Thesis (M.S.)--Villanova University, 2006. / Biology Dept. Includes bibliographical references.

The use of common species as surrogates for those that are threatened or endangered is best conducted using species that are biologically related. If the two species are fairly dissimilar then conclusions based on data collected from surrogates may be misleading. The abundant little brown bat (Myotis lucifugus) has been suggested as a suitable surrogate for the endangered Indiana bat (Myotis sodalis) due to their close morphological similarities. In order to examine the suitability of little brown bats as surrogates in ecological based research and management, research was conducted on the roosting ecology, foraging home ranges, foraging habitat selection, and diets of both species. While research is available on Indiana bats in these subjects, there is a paucity of information on little brown bat roosting ecology and foraging ecologies. Therefore, data were collected concerning these ecological factors to determine the similarity between the species. There was enough research on little brown bat and Indiana bat diets available to compile data and compare them without conducing additional research. Roosting ecology and foraging ecology data were collected during the summers of 2003, 2007, and 2009-2011 from 2 study areas in the Shawnee National Forest, IL, and 2 study areas in south-central Indiana. Bats of both species were tracked during the day to record maternity roost characteristics and again at night to record foraging locations. A total of 67 Indiana bats and 31 little brown bats were tracked during our study. Our results show that while the species are similar in some ecological characteristics (roosting habitat, roost tree species) they are also different in several other characteristics (roost type, home range, and habitat selection). Therefore, little brown bats may be suitable surrogates for some research and management projects and unsuitable for others, depending on the objectives of the project. However, holistically little brown bats are unsuitable surrogates for Indiana bat summer habitat management. / Introduction and literature review -- An examination of the characteristics of little brown bat (Myotis lucifugus) natural tree roosts within the central portion of the species' range -- Horizontal resource partitioning between sympatric populations of the endangered Indiana bat (Myotis sodalis) and the little brown bat (M. lucifugus) -- Suitability of little brown bats (Myotis lucifugus) as surrogates for Indiana bat (Myotis sodalis) summer research and management. / Department of Biology

Thesis (M.S.)--Marshall University, 2002. / Title from document title page. Document formatted into pages; contains vi, 50 p. with illustrations and maps. Includes bibliographical references (p. 22-26).

In 2021, 17-year periodical cicadas (Magicicada spp.) in Brood X emerged throughout much of the eastern United States. Due to their abundance and lack of predator avoidance during their short six-week period on the above-ground landscape, many species of animals consume cicadas and in turn have short-term habitat use and population responses. The response of bats to periodical cicadas is largely unknown. Using a before-after-control-impact study design, we deployed ultrasonic acoustic detectors during the summers of 2020–2022 within and just outside the range of the cicada emergence along the Potomac River corridor of Maryland and Virginia. For total bat activity, there was significantly more acoustic activity within the range of the cicada emergence the year during and the year following emergence than where emergence did not occur. Additionally, for all individual species and phonic groups, bat activity increased the year during and year after the emergence within the range of periodical cicadas compared to the year prior to emergence. Our study demonstrates that periodical cicadas may serve as a resource pulse that can cause an increase in bat activity and suggests at least a short-term local to regional population increase from immigration the year during and from recruitment the year following. Bats of the mid-Atlantic have been negatively affected by numerous stressors including white-nose syndrome, wind turbine development, and land use change. One species suffering widespread population decline over the last decade in the mid-Atlantic has been the little brown bat (Myotis lucifugus). Understanding the space use and resource selection of remaining populations is critical for management and species recovery. Nevertheless, there are difficulties with studying the movement of insectivorous bats due to their small size and high vagility. Traditional foraging studies of Myotis spp. have used fixed station telemetry and associated multi-azimuthal observations to estimate the location of individuals. However, single azimuth observations are often unable to be included in these studies leading to more potential location estimates missing from movement models. During the summer of 2022, I radio-tagged little brown bats from a maternity colony along the Potomac River in Maryland and collected bearings on nine individuals using fixed station telemetry from sunset until bats returned to the maternity roost. Location estimates were obtained from both single and multi-azimuthal observations. I fit movement models for each individual and used auto-correlated kernel density estimation (AKDE) to estimate space use. I also assessed second and third order habitat selection of individual bats. The average 95% AKDE for males was 889 ha ± 424.6 and 699.3 ha ± 129 for adult females. I found bats had higher predicted use of habitat that was closer in distance to water and wetlands and further from open habitat at the second order and closer to water and open habitat at the third order of resource selection. Habitat associations were similar to previous little brown bat resource selection studies. However, estimates of space use were larger than those using other movement models. This study was novel in that it incorporated single azimuth observations and periodicity into models of space use, thereby increasing sample size and offering a new framework for future telemetry studies. These estimates of space use can be used by land managers to protect the habitat of this imperiled species. / Master of Science / In 2021, 17-year periodical cicadas (Magicicada spp.) in Brood X emerged throughout much of the eastern United States in high abundance. As an abundant food resource, many animals consume periodical cicadas while they are above ground during the summers. This has allowed for short-term population increases and changes in reproduction in some species. However, the response of bats to periodical cicadas is largely unknown. To study this, I deployed ultrasonic acoustic detectors that recorded six species/species groups of bats during the summers of 2020–2022 within and just outside the range of the cicada emergence along the Potomac River Corridor, Maryland, and Virginia. I observed significantly more total bat acoustic activity within the range of the cicada during the emergence year and the year following than where emergence did not occur. Also, for all individual species and species groups, bat activity increased in the year during and after the emergence within the range of periodical cicadas compared to the year before emergence. My study demonstrates that periodical cicadas cause an increase in bat activity and may suggest a population increase in the areas where the emergence has occurred. Bats of the mid-Atlantic have experienced population declines due to numerous stressors including white-nose syndrome caused by the fungus Pseudogymnoascus destructans, wind turbine development, and habitat fragmentation. One species that has been heavily affected by white-nose syndrome is the little brown bat (Myotis lucifugus). To help conserve the species, understanding their home range and their resource needs is critical. However, little brown bats are small and agile fliers which poses difficulties for tracking them. Traditional foraging studies of species in this genus have used telemetry to obtain triangulations and location estimates of individuals but often leave out data collected from a single bearing as it is difficult to calculate the true location of the animal. During the summer of 2022, I radio-tagged little brown bats from a maternity colony along the Potomac River in Maryland and collected bearings on nine individuals using fixed station telemetry from sunset until bats returned to the maternity roost. We estimated locations from both triangulations and single bearings. I calculated movement models for each individual and fit them to an auto-correlated kernel density estimator (AKDE) of space use. The average 95% auto-correlated kernel density estimates of space use (AKDE) for males was 889 ha ± 424.6 and 699.3 ha ± 129 for adult females. I also assessed the habitat selection of individuals within their home range and across the nearby landscape. I found that bats preferred to use areas closer to water and wetlands and preferred to use areas closer to open habitat within their home range but preferred to use areas further from open habitat across the landscape. Habitat associations were similar to previous little brown bat resource selection studies. However, estimates of space use were larger than those using other movement models. My study was novel in that it incorporated single azimuth observations and periodicity into models of space use, thereby increasing sample size and offering a new framework for future telemetry studies. These estimates of space use can be used by land managers to protect the habitat of this imperiled species.

The endangered Indiana bat (Myotis sodalis) has been the focus of much research in the past 40 years, primarily with respect to the summer habitat requirements for the species. Recent advances in radio telemetry have allowed researchers to learn about the specific activity patterns for roosting bats. Torpor is an energetic process that bats use to conserve energy through the day. We used an equation that gives a threshold for when the animal enters torpor to quantify the amount of energy conservation among Indiana bats, northern long-eared bat (M. septentrionalis) and little brown bat (M. lucifugus) and their reproductive stage. Additionally, we used the torpor threshold to determine if researchers were causing disturbances to roosting female Myotis bats in the summer. / Department of Biology

Le syndrome du museau blanc (SMB), causé par le champignon Pseudogymnoascus destructans (Pd), a mis en péril les populations de chauves-souris hibernantes en Amérique du Nord. Certaines espèces sont hautement vulnérables à la maladie alors que d’autres espèces semblent être résistantes ou tolérantes à l’infection. Plusieurs facteurs physiologiques et environnementaux peuvent expliquer ces différences. Or avant 2015, peu d’études avaient porté sur le microbiome de la peau en relation avec cette maladie. La présente thèse vise à caractériser le microbiome cutané de chiroptères affectés par le SMB afin d’identifier les facteurs de vulnérabilité ou de résistance à la maladie. L’objectif principal est de déterminer comment le microbiome est affecté par la maladie ainsi que de déterminer si celui-ci à un rôle dans la protection face à l’infection fongique. Au Chapitre 1, nous avons tout d’abord exploré et comparé le microbiote cutané de petites chauves-souris brunes (Myotis lucifugus) non affectées par le SMB avec celui de chauves-souris survivantes au SMB pour tester l’hypothèse selon laquelle le microbiote cutané est modifié par la maladie. Nos résultats montrent que le site d’hibernation influence fortement la composition et la diversité du microbiote cutané. Les sites d’hibernations Pd positifs et négatifs diffèrent significativement en termes de diversité, ainsi qu’en termes de composition du microbiote. La diversité est réduite au sein du microbiote des chauves-souris survivantes au SMB et enrichi en taxons tels que Janthinobacterium, Micrococcaceae, Pseudomonas, Ralstonia et Rhodococcus. Certains de ces taxons sont reconnus pour leur potentiel antifongique et des souches spécifiques de Rhodococcus et de Pseudomonas peuvent inhiber la croissance de Pd. Nos résultats sont cohérents avec l’hypothèse selon laquelle l’infection par Pd modifie le microbiote cutané des chauves-souris survivantes et suggèrent que le microbiote peut jouer un rôle de protection face au SMB. Au Chapitre 2, nous avons étudié le microbiote d’une espèce résistante au champignon Pd en milieu contrôlé avant et après infection afin d’établir la réponse potentielle à la maladie. L’espèce étudiée est la grande chauve-souris brune (Eptesicus fuscus) dont le microbiote cutané pourrait jouer un rôle de protection contre l’infection. Nos résultats montrent que la diversité du microbiote de la grande chauve-souris brune inoculée avec Pd est plus variable dans le temps, tandis que la diversité du microbiote des chauves-souris du groupe contrôle demeure stable. Parmi les taxons les plus abondants, Pseudomonas et Rhodococcus, deux taxons connus pour leur potentiel antifongique contre Pd et d’autres champignons, sont restés stables durant l’expérience. Ainsi, bien que l’inoculation par le champignon Pd ait déstabilisé le microbiote cutané, les bactéries aux propriétés antifongiques n’ont pas été affectées. Cette étude est la première à démontrer le potentiel du microbiote cutané d’une espèce de chauves-souris pour la résistance au SMB. Au Chapitre 3, le microbiome cutané de la petite chauve-souris brune a été évalué en milieu naturel dans le contexte du SMB, à l’aide de la métagénomique, une approche haute résolution pour observer le potentiel fonctionnel du microbiome (métagénome fonctionnel). Nos résultats ont permis d’établir que le temps depuis l’infection a un effet significatif sur le métagénome fonctionnel. En effet, les chauves-souris dans la première année suivant l’infection ont un métagénome fonctionnel perturbé qui subit une perte de diversité fonctionnelle importante. Toutefois, le métagénome fonctionnel revient à une structure et composition similaire d’avant infection après 10 ans. Certaines fonctions détectées suite à l’infection sont associées à des gènes reliés au transport et à l’assimilation de métaux, des facteurs limitants pour la croissance du champignon. Ces gènes pourraient donc avoir un rôle à jouer dans la résistance ou la vulnérabilité à la maladie. Globalement, l’étude du métagénome chez la petite chauve-souris brune indique une vulnérabilité du métagénome fonctionnel au champignon, mais que celui-ci semble se rétablir après 10 ans. Une telle réponse pourrait avoir un impact sur la résilience de M. lucifugus. Cette thèse a permis d’acquérir des connaissances fondamentales sur le microbiome cutané des chauves-souris en hibernation pour mieux comprendre les communautés microbiennes de la peau dans le contexte du SMB. Le microbiome pourrait en effet jouer un rôle dans la vulnérabilité et la résistance des chauves-souris à la maladie, et il est essentiel d’adapter notre façon d’aborder la protection de ces espèces et de leur microbiome. Nous souhaitons que les travaux de cette thèse permettent de sensibiliser les acteurs de la conservation à l’existence et à l’importance potentielle du microbiome pour la santé de son hôte. Cette thèse fait également état de l’avancement des méthodes d’analyses qui permettront d’être de plus en plus précis et d’appliquer les connaissances du microbiome en biologie de la conservation. / White-nose syndrome (WNS) caused by the fungus Pseudogymnoascus destructans (Pd) has put hibernating bat populations at risk in North America. Some species are highly vulnerable to the disease while other species appear to be resistant or tolerant. Several physiological and environmental factors can explain these differences. However, before 2015, few studies have focused on the skin microbiome in relation to this disease. The present thesis aims to characterize the cutaneous microbiome of bats affected by WNS in order to identify the factors of vulnerability or resistance to the disease. The main objective is to determine how the microbiome can protect against the Pd fungus, or conversely how the microbiome is altered by the fungal infection. In Chapter 1, we first explored and compared the skin microbiota of little brown bats (Myotis lucifugus) unaffected by WNS with that of WNS survivors to test the hypothesis that the skin microbiota is modified by the disease. Our results show that the hibernation site strongly influences the composition and diversity of the skin microbiota. The Pd positive and negative sites differ significantly in terms of diversity, as well as in terms of the composition of the microbiota. Diversity is reduced within the microbiota of bats surviving WNS and enriched in taxa such as Janthinobacterium, Micrococcaceae, Pseudomonas, Ralstonia, and Rhodococcus. Some of these taxa are recognized for their antifungal potential and specific strains of Rhodococcus and Pseudomonas may inhibit the growth of Pd. Our results are consistent with the hypothesis that Pd infection modifies the skin microbiota of surviving bats and suggest that the microbiota may play a protective role against WNS. In Chapter 2, we studied in a controlled environment the microbiota of a species that exhibits evidence of resistance with mild WNS symptoms, before and after infection, to establish the potential response to the disease. The species studied is the big brown bat (Eptesicus fuscus), whose skin microbiota could play a protective role against infection. Our results show that the diversity of the microbiota of big brown bats inoculated with Pd is more variable over time, while the diversity of the microbiota of the control bats remains stable. Among the most abundant taxa, Pseudomonas and Rhodococcus, two taxa known for their antifungal potential against Pd and other fungi, remained stable during the experiment. Thus, although inoculation with the Pd fungus destabilized the skin microbiota, bacteria with antifungal properties were not affected. This study is the first to demonstrate the potential of the skin microbiota of a bat species for resistance to WNS. In Chapter 3, the skin microbiome of the little brown bat was evaluated in the natural environment in the context of WNS, using metagenomics, a higher-resolution approach to observe the functional potential of the microbiome (functional metagenome). Our results established that the time since infection has a significant effect on the functional metagenome. Indeed, bats in the first year after infection have a disrupted functional metagenome that undergoes a significant loss of functional diversity. However, the functional metagenome returns to a similar structure and composition to that observed before infection after 10 years. Certain functions detected following infection are associated with genes linked to the transport and assimilation of metals, known limiting factors for the growth of the fungus. These genes could therefore have a role to play in resistance or vulnerability to the disease. Overall, this metagenomics study indicates functional metagenome vulnerability to the fungus, although the original functional metagenome is reestablished after 10 years. Such diversified response could impact M. lucifugus resilence. This thesis provides fundamental knowledge on the skin microbiome of hibernating bats to better understand the microbial communities of the skin in the context of WNS. The microbiome could indeed play a role in the vulnerability and resistance of bats to disease and it is essential to adapt our way of approaching the protection of these species and their microbiomes. We hope that the results of this thesis will raise awareness among conservation stakeholders about the existence and potential importance of the microbiome for the health of its host. This thesis also reports on the advancement of analytical methods that will make it possible to be more and more precise and to apply knowledge of the microbiome in conservation biology.