Emerging wildlife diseases represent a serious threat to conservation efforts. Impacts of emerging multi-host pathogens can vary greatly among species as well as geographically, and understanding which populations will be at greatest risk is essential for conserving biodiversity. Snake fungal disease (SFD), caused by the fungal pathogen Ophidiomyces ophidiicola, is responsible for lethal infections in snakes and has contributed to the decline of multiple North American snake populations. However, which species are most affected by this disease and how infections vary regionally remains unknown. Here we sampled 44 different species across 14 sites throughout the Southeastern and Mid-Atlantic United States. We found a strong effect of latitude on both pathogen prevalence and severity, with more severe infections at more northern latitudes. We also found high variability in pathogen prevalence and infection severity among species. There was a strong positive relationship between pathogen prevalence and disease severity, suggesting that SFD is not just highly prevalent in some populations but also highly virulent. More broadly, our results support that SFD likely has continued impacts on snake populations with some species experiencing greater disease than others attributed to spatial and host variation. / Master of Science / Conserving biodiversity is a significant challenge. Wildlife species are under multiple threats including habitat loss, changing climate, species introductions, pollution, and infectious diseases. Emerging wildlife diseases can pose a major problem for wildlife as they often go undetected until they cause substantial declines for the affected species, sometimes leading to population extirpations and extinction events. Snake fungal disease (SFD) is an emerging disease caused by the fungal pathogen Ophidiomyces ophidiicola, which has contributed to the decline of some North American snake populations. However, little is known about differences in infection, transmission, and host responses to SFD in a broader community context. To investigate the dynamics of this pathogen, we collected swab samples from 44 species from a total of 14 sites in New Jersey, Virginia, North Carolina, South Carolina, Georgia, Florida, and Louisiana. We sampled individual snakes to examine variation over a geographic gradient and among species. We found high variability among sites with more severe disease at northern sites. There was also high variability among species and some populations experienced both high pathogen prevalence and disease severity. Our results show that SFD is highly variable within snake communities and may still be causing population level effects.

Pathogenic fungi are increasingly associated with epidemics in wildlife populations and represent a significant threat to global biodiversity. Snake fungal disease is an emerging disease caused by the fungus, Ophidiomyces ophiodiicola, and appears to be widespread in the eastern United States. Yet an evaluation of field diagnostics, and an understanding of the population-level consequences of the disease, are lacking. First, I evaluated the use of clinical signs to predict the presence of O. ophiodiicola across season and snake habitat affiliation (aquatic or terrestrial) and I compared two sampling methods to see if collection method impacts PCR result. Overall, snakes with clinical signs had a higher probability of testing positive regardless of season or habitat association. However, terrestrial snakes had a lower overall probability of testing positive for O. ophiodiicola compared to aquatic snakes. I found no significant difference between sampling methods. Second, I used Passive Integrated Transponder (PIT) telemetry, and multistate capture-mark-recapture modelling to determine if SFD affects the short-term survival, movement, and behavior of wild snakes. I found no difference in short-term survival for snakes with SFD. Snakes with SFD spend more time surface-active and have lower permanent emigration and temporary immigration rates than snakes without SFD.

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Emerging infectious diseases represent a threat to biodiversity, posing significant challenges to wildlife conservation globally. Infectious diseases can cause population declines, local extirpations and, in rare cases, complete species extinction. Among emerging pathogens, pathogenic fungi have been responsible for drastic declines in several high-profile vertebrate taxa, such as Batrachochytrium dendrobatidis causing chytridiomycosis in many species of amphibians worldwide. Recently, an emerging infectious disease, 'snake fungal disease' (SFD), caused by the fungal pathogen Ophidiomyces ophidiicola, is affecting the health of snake populations in North America by causing skin infections which can be fatal. Given the potential impact of this disease on snake biodiversity worldwide, compounded by the pressure of anthropogenic stressors that already jeopardize the viability of many snake populations, there is a clear need for ecological research in this understudied system. This dissertation is comprised of 4 data chapters focusing on the disease dynamics of snake fungal disease in Europe, and the factors resulting in differential infection. In chapter 2, I develop a large field-based data collection in 10 countries in Europe to investigate the presence of disease hotspots and the variation of disease prevalence across host species, and to examine the pathogen genotypes that are present on the landscape. I found isolated areas of disease hotspots, and models including an interactive effect of host species and which pathogen clade are present on the landscape were best at explaining disease prevalence. In chapter 3, I perform a virulence challenge assay using 120 corn snakes (Pantherophis guttatus) and 7 strains of O. ophidiicola (3 collected from Europe, 4 from the USA). This experiment reveals that pathogen genotypes associated with higher disease prevalence in Europe also have higher pathogen virulence, and that different strains from the USA show variation in virulence. These results also match both physiological host responses measured in the lab and landscape patterns of disease. In chapter 4, I explore two mitigation-driven snake translocation projects in Europe that were complicated due to O. ophidiicola outbreaks. One snake species, N. tessellata, appears highly susceptible to SFD, indicating that under stressful conditions, O. ophidiicola can cause mortality regardless of pathogen genotype, and that this snake species may be important in pathogen maintenance. Finally in chapter 5, I report the presence of a different fungal pathogen in Spain, Parannannizziopsis sp., never reported in wild snakes in Europe before. Broadly, my dissertation demonstrates coevolutionary relationships between hosts and pathogens and has important implications to snake conservation over large scales. / Doctor of Philosophy / Biodiversity conservation is under significant threat globally due to the ever-growing human population. Threats such as habitat loss, climate change, pollution and infectious diseases are all important factors that are affecting wildlife populations. Snakes, and specifically infectious diseases of snakes, have been understudied compared to that of other types of wildlife in Europe. My dissertation focuses on understanding the disease ecology and conservation implications of snake fungal disease, an infectious disease that can be life-threatening to snakes. I first developed a study of this disease in multiple countries over three years to understand how common the disease is across the landscape, which species of snakes are most infected, and how severe skin infections are. I found specific areas in Europe where disease prevalence is high and attributed these higher disease areas to specific snake species and fungal strains that interact together to cause higher infection rates (chapter 2). Secondly, I designed a controlled experimental study in the laboratory to test the capacity of different pathogenic strains, collected in Europe and the USA, to harm its host. I chose a single host species, the corn snake (Pantherophis guttatus) to test this question. I found that different pathogen strains vary in their ability to cause severe disease, and these results were confirmed with field observations. I also found that one strain collected from coastal Virginia is able to cause more severe disease when compared to all other strains (chapter 3). Finally, I found that under captive stress, strains that might not be able to cause severe disease in the wild can lead to snake mortality, specifically in one snake species that might be more susceptible than others (chapter 4). Broadly, this dissertation describes complex interactions between snakes and fungal pathogens and has relevance to reptile conservation.

<p>  </p> <p>Emerging pathogenic fungi have become a topic of conservation concern due to declines seen in several host taxa. One newly emerging fungal pathogen, <em>Ophidiomyces ophiodiicola</em>, has been well documented as the causative agent of Snake Fungal Disease (SFD). SFD has been found in a variety of snake species across the United States, including the Eastern Massasauga (<em>Sistrurus catenatus</em>), a federally threatened rattlesnake species. Most work to date has involved detecting SFD for diagnosis of infection through direct sampling from snakes. Attempts to detect <em>O. ophiodiicola</em> in the environment to better understand its distribution, seasonality, and habitat associations are lacking. I collected topsoil and ground water samples from four macrohabitat types in northern Michigan at a site where SFD infection has been seen in Eastern Massasauga. I used a quantitative PCR (qPCR) assay targeting the internal transcribed spacer region (ITS) developed for diagnosis of SFD after extracting DNA from samples. <em>Ophidiomyces</em> DNA was successfully detected in topsoil, with minimal to no detection in groundwater samples. The frequency in which <em>Ophidiomyces</em> was detected in a sample did not differ between habitats, but samples grouped seasonally showed higher detection occurring during mid-summer. Investigation of the correlation of environmental parameters on <em>Ophidiomyces</em> occurrence recovered no relationships. Our data suggests that season has some effect on the presence of <em>Ophidiomyces</em>. Differences between habitats may exist but are likely more dependent on the time of sampling and currently uninvestigated soil parameters. These findings build on our understanding of <em>Ophidiomyces</em> ecology and epidemiology and inform where snakes like the Eastern Massasauga may be encountering the fungal pathogen. Furthermore, they assist with developing conservation practices aimed at reducing <em>O. ophiodiicola </em>exposure in imperiled snake species. </p>

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