. While bat communities across Eurasia experience greatly reduced WNS disease severity with no evidence of mass mortality28,29, naive host communities in North America experienced unprecedented population declines1,2,3,4,5,6,7,8,9,10,11,12,13,14,15 on first exposure to this virulent pathogen26,27.

Routine monitoring and retrospective photo documentation of bat populations enabled biologists to estimate the timing of P. destructans’ introduction to North America with some certainty, making this disease emergence unique among other wildlife diseases. Early detection enabled the spread of P. destructans across North America to be tracked and the impacts of the pathogen on hosts to be accurately assessed. Building on this information, the first decade of WNS research has led to considerable advances in the understanding of the closely tied interactions between P. destructans and its hosts compared with other emerging wildlife diseases over similar timescales30,31. In this Review, we describe the origins, distribution, seasonal life history, pathogenesis, and the impacts and persistence of bats with P. destructans across the globe. Finally, we highlight conservation measures that have been taken to reduce the impacts of this pathogen and outline several areas of host and pathogen biology that require additional research.

Origins and introduction

Experimental27, ecological28,32 and molecular20,21,33 evidence has shown that a single clonally spreading genotype of P. destructans was introduced into North America from Eurasia in the early-to-mid 2000s21,33,34,35,36. Photographic evidence, isolation from museum specimens and genomic data21,37,38,39,40 indicate that P. destructans has likely been present in Europe and Asia for thousands of years or longer, with no evidence of host mass mortality in at least the past several decades28,29. Although the exact source of P. destructans and its mode of introduction into North America remain unknown21, the introduction of this pathogen was most likely mediated by humans, either through direct or indirect transfer of infectious propagules. Proposed hypotheses include accidental transport of an infected bat or the transfer of infectious propagules on contaminated gear and equipment, on specialty European cave-aged food items, or by tourists. Currently, no data exist to distinguish among these modes of introduction, and further molecular epidemiological investigation of the source of the North American isolates could shed light on how this devastating pathogen was introduced.

The analysis of P. destructans isolates using microsatellites and single-nucleotide polymorphisms suggests that there are at least three distinct clades, representing geographic groupings of isolates from Far-east Asia (China), Central Asia (Mongolia) and Europe21 (Fig. 1). The P. destructans genotype distributed across North America is a member of the European clade and is currently most closely related to an isolate collected from Ukraine (Fig. 1). However, sampling coverage in Eastern Europe and Central Asia is limited (Fig. 1), and a closer match to the North American isolate likely exists but is yet to be collected from this region. The greater diversity of isolates in East Asia in comparison to those in Europe, despite similar geographic distances, may suggest that the fungus first emerged in bats in Far-east Asia and then spread to Europe21 (Fig. 1). However, more samples from across Asia are needed to fully examine the differences in diversity and their historic origins. Genetic evidence supports the idea that Eurasian bat species were present when P. destructans likely diverged from other closely related Pseudogymnoascus spp., indicating that P. destructans has had a long period of co-evolution with its bat hosts21,41.

Fig. 1: Global distribution of Pseudogymnoascus destructans.

a | Points show locations that have been sampled for P. destructans28,33,39,40,53,54,55,68,77,161,162,163,164,165,166. Filled circles indicate sites where P. destructans was detected through qPCR, photographs and sampling of museum specimens and red open circles indicate sites where P. destructans was not detected (these sites in North America are not shown). This fungus has now been found in 23 countries/regions across Europe (including Austria, Belgium, Croatia, Czech Republic, Denmark, Estonia, France (FRA), Germany (DEU), Hungary (HUN), Italy, Latvia, Luxembourg, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Switzerland (CHE), Turkey, Ukraine (UKR), the United Kingdom and over the entire span of Russia) and 5 countries/regions across Asia (China (CHN), Georgia, Israel, Japan and Mongolia (MNG)) and likely exists across this entire region where bats hibernate. In North America, the circle colour indicates the year of first detection in each administrative subdivision (such as a county or provincial district). b | A phylogeny adapted from ref.21 shows a maximum clade credibility tree constructed from genomic single-nucleotide polymorphisms (SNPs) with branch length representing time. Isolates from North America are nearly indistinguishable at the SNP loci analysed, as indicated by the triangle. The three supported clades include Far-east Asia (dark blue), Central Asia (blue) and Europe (light blue). c | Timeline showing the distances of maximum P. destructans spread during consecutive winters in North America. Year labels show the second half of the winter period (for example, 2006 corresponds to the winter of 2005–2006). Distance (circle diameter) is measured as the distance (± 25 km) between the centroid of the farthest county or administrative division (as reported by detected in winter t + 1 from its nearest county in the previous winter (t) (for example, the size of the circle above 2009 is the distance P. destructans spread from the end of winter 2008–2009 to the end of winter 2009–2010). The jump from eastern North America to Washington state (dashed circle) represents an ~2,100 km movement; the black circle in the centre of the dashed circle indicates the distance spread excluding this jump. The initial introduction into New York, USA, in 2006, is indicated by a red star. Part b is adapted from ref.21, CC BY 4.0 (

Patterns of spread

Over the past 15 years, P. destructans has spread across most of North America and, to date, it has been detected in 39 US states and 7 Canadian provinces (Fig. 1). The observed rate of spread of P. destructans in the first 8 years after the earliest North American record of the pathogen was gradual compared with that of other emerging pathogens that infect highly mobile hosts42,43, with an expansion of 200–900 km per year. The rate of spread accelerated in the period 2008–2012 as the pathogen spread southwest along the dense karst region of the Appalachian Mountains and west into Missouri during the winter of 2009–2010 (Fig. 1c). In 2016, the North American genotype of P. destructans was detected in western Washington state, 2,100 km from the nearest known contaminated hibernacula in Nebraska44 (Fig. 1). This long-distance dispersal likely represents a human-mediated movement and is not consistent with normal movement of bats. The fungus has subsequently been detected in other counties in Washington as well as in California, indicating a second expanding front in the western US (Fig. 1). Currently, the fungus has yet to be detected in Florida, despite being present in the nearby states of Georgia, South Carolina, Mississippi and Alabama for at least 7 years, suggesting that these states may represent the southern limit of the fungus’ distribution (Fig. 1).

Studies examining patterns of spatial spread have estimated the probability of detecting the fungus as a function of distance from the first affected hibernacula in NY. WNS was more likely to be observed at sites with larger host colony sizes, a higher fraction of host species using high-humidity environments45 and more densely aggregated host colonies with warmer temperatures46. Research based on patterns of P. destructans detection from 2007 to 2011 suggests that the density of karst habitat (a landscape underlain by soluble rocks, such as limestone, which is used as a surrogate for the number of natural caves) and longer winter duration increased the rate of spread47. Unfortunately, the fungus arrived in most US counties decades earlier than predicted47, and the more rapid expansion across North America showed that the proposed barriers to fungal spread, such as large gaps between sites, were only temporary obstacles. Past patterns of spread indicate that P. destructans will reach all or nearly all hibernacula in the US and Canada over the next decade, if not much sooner.

The spatiotemporal pattern of P. destructans spread among hibernacula is not consistent with seasonal patterns of host movement between hibernacula. Bat movements are higher during autumn, when bats visit multiple sites for mating, than during winter, when their movements are restricted by cold temperatures, limited fat reserves and a lack of resources48,49. However, P. destructans was more likely to be first detected at a site in late winter than in early winter (~1–2 months from the start of hibernation)50. This observation suggests that the majority of spread occurs over winter, likely due to much higher levels of infection during this period, which increases the probability of successful introduction and establishment at a site50.

The genetic population structure of one bat species, Myotis lucifugus, is similar to the broad patterns of spatial spread, which shows panmictic populations of this species east of the Rocky Mountains and more genetic structuring in western populations51. However, the spread of the fungus into Washington state in 2016 and the introduction of the fungus into North America in 2006 are inconsistent with normal movements by hibernating bats and suggest that human-mediated mechanisms, such as those described above, are necessary to explain these spreading events.

Genetic analyses to examine the patterns of spatial spread of P. destructans within North America have found no correlation between genetic and geographical distance, which suggests widespread mixing of P. destructans genotypes and frequent spread among infected hibernacula21,35. However, it is also possible that the lack of genetic diversity among clonal isolates has masked patterns of geographic spread. The analysis of mycoviruses that infect North American P. destructans has shown increased genetic clustering by distance52, suggesting that more-rapidly changing fungal viruses may be a promising tool for examining finer scale spatial spread.

Although P. destructans has spread throughout much of North America (Fig. 1) and is present throughout Eurasia28,32,39,53, there is no evidence that the fungus is present in the southern hemisphere in regions where bats hibernate (for example, South America and Australia54,55; Fig. 1). A risk assessment of the possibility of P. destructans introduction into Australian bat populations performed in 2019 suggests that introduction by a tourist, caver or researcher is likely in the next decade56. However, the impact of this pathogen on Australian bats is hypothesized to be lower than on North American bats owing to the shorter duration of the Australian winter56.

Seasonal cycles of infection

Host and pathogen ecology drive strong seasonal patterns of P. destructans infections (Fig. 2). Given the cyclical nature of most fungi, which generally undergo periods of intense proliferation followed by dormancy or dispersal, their life histories are intimately tied to their primary nutrient sources. Like many other fungi with an environmentally dormant stage, P. destructans produces conidia that are capable of surviving for long periods of time in underground hibernation sites57,58, allowing the fungus to persist over summer when it is unable to replicate on and infect bats.

Fig. 2: Seasonality and within-site transmission of Pseudogymnoascus destructans.

The seasonal pattern of P. destructans and its bat hosts is depicted. The internal circle shows the abundance and growth phases of P. destructans during different stages in bat life history. The outer circle shows the seasonal life history of a typical temperate hibernating bat. P. destructans persists in subterranean environments when bats are absent from these sites or are active in the landscape. During autumn, bats return to hibernacula, begin to accumulate fat stores for the winter, mate and start hibernating. Bats become infected or reinfected during autumn from environment-to-host and host-to-host contact. These infections progress over the winter while bats are hibernating in subterranean sites (such as caves, mines and tunnels) from late autumn until early spring. If bats survive P. destructans infection, they then emerge onto the landscape in spring, when females will typically form maternity colonies and communally raise their young. Males disperse singly on the landscape, occasionally forming small bachelor colonies. Infections are cleared over this active period when the fungus cannot grow. Although this is a typical annual cycle, some species remain in caves and mines all year round but still appear to clear infections over the summer. The graph inset shows general trends of P. destructans on bats in North America and Eurasia. The reduced environmental reservoir in Eurasia results in delayed infection for bats across this region compared to North America28.

The temperature-dependence of P. destructans growth strongly dictates when infections associated with WNS can occur59,60,61. As a psychrophile, P. destructans can only grow at temperatures <20 °C (ref.60). Temperate bat species affected by WNS are heterothermic and have seasonal fluctuations in body temperature. When bats are euthermic and active on the landscape, their body temperatures are typically higher (37–41 °C (ref.62)) than the 20 °C upper critical limit of fungal growth. However, the body temperature of bats drops to near ambient (1–16 °C (refs63,64)) at the start of hibernation in mid-to-late autumn, which is within the P. destructans growth range. This drop in body temperature coincides with a reduction in host immune function, enabling the fungus to colonize their epidermal tissue16 and grow26,27.

Seasonal patterns of pathogen prevalence and intensity were similar for six bat species after P. destructans establishment in North America26. Most bats (~75%) in North America become infected over a short, ~2–3 week period between late autumn and early winter, whereas bats across Europe and Asia acquire new infections over a much longer time period (6–7 months) and have a lower average pathogen prevalence (~20%) in early winter28 (Fig. 2). Across all regions, prevalence and fungal loads peak at the end of winter, which is when mortality occurs in North America27,28,53,61,65,66,67,68. Levels of P. destructans in the environment also increase over winter28,66, which is likely due to the shedding of infectious propagules and the movement of bats within sites during arousal periods27,69,70, intensifying the environmental contamination of P. destructans28,66.

For bats that survive until spring, the return to euthermia can result in an intense inflammatory response in P. destructans-infected tissue, primarily in the wing and tail membranes71,72. This immune response can reduce fungal infection73 but can also result in immune reconstitution inflammatory syndrome71,74, which causes severe immune-mediated tissue damage and can result in death for already compromised individuals75.

If bats survive through emergence from hibernation, they begin to clear infections within a few weeks61,72,73,76. Fungal loads drop significantly within 10 days following emergence and reach nearly undetectable levels (<1%) by mid summer61,72,73. Over this period, surviving individuals regenerate damaged tissue, and most lesions are healed between 25 and 40 days from the start of recovery61,72,73. P. destructans conidia can survive for only 5 days at 37 °C (the body temperature of active bats) on bat fur59, which likely contributes to the clearance of P. destructans after the end of hibernation. Although no comprehensive study of P. destructans seasonality has been conducted across Europe or Asia, one study sampled over 200 individuals from 9 bat species in China during the summer months (June–July) and found a prevalence of P. destructans of ~1%77, suggesting that seasonal patterns are likely similar across the entire distribution of this fungus.

The prevalence and fungal loads of P. destructans in Eurasian hibernacula environments have been found to decrease significantly during the summer28, whereas the prevalence in North American hibernacula remains nearly constant at an average of ~45%28,57,58. These higher levels of environmental contamination result in the earlier timing of infection for bats in North America compared to bats across Eurasia28. P. destructans prevalence in North American summer roosts has been found to be far lower (~2–7%78,79) and probably represents contamination from bats rather than from a persistent pathogen reservoir, as this fungus has limited viability given the sustained temperatures of over 30 °C in these roosts59. During autumn, bats return to hibernacula and engage in the ‘autumn swarm’, a behaviour characterized by promiscuous mating, long-distance movements between hibernacula and contact with hibernacula surfaces80,81,82,83,84, while also fattening in preparation for hibernation83,85. Bats become infected or reinfected from contact with the P. destructans environmental reservoir in hibernacula and subsequent contact with other bats during mating, which restarts the seasonal epizootic28,58,61,78,86. The autumn swarm is a phenomenon common to all temperate hibernating bat species80,81,82; however, the increased levels of P. destructans in the environment across North America leads to more transmission during this period than in Eurasia28 (Fig. 2).

Modes of transmission

P. destructans is primarily transmitted by direct contact between bats and through contact with contaminated environmental surfaces during autumn and winter26,28,86 (Fig. 2). The fission–fusion and highly gregarious social structure of many bat species results in the efficient transmission of P. destructans (Fig. 2). While bat activity is greatly reduced during hibernation, bats cycle through periods of torpor with brief (~1–3 hours) intermittent arousals every ~2–3 weeks69,87,88. Activity during these arousal periods results in infected bats transmitting P. destructans to other individuals or an uninfected bat coming into contact with a contaminated environment. A study using a surrogate pathogen (a trackable ultraviolet (UV)-fluorescent dust)86, revealed that, for two species (M. lucifugus and Myotis septentrionalis), a single individual bat transmitted the surrogate pathogen to a large fraction of the total population (~25%) at a site. However, a third species examined (Perimyotis subflavus) showed that spatial segregation within hibernacula reduced transmission to ~2%.

Examination of other potential transmission modes has found little evidence to suggest that aerosolized, vectored or vertical transmission are important in the dispersal of P. destructans26,61,89. For example, a study examined whether P. destructans conidia could be transmitted through the air by housing uninfected and infected bats in close proximity (~1.3 cm apart), though not in direct contact, for over 3 months26. None of the exposed bats became infected, suggesting that P. destructans conidia do not move freely through the air. A study examining the potential for vectored transmission found that spinturnicid mites collected from a colony of Myotis myotis tested positive for P. destructans89. However, this study did not explicitly examine whether these mites were responsible for initial infection or were simply contaminated as a consequence of the bats themselves becoming infected. Vertical transmission, the movement of a pathogen from parent to offspring, has also been explored in maternity colonies of several bat species. While a small fraction of offspring tested positive for P. destructans, the thermal requirements for the growth of this fungus and the timing of births (in summer) means that it is unlikely that P. destructans could survive the summer to infect bats the following winter59,61,72,73.

Biology and pathogenesis

A specialist bat pathogen

Many fungi are saprophytes, meaning that they rely on decomposing matter that they break down into macromolecules, such as proteins, lipids and starch, which are absorbed through their cell walls to fuel growth90. Saprophytic fungi can range from fully obligate to facultative saprophytes, as some species can also exploit nutrients from living organisms (for example, parasites)91. Studies comparing P. destructans to other closely related non-pathogenic Pseudogymnoascus spp. found that the P. destructans genome encoded ~65% fewer carbohydrate-activating enzymes (CAZymes) than other congeners22. CAZymes are involved in the breakdown and synthesis of carbon and are typically more abundant in decomposers than in parasitic fungi92. In conjunction with decreased enzyme potential, growth experiments revealed that P. destructans grows slower in vitro and utilizes a narrower range of carbon sources than its closely related species22,23,24. By contrast, enzymes that degrade collagen, the core structural protein in mammals, were the predominant hydrolytic enzymes in the P. destructans secretome and were not found in the secretomes of other Pseudogymnoascus spp.25.

The examination of proteins associated with DNA repair pathways also showed that P. destructans lacks a gene (UVE1) that is important for the repair of UV-induced DNA damage22. Closely related Pseudogymnoascus spp. and most other microorganisms that are found in underground sites still harbour the UVE1 gene, suggesting that loss of this gene is not a trait that is associated only with microorganisms that have evolved in the absence of UV light22. The reduced CAZyme production and inability to repair DNA damage may represent an evolutionary trade-off as P. destructans invested in mechanisms to exploit living animal tissue (for example, collagen-degrading enzymes) and evade the mammalian immune system25.


P. destructans has been found on at least 62 species from 14 different genera of hibernating bats across all temperate regions of the northern hemisphere28,32,39,40,53,93,94 (Supplementary Table 1) but has not been found to infect other mammalian taxa. In North America, epidermal skin lesions that are diagnostic of WNS have been confirmed in at least 12 bat species, and another 9 species have tested positive for P. destructans through a combination of DNA detection and pathogen culturing17,95,96. Across Eurasia, 41 bat species have tested positive for P. destructans, and >76% of these species have been confirmed with lesions diagnostic of WNS28,32,39,40,53,93,94.

The lesions caused by P. destructans are found predominately on the ears, nose and muzzle of hibernating bats but are most severe in their wing and tail tissue (Fig. 3), which can serve vital regulatory functions, including thermoregulation, gas exchange, water balance and immune function16,97,98,99,100,101. These infections lead to a cascade of physiological effects99,101,102,103,104 that eventually result in increased arousal frequency27,70,87,105,106, loss of fat stores and starvation87 and, in many cases, death. In captive M. lucifugus, death occurred 88–114 days after experimental infection27. Evaporative water loss and increased frequency of arousals likely create a feedback loop that can exacerbate the physiological effects of the disease99,101,104. Dehydration (for example, electrolyte depletion and hypovolaemia) caused by excess evaporative water loss in infected bats is a key contributor to WNS mortality99,101,104, and there are multiple hypotheses about the pathways by which P. destructans infection may result in dehydration102,107 (Fig. 3). Other physiological markers of early infection that precede increased arousals include a higher metabolic rate, acidosis (elevated blood partial pressure of carbon dioxide and bicarbonate) and elevated blood potassium levels99,101,104.

Fig. 3: Effects of Pseudogymnoascus destructans infection on bat hosts.

Under the right conditions, a P. destructans conidium germinates, producing a germ tube156 that develops into hyphae, which eventually form hyphal mats termed mycelia that comprise the vegetative fungal growth on and in bat epidermal tissue16,167,168. The fungus initially grows on the surface of the skin but progresses to invasion of the epidermal tissue. These infections alter the skin lipid profile and eventually form cup-like epidermal lesions and ulcerations of the wing membrane, which can extend into the connective tissue and result in necrosis16,76,129. The hyphae also invade hair follicles and sebaceous glands, filling the epidermal sheath and invading nearby connective tissue16,97. Growth on the surface of the skin produces non-motile, unicellular arthroconidia or conidia through septation and fragmentation of existing hyphae19,167,168. P. destructans possesses the genetic machinery for sexual recombination (not shown in diagram) in some regions (Europe and Asia)169. However, the fungus introduced and circulating in North America seems to only be capable of asexual reproduction21,68,169. The introduction of additional mating types to North America could increase the rate of P. destructans evolution in North America, allowing it to further adapt to bats across this region and potentially escape the accumulation of deleterious mutations. The flow chart shows the physiological cascade initiated by P. destructans infections99,101,102,104,107,126. Dashed arrows indicate hypothetical relationships. Immune reconstitution inflammatory syndrome (IRIS) may lead directly to mortality during spring emergence when an intense immune response is initiated in reponse to P. destrcutans infection that has accumulated over winter in epidermal and connective tissues.

WNS-induced mortality in bats seems to be partly related to an ineffective and possibly damaging immune reaction to infection, which does not limit fungal growth108 and is not exhibited in species that suffer lower disease impacts109,110,111,112,113. The transcription of genes associated with inflammation, the immune response and metabolism was upregulated only during arousals from torpor in infected M. lucifugus114. While localized inflammation in response to infections does occur, hosts typically show a lack of leukocyte recruitment to sites of infection74. Torpor seems to limit the ability of bats to mount a full immunological response to P. destructans infection and the titres of antibodies to P. destructans could not explain the differences in WNS-related mortality among North American bat species and between North American and European bats115. More generally, bat species that suffer lower mortality from WNS exhibited fewer changes in gene expression in response to infection116 and less alteration of arousal frequencies113 than did species with a higher WNS-related mortality.

Impact on the host

P. destructans has caused widespread declines in multiple bat species across eastern North America1,2,3,4,5,6,7,8,9,10,11,12,13,14,15 (Fig. 4). Prior to the arrival of WNS, populations of six bat species in the Northeastern US (defined here as including NY, Vermont (VT) and Connecticut (CT)1) and the Midwestern US (defined here as including Michigan (MI) and Wisconsin (WI)28) were growing (average growth of 11% in the Northeastern US1 and 10% in the Midwestern US28). Following the arrival of WNS, millions of bats died from the disease, with declines in some species exceeding 95% and entire populations of several species extirpated3. Steep declines in counts of wintering bat colonies were corroborated by declines in estimates of bat abundance during the summer7,8,11. However, in some areas, observed summer declines were delayed by a year, potentially due to the movement of bats from unaffected areas into optimal summer habitats6.

Fig. 4: Impacts of Pseudogymnoascus destructans on bat populations.

a | Fungal loads on North America and Eurasian bat species. Circles show the predicted fungal loads (log10 ng of DNA) on different bat species (indicated on the X axis) standardized to March 1; data from refs28,61,65,67. Loads are corrected for bat size by dividing predicted loads by the average forearm length to give log10 ng of DNA/mm2. The diameter of the circle is the inverse of the standard error, with larger circles having smaller standard error. Circle colour indicates the intensity of fungal infection. b | Annual population growth rates of bats affected by white-nose syndrome (WNS) across all regions. These data are from published accounts1,9,25 and federal and state government reports1,9,28,96,170,171,172,173,174,175,176. The dashed line indicates stability and solid lines show Loess curve fits to annual population growth rates for each species. Myotis lucifugus is the only species with an increasing population growth rate ~6 years after the arrival of WNS, and Myotis septentrionalis shows a trajectory towards extinction. c | Percent change in bat populations 2–3 years after P. destructans arrival in different US states (shown by two-letter state codes; data sources as in part b). Bold points show mean and 95% CIs. In some species, such as Eptesicus fuscus and Myotis sodalis, declines were highly variable among regions. In Wisconsin, E. fuscus, which can hibernate outside of conventional bat hibernacula, declined by 78%. Observed declines were not just due to emigration during mild winters, as pathogen arrival to sites occurred over 5 years with differing winter severity.

Variability in host declines

Declines caused by WNS have varied among host species, over time and across space (Fig. 4). Across several species, the impacts of WNS are load dependent, with the highest mortality observed in species experiencing the highest fungal loads65 (Fig. 4). M. septentrionalis is at serious risk of extinction as multiple studies showed similar drastic declines in both the Northeastern US1,3 and Midwestern US28,66, with complete extirpation occurring in nearly 70% of sites where WNS had been present for at least 4 years3. M. lucifugus populations experienced cumulative declines of 96% in the Northeastern US and 97% in the Midwestern US1,2 and also declined in the Southern US (defined here as including Virginia (VA), South Carolina (SC), Georgia (GA) and Tennessee (TN)) (Fig. 4), suggesting that shorter hibernation periods in the Southern US were not entirely protective. P. subflavus experienced similar population declines to M. lucifugus (95% and 99% cumulative decline in the Northeastern US and Midwestern US, respectively), although non-hibernating populations of this species in the Southern US and Central America may protect P. subflavus from global extinction. For several species, including Eptesicus fuscus and Myotis leibii, average population growth rates after the arrival of WNS were nearly stable but populations were no longer growing. This change in population growth rate likely represents some mortality in these species, not just emigration during mild winters, as pathogen arrival to sites occurred over multiple years with differing winter severity. Myotis sodalis, an endangered species, experienced serious (70% cumulative) population declines in the Northeastern US but some populations were less affected117.

Population declines have not yet been quantified for several other bat species that are infected by P. destructans. Lower fungal loads in some of these less-studied species, such as the endangered species Myotis grisescens, may indicate a lower impact67. Regardless, sustained hibernation seems to be critical in determining whether a species will be affected by this pathogen, as the non-obligate hibernator Tadarida brasiliensis was not highly susceptible to mortality in an experimental infection study118. Impacts of WNS in the more diverse bat communities of the Western US, where P. destructans recently arrived, remain largely unexplored (but see ref.119).

Drivers of variation in host impacts

Temperature and humidity are strong modifiers of P. destructans growth60,120 and have been shown to be important factors influencing the impacts of WNS at the individual121,122,123, species65 and population level1. Within the range of temperatures at which bats hibernate (generally 1–16 °C)28,63,64,65, P. destructans growth is higher at warmer hibernation temperatures60,65,124. Increased fungal growth on bats leads to more severe disease pathology, which in turn decreases survival125. As a result, bats that select warmer roosts have higher fungal loads and experience more severe disease impacts65. Higher humidity also increases fungal growth120 and was positively correlated with population impacts of P. destructans in M. sodalis1. However, lower humidity increases bat evaporative water loss, which is exacerbated by WNS99,101,102,104,126, making the link between humidity and WNS survival less clear127.

Numerous other factors may influence the variation in survival among bat species and populations. For some species, smaller populations suffered less severe declines, suggesting that lower bat densities might reduce transmission1,86. Bat populations across all temperate regions roosting in areas where P. destructans is more abundant in the environmental reservoir have lower population growth rates, suggesting a dose-dependent effect of the P. destructans environmental reservoir28,66,124. Other host factors are probably important in determining the variation in outcomes among species, including differences in torpor physiology104,113, skin lipids128,129, the skin microbiota130,131,132,133, immune response74,108,109,134,135,136 and co-infection with viruses137, although more detailed studies and experiments are needed to identify the importance of each of these factors. Climate is also likely to be an important contributor to variability among populations123,138 due to its effects on hibernation length, but the joint effects of hibernacula temperature and winter severity have not yet been comprehensively analysed.

Host persistence

Following severe declines in several formally abundant bat species, growth rates of some populations across North America began to stabilize1,2,5,139,140 (Fig. 4b). In particular, colonies of M. lucifugus in the Northeastern US are now stable or growing. To date, there is little evidence to suggest that the populations of other affected species in North America are increasing (Fig. 4b). For example, growth rates are still negative for many affected M. sodalis populations117,141. Coastal refugia have been implicated in the persistence of a few remnant M. septentrionalis142, although more research is needed to understand whether bats are actually surviving P. destructans infections in these habitats. Multiple studies have investigated the drivers of bat survival with WNS, mainly focusing on M. lucifugus or Eurasian bat species, spanning general (Fig. 5) to specific explanations of bat persistence and often reporting conflicting results. Broadly, the general mechanisms of bat persistence that have been investigated include resistance32,65,116,139, tolerance67,68,139, infection avoidance through reduced transmission1,28,139, and pathogen evolution21,27.

Fig. 5: General mechanisms of host persistence.

Following the introduction of novel pathogens, several general mechanisms could allow hosts to persist with disease. All graphs show hypothetical realizations of simulated data based on the relationships between pathogen burden (orange) and host health (blue), extrapolated from Raberg et al.145. For white-nose syndrome, burden measurements are typically fungal loads, whereas health measurements might include survival or tissue invasion. Simulations assume hosts become infected with identical pathogen doses at identical times, with the exception of part c, where healthier host populations initially acquire lower pathogen burdens (dose-dependence) or are infected later, as might happen if transmission decreases as populations decline. Epidemic declining populations (dashed lines) and persisting populations (solid lines) are compared. Grey dotted lines connect individual hosts from epidemic (open circles) or persisting (filled circles) populations. Resistance (part a): persisting hosts experience slower pathogen growth resulting in lower average burdens at the end of hibernation and higher health. Tolerance (part b): persisting hosts have similar pathogen growth rates to the epidemic population but have higher health. Pathogen avoidance (part c): Persisting hosts have lower pathogen burdens because they have lower or delayed pathogen exposure enabling higher health, despite similar pathogen growth rates. Resistance and tolerance (part d): two persisting populations with identical health differ in their resistance and tolerance. Both persisting populations (A and B) are more resistant (for example, have lower fungal growth rates) than the epidemic population but all individuals in population A (open triangles) are resistant, with low fungal burdens. Hosts in population B (closed triangles) are overall more resistant than epidemic hosts but also more tolerant, with higher health at the same fungal burdens. General vigour (part e): the persisting population does not differ in pathogen growth and thus average burden but differs in health (different health intercepts) due to innate differences that would be present in uninfected hosts. Pathogen virulence (part f): persisting populations have lower growth in this example, as would be predicted by trade-off theory177; however, actual patterns depend on evolutionary changes and could thus mimic parts bd.

In North America, there is widespread agreement among studies that most individuals continue to be infected at very high rates during early hibernation28,67,139,143 and therefore pathogen avoidance or reduced transmission owing to lower host density are less important in enabling the survival of M. lucifugus. This mechanism, and more generally a reduction in transmission due to reduced bat densities, was one of the original hypotheses to explain differences in the effects of WNS among host populations1. However, subsequent studies showed that spatial separation of individuals at the onset of WNS is likely a sickness response that occurs after P. destructans has already been transmitted to most of the colony70,144.

Several studies have examined other general mechanisms of host persistence. A study using an epidemiological model fit to infection data139 found that fungal growth was lower in persisting M. lucifugus populations in the Northeastern US than in epidemic populations where P. destructans had recently invaded. This finding is consistent with higher host resistance in persisting populations than in more recently exposed populations (Fig. 5a), which supports more anecdotal evidence of less visible fungal infections in surviving bat populations over time. By contrast, another study examining infection dynamics67 found that fungal loads in some persisting colonies were fairly stable over time and suggested that bat persistence might also be mediated by tolerance. Factors that could explain these discrepancies include a lack of dynamic pathogen data during the epidemic phase in the Northeastern US and a lack of individual-level data in both studies as well as an inability to account for transmission differences or to link fungal growth and bat health in the second study67. As neither study collected individual-level health data, it is unclear whether population-level data showing colony persistence could mask reduced individual survival probabilities, particularly if there is compensatory reproduction or immigration from other persisting colonies. Northeastern US populations may also be behaviourally resistant if they are using colder microclimates than epidemic Midwestern US populations. Therefore, while populations in the Northeastern US are unequivocally more resistant than Midwestern US populations during the WNS epizootic, whether population survival is mediated by resistance (either innate or behavioural), tolerance or a combination of both remains unknown. Comprehensively investigating each factor requires accounting for initial transmission and pathogen dose while following individual hosts within multiple populations over time in order to disentangle the mechanisms producing similar patterns (Fig. 5). For example, the mechanisms conferring tolerance or increases in general vigour appear similar and are only disentangled by comparing two populations to determine if differences still exist when hosts are uninfected145. In all cases, pathogen dynamics must be measured in conjunction with bat health.

Other more specific factors underlying the survival of bats with WNS in North America continue to be investigated and potentially include differences in arousal frequencies106 and fat deposition143, although it is unknown whether these factors are the cause of stable populations or the consequence of some other mechanism (Fig. 5). Differences in pathogen virulence are unlikely to be the most important factor currently determining host stabilization in North America, as experimental studies indicate that the virulence of European and North American P. destructans isolates are comparable27 and that there is little genetic spatial or temporal structure in P. destructans populations across North America21,33,35.

Studies investigating changes in M. lucifugus population genetic structure before and after WNS declines also found conflicting patterns. Three studies reported evidence of genetic changes between declining and persisting M. lucifugus136,146,147. However, another study148 found no such differences in M. lucifugus populations before and after WNS-induced declines but did find increased differentiation between bat populations in NY and Pennsylvania after WNS declines. Differences among these studies may be due to differences in sampling design and methodology or could reflect biological differences in selection among populations.

In Eurasia, a key factor allowing host coexistence with P. destructans is the delayed timing of infection. Across this region, the decay of the environmental reservoir of P. destructans during summer results in a slower transmission and reduced early winter infection in Eurasian bat colonies, resulting in delayed exposure, a form of pathogen avoidance28 (Fig. 5c). Eurasian bats return each autumn to hibernacula that are far less contaminated with P. destructans than North American hibernacula, resulting in lower fungal loads and reduced mortality by the end of winter28. Comparisons using identical sampling and testing procedures to measure fungal burdens in both Eurasia and North America have found consistently lower fungal loads on European and Asian bat species than on bat species in North America (Fig. 4), which is consistent with reduced fungal lesions and visible infections across Eurasia28,32,53. One study reported high fungal loads on European bats and suggested that they might be surviving by a higher tolerance to P. destructans68. However, this study used a qPCR assay with different quantification standards149 than that used to analyse samples collected from North American bats150 and was unable to account for the timing of transmission or initial exposure; therefore, the persistence of European species with WNS cannot be attributed to pathogen tolerance. In addition, experimental infections of Eurasian M. myotis bats found very limited fungal growth, which is consistent with resistance rather than tolerance151. It remains unknown whether other Eurasian species would experience similar disease severity to their North American counterparts if challenged with pathogen doses comparable to those that North American species experience.


The introduction of P. destructans has had devastating consequences for North American bat communities1,2,3,4,5,6,7,8,9,10,11,12,13,14,15. Some impacts of WNS are likely to last for many decades, while others may be permanent (Box 1). The slow population growth rates of heavily affected bat species, which usually give birth to only one young per year, means that it will take decades or longer for populations to recover to their original densities, even if they could return to pre-WNS growth rates140,141,152,153.

As P. destructans can establish long-term environmental reservoirs, it is unlikely that this pathogen could ever be eradicated from North America, which has resulted in research being focused on preventing spread and mitigating impacts30. Mitigation efforts have included both topical, oral and implanted treatments for hosts as well as attempts to reduce the environmental pathogen reservoir and delay transmission. Several treatments have now been tested in vitro, in vivo or in situ133,135,154,155,156,157,158, including antifungal chemicals, volatile organic compounds, probiotic microbes, biopolymers and vaccines (reviewed elsewhere153,155). Currently, only one probiotic treatment and a vaccine have been shown to reduce mortality in a single species, M. lucifugus135,155; however, no treatment has been deployed on a landscape scale. Other actions taken to minimize the impacts of WNS include limiting recreational activities in caves to reduce the disturbance of bat populations, restricting habitat alteration near hibernacula, and an early and unsuccessful effort at captive breeding30. The development of effective tools is still urgently needed to help reduce impacts in bat species that have shown no sign of stabilization and are most at risk of extinction.

There has been a rigorous surveillance effort to track the spread of P. destructans across the US and Canada, using a combination of passive and active measures, with confirmation through qPCR detection and histology in new counties, states/provinces or species. Concern about research-related disturbance to bats has occasionally resulted in reduced surveillance in some regions and in an inability to comprehensively assess population trajectories and species persistence. However, recent research suggests that visits related to population monitoring and research have no detectable effect on population growth rates159. Continued monitoring will be critical in assessing the impacts of WNS on bat populations as P. destructans spreads, just as it was for the initial discovery of this disease160.

There are multiple areas of uncertainty where additional research could help to advance WNS epidemiology and ecology. WNS research has been constrained by the limited ability to perform host experimental infection studies relative to other emerging diseases and much of our knowledge comes from a single North American species, M. lucifugus. Thus, additional work in other affected bat species or the development of a model organism system would greatly expand our knowledge about the impacts of WNS. Experimental work that needs to be undertaken includes analysing differences in pathogen virulence and understanding the susceptibility to mortality in multiple North American and Eurasian species. While substantial effort has been made to understand how some bat populations are now persisting with WNS, additional attention is needed to achieve a comprehensive understanding of the complexity of multi-host community persistence. To truly appreciate the contribution of different persistence mechanisms will likely require the use of experimental infections and the integration of epidemiological models with field and laboratory data. Enhanced knowledge of P. destructans biology across Eurasia and North America will also provide additional insights into the factors contributing to regional differences in pathology and help to elucidate the risks of introducing other novel strains of P. destructans. Finally, the ecosystem consequences of WNS-induced bat population declines have only been superficially explored (Box 1) and a more detailed analysis of the effects on agricultural, terrestrial and aquatic systems is needed. Collectively, this information could promote conservation and policy considerations that can help to prevent and mitigate the consequences of novel pathogen emergence in the future.


  1. 1.

    Langwig, K. E. et al. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol. Lett. 15, 1050–1057 (2012).

    PubMed  Google Scholar 

  2. 2.

    Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682 (2010).

    CAS  PubMed  Google Scholar 

  3. 3.

    Frick, W. F. et al. Disease alters macroecological patterns of North American bats. Glob. Ecol. Biogeogr. 24, 741–749 (2015).

    Google Scholar 

  4. 4.

    Turner, G. & Reeder, D. Update of white-nose syndrome in bats, September 2009. Bat Res. News 50, 47–53 (2009).

    Google Scholar 

  5. 5.

    Reichard, J. D. et al. Interannual survival of Myotis lucifugus (Chiroptera: Vespertilionidae) near the epicenter of white-nose syndrome. Northeast. Nat. 21, N56–N59 (2014).

    Google Scholar 

  6. 6.

    Dzal, Y., McGuire, L. P., Veselka, N. & Fenton, M. B. Going, going, gone: the impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus). Biol. Lett. 7, 392–394 (2011).

    PubMed  Google Scholar 

  7. 7.

    Francl, K. E., Ford, W. M., Sparks, D. W. & Brack, V. Capture and reproductive trends in summer bat communities in West Virginia: assessing the impact of white-nose syndrome. J. Fish. Wildl. Manag. 3, 33–42 (2012).

    Google Scholar 

  8. 8.

    Ford, W. M., Britzke, E. R., Dobony, C. A., Rodrigue, J. L. & Johnson, J. B. Patterns of acoustical activity of bats prior to and following white-nose syndrome occurrence. J. Fish. Wildl. Manag. 2, 125–134 (2011).

    Google Scholar 

  9. 9.

    Powers, K. E., Reynolds, R. J., Orndorff, W., Ford, W. M. & Hobson, C. S. Post-white-nose syndrome trends in Virginias cave bats, 2008–2013. J. Ecol. Nat. Environ. 7, 113–123 (2015).

    Google Scholar 

  10. 10.

    Powers, K. E. et al. Monitoring the status of gray bats (Myotis grisescens) in Virginia, 2009–2014, and potential impacts of white-nose syndrome. Southeast. Nat. 15, 127–137 (2016).

    Google Scholar 

  11. 11.

    Reynolds, R. J., Powers, K. E., Orndorff, W., Ford, W. M. & Hobson, C. S. Changes in rates of capture and demographics of Myotis septentrionalis (northern long-eared bat) in western Virginia before and after onset of white-nose syndrome. Northeast. Nat. 23, 195–204 (2016).

    Google Scholar 

  12. 12.

    Coleman, J. T. H. & Reichard, J. D. Bat white-nose syndrome in 2014: a brief assessment seven years after the discovery of a virulent fungal pathogen in North America. Outlooks Pest Manag. 25, 374–377 (2014).

    Google Scholar 

  13. 13.

    Turner, G. G., Reeder, D. M. & Coleman, J. T. H. A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and look to the future. Bat Res. News 52, 13–27 (2011).

    Google Scholar 

  14. 14.

    Nocera, T., Ford, W. M., Silvis, A. & Dobony, C. A. Patterns of acoustical activity of bats prior to and 10 years after WNS on Fort Drum Army Installation, New York. Glob. Ecol. Conserv. 18, e00633 (2019).

    Google Scholar 

  15. 15.

    Brooks, R. T. Declines in summer bat activity in central New England 4 years following the initial detection of white-nose syndrome. Biodivers. Conserv. 20, 2537–2541 (2011).

    Google Scholar 

  16. 16.

    Meteyer, C. U. et al. Histopathologic criteria to confirm white-nose syndrome in bats. J. Vet. Diagn. Invest. 21, 411–414 (2009).

    PubMed  Google Scholar 

  17. 17.

    Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227–227 (2009).

    CAS  PubMed  Google Scholar 

  18. 18.

    Chaturvedi, V. et al. Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PLoS ONE 5, e10783 (2010).

    PubMed  PubMed Central  Google Scholar 

  19. 19.

    Gargas, A., Trest, M. T., Christensen, M., Volk, T. J. & Bleher, D. S. Geomyces desctructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108, 147–154 (2009).

    Google Scholar 

  20. 20.

    Minnis, A. M. & Lindner, D. L. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 117, 638–649 (2013).

    PubMed  Google Scholar 

  21. 21.

    Drees, K. P. et al. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio 8, e01941-17 (2017).

    PubMed  PubMed Central  Google Scholar 

  22. 22.

    Palmer, J. M., Drees, K. P., Foster, J. T. & Lindner, D. L. Extreme sensitivity to ultraviolet light in the fungal pathogen causing white-nose syndrome of bats. Nat. Commun. 9, 35 (2018).

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Reynolds, H. T. & Barton, H. A. Comparison of the white-nose syndrome agent Pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprotrophic enzyme activity. PLoS ONE 9, e86437 (2014).

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Wilson, M. B., Held, B. W., Freiborg, A. H., Blanchette, R. A. & Salomon, C. E. Resource capture and competitive ability of non-pathogenic Pseudogymnoascus spp. and P. destructans, the cause of white-nose syndrome in bats. PLoS ONE 12, e0178968 (2017).

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    O’Donoghue, A. J. et al. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc. Natl Acad. Sci. USA 112, 7478–7483 (2015).

    PubMed  Google Scholar 

  26. 26.

    Lorch, J. M. et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl Acad. Sci. USA 109, 6999–7003 (2012).

    CAS  PubMed  Google Scholar 

  28. 28.

    Hoyt, J. R. et al. Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome. Proc. Natl Acad. Sci. USA 117, 7255–7262 (2020).

    CAS  PubMed  Google Scholar 

  29. 29.

    Fritze, M. & Puechmaille, S. J. Identifying unusual mortality events in bats: a baseline for bat hibernation monitoring and white-nose syndrome research. Mammal. Rev. 48, 224–228 (2018).

    Google Scholar 

  30. 30.

    Langwig, K. E. et al. Context dependent conservation responses to wildlife disease. Front. Ecol. Environ. 13, 195–202 (2015).

    Google Scholar 

  31. 31.

    Lorch, J. M. et al. Snake fungal disease: an emerging threat to wild snakes. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150457 (2016).

    Google Scholar 

  32. 32.

    Hoyt, J. R. et al. Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions. Proc. R. Soc. B Biol. Sci. (2016).

    Article  Google Scholar 

  33. 33.

    Leopardi, S., Blake, D. & Puechmaille, S. J. White-Nose Syndrome fungus introduced from Europe to North America. Curr. Biol. 25, R217–R219 (2015).

    CAS  PubMed  Google Scholar 

  34. 34.

    Rajkumar, S. S. et al. Clonal genotype of Geomyces destructans among bats with white nose syndrome, New York, USA. Emerg. Infect. Dis. 17, 1273–1276 (2011).

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Ren, P. et al. Clonal spread of Geomyces destructans among bats, midwestern and southern United States. Emerg. Infect. Dis. 18, 883–885 (2012).

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Puechmaille, S. J. et al. White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol. Evol. 26, 570–576 (2011).

    PubMed  Google Scholar 

  37. 37.

    Campana, M. G. et al. White-nose syndrome fungus in a 1918 bat specimen from France. Emerg. Infect. Dis. (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Martínková, N. et al. Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE 5, e13853 (2010).

    PubMed  PubMed Central  Google Scholar 

  39. 39.

    Puechmaille, S. J. et al. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE 6, e19167 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Zahradníková, A. Jr. et al. Historic and geographic surveillance of Pseudogymnoascus destructans possible from collections of bat parasites. Transbound. Emerg. Dis. 65, 303–308 (2018).

    PubMed  Google Scholar 

  41. 41.

    Ruedi, M. et al. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Mol. Phylogenet. Evol. 69, 437–449 (2013).

    PubMed  Google Scholar 

  42. 42.

    Hosseini, P. R., Dhondt, A. A. & Dobson, A. P. Spatial spread of an emerging infectious disease: conjunctivitis in house finches. Ecology 87, 3037–3046 (2006).

    PubMed  Google Scholar 

  43. 43.

    Kilpatrick, A. M. et al. Predicting the global spread of H5N1 avian influenza. Proc. Natl Acad. Sci. USA 103, 19368–19373 (2006).

    CAS  PubMed  Google Scholar 

  44. 44.

    Lorch, J. M. et al. First detection of bat white-nose syndrome in Western North America. mSphere 1, e00148-16 (2016).

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Wilder, A. P., Frick, W. F., Langwig, K. E. & Kunz, T. H. Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biol. Lett. 7, 950–953 (2011).

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Lilley, T. M., Anttila, J. & Ruokolainen, L. Landscape structure and ecology influence the spread of a bat fungal disease. Funct. Ecol. 32, 2483–2496 (2018).

    Google Scholar 

  47. 47.

    Maher, S. P. et al. Spread of white-nose syndrome on a network regulated by geography and climate. Nat. Commun. 3, 1306 (2012).

    PubMed  Google Scholar 

  48. 48.

    Davis, W. H. & Hitchcock, H. B. Biology and migration of the bat, Myotis lucifugus, in New England. J. Mammal. 46, 296–313 (1965).

    Google Scholar 

  49. 49.

    Norquay, K. J. O., Martinez-Nunez, F., Dubois, J. E., Monson, K. M. & Willis, C. K. R. Long-distance movements of little brown bats (Myotis lucifugus). J. Mammal. 94, 506–515 (2013).

    Google Scholar 

  50. 50.

    Langwig, K. E. et al. Tradeoffs between mobility and infectiousness in the spatial spread of an emerging pathogen. Preprint at bioRxiv (2020).

    Article  Google Scholar 

  51. 51.

    Wilder, A. P., Kunz, T. H. & Sorenson, M. D. Population genetic structure of a common host predicts the spread of white-nose syndrome, an emerging infectious disease in bats. Mol. Ecol. 24, 5495–5506 (2015).

    PubMed  Google Scholar 

  52. 52.

    Thapa, V. et al. Using a novel partitivirus in Pseudogymnoascus destructans to understand the epidemiology of white-nose syndrome. PLoS Pathog. 12, e1006076 (2016).

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Kovacova, V. et al. White-nose syndrome detected in bats over an extensive area of Russia. BMC Vet. Res. 14, 192 (2018).

    PubMed  PubMed Central  Google Scholar 

  54. 54.

    Holz, P. H., Lumsden, L. F., Marenda, M. S., Browning, G. F. & Hufschmid, J. Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLoS ONE 13, e0204282 (2018).

    PubMed  PubMed Central  Google Scholar 

  55. 55.

    Lilley, T. M. et al. Population connectivity predicts vulnerability to white-nose syndrome in the Chilean myotis (Myotis chiloensis) — a genomics approach. G3 10, 2117–2126 (2020).

    CAS  PubMed  Google Scholar 

  56. 56.

    Holz, P. et al. Does the fungus causing white-nose syndrome pose a significant risk to Australian bats? Wildl. Res. 46, 657–668 (2019).

    Google Scholar 

  57. 57.

    Hoyt, J. R. et al. Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats. EcoHealth 12, 330–333 (2015).

    PubMed  Google Scholar 

  58. 58.

    Lorch, J. M. et al. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl. Environ. Microbiol. 79, 1293–1301 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Campbell, L. J., Walsh, D. P., Blehert, D. S. & Lorch, J. M. Long-term survival of Pseudogymnoascus destructans at elevated temperatures. J. Wildl. Dis. 56, 278–287 (2020).

    PubMed  Google Scholar 

  60. 60.

    Verant, M. L., Boyles, J. G., Waldrep, W. Jr. Wibbelt, G. & Blehert, D. S. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7, e46280 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Langwig, K. E. et al. Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc. R. Soc. B Biol. Sci. 282, 20142335 (2015).

    Google Scholar 

  62. 62.

    O’shea, T. J. et al. Bat flight and zoonotic viruses. Emerg. Infect. Dis. 20, 741 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. 63.

    Perry, R. W. A review of factors affecting cave climates for hibernating bats in temperate North America. Environ. Rev. 21, 28–39 (2013).

    Google Scholar 

  64. 64.

    Webb, P. I., Speakman, J. R. & Racey, P. A. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can. J. Zool. 74, 761–765 (1996).

    Google Scholar 

  65. 65.

    Langwig, K. E. et al. Drivers of variation in species impacts for a multi-host fungal disease of bats. Phil. Trans. R. Soc. B Biol. Sci. (2016).

    Article  Google Scholar 

  66. 66.

    Langwig, K. E. et al. Invasion dynamics of white-nose syndrome fungus, midwestern United States, 2012–2014. Emerg. Infect. Dis. 21, 1023–1026 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Frick, W. F. et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631 (2017).

    PubMed  Google Scholar 

  68. 68.

    Zukal, J. et al. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci. Rep. 6, 19829 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Czenze, Z. J., Jonasson, K. A. & Willis, C. K. Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiol. Biochem. Zool. 90, 502–511 (2017).

    PubMed  Google Scholar 

  70. 70.

    Wilcox, A. et al. Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. Anim. Behav. 88, 157–164 (2014).

    Google Scholar 

  71. 71.

    Meteyer, C. U., Barber, D. & Mandl, J. N. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence 3, 583–588 (2012).

    PubMed  PubMed Central  Google Scholar 

  72. 72.

    Meteyer, C. U. et al. Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome. J. Wildl. Dis. 47, 618–626 (2011).

    PubMed  Google Scholar 

  73. 73.

    Fuller, N. W. et al. Disease recovery in bats affected by white-nose syndrome. J. Exp. Biol. 223, jeb211912 (2020).

    PubMed  Google Scholar 

  74. 74.

    Field, K. A. et al. The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating bats. PLOS Pathog. 11, e1005168 (2015).

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Shelburne, S. A. et al. Immune reconstitution inflammatory syndrome: emergence of a unique syndrome during highly active antiretroviral therapy. Medicine 81, 213–227 (2002).

    PubMed  Google Scholar 

  76. 76.

    Pikula, J. et al. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE 12, e0180435 (2017).

    PubMed  PubMed Central  Google Scholar 

  77. 77.

    Hoyt, J. R. et al. Widespread occurrence of Pseudogymnoascus destructans in northeast China. Emerg. Infect. Dis. 22, 140–142 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Ballmann, A. E., Torkelson, M. R., Bohuski, E. A., Russell, R. E. & Blehert, D. S. Dispersal hazards of Pseudogymnoascus destructans by bats and human activity at hibernacula in summer. J. Wildl. Dis. 53, 725–735 (2017).

    PubMed  Google Scholar 

  79. 79.

    Dobony, C. A. et al. Little brown myotis persist despite exposure to white-nose syndrome. J. Fish Wildl. Manag. 2, 190–195 (2011).

    Google Scholar 

  80. 80.

    Thomas, D. W., Fenton, M. B. & Barclay, R. M. R. Social behavior of the little brown bat, Myotis lucifugus. I. Mating behavior. Behav. Ecol. Sociobiol. 6, 129–136 (1979).

    Google Scholar 

  81. 81.

    Parsons, K. N., Jones, G., Davidson-Watts, I. & Greenaway, F. Swarming of bats at underground sites in Britain — implications for conservation. Biol. Conserv. 111, 63–70 (2003).

    Google Scholar 

  82. 82.

    Jiang, T. et al. Autumn flight activity of the greater horseshoe bat at hibernacula. Anim. Biol. 66, 119–131 (2016).

    Google Scholar 

  83. 83.

    van Schaik, J. et al. Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites. PLoS ONE 10, 1 (2015).

    Google Scholar 

  84. 84.

    Fenton, M. B. Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Can. J. Zool. 47, 597–602 (1969).

    Google Scholar 

  85. 85.

    Kunz, T. H., Wrazen, J. A. & Burnett, C. D. Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5, 8–17 (1998).

    Google Scholar 

  86. 86.

    Hoyt, J. R. et al. Cryptic connections illuminate pathogen transmission within community networks. Nature 563, 710–713 (2018).

    CAS  PubMed  Google Scholar 

  87. 87.

    Reeder, D. M. et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7, e38920 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Jonasson, K. A. & Willis, C. K. R. Hibernation energetics of free-ranging little brown bats. J. Exp. Biol. 215, 2141–2149 (2012).

    PubMed  Google Scholar 

  89. 89.

    Lučan, R. K. et al. Ectoparasites may serve as vectors for the white-nose syndrome fungus. Parasit. Vectors 9, 16 (2016).

    PubMed  PubMed Central  Google Scholar 

  90. 90.

    Hudson, H. J. Fungal Biology (CUP Archive, 1992).

  91. 91.

    Ainsworth, G. Fungal parasites of vertebrates. in Fungal Population: An Advanced Treatise Vol. 211 (Elsevier, 2013).

  92. 92.

    Zhao, Z., Liu, H., Wang, C. & Xu, J. R. Erratum to: comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 15, 6 (2014).

    PubMed  PubMed Central  Google Scholar 

  93. 93.

    Zukal, J. et al. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS ONE 9, e97224 (2014).

    PubMed  PubMed Central  Google Scholar 

  94. 94.

    Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L. & McCracken, G. F. Molecular detection of the causative agent of white-nose syndrome on Rafinesque’s big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the southeastern USA. J. Wildl. Dis. 51, 519–522 (2015).

    PubMed  Google Scholar 

  95. 95.

    Turner, G. G. et al. Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. J. Wildl. Dis. 50, 566–573 (2014).

    PubMed  Google Scholar 

  96. 96.

    USFWS. White-nose syndrome occurrence map - by year. (2020).

  97. 97.

    Wibbelt, G. et al. Skin lesions in European hibernating bats associated with Geomyces destructans, the etiologic agent of white-nose syndrome. PLoS ONE 8, e74105 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 98.

    Bandouchova, H. et al. Alterations in the health of hibernating bats under pathogen pressure. Sci. Rep. 8, 6067 (2018).

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Warnecke, L. et al. Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol. Lett. (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Herreid, C. F. 2nd, Bretz, W. L. & Schmidt-Nielsen, K. Cutaneous gas exchange in bats. Am. J. Physiol. 215, 506–508 (1968).

    PubMed  Google Scholar 

  101. 101.

    Verant, M. L. et al. White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol. 14, 10 (2014).

    PubMed  PubMed Central  Google Scholar 

  102. 102.

    Cryan, P. M., Uphoff Meteyer, C., Boyles, J. G. & Blehert, D. S. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 8, 135 (2010).

    PubMed  PubMed Central  Google Scholar 

  103. 103.

    Mayberry, H. W., McGuire, L. P. & Willis, C. K. Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome. J. Comp. Physiol. B 188, 333–343 (2018).

    CAS  PubMed  Google Scholar 

  104. 104.

    McGuire, L. P., Mayberry, H. W. & Willis, C. K. White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 313, R680–R686 (2017).

    PubMed  PubMed Central  Google Scholar 

  105. 105.

    Brownlee-Bouboulis, S. A. & Reeder, D. M. White-nose syndrome-affected little brown myotis (Myotis lucifugus) increase grooming and other active behaviors during arousals from hibernation. J. Wildl. Dis. (2013).

    Article  PubMed  Google Scholar 

  106. 106.

    Lilley, T. M. et al. White-nose syndrome survivors do not exhibit frequent arousals associated with Pseudogymnoascus destructans infection. Front. Zool. 13, 12 (2016).

    PubMed  PubMed Central  Google Scholar 

  107. 107.

    Carey, C. S. & Boyles, J. G. Interruption to cutaneous gas exchange is not a likely mechanism of WNS-associated death in bats. J. Exp. Biol. 218, 1986–1989 (2015).

    PubMed  Google Scholar 

  108. 108.

    Lilley, T. M. et al. Immune responses in hibernating little brown myotis (Myotis lucifugus) with white-nose syndrome. Proc. R. Soc. B Biol. Sci. 284, 20162232 (2017).

    Google Scholar 

  109. 109.

    Field, K. et al. Anti-fungal immune responses to Pseudogymnoasces destructans in bats affected by white-nose syndrome. J. Immunol. 192 (Suppl. 1), 207.13 (2014).

    Google Scholar 

  110. 110.

    Reeder, S. M. et al. Pseudogymnoascus destructans transcriptome changes during white-nose syndrome infections. Virulence 8, 1695–1707 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Harazim, M. et al. Natural selection in bats with historical exposure to white-nose syndrome. BMC Zool. 3, 8 (2018).

    Google Scholar 

  112. 112.

    Davy, C. M. et al. Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome. Virulence 11, 781–794 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Moore, M. S. et al. Energy conserving thermoregulatory patterns and lower disease severity in a bat resistant to the impacts of white-nose syndrome. J. Comp. Physiol. B 188, 163–176 (2018).

    PubMed  Google Scholar 

  114. 114.

    Field, K. A. et al. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol. Ecol. 27, 3727–3743 (2018).

    CAS  Google Scholar 

  115. 115.

    Johnson, J. S. et al. Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white-nose syndrome. Ecol. Evol. 5, 2203–2014 (2015).

    PubMed  PubMed Central  Google Scholar 

  116. 116.

    Lilley, T. M. et al. Resistance is futile: RNA-sequencing reveals differing responses to bat fungal pathogen in Nearctic Myotis lucifugus and Palearctic Myotis myotis. Oecologia 191, 295–309 (2019).

    PubMed  PubMed Central  Google Scholar 

  117. 117.

    Thogmartin, W. E., King, R. A., McKann, P. C., Szymanski, J. A. & Pruitt, L. Population-level impact of white-nose syndrome on the endangered Indiana bat. J. Mammal. 93, 1086–1098 (2012).

    Google Scholar 

  118. 118.

    Verant, M. L., Meteyer, C. U., Stading, B. & Blehert, D. S. Experimental infection of Tadarida brasiliensis with Pseudogymnoascus destructans, the fungus that causes white-nose syndrome. mSphere 3, e00250-18 (2018).

    PubMed  PubMed Central  Google Scholar 

  119. 119.

    Rodhouse, T. J. et al. Evidence of region-wide bat population decline from long-term monitoring and Bayesian occupancy models with empirically informed priors. Ecol. Evol. 9, 11078–11088 (2019).

    PubMed  PubMed Central  Google Scholar 

  120. 120.

    Marroquin, C. M., Lavine, J. O. & Windstam, S. T. Effect of humidity on development of Pseudogymnoascus destructans, the causal agent of bat white-nose syndrome. Northeast. Nat. 24, 54–64 (2017).

    Google Scholar 

  121. 121.

    Grieneisen, L. E., Brownlee-Bouboulis, S. A., Johnson, J. S. & Reeder, D. M. Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis (Myotis lucifugus). R. Soc. Open Sci. 2, 140470 (2015).

    PubMed  PubMed Central  Google Scholar 

  122. 122.

    Johnson, J. S. et al. Host, pathogen, and environmental characteristics predict white-nose syndrome mortality in captive little brown myotis (Myotis lucifugus). PLoS ONE (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Hayman, D. T., Pulliam, J. R., Marshall, J. C., Cryan, P. M. & Webb, C. T. Environment, host, and fungal traits predict continental-scale white-nose syndrome in bats. Sci. Adv. 2, e1500831 (2016).

    PubMed  PubMed Central  Google Scholar 

  124. 124.

    Verant, M. L. et al. Determinants of Pseudogymnoascus destructans within bat hibernacula: Implications for surveillance and management of white-nose syndrome. J. Appl. Ecol. 55, 820–829 (2018).

    PubMed  PubMed Central  Google Scholar 

  125. 125.

    McGuire, L. P. et al. White-nose syndrome disease severity and a comparison of diagnostic methods. EcoHealth 13, 60–71 (2016).

    PubMed  Google Scholar 

  126. 126.

    Willis, C. K. R., Menzies, A. K., Boyles, J. G. & Wojciechowski, M. S. Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. Integr. Comp. Biol. 51, 364–373 (2011).

    PubMed  Google Scholar 

  127. 127.

    Haase, C. G. et al. Incorporating evaporative water loss into bioenergetic models of hibernation to test for relative influence of host and pathogen traits on white-nose syndrome. PLoS ONE 14, e0222311 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. 128.

    Pannkuk, E. L., Gilmore, D. F., Savary, B. J. & Risch, T. S. Triacylglyceride (TAG) profiles of integumentary lipids isolated from three bat species determined by matrix-assisted laser desorption-ionization time-of-flight mass spectrometry (MALDI-TOF MS). Can. J. Zool. 90, 1117–1127 (2012).

    CAS  Google Scholar 

  129. 129.

    Pannkuk, E. L. et al. Glycerophospholipid profiles of bats with white-nose syndrome. Physiol. Biochem. Zool. 88, 425–432 (2015).

    PubMed  PubMed Central  Google Scholar 

  130. 130.

    Avena, C. V. et al. Deconstructing the bat skin microbiome: influences of the host and the environment. Front. Microbiol. 7, 1753 (2016).

    PubMed  PubMed Central  Google Scholar 

  131. 131.

    Lemieux-Labonté, V., Simard, A., Willis, C. K. & Lapointe, F.-J. Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5, 115 (2017).

    PubMed  PubMed Central  Google Scholar 

  132. 132.

    Ange-Stark, M. A. et al. White-nose syndrome restructures bat skin microbiomes. Preprint at bioRxiv (2019).

    Article  Google Scholar 

  133. 133.

    Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE 10, e0121329 (2015).

    PubMed  PubMed Central  Google Scholar 

  134. 134.

    Moore, M. S. et al. Hibernating little brown myotis (Myotis lucifugus) show variable immunological responses to white-nose syndrome. PLoS ONE 8, e58976 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Rocke, T. E. et al. Virally-vectored vaccine candidates against white-nose syndrome induce anti-fungal immune response in little brown bats (Myotis lucifugus). Sci. Rep. 9, 6788 (2019).

    PubMed  PubMed Central  Google Scholar 

  136. 136.

    Donaldson, M. E. et al. Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white-nose syndrome. Evolut. Appl. 10, 1076–1090 (2017).

    CAS  Google Scholar 

  137. 137.

    Davy, C. M. et al. White-nose syndrome is associated with increased replication of a naturally persisting coronaviruses in bats. Sci. Rep. 8, 15508 (2018).

    PubMed  PubMed Central  Google Scholar 

  138. 138.

    Martínková, N. et al. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence 9, 1734–1750 (2018).

    Google Scholar 

  139. 139.

    Langwig, K. E. et al. Resistance in persisting bat populations after white-nose syndrome invasion. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160044 (2017).

    Google Scholar 

  140. 140.

    Maslo, B., Valent, M., Gumbs, J. F. & Frick, W. F. Conservation implications of ameliorating survival of little brown bats with white-nose syndrome. Ecol. Appl. 25, 1832–1840 (2015).

    PubMed  Google Scholar 

  141. 141.

    Maslo, B. et al. High annual survival in infected wildlife populations may veil a persistent extinction risk from disease. Ecosphere 8, e02001 (2017).

    Google Scholar 

  142. 142.

    Dowling, Z. R. & O’Dell, D. I. Bat use of an island off the coast of Massachusetts. Northeast. Nat. 25, 362–382 (2018).

    Google Scholar 

  143. 143.

    Cheng, T. L. et al. Higher fat stores contribute to persistence of little brown bat populations with white-nose syndrome. J. Anim. Ecol. 88, 591–600 (2019).

    PubMed  Google Scholar 

  144. 144.

    Bohn, S. et al. Evidence of ‘sickness behaviour’ in bats with white-nose syndrome. Behaviour 153, 981–1003 (2016).

    Google Scholar 

  145. 145.

    Raberg, L., Sim, D. & Read, A. F. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812–814 (2007).

    CAS  PubMed  Google Scholar 

  146. 146.

    Auteri, G. G. & Knowles, L. L. Decimated little brown bats show potential for adaptive change. Sci. Rep. 10, 3023 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. 147.

    Gignoux-Wolfsohn, S. A. et al. Genomic signatures of evolutionary rescue in bats surviving white-nose syndrome. Preprint at bioRxiv (2019).

    Article  Google Scholar 

  148. 148.

    Lilley, T. M. et al. Genome-wide changes in genetic diversity in a population of Myotis lucifugus affected by white-nose syndrome. G3 10, 2007–2020 (2020).

    CAS  PubMed  Google Scholar 

  149. 149.

    Shuey, M. M., Drees, K. P., Lindner, D. L., Keim, P. & Foster, J. T. Highly sensitive quantitative PCR for the detection and differentiation of Pseudogymnoascus destructans and other Pseudogymnoascus species. Appl. Environ. Microbiol. 80, 1726–1731 (2014).

    PubMed  PubMed Central  Google Scholar 

  150. 150.

    Muller, L. K. et al. Bat white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. Mycologia 105, 253–259 (2013).

    CAS  PubMed  Google Scholar 

  151. 151.

    Davy, C. M. et al. The other white-nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans. Ecol. Evol. 7, 7161–7170 (2017).

    PubMed  PubMed Central  Google Scholar 

  152. 152.

    Russell, R. E., Thogmartin, W. E., Erickson, R. A., Szymanski, J. & Tinsley, K. Estimating the short-term recovery potential of little brown bats in the eastern United States in the face of white-nose syndrome. Ecol. Model. 314, 111–117 (2015).

    Google Scholar 

  153. 153.

    Fletcher, Q. E., Webber, Q. M. & Willis, C. K. Modelling the potential efficacy of treatments for white-nose syndrome in bats. J. Appl. Ecol. 57, 1283–1291 (2020).

    Google Scholar 

  154. 154.

    Cheng, T. L. et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J. Appl. Ecol. 54, 701–708 (2017).

    Google Scholar 

  155. 155.

    Hoyt, J. R. et al. Field trial of a probiotic bacteria to protect bats from white-nose syndrome. Sci. Rep. 9, 9158 (2019).

    PubMed  PubMed Central  Google Scholar 

  156. 156.

    Cornelison, C., Gabriel, K., Barlament, C. & Crow, S. Jr. Inhibition of Pseudogymnoascus destructans growth from conidia and mycelial extension by bacterially produced volatile organic compounds. Mycopathologia 177, 1–10 (2014).

    CAS  PubMed  Google Scholar 

  157. 157.

    Chaturvedi, S. et al. Antifungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of geomycosis (WNS) in bats. PLoS ONE 6, e17032 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. 158.

    Court, M. H. et al. Pharmacokinetics of terbinafine in little brown myotis (Myotis lucifugus) infected with Pseudogymnoascus destructans. Am. J. Vet. Res. 78, 90–99 (2017).

    CAS  PubMed  Google Scholar 

  159. 159.

    Kilpatrick, A. M. et al. Impact of censusing and research on wildlife populations. Conserv. Sci. Pract. 2, e264 (2020).

    Google Scholar 

  160. 160.

    Weller, T. J. et al. A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management. PLoS ONE 13, e0205647 (2018).

    PubMed  PubMed Central  Google Scholar 

  161. 161.

    Garzoli, L. et al. First isolation of Pseudogymnoascus destructans, the fungal causative agent of white-nose disease, in bats from Italy. Mycopathologia 184, 637–644 (2019).

    CAS  PubMed  Google Scholar 

  162. 162.

    Pavlinić, I., Đaković, M. & Lojkić, I. Pseudogymnoascus destructans in Croatia confirmed. Eur. J. Wildl. Res. 61, 325–328 (2015).

    Google Scholar 

  163. 163.

    das Neves Paiva-Cardoso, M. et al. First isolation of Pseudogymnoascus destructans in bats from Portugal. Eur. J. Wildl. Res. 60, 645–649 (2014).

    Google Scholar 

  164. 164.

    Barlow, A. et al. First confirmation of Pseudogymnoascus destructans in British bats and hibernacula. Vet. Rec. 177, 73–73 (2015).

    CAS  PubMed  Google Scholar 

  165. 165.

    Simonovicova, A., Pangallo, D., Chovanova, K. & Lehotska, B. Geomyces destructans associated with bat disease WNS detected in Slovakia. Biologia 66, 562–564 (2011).

    Google Scholar 

  166. 166.

    Sachanowicz, K., Stępień, A. & Ciechanowski, M. Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland. Cent. Eur. J. Biol. 9, 437–443 (2014).

    Google Scholar 

  167. 167.

    Hayes, M. A. The geomyces fungi: ecology and distribution. Bioscience 62, 819–823 (2012).

    Google Scholar 

  168. 168.

    Kendrick, B. The Fifth Kingdom (Hackett Publishing, 2017).

  169. 169.

    Palmer, J. M. et al. Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white-nose syndrome of bats. G3 4, 1755–1763 (2014).

    PubMed  Google Scholar 

  170. 170.

    Tennessee Wildlife Resources Agency. Tennessee Winter Bat Population and White-nose Syndrome Monitoring Reports (Tennessee Wildlife Resources Agency, 2020).

  171. 171.

    Colatskie, S. Missouri Bat Hibernacula Survey Results of 2011–2017, Following White-Nose Syndrome Arrival (Missouri Department of Conservation, 2017).

  172. 172.

    Graeter, G. Annual Program Report 2008–2009. 110–115 (Wildlife Diversity Program, Division of Wildlife Management, NC Wildlife Resources Commission, 2009).

  173. 173.

    Graeter, G. Annual Program Report 2009–2010. 127–137 (Wildlife Diversity Program, Division of Wildlife Management, NC Wildlife Resources Commission, 2010).

  174. 174.

    Kindel, J. Final Report: White-nose Syndrome Grants to States, F15AC00694 (South Carolina Department of Natural Resources, 2016).

  175. 175.

    Kindel, J. Final Report: White-nose Syndrome Grants to States SC-E-F16AP00833 (South Carolina Department of Natural Resources, 2017).

  176. 176.

    Morris, T. & Ferrall, E. 2019 White-nose Syndrome Season Summary (Wildlife Resources Division, Georgia Department of Natural Resources, 2020).

  177. 177.

    Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).

    PubMed  Google Scholar 

  178. 178.

    Lacki, M. J., Hayes, J. P., Kurta, A. & Tuttle, M. D. Bats in Forests: Conservation and Management (JHU Press, 2007).

  179. 179.

    Miller, K. E. Trophic, habitat, distubance and conservation linkages between bat and aquatic communities in two Connecticut rivers. Doctoral dissertation, Wesleyan University. (2013).

  180. 180.

    Morningstar, D. E., Robinson, C. V., Shokralla, S. & Hajibabaei, M. Interspecific competition in bats and diet shifts in response to white-nose syndrome. Ecosphere 10, e02916 (2019).

    Google Scholar 

  181. 181.

    Jachowski, D. S. et al. Disease and community structure: white-nose syndrome alters spatial and temporal niche partitioning in sympatric bat species. Divers. Distrib. 20, 1002–1015 (2014).

    Google Scholar 

  182. 182.

    Kunz, T. H., de Torrez, E. B., Bauer, D., Lobova, T. & Fleming, T. H. in Year in Ecology and Conservation Biology Vol. 1223 Annals of the New York Academy of Sciences (eds Ostfeld, R. S. & Schlesinger, W. H.) 1–38 (Blackwell Science Publishing, 2011).

  183. 183.

    Maine, J. J. & Boyles, J. G. Bats initiate vital agroecological interactions in corn. Proc. Natl Acad. Sci. (2015).

    Article  PubMed  Google Scholar 

  184. 184.

    Frank, E. G. The Effects of Bat Population Losses on Infant Mortality through Pesticide Use in the US. (PhD thesis, Columbia University, 2016).

  185. 185.

    Wray, A. K. et al. Incidence and taxonomic richness of mosquitoes in the diets of little brown and big brown bats. J. Mammal. 99, 668–674 (2018).

    Google Scholar 

  186. 186.

    Reiskind, M. H. & Wund, M. A. Experimental assessment of the impacts of northern long-eared bats on ovipositing Culex (Diptera: Culicidae) mosquitoes. J. Med. Entomol. 46, 1037–1044 (2009).

    PubMed  PubMed Central  Google Scholar 

  187. 187.

    Clare, E. L. et al. The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability. Mol. Ecol. 23, 3618–3632 (2014).

    PubMed  Google Scholar 

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The authors thank S. Yamada for assistance with data curation, N. Fuller, N. Laggan, A. Grimaudo and J. Reichard for helpful comments on the manuscript, and the US National Science Foundation for funding (DEB-1911853).

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J.R.H. and K.E.L. drafted the original figures. All authors contributed to writing the original draft and to the editing of the revised work.

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Hoyt, J.R., Kilpatrick, A.M. & Langwig, K.E. Ecology and impacts of white-nose syndrome on bats. Nat Rev Microbiol 19, 196–210 (2021).

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