An Abstract of the Dissertation Of
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AN ABSTRACT OF THE DISSERTATION OF Rhea Hanselmann for the degree of Doctor of Philosophy in Zoology presented on August 16, 2016 Title: Wildlife Health in Managed Forests: Immunity and Infectious Diseases in Wild Rodents of Oregon. Abstract approved: _____________________________________ Anna E. Jolles With continual and worldwide human population growth, our impact on the natural environment expands and intensifies every day. We consume natural resources, burn fossil fuels, and release toxic compounds into the air, water, and earth. We build roads that fragment the landscape, construct new settlements, and develop agricultural lands in previously undisturbed areas. And, we introduce non-native species, which compete with and/or prey on native ones. Our actions change the composition of ecosystems by effacing natural environments and decimating plant and animal populations. We have reached a time of unprecedented anthropogenic environmental change. And, while we recognize, and work feverishly to mitigate, countless consequences of our actions, we still lack a profound understanding of just as many of the corollaries of the environmental changes we provoke. One thing we do know is that human-induced changes in environmental conditions can affect health – from individual organisms, to plant and animal populations, all the way to the level of the ecosystem. Yet, the mechanisms underlying such adverse health outcomes are only partially understood. For instance, we know that alterations in the structure of plant and animal communities, the distribution and demographics of populations, and the abundance of individuals can influence the emergence or re-emergence of infectious diseases. Which species are present in a community, where, when, and in what numbers can all determine the dynamics of pathogens, lead to disease outbreaks, and provide opportunities for spillover into new species. However, given the many environmental-, population-, and organism-level factors involved, and the complexity by which these variables interact, detecting and predicting the ultimate consequences for the health of animal, including human, populations remains diffic ult. Wild animals play important roles in numerous infectious disease cycles, many of which are shared with humans. Considering this and the well-documented effects that human activity can have on wildlife populations, studying the impacts of anthropogenic environmental change on health in wildlife is highly relevant. To understand how human-induced environmental changes affect wildlife health and to make predictions about potential regional or even global consequences for the dynamics of infectious diseases, however, we first need to understand patterns at a local scale. Here, I describe variation in immune function in captive and wild rodent species native to managed forests in northwestern Oregon, and examine how intensive forest management practices affect these and other physiological processes, and the prevalence of infectious diseases, in a large-scale field experiment. In Chapter 2 of this dissertation, I present baseline data on simple immune parameters in an iconic inhabitant of old-growth forests in the Pacific Northwest, the red tree vole (Arborimus longicaudus). I show that both body condition and age are important for immune defenses in this species. Translating these findings to wild populations leads me to predict that degradation of habitat may affect red tree voles not only at the population scale, as is currently the case, but that less obvious consequences for the health of individuals surviving in disturbed or suboptimal habitat are also possible. It is important, therefore, that efforts to conserve this species consider adverse effects of present forest management practices on red tree vole health, as potentially increased disease susceptibility could have detrimental outcomes for this species. In Chapters 3 and 4, I took advantage of a rare and large-scale experiment to test my predictions regarding the negative consequences of habitat degradation for individual animals in more ubiquitous rodent species known for their resilience to environmental disturbance. I investigated the effects of intensive forest management on stress, health, and immunity (Chapter 3), and on the prevalence of infectious diseases transmissible to humans (Chapter 4) in deer mice (Peromyscus maniculatus), Townsend chipmunks (Tamias townsendii), and creeping voles (Microtus oregoni) inhabiting managed forest plots in northwestern Oregon. The experimental design employed allowed me to test the effect of regionally representative forest management practices on health and disease outcomes with important implications for public health. In Chapter 3, I present results which suggest that intensive forest management can have complex, but highly context-dependent effects on the health of wild deer mice. Intensive forest management can shape animals’ condition and reproductive activity, increase levels of stress hormone, and stimulate some but depress other immune responses. However, deer mice are only able to respond to the extreme stressor of this disturbance when underlying environmental conditions are favorable. When inhabiting inherently harsh habitat, mice appear unable to cope with additional disturbance imposed by intensive forest management, and only the fittest mice survive. Finally, in Chapter 4, I identify moderate prevalence of two important and potentially fatal human infections in rodents inhabiting managed forests in northwestern Oregon. In deer mouse populations, Sin Nombre virus was clustered spatially, and prevalence varied between years. But, in the focus of highest infection, the proportion of infected mice, albeit low, appeared to increase with intensity of forest management. For Leptospirosis, I found a similar pattern in creeping voles, but did not observe an association between infection prevalence and forest management in deer mice or chipmunks. I conclude that forest management may drive infectious disease patterns, but that the direction and magnitude of such effects depends on the host-pathogen system. Taken together, my findings indicate that wild animal health can suffer from declines in habitat quality associated with forest management. For a near-threatened species such as the red tree vole, decreases in the availability of food and nesting habitat have the potential to change susceptibility to infection, which could facilitate disease invasion and further threaten populations. For wild animals that serve as reservoirs for human infections, especially abundant and apparently resilient species, impaired health can drive the dynamics of pathogens and increase the risk of transmission to humans and other animals. Although many more questions remain, my work contributes to our understanding of the effects of anthropogenic environmental change for wildlife and human health. ©Copyright by Rhea Hanselmann August 16, 2016 All Rights Reserved Wildlife Health in Managed Forests: Immunity and Infectious Diseases in Wild Rodents of Oregon by Rhea Hanselmann A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented August 16, 2016 Commencement June 2017 Doctor of Philosophy dissertation of Rhea Hanselmann presented on August 16, 2016. APPROVED: _____________________________________________________________________ Major Professor, representing Zoology _____________________________________________________________________ Chair of the Department of Integrative Biology _____________________________________________________________________ Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. _____________________________________________________________________ Rhea Hanselmann, Author ACKNOWLEDGEMENTS First and foremost, I thank my PhD adviser Anna E. Jolles for outstanding mentorship, support, and friendship over the years. Thank you for teaching me how to think like an ecologist, and for encouraging me to always pursue my scientific interests, however well they aligned with your own. Thanks to you, I am a stronger scientist, writer, mentor, and teacher than I could have ever imagined. Thank you for sharing your wisdom and letting your infinite optimism rub off on me. The Himalayas may never appear flat from where I stand, but at least, thanks to you, I can see them sparkle! I am also deeply indebted to my dissertation committee, including current members Julia Burco, Malcolm Lowry, Rebecca Terry, and my Graduate Council Representative Jerry Heidel, as well as former members Sally Hacker and Dan Edge. I appreciate you sharing your expertise and helpful insights with me and I thank you all for being supportive and extraordinarily flexible throughout my career as a graduate student at Oregon State University (OSU). You were a positive force that provided stimulating conversations and ideas, and helped keep me moving forwards. Truly excellent collaborations have developed from my dissertation work. I am especially thankful to Laurie Dizney at the University of Portland, Erin Gorsich at the OSU Department of Biomedical Sciences, Chad Marks-Fife and Megan Cummings in the OSU Department of Fisheries and Wildlife, and Eric Forsman at the US Forest Service Pacific Northwest Research Station for all their help in data collection, analysis,