Effects of multiple stressors on the dynamics of a fungal pathogen associated with global amphibian declines

Within the biological sciences there is increasing interest in understanding how ecological context alters host-pathogen interactions. Incidences of emerging infectious diseases (EIDs) are increasing around the globe with devastating impacts on many taxonomic groups. This trend is thought to result, in part, from increased frequency or intensity of interactions with stressors that facilitate the spread of a pathogen or increase its virulence. The mechanisms underlying these interactions are poorly understood. This thesis explored how the stress of predators, competitors, and the insecticide malathion alter interactions between the fungal pathogen (Batrachochytrium dendrobatidis, Bd) and two of its amphibian hosts (Rana sylvatica and R. pipiens). Malathion is a widely-used insecticide that has been implicated amphibian declines. I examined how these interactions altered traits associated with within-host interactions (immune responses) and between-host interactions (life history, survival and behavior). More than 200 amphibian species suffer from the EID caused by Bd, and the results of this study suggest that natural environmental stressors can alter patterns of infection. Sublethal exposure to predators caused decreases in releases of antimicrobial peptides (AMPs) from the skin. AMPs are an important defense against infection. The extent of this effect depended on the timing of exposure to predators as well as the length of exposure. In addition, AMPs were also more concentrated in high competition environments. This may be an adaptive response to increased risk of infection by pathogens with density-dependent transmission. Predation would also be expected to reduce disease incidence. Tadpoles infected with Bd were more active than uninfected and resistant tadpoles, suggesting that they would be more susceptible to predation by visually-cued predators. In contrast, resistant tadpoles were the least active, making them most likely to avoid detection by predators. While the pesticide malathion had no effect on susceptibility to Bd infection or antimicrobial peptide releases, a separate study showed that it and other pesticides in the same class (acetylcholine esterase inhibitors) can alter survival and life history trajectories of amphibians through direct toxic effects and indirectly through trait- and density-mediated trophic cascades. Overall these results suggest that environmental context can have complex effects on host-pathogen interactions

Using agent-based modelling to predict the role of wild refugia in the evolution of resistance of sea lice to chemotherapeutants

A major challenge for Atlantic salmon farming in the northern hemisphere is infestation by the sea louse parasite Lepeophtheirus salmonis. The most frequent method of controlling these sea louse infestations is through the use of chemical treatments. However, most major salmon farming areas have observed resistance to common chemotherapeutants. In terrestrial environments, many strategies employed to manage the evolution of resistance involve the use of refugia, where a portion of the population is left untreated to maintain susceptibility. While refugia have not been deliberately used in Atlantic salmon farming, wild salmon populations that migrate close to salmon farms may act as natural refugia. In this paper we describe an agent-based model that explores the influence of different sizes of wild salmon populations on resistance evolution in sea lice on a salmon farm. Using the model, we demonstrate that wild salmon populations can act as refugia that limit the evolution of resistance in the sea louse populations. Additionally, we demonstrate that an increase in the size of the population of wild salmon results in an increased effect in slowing the evolution of resistance. We explore the effect of a population fitness cost associated with resistance, finding that in some cases it substantially reduces the speed of evolution to chemical treatments

Modelling sea lice control by lumpfish on Atlantic salmon farms : interactions with mate limitation, temperature and treatment rules

Atlantic salmon farming is one of the largest aquaculture sectors in the world. A major impact on farm economics, fish welfare and, potentially, nearby wild salmonid populations, is the sea louse ectoparasite Lepeophtheirus salmonis. Sea louse infestations are most often controlled through application of chemicals, but in most farming regions, sea lice have evolved resistance to the small set of available chemicals. Therefore, alternative treatment methodologies are becoming more widely used. One increasingly common alternative treatment involves the co-culture of farmed salmon with cleaner fish, which prey on sea lice. However, despite their wide use, little is understood about the situations in which cleaner fish are most effective. For example, previous work suggests that a low parasite density results in sea lice finding it difficult to acquire mates, reducing fecundity and population growth. Other work suggests that environmental conditions such as temperature and external sea louse pressure have substantial impact on this mate limitation threshold and may even remove the effect entirely. We used an Agent-Based Model (ABM) to simulate cleaner fish on a salmon farm to explore interactions between sea louse mating behaviour, cleaner fish feeding rate, temperature and external sea louse pressure. We found that sea louse mating has a substantial effect on sea louse infestations under a variety of environmental conditions. Our results suggest that cleaner fish can control sea louse infestations most effectively by maintaining the population below critical density thresholds

Evaluation of Striped Bass Stocks in Virginia: Monitoring and Tagging Studies, 2015-2019 Progress Report 1 September 2016 - 31 November 2017

This report presents the results of striped bass (Morone saxatilis) tagging and monitoring activities in Virginia during the period 1 September 2016 through 31 August 2017. It includes an assessment of the biological characteristics of striped bass taken from the 2017 spring spawning run and estimates of annual survival and fishing mortality based on annual spring tagging. Also included is an investigation on the potential use of close-kin analyses to determine the size of the spawning stock in the Rappahannock River and an evaluation of mortality rates associated with the bacterial dermal disease mycobacteriosis in relation to water temperatures and dissolved oxygen. The information contained in this report is required by the Atlantic States Marine Fisheries Commission and is used to implement a coordinated management plan for striped bass in Virginia, and along the eastern seaboard

Dermal mycobacteriosis and warming sea surface temperatures are associated with elevated mortality of striped bass in Chesapeake Bay

Temperature is hypothesized to alter disease dynamics, particularly when species are living at or near their thermal limits. When disease occurs in marine systems, this can go undetected, particularly if the disease is chronic and progresses slowly. As a result, population-level impacts of diseases can be grossly underestimated. Complex migratory patterns, stochasticity in recruitment, and data and knowledge gaps can hinder collection and analysis of data on marine diseases. New tools enabling quantification of disease impacts in marine environments include coupled biogeochemical hydrodynamic models (to hindcast key environmental data), and multievent, multistate mark-recapture (MMSMR) (to quantify the effects of environmental conditions on disease processes and assess population-level impacts). We used MMSMR to quantify disease processes and population impacts in an estuarine population of striped bass (Morone saxatilis) in Chesapeake Bay from 2005 to 2013. Our results supported the hypothesis that mycobacteriosis is chronic, progressive, and, frequently, lethal. Yearly disease incidence in fish age three and above was 89%, suggesting that this disease impacts nearly every adult striped bass. Mortality of diseased fish was high, particularly in severe cases, where it approached 80% in typical years. Severely diseased fish also had a 10-fold higher catchability than healthy fish, which could bias estimates of disease prevalence. For both healthy and diseased fish, mortality increased with the modeled average summer sea surface temperature (SST) at the mouth of the Rappahannock River; in warmer summers (average SST29 degrees C), a cohort is predicted to experience \u3e90% mortality in 1year. Regression of disease signs in mildly and moderately diseased fish wa

Impact of Disease on the Survival of Three Commercially Fished Species

Recent increases in emergent infectious diseases have raised concerns about the sustainability of some marine species. The complexity and expense of studying diseases in marine systems often dictate that conservation and management decisions are made without quantitative data on population-level impacts of disease. Mark-recapture is a powerful, underutilized, tool for calculating impacts of disease on population size and structure, even in the absence of etiological information. We applied logistic regression models to mark-recapture data to obtain estimates of disease-associated mortality rates in three commercially important marine species: snow crab (Chionoecetes opilio) in Newfoundland, Canada, that experience sporadic epizootics of bitter crab disease; striped bass (Morone saxatilis) in the Chesapeake Bay, USA, that experience chronic dermal and visceral mycobacteriosis; and American lobster (Homarus americanus) in the Southern New England stock, that experience chronic epizootic shell disease. All three diseases decreased survival of diseased hosts. Survival of diseased adult male crabs was 1% (0.003-0.022, 95% CI) that of uninfected crabs indicating nearly complete mortality of infected crabs in this life stage. Survival of moderately and severely diseased striped bass (which comprised 15% and 11% of the population, respectively) was 84% (70-100%, 95% CI), and 54% (42-68%, 95% CI) that of healthy striped bass. The disease-adjusted yearly natural mortality rate for striped bass was 0.29, nearly double the previously accepted value, which did not include disease. Survival of moderately and severely diseased lobsters was 30% (15-60%, 95% CI) that of healthy lobsters and survival of mildly diseased lobsters was 45% (27-75%, 95% CI) that of healthy lobsters. High disease mortality in ovigerous females may explain the poor recruitment and rapid declines observed in this population. Stock assessments should account for disease-related mortality when resource management options are evaluated. © 2017 by the Ecological Society of America

Improving marine disease surveillance through sea temperature monitoring, outlooks and projections

International audienceTo forecast marine disease outbreaks as oceans warm requires new environmental surveillance tools. We describe an iterative process for developing these tools that combines research, development and deployment for suitable systems. The first step is to identify candidate host–pathogen systems. The 24 candidate systems we identified include sponges, corals, oysters, crustaceans, sea stars, fishes and sea grasses (among others). To illustrate the other steps, we present a case study of epizootic shell disease (ESD) in the American lobster. Increasing prevalence of ESD is a contributing factor to lobster fishery collapse in southern New England (SNE), raising concerns that disease prevalence will increase in the northern Gulf of Maine under climate change. The lowest maximum bottom temperature associated with ESD prevalence in SNE is 128C. Our seasonal outlook for 2015 and long-term projections show bottom temperatures greater than or equal to 128C may occur in this and coming years in the coastal bays of Maine. The tools presented will allow managers to target efforts to monitor the effects of ESD on fishery sustainability and will be iteratively refined. The approach and case example highlight that temperature-based surveillance tools can inform research, monitoring and management of emerging and continuing marine disease threats

Oysters and Eelgrass: Potential Partners in a High PCO2 Ocean

Ocean acidification (OA) threatens calcifying organisms such as the Pacific oyster, Crassostrea gigas. In contrast, eelgrass, Zostera marina, can benefit from the increase in available carbon for photosynthesis found at a lower seawater pH. Seagrasses can remove dissolved inorganic carbon from OA environments, creating local daytime pH refugia. Pacific oysters may improve the health of eelgrass by filtering out pathogens such as Labyrinthula zosterae, which causes eelgrass wasting disease (EWD). Using a laboratory experiment, we found that co-culture of eelgrass with oysters reduced the severity of EWD. EWD was also reduced in more acidic waters, which negatively affect oyster growth

Managing marine disease emergencies in an era of rapid change

Infectious marine diseases can decimate populations and are increasing among some taxa due to global change and our increasing reliance on marine environments. Marine diseases become emergencies when significant ecological, economic or social impacts occur. We can prepare for and manage these emergencies through improved surveillance, and the development and iterative refinement of approaches to mitigate disease and its impacts. Improving surveillance requires fast, accurate diagnoses, forecasting disease risk and real-time monitoring of disease-promoting environmental conditions. Diversifying impact mitigation involves increasing host resilience to disease, reducing pathogen abundance and managing environmental factors that facilitate disease. Disease surveillance and mitigation can be adaptive if informed by research advances and catalysed by communication among observers, researchers and decision-makers using information-sharing platforms. Recent increases in the awareness of the threats posed by marine diseases may lead to policy frameworks that facilitate the responses and management that marine disease emergencies require

Larval exposure to predator cues alters immune function and response to a fungal pathogen in post-metamorphic wood frogs

For the past several decades, amphibian populations have been decreasing around the globe at an unprecedented rate. Batrachochytrium dendrobatidis (Bd), the fungal pathogen that causes chytridiomycosis in amphibians, is contributing to amphibian declines. Natural and anthropogenic environmental factors are hypothesized to contribute to these declines by reducing the immunocompetence of amphibian hosts, making them more susceptible to infection. Antimicrobial peptides (AMPs) produced in the granular glands of a frog’s skin are thought to be a key defense against Bd infection. These peptides may be a critical immune defense during metamorphosis because many acquired immune functions are suppressed during this time. To test if stressors alter AMP production and survival of frogs exposed to Bd, we exposed wood frog (Lithobates sylvaticus) tadpoles to the presence or absence of dragonfly predator cues crossed with a single exposure to three nominal concentrations of the insecticide malathion (0, 10, or 100 parts per billion [ppb]). We then exposed a subset of post-metamorphic frogs to the presence or absence of Bd zoospores and measured frog survival. Although predator cues and malathion had no effect on survival or size at metamorphosis, predator cues increased the time to metamorphosis by 1.5 days and caused a trend of a 20% decrease in hydrophobic skin peptides. Despite this decrease in peptides determined shortly after metamorphosis, previous exposure to predator cues increased survival in both Bd-exposed and unexposed frogs several weeks after metamorphosis. These results suggest that exposing tadpoles to predator cues confers fitness benefits later in life.Keywords: immunosuppression, AchE inhibitor, chytridiomycosis, disease ecology, brevinin, emerging infectious disease, Batrachochytrium dendrobatidis, temporin, Lithobates sylvaticus, indirect effect