Emerging infectious diseases in aquatic systems, both in aquaculture and in the wild, are a global concern. Many have proposed an uptick in marine diseases as a result of environmental changes including a warming climate, habitat modifications, trade and transfer of wildlife and aquaculture products, pollution, overharvesting of resources, and other anthropogenic impacts. These perturbations can disturb the delicate host-pathogen relationships and result in new diseases or exacerbate the existing diseases in a population. Diseases can lead to several direct and indirect effects in the ecosystem such as population declines and extinctions, and thereby a change in population dynamics, as well as loss of numerous ecosystem services. Marine diseases can also tremendously distress the local communities that rely on them by affecting their livelihoods, sustenance, and culture. Understanding the etiology, epidemiology, and the impacts of a disease is the key to its management. However, this can be particularly challenging in cases of understudied and emerging diseases, as there are several unknowns and time is of the essence for disease mitigation and future prevention. Here, we investigated an emerging infectious disease, called the ‘red sore disease (RSD)’, in American eels in the Chesapeake Bay region with the aim of enhancing the sustainability of American eel fishery and aquaculture. The American eel is the only species of freshwater eel found in the North America and is an ecologically and economically important finfish. RSD is characterized by skin lesions on eels and is reported to cause high mortality by the eel distributors in the Chesapeake Bay. Our findings provide new information on the biotic and abiotic drivers of RSD in the American eels in the Chesapeake Bay region. First, we explored the microbial and environmental correlates of RSD in American eel aquaculture in the Chesapeake Bay region by sampling diseased animals at two different aquaculture operations. We developed a scale to score the severity of RSD in eels. By using standard bacteriological and molecular methods, we identified the disease to be associated with bacteria in the genera Aeromonas and Vibrio. While previous studies have implicated Aeromonas, this is the first report identifying Vibrio as a potential causative agent for RSD in American eels. We also found that increasing temperature was positively associated with the presence of Vibrio spp. in the aquaculture operations. Next, we conducted in vivo laboratory challenges using American eels as experimental animals, to confirm if Vibrio vulnificus, the most commonly isolated Vibrio species from diseased eels, is a causative agent of RSD in American eels by applying Koch’s postulates. We also assessed the role of temperature on clinical severity of RSD. We observed that V. vulnificus led to similar lesions, when injected into fish, as previously documented for RSD in aquaculture. In addition, we found the mortality to be greater and more acute at higher temperatures in this experiment. Lastly, we investigated the etiology and epidemiology of RSD in wild-caught American eels from the York River, Virginia by collaborating with a local commercial eel potter and quantifying the prevalence of RSD bi-weekly. Using previously established methods, we again found aeromonads and vibrios to be the dominant bacteria isolated from diseased eels. Septicemia with Vibrio spp. was also observed and prevalence in the wild was associated with higher temperatures and the longer holding time (number of days eels were held in underwater floating cages). These results expand our overall understanding of RSD in American eels in the Chesapeake Bay region. Our findings suggest that a warming climate may exacerbate RSD in the wild. High temperature and handling stress may also exacerbate the disease in aquaculture. We have identified some best practices for the growing aquaculture industry. Recommendations for reducing disease-associated mortality in aquaculture include improvement of water quality by addition of adequate mechanical and biological filters, maintenance of optimum water temperature, and reducing handling trauma and injury by reducing holding time. Given the prevalence of RSD observed in the wild, there are also important implications for considering disease-associated mortality in the assessment of the wild eel stock along the Mid-Atlantic coast. Further research on RSD in American eels is warranted, particularly as V. vulnificus has zoonotic potential and environmental modeling predicts its abundance to increase in the Chesapeake Bay. Safety of eel handlers in aquaculture operations also needs to be ensured. Critical directions for future research have been detailed and include biochemical profiling of the etiological agents as well as additional investigation of environmental stress as a driver of RSD.

Climate change has altered marine environments, most notably by increasing water temperatures and reducing dissolved oxygen concentrations. These persistent changes have impacted the phenology and spatiotemporal habitat usage of mobile species, often through distributional shifts poleward or to deeper water. Climate-driven distributional shifts have been documented for numerous species inhabiting the Atlantic Ocean along the US East Coast, a region disproportionately affected by climate change. Adjacent estuaries are experiencing similar alterations to their physical environments and biotic community composition. Many estuarine species are seasonal residents and changes to environmental conditions within an estuary can result in altered usage and residence times. The Chesapeake Bay is one such estuary experiencing these climate-associated effects. The bay serves as an important habitat for a diverse array of seasonally resident marine and estuarine taxa, providing valuable foraging, refuge, and spawning grounds. Concurrent with physical changes, survey data have indicated decreases in relative abundance of many finfishes. However, environmental drivers associated with these declines have not been fully quantified. To evaluate the role of climate change on spatiotemporal habitat usage of Chesapeake Bay fauna, state-of-the-art statistical models were applied to several long-term monitoring data sets. Changes in Chesapeake Bay inhabitance by a suite of seasonally resident species were explored by evaluating estuarine-coastal ocean exchange and comparing the patterns to a more northern estuary, Delaware Bay. Relative habitat utilization of Chesapeake Bay declined for most species, while utilization patterns for Delaware Bay were largely constant or increasing over time. Broad-scale, multispecies analyses of relative habitat utilization time series revealed that the North Atlantic Oscillation, a signal of long-term warming, was an important driver of Chesapeake Bay exchange. Baseline habitat associations for several seasonal resident species in Chesapeake Bay were quantified through the development of ecological niche models. Model output indicated that impacts of climate change on environmental conditions of the bay, including continued increases in temperature and hypoxic volume, will likely exacerbate the decline in relative abundance. The niche envelopes were paired with an estuarine-carbon-biogeochemical regional ocean model to derive estimates of habitat suitability. The temporal patterns in habitat suitability did not match abundance trends, indicating that dynamics outside of the physical conditions of Chesapeake Bay are likely driving the decreased utilization of this estuary. Finally, the traditional mark-recapture modeling framework that includes catch-and-release fishing was extended to a subannual, multi-stock, spatially and temporally explicit version that allowed for simultaneous estimation of key parameters, including mortality rates and occupancy probabilities. Model estimated instantaneous natural mortality increased over time within Chesapeake Bay, particularly for older fish, but has not changed appreciably outside of the estuary, supporting previous findings of increased disease-associated mortality with age, and a possible role of climate change-associated suboptimal environmental conditions. Estimated occupancy probabilities exhibited differences in likelihood of estuarine inhabitance based on age, season, and producer region. Collectively, the results demonstrate heterogeneous changes in spatiotemporal habitat use of several Mid-Atlantic species on various scales. This information can be used by managers tasked with temporally and spatially dynamic policy development in a changing environment.

Harmful algal blooms (HABs) and their associated phycotoxins pose a threat to both human and shellfish health around the world. Dinophysis spp., a causative organism of diarrhetic shellfish poisoning (DSP) in humans, and its two toxin classes: dinophysistoxins (DTXs) and pectenotoxins (PTXs), have been documented throughout the year in the Chesapeake Bay. While DTX concentrations currently remain below regulatory limits in regional seafood products, further research is needed to understand environmental drivers, both biotic and abiotic, that may be impacting Dinophysis spp. feeding on prey, growth, and toxin production. To characterize populations of Dinophysis in situ, an Imaging FlowCytobot (IFCB) was deployed off the Virginia Institute of Marine Science (VIMS) pier for five sampling seasons. The IFCB captures images of phytoplankton cells every ~20 minutes, generating large, continuous data sets that are then automatically classified using a machine learning algorithm, in this case, a convolutional neural network (CNN) framework. The IFCB-generated abundance data for the dinoflagellates Dinophysis acuminata, and Prorocentrum cordatum, as well as the ciliate Mesodinium rubrum, were then incorporated into an ecological predictive model along with abiotic variables such as sea surface temperature, salinity, turbidity, pH, and discharge. Given that Dinophysis is an obligate mixotroph, the relationship between bloom timing of the prey item M. rubrum and D. acuminata were explored by fitting models with no lag of M. rubrum, a 14-day lag, and a 75-day lag. Additionally, P. cordatum abundance was explored as a proxy for D. acuminata abundance. Results revealed that D. acuminata abundance was significantly linked with salinity, time of year, M. rubrum abundance with a 14-day lag, and P. cordatum abundance. The results of this study provide further insight into potential biotic and abiotic factors regulating Dinophysis populations in Chesapeake Bay.To test another possible abiotic factor, turbulence, a culturing study was undertaken in the laboratory with four isolates of three species of Dinophysis: D. acuminata, D. ovum, and D. caudata. These isolates, from the Gulf and East Coasts of the U.S., were exposed to two levels of turbulence for six days to determine its effect on feeding, growth, and toxin production. While an effect of turbulence on ingestion rates of M. rubrum by Dinophysis was not detected, exposure to high turbulence inhibited growth of both D. acuminata and D. ovum and stimulated growth of D. caudata. As a result of inhibited growth, both D. acuminata and D. ovum had reduced toxin production rates, but D. acuminata was shown to accumulate toxin inside cells, while D. ovum released toxin extracellularly into the media. Conversely, the stimulation of growth for D. caudata resulted in decreased intracellular toxin content, but no effect on toxin production rate. While understanding phytoplankton population dynamics in the natural environment is complex, the results of these studies highlight some important environmental factors impacting Dinophysis spp. feeding, growth, and toxin production in the lab and field in both Chesapeake Bay and the East and Gulf Coasts of the U.S.

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The istiophorid billfishes (marlins, spearfishes, and sailfish) are highly migratory pelagic fishes exhibiting broad and continuous spatial distributions in the Atlantic, Pacific, and Indian oceans. These species are targeted by a number of recreational, commercial, artisanal, and subsistence fisheries worldwide, and are also caught as bycatch in pelagic longline fisheries targeting tunas and swordfish. Though stock assessments have not been conducted for all istiophorids, assessments available for some species indicate that many istiophorid stocks are overfished and/or experiencing overfishing. However, the development of stock-specific recovery efforts is often impeded by a lack of information on basic species biology, including stock structure. The species status of some istiophorids is also uncertain, further complicating management efforts as well as strategies to conserve genetic diversity characteristic of distinct evolutionary lineages. In this dissertation, a molecular approach is used to address questions currently contributing uncertainty to the conservation and management of two istiophorid billfishes, white marlin (Kajikia albida) and striped marlin (K. audax). These closely related sister species are distributed in the Atlantic and Indo-Pacific oceans, respectively. Previous assessment of genetic population structure for white marlin based on mitochondrial (mt) DNA and five nuclear microsatellite markers suggested the possibility of population structuring for this species; however, results from the evaluation of mtDNA and 24 microsatellites across a larger number of samples, including a collection of larvae, are consistent with the presence of a single genetic stock (Chapter II). This result highlights the importance of analyses based on large numbers of molecular markers and samples, as well as a biologically informed sampling design, for studies of population structure in highly migratory pelagic species. Compared to the apparent lack of genetic population structure for white marlin, analysis of nearly 4,000 single nucleotide polymorphism (SNP) molecular markers across collections of striped marlin from the Pacific and, for the first time, Indian oceans resolved multiple genetically distinct populations (Chapter III). These populations correspond with striped marlin sampled from the western Indian Ocean, Oceania, North Pacific Ocean, and eastern central Pacific Ocean. Results from individual-based cluster analyses also suggest the presence of a second genetically distinct population in the North Pacific Ocean. Comparisons of replicate sample collections for some regions demonstrate the stability of allele frequencies across multiple generations. Finally, the uncertain species status of striped marlin and white marlin was evaluated using over 12,000 genome-wide SNPs surveyed across large numbers of exemplars per species (white marlin: n = 75, striped marlin: n = 250; Chapter IV). Results from individual-based cluster and maximum likelihood phylogenetic analyses suggest the presence of distinct evolutionary lineages for striped marlin and white marlin. This result is consistent with levels of genetic differentiation between striped marlin and white marlin which are an order of magnitude higher than those calculated between populations of striped marlin. Collectively, results of this dissertation provide practical insights for improving the conservation and management of white marlin and striped marlin, including revised stock structures which should be recognized in assessment and management plans for striped marlin. Future genomic studies should focus on addressing uncertainties regarding rangewide stock structure and species relationships for other istiophorids. Additionally, studies which continue to improve the genomic resources available for istiophorid billfishes and other large pelagic fishes may ultimately facilitate the evaluation of questions previously unexplored for the pelagic marine environment, such as localized adaptation and speciation.

Eighty-five monitored sets were used to investigate the interactions of pelagic fishes with commercial pelagic longline gear in the western North Atlantic during the fall mixed species fishery north of Cape Hatteras, North Carolina, and the spring swordfish fishery in the southern Gulf of Mexico and northern Caribbean Sea. This dissertation incorporates four components: (1) direct analyses of longline gear behavior using small time-depth recorders, (2) comparisons of catch rates and mortality of all species caught on size 16/0 non-offset circle and size 9/0 straight-shank J-style hooks, including analyses of time-of-capture utilizing electronic hook time recorders, (3) an evaluation of post-release survival of white marlin captured by longline gear using pop-off satellite archival tags (PSATs), and (4) a description of two PSATs attached to white marlin and subsequently ingested by sharks. Data indicated that pelagic longline gear in the shallow coastal U.S. fishery is frequently in motion, even after hooks were presumed to have settled at depth. Effective fishing depths of the gear under several configurations were also shallower than predicted by commonly used catenary curve-based depth calculations. Catch rates between circle and J-style hook types were similar for most species, with only pelagic rays in the fall fishery showing an increased catch rate with J-style hooks. Yellowfin tuna and dolphinfish caught on circle hooks in the fall fishery were larger than those caught on J-style hooks. Most species were more commonly caught in the mouth with circle hooks rather than internally. A total of 28 white marlin were tagged with PSATs. Transmitted data from 17 of 19 reporting PSATs demonstrated survival following release. Estimates of post-release survival range from 60.7% (assuming that non-reporting tags were mortalities) to 89.5% (excluding non-reporting tags from the analysis). Two white marlin PSATs reported data consistent with predation or scavenging by sharks, including ingestion of the tags for seven and ten days respectively. This suggests that non-reporting PSATs may also be the result of unreported biological interactions.

The blue crab is an iconic species in Chesapeake Bay, supporting important commercial and recreational fisheries and functioning as a critical link in the food web. Structurally complex habitats are often cited as nurseries for the blue crab, and other commercially important fish and crustacean species, by providing enhanced growth and survival for juveniles. I quantified the value of shallow habitats as nurseries for blue crabs through field studies and a demographic model. In Chapter 2, I utilized a two-year juvenile survey in vegetated habitats of the lower Bay to examine the effect of habitat complexity on the density of juvenile blue crabs. The functional relationship between seagrass cover and juvenile density was exponential, such that there were proportionally more crabs per unit increase in cover of vegetated habitat at high percent cover than at low percent cover. The relationship varied spatially, with higher densities on the eastern shore, and between the two years. The high spatial and annual variability led to questions about how habitat utilization varied throughout the recruitment season. I addressed the timing of recruitment and migration between habitats in Chapter 3 through the development of a survey of shallow habitats in the York River with high temporal and spatial resolution. The study provided evidence for a carrying capacity of juvenile blue crabs in vegetated habitats at 10-15 crabs m2. I found substantially higher densities of small juveniles in shallow unvegetated habitats than previously documented, which suggested that the current paradigm for blue crab recruitment requires modification to include the importance of shallow unvegetated habitats for small juveniles. In Chapter 4, I examined the effect of habitat utilization patterns as a function of age or ontogeny on the blue crab stock assessment by comparing juvenile density and abundance estimates from shallow vegetated and unvegetated habitats to estimates from deep habitats sampled by the primary survey for the stock assessment. Juvenile abundance was very high in both shallow habitats despite the relatively smaller area, thus suggesting that the winter dredge survey substantially underestimated the abundance of juvenile crabs. If this bias is inconsistent inter-annually, potentially as a function of temperature, then stock assessments may be producing biased reference points. Finally, I developed an exploratory habitat-specific demographic model to quantify the effects of habitat on population fitness in Chapter 5. Under all fishing mortality rates, including a complete fishing moratorium, the population growth rate was less than 1 when only unvegetated habitat was present; the increased survival of age-0 crabs provided by vegetated habitats led to increases in the population growth rates. The vegetated habitats provided a buffer from fishing mortality; that is, as the survival of juveniles increased in vegetated habitats, the population could sustain higher fishing mortality rates while still remaining stable or even increasing. Shallow vegetated habitats substantially influence juvenile blue crabs and the overall population growth rate. It is essential that these habitats be considered in future explorations of the dynamics of blue crabs, as well as other species that exhibit ontogenetic shifts in habitat utilization.

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