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Microbial Dynamics in Amphibian Conservation and Disease Ecology

Abstract

The emerging fungal disease, chytridiomycosis, caused by the chytrid pathogen Batrachochytrium dendrobatidis (Bd), has contributed to declines or extinctions of hundreds of amphibian species globally. Recent evidence has elucidated the importance of skin microbiomes to Bd resistance, revealing the potential of microbial communities to assist in the conservation of endangered species. However, an understanding of the historical and present distribution of Bd is needed to identify where amphibians are at risk. Moreover, amphibian microbiomes require further investigation to determine the extent of their protective power and how it may be harnessed. My dissertation addresses gaps in our knowledge in both of these areas. Chapter One provides evidence for the recent emergence of Bd in African amphibians, identifying multiple Bd lineages infecting hosts and predicting Bd risk across the continent. Next, I present several studies on the skin microbiome of an endangered amphibian, the Sierra Nevada yellow-legged frog (Rana sierrae), including investigations of the impacts of restoration efforts for this species. In Chapter Two, I show that skin regions primarily infected by Bd, including ventral surfaces and hindfeet, harbor higher relative abundances of putatively Bd-inhibitory bacteria compared to the back of frogs, where Bd is often absent. In Chapter Three, I evaluate a common microbiome sampling protocol for amphibian skin and demonstrate that rinsing prior to swab collection does not significantly alter microbiomes detected. Chapter Four examines experimental Bd inoculation and antifungal treatment, describing short-term impacts on R. sierrae microbiomes and providing evidence for legacy effects of Bd to captive frog microbiomes post-treatment. In Chapter Five, I compare microbiomes and Bd infections of naturally persisting populations and restored populations consisting of frogs directly translocated from natural populations, frogs reintroduced from captivity, and descendants of relocated frogs. I provide evidence of higher Bd loads and lower predicted Bd-inhibitory microbiome function in restored populations, which I hypothesize may be related to site parameters and host genotypes present at restored sites. I did not find evidence for associations of microbiomes or infections with history of specific restoration strategy within restored populations (i.e., reintroduction versus translocation, and Bd inoculation treatment group post-reintroduction). Together, these microbiome studies suggest that the present environment outweighs individual identity or history in determining microbiome structure and diversity, though impacts of host genetics require investigation. This work also suggests that bacteria in the family Burkholderiaceae are important to R. sierrae, because of their dominance on the skin, their responsiveness to Bd infection, and their putative Bd-inhibitory function contributing to population-level differences in Bd loads.