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Copper is an essential micronutrient and the ability to scavenge tightly bound or trace levels of copper ions at the host–pathogen interface is vital for fungal proliferation in animal hosts. Recent studies suggest that trace metal ion acquisition is critical for the establishment and propagation of Pseudogymnoascus destructans, the fungal pathogen responsible for white-nose syndrome (WNS), on their bat host. However, little is known about these metal acquisition pathways in P. destructans. In this study, we report the characterization of the P. destructans high-affinity copper transporter VC83_00191 (PdCTR1a), which is implicated as a virulence factor associated with the WNS disease state. Using Saccharomyces cerevisiae as a recombinant expression host, we find that PdCTR1a can efficiently traffic Cu ions into the yeast cytoplasm. Complementary studies in the native P. destructans fungus provide evidence that PdCTR1a transcripts and protein levels are dictated by Cu-bioavailability in the growth media. Our study demonstrates that PdCTR1a is a functional high-affinity copper transporter and is relevant to Cu homeostasis pathways in P. destructans. [ABSTRACT FROM AUTHOR]

Several bat species have experienced rapid population declines in the northern United States and Canada in response to the white-nose syndrome (WNS) epizootic. The pathogen has since spread across the United States, including the Southeast, where relatively warm temperatures may change host–pathogen interactions. In the cave-rich Tennessee–Alabama–Georgia (TAG) region, we examined the impacts of WNS and forest cover on the Tricolored Bat (Perimyotis subflavus) metapopulation using a long-term data set of 832 cave surveys conducted in summer and winter from 2004 to 2022. Most bat colonies were small (<30 individuals), and bats were more likely to be present and abundant in caves surrounded by high percent forest cover, reiterating the importance of forest management for bat conservation. When comparing the years before and after the pathogen arrived in 2010 to 2012, bat presence and abundance during winter hibernation did not change. This stability contrasts with significant declines in other studies, suggesting that Tricolored Bat populations respond differently to WNS in small colonies in the TAG region. Fewer tricolored bats used caves in the summer than during hibernation, but across all years, we observed 1,021 tricolored bats in 121 caves during summer surveys. Unlike stable winter trends, bat presence and abundance declined in the post-WNS period in summer, when cave use is optional. This first broad geographical analysis of summer cave use highlights a potentially important change in bat behavior. Disease surveillance and conservation efforts that target caves with relatively small Tricolored Bat colonies in winter and/or summer may be important for regional population persistence of this threatened species. [ABSTRACT FROM AUTHOR]

ImportanceInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes of Myotis lucifugus and Perimyotis subflavus indicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd.

The emergence of white-nose syndrome (WNS) in North America has resulted in mass mortalities of hibernating bats and total extirpation of local populations. The need to mitigate this disease has stirred a significant body of research to understand its pathogenesis. Pseudogymnoascus destructans, the causative agent of WNS, is a psychrophilic (cold-loving) fungus that resides within the class Leotiomycetes, which contains mainly plant pathogens and is unrelated to other consequential pathogens of animals. In this review, we revisit the unique biology of hibernating bats and P. destructans and provide an updated analysis of the stages and mechanisms of WNS progression. The extreme life history of hibernating bats, the psychrophilic nature of P. destructans, and its evolutionary distance from other well-characterized animal-infecting fungi translate into unique host–pathogen interactions, many of them yet to be discovered. [ABSTRACT FROM AUTHOR]

Emerging infectious diseases threaten wildlife globally. While the effects of infectious diseases on hosts with severe infections and high mortality rates often receive considerable attention, effects on hosts that persist despite infection are less frequently studied. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a persisting species susceptible to infection by the invasive fungal pathogen Pseudogymnoascus destructans (Pd; causative agent for white‐nose syndrome), across the eastern US using a 30‐year dataset. Capture rates of male and female E. fuscus increased from preinvasion to pathogen establishment years, with greater increases to the capture rates of females than males. Among females, capture rates of pregnant and post‐lactating females increased by pathogen establishment. We outline potential mechanisms for these broad demographic changes in E. fuscus capture rates (i.e., increases to foraging from energy deficits created by Pd infection, increases to relative abundance, or changes to reproductive cycles), and suggest future research for identifying mechanisms for increasing capture rates across the eastern US. These data highlight the importance of understanding how populations of persisting host species change following pathogen invasion across a broad spatial scale. Understanding changes to population composition following pathogen invasion can identify broad ecological patterns across space and time, and open new avenues for research to identify drivers of those patterns. [ABSTRACT FROM AUTHOR]

White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has decimated bat populations across North America. Despite ongoing management programs, WNS continues to expand into new populations, including in US states previously thought to be free from the pathogen and disease. This expansion highlights a growing need for surveillance tools that can be used to enhance existing monitoring programs and support the early detection of P. destructans in new areas. We evaluated the feasibility of using a handheld, field-portable, real-time (quantitative) PCR (qPCR) thermocycler known as the Biomeme two3 and the associated field-based nucleic acid extraction kit and assay reagents for the detection of P. destructans in little brown bats (Myotis lucifugus). Results from the field-based protocol using the Biomeme platform were compared with those from a commonly used laboratory-based qPCR protocol. When using dilutions of known conidia concentrations, the lowest detectable concentration with the laboratory-based approach was 108.8 conidia/mL, compared with 1,087.5 conidia/mL (10 times higher, i.e., one fewer 103 dilution) using the field-based approach. Further comparisons using field samples suggest a high level of concordance between the two protocols, with positive and negative agreements of 98.2% and 100% respectively. The cycle threshold values were marginally higher for most samples using the field-based protocol. These results are an important step in establishing and validating a rapid, field-assessable detection platform for P. destructans, which is urgently needed to improve the surveillance and monitoring capacity for WNS and support on-the-ground management and response efforts. [ABSTRACT FROM AUTHOR]

Abstract Emerging infectious diseases threaten wildlife globally. While the effects of infectious diseases on hosts with severe infections and high mortality rates often receive considerable attention, effects on hosts that persist despite infection are less frequently studied. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a persisting species susceptible to infection by the invasive fungal pathogen Pseudogymnoascus destructans (Pd; causative agent for white‐nose syndrome), across the eastern US using a 30‐year dataset. Capture rates of male and female E. fuscus increased from preinvasion to pathogen establishment years, with greater increases to the capture rates of females than males. Among females, capture rates of pregnant and post‐lactating females increased by pathogen establishment. We outline potential mechanisms for these broad demographic changes in E. fuscus capture rates (i.e., increases to foraging from energy deficits created by Pd infection, increases to relative abundance, or changes to reproductive cycles), and suggest future research for identifying mechanisms for increasing capture rates across the eastern US. These data highlight the importance of understanding how populations of persisting host species change following pathogen invasion across a broad spatial scale. Understanding changes to population composition following pathogen invasion can identify broad ecological patterns across space and time, and open new avenues for research to identify drivers of those patterns.

The accessibility to CRISPR/Cas (Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR‐associated protein) genetic tools has given rise to applications beyond site‐directed genome editing for the detection of DNA and RNA. These tools include precise diagnostic detection of human disease pathogens, such as SARS‐CoV‐2 and Zika virus. Despite the technology being rapid and cost‐effective, the use of CRISPR/Cas tools in the surveillance of the causative agents of wildlife diseases has not been prominent. This study presents the development of a minimally invasive, field‐applicable and user‐friendly CRISPR/Cas‐based biosensor for the detection of Pseudogymnoascus destructans (Pd), the causative fungal agent of white‐nose syndrome (WNS), an infectious disease that has killed more than five million bats in North America since its discovery in 2006. The biosensor assay combines a recombinase polymerase amplification (RPA) step followed by CRISPR/Cas12a nuclease cleavage to detect Pd DNA from bat dermal swab and guano samples. The biosensor had similar detection results when compared to quantitative PCR in distinguishing Pd‐positive versus negative field samples. Although bat dermal swabs could be analysed with the biosensor without nucleic acid extraction, DNA extraction was needed when screening guano samples to overcome inhibitors. This assay can be applied to help with more rapid delineation of Pd‐positive sites in the field to inform management decisions. With further optimization, this technology has broad translation potential to wildlife disease‐associated pathogen detection and monitoring applications. [ABSTRACT FROM AUTHOR]

Introduction: Serological tests can be used to test whether an animal has been exposed to an infectious agent, and whether its immune system has recognized and produced antibodies against it. Paired samples taken several weeks apart then document an ongoing infection and/or seroconversion. Methods: In the absence of a commercial kit, we developed an indirect enzymelinked immunosorbent assay (ELISA) to detect the fungus-specific antibodies for Pseudogymnoascus destructans, the agent of white-nose syndrome in bats. Results and Discussion: Samples collected from European Myotis myotis (n=35) and Asian Myotis dasycneme (n=11) in their hibernacula at the end of the hibernation period displayed 100% seroprevalence of antibodies against P. destructans, demonstrating a high rate of exposure. Our results showed that the higher the titre of antibodies against P. destructans, the lower the infection intensity, suggesting that a degree of protection is provided by this arm of adaptive immunity in Palearctic bats. Moreover, P. destructans infection appears to be a seasonally self-limiting disease of Palearctic bats showing seroconversion as the WNS skin lesions heal in the early post-hibernation period. [ABSTRACT FROM AUTHOR]

The skin of animals is enveloped by a symbiotic microscopic ecosystem known as the microbiome. The host and microbiome exhibit a mutualistic relationship, collectively forming a single evolutionary unit sometimes referred to as a holobiont. Although the holobiome theory highlights the importance of the microbiome, little is known about how the skin microbiome contributes to protecting the host. Existing studies focus on humans or captive animals, but research in wild animals is in its infancy. Specifically, the protective role of the skin microbiome in hibernating animals remains almost entirely overlooked. This is surprising, considering the massive population declines in hibernating North American bats caused by the fungal pathogen Pseudogymnoascus destructans, which causes white-nose syndrome. Hibernation offers a unique setting in which to study the function of the microbiome because, during torpor, the host's immune system becomes suppressed, making it susceptible to infection. We conducted a systematic review of peer-reviewed literature on the protective role of the skin microbiome in non-human animals. We selected 230 publications that mentioned pathogen inhibition by microbes residing on the skin of the host animal. We found that the majority of studies were conducted in North America and focused on the bacterial microbiome of amphibians infected by the chytrid fungus. Despite mentioning pathogen inhibition by the skin microbiome, only 30.4% of studies experimentally tested the actual antimicrobial activity of symbionts. Additionally, only 7.8% of all publications studied defensive cutaneous symbionts during hibernation. With this review, we want to highlight the knowledge gap surrounding skin microbiome research in hibernating animals. For instance, research looking to mitigate the effects of white-nose syndrome in bats should focus on the antifungal microbiome of Palearctic bats, as they survive exposure to the Pseudogymnoascus destructans -pathogen during hibernation. We also recommend future studies prioritize lesser-known microbial symbionts, such as fungi, and investigate the effects of a combination of anti-pathogen microbes, as both areas of research show promise as probiotic treatments. By incorporating the protective skin microbiome into disease mitigation strategies, conservation efforts can be made more effective. [ABSTRACT FROM AUTHOR]

Infectious diseases are powerful ecological forces structuring ecosystems, causing devastating economic impacts and disrupting society. Successful prevention and control of pathogens requires knowledge of the current scope and severity of disease, as well as the ability to forecast future disease dynamics. Assessment of the current situation as well as prediction of the future conditions, rely on spatially referenced information regarding the presence or absence of a pathogen, and the prevalence of the pathogen in the population. In particular, knowledge about the location of the disease front is foundational for deploying disease countermeasures to prevent further disease spread and focusing control efforts to reduce disease intensity in affected areas. In this paper, we develop a model-based approach to designing sampling strategies for wildlife disease surveillance at the disease front. Specifically, we use a mechanistic spatio-temporal model based on an underlying partial differential equation to track the disease dynamics and predict the disease prevalence in the future. We also devise an optimal surveillance system design at the disease front that takes into account the practical constraints of sampling. We evaluate the effectiveness of our proposed design via a simulation study and demonstrate the application of the proposed approach by designing a surveillance strategy for the pathogen that causes white-nose syndrome. [ABSTRACT FROM AUTHOR]

ABSTRACT Skin acts as a mechanical barrier between the body and its surrounding environment and plays an important role in resistance to pathogens. However, we still know little regarding skin responses to physiological changes, particularly with regard to responses against potential pathogens. We herein executed RNA-seq on the wing of the Rhinolophus ferrumequinum to assess gene-expression variations at four physiological stages: pre-hibernation, hibernation (early-hibernation and late-hibernation), and post-hibernation, as well as the gene-expression patterns of infected and uninfected bats with the Pseudogymnoascus destructans (Pd). Our results showed that a greater number of differentially expressed genes between the more disparate physiological stages. Functional enrichment analysis showed that the down-regulated response pathways in hibernating bats included phosphorus metabolism and immune response, indicating metabolic suppression and decreased whole immune function. We also found up-regulated genes in post-hibernating bats that included C-type lectin receptor signalling, Toll-like receptor signalling pathway, and cell adhesion, suggesting that the immune response and skin integrity of the wing were improved after bats emerged from their hibernation and that this facilitated clearing Pd from the integument. Additionally, we found that the genes involved in cytokine or chemokine activity were up-regulated in late-hibernation compared to early-hibernation and that FOSB regulation of immune cell activation was differentially expressed in bats infected with Pd during late-hibernation, implying that the host’s innate immune function was enhanced during late-hibernation so as to resist pathogenic infection. Our findings highlight the concept that maintenance of intrinsic immunity provides protection against pathogenic infections in highly resistant bats.

Since the emergence of White-nose Syndrome, a fungal disease in bats, caused by Pseudogymnoascus destructans, hibernating populations of little brown bats (Myotis lucifugus) have declined by 70-90% within P. destructans positive hibernacula. To reduce the impact of White-nose Syndrome to North American little brown bat populations we evaluated if exposure to volatile organic compounds produced by induced cells from Rhodococcus rhodochrous strain DAP96253 could improve the overwinter survival of bats infected by P. destructans. Two simultaneous field treatment trials were conducted at natural hibernacula located in Rockcastle and Breckinridge counties, Kentucky, USA. A combined total of 120 little brown bats were randomly divided into control groups (n = 60) which were not exposed to volatile organic compounds and treatment groups (n = 60) which were exposed to volatile organic compounds produced by non-growth, fermented cell paste composed of R. rhodochrous strain DAP96253 cells. Cox proportional hazard models revealed a significant decreased survival at the Rockcastle field trial site but not the Breckinridge field site. At the Breckinridge hibernacula, overwinter survival for both treatment and control groups were 60%. At the Rockcastle hibernacula, Kaplan-Meier survival curves indicated significantly increased overwinter survival of bats in the control group (43% survived) compared to the treatment group (20% survived). Although complete inhibition of P. destructans by volatile organic compounds produced by induced R. rhodochrous strain DAP96253 cells was observed in vitro studies, our results suggest that these volatile organic compounds do not inhibit P. destructans in situ and may promote P. destructans growth. [ABSTRACT FROM AUTHOR]

Infectious diseases caused by invasive, environmentally persistent fungal pathogens have increasingly endangered global biodiversity, yet disease management remains a major conservation challenge. A prominent example is white‐nose syndrome (WNS), a disease caused by the invasive fungal pathogen Pseudogymnoascus destructans (Pd) that has devastated populations of multiple North American bat species, but for which few effective management tools exist. Here, we propose that strategies to delay environmental transmission of Pd during early winter could limit WNS disease effects across winter, benefitting bats. We used a small captive experiment and a multi‐year field trial on wild, free‐ranging bats to assess an environmental control strategy to manage Pd within its environmental reservoir in Pennsylvania, USA, where the pathogen has become endemic. The strategy centers on the application of Polyethylene Glycol 8000 (PEG) to roost substrates in summer, prior to bat hibernation, as a means to disrupt environmental transmission to bats in early winter. In the captive experiment, environmental transmission of Pd to immunologically naïve little brown myotis (Myotis lucifugus) occurred from roost substrates inoculated with Pd, but the application of PEG to these substrates effectively blocked this transmission. In the field trial, Pd load and infection extent both declined substantially in free‐ranging M. lucifugus after treatment relative to controls, with declines exceeding effects of inter‐site and inter‐annual variation. Pathogen prevalence and load also declined substantially after PEG treatment in big brown bats (Eptesicus fuscus). No negative effects of PEG treatment were observed in body condition or colony counts of bats or in the microbial community. Together, these results are consistent with effective environmental control of Pd and reduced WNS disease effects in bats within contaminated hibernacula. The results also highlight the potential of carefully designed environmental control strategies for managing environmentally persistent pathogens. [ABSTRACT FROM AUTHOR]

The patterns of recovery from injury or infection are not well studied in free-ranging animals. Bats that survive the fungal disease white-nose syndrome (WNS) often emerge from hibernation suffering from skin infections and wing damage. The extent of wing damage reflects physiological and immunological responses to WNS and may impact the ability of bats to fly, forage, and reproduce. Here, we built on previous studies of wing damage in both captive and free-ranging bats to better understand the patterns and extent of wing damage healing in little brown bats (Myotis lucifugus) post-hibernation. We quantified two main types of wing damage, black necrotic dots and white spots, and used the extent of damage to assign bats 1 of 6 wing damage scores. We found that the patterns of black dots and white spots on wing membranes of free-ranging bats aligned with the patterns observed in captive bats soon after emergence from hibernation. Black dot extent was highest at the beginning of the active season in May, while white spot extent peaked 3–4 weeks later. Our study also extends our knowledge of wing damage healing throughout the active season. Wing scores of bats recaptured within the summer decreased or stayed the same and >95% had negligible signs of wing damage by August. We found that black dots were more indicative of disease status than other types of wing damage and could be consistently quantified in the field and from photographs by multiple observers. These results suggest that black dots and our wing damage scoring system can be used to better understand the patterns of post-hibernation healing in little brown bats impacted by WNS. [ABSTRACT FROM AUTHOR]

Environmental pathogen reservoirs exist for many globally important diseases and can fuel epidemics, influence pathogen evolution, and increase the threat of host extinction. Species composition can be an important factor that shapes reservoir dynamics and ultimately determines the outcome of a disease outbreak. However, disease-induced mortality can change species communities, indicating that species responsible for environmental reservoir maintenance may change over time. Here we examine the reservoir dynamics of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats. We quantified changes in pathogen shedding, infection prevalence and intensity, host abundance, and the subsequent propagule pressure imposed by each species over time. We find that highly shedding species are important during pathogen invasion, but contribute less over time to environmental contamination as they also suffer the greatest declines. Less infected species remain more abundant, resulting in equivalent or higher propagule pressure. More broadly, we demonstrate that high infection intensity and subsequent mortality during disease progression can reduce the contributions of high-shedding species to long-term pathogen maintenance. [ABSTRACT FROM AUTHOR]

Since the emergence of White-nose Syndrome, a fungal disease in bats, caused by Pseudogymnoascus destructans, hibernating populations of little brown bats (Myotis lucifugus) have declined by 70–90% within P. destructans positive hibernacula. To reduce the impact of White-nose Syndrome to North American little brown bat populations we evaluated if exposure to volatile organic compounds produced by induced cells from Rhodococcus rhodochrous strain DAP96253 could improve the overwinter survival of bats infected by P. destructans. Two simultaneous field treatment trials were conducted at natural hibernacula located in Rockcastle and Breckinridge counties, Kentucky, USA. A combined total of 120 little brown bats were randomly divided into control groups (n = 60) which were not exposed to volatile organic compounds and treatment groups (n = 60) which were exposed to volatile organic compounds produced by non-growth, fermented cell paste composed of R. rhodochrous strain DAP96253 cells. Cox proportional hazard models revealed a significant decreased survival at the Rockcastle field trial site but not the Breckinridge field site. At the Breckinridge hibernacula, overwinter survival for both treatment and control groups were 60%. At the Rockcastle hibernacula, Kaplan-Meier survival curves indicated significantly increased overwinter survival of bats in the control group (43% survived) compared to the treatment group (20% survived). Although complete inhibition of P. destructans by volatile organic compounds produced by induced R. rhodochrous strain DAP96253 cells was observed in vitro studies, our results suggest that these volatile organic compounds do not inhibit P. destructans in situ and may promote P. destructans growth.

Skin microbiota play an important role in protecting bat hosts from the fungal pathogen Pseudogymnoascus destructans, which has caused dramatic bat population declines and extinctions. Recent studies have provided insights into the bacterial communities of bat skin, but variation in skin bacterial community structure in the context of the seasonal dynamics of fungal invasion, as well as the processes that drive such variation, remain largely unexplored. In this study, we characterized bat skin microbiota over the course of the bat hibernation and active season stages and used a neutral model of community ecology to determine the relative roles of neutral and selective processes in driving microbial community variation. Our results showed significant seasonal shifts in skin community structure, as well as less diverse microbiota in hibernation than in the active season. Skin microbiota were influenced by the environmental bacterial reservoir. During both the hibernation and active season stages, more than 78% of ASVs in bat skin microbiota were consistent with neutral distribution, implying that neutral processes, that is, dispersal or ecological drift contributing the most to shifts in skin microbiota. In addition, the neutral model showed that some ASVs were actively selected by the bats from the environmental bacterial reservoir, accounting for approximately 20% and 31% of the total community during hibernation and active season stages, respectively. Overall, this research provides insights into the assemblage of bat‐associated bacterial communities and will aid in the development of conservation strategies against fungal disease. [ABSTRACT FROM AUTHOR]

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

White‐nose syndrome is a fungal disease that is threatening bat populations across North America. The disease primarily affects cave‐hibernating bats by depleting fat reserves during hibernation and causing a range of other physiological consequences when immune responses are suppressed. Since it was first detected in 2006, the disease has killed millions of bats and is responsible for extensive local extinctions. To better understand the effects of white‐nose syndrome on various bat species, we analyzed summer acoustic survey data collected from 2016 to 2020 at nine US National Parks within the Great Lakes region. We examined the effect that white‐nose syndrome, time of the year relative to pup volancy, habitat type, and regional variation (i.e., park) have on the acoustic abundance (i.e., mean call abundance) of six bat species. As expected, little brown bat (Myotis lucifugus) and northern long‐eared bat (Myotis septentrionalis), both hibernating species, experienced a significant decline in acoustic abundance following white‐nose syndrome detection. We observed a significant increase in acoustic abundance as white‐nose syndrome progressed for hoary bats (Lasiurus cinereus) and silver‐haired bats (Lasionycteris noctivagans), both migratory species that are not impacted by the disease. Contrary to our predictions, we observed an increase in big brown bat (Eptesicus fuscus; hibernating) acoustic abundance and a decrease in eastern red bat (Lasiurus borealis; migratory) acoustic abundance following the detection of white‐nose syndrome. We did not observe any significant changes after the onset of white‐nose syndrome in the seasonal patterns of acoustic activity related to pup volancy, suggesting that production or recruitment of young may not be affected by the disease. Our results suggest that white‐nose syndrome is affecting the acoustic abundance of certain species; however, these changes may not be a result of reduced reproductive success caused by the disease. In addition, species population dynamics may be indirectly affected by white‐nose syndrome as a result of reduced competition or a foraging niche release. We also found that for parks located at higher latitudes, little brown bat and northern long‐eared bat were more likely to experience greater declines in acoustic abundance as a result of white‐nose syndrome. Our work provides insight into species‐specific responses to white‐nose syndrome at a regional scale and examines factors that may facilitate resistance or resiliency to the disease. [ABSTRACT FROM AUTHOR]

Bats can be affected by fungal pathogens such as Pseudogymnoascus destructans, the causative agent of the white-nose syndrome. Their body surface can also be colonized by fungal commensals or carry transient fungal species and participate in their dispersal. In this study, 114 bat specimens belonging to seven species were sampled from various locations in northern Belgium. Culture-based methods revealed an important mycological diversity, with a total of 209 different taxa out of the 418 isolates. Overall, a mean of 3.7 taxa per bat was recorded, but significant differences were observed between sampling sites and seasons. The mycobiomes were dominated by cosmopolitan and plant-associated species, in particular from the genera Cladosporium, Penicillium, and Aspergillus. Other species known to be related to bats or their environment, such as Apiotrichum otae, were also retrieved. Sampling of hibernacula indicated that diverse fungal species can inhabit these sites, including a yet undescribed Pseudogymnoascus species, distinct from Ps. destructans, namely, Ps. cavicola. [ABSTRACT FROM AUTHOR]

Understanding how host-associated microbial assemblages respond to pathogen invasion has implications for host health. Until recently, most investigations have focused on understanding the taxonomic composition of these assemblages. However, recent studies have suggested that microbial assemblage taxonomic composition is decoupled from its function, with assemblages being taxonomically varied but functionally constrained. The objective of this investigation was to understand how the Tri-colored bat, Perimyotis subflavus cutaneous microbial assemblage responds to fungal pathogen invasion within a functional context. We hypothesized that at a broad scale (e.g., KEGG pathways), there will be no difference in the functional assemblages between the white nose pathogen, Pseudogymnoascus destructans, positive and negative bats; and this pattern will be driven by the functional redundancy of bacterial taxa. At finer scales (e.g., gene models), we postulate differences in function attributed to interactions between bacteria and P. destructans, resulting in the production of antifungal metabolites. To test this, we used a combination of shotgun metagenomic and amplicon sequencing to characterize the bat cutaneous microbial assemblage in the presence/absence of P. destructans. Results showed that while there was a shift in taxonomic assemblage composition between P. destructans positive and negative bats, there was little overall difference in microbial function. Functional redundancy across bacterial taxa was clear at a broad-scale; however, both redundancy and variation in bacterial capability related to defense against pathogens was evident at finer scales. While functionality of the microbial assemblage was largely conserved in relation to P. destructans, the roles of particular functional pathways in resistance to fungal pathogens require further attention. [ABSTRACT FROM AUTHOR]

Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.

Emerging infectious diseases have caused population declines and biodiversity loss. The ability of pathogens to survive in the environment, independent of their host, can exacerbate disease impacts and increase the likelihood of species extinction. Control of pathogens with environmental stages remains a significant challenge for conservation and effective management strategies are urgently needed.We examined the effectiveness of managing environmental exposure to reduce the impacts of an emerging infectious disease of bats, white‐nose syndrome (WNS). We used a chemical disinfectant, chlorine dioxide (ClO2), to experimentally reduce Pseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We combined laboratory experiments with 3 years of field trials at four abandoned mines to determine whether ClO2 could effectively remove P. destructans from the environment, reduce host infection and limit population impacts.ClO2 was effective at killing P. destructans in vitro across multiple concentrations. In field settings, higher concentrations of ClO2 treatment were needed to sufficiently reduce viable P. destructans conidia in the environment.The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was also higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus).Synthesis and applications. Our results highlight that targeted management of sources for environmental transmission can be an effective control strategy for wildlife disease. We found that successfully reducing pathogen in the environment decreased disease severity and increased survival, but required higher treatment exposure than was effective in laboratory experiments, and the effects varied among species. More broadly, our findings have implications for other emerging wildlife diseases with free‐living pathogen stages by highlighting how the degree of environmental contamination can have cascading impacts on hosts, presenting an opportunity for intervention. [ABSTRACT FROM AUTHOR]

Surveillance programmes are essential for detecting emerging pathogens and often rely on molecular methods to make inference about the presence of a target disease agent. However, molecular methods rarely detect target DNA perfectly. For example, molecular pathogen detection methods can result in misclassification (i.e. false positives and false negatives) or partial detection errors (i.e. detections with 'ambiguous', 'uncertain' or 'equivocal' results). Then, when data are to be analysed, these partial observations are either discarded or censored; this, however, disregards information that could be used to make inference about the true state of the system. There is a critical need for more direction and guidance related to how many samples are enough to declare a unit of interest 'pathogen free'.Here, we develop a Bayesian hierarchal framework that accommodates false negative, false positive and uncertain detections to improve inference related to the occupancy of a pathogen. We apply our modelling framework to a case study of the fungal pathogen Pseudogymnoascus destructans (Pd) identified in Texas bats at the invasion front of white‐nose syndrome. To improve future surveillance programmes, we provide guidance on sample sizes required to be 95% certain a target organism is absent from a site.We found that the presence of uncertain detections increased the variability of resulting posterior probability distributions of pathogen occurrence, and that our estimates of required sample size were very sensitive to prior information about pathogen occupancy, pathogen prevalence and diagnostic test specificity. In the Pd case study, we found that the posterior probability of occupancy was very low in 2018, but occupancy probability approached 1 in 2020, reflecting increasing prior probabilities of occupancy and prevalence elicited from the site manager.Our modelling framework provides the user a posterior probability distribution of pathogen occurrence, which allows for subjective interpretation by the decision‐maker. To help readers apply and use the methods we developed, we provide an interactive RShiny app that generates target species occupancy estimation and sample size estimates to make these methods more accessible to the scientific community (https://rmummah.shinyapps.io/ambigDetect%5fsampleSize). This modelling framework and sample size guide may be useful for improving inferences from molecular surveillance data about emerging pathogens, non‐native invasive species and endangered species where misclassifications and ambiguous detections occur. [ABSTRACT FROM AUTHOR]

Pathogens with persistent environmental stages can have devastating effects on wildlife communities. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in bat populations of North America. In 2009, during the early stages of the WNS investigation and before molecular techniques had been developed to readily detect P. destructans in environmental samples, we initiated this study to assess whether P. destructans can persist in the hibernaculum environment in the absence of its conclusive bat host and cause infections in naive bats. We transferred little brown bats (Myotis lucifugus) from an unaffected winter colony in northwest Wisconsin to two P. destructans contaminated hibernacula in Vermont where native bats had been excluded. Infection with P. destructans was apparent on some bats within 8 weeks following the introduction of unexposed bats to these environments, and mortality from WNS was confirmed by histopathology at both sites 14 weeks following introduction. These results indicate that environmental exposure to P. destructans is sufficient to cause the infection and mortality associated with WNS in naive bats, which increases the probability of winter colony extirpation and complicates conservation efforts. [ABSTRACT FROM AUTHOR]

Abstract White‐nose syndrome is a fungal disease that is threatening bat populations across North America. The disease primarily affects cave‐hibernating bats by depleting fat reserves during hibernation and causing a range of other physiological consequences when immune responses are suppressed. Since it was first detected in 2006, the disease has killed millions of bats and is responsible for extensive local extinctions. To better understand the effects of white‐nose syndrome on various bat species, we analyzed summer acoustic survey data collected from 2016 to 2020 at nine US National Parks within the Great Lakes region. We examined the effect that white‐nose syndrome, time of the year relative to pup volancy, habitat type, and regional variation (i.e., park) have on the acoustic abundance (i.e., mean call abundance) of six bat species. As expected, little brown bat (Myotis lucifugus) and northern long‐eared bat (Myotis septentrionalis), both hibernating species, experienced a significant decline in acoustic abundance following white‐nose syndrome detection. We observed a significant increase in acoustic abundance as white‐nose syndrome progressed for hoary bats (Lasiurus cinereus) and silver‐haired bats (Lasionycteris noctivagans), both migratory species that are not impacted by the disease. Contrary to our predictions, we observed an increase in big brown bat (Eptesicus fuscus; hibernating) acoustic abundance and a decrease in eastern red bat (Lasiurus borealis; migratory) acoustic abundance following the detection of white‐nose syndrome. We did not observe any significant changes after the onset of white‐nose syndrome in the seasonal patterns of acoustic activity related to pup volancy, suggesting that production or recruitment of young may not be affected by the disease. Our results suggest that white‐nose syndrome is affecting the acoustic abundance of certain species; however, these changes may not be a result of reduced reproductive success caused by the disease. In addition, species population dynamics may be indirectly affected by white‐nose syndrome as a result of reduced competition or a foraging niche release. We also found that for parks located at higher latitudes, little brown bat and northern long‐eared bat were more likely to experience greater declines in acoustic abundance as a result of white‐nose syndrome. Our work provides insight into species‐specific responses to white‐nose syndrome at a regional scale and examines factors that may facilitate resistance or resiliency to the disease.

Background: North American bat populations have suffered severe declines over the last decade due to the Pseudogymnoascus destructans fungus infection. The skin disease associated with this causative agent, known as white-nose syndrome (WNS), is specific to bats hibernating in temperate regions. As cultured fungal isolates are required for epidemiological and phylogeographical studies, the purpose of the present work was to compare the efficacy and reliability of different culture approaches based on either skin swabs or wing membrane tissue biopsies for obtaining viable fungal isolates of P. destructans. Results: In total, we collected and analysed 69 fungal and 65 bacterial skin swabs and 51 wing membrane tissue biopsies from three bat species in the Czech Republic, Poland and the Republic of Armenia. From these, we obtained 12 viable P. destructans culture isolates. Conclusions: Our results indicated that the efficacy of cultures based on wing membrane biopsies were significantly higher. Cultivable samples tended to be based on collections from bats with lower body surface temperature and higher counts of UV-visualised lesions. While cultures based on both skin swabs and wing membrane tissue biopsies can be utilised for monitoring and surveillance of P. destructans in bat populations, wing membrane biopsies guided by UV light for skin lesions proved higher efficacy. Interactions between bacteria on the host's skin also appear to play an important role. [ABSTRACT FROM AUTHOR]

Pseudogymnoascus is a psychrophilic fungus, which is a genus widely distributed in cold regions around the world. Recently, the presence of Pseudogymnoascus destructans (Pd), the causative agent of white-nose syndrome (WNS) belonging to Pseudogymnoascus, has been reported in neighboring countries of Korea. However, no investigation on Pd has been reported in Korea. In this study, cave-inhabiting bats and their habitats were investigated in terms of the diversity of cave fungi, and we tried to confirm the presence of Pd. Three caves suspected of hosting Pd were selected, and 83 environmental and 53 bat samples were collected. A total of 154 fungal strains belonging to 31 different genera were isolated, and 20 of 154 were confirmed to belong to Pseudogymnoascus. Pd-diagnostic PCR was performed to check whether Pd was present in the isolated Pseudogymnoascus, and seven positives were confirmed. However, phylogenetic analyses revealed that no isolates belonged or were closely related to the clade with Pd. Although samples were collected from limited areas, undescribed Pseudogymnoascus species were isolated, and it was confirmed that Korean isolates were distributed in various clades. In conclusion, it is hypothesized that Korean Pseudogymnoascus presents high diversity. [ABSTRACT FROM AUTHOR]

Invasive pathogens threaten wildlife health and biodiversity. Physiological responses of species highly susceptible to pathogen infections following invasion are well described. However, the responses of less susceptible species (relative to highly susceptible species) are not well known. Latitudinal gradients, which can influence body condition via Bergmann's rule and/or reflect the time it takes for an introduced pathogen to spread geographically, add an additional layer for how mammalian species respond to pathogen exposure. Our goal was to understand how hosts less susceptible to pathogen infections respond to long‐term pathogen exposure across a broad latitudinal gradient. We examined changes in body mass throughout pathogen exposure time across the eastern United States (latitude ranging 30.5° N–44.8° N) in Eptesicus fuscus, a bat species classified as less susceptible to infection (relative to highly susceptible species) by the invasive fungal pathogen that causes white‐nose syndrome, Pseudogymnoascus destructans (Pd). Using 30 years of spring through fall adult capture records, we created linear mixed‐effects models for female and male bats to determine how mass or mass variation changed across the eastern United States from pre‐Pd invasion years through Pd invasion (0–1 years with Pd), epidemic (2–4 years with Pd), and established years (5+ years with Pd). By Pd establishment, all female and male bats decreased body mass with increasing latitude across a spatial threshold at 39.6° N. Differences in bat mass north and south of the spatial threshold progressively increased over Pd exposure time‐steps such that body mass was lower in northern latitudes compared to southern latitudes by Pd establishment. Results indicated that the progressive differences in E. fuscus body mass with latitude across the eastern United States are due to long‐term pathogen exposure; however, other environmental and ecological pressures may contribute to decreases in E. fuscus body mass with latitude and long‐term pathogen exposure. As pathogen introductions and emerging infectious diseases become more prevalent on the landscape, it is imperative that we understand how less susceptible species directly and indirectly respond to long‐term pathogen exposure in order to maintain population health in surviving species. [ABSTRACT FROM AUTHOR]

Pseudogymnoascus destructans (= Geomyces destructans) is a psychrophilic filamentous fungus that causes White-Nose Disease (WND; the disease associated with White-Nose Syndrome, WNS) in hibernating bats. The disease has caused considerable reductions in bat populations in the USA and Canada since 2006. Identification and detection of the pathogen in pure cultures and environmental samples is routinely based on qPCR or PCR after DNA isolation and purification. Rapid and specific direct detection of the fungus in the field would strongly improve prompt surveillance, and support control measures. Based on the genes coding for ATP citrate lyase1 (acl1) and the 28S-18S ribosomal RNA intergenic spacer (IGS) in P. destructans, two independent LAMP assays were developed for the rapid and sensitive diagnosis of the fungus. Both assays could discriminate P. destructans from 159 tested species of filamentous fungi and yeasts. Sensitivity of the assays was 2.1 picogram per reaction (pg/rxn) and 21 femtogram per reaction (fg/rxn) for the acl1 and IGS based assays, respectively. Moreover, both assays also work with spores and mycelia of P. destructans that are directly added to the master mix without prior DNA extraction. For field-diagnostics, we developed and tested a field-applicable version of the IGS-based LAMP assay. Lastly, we also developed a protocol for preparation of fungal spores and mycelia from swabs and tape liftings of contaminated surfaces or infected bats. This protocol in combination with the highly sensitive IGS-based LAMP-assay enabled sensitive detection of P. destructans from various sources. [ABSTRACT FROM AUTHOR]

Pseudogymnoascus destructans is a fungal pathogen responsible for a deadly disease among North American bats known as white-nose syndrome (WNS). Since detection of WNS in the United States in 2006, its rapid spread and high mortality has challenged development of treatment and prevention methods, a significant objective for wildlife management agencies. In an effort to mitigate precipitous declines in bat populations due to WNS, we have developed and implemented a multi-year mitigation strategy at Black Diamond Tunnel (BDT), Georgia, singly known as one of the most substantial winter colony sites for tricolored bats (Perimyotis subflavus), with pre-WNS abundance exceeding 5000 individuals. Our mitigation approach involved in situ treatment of bats at the colony level through aerosol distribution of antifungal volatile organic compounds (VOCs) that demonstrated an in vitro ability to inhibit P. destructans conidia germination and mycelial growth through contact-independent exposure. The VOCs evaluated have been identified from microbes inhabiting naturally-occurring fungistatic soils and endophytic fungi. These VOCs are of low toxicity to mammals and have been observed to elicit antagonism of P. destructans at low gaseous concentrations. Cumulatively, our observations resolved no detrimental impact on bat behavior or health, yet indicated a potential for attenuation of WNS related declines at BDT and demonstrated the feasibility of this novel disease management approach. [ABSTRACT FROM AUTHOR]

Abstract Invasive pathogens threaten wildlife health and biodiversity. Physiological responses of species highly susceptible to pathogen infections following invasion are well described. However, the responses of less susceptible species (relative to highly susceptible species) are not well known. Latitudinal gradients, which can influence body condition via Bergmann's rule and/or reflect the time it takes for an introduced pathogen to spread geographically, add an additional layer for how mammalian species respond to pathogen exposure. Our goal was to understand how hosts less susceptible to pathogen infections respond to long‐term pathogen exposure across a broad latitudinal gradient. We examined changes in body mass throughout pathogen exposure time across the eastern United States (latitude ranging 30.5° N–44.8° N) in Eptesicus fuscus, a bat species classified as less susceptible to infection (relative to highly susceptible species) by the invasive fungal pathogen that causes white‐nose syndrome, Pseudogymnoascus destructans (Pd). Using 30 years of spring through fall adult capture records, we created linear mixed‐effects models for female and male bats to determine how mass or mass variation changed across the eastern United States from pre‐Pd invasion years through Pd invasion (0–1 years with Pd), epidemic (2–4 years with Pd), and established years (5+ years with Pd). By Pd establishment, all female and male bats decreased body mass with increasing latitude across a spatial threshold at 39.6° N. Differences in bat mass north and south of the spatial threshold progressively increased over Pd exposure time‐steps such that body mass was lower in northern latitudes compared to southern latitudes by Pd establishment. Results indicated that the progressive differences in E. fuscus body mass with latitude across the eastern United States are due to long‐term pathogen exposure; however, other environmental and ecological pressures may contribute to decreases in E. fuscus body mass with latitude and long‐term pathogen exposure. As pathogen introductions and emerging infectious diseases become more prevalent on the landscape, it is imperative that we understand how less susceptible species directly and indirectly respond to long‐term pathogen exposure in order to maintain population health in surviving species.

White‐nose syndrome has been decimating populations of several bat species since its first occurrence in the Northeastern United States in the winter 2006–2007. The spread of the disease has been monitored across the continent through the collaboration of many organizations. Inferring the rate of spread of the disease and predicting its arrival at new locations is critical when assessing the current and predicting the future status and trends of bat species. We developed a model of disease spread that simultaneously achieves high‐predictive performance, computational efficiency, and interpretability. We modeled white‐nose syndrome spread using Gaussian process variations to infer the spread rate of the disease front, identify areas of anomalous time of arrival, and provide future forecasts of the expected time of arrival throughout North America. Cross‐validation of model predictive performance identified a stationary Gaussian process without an additional residual error process as the best‐supported model. Results indicated that white‐nose syndrome is likely to spread throughout the entire continental United States by 2030. These annually updatable model predictions will be useful in determining the horizon over which disease management actions must take place as well as in status and trend assessments of disease‐affected bats. [ABSTRACT FROM AUTHOR]

Since its introduction to North America, white‐nose syndrome has been associated with declines greater than 90% in several bat species, prompting the development of treatments to reduce disease‐related mortality. As treatment application is scaled up, predicting responses at the population level will help in the development of management plans.We develop a model allowing for the implementation of multiple treatment scenarios in bat populations at risk of severe mortality from white‐nose syndrome. Our model allows for variation in over 10 parameters, including effectiveness of treatment, treatment‐related disturbance, number of individuals treated, number of hibernacula treated, herd immunity and movement among hibernacula. Additionally, the model allows treatments to be applied to individuals, the hibernaculum or a combination of the two. We simulated treatments for populations of 1000, 10,000 and 100,000 individuals, with the distribution of individuals within hibernacula based on field surveys of Myotis lucifugus.When treatments are applied to individuals, we found that treatment success was most influenced by the number of bats effectively treated, the magnitude of disturbance and the year of first treatment relative to initial mortality. For treatments applied to hibernacula, we found year of first treatment relative to initial mortality, magnitude of disturbance and effectiveness of treatment to be the best predictors of success.Treatments have the potential to mitigate white‐nose syndrome‐related mortality, but application of treatments after initial mass mortality seems to be of limited benefit. Unknowns surrounding influential treatment parameters, such as disturbance to hibernating bats, created substantial variation across outcomes and highlight the importance of obtaining field estimates of parameters associated with treatments.Synthesis and applications: While treatment applications can increase survival from white‐nose syndrome, their potential is strongly diminished when not applied before or during the early epidemic stages. Once the disease is established, increasing survival and reproduction through methods other than disease treatments could be a better option. In the United States, most areas yet to reach the late epidemic or established stage are in the west where bats do not aggregate in large colonies and treating a substantial number of individuals will be difficult. [ABSTRACT FROM AUTHOR]

White-nose syndrome (WNS), caused by Pseudogymnoascus destructans (Pd), is a lethal fungal disease that affects hibernating bats in North America. Recently, the presence of Pd was reported in countries neighboring Korea. However, Pd has not been investigated in Korea. Therefore, this study aimed to identify the presence of Pd in Korean bats. Altogether, wings from 241 bats were collected from 13 cities and cultured. A total of 79 fungal colonies were isolated, and two isolates were identified as Pd using polymerase chain reaction. Of the nine bat species captured in 13 cities, Pd was isolated only from Myotis petax in Goryeong. Atypical, curved conidia were observed in two isolated fungal colonies. Although histological lesions were not observed by hematoxylin and eosin or periodic acid–Schiff staining, fungal invasion was observed in the tissue sections. Taken together, these results confirmed the presence of Pd in Korean bats and suggest the possibility of WNS outbreaks in Korean bats. This is the first report of the isolation and molecular analysis of Pd from Korean bats. [ABSTRACT FROM AUTHOR]

The role of the skin microbiome in resistance and susceptibility of wildlife to fungal pathogens has been examined from a taxonomic perspective but skin microbial function, in the context of fungal infection, has yet to be studied. Our objective was to understand effects of a bat fungal pathogen site infection status and course of invasion on skin microbial function. We sampled seven hibernating colonies of Myotis lucifugus covering three-time points over the course of Pseudogymnoascus destructans (Pd) invasion and white nose syndrome (pre-invasion, epidemic, and established). Our results support three new hypotheses about Pd and skin functional microbiome: (1) there is an important effect of Pd invasion stage, especially at the epidemic stage; (2) disruption by the fungus at the epidemic stage could decrease anti-fungal functions with potential negative effects on the microbiome and bat health; (3) the collection site might have a larger influence on microbiomes at the pre-invasion stage rather than at epidemic and established stages. Future studies with larger sample sizes and using meta-omics approaches will help confirm these hypotheses, and determine the influence of the microbiome on wildlife survival to fungal disease., (© The Author(s) 2024. Published by Oxford University Press on behalf of FEMS.)

White-nose syndrome (WNS), a disease affecting hibernating bats, is caused by the fungal pathogen Pseudogymnoascus destructans (Pd). Since the initial introduction of Pd from Eurasia to the United States in 2006, WNS has killed millions of bats throughout the temperate parts of North America. There is concern that if Pd is accidentally introduced to the Southern Hemisphere, WNS could pose similar threats to the bat fauna of the Southern Hemisphere's more temperate regions. Efforts are required to better understand the vulnerability of bats globally to WNS. We examined phylogenetic distances among cave roosting bat species globally to estimate the probability of infection by Pd. We predicted cave thermal suitability for Pd for 441 cave-roosting bat species across the globe via spatial analysis. We used host specificity models based on 65 species tested for Pd to determine phylogenetic specificity of Pd. Phylogenetic distance was not an important predictor of Pd infection, confirming that Pd has low host specificity. We found extensive areas (i.e., South America, Africa, and Australia) in the Southern Hemisphere with caves that were suitable for cave-roosting bat species and for Pd growth. Hence, if Pd spreads to the Southern Hemisphere, the risk of exposure is widespread for cave-roosting bats, and infection is possible regardless of relatedness to infected species in the Northern Hemisphere. Predicting the consequences of infection remains difficult due to lack of species-specific information about bat winter biology. Nevertheless, WNS is an important threat to naive Southern Hemisphere bat populations. Hence, biosecurity measures and planning of management responses that can help prevent or minimize a potential WNS outbreak in the Southern Hemisphere are urgently needed., (© 2024 The Author(s). Conservation Biology published by Wiley Periodicals LLC on behalf of Society for Conservation Biology.)

Abstract White‐nose syndrome (WNS) has decimated hibernating bat populations across eastern and central North America for over a decade. Disease severity is driven by the interaction between bat characteristics, the cold‐loving fungal agent, and the hibernation environment. While we further improve hibernation energetics models, we have yet to examine how spatial heterogeneity in host traits is linked to survival in this disease system. Here, we develop predictive spatial models of body mass for the little brown myotis (Myotis lucifugus) and reassess previous definitions of the duration of hibernation of this species. Using data from published literature, public databases, local experts, and our own fieldwork, we fit a series of generalized linear models with hypothesized abiotic drivers to create distribution‐wide predictions of prehibernation body fat and hibernation duration. Our results provide improved estimations of hibernation duration and identify a scaling relationship between body mass and body fat; this relationship allows for the first continuous estimates of prehibernation body mass and fat across the species' distribution. We used these results to inform a hibernation energetic model to create spatially varying fat use estimates for M. lucifugus. These results predict WNS mortality of M. lucifugus populations in western North America may be comparable to the substantial die‐off observed in eastern and central populations.

Abstract White‐nose syndrome has been decimating populations of several bat species since its first occurrence in the Northeastern United States in the winter 2006–2007. The spread of the disease has been monitored across the continent through the collaboration of many organizations. Inferring the rate of spread of the disease and predicting its arrival at new locations is critical when assessing the current and predicting the future status and trends of bat species. We developed a model of disease spread that simultaneously achieves high‐predictive performance, computational efficiency, and interpretability. We modeled white‐nose syndrome spread using Gaussian process variations to infer the spread rate of the disease front, identify areas of anomalous time of arrival, and provide future forecasts of the expected time of arrival throughout North America. Cross‐validation of model predictive performance identified a stationary Gaussian process without an additional residual error process as the best‐supported model. Results indicated that white‐nose syndrome is likely to spread throughout the entire continental United States by 2030. These annually updatable model predictions will be useful in determining the horizon over which disease management actions must take place as well as in status and trend assessments of disease‐affected bats.

Temperature is a critically important factor in many infectious disease systems, because it can regulate responses in both the host and the pathogen. White-nose syndrome (WNS) in bats is a severe infectious disease caused by the temperature-sensitive fungus, Pseudogymnoascus destructans (Pd). One feature of WNS is an increase in the frequency of arousal bouts (i.e. when bat body temperatures are elevated) in Pd-infected bats during hibernation. While several studies have proposed that increased frequency of arousals may play a role in the pathophysiology of WNS, it is unknown if the temperature fluctuations might mediate Pd growth. We hypothesized that exposure to a high frequency of elevated temperatures would reduce Pd growth due to thermal constraints on the pathogen. We simulated the thermal conditions for arousal bouts of uninfected and infected bats during hibernation (fluctuating from 8 to 25°C at two different rates) and quantified Pd growth in vitro. We found that increased exposure to high temperatures significantly reduced Pd growth. Because temperature is one of the most critical abiotic factors mediating host–pathogen interactions, resolving how Pd responds to fluctuating temperatures will provide insights for understanding WNS in bats and other fungal diseases.

White-nose syndrome (WNS) is an emerging fungal epizootic disease that has caused large-scale mortality in several species of North American bats. The fungus that causes WNS, Pseudogymnoascus destructans (Pd), has also been detected in bat species without diagnostic signs of WNS. Although these species could play a role in WNS spread, understanding of the spatial and temporal extents of Pd occurrence on WNS-resistant species is limited. This study evaluated the presence of Pd on 272 individuals of three species of migratory tree-roosting bats: hoary (Lasiurus cinereus), eastern red (Lasiurus borealis), and silver-haired (Lasionycteris noctivagans) bats, obtained opportunistically during summer and autumn from throughout much of their ranges in North America. We also compared tissue sampling protocols (i.e., tissue swabbing, fur swabbing, and DNA extraction of excised wing tissue). We detected Pd on three eastern red bats from Illinois and Ohio, US, one silver-haired bat from West Virginia, US, and one hoary bat from New York, US, all via DNA extracted from wing tissue of carcasses. These results document the first publicly reported detections of Pd on a hoary bat and on migratory bats during the autumn migratory period, and demonstrate the potential for using carcasses salvaged at wind-energy facilities to monitor for Pd. [ABSTRACT FROM AUTHOR]

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

White-nose syndrome (WNS) is caused by the fungus Pseudogymnoascus destructans and has led to the deaths of millions of North American bats since it was first documented in New York in 2006. Since the first cases were recorded, WNS has spread rapidly across North America and is now confirmed or suspected in 40 US states and seven Canadian provinces. Often, the presence of P. destructans is detected in a cave or hibernaculum before signs of WNS manifest in the resident bat population, making presence of the fungus a more reliable assessment of potential epidemic spread than expansion of manifested WNS. An analysis of 43 cave internal climates across the state of Texas revealed a pattern of thermal suitability for P. destructans that correlated significantly with landscape (elevation, lithology) and external climate (mean surface temperature and precipitation). We generated a predictive model to assess the potential spread of P. destructans through Texas karst systems based on external features that correlate with suitable internal climates for fungal growth. Applications of this model to external climatic variables from 2019 showed seasonally varying patterns of suitability for fungal growth in select regions of Texas karst systems. Results from these surveys and models showed that internal climates of Texas caves are likely able to sustain the growth of P. destructans and could cause disease and resulting declines in Texas bats, and act as stepping-stones for the fungus, allowing it to travel southward into Mexican and Central American cave systems. The resulting work will inform researchers and natural resource managers of areas of significant concern to monitor for the spread of WNS. [ABSTRACT FROM AUTHOR]

Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat (Myotis lucifugus) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans, which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting populations than in declining populations where the fungus has recently invaded. Fitted models indicate that this is most consistent with a reduction in the growth rate of the pathogen when fungal loads become high. The data are inconsistent with the evolution of tolerance or an overall reduced pathogen growth rate that might be caused by environmental factors. The existence of resistance in some persisting populations of little brown bats offers a glimmer of hope that a precipitously declining species will persist in the face of this deadly pathogen.This article is part of the themed issue Human influences on evolution, and the ecological and societal consequences.

White‐nose syndrome (WNS), a catastrophic fungal disease of hibernating bats, is perpetuated by environmental reservoirs of the fungal pathogen, Pseudogymnoascus destructans. Surviving bats clear infection each summer but are re‐infected upon return to the hibernaculum. Therefore, addressing environmental reservoirs is critical for managing WNS. Ultraviolet (UV) light is known to kill P. destructans in the lab, and whole‐room UV sanitization is a common practice in many commercial settings. However, effective UV treatment at the hibernaculum scale has yet to be confirmed. Importantly, existing standard practices likely require modification for implementation in hibernation sites. Prior to field testing, confirming the ability of UV sanitizers to treat the complex topography of hibernacula, as well as quantifying the effects of such topography on effective treatment times is necessary. Here we use a laboratory setting to investigate the feasibility of whole‐room UV‐C sanitization in treating environmental reservoirs of P. destructans. All trials resulted in mean fungal reductions of 97.3% (range: 91.9‐99.7%) relative to controls. To prepare for future implementation within a hibernaculum, we quantified the effect of distance, emission angle, and incidence angle on UV‐C irradiance delivered to target locations. From these data, we calculated treatment times required for killing P. destructans at the scale of a natural setting. Measurable UV‐C irradiance extended to a maximum distance of 21.3 m. Angles of emission and incidence both reduced irradiance; however, we conclude that ~325 m3 of surface volume could be treated in <2 h. Taken together, UV‐C sanitization may provide a feasible, scalable, and relatively ecologically benign method of reducing P. destructans populations. [ABSTRACT FROM AUTHOR]

White-nose syndrome (WNS) is a disease among hibernating North American bats caused by the psychrophilic fungus Pseudogymnoascus destructans. Since its discovery in New York state, US, in 2006, and as of 2020, WNS has rapidly spread to 34 American states and seven Canadian provinces, causing precipitous declines of native bat populations across North America. The rapid spread of this fungal pathogen has been facilitated by the social behavior of bats, as well as the ability of subterranean hibernacula to support a favorable environment for P. destructans, and is probably exacerbated by anthropogenic transmission events. Although many bat species roost in natural cave environments, bats also selectively use diverse structures for hibernacula. Certain areas of the US lack caves, forcing bats to select different winter roosting environments. Bats have been observed using roadway-associated structures, such as bridges and culverts, for roosting, especially in regions that lack natural cave environments. However, the potential for P. destructans transmission in such roadway-associated structures requires further investigation. Understanding potential pathogen transmission in these widely used anthropogenic structures is crucial to disease management and preventing further declines of imperiled bat populations. Our study investigated these structures as potential pathogen transmission corridors by surveying the use of these structures by Perimyotis subflavus and other susceptible bat populations and by measuring their temperature. The results suggest the environments of roadway-associated culverts are thermally conducive to the proliferation of P. destructans—even in regions with mild winters—and the development of WNS in susceptible bat populations. It is apparent these roadway-associated structures have the potential to spread P. destructans and exacerbate the effect of WNS on susceptible bat populations. [ABSTRACT FROM AUTHOR]

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Copyright of Western North American Naturalist is the property of Monte L. Bean Life Science Museum and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)