MEES Theses and Dissertations
Permanent URI for this collectionhttp://hdl.handle.net/1903/19655
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Item MOVING THE GOALPOSTS: MIGRATORY BIRDS IN A CHANGING WORLD(2023) Nemes, Claire E.; Cohen, Emily B; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Billions of birds undertake migratory movements each year, traveling distances that range from several hundreds to tens of thousands of kilometers. Migratory birds must be flexible enough to cope with the fluctuating conditions they encounter during these journeys and at their destinations. However, humans are rapidly and dramatically changing the environment across all portions of migratory species’ ranges through habitat destruction and conversion, introduction of invasive species, climate change, and other alterations. My dissertation research seeks to understand the constraints and threats facing birds during two understudied phases of the annual cycle: migration and the non-breeding stationary period. In Chapter 1, I explore how human activities may nonlethally affect birds during migration. I reviewed the scientific literature for evidence of nonlethal effects and of interacting threats that may compound fitness costs to migrating birds. In general, I found that scientific understanding of nonlethal effects during migration lags behind research on direct mortality. Because birds migrate through increasingly anthropogenic landscapes and airspaces, I identify this knowledge gap as a hindrance to effective conservation of migratory birds. In Chapter 2, I investigate if individual songbirds adjust the rate and timing of spring migration based on the vegetation phenology they encounter within North America which may allow them to keep pace with advancing spring phenology under climate change. In the spring, migrating birds must quickly reach their breeding grounds to secure territories and mates ahead of the competition, but individuals that arrive too early may encounter inclement weather or food shortages. Using the Motus automated radio telemetry network, I tracked individual songbirds as they traveled from the southern U.S. towards their breeding areas in spring. I used estimates of spring onset timing at different points on their migration routes to determine if birds traveled in sync with the “green wave” of emerging vegetation or if they used a different strategy. I found that birds migrating from their non-breeding areas arrived in the southern U.S. well after local spring onset, but were able to catch up to the wave of emerging spring vegetation as they traveled northwards, following a “catching up” strategy rather than a “surfing” one. In Chapter 3, I examine how individual songbirds respond to the threat of predation during migratory stopover, when they must balance conflicting demands of refueling and avoiding predators. Migrating birds must contend with both native avian predators such as hawks (Accipiter sp.) and abundant introduced predators such as free-roaming domestic cats (Felis catus), yet their behavioral responses to cats have been little studied during migration. Using an aviary experiment, I exposed wild Gray Catbirds Dumetella carolinensis to either a hawk or a domestic cat and observed their behaviors before and after exposure to determine if they responded appropriately to the threat posed by each predator. When compared with a control group, Catbirds responded differently to both types of predators in the short term, but I detected no differences in their behavior after release. This study provides novel insights into the possible nonlethal effects of introduced predators that birds may encounter during migration. In Chapter 4, I shift focus to explore the threat that free-roaming domestic cats pose to birds in the Caribbean within a Neotropical city. Urban regions are increasingly recognized to provide valuable wildlife habitat but may also contain hazards such as introduced predators, and we currently lack information on the effects of free-roaming cats on migratory and resident bird species during non-breeding seasons. I designed a camera trapping project in San Juan, Puerto Rico to estimate free-roaming cat densities across a gradient of urbanization as a step towards understanding their potential impacts on wildlife. I deployed cameras across 16 trapping grids at three levels of urbanization and used photographic captures of cats to build spatial capture-recapture models. Estimated cat densities ranged from 48 8 (SE) cats/km2 in exurban areas to 473 40 cats/km2 in the most heavily urbanized parts of the city. These data may prove useful for conservation practitioners in San Juan deciding where to target cat management efforts for the benefit of urban wildlife and public health.Item Understanding the Reproductive Biology and Endocrinology of the Female Red Deep-Sea Crab, Chaceon Quinquedens(2022) Green, Shadaesha Renee; Chung, J. Sook; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)The red deep-sea crab, Chaceon quinquedens, a cold-water decapod found along the continental shelf and slope of the eastern United States has a limited amount of literature available describing their physiological processes. The present research aimed to advance the current knowledge of the reproductive physiology of C. quinquedens females by investigating essential hormones regulating vitellogenesis and ovarian development. In decapod crustaceans, members of the crustacean hyperglycemic hormone (CHH) superfamily control molting, growth, and reproduction, while reproduction and somatic growth are antagonistic. The red deep-sea crab with an extended intermolt period may adopt a similar approach to the blue crab, Callinectes sapidus, which utilizes the molt-inhibiting hormone (MIH) as a gonad-stimulating factor. Hence, a relationship between MIH and CHH levels and vitellogenin is examined, together with the potential role of other eyestalk neuropeptides in vitellogenesis using a transcriptomic analysis. Ten of the 28 eyestalk-neuropeptides found in the de novo assembly are differentially expressed between ovarian stages 1 and 3, suggesting their role in vitellogenesis. The onset of vitellogenesis (synthesis of vitellogenin, the precursor of vitellin) initiates the ovarian development of all oviparous animals. Decapod crustaceans mainly utilize two tissues for vitellogenesis: hepatopancreas and ovary. The hepatopancreas of most crab species is the primary site for vitellogenesis, producing >99.9% of vitellogenin for ovarian development, while the ovary takes up vitellogenin subunits from the hemolymph. It is found using qPCR assay that the hepatopancreas of C. quinquedens also is the main site and provides >99.9% of vitellogenin. The following is then investigated on how the vitellogenin is cleaved into two subunits using a transcriptomic analysis. First, two transcripts are pieced together to obtain the putative 2,570 amino acid vitellogenin protein. Following three subtilisin-like endopeptidases are found in the de novo assembly, potentially cleaving vitellogenin into subunits: trypsin-like serine protease, furin, and proprotein convertase subtilisin/Kexin7. Since the 1970s, the red deep-sea crab has been supporting a small fishing industry in the Atlantic Ocean, mainly harvesting adult males with >94 mm carapace width. However, a recent study reports that there is a reduction in the size of the males. To address the population structure of this species in the future, microsatellite markers are developed using MiSeq data combined with a bioinformatic pipeline. Over 37,000 microsatellites are identified, from which 122 markers are considered for initial PCR testing with a limited number of crabs. Overall, 14 novel, polymorphic microsatellite markers are developed. In conclusion, the reproduction of female C. quinquedens is regulated by eyestalk neuropeptides. With this study, the reproductive role of MIH needs investigating in the decapod crustaceans experiencing an extended intermolt stage. Novel microsatellite markers developed here will assist to study population structure and connectivity that will help towards the conservation of this species facing increasing fishing pressure.Item PREDICTING THE SALINITY HISTORY OF OYSTERS IN DELAWARE BAY USING OBSERVING SYSTEMS DATA AND NONLINEAR REGRESSION(2022) HOWLADER, ARCHI; NORTH, ELIZABETH; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Salinity is a major environmental factor that influences the population dynamics of fish and shellfish along coasts and estuaries, yet methods for predicting the salinity history at specific sampling stations are not widely available. The specific aim of this research was to predict the history of salinity experienced by juvenile and adult oysters (Crassostrea virginica) collected at sampling stations in Delaware Bay as part of the Selection along Estuarine Gradients in Oysters (SEGO) project. To do so, empirical relationships were created to predict salinity at five oyster bed stations using observing systems data and then applied to construct indices of salinity exposure over an oyster’s lifetime. The desired accuracy was +/- 2 psu. Three independent sources of salinity data were used in conjunction with observing systems data to construct and validate the predictive relationships. Observing systems data from the USGS station at Reedy Island Jetty and continuous near-bottom measurements taken by the U.S. Army Corps of Engineers (ACOE) from 2012-2015 and 2018 were employed to fit nonlinear empirical models at each station. Haskin Shellfish Research Laboratory (Haskin) data were used to evaluate model fit, then ACOE data from 2018 (withheld from model fitting in the validation analysis) and SEGO data from 2021 were used to validate models. The best-fitting models for predicting salinity at the oyster bed stations given the salinity at Reedy Island Jetty were logarithmic in form. The root mean square error (RMSE) of the models ranged from 1.3 to 1.6 psu when model predictions were compared with Haskin data, 0.5 to 1.5 when compared with ACOE data, and 0.6 to 0.8 when compared with SEGO data. All of these models were within the desired accuracy range. Results demonstrate that observing systems data can be used for predicting salinity within +/- 2 psu at oyster bed stations within 39 km in upper Delaware Bay. When these models were applied to estimate low salinity exposure of 2-year-old oysters via the metric of consecutive days below 5 psu, the indices suggested that there could be as much as a 42-day difference in low salinity exposure for oysters at stations 31 km apart. This study helps further our understanding of the salt distribution in Delaware Bay as well as the effect of low-salinity stress on the life cycle and genetic differentiation of oysters. In addition, the approach of using observing systems data to predict salinity could be applied to advance understanding of salt distribution and the effect of low salinity exposure on living resources in other estuaries.Item Insights into benthic macroinvertebrate ecology in the northern Bering and southern Chukchi Seas from stable isotope analysis(2022) Green, Emma Mackenzie; Cooper, Lee W; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)In the Pacific Arctic Region, the northern Bering Sea and southern Chukchi Sea support large and diverse communities of benthic macroinvertebrates that provide an important link to the pelagic communities and marine mammals that rely on the benthic populations for food. While the abundance and biomass of these benthic macroinvertebrates are well documented, little is known about how benthic macroinvertebrates interact with each other and how these interactions are affected by climate change. I measured the stable isotope composition (bulk δ15N and δ13C values) of similar species collected in 2014, 2016, 2017, and 2021 in the northern Bering and southern Chukchi Seas. Although there was little change over time in either δ15N or δ13C values, both stable isotope ratios were significantly different between stations with differing production phenologies. The southern Chukchi Sea (a productive set of sites with high chlorophyll concentrations throughout the summer) had lower δ15N values and higher δ13C values, while the northern Bering Sea site with production mostly associated with the period of sea ice breakup had higher δ15N values and lower δ13C values. This pattern was observed across similar species and feeding types. The higher δ15N values in the northern Bering Sea could be due to an extra step in the food chain from bacterial reworking. The contrast between these two regions in δ13C might indicate higher primary production in the southern Chukchi Sea compared to the northern Bering Sea. The differing food web dynamics between these two sites highlight the benthic diversity across small scales and similar organisms in Pacific Arctic food webs.Item DRIVERS OF EPIBENTHIC BIODIVERSITY AND ABUNDANCE IN BARROW CANYON, CHUKCHI SEA UTILIZING DROP CAMERA VIDEO DATA(2022) Pfaff, Andrea Ruth; Grebmeier, Jacqueline M; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)In the Northeastern Chukchi Sea’s Barrow Canyon, modeling indicates that converging currents rapidly downwell high volumes of labile carbon creating a benthic biological hotspot. Utilizing a Drop Camera Video System, this thesis analyzes the epibenthic population across upper Barrow Canyon along the Distributed Biological Observatory transect DBO5. Results show that overall abundance of epibenthic fauna is highly correlated with depth while diversity is correlated with water mass variables such as bottom water temperature, salinity, nutrient concentrations, current speeds, and sediment grain size. Higher taxonomic diversity is found along the inshore slope of Barrow Canyon and correlated with conditions associated with the swifter inshore Alaskan Coastal Water. Taken together these data show that while particulate food and associated epibenthic abundance is highest in the Canyon’s trough, there is a zonation of organisms between the inshore and offshore slope with the inshore slope supporting a higher diversity and predominantly suspension feeding organisms.Item EFFECTS OF SHELL DAMAGE ON MORTALITY OF THE EASTERN OYSTER (CRASSOSTREA VIRGINICA) IN NORMOXIC AND ANOXIC CONDITIONS(2022) Schlenoff, Jake I; Miller, Thomas; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Deoxygenation is increasingly problematic in coastal waters globally, with many costal estuaries subject to zones of hypoxia (< 2 mg/L dissolved oxygen) or anoxia (< 0.5 mg/L dissolved oxygen). The presence of hypoxic and anoxic zones can place a unique physiological burden on marine fauna and flora, potentially leading to mass mortality and resulting in dead zones. Anthropogenic stressors, such as increased nutrient input (primarily Nitrogen and Phosphorus), have led to long-term increases of hypoxia in the Chesapeake Bay over the 20th century. Although environmental management policies for the Bay have mitigated hypoxia trends, hypoxia continues to be prevalent through many parts of the Bay. While motile aquatic organisms can change locations to avoid seasonal or long-term bouts of deoxygenation, organisms with sessile adult life stages cannot move to avoid this ecological stressor. The Eastern Oyster (Crassostrea virginica) is a foundational species in the Chesapeake Bay’s ecosystem, performing many ecosystem services such as water filtration, nutrient cycling, and fostering benthic-pelagic connectivity while also serving as an economic resource for commercial fishing. However, long-term trends in hypoxia and anoxia, combined with other anthropogenic stressors, have contributed to a decline in Eastern Oyster in the Bay, leaving populations at a fraction of historical levels, fostering a need for research to better understand the physiological and biomechanical responses of C. virginica to depletion of dissolved oxygen. While the Eastern Oyster has been termed a champion of hypoxic tolerance, and studies have been published exploring the impacts of low DO on oyster mortality and sublethal responses, research is still in search of answers to whether the response of the oyster comes from shell-based behavioral resilience to isolate the animal from environmental conditions, or physiological adaptions from the tissue of the oyster. By drilling holes of three different sizes into one valve of the oyster and exposing it to anoxic external conditions, this study aims to bridge the gap in knowledge of whether anoxic tolerance is a behavioral or physiological response. Oysters with a hole drilled in the shell of any size experienced much faster mortality in anoxic environments than oysters with no hole in the shell (χ2= 8, p = 0.005), while the size of the hole drilled did not impact time to death. These results shed new light on the behavioral response of the Eastern Oyster to depleted dissolved oxygen and the importance of clamping to ostracize internal tissue from environmental deviations.Item INSIGHTS INTO DINOFLAGELLATE NATURAL PRODUCT SYNTHESIS VIA CATALYTIC DOMAIN INTERACTIONS(2022) Williams, Ernest Patrick; Place, Allen R; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Dinoflagellates are protists that can be split into two evolutionary groups, the parasitic syndinians and the largely photosynthetic “core” dinoflagellates. They represent a major portion of aquatic biomass which means that they are responsible for large portions of carbon that are both fixed and released. Other than biomass, the fixed carbon can be made into natural products such as polyunsaturated fatty acids that support the biota of many ecosystems or toxins that are harmful to aquatic life and humans. DNA and RNA analyses have been used to discover the putative genes that may make these compounds, but their non-colinear arrangement in the genome is very different from model organisms and their gene copy number is very high, making it nearly impossible to determine the exact biosynthetic pathways. The goal of my studies was to develop methods to differentiate biosynthetic pathways such as lipid and toxin synthesis by comparing the ability of domains to interact with each other with the assumption that domains that preferentially interact are more likely to participate in the same pathway. Initially, a survey was performed on available dinoflagellate transcriptomes to enumerate domains potentially involved in natural product synthesis and bin them based on sequence similarity to identify genes that could be used in biochemical assays. An interesting integration of analogous genes involved in lipid synthesis with those involved in natural product synthesis was observed as well as trends in domain expansion and contraction during core dinoflagellate evolution. Ultimately, the domain that scaffolds natural product synthesis, the thiolation domain, was chosen for further study because it exhibited two clear functional bins and is acted on directly by another enzyme, a phosphopantetheinyl transferase (PPTase). The PPTase activates the thiolation domain by transferring the phosphopantetheinate group from Coenzyme A to the thiolation domain, creating a free thiol group upon which the natural products are synthesized. These PPTases were then enumerated in dinoflagellates and characterized by looking for sequence motifs and observing expression patterns over a diel cycle as well as during growth in the model species Amphidinium carterae, a basal toxic dinoflagellate. Amphidinium carterae appears to have three PPTases, two of which (PPTase 1 and 2) are very similar, except that PPTase 2 does not appear to have a stop codon and has never been observed as a full-size protein. The remaining two PPTases (PPTase 1 and 3) had alternating expression patterns that did not appear to directly correlate to the acyl carrier protein, the thiolation domain required specifically for lipid biosynthesis. This carrier protein, like other enzymes for natural product synthesis in dinoflagellates, had a chloroplast targeting sequence while the three PPTases did not. To investigate the ability of these three PPTases to activate various thiolation domains, a total of 8 domains from A. carterae were substituted into the blue pigment synthesizing gene BpsA from Streptomyces lavendulae. These recombinant constructs were used for coexpression in E. coli as well as in vitro to reduce as many artifacts as possible and assess the interactions of each PPTase with the thiolation domains. Some of the recombinant BpsA genes were able to make blue dye with all three PPTases, while others never made blue dye both in E. coli as well as in vitro. In vitro quantification of free thiol added by the PPTase showed that all the thiolation domains, as well as the acyl carrier protein could be phosphopantetheinated by all the PPTases. This generalist substrate recognition, along with the alternating expression patterns and lack of chloroplast signaling peptide, indicate that the two active PPTases are performing the same function on all available thiolation domains, probably before export to the chloroplast. This lack of pathway segregation by PPTases is a completely novel way of synthesizing natural products compared to bacteria and fungi, likely due to the acquisition of both photosynthesis and natural product/lipid biosynthesis during dinoflagellate evolution that was not present in the common ancestor. Additionally, the techniques to identify genes of interest and perform biochemical characterization developed here are useful for future experiments annotating the function of dinoflagellate genes.Item EXAMINING THE GENETIC BASIS AND PHYSIOLOGY OF SURVIVAL IN EXTREME LOW SALINITY TO IMPROVE AQUACULTURE OF THE EASTERN OYSTER Crassostrea virginica(2022) McCarty, Alexandra J; Plough, Louis; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)The eastern oyster, Crassostrea virginica, is an important aquaculture species and supports a growing industry along the east coast of the United States. However, increases in freshwater from storm events and intentional diversions can expose coastal aquaculture operations to extreme low salinity (< 5), resulting in reduced productivity and mortality. The primary objectives of this dissertation were to investigate the biology and genetic basis of low salinity tolerance to improve eastern oyster aquaculture. In Chapter 2, I developed and conducted a series of extreme low salinity (2.5) challenges to estimate the quantitative genetic parameters of low salinity survival. A moderate narrow-sense heritability was estimated for challenge survival, h2 ≈ 0.4. In addition, osmolality of hemolymph collected from oysters during the first week of the challenge suggest that all individuals conformed to the surrounding low salinity regardless of challenge survival. In Chapter 3, I performed additional low salinity challenges to assess the importance of challenge duration (2 or 6 months) and temperature (chronic or fluctuating) on low salinity survival. I also investigated algae removal during the chronic challenge to better understand oyster response during low salinity stress. Phenotypic (rS = 0.89) and genetic (rG = 0.81) correlations between family mortality were high across the two challenges, indicating that a 30-day exposure at a constant low salinity (2.5) and temperature (27°C) is a sufficient progeny test for low salinity survival. Modest associations between algae removal metrics and survival in extreme low salinity indicate that individual feeding ability may relate to differential low salinity survival. Lastly, in Chapter 4, I performed genome mapping to investigate the genomic architecture of low salinity survival. Quantitative trait locus mapping and linkage disequilibrium analysis revealed a significant region on eastern oyster chromosome 1 and 7. Genomic prediction accuracies for survival and day to death in extreme low salinity were moderate and encouraging, 0.49 – 0.57. The results from my dissertation characterize the genetic basis of survival during low salinity events and support the incorporation of this trait into breeding efforts to improve production and enhance the resiliency of the eastern oyster aquaculture industry.Item PHYSIOLOGICAL, MOLECULAR, AND ECOLOGICAL RESPONSES OF THE EASTERN OYSTER, CRASSOSTREA VIRGINICA, TO HYPOXIA EXPOSURE IN THE CHESAPEAKE BAY(2021) Davis, Anna Manyak; Plough, Louis; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Hypoxia is a naturally occurring phenomenon in coastal waters that is increasing in frequency and extent due to human activities. There is a pressing need to understand how organisms will be able to respond and adapt to future oxygen limitation. The eastern oyster, Crassostrea virginica, is an ecologically important bivalve that is threatened by the increasing incidence of low oxygen events. Little is known about the capacity of C. virginica to cope with projected deoxygenation or the potential ecological implications of reduced oxygen availability. The primary objectives of this dissertation research were to 1) characterize the intraspecific variability in physiological and molecular responses to hypoxia for oysters from the Chesapeake Bay and 2) develop a model to predict the implications of hypoxia on oyster population ecology. In Chapter 2 I assessed the survival and heart rate responses under low oxygen stress for oysters sourced from reefs experiencing varying frequencies of hypoxia exposure. Results indicated that prior hypoxia exposure does not confer increased survival under low oxygen stress but may relate to sublethal physiological differences in tolerance, particularly for oysters with a greater frequency of prior hypoxia exposure. In Chapter 3, I used four different analytical approaches, principal components, differential gene expression, co-expression gene network, and transcriptional frontloading analyses, to assess intraspecific differences in oyster transcriptomic response to hypoxia. No statistically significant differences in gene expression response between sites were observed indicating that prior hypoxia exposure may not have affected the regulation of expression under hypoxic stress. However, while not statistically significant, gene expression patterns suggested transcriptional frontloading as a possible mechanism of increased hypoxia tolerance in oysters. Finally, in Chapter 4, I developed a Dynamic Energy Budget model integrating dissolved oxygen concentration as a forcing variable to make predictions about oyster growth and reproduction under varying oxygen conditions. Model outputs indicated that low oxygen exposure reduces oyster growth, fecundity, and spawning frequency. Collectively, this dissertation research affirms that low oxygen availability negatively affects oyster physiology and ecology, and emphasizes the importance of continued research into the capacity of oysters to tolerate future increases in coastal hypoxia.Item EXAMINING HIBERNATION IN THE BIG BROWN BAT THROUGH DNA METHYLATION(2021) Sullivan, Isabel; Wilkinson, Gerald S; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Hibernation allows individuals to conserve energy during seasonal low temperatures. As the physiological regulation of hibernation is inadequately understood, I examine hibernation using DNA methylation (DNAm). DNAm is the addition of a methyl group to cytosine at cytosine guanine dinucleotide (CpG) sites in the genome. DNAm in promoters can repress gene expression and be influenced by histone modifications. Using the big brown bat, Eptesicus fuscus, I examined how hibernation influences DNAm, independent of age, through comparing DNAm from bats that differed in hibernation history and comparing DNAm from the same individual between hibernating and active seasons. Both comparisons found evidence of differential enrichment of genes near significant CpG sites resulting from hibernation. The latter analysis found evidence consistent with a histone mark, associated with active transcription, is likely enriched in hibernating bats. These results suggest that DNAm and histone modifications associated with transcription factor binding regulate gene expression during hibernation.