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The extent to which persisting species may fill the functional role of extirpated or declining species has profound implications for the structure of biological communities and ecosystem functioning. In North America, arthropodivorous bats are threatened on a continent‐wide scale by the spread of white‐nose syndrome (WNS), a disease caused by the fungus Pseudogymnoascus destructans. We tested whether bat species that display lower mortality from this disease can partially fill the functional role of other bat species experiencing population declines. Specifically, we performed high‐throughput amplicon sequencing of guano from two generalist predators: the little brown bat (Myotis lucifugus) and big brown bat (Eptesicus fuscus). We then compared changes in prey consumption before versus after population declines related to WNS. Dietary niches contracted for both species after large and abrupt declines in little brown bats and smaller declines in big brown bats, but interspecific dietary overlap did not change. Furthermore, the incidence and taxonomic richness of agricultural pest taxa detected in diet samples decreased following bat population declines. Our results suggest that persisting generalist predators do not necessarily expand their dietary niches following population declines in other predators, providing further evidence that the functional roles of different generalist predators are ecologically distinct. While many bat species are known to function as suppressors of arthropod abundance, including several economically important agricultural pest taxa, the broader ecological consequences of disease‐related bat declines have not been fully assessed in many regions. In our study, we tested whether big brown bats (Eptesicus fuscus), which demonstrate lower mortality from white‐nose syndrome, could potentially fill the ecological role formerly occupied by the more severely affected little brown bat (Myotis lucifugus). Overall, we found that big brown bats did not adopt more of the prey formerly consumed by little brown bats and that the dietary niche overlap between the two bat species did not change over time.

AIM: We investigated the effects of disease on the local abundances and distributions of species at continental scales by examining the impacts of white‐nose syndrome, an infectious disease of hibernating bats, which has recently emerged in North America. LOCATION: North America and Europe. METHODS: We used four decades of population counts from 1108 populations to compare the local abundances of bats in North America before and after the emergence of white‐nose syndrome to the situation in Europe, where the disease is endemic. We also examined the probability of local extinction for six species of hibernating bats in eastern North America and assessed the influence of winter colony size prior to the emergence of white‐nose syndrome on the risk of local extinction. RESULTS: White‐nose syndrome has caused a 10‐fold decrease in the abundance of bats at hibernacula in North America, eliminating large differences in species abundance patterns that existed between Europe and North America prior to disease emergence. White‐nose syndrome has also caused extensive local extinctions (up to 69% of sites in a single species). For five out of six species, the risk of local extinction was lower in larger winter populations, as expected from theory, but for the most affected species, the northern long‐eared bat (Myotis septentrionalis), extinction risk was constant across winter colony sizes, demonstrating that disease can sometimes eliminate numerical rarity as the dominant driver of extinction risk by driving both small and large populations extinct. MAIN CONCLUSIONS: Species interactions, including disease, play an underappreciated role in macroecological patterns and influence broad patterns of species abundance, occurrence and extinction.

Disease dynamics during pathogen invasion and establishment determine the impacts of disease on host populations and determine the mechanisms of host persistence. Temporal progression of prevalence and infection intensity illustrate whether tolerance, resistance, reduced transmission, or demographic compensation allow initially declining populations to persist. We measured infection dynamics of the fungal pathogen Pseudogymnoascus destructans that causes white-nose syndrome in bats by estimating pathogen prevalence and load in seven bat species at 167 hibernacula over a decade as the pathogen invaded, became established, and some host populations stabilized. Fungal loads increased rapidly and prevalence rose to nearly 100% at most sites within 2 yr of invasion in six of seven species. Prevalence and loads did not decline over time despite huge reductions in colony sizes, likely due to an extensive environmental reservoir. However, there was substantial variation in fungal load among sites with persisting colonies, suggesting that both tolerance and resistance developed at different sites in the same species. In contrast, one species disappeared from hibernacula within 3 yr of pathogen invasion. Variable host responses to pathogen invasion require different management strategies to prevent disease-induced extinction and to facilitate evolution of tolerance or resistance in persisting populations.

1. The management of infectious diseases is an important conservation concern for a growing number of wildlife species. However, effective disease control in wildlife is challenging because feasible management options are often lacking. White-nose syndrome (WNS) is an infectious disease of hibernating bats that currently threatens several North American species with extinction. Currently, no effective treatments exist for WNS. 2. We conducted a laboratory experiment to test the efficacy of probiotic treatment with Pseudomonas fluorescens, a bacterium that naturally occurs on bats, to reduce disease severity and improve survival of little brown bats Myotis lucifugus exposed to Pseudogymnoascus destructans, the fungal pathogen that causes WNS. 3. We found that application of the probiotic bacteria at the time of fungal infection reduced several measures of disease severity and increased survival, whereas bacterial treatment prior to pathogen exposure had no effect on survival and worsened disease severity. 4. Synthesis and applications. Our results suggest that probiotic treatment with Ps. fluorescens has potential for white-nose syndrome disease management, but the timing of application is critical and should coincide with natural exposure of bats to P. destructans. These results add to the growing knowledge of how natural host microbiota can be implemented as a biocontrol treatment to influence disease outcomes.

White‐nose syndrome (WNS) has devastated populations of hibernating bats in eastern North America, leading to emergency conservation listings for several species including the previously ubiquitous little brown myotis (Myotis lucifugus). However, some bat populations near the epicenter of the WNS panzootic appear to be stabilizing after initial precipitous declines, which could reflect a selective immunogenetic sweep. To investigate the hypothesis that WNS exerts significant selection on the immunome of affected bat populations, we developed a novel, high‐throughput sequence capture assay targeting 138 adaptive, intrinsic, and innate immunity genes of putative adaptive significance, as well as their respective regulatory regions (~370 kbp of genomic sequence/individual). We used the assay to explore baseline immunogenetic variation in M. lucifugus and to investigate whether particular immune genes/variants are associated with WNS susceptibility. We also used our assay to detect 1,038 putatively neutral single nucleotide polymorphisms and characterize contemporary population structure, providing context for the identification of local immunogenetic adaptation. Sequence capture provided a cost‐effective, “all‐in‐one” assay to test for neutral genetic and immunogenetic structure and revealed fine‐scale, baseline immunogenetic differentiation between sampling sites <600 km apart. We identified functional immunogenetic variants in M. lucifugus associated with WNS susceptibility. This study lays the foundations for future investigations of rangewide immunogenetic adaptation to WNS in M. lucifugus and provides a blueprint for studies of evolutionary rescue in other host–pathogen systems.

Over the past 13 years, White-nose Syndrome (WNS) has caused North American bat population declines and shifted community structure towards species less or unaffected by the disease. Mistnetting, acoustic surveys, and cave count data have been used to document changes in bat presence and activity through site-specific, pre- and post-WNS studies. Management and survey guidance often must be applied at a combined landscape and site-specific scale. Our objective was to explore the relationships among WNS impact, influence of available hibernacula, and environmental factors for the nightly presence of 3 WNS-affected bats: the Indiana bat (Myotis sodalis), northern long-eared bat (M. septentrionalis), and big brown bat (Eptesicus fuscus). We used recordings from 10 acoustic monitoring study areas, each with 3 survey locations across the states of Virginia, West Virginia, Ohio and Kentucky to assess changes in nightly bat presence during the summer of 2017. There were significant positive and negative correlates of broad land-cover categories for presence of all 3 bat species. Our findings also corroborated trends in abundance and distribution patterns found in prior, smaller-scale studies, supporting the relevance of land cover categories in a large-scale acoustic monitoring framework. We observed a negative association between WNS impact-years and nightly northern long-eared bat presence, but low occurrence and patchy distribution reduced our ability to infer strong relationships. Big brown bat presence showed a significant positive relationship with WNS occurrence on the landscape, providing evidence that big brown bats are maintaining populations after years of exposure. Indiana bats were the least-documented species, limiting the strength of our conclusions, but we did observe significant temporal patterns in nightly presence, with higher probabilities of presence earlier in the summer. Our results show the potential efficacy of using a WNS impact metric to predict summer bat presence, inform current U.S. Fish and Wildlife Service acoustic monitoring guidelines, and highlight which environmental variables are relevant for large-scale acoustic monitoring.

Genome‐wide scans for selection have become a popular tool for investigating evolutionary responses in wildlife to emerging diseases. However, genome scans are susceptible to false positives and do little to demonstrate specific mechanisms by which loci impact survival. Linking putatively resistant genotypes to observable phenotypes increases confidence in genome scan results and provides evidence of survival mechanisms that can guide conservation and management efforts. Here we used an expression quantitative trait loci (eQTL) analysis to uncover relationships between gene expression and alleles associated with the survival of little brown bats (Myotis lucifugus) despite infection with the causative agent of white‐nose syndrome. We found that 25 of the 63 single‐nucleotide polymorphisms (SNPs) associated with survival were related to gene expression in wing tissue. The differentially expressed genes have functional annotations associated with the innate immune system, metabolism, circadian rhythms, and the cellular response to stress. In addition, we observed differential expression of multiple genes with survival implications related to loci in linkage disequilibrium with focal SNPs. Together, these findings support the selective function of these loci and suggest that part of the mechanism driving survival may be the alteration of immune and other responses in epithelial tissue.

Disease outcomes result from the interaction between host, pathogen, and environmental factors. Understanding how these components interact to influence spatial and temporal variations in disease severity can enhance our insights into the drivers of disease outbreaks, ultimately improving our ability to mitigate the impact of disease through better forecasts and management actions. White‐nose syndrome (WNS) in bats, caused by the fungal pathogen Pseudogymnoascus destructans (Pd), has been detected in hibernating bats across much of the United States and Canada. This pathogen has led to widespread population declines in some bat species, for example, Myotis lucifugus; however, not all infected populations exhibit similar decreases in numbers. Despite long‐term detection and high infection levels, the population of M. lucifugus that uses Tippy Dam, in northern Michigan, as a hibernaculum has not experienced a decline compared to other populations in the state. To assess local population effects that may contribute to reduced disease severity at Tippy Dam, we brought 30 hibernating M. lucifugus from Tippy Dam and 30 from a geographically similar hibernaculum with a history of declines from WNS into captivity at the U.S. Geological Survey, National Wildlife Health Center. We challenged the bats with a Pd inoculum and monitored survival, pathology, and Pd loads for up to 120 days. This allowed us to remove local environmental effects that could influence WNS disease severity. We observed no effect of source population on either survival or wing damage from Pd infection. Our results suggest that population persistence and lowered disease severity in Tippy Dam are likely driven by local environmental factors found within the dam. As Pd continues to spread westward, understanding environmental factors that influence the severity of Pd infection in hibernating bats has the potential to guide management decisions and help predict the survival of susceptible bat species in the western United States. The study investigates the factors influencing the reduced severity of white‐nose syndrome (WNS) in Myotis lucifugus bats at Tippy Dam, Michigan, despite high infection levels. Through controlled experiments, we show that environmental factors, rather than host adaptation, play a critical role in the bats' long‐term persistence and lower disease severity.

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