Long-Term Exposure to an Invasive Fungal Pathogen Decreases Eptesicus fuscus Body Mass With Increasing Latitude

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\u27s 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

Seasonal roost selection and activity of a remnant population of northern myotis in Pennsylvania

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 puprearing season. These data also support the growing evidence that some northern myotis hibernate outside of caves and mines

Cooling of bat hibernacula to mitigate white-nose syndrome

Fungal diseases increasingly threaten wildlife with extinction. White-nose syndrome (WNS) is a fungal disease that has caused precipitous declines in several North American bat species, creating an urgent need for conservation. We sought to determine how microclimates and other characteristics of hibernacula have affected bat populations following WNS-associated declines. We also evaluated whether cooling of warm, little-used hibernacula could benefit bats. We found that winter counts of Myotis lucifugus were higher and increased over time in colder hibernacula (with mid-winter temperatures of 3–6°C). Counts of Eptesicus fuscus, M. leibii, and M. septentrionalis were likewise higher in colder hibernacula. Populations of M. lucifugus and M. septentrionalis increased most over time where there were more nearby sites, while E. fuscus counts remained high where they had been high before WNS onset. Winter counts were also higher in M. leibii in hibernacula with higher vapor pressure deficit (VPD) (particularly where > ∼0.1 kPa), and we found some evidence that M. lucifugus increased and E. fuscus counts were higher with higher VPD. In contrast, Perimyotis subflavus counts increased over time in warmer hibernacula and were unaffected by VPD. Separately, at manipulated sites, we achieved cooling of an average of 2.1°C. Within manipulated hibernacula, counts of M. lucifugus and P. subflavus increased with time since manipulation. Further, there were more E. fuscus where cooling was greatest, with some evidence for more P. subflavus in hibernacula sections that remained warm after manipulation. These data show bats are responding effectively to WNS through habitat selection. In M. lucifugus, M. septentrionalis, and possibly P. subflavus, this response is ongoing, with bats increasingly aggregating at suitable hibernacula, while E. fuscus bats remain in previously favored sites. Finally, our results suggest that cooling warm sites receiving little use by bats is a viable strategy for combating WNS.White-nose syndrome (WNS) is a fungal disease that has caused precipitous declines in several North American bat species, creating an urgent need for conservation. We examined how microclimates and other characteristics of hibernacula have affected bat populations following WNS-associated declines and evaluated whether cooling of warm, little-used hibernacula could benefit bats. During the period following mass mortality (2013-2020), we conducted 191 winter surveys of 25 unmanipulated hibernacula and 6 manipulated hibernacula across Pennsylvania (USA). We joined these data with additional datasets on historical (pre-WNS) bat counts and on the spatial distribution of underground sites. We used generalized linear mixed models and model selection to identify factors affecting bat populations. Winter counts of Myotis lucifugus were higher and increased over time in colder hibernacula (those with midwinter temperatures of 3-6 degrees C) compared with warmer (7-11 degrees C) hibernacula. Counts of Eptesicus fuscus, Myotis leibii, and Myotis septentrionalis were likewise higher in colder hibernacula (temperature effects = -0.73 [SE 0.15], -0.51 [0.18], and -0.97 [0.28], respectively). Populations of M. lucifugus and M. septentrionalis increased most over time in hibernacula surrounded by more nearby sites, whereas Eptesicus fuscus counts remained high where they had been high before WNS onset (pre-WNS high count effect = 0.59 [0.22]). Winter counts of M. leibii were higher in hibernacula with high vapor pressure deficits (VPDs) (particularly over 0.1 kPa) compared with sites with lower VPDs (VPD effect = 15.3 [4.6]). Counts of M. lucifugus and E. fuscus also appeared higher where VPD was higher. In contrast, Perimyotis subflavus counts increased over time in relatively warm hibernacula and were unaffected by VPD. Where we manipulated hibernacula, we achieved cooling of on average 2.1 degrees C. At manipulated hibernacula, counts of M. lucifugus and P. subflavus increased over time (years since manipulation effect = 0.70 [0.28] and 0.51 [0.15], respectively). Further, there were more E. fuscus where cooling was greatest (temperature difference effect = -0.46 [SE 0.11]), and there was some evidence there were more P. subflavus in hibernacula sections that remained warm after manipulation. These data show bats are responding effectively to WNS through habitat selection. In M. lucifugus, M. septentrionalis, and possibly P. subflavus, this response is ongoing, with bats increasingly aggregating at suitable hibernacula, whereas E. fuscus remain in previously favored sites. Our results suggest that cooling warm sites receiving little use by bats is a viable strategy for combating WNS.Peer reviewe

Long-term spring through fall capture data of Eptesicus fuscus in the eastern USA before and after white-nose syndrome

Emerging infectious diseases threaten wildlife populations. Without well monitored wildlife systems, it is challenging to determine accurate population and ecosystem losses following disease emergence. North American temperate bats present a unique opportunity for studying the broad impacts of wildlife disease emergence, as their federal monitoring programs were prioritized in the USA throughout the 20th century and they are currently threatened by the invasive fungal pathogen, Pseudogymnoascus destructans (Pd), which causes white-nose syndrome. Here we provide a long-term dataset for capture records of Eptesicus fuscus (big brown bat) across the eastern USA, spanning 16 years before and 14 years after Pd invasion into North America. These data represent 30,496 E. fuscus captures across 3,567 unique sites. We encourage the use of this dataset for quantifying impacts of wildlife disease and other threats to wildlife (e.g., climate change) with the incorporation of other available data. We welcome additional data contributions for E. fuscus captures across North and Central America as well as the inclusion of other variables into the dataset that contribute to the quantification of wildlife health

The scope and severity of white-nose syndrome on hibernating bats in North America.

Assessing the scope and severity of threats is necessary for evaluating impacts on populations to inform conservation planning. Quantitative threat assessment often requires monitoring programs that provide reliable data over relevant spatial and temporal scales, yet such programs can be difficult to justify until there is an apparent stressor. Leveraging efforts of wildlife management agencies to record winter counts of hibernating bats, we collated data for 5 species from over 200 sites across 27 U.S. states and 2 Canadian provinces from 1995 to 2018 to determine the impact of white-nose syndrome (WNS), a deadly disease of hibernating bats. We estimated declines of winter counts of bat colonies at sites where the invasive fungus that causes WNS (Pseudogymnoascus destructans) had been detected to assess the threat impact of WNS. Three species undergoing species status assessment by the U.S. Fish and Wildlife Service (Myotis septentrionalis, Myotis lucifugus, and Perimyotis subflavus) declined by more than 90%, which warrants classifying the severity of the WNS threat as extreme based on criteria used by NatureServe. The scope of the WNS threat as defined by NatureServe criteria was large (36% of Myotis lucifugus range) to pervasive (79% of Myotis septentrionalis range) for these species. Declines for 2 other species (Myotis sodalis and Eptesicus fuscus) were less severe but still qualified as moderate to serious based on NatureServe criteria. Data-sharing across jurisdictions provided a comprehensive evaluation of scope and severity of the threat of WNS and indicated regional differences that can inform response efforts at international, national, and state or provincial jurisdictions. We assessed the threat impact of an emerging infectious disease by uniting monitoring efforts across jurisdictional boundaries and demonstrated the importance of coordinated monitoring programs, such as the North American Bat Monitoring Program (NABat), for data-driven conservation assessments and planning