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• 1. [Article] The effects of an emerging pathogen on amphibian host behaviors and interactions

  Contemporary environmental change encompasses massive biodiversity loss and increasing numbers of emerging diseases worldwide. As part of a global biodiversity crisis, amphibians are disappearing at unprecedented ...

  Citation × Citation Citation Abstract Copy Title: The effects of an emerging pathogen on amphibian host behaviors and interactions Author: Han, Barbara A. Contemporary environmental change encompasses massive biodiversity loss and increasing numbers of emerging diseases worldwide. As part of a global biodiversity crisis, amphibians are disappearing at unprecedented rates. Batrachochytrium dendrobatidis is an emerging infectious pathogen prominently associated with many declines. Chapter 1 reviews the past decade of research on this system and highlights areas where knowledge is notably lacking. Host behavior remains a crucial determinant of host-pathogen dynamics yet studies addressing the effects of Batrachochytrium on amphibian behaviors are virtually nonexistent. Remaining chapters examine behavioral responses of host species to Batrachochytrium. Chapter 2 examines how ancient behaviors that have persisted in amphibians for millions of years change with exposure to Batrachochytrium. I examined thermoregulatory behavior in tadpoles of four species (Pseudacris regilla, Rana aurora, Bufo boreas, Rana cascadae), and aggregation behavior in two species that school as tadpoles (B. boreas, R. cascadae). Results suggest that some amphibians will continue seeking optimal temperatures and continue aggregating regardless of infection risk. I discuss the importance of behavioral plasticity and evolutionary inertia in interpreting host behavioral responses to infection. Chapter 3 examines Batrachochytrium dynamics when multiple host species interact. I manipulated infection status in tadpoles of three naturally co-occurring hosts (P. regilla, B. boreas, R. cascadae) in various combinations and measured growth, survival and infection severity. There were strong interactions between species combinations and infection leading to pathogen-mediated mutualism and competition. Results also suggest that both species richness and species identity may be important factors moderating a dilution effect in this system. Coexisting, interacting hosts must also contend with predators in a community. Chapter 4 explores Batrachochytrium-induced changes in antipredator behaviors in four species (P. regilla, R. aurora, B. boreas, R. cascadae). I also examined whether antipredator behaviors increased survivorship in the presence of lethal predators in R. cascadae, R. aurora. Exposure to Batrachochytrium changed activity rate and refuge use in Bufo, but not in the other species. Nonselective predation of Batrachochytriumexposed prey by susceptible predators adds an unexplored dimension of complexity to this system. Chapter 5 summarizes the ecological implications of studies presented in this dissertation. Title: The effects of an emerging pathogen on amphibian host behaviors and interactions Author: Han, Barbara A. Contemporary environmental change encompasses massive biodiversity loss and increasing numbers of emerging diseases worldwide. As part of a global biodiversity crisis, amphibians are disappearing at unprecedented rates. Batrachochytrium dendrobatidis is an emerging infectious pathogen prominently associated with many declines. Chapter 1 reviews the past decade of research on this system and highlights areas where knowledge is notably lacking. Host behavior remains a crucial determinant of host-pathogen dynamics yet studies addressing the effects of Batrachochytrium on amphibian behaviors are virtually nonexistent. Remaining chapters examine behavioral responses of host species to Batrachochytrium. Chapter 2 examines how ancient behaviors that have persisted in amphibians for millions of years change with exposure to Batrachochytrium. I examined thermoregulatory behavior in tadpoles of four species (Pseudacris regilla, Rana aurora, Bufo boreas, Rana cascadae), and aggregation behavior in two species that school as tadpoles (B. boreas, R. cascadae). Results suggest that some amphibians will continue seeking optimal temperatures and continue aggregating regardless of infection risk. I discuss the importance of behavioral plasticity and evolutionary inertia in interpreting host behavioral responses to infection. Chapter 3 examines Batrachochytrium dynamics when multiple host species interact. I manipulated infection status in tadpoles of three naturally co-occurring hosts (P. regilla, B. boreas, R. cascadae) in various combinations and measured growth, survival and infection severity. There were strong interactions between species combinations and infection leading to pathogen-mediated mutualism and competition. Results also suggest that both species richness and species identity may be important factors moderating a dilution effect in this system. Coexisting, interacting hosts must also contend with predators in a community. Chapter 4 explores Batrachochytrium-induced changes in antipredator behaviors in four species (P. regilla, R. aurora, B. boreas, R. cascadae). I also examined whether antipredator behaviors increased survivorship in the presence of lethal predators in R. cascadae, R. aurora. Exposure to Batrachochytrium changed activity rate and refuge use in Bufo, but not in the other species. Nonselective predation of Batrachochytriumexposed prey by susceptible predators adds an unexplored dimension of complexity to this system. Chapter 5 summarizes the ecological implications of studies presented in this dissertation. Close

• 2. [Article] Ecology and applications of cutaneous mechanisms of resistance to amphibian chytridiomycosis

  Amphibian biodiversity is in rapid global decline, due in part to the fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd). Susceptibility to Bd and chytridiomycosis varies between ...

  Citation × Citation Citation Abstract Copy Title: Ecology and applications of cutaneous mechanisms of resistance to amphibian chytridiomycosis Author: Nebergall, Emily E. Amphibian biodiversity is in rapid global decline, due in part to the fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd). Susceptibility to Bd and chytridiomycosis varies between species and populations. Skin peptides and symbiotic skin bacteria appear to be important mechanisms of Bd resistance. However, not much is known about the ways in which these mechanisms vary between species and locations or about the relative importance of these mechanisms to different amphibian species. This thesis sought to explore the ecology and applications of mechanisms of resistance to Bd. In the second chapter, I use an information theoretic approach to investigate the source of intraspecies and interspecies variation in three measures of predicted resistance against chytridiomycosis: skin peptide inhibition of Bd, skin peptide quantity, and prevalence of Bd-inhibitory bacteria. I collected peptide and bacterial samples from three amphibian species in Mt. Rainier National Park, which is characterized by landscape heterogeneity and low connectivity and hence is likely to produce high variability between amphibian populations in different park regions. I found that skin peptide defenses may vary primarily by species, whereas anti-Bd skin bacteria may vary primarily by location. In the third chapter, I investigate the feasibility of using anti- Bd bacteria to bioaugment an endangered amphibian species, Rana chiricahuensis, against infection with Bd. I screened skin bacterial communities from wild R. chiricahuensis for anti- Bd bacteria and selected Pseudomonas fluorescens as an experimental bioaugmentation agent. I tested P. fluorescens alongside Janthinobacterium lividum in Bd challenges studies with wild adult R. chiricahuensis. Results of these studies do not indicate bioaugmentation with either of these two bacteria as a feasible Bd management strategy for R. chiricahuensis. Title: Ecology and applications of cutaneous mechanisms of resistance to amphibian chytridiomycosis Author: Nebergall, Emily E. Amphibian biodiversity is in rapid global decline, due in part to the fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd). Susceptibility to Bd and chytridiomycosis varies between species and populations. Skin peptides and symbiotic skin bacteria appear to be important mechanisms of Bd resistance. However, not much is known about the ways in which these mechanisms vary between species and locations or about the relative importance of these mechanisms to different amphibian species. This thesis sought to explore the ecology and applications of mechanisms of resistance to Bd. In the second chapter, I use an information theoretic approach to investigate the source of intraspecies and interspecies variation in three measures of predicted resistance against chytridiomycosis: skin peptide inhibition of Bd, skin peptide quantity, and prevalence of Bd-inhibitory bacteria. I collected peptide and bacterial samples from three amphibian species in Mt. Rainier National Park, which is characterized by landscape heterogeneity and low connectivity and hence is likely to produce high variability between amphibian populations in different park regions. I found that skin peptide defenses may vary primarily by species, whereas anti-Bd skin bacteria may vary primarily by location. In the third chapter, I investigate the feasibility of using anti- Bd bacteria to bioaugment an endangered amphibian species, Rana chiricahuensis, against infection with Bd. I screened skin bacterial communities from wild R. chiricahuensis for anti- Bd bacteria and selected Pseudomonas fluorescens as an experimental bioaugmentation agent. I tested P. fluorescens alongside Janthinobacterium lividum in Bd challenges studies with wild adult R. chiricahuensis. Results of these studies do not indicate bioaugmentation with either of these two bacteria as a feasible Bd management strategy for R. chiricahuensis. Close

• 3. [Article] Environmental influences on host-pathogen dynamics of the amphibian chytrid fungus

  The causes of the global biodiversity crisis are varied and complex. Anthropogenic threats may act in isolation, or interact additively or synergistically with each other or with natural stressors to affect ...

  Citation × Citation Citation Abstract Copy Title: Environmental influences on host-pathogen dynamics of the amphibian chytrid fungus Author: Buck, Julia C. The causes of the global biodiversity crisis are varied and complex. Anthropogenic threats may act in isolation, or interact additively or synergistically with each other or with natural stressors to affect sensitive taxa. The recent emergence of many infectious diseases in wildlife has brought attention to the role of disease in population declines and species extinctions. Both abiotic and biotic components of the environment may mitigate or exacerbate effects of pathogens on their hosts through direct or indirect mechanisms. The effects of the environment on host-pathogen dynamics are complex, context-dependent, and in need of further examination. One particularly sensitive group, amphibians, is at the leading edge of the sixth mass extinction. The emerging infectious disease (EID) chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatis (Bd), is implicated in population declines and extinctions of amphibians globally. My disseration addresses questions pertaining to environmental influences on disease dynamics of Bd. As described in chapter 1, various abiotic and biotic components of the environment may affect host-pathogen dynamics of Bd, resulting in changes to the dynamics of Bd transmission and spread. Chapter 2 examines the influence of an abiotic factor, the insecticide (carbaryl) and three different assemblages of larval Pacific treefrogs (Pseudacris regilla) and Cascades frogs (Rana cascadae) on host-pathogen dynamics of Bd within a community context. I found separate effects of each treatment on amphibian growth and development, but no interactive effects among the treatments. However, Bd appeared to reduce phytoplankton abundance and increase periphyton biomass, an unexpected result that merited further investigation. One possible explanation for the results described in chapter 2 is that zooplankton might consume Bd zoospores, the infective stage of the pathogen, a hypothesis that I examine in chapter 3. I conducted laboratory experiments and confirmed the presence of Bd zoospores in the gut of Daphnia sp. through quantitative PCR and visual inspection. I discuss conservation implications of this finding. To determine whether predation on Bd zoospores by zooplankton could reduce infection in amphibians, I conducted a mesocosm experiment, which is described in chapter 4. I found complex effects on species interactions: competition between larval Cascades frogs and zooplankton for phytoplankton resources reduced phytoplankton concentration, zooplankton abundance, and survival of amphibians. These effects were diminished in the presence of Bd, suggesting that zooplankton may have at least partially substituted Bd zoospores for phytoplankton in their diet, thus stimulating competitive release. However, competitive effects between zooplankton and larval amphibians overshadowed indirect positive benefits of zooplankton predation on Bd zoospores. In chapter 4, competitive effects between zooplankton and larval amphibians for phytoplankton suggested that host-pathogen dynamics might be affected by the host’s supply of resources. Chapter 5 describes a mesocosm experiment that examined how eutrophication might affect Bd-infected Pacific treefrogs and other members of the aquatic community. Nutrient additions caused increased algal growth, which benefitted herbivorous larval amphibians. Larvae exposed to Bd altered their growth, development, and diet, and allocated resources differently than unexposed individuals. However, nutrient supplementation did not alter the response of larval amphibians to Bd. As described in chapter 6, consideration of hosts and pathogens as functional members of the ecological communities in which they exist can lead to important insights in host-pathogen dynamics. My PhD research may contribute to control measures for the emerging infectious disease chytridiomycosis. Title: Environmental influences on host-pathogen dynamics of the amphibian chytrid fungus Author: Buck, Julia C. The causes of the global biodiversity crisis are varied and complex. Anthropogenic threats may act in isolation, or interact additively or synergistically with each other or with natural stressors to affect sensitive taxa. The recent emergence of many infectious diseases in wildlife has brought attention to the role of disease in population declines and species extinctions. Both abiotic and biotic components of the environment may mitigate or exacerbate effects of pathogens on their hosts through direct or indirect mechanisms. The effects of the environment on host-pathogen dynamics are complex, context-dependent, and in need of further examination. One particularly sensitive group, amphibians, is at the leading edge of the sixth mass extinction. The emerging infectious disease (EID) chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatis (Bd), is implicated in population declines and extinctions of amphibians globally. My disseration addresses questions pertaining to environmental influences on disease dynamics of Bd. As described in chapter 1, various abiotic and biotic components of the environment may affect host-pathogen dynamics of Bd, resulting in changes to the dynamics of Bd transmission and spread. Chapter 2 examines the influence of an abiotic factor, the insecticide (carbaryl) and three different assemblages of larval Pacific treefrogs (Pseudacris regilla) and Cascades frogs (Rana cascadae) on host-pathogen dynamics of Bd within a community context. I found separate effects of each treatment on amphibian growth and development, but no interactive effects among the treatments. However, Bd appeared to reduce phytoplankton abundance and increase periphyton biomass, an unexpected result that merited further investigation. One possible explanation for the results described in chapter 2 is that zooplankton might consume Bd zoospores, the infective stage of the pathogen, a hypothesis that I examine in chapter 3. I conducted laboratory experiments and confirmed the presence of Bd zoospores in the gut of Daphnia sp. through quantitative PCR and visual inspection. I discuss conservation implications of this finding. To determine whether predation on Bd zoospores by zooplankton could reduce infection in amphibians, I conducted a mesocosm experiment, which is described in chapter 4. I found complex effects on species interactions: competition between larval Cascades frogs and zooplankton for phytoplankton resources reduced phytoplankton concentration, zooplankton abundance, and survival of amphibians. These effects were diminished in the presence of Bd, suggesting that zooplankton may have at least partially substituted Bd zoospores for phytoplankton in their diet, thus stimulating competitive release. However, competitive effects between zooplankton and larval amphibians overshadowed indirect positive benefits of zooplankton predation on Bd zoospores. In chapter 4, competitive effects between zooplankton and larval amphibians for phytoplankton suggested that host-pathogen dynamics might be affected by the host’s supply of resources. Chapter 5 describes a mesocosm experiment that examined how eutrophication might affect Bd-infected Pacific treefrogs and other members of the aquatic community. Nutrient additions caused increased algal growth, which benefitted herbivorous larval amphibians. Larvae exposed to Bd altered their growth, development, and diet, and allocated resources differently than unexposed individuals. However, nutrient supplementation did not alter the response of larval amphibians to Bd. As described in chapter 6, consideration of hosts and pathogens as functional members of the ecological communities in which they exist can lead to important insights in host-pathogen dynamics. My PhD research may contribute to control measures for the emerging infectious disease chytridiomycosis. Close