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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.

Emerging infectious diseases are a key threat to wildlife. Several fungal skin pathogens have recently emerged and caused widespread mortality in several vertebrate groups, including amphibians, bats, rattlesnakes and humans. White-nose syndrome, caused by the fungal skin pathogen Pseudogymnoascus destructans, threatens several hibernating bat species with extinction and there are few effective treatment strategies. The skin microbiome is increasingly understood to play a large role in determining disease outcome. We isolated bacteria from the skin of four bat species, and co-cultured these isolates with P. destructans to identify bacteria that might inhibit or kill P. destructans. We then conducted two reciprocal challenge experiments in vitro with six bacterial isolates (all in the genus Pseudomonas) to quantify the effect of these bacteria on the growth of P. destructans. All six Pseudomonas isolates significantly inhibited growth of P. destructans compared to non-inhibitory control bacteria, and two isolates performed significantly better than others in suppressing P. destructans growth for at least 35 days. In both challenge experiments, the extent of suppression of P. destructans growth was dependent on the initial concentration of P. destructans and the initial concentration of the bacterial isolate. These results show that bacteria found naturally occurring on bats can inhibit the growth of P. destructans in vitro and should be studied further as a possible probiotic to protect bats from white-nose syndrome. In addition, the presence of these bacteria may influence disease outcomes among individuals, populations, and species.

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

Hibernating bats have undergone severe recent declines across the eastern United States, but the cause of these regional-scale declines has not been systematically evaluated. We assessed the influence of white-nose syndrome (an emerging bat disease caused by the fungus Pseudogymnoascus destructans, formerly Geomyces destructans) on large-scale, long-term population patterns in the little brown myotis (Myotis lucifugus), the northern myotis (Myotis septentrionalis), and the tricolored bat (Perimyotis subflavus). We modeled population trajectories for each species on the basis of an extensive data set of winter hibernacula counts of more than 1 million individual bats from a 4-state region over 13 years and with data on locations of hibernacula and first detections of white-nose syndrome at each hibernaculum. We used generalized additive mixed models to determine population change relative to expectations, that is, how population trajectories differed with a colony's infection status, how trajectories differed with distance from the point of introduction of white-nose syndrome, and whether declines were concordant with first local observation of the disease. Population trajectories in all species met at least one of the 3 expectations, but none met all 3. Our results suggest, therefore, that white-nose syndrome has affected regional populations differently than was previously understood and has not been the sole cause of declines. Specifically, our results suggest that in some areas and species, threats other than white-nose syndrome are also contributing to population declines, declines linked to white-nose syndrome have spread across large geographic areas with unexpected speed, and the disease or other threats led to declines in bat populations for years prior to disease detection. Effective conservation will require further research to mitigate impacts of white-nose syndrome, renewed attention to other threats to bats, and improved surveillance efforts to ensure early detection of white-nose syndrome. Los murciélagos que hibernan ban experimentado declinaciones severas recientes a lo largo del este de los Estados Unidos pero la causa de estas declinaciones a escala regional no ha sido evaluada sistemáticamente. Valoramos la influencia del síndrome de nariz blanca (una enfermedad emergente de los murciélagos causada por el hongo Pseudogymnoascus destructans, antes Geomyces destructans) en el myotis café (Myotis lucifugs), el myotis del norte (M. septentrionalis) y el murciélago tricolor (Perimyotis subflavus). Modelamos las trayectorias poblacionales para cada especie con base en un conjunto extenso de datos de conteos de sitios de hibernación de más de un millón de murciélagos individuales en una región de cuatro estados durante más de 13 años y con datos sobre las localidades de los sitios de hibernación y las primeras detecciones del síndrome de nariz blanca en cada sitio de hibernación. Usamos modelos aditivos mixtos generalizados para determinar el cambio poblacional en relación a las expectativas, es decir, cómo las trayectorias poblacionales difirieron con el estado de infección de una colonia, cómo difirieron con la distancia desde el punto de introducción del síndrome de nariz blanca y si las declinaciones fueron concordantes con la primera observación local de la enfermedad. Las trayectorias poblacionales de todas las especies cumplieron con al menos una de las tres expectativas, pero ninguna cumplió con las tres. Nuestros resultados sugieren que el síndrome de nariz blanca ha afectado a las poblaciones regionales de maneras diferentes a como se entendía previamente y no ha sido la causa única de las declinaciones. Específicamente, nuestros resultados sugieren que en algunas áreas y en algunas especies, otras amenazas además del síndrome de nariz blanca también están contribuyendo a las declinaciones poblacionales, que las declinaciones conectadas al síndrome de nariz blanca se han esparcido en extensas áreas geográficas con una velocidad inesperada, y que la enfermedad y otras amenazas resultaron en declinaciones de la población de murciélagos durante años previos a la detección. La conservación efectiva requerirá de una investigación más profunda para mitigar los impactos del síndrome de nariz blanca, de una atención renovada a las otras amenazas y de esfuerzos mejorados de vigilancia para asegurar la detección temprana del síndrome de nariz blanca.

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.

The disease white-nose syndrome (WNS) has caused widespread decline of North American bat species. Species like little brown myotis (Myotis lucifugus) have received more attention than others, such as northern myotis (Myotis septentrionalis). We were concerned that management decisions based on the demographic condition of little brown myotis may be inappropriate for northern myotis due to the potential for variation in species-specific responses to WNS. We therefore compiled capture data from Canada’s Maritime provinces collected between 2003 and 2019 to identify if disparate population trends exist between the 2 species. We identified a decline in northern myotis capture-per-unit-effort (CPUE) after the detection of WNS (hereafter, post-WNS), in each study region and a divergence from the historic CPUE ratio between the 2 species. Whereas 380 northern myotis were captured pre-WNS, only 4 were captured post-WNS. The pre-WNS ratio of northern myotis to little brown myotis CPUE in New Brunswick, Prince Edward Island, and Nova Scotia declined from 0.541, 0.273, and 0.291 to 0.046, 0, and 0 respectively, post-WNS. Our results indicate that northern myotis populations in the Maritimes have experienced a serious decline. Standardized and systematic capture surveys should be conducted at summer roosting areas and swarming sites in combination with counts in hibernacula to clarify the current distribution, population size, and resource selection patterns of northern myotis.

Confirming presence and distribution of a species is necessary for effective conservation. However, obtaining robust occupancy estimates and confidently identifying factors important to occupancy may be difficult for rare and elusive species. Further, in surveys to assess presence, false-positive detections bias results; however, false-positive occupancy models can resolve this bias and, thus, better support conservation. We assessed the performance of false-positive versus standard occupancy models and important factors predicting presence for a low-density bat population in the southern Appalachian Mountains. From May to August 2013–2015, we surveyed 35 sites for northern long-eared bats (Myotis septentrionalis) using both mist-net and acoustic methods. We compared AICcvalues for 13 standard occupancy models and 13 corresponding false-positive occupancy models. In our model comparison, false-positive models received more support, while none of the standard occupancy models were plausible. False-positive occupancy models produced a wider range of probability of occupancy estimates (0.004–0.998) and lower mean occupancy estimate (0.62) than standard models (0.482–0.970, mean = 0.86). Weighted parameter estimates for important predictors in two plausible false-positive occupancy models indicated the probability of occupancy for northern long-eared bats was higher at less-rugged, lowerelevation sites. In contrast, there was more ambiguity regarding the most plausible standard occupancy models and important predictors of occupancy from standard models. Due to low capture rates and the uncertainty of acoustic identifications, we recommend coupling a certain method with uncertain methods when surveying rare and elusive bat species. Applying false-positive occupancy models to our data yielded less-biased site-specific occupancy estimates and informative predictors, and, hence, more reliable predictions to inform conservation management plans.

The decline in northern myotis ( Myotis septentrionalis ) populations due to the disease white-nose syndrome (WNS) has led to the species receiving federal protection in the United States and Canada, requiring conservation of critical habitats. However, considerably more is known about summer habitat preferences of northern myotis compared to late summer through winter. Our goal was to describe the seasonal presence and habitat use of a remnant colony of northern myotis in central Pennsylvania. We radio-tagged 31 northern myotis and established 6 acoustic monitoring stations to document activity from 2017–2021. We found that roost trees used during the maternity season by reproductive females were occupied by bats during both summer (21 June–14 August) and autumn (15 August–31 October), indicating similar habitat use patterns between seasons. During this time, both males and females preferred to roost in dead and declining trees. No other variable influenced male use, but females also preferred trees located close to water and in forest stands with higher basal area than randomly located trees. Northern myotis with active transmitters never left the study area and were tracked to roosts until early November. During October and November, a female and male were tracked to an underground network of air-filled voids (the Milieu Souterrain Superficiel) we presume to be a hibernaculum. Northern myotis calls were recorded outside this roost between March and October, and bats were observed emerging from this roost during spring and autumn but not summer. Acoustic activity at this site exhibited a seasonal pattern that differed from acoustic activity near roost trees and foraging areas, with a peak of activity during late summer when northern myotis are known to swarm. These data show that northern myotis maternity roosts are used extensively outside of summer and may be vulnerable to forestry practices that occur even outside of the pup-rearing season. These data also support the growing evidence that some northern myotis hibernate outside of caves and mines.

Sensitivity of bats to land use change depends on their foraging ecology, which varies among species based on ecomorphological traits. Additionally, because prey availability, vegetative clutter, and temperature change throughout the year, some species may display seasonal shifts in their nocturnal habitat use. In the Coastal Plain of South Carolina, USA, the northern long-eared bat (Myotis septentrionalis), southeastern myotis (Myotis austroriparius), tri-colored bat (Perimyotis subflavus), and northern yellow bat (Lasiurus intermedius) are species of conservation concern that are threatened by habitat loss. Our objective was to identify characteristics of habitat used by these species during their nightly active period and compare use between summer and winter. We conducted acoustic surveys at 125 sites during May–August and at 121 of the same 125 sites December–March 2018 and 2019 in upland forests, bottomland forests, fields, ponds, and salt marsh and used occupancy models to assess habitat use. The northern long-eared bat and southeastern myotis (i.e., myotis bats) used sites that were closer to hardwood stands, pine stands, and fresh water year-round. We did not identify any strong predictors of tri-colored bat habitat use in summer, but during winter they used bottomland forests, fields, and ponds more than salt marsh and upland forests. During summer and winter, northern yellow bats used sites close to fresh water and salt marsh. Additionally, during summer they used fields, ponds, and salt marsh more than upland and bottomland forests, but in winter they used bottomland forests, fields, and ponds more than upland forest and salt marsh. Our results highlight important land cover types for bats in this area (e.g., bottomland forests, ponds, and salt marsh), and that habitat use changes between seasons. Accounting for and understanding how habitat use changes throughout the year will inform managers about how critical habitat features may vary in their importance to bats throughout the year.

Aim White‐nose syndrome has caused severe declines in eastern North American cave bats, leading to the federal listing of the northern long‐eared bat (Myotis septentrionalis) as endangered in the United States and Canada. This has heightened the importance of long‐term monitoring to inform species status assessments. We employed a combination of long‐term repeated and single‐season acoustic survey data to assess the regional presence, spatial distribution, occupancy, and detection probability of northern long‐eared bats. Location New England, United States. Methods We analysed acoustic data from 2357 detector sites, aggregated by year, using Bayesian single‐species occupancy models. We investigated the influence of habitat characteristics, climatic variables, and year (2015–2022) on occupancy and the effects of weather conditions and survey month (May to August) on detection probability. Spatial random effects were included to address residual spatial autocorrelation, with a 1‐km resolution chosen based on significant positive autocorrelation observed in a non‐spatial model. Results Occupancy was highest on steep, forested hillsides with minimal anthropogenic development, higher in warmer regions, particularly along coastlines and on offshore islands, and declined across survey years. Including a 1‐km spatial random effect reduced residual autocorrelation and suggests northern long‐eared bats utilise resources at small to medium landscape scales. Detection probability was highest earlier in the maternity season, but declined when monthly precipitation or temperature exceeded average conditions. Conclusions Conservation efforts that focus on steep, forested hillsides in warmer regions with low anthropogenic development could be beneficial. Our analysis supports the use of spatial random effects at a 1‐km2 scale, highlighting the importance of survey designs that capture ecological variation at species‐specific resolutions. Additionally, early‐season acoustic surveys conducted during favourable weather conditions may improve monitoring effectiveness. Acoustic sampling and spatial occupancy modelling offer powerful tools for monitoring remnant populations of northern long‐eared bats and guiding conservation practices.