The proposed thesis concerns in the study of tribosphenic molar, the key apomorphy of mammalian clade, mainly in structure and development of its enamel coat. As the main model species served us European vespertilionid bat Myotis myotis. The aims of this thesis are: (1) to describe structure and microstructure of enamel in tribosphenic molars in detail; (2) to compare it with unicuspid teeth of the same dentition; (3) to describe mineralization process and enamel maturation in insectivorous dentition; (4) to describe late odontogenesis in molars of insectivorous dentition and its interlacing with enamel maturation, and how they come to occlusion.

Bats occupy diverse and unique niches and are regarded as important components in maintaining ecosystem health. They are major consumers of nocturnal insects, serve as pollinators, seed disperser, and provide important economic benefits as consumers of agricultural and forest pest insects. Bats have been proposed as good indicators of the integrity of natural communities because they integrate a number of resource attributes and may show population declines quickly if a resource attribute is missing. Establishing community- and population-level data, and understanding species interactions is especially important in changing landscapes and for species whose populations levels are threatened by outside factors of anthropomorphic disturbance from hibernacular visitation to energy production and fungal pathogens. For these reasons I have set out to establish habitat use patterns, detection probabilities, spatial and temporal occupancy, and investigate species interactions. This thesis is broken down into three distinct chapters each intended to be a stand-alone document. The first establishes the basic ecology from natural history accounts, provides an overview of the various sampling strategies, and gives a comprehensive description of the study area. The seconds sets out to identify the factors influencing detection probabilities and occupancy of six sympatric bats species and provide insight into habitat use patterns. The third examines spatial and temporal activity patterns and investigates species interactions. This study can provide understanding into the secretive and poorly understood patterns of free flying bats across the landscape. It can also deliver useful information to land managers regarding potential changes in landscape practices for the conservation of bat species. / Master of Science

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.

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.

Fifty-nine female and six male little brown myotis (Myotis lucifugus) were radio-tagged during the summers of 2012, 2013, 2014, and 2015 in Yellowstone National Park. The grand models for daily maximum skin temperature (F98,154 = 1.55, P = 0.007), daily minimum skin temperature (F98,154 = 1.33, P = 0.05), and daily variation in skin temperature (F98,154 = 1.56, P = 0.006) were significant across roost type and reproductive condition class for adult females. Roosts were classified into Types A (warmest roosts), B (roosts with largest daily temperature variance), and C (stable and cool roosts) depending on differences in mean maximum, minimum, and variance in temperatures per day (P < 0.001). A total of 347 torpor bouts were recorded from 38 females across the 2012 to 2015 summer seasons. Bats across different reproductive classes and roost types used torpor at different hours of the day. My research suggests that adult female little brown myotis at high elevations in the Park extensively use and rely on building structures for roosting sites during the reproductive season, whereas males used primarily natural roosts.

The endangered northern long-eared bat (<i>Myotis septentrionalis</i>) has experienced severe population declines since the 2007 introduction of <i>Pseudogymnoascus destructans</i>, the fungal pathogen that causes white-nose syndrome (WNS). Due to continued mortality, failed recruitment, and range fragmentation, effective species conservation would benefit from local and regional research related to habitat selection and suitability, seasonal activity, and large-scale estimates of continued occupancy across the post-WNS landscape. In this dissertation, I explored maternity colony home range size and habitat selection, both coastal and interior seasonal activity patterns, habitat suitability, and species occupancy trends in the Mid-Atlantic and Northeastern United States. Research from the Coastal Plain of North Carolina, based on diurnal roost locations, revealed that core and peripheral home range estimates were large but comparable to areas of contiguous forest cover in other regions of the species' range. Prior to juvenile volancy, female northern long-eared bats selected red maple (<i>Acer rubrum</i>), water ash (<i>Fraxinus caroliniana</i>), and loblolly pine (<i>Pinus taeda</i>) as day-roosts, but then used sweetgum (<i>Liquidambar styraciflua</i>), swamp bay (<i>Persea palustris</i>), and water tupelo (<i>Nyssa aquatica</i>) after juvenile volancy. At the second-order spatial scale (i.e., home range within a region), roosting home ranges were associated with woody wetlands farther from anthropogenic development and open water. However, within the third-order scale (i.e., core home range within a periphery), northern long-eared bats selected woody wetlands adjacent to intact upland forests, areas containing shorter trees and occurring proximal to open water. Research utilizing passive acoustic monitoring on the Coastal Plain of both Virginia and North Carolina found that northern long-eared bat relative activity was highest in areas containing greater proportions of woody wetlands and upland pine-dominated evergreen forests. Conversely, the likelihood to record northern long-eared bats was associated with smaller proportions of woody wetlands and open water resources, emphasizing the importance of upland forests adjacent to these features. I also observed a higher probability of recording northern long-eared bats during non-winter seasons and when temperatures were between 10 and 25 °C, potentially highlighting an optimal thermoneutral zone for the species regionally. Research using presence data from the Monongahela National Forest (MNF) in the Central Appalachians of West Virginia found that northern long-eared bat habitat, whether occupied or not, was abundant (43.1% of the MNF) and widely dispersed. Northern long-eared bat habitat on the MNF was often characterized as mature, interior mixed mesophytic forests. Research using passive acoustic surveys associated with hibernacula in western Virginia found that northern long-eared bats were most active near hibernacula during warmer weeks of the fall swarm and spring emergence, when rainfall was low. Similarly, the probability of northern long-eared bat activity was highest near hibernacula during the spring/summer season. However, unlike relative activity, the likelihood of recording northern long-eared bats was associated with more heterogeneous, interior forests. Finally, research using a combination of long-term repeated and single-season clearance survey data from New England found that northern long-eared bat occupancy was highest on steep hillsides in contiguous forested landscapes with minimal anthropogenic development. My results also indicated higher occupancy of northern long-eared bats in warmer regions, particularly along the New England coastline and offshore islands. These findings collectively stress the importance of managing areas of large core forest to promote sustainable roost formation and productive foraging areas, often associated with dynamic ecotones, to support the survival and recovery of northern long-eared bats in the post-WNS Mid-Atlantic and Northeast. / Doctor of Philosophy / The northern long-eared bat was once one of the most common bat species in North America. However, due to population impacts caused by white-nose syndrome (WNS) the species is now recognized as endangered by the United States Fish and Wildlife Service. In this dissertation, I explore habitat selection and suitability, seasonal activity, and occupancy trends of remnant populations of northern long-eared bats in the Mid-Atlantic and Northeast of the United States, representing approximately 25% of the species' historical range. Specifically, I examined home range size and habitat selection of a reproductively successful maternity colony on the Mid-Atlantic Coastal Plain, overwintering activity at both interior and coastal sites, habitat suitability in the Central Appalachians, and spatial occupancy trends across New England. My research found that reproductive northern long-eared bats actively selected for specific cover features and displayed notable shifts in roost tree selection throughout the maternity season on the Coastal Plain of North Carolina. My research also indicated that northern long-eared bats were more active during non-winter seasons, favoring moderate temperatures and areas of forested wetlands adjacent to evergreen forests in coastal North Carolina and Virginia. In Virginia, northern long-eared bat activity near mountain hibernacula was highest in areas of greater landscape richness prior to and after hibernation. Finally, my research from New England found that northern long-eared bat occupancy was highest in steeper, forested landscapes in the absence of human development. Overall, this research highlights the need to conserve and manage forest ecosystems to promote recovery of the endangered northern long-eared bat. Conservation and management efforts informed by population status, activity trends, and habitat associations will be invaluable in guiding species recovery efforts.

No description available.

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.

No description available.