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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] The effects of multiple pathogens on amphibians in the Pacific Northwest

  The earth is undergoing a “biodiversity crisis” characterized by loss of populations, species, genetic diversity, and ecosystem services. Part of this crisis consists of population declines, extinctions, ...

  Citation × Citation Citation Abstract Copy Title: The effects of multiple pathogens on amphibians in the Pacific Northwest Author: Romansic, John M. The earth is undergoing a “biodiversity crisis” characterized by loss of populations, species, genetic diversity, and ecosystem services. Part of this crisis consists of population declines, extinctions, and increased incidence of deformities in amphibians. It is unknown whether deformities contribute to these declines. Many cases of population declines in amphibians are associated with infectious disease. Water molds (Oomycota: Oomycetes: Saprolegniales) (e.g. Achlya and Saprolegnia) may contribute to amphibian population declines whereas parasitic flatworms (Ribeiroia) appear to be major causes of amphibian deformities. I found that Saprolegnia can kill larval and newly-metamorphosed juvenile amphibians. In addition, I investigated synergistic effects of Saprolegnia and the environmental contaminant nitrate on survival of amphibian larvae. No synergisms were found. However, there was a less-than-additive interaction affecting one frog species. Saprolegnia killed Rana aurora (red-legged frog) larvae, but only when nitrate was not added, consistent with nitrate preventing Saprolegnia from killing R. aurora. I also tested for possible interactions among the pathogenic water mold A. flagellata, the pathogenic fungus Batrachochytrium dendrobatidis (BD), and the parasitic trematode Ribeiroia. No between-pathogen interactions were found, however, there were main effects of Ribeiroia and BD. Ribeiroia caused mortality and increased frequency of limb deformities. There were differences in the composition of deformity types between my study and previous work, suggesting that the relative frequencies of different deformity types produced by Ribeiroia may be context-dependent. Also, there was an overall effect of delayed development in Ribeiroia-exposed individuals. In addition, individuals that did not die or display limb deformities following Ribeiroia exposure had slower development than controls not exposed to Ribeiroia. Delayed development may contribute to the effects of Ribeiroia on amphibian populations. In contrast, BD sped up development, although there was no evidence of BD infection. These results are consistent with amphibian larvae responding to the presence of BD by increasing the rate of development. Hastened metamorphosis and dispersal from larval habitats may decrease the risk of BD infection or reduce BD infection load. Mortality of post-embryonic life stages from water molds and sublethal effects of Ribeiroia and BD on amphibian development may influence how these pathogens interact with amphibian populations. Title: The effects of multiple pathogens on amphibians in the Pacific Northwest Author: Romansic, John M. The earth is undergoing a “biodiversity crisis” characterized by loss of populations, species, genetic diversity, and ecosystem services. Part of this crisis consists of population declines, extinctions, and increased incidence of deformities in amphibians. It is unknown whether deformities contribute to these declines. Many cases of population declines in amphibians are associated with infectious disease. Water molds (Oomycota: Oomycetes: Saprolegniales) (e.g. Achlya and Saprolegnia) may contribute to amphibian population declines whereas parasitic flatworms (Ribeiroia) appear to be major causes of amphibian deformities. I found that Saprolegnia can kill larval and newly-metamorphosed juvenile amphibians. In addition, I investigated synergistic effects of Saprolegnia and the environmental contaminant nitrate on survival of amphibian larvae. No synergisms were found. However, there was a less-than-additive interaction affecting one frog species. Saprolegnia killed Rana aurora (red-legged frog) larvae, but only when nitrate was not added, consistent with nitrate preventing Saprolegnia from killing R. aurora. I also tested for possible interactions among the pathogenic water mold A. flagellata, the pathogenic fungus Batrachochytrium dendrobatidis (BD), and the parasitic trematode Ribeiroia. No between-pathogen interactions were found, however, there were main effects of Ribeiroia and BD. Ribeiroia caused mortality and increased frequency of limb deformities. There were differences in the composition of deformity types between my study and previous work, suggesting that the relative frequencies of different deformity types produced by Ribeiroia may be context-dependent. Also, there was an overall effect of delayed development in Ribeiroia-exposed individuals. In addition, individuals that did not die or display limb deformities following Ribeiroia exposure had slower development than controls not exposed to Ribeiroia. Delayed development may contribute to the effects of Ribeiroia on amphibian populations. In contrast, BD sped up development, although there was no evidence of BD infection. These results are consistent with amphibian larvae responding to the presence of BD by increasing the rate of development. Hastened metamorphosis and dispersal from larval habitats may decrease the risk of BD infection or reduce BD infection load. Mortality of post-embryonic life stages from water molds and sublethal effects of Ribeiroia and BD on amphibian development may influence how these pathogens interact with amphibian populations. Close