Biology Theses and Dissertations
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Item INFORMING CONSERVATION OF THREATENED BAT SPECIES USING GENOMICS AND ACOUSTICS(2022) Nagel, Juliet Joy; Nelson, David; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Bats are vital to healthy ecosystems, providing billions of dollars of services in the form of forest and crop pest control. Unfortunately, North American bat populations have faced novel pressures during the past decade that may threaten their persistence. First, several species of tree-roosting bats (primarily hoary [Lasiurus cinereus], eastern red [L. borealis], and silver-haired [Lasionycteris noctivagans] bats) are experiencing large numbers of fatalities at industrial wind-energy facilities. Second, several species of cave-dependent bats have experienced large-scale mortality as the result of infection by a fungal pathogen that causes white-nose syndrome (WNS). As bats are generally long-lived and have low reproductive rates, such increases in mortality can cause significant population declines from which they may be unable to recover. Basic questions about population trends, size and structure remain largely unanswered for these species because of challenges in applying traditional wildlife monitoring approaches to bats. This lack of understanding impedes conservation and management efforts. In my dissertation, I use genomic and acoustic survey techniques to investigate questions related to the threats that wind-energy development and WNS are posing to bat species in North America. In my first chapter, I evaluate range-wide population structure and effective population size (Ne) for hoary, eastern red, and silver-haired bats. Using genotyping-by-sequencing (GBS), I genotyped single-nucleotide polymorphism (SNP) data from 173 hoary, 113 eastern red, and 89 silver-haired bats from multiple locations spread across their geographic distributions. Hoary bats and eastern red bats showed no geographic structure in genetic diversity, whereas silver-haired bats displayed longitudinal population variation. Coalescent modeling suggested that eastern red bats have the largest evolutionary Ne, followed by hoary bats, then silver-haired bats. In my second chapter, I used GBS to assess the population structure of two federally endangered cave bat species: Indiana bats (Myotis sodalis) and gray bats (M. grisescens). Using tissue samples from 45 Indiana bats and 47 gray bats spread across their ranges, I showed that Indiana bats display no geographic genetic structure, whereas gray bats exhibit east–west population variation across the Mississippi River Valley. In my final chapter, I used acoustic surveys across the State of Maryland to investigate bat community changes in the decade following the arrival of WNS. From 2010 through 2019, I conducted annual mobile acoustic routes each summer, for a total of 344 completed routes resulting in 426 hours of recordings and 24,375 identified bat passes. I detected massive (> 92%) declines of little brown bats (M. lucifugus), northern long-eared bats (M. septentrionalis), eastern small-footed bats (M. leibii), and tricolored bats (Perimyotis subflavus), with no evidence of recovery in recent years. Trends in hoary bats and eastern red bats were non-significant during this period. Bat community composition varied among Maryland’s physiographic regions, with eastern red bats comprising a larger percentage in the east. Species composition across the state likely reflects the impact of several factors, including mortality from WNS and wind-energy development, and perhaps reduced interspecific competition. Overall, my results illustrate the unique insights, but also distinct limitations, that genomic and acoustic data can provide regarding the conservation of bats in North America.Item ECOLOGICAL APPLICATIONS OF MACHINE LEARNING TO DIGITIZED NATURAL HISTORY DATA(2022) Robillard, Alexander John; Rowe, Christopher; Bailey, Helen; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Natural history collections are a valuable resource for assessment of biodiversity and species decline. Over the past few decades, digitization of specimens has increased the accessibility and value of these collections. As such the number and size of these digitized data sets have outpaced the tools needed to evaluate them. To address this, researchers have turned to machine learning to automate data-driven decisions. Specifically, applications of deep learning to complex ecological problems is becoming more common. As such, this dissertation aims to contribute to this trend by addressing, in three distinct chapters, conservation, evolutionary and ecological questions using deep learning models. For example, in the first chapter we focus on current regulations prohibiting the sale and distribution of hawksbill sea turtle derived products, which continues internationally in physical and online marketplaces. To curb the sale of illegal tortoiseshell, application of new technologies like convolutional neural networks (CNNs) is needed. Therein we describe a curated data set (n = 4,428) which was used to develop a CNN application we are calling “SEE Shell”, which can identify real and faux hawksbill derived products from image data. Developed on a MobileNetV2 using TensorFlow, SEE Shell was tested against a validation (n = 665) and test (n = 649) set where it achieved an accuracy between 82.6-92.2% correctness depending on the certainty threshold used. We expect SEE Shell will give potential buyers more agency in their purchasing decision, in addition to enabling retailers to rapidly filter their online marketplaces. In the second chapter we focus on recent research which utilized geometric morphometrics, associated genetic data, and Principal Component Analysis to successfully delineate Chelonia mydas (green sea turtle) morphotypes from carapace measurements. Therein we demonstrate a similar, yet more rapid approach to this analysis using computer vision models. We applied a U-Net to isolate carapace pixels of (n = 204) of juvenile C. mydas from multiple foraging grounds across the Eastern Pacific, Western Pacific, and Western Atlantic. These images were then sorted based on general alignment (shape) and coloration of the pixels within the image using a pre-trained computer vision model (MobileNetV2). The dimensions of these data were then reduced and projected using Universal Manifold Approximation and Projection. Associated vectors were then compared to simple genetic distance using a Mantel test. Data points were then labeled post-hoc for exploratory analysis. We found clear congruence between carapace morphology and genetic distance between haplotypes, suggesting that our image data have biological relevance. Our findings also suggest that carapace morphotype is associated with specific haplotypes within C. mydas. Our cluster analysis (k = 3) corroborates past research which suggests there are at least three morphotypes from across the Eastern Pacific, Western Pacific, and Western Atlantic. Finally, within the third chapter we discuss the sharp increase in agricultural and infrastructure development and the paucity of widespread data available to support conservation management decisions around the Amazon. To address these issues, we outline a more rapid and accurate tool for identifying fish fauna in the world's largest freshwater ecosystem, the Amazon. Current strategies for identification of freshwater fishes require high levels of training and taxonomic expertise for morphological identification or genetic testing for species recognition at a molecular level. To overcome these challenges, we built an image masking model (U-Net) and a CNN to mask and classify Amazonian fish in photographs. Fish used to generate training data were collected and photographed in tributaries in seasonally flooded forests of the upper Morona River valley in Loreto, Peru in 2018 and 2019. Species identifications in the training images (n = 3,068) were verified by expert ichthyologists. These images were supplemented with photographs taken of additional Amazonian fish specimens housed in the ichthyological collection of the Smithsonian’s National Museum of Natural History. We generated a CNN model that identified 33 genera of fishes with a mean accuracy of 97.9%. Wider availability of accurate freshwater fish image recognition tools, such as the one described here, will enable fishermen, local communities, and citizen scientists to more effectively participate in collecting and sharing data from their territories to inform policy and management decisions that impact them directly.Item POPULATION GENETICS OF EASTERN OYSTER Crassostrea virginica RESTORATION IN THE CHESPEAKE BAY(2020) Hornick, Katherine; Plough, Louis V; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)The strategic release of captive-bred organisms is one of the most popular methods to restore species, but concerns exist regarding genetic impacts on natural populations over the long-term. Slow recovery of depleted eastern oyster C. virginica populations in the Chesapeake Bay prompted a large-scale hatchery-based restoration program consisting of the mass-release of hatchery-produced juveniles from local, wild broodstock. This dissertation characterized the genetic impact of this program, with the overall goal of understanding how characteristics of species life-history interact with hatchery practices to shape genetic variation in populations over short and long-time scales. In Chapter 2, analysis of genetic diversity changes resulting from hatchery production under two spawning designs (mass- and controlled-spawns) revealed substantial reductions in diversity and the number of breeders from parents to offspring, due primarily to high variance in reproductive success among adults in hatchery culture. In Chapter 3, high-resolution genomic data was used in a population genetic analysis comparing diversity of restored reefs in Harris Creek with variable planting histories and husbandry practices to ‘wild’ Chesapeake Bay oyster reefs. While restored reefs showed similar levels of diversity as wild reefs, strong positive relationships between planting frequency or broodstock numbers and genetic diversity were found, suggesting that hatchery practices can significantly impact diversity in natural populations. These genomic data also permitted the investigation of local adaptation and genotype by environment associations which revealed that salinity was correlated with loci putatively under selection, suggesting potential fitness tradeoffs for sourcing non-local broodstock. In Chapter 4, an individual-based model was created using biological and demographic data from Chesapeake Bay oysters to simultaneously evaluate the impact of multiple hatchery practices on natural population genetic diversity over time scales not possible with empirical methods. Overall, hatchery practices had a large effect on genetic diversity in most scenarios, but spawning practices (mass or controlled) and broodstock rotation were more important than broodstock number, suggesting that broodstock-limited programs may have other options to maintain diversity. In summary, these studies advance our understanding of how marine supplementation impacts both neutral and adaptive variation and will provide critical information for future oyster restoration efforts.Item ECOLOGICAL CAUSES AND CONSEQUENCES OF NON-BREEDING MOVEMENTS IN A DECLINING MIGRATORY SONGBIRD, WOOD THRUSH (HYLOCICHLA MUSTELINA)(2019) Stanley, Calandra Quinn; Dudash, Michele R; Marra, Peter P; Behavior, Ecology, Evolution and Systematics; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)In this dissertation I evaluate the ecological correlates of non-breeding space-use strategies and how these drive within and between season movement dynamics in a declining migratory songbird, wood thrush (Hylocichla mustelina). In Chapter 1, I deployed high-resolution GPS transmitters across 5 breeding populations to quantify habitat selection as wood thrush moved across the annual cycle. I found seasonal variation in habitat selection at the regional, landscape and local scales which suggests the factors driving the evolution of habitat selection preferences vary across seasons and environmental conditions. In Chapter 2, I combined radio telemetry and GPS tracking to examine how environmental conditions drove space-use strategies during the non-breeding stationary period. I found evidence that both small- and large-scale movement dynamics were dependent on moisture levels on tropical non-breeding grounds. At small spatial scales, dry conditions drove low food availability, reduced individual body condition and these individuals had larger home ranges. In this same chapter I integrated archival GPS tag data to demonstrate that wood thrush from across the breeding range engaged in permanent large-scale mid-winter shifts in home ranges and, similar to radio-tagged birds, that individuals from wetter, higher quality habitats were more likely to use this strategy. I suggest that the facultative movements are a condition-dependent strategy allowing wood thrush to find alternative habitats as conditions deteriorate across the dry season in their non-breeding grounds. Finally, to determine how food availability may influence timing of spring migration, I performed a food manipulation experiment with captive wood thrush in Chapter 3. I found that food availability and body condition modulated the intensity, but not onset, of migratory restlessness (Zugunruhe), an index of migratory disposition in captive birds. These results suggest that non-breeding food limitations could constrain migration preparation in wood thrush. Low food availability also advanced the onset of migratory fattening. I suggest that advancing migratory fattening when food availability is low may provide a mechanism to flexibly adjust migration timing under poor environmental conditions. Together these findings suggest that wood thrush exhibit a diversity of behavioural mechanisms to handle environmental heterogeneity across the annual cycle.Item THE INFLUENCE OF THE RIVER OTTER ON AQUATIC CONSERVATION IN THE GREATER YELLOWSTONE ECOSYSTEM: A SOCIO-ECOLOGICAL APPROACH TO EVALUATING CONSERVATION FLAGSHIPS(2019) Pearce, Kelly J; Stylinski, Cathlyn; Serfass, Thomas L; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Large scale habitat loss, unprecedented rates of species extinction, and other biodiversity issues have prompted wildlife conservationists to increasingly apply the “flagship” species concept to guide conservation decision making. Flagships are designated based on their ability to serve a socio-economic role, attracting public attention and financial support to conservation initiatives. Critical to flagships success is selecting an appropriate flagship—one that will be widely supported and will not invoke ill-will among any stakeholders. Thus, determining if the species meets certain pre-established criteria that are known to influence social-psychological processes is a critical step in flagship selection. The river otter (Lontra canadensis) is a widely distributed apex predator and possesses various other socio-ecological traits that make it suitable for a flagship species. However, empirical evidence supporting the use of the river otter as a flagship is lacking. In this dissertation, I study the ability of the river otter to serve as a flagship species in the Greater Yellowstone Ecosystem, one of the largest intact temperate-zone ecosystems in the world. I examine visitor attitudes and perceived resource conflicts with river otters and anglers, assess visitor willingness to engage in pro-conservation behaviors to help river otter conservation, and estimate probability of viewing the river otter using camera-traps along the Snake River. In addition to fulfilling certain recommended criteria of a flagship species, such as having a large body size, being charismatic, encompassing a wide-spread geographic range, and being uncommon across the landscape, my results suggest that visitors and anglers have positive attitudes towards the river otter, and that exposure to the river otter increases people’s willingness to engage in pro-conservation behaviors to help conserve the river otter and its aquatic habitat. However, pre-existing negative media portrayals as well as low visibility of the species, are potential liabilities of the river otter as a conservation flagship. The studies in this dissertation deepen the understanding of river otter socio-ecology as well as develop and apply elements of a socio-ecological framework that refine the approach of effectively selecting a successful conservation flagship.Item Thermal Physiology in a Widespread Lungless Salamander(2018) Novarro, Alexander Joseph; Bely, Alexandra E; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Understanding species responses to climate change has become a top priority for conservation biologists. Unfortunately, current models often treat species as a single entity, ignoring population-level variation. This approach may result in major oversights when managing widespread species, which generally exhibit physiological variation across their geographic range. The eastern red-backed salamander (Plethodon cinereus) is the most widely distributed Plethodon species, extending farther north than any other lungless salamander. This species’ geographic distribution raises two major questions: How does P. cinereus thrive across a wide range of temperatures, and does it possess thermal adaptations that will buffer the ecological consequences of climate change? To explore these questions, I first examined the effects of elevated temperature on metabolic hormone release rates and physiological performance (i.e., ingestion rate and mass gain) across a latitudinal population gradient. I found that physiological traits and populations differ in their thermal flexibility, and that salamanders from warmer localities are more resilient to elevated temperatures. Second, I performed a study to disentangle the environmental and evolutionary drivers of thermal limits across the geographic range of P. cinereus. I found strong support for evolutionary constraints on lower thermal limits, though there was some degree of plasticity in relation to local environmental temperatures. By contrast, upper thermal limits showed little variation across the species’ geographic range and among clades, and far exceeded survival requirements. Third, I combined laboratory experiments, field observations, and population models to explore the role of behavioral thermoregulation in shaping physiological performance in P. cinereus. I found that individuals are likely to exploit moist conditions at the cost of reduced performance, and that populations living in poor thermal quality habitats have greater thermoregulatory accuracy. Overall, my work demonstrates significant variation in thermal physiology across the geographic range and among lineages of P. cinereus and shows that thermal traits differ in their responsiveness to thermal variability. Together, these results highlight the importance of considering multiple physiological metrics and sampling large geographic areas to understand species’ abundance and distributions, and to assess species’ vulnerability to climate change.Item LEATHERBACK TURTLE MOVEMENT AND DISPERSAL FROM NESTING BEACHES IN COSTA RICA WITH IMPLICATIONS FOR MANAGEMENT AND CONSERVATION(2017) Hoover, Aimee Lynn; Bailey, Helen; Secor, David H; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Electronic tagging permits movement and distribution studies of sea turtles as they traverse large distances through a dynamic ocean environment. However, little is known about the movements of early life stages at sea, a period termed the 'lost years'. I developed and tested a method for attaching an acoustic tag suitable for use on leatherback turtles that was then applied to hatchlings in Costa Rica to obtain measures of speed and directionality. This was compared with ocean currents and revealed that the hatchlings actively swam against nearshore currents, although they were still advected by them. Finally, a Poisson generalized linear model in a continuous-time Markov chain model framework was used to predict adult, post-nesting Eastern Pacific leatherback movement based on environmental drivers, such as sea surface temperature. Monthly, near real-time predictions of leatherback movement were estimated using the most recent satellite-derived environmental information to help inform conservation management strategies.Item Enhancing Vallisneria americana restoration using knowledge of genotypic and phenotypic diversity(2015) Marsden, Brittany West; Neel, Maile C; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Vallisneria americana Michx. (Hydrocharitaceae) is an ecologically important submersed aquatic plant that once dominated freshwater to oligohaline environments in eastern North America. After dramatic declines it is the target of many restoration initiatives. To increase knowledge of the capacity of remaining populations to either adapt through natural selection or acclimate to emerging environmental conditions, I combined genetic data and common environment experiments to quantify V. americana genetic diversity and differentiation at local to regional scales, evaluate evidence of local adaptation to different climate conditions, and assess evidence of inbreeding or outbreeding depression. I quantified the structure of genetic diversity in five sites from the tidal Potomac, Hudson, and Kennebec Rivers, and 33 sites across the species' distribution in the Potomac. Genotypic (0.1-1.0) and allelic diversity (1.5-5.5), observed heterozygosity (0.34-0.72), and relatedness (-0.06-1.00) varied greatly along rivers and across latitude. Hudson V. americana had the lowest genetic diversity and Potomac had the highest. Differentiation and network analysis of relatedness revealed no common genetic diversity distribution patterns within rivers. Major differences in genetic structure were observed across the tidal and non-tidal Potomac. Common environment experiments evaluating growth and reproductive performance of Potomac, Hudson, and Kennebec V. americana grown in different temperature and photoperiod conditions only found evidence of local adaption in Potomac plants. Few overall differences in morphological and life history traits were observed between local and foreign plants. Plants grown under global warming conditions had reduced performance. Limited evidence of local adaptation and high acclimation to different conditions suggest that populations have high potential for resilience in the face of climate change, so long as temperatures do not exceed thermal tolerances. Climate change mitigation strategies that involve transplanting individuals may also be successful. To investigate consequences of restoration strategies that translocate individuals, I evaluated seed production and germination success of controlled reproductive crosses between V. americana within and among genetically differentiated populations in the Chesapeake Bay. There were no consistent patterns of inbreeding or outbreeding depression in crosses. Effects of mixing sources were site-specific and not predicted by levels of relatedness among individuals, genetic diversity within, or differentiation among populations.Item Identifying the elusive dwarf wedgemussel habitat through modeling and field approaches(2014) Campbell, Cara Ann; Prestegaard, Karen L.; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Habitat identification is an important step in the conservation of at-risk species, but difficult due to the small, fragmented populations of rare species. In particular, fine-scale habitat features that constrain species occurrence may not be captured by landscape models. Thus, I used both modeling and field-based approaches to identify habitat characteristics for the endangered dwarf wedgemussel, Alasmidonta heterodon. Community analyses and modeling were combined to identify characteristics of suitable habitat for A. heterodon in the Maryland Coastal Plain. Community analyses suggested that landscape, rather than biological, surrogates would be preferable for predictive habitat modeling. Subsequent MaxEnt modeling associated A. heterodon habitat in the Maryland Coastal Plain with the following variables: depth to the water table, pasture/hay land cover, woody wetlands, low intensity development, Tertiary-aged sediments, and minimum elevation. The results from this model directed field work to evaluate thermal, geochemical, and physical characteristics of A. heterodon reaches throughout the species' range. Paired air-water temperature sensors placed in A. heterodon reaches suggested a potential thermal threshold of 29°C. Southern sites had higher maximum water temperatures but exhibited less diurnal variation and lower rates of temperature change than northern sites; characteristics that suggest intermediate to deep groundwater sources. Physical and chemical characteristics were measured along the length of Flat Brook, a stream with A. heterodon in the Delaware River basin. Data indicated that the mussel occurred in reaches that were stable during bankfull and lower discharges and water chemistry data indicated saturation with respect to aragonite during summer base flow. Field studies suggest several potential essential habitats for A. heterodon: (1) habitats with stable streambeds at bankfull and lower discharges; (2) stream waters in equilibrium with aragonite precipitation during baseflow conditions; and (3) habitats with maximum temperatures < 29°C and stable thermal regimes. The different thermal regimes and contributing groundwater sources between northern and southern populations suggest that geographic region be a consideration in species' reintroductions. Until essential habitats are identified and management plans instituted, all populations should be similarly protected and the loss of individual populations prevented.Item NOVEL APPROACHES TO STUDYING BIODIVERSITY IN REMOTE AREAS: DISTRIBUTION OF LICHENS AND PENGUINS ACROSS THE ANTARCTIC PENINSULA(2013) Casanovas, Paula Victoria; Fagan, William F; Lynch, Heather J; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Biodiversity inventories are a critical resource, providing baseline information for assessing environmental changes over time. In many cases, the underlying datasets are generated by "opportunistic" sampling efforts or they are consolidated from diverse datasets collected for different purposes. These datasets are typically patchy and incomplete, requiring the use of sophisticated statistical analyses. The Antarctic Peninsula (AP) is one of those areas where direct observation of species distribution is difficult; it is also an area that in recent decades has been experiencing important environmental changes, which influence population and ecosystem dynamics. I addressed biogeographical questions in the AP archipelago, using remote sensing and opportunistic data sets for two very different groups of organisms: lichens and penguins. Although taxonomically different, both groups are key components of the AP terrestrial ecosystem, and share the need to couple biodiversity surveys with modeling to understand species distribution and abundance patterns in large areas of remote wilderness. The results of this dissertation work are interesting to polar biologists, because evidence suggests that the input of nutrients by seabirds can significantly impact floral diversity and abundance in nutrient-poor polar communities. The datasets and protocols for data collection and analyses generated in this project are valuable in themselves for the scientific community. They could be used as the basis for a valuable and practicable monitoring program and procedures for the evaluation of the data derived from it. In the Antarctic Peninsula in particular, this information will aid in the delineation and management of protected areas, as well as in the evaluation of the impacts of climate change and human visitation to the most traveled locations. Furthermore, this research provided an example of how an approach that integrates the use of existing remote-sensing products with independent ongoing field sampling efforts, "citizen scientist" data collection, and historical datasets can yield low-cost, high-benefit studies that can be useful both to understand how species respond to their environment, and to help environmental managers to predict and cope with imminent changes due to global warming.