Emerging infectious diseases of wildlife are among the greatest threats to biodiversity. Indeed, when pathogens are introduced into naïve host populations, they can impose novel selective pressures that may cause severe host declines or even extinction. However, disease impacts may vary both within and among host species. Thus, one of the key goals for management is to identify factors that drive variation in host susceptibility to infection, as they may improve our understanding of hosts' potential to develop disease resistance and/or tolerance and inform conservation strategies aimed at facilitating host persistence. For instance, Pseudogymnoascus destructans (Pd) - an invasive pathogenic fungus that causes white-nose syndrome (WNS) in hibernating bats - is highly virulent, has killed millions of bats in North America, and continues to spread at an alarming rate. Yet, the continued persistence of bat colonies in contaminated areas despite initial mass mortality events suggests variation in survival among infected individuals. I thus aimed to better understand intraspecific drivers of variation in bat susceptibility to WNS and their implications for population persistence and management in affected areas. Specifically, my objectives were to: 1) evaluate the extent to which variation in hibernaculum microclimate temperature and humidity affects Pd infection severity and disease progression in affected bats during hibernation, 2) compare how bats from colonies that vary in duration of exposure to Pd and from different age classes behaviorally respond to the infection, and examine how these behavioral changes affect host fitness and 3) model the population dynamics of remnant bat populations to assess the likeliness of persistence and the potential effectiveness of management interventions in affected colonies. I addressed these objectives through field research, experimental infection studies, and demographic modeling of the little brown myotis (Myotis lucifugus). In my dissertation, I first provide causal evidence of environmentally-driven variation in pathogen growth and infection severity on bats in the field. Both warmer and more humid microclimates contribute to the severity of the infection by promoting the production of conidia, the erosion of wing tissues, and, therefore, the transmission potential and virulence of Pd. I then document potential mechanistic links between Pd-induced behavioral change and host fitness. Higher infection levels, independent of bats' past exposure to Pd or age class, may cause individuals to groom longer, prolong euthermic arousals, accelerate the depletion of fat reserves, and ultimately increase mortality risk. Finally, I predict that populations will face a high risk of extirpation in the next decade or two if no management action is taken, but that interventions such as environmental control of Pd and hibernaculum microclimate manipulation can prevent short-term population collapse in remnant bat populations. Together, these studies provide key, mechanistic insight into the pathology of WNS and the probability of persistence of affected bat colonies, while highlighting the importance of prioritizing winter habitat preservation and enhancement for the conservation of hibernating bats. / Biology

Critical to our understanding of wildlife diseases is the recovery phase, a period during which individuals clear infections and return to normal patterns of behavior and physiology. Most research on effects of white nose syndrome (WNS), an emerging fungal disease in bats, has focused on the pathophysiology of winter mortality and the effects of WNS on hibernating populations. The period immediately following emergence from hibernation has received little attention, but is a critically important time for survivors of the disease. During this time, survivors face significant physical and physiological challenges as they migrate to summer habitats, potentially begin gestation in the case of reproductive females, and begin to recover from wing damage caused by the fungus, which can be extensive and may greatly increase the energetic cost of flight. In this study, I (1) test the hypothesis that free-ranging bats heal from WNS-induced wing damage, (2) determine how WNS-induced wing damage changes skin surface lipid profiles on free-ranging bats, and (3) describe the temporal process of disease recovery in a colony of captive bats, including analyses of body mass, wing damage, pathogen load, skin surface lipid profiles, and histopathological metrics of WNS. I find that bats can quickly heal from wing damage in the wild and appear healthy as early as mid-July in New England. Analysis of skin surface lipids does not reveal any striking differences between bats with wing damage and those without, although there are trends towards lower total surface lipids and increased levels of cutaneous cholesterol in bats with severe wing damage. Finally, I show that within 40 days of emerging from hibernation, bats quickly clear the fungal infection and gain body mass, undergoing rapid healing of wing damage and changes in skin surface lipid composition. Bats depend on their wings for a variety of vital processes including physiological regulation, locomotion and feeding. To fully understand the consequences of WNS and develop actionable management strategies, it is important to consider the long-term effects of this disease. My study helps fill critical knowledge gaps and will aid in the future conservation and management of affected bat species.

No description available.

White-nose syndrome (WNS) has reduced the abundance of many bat species within the United States' mid-Atlantic region, including the endangered Indiana (Myotis sodalis), threatened Myotis septentrionalis (northern long-eared bat) and other bats of conservation concern, such as Perimyotis subflavus (tri-colored bat), Myotis leibii (eastern small-footed bat) and Myotis lucifugus (little brown bat). Impacts to Eptesicus fuscus (big brown bat) populations have been negative, positive or neutral. Migratory bat species such as Lasiurus borealis (eastern red bat) are not impacted by WNS. To determine changes within the National Park Service National Capital Region bat communities, I surveyed the area with mist netting and active acoustic sampling (2016–2018) and compared findings to pre-WNS (2003–2004) data. I documented a significant reduction in the numbers and distributions of M. lucifugus and P. subflavus, a decrease in the distribution of M. septentrionalis, and an increase in Eptesicus fuscus. Documented M. septentrionalis reproduction suggests that portions of the National Capital Region may be important bat conservation areas. To explore the relationship between bat life history and passive acoustic sampling echolocation call data, as well as to review the sampling effort required to detect the presence of extant species, I used mist-netting captures and acoustic call data collected 2015 – 2018 within the District of Columbia, Maryland, Pennsylvania, Virginia, and West Virginia. Based on locally estimated scatterplot smoothing line calculations, I determined that the highest levels of maternity season acoustic activity for Eptesicus fuscus and Lasiurus borealis corresponded primarily to lactation periods. To determine sampling effort, I developed simulations based on species accumulation curves for individual species within different physiographic regions and land-cover types. I determined that the smallest sampling efforts typically corresponded to sampling additional sites versus sampling the same sites with more nights. Detection effort varied greatly by species, physiographic region and land-cover type. Eptesicus fuscus diet has been well-studied throughout North America with visual identification methods from fecal and stomach content samples. Next-generation sequencing provides large genetic data sets analyses in a cost-effective manner and has been used to identify bat prey items. I collected Eptesicus fuscus fecal samples from mid-Atlantic regions and used next-generation sequencing to identify their prey. I documented high variation between survey areas, but did not note a clear pattern of urbanization or fragmentation impacts upon Insecta diversity. All order-level taxa that I documented had been previously documented in morphological studies; however, I did document new families, genera and species. However, I would suggest caution in using next-generation sequencing technologies as authoritative sources for documenting new diet taxa, as I noted frequent occurrences of confounding environmental DNA within the samples. / Doctor of Philosophy / White-nose syndrome (WNS) has reduced the abundance of many bat species within the United States' mid-Atlantic region, including the endangered Indiana (Myotis sodalis), threatened Myotis septentrionalis (northern long-eared bat) and other bats of conservation concern, such as the Perimyotis subflavus (tri-colored bat), Myotis leibii (eastern small-footed bat) and Myotis lucifugus (little brown bat). WNS-impacts to Eptesicus fuscus (big brown bat) populations have been negative, positive or neutral. Migratory bat species such as Lasiurus borealis (eastern red bat) are not impacted by WNS. To determine changes within the National Park Service National Capital Region bat communities, I captured bats with mist-netting techniques and recorded bat echolocation calls with active acoustics (20-minute periods; 2016–2018) and compared findings to pre-WNS (2003–2004) data. I documented a significant reduction in the numbers and distributions of M. lucifugus and P. subflavus, a decrease in the distribution of M. septentrionalis, and an increase in Eptesicus fuscus. Documented M. septentrionalis reproduction suggests that portions of the National Capital Region may be important bat conservation areas. To explore the relationship between bat echolocation calls recorded with passive (over-night) acoustic data and bat reproduction trends, as well as the amount of effort required to document bat species, I sampled 849 sites with passive acoustics and 482 sites with mist-netting during 2016 – 2018 within the District of Columbia, Maryland, Pennsylvania, Virginia, and West Virginia. I determined that the highest levels of acoustic activity for Eptesicus fuscus and Lasiurus borealis (eastern red bat) within the maternity season are associated with the period of highest levels of lactation. To determine sampling effort, I used simulations to detect species in different landscape conditions. I determined that sampling additional sites requires less sampling effort than sampling more nights. The amount of effort required to detect each bat species varied, as did the impact of different landscape conditions. Eptesicus fuscus diet has been well-studied throughout North America by identifying insect parts in feces and stomach contents. Next-generation sequencing is a process which produced large amounts of genetic data sets in a cost-effective manner, and it can be used to identify prey within bat feces. I collected Eptesicus fuscus fecal samples from mid-Atlantic regions and used next-generation sequencing to identify potential prey. I determined that bat diet varied greatly based on survey area and number of feces analyzed. At the order-level, I did not document new taxa: however, I did document new families, genera and species. However, I would suggest caution in using next-generation sequencing technologies as authoritative sources for documenting new diet taxa, as many taxa apparent within my samples were subsequently excluded, as the bats may have been incidentally ingested them.

Emerging infectious diseases (EID) pose significant threats to biodiversity. Human influence over the environment has increased opportunities for the introduction of novel pathogens to naïve hosts, potentially leading to host extinction. Understanding mechanisms of host persistence is critical for effectively conserving species affected by EIDs. Our study investigated the disease dynamics of white-nose syndrome (WNS), caused by the fungal pathogen Pseudogymnoascus destructans (Pd), in little brown bats (Myotis lucifugus) across a spatiotemporal gradient. We explored the relationship between bat roosting temperatures and Pd growth rates across three phases of pathogen invasion comprising years since WNS has been present at sites: invasion (0-3), established (4-8), and endemic (9+ years). Data used by this study comes from a combination of field-based data collection in New York where WNS has been present the longest and data from a long-running project which includes from other locations in the Northeast and Midwest regions of the United States. Our results reveal a weakening interaction between temperature and fungal growth rates time with WNS progresses. We additionally observed a decrease in early hibernation fungal loads and variation in infection prevalence over time, suggesting the onset of a coevolutionary relationship between bats and Pd. This study highlights the importance of investigating changing disease dynamics when understanding the reasonings for host persistence. / Master of Science / Emerging infectious diseases threaten species with the risk of extinction. Human activities have altered habitats which has increased the spread of new pathogens to vulnerable host populations. This research focuses on white-nose syndrome (WNS), an emerging disease caused by the fungal pathogen Pseudogymnoascus destructans (Pd). The arrival of Pd to North America resulted in widespread declines in little brown bat (Myotis lucifugus) populations, however, some populations persist at stable or growing rates. This study aims to investigate how the relationship between the growth rate of Pd and bat hibernation temperature may have changed over time. We used a combination of contemporary data collected in New York and a long-running dataset that documents the invasion and establishment of Pd across the Northeast and Midwestern regions of the United States to investigate fungal growth rates during different phases of Pd invasion: invasion, established, and endemic phases. Our results indicate the relationship between temperature and pathogen growth rate has weakened over time, suggesting potential changes in the host-pathogen relationship. Additionally, we found changes in fungal loads and infection prevalence throughout hibernation, suggesting the foundation of a coevolutionary relationship between bats and Pd. This research highlights the importance of understanding changes in disease dynamics to help understand how other species at risk of emerging infectious diseases may be able to persist.

Two threats to bats are especially pervasive in the central Appalachian Mountains of the eastern United States: a fungal disease called White-nose Syndrome (WNS) and wind energy development. White-nose Syndrome has caused the death of millions of bats in North America, and multiple hibernating bat species are affected in the central Appalachians. Wind energy is one of the most rapidly-growing energy sources in eastern United States, and bats are often killed when they fly near wind turbines. Fatality rates at wind turbines is highest in bat species that migrate instead of hibernate. There is limited data on bats during the autumn and spring seasons in the central Appalachian Mountains, and the impacts of WNS and wind energy development may be exacerbated during these seasons. Therefore, I sought to determine patterns and drivers of activity for hibernating bat species during autumn and spring around hibernacula. Similarly, I set out to determine patterns and drivers of activity for migratory bat species during autumn and spring along mountain ridgelines in the central Appalachians. Lastly, I searched for evidence of potential WNS-induced changes in the summer ecology of the once common northern long eared bat. This study can help elucidate patterns of bat activity during largely understudied seasons. Furthermore, it can provide useful information needed by land managers to implement actions that could help alleviate and/or avoid potential additive negative impacts on bat species with existing conservation concerns. / MS

Northern long-eared bat (Myotis septentrionalis) populations have declined sharply in recent years due to the introduction and rapid spread of White-nose Syndrome. This has prompted an urgent need for a greater understanding of their natural history in order to support the conservation of extant populations, particularly where forested day-roost and foraging habitats are being fragmented by development. Prior to 2006, with other Myotis species on the endangered species list, northern long-eared bats were understudied. In recent years, with the pressing concern to document the ecology of all cave bats affected by White-nose Syndrome on the landscape, researchers have now prioritized northern long-eared bat habitat needs, day-roost use, social dynamics, and barriers to gene flow. A relatively new discovery has been the numerous coastal populations that occur in smaller forest patches often surrounded by anthropogenic development. The goal of my research is to aid in informing future monitoring and management protocols that are specific to northern long-eared bats, particularly as they may shift from Threatened to Endangered under the Endangered Species Act. The chapters of this dissertation explore (1) similarities and differences between coastal and more documented upland habitat associations for populations of northern long-eared bats throughout the summer months through the use of acoustic detectors; (2) relationships between acoustic activity patterns and weather on an hourly basis for several bat species on Long Island, New York; and (3–4) day-roost characteristics and social network dynamics of a coastal northern long-eared bat maternity colony on Long Island, New York. I found that northern long-eared bat colonies have larger spatial footprints in – and a moderate tolerance for – forests in anthropogenically-developed areas than previously believed, though many natural history aspects of the bat were similar among coastal and interior populations. Installation of artificial day-roost structures such as bat boxes would likely be used and highly beneficial to colonies in these conditions, particularly to offset the deleterious effects of stochastic disturbance events on day-roost availability and to support social cohesion (and, by extension, reproductive success) for coastal maternity colonies. Additionally, I found that acoustic activity increased in riparian areas, or at sites closer to water features, and as proportion of forest coverage increased at a broad scale. However, immediately around the detector this relationship was reversed. Taken together, this demonstrates that riparian corridors, water features, and forest structural heterogeneity should explicitly be included in management guidelines. / Doctor of Philosophy / White-nose Syndrome is a fungal disease that has killed millions of cave bats in North America, including the northern long-eared bat (Myotis septentrionalis) that during the spring through fall uses forests for roosting and foraging habitat. As the disease continues to spread, and as forests are increasingly being lost to urbanization, it is imperative for researchers and land managers to understand the landscape needs of this species so that they can retain those forests that are used by this species. In addition to broader landscape needs, it is important to understand what specific forest stand to tree features the bats are using, how their social dynamics support their reproductive success, and how to best support habitat conditions foster mating in the fall swarm to avoid inbreeding. In recent years, more northern long-eared bats have been documented in coastal landscapes, suggesting that these areas might be more important to the conservation of the species than previously believed. In this dissertation, my aim was to explore how or why the landscapes in these coastal areas were being used by these bats both during nightly foraging and during the day as resting areas (day-roosts). Additionally, I explored how multiple species of bats were responding to weather conditions on the coast across seasons. Overall, I found that complex forests continue to be an important resource for northern long-eared bats, as well as water features whereby the latter should be more explicitly included in conservation management plans. Northern long-eared bats also show an ability to successfully use small forest patches within a larger urbanized landscape, including using human structures for day-roosts. Human structures might provide reliable, multi-year day-roosts in areas where extreme coastal weather events (hurricanes) occur or increase or as natural processes reduce the suitability of these forests to provide day-roosts. These structures, particularly artificial roost boxes could also support the social network of reproductive northern long-eared bats and thus maintain population stability to some extent.

No description available.

Bat populations across North America are either facing new threats from white-nose syndrome (WNS) and wind energy development or have already experienced precipitous declines. Accordingly, researchers and managers need to know how to best monitor bats to document population and distribution changes, as well as where to look for persisting populations. Landscape-scale WNS impacts to summer bat populations are not well understood, and although acoustic monitoring is commonly used to monitor these populations, there is limited information about differences among acoustic detectors and the implications to managers thereof. My objectives were to model the relationship between WNS impact, influence of available hibernacula, and environmental factors for summer nightly presence of three WNS-affected bats and to compare how multiple models of acoustic detectors perform in terms of detection probability and nightly recorded bat activity. I collected acoustic data from 10 study areas across Virginia, West Virginia, Ohio and Kentucky to describe changes in nightly presence of WNS-affected bat species during summer 2017. During the same period of time, I compared five types of acoustic detectors at Fort Knox, Kentucky. My results show the potential efficacy of using a WNS impact-year metric to predict summer bat presence, and highlight which environmental variables are relevant for large-scale acoustic monitoring. Additionally, my findings suggest that each of the detector types tested would suffice for most research and monitoring activities, but standardization of detector type within the scope of a project or study should be encouraged. / Master of Science / Bat populations across North America are either facing new threats from white-nose syndrome (WNS) and wind energy development or have already experienced devastating declines. Accordingly, wildlife biologists need to know how to best monitor bats to document population and distribution changes, as well as where to look for remaining populations. Landscape-scale WNS impacts to summer bat populations are not well understood, and although acoustic technology is commonly used to monitor these populations, there is limited information about differences among acoustic detectors and the implications to managers thereof. My objectives were to model the relationship between WNS impact, influence of available bat hibernation caves, and environmental factors for summer nightly presence of three WNS-affected bats and to compare how multiple models of acoustic detectors perform in terms of detection probability and nightly recorded bat activity. I collected acoustic data from 10 study areas across Virginia, West Virginia, Ohio and Kentucky to describe changes in nightly presence of WNS-affected bat species during summer 2017. During the same period of time, I compared five types of acoustic detectors at Fort Knox, Kentucky. My results show potential viability of a WNS impact-year metric to predict summer bat presence, and highlight which environmental variables are relevant for large-scale acoustic monitoring. Additionally, my findings suggest that each of the detector types tested would suit most research and monitoring activities, but standardization of detector type within the scope of a project or study should be encouraged.

With declines in abundance and changing distribution of White-nose Syndrome (WNS)-affected bat species, increased reliance on acoustic monitoring is now the new "normal". As such, the ability to accurately identify individual bat species with acoustic identification programs has become increasingly important. Additionally, how bat distribution and habitat associations have changed at the local to sub-landscape scale in the post WNS environment is important to understand. The significance of these changes, relative to bat activity, may be based on the species-specific susceptibility to WNS. We used data collected from Fort Drum Military Installation, New York from the summers of 2003-2017 to analyze the accuracy of acoustic software programs, and assess the changes in relative bat activity, occupancy, and distribution induced by WNS. Our results indicate that continued acoustic monitoring of bat species, such as the little brown bat (Myotis lucifugus) in the Northeast, to assess ongoing temporal and spatial changes, habitat associations, and as a guide to direct future mist-netting should rely more on relative activity as the metric of choice. Furthermore, the continuous spread of WNS across North America will have strong negative effects on bat populations and communities, this study points to how individual species (both impacted and non-impacted) will respond to WNS. We believe that our results can help users choose automated software and MLE thresholds more appropriate for their needs to accurately address potential changes in communities of bat species due to impacts of WNS or other factors. / MS