Infectious Diseases of the Felidae: Parasite Communities from Miniature to Massive

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Infectious Diseases of the Felidae: Parasite Communities from Miniature to Massive AN ABSTRACT OF THE DISSERTATION OF Heather Broughton for the degree of Doctor of Philosophy in Integrative Biology presented on July 3, 2017. Title: INFECTIOUS DISEASES OF THE FELIDAE: PARASITE COMMUNITIES FROM MINIATURE TO MASSIVE Abstract approved: ______________________________________________________ Anna Jolles Direct anthropogenic stressors have caused drastic declines in wildlife populations over the past two centuries. In the face of these threats, spillover of infectious disease from domestic animals and livestock into wildlife, and novel interactions between parasites and pathogens within wildlife communities, have further suppressed already vulnerable populations. As management officials and conservationists fight to counteract these influences, a sound understanding of how pathogens and parasites interact to shape host health, and the level of disease threat posed from outside species, has become paramount to ensuring long term population viability. Here I use two model systems to examine these interactions. The first study system (Chapters 1, 2, and 3) examines the potential implications of an immunosuppressive lentivirus, feline immunodeficiency virus (FIV), for structuring host health, immunity, and coinfection dynamics in a population of 219 free-ranging African lions (Panthera leo) living in Kruger National Park, South Africa. Similar to HIV in humans, FIV has been linked to an AIDS-like syndrome in domestic cats characterized by decreased functional immunity; alterations to biochemical, histological, and serological markers; and increased susceptibility to other parasites and pathogens. While recent evidence suggests similar mechanisms may be at play in FIV-infected lion hosts, less is known about the health implications of FIV for this species or what role coinfections may play in structuring disease outcome. In Chapter 1 I set the stage for this investigation by expanding the available toolbox for lion health research and creating a set of normal reference intervals against which health metrics for free-ranging lions can be compared. Using metrics and tools established in Chapter 1, I then use Chapters 2 and 3 to show that FIV exhibits wide scale immunosuppressive and negative health effects within lion hosts, but that parasite and pathogen communities facilitated by the virus may be of equal or greater importance for determining both health outcome and susceptibility to other coinfections when compared to FIV alone. In the second study system, I examine disease prevalence and incidence in a common, highly adaptable species, the feral cat (Felis catus), to determine its potential as a disease reservoir for sympatrically dwelling human and animal populations. Using a healthy population of 129 feral cats presented at a local trap-neuter-release program in Portland, Oregon, I show that prevalence and incidence of viral and bacterial pathogens, as well as endo- and ectoparasites, is high among this untreated population. Together, findings of these respective studies show potential points for disease intervention on both the parasite and host level. ©Copyright by Heather Broughton July 3, 2017 All Rights Reserved INFECTIOUS DISEASES OF THE FELIDAE: PARASITE COMMUNITIES FROM MINIATURE TO MASSIVE by Heather Broughton A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented July 3, 2017 Commencement June 2018 Doctor of Philosophy dissertation of Heather Broughton presented on July 3, 2017 APPROVED: Major Professor representing Integrative Biology 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. Heather Broughton, Author ACKNOWLEDGEMENTS First, to my major advisor Dr. Anna Jolles, who didn’t think I was crazy for pursuing PhD work while concurrently enrolled in a veterinary program, this project would not have been possible without your endless council, expertise, and supportive friendship. To my co-advisor, Dr. Danny Govender, and our laboratory/field technician, Purvance Shikwambana, your expertise in the field and laboratory, and working knowledge of wildlife and disease systems, has taught me far more than I could ever have learned in a classroom. Together, the continued friendship, council, and hard work of the girl’s lion team made fieldwork not only possible, but something I looked forward to every summer (winter). In addition, data collection for the lion FIV study would not have been possible without supportive infrastructure and funding from the larger lion project headed by Drs. Sam Ferreira and Paul Funston. Without the expertise, equipment, accommodations, and thousands of dedicated man hours provided by that study through the collaboration of scientists, technicians, and veterinarians from both SANPARKs’ Veterinary Wildlife Services and Scientific Services, lion captures would never have taken place. In both the field and the laboratory, data collection and fun were also facilitated by a large dedicated team of undergraduate, veterinary, and graduate students including Tanya Kerr, Emily Magnuson, Zaya McSky, Kadie Anderson, Elena Alonso, and Ignatius Viljoen. Continual monitoring of the tagged lion population was made possible through the efforts of Darius Scholtz, Nkabeng Maruping, Trevor Valoyi, Travis Smit, and Katlego Makutulela. Funding for the FIV portion of the lion study was provided by Oregon State University, SANPARKs Scientific Services, Ajubatus, and Morris Animal Foundation (Grant # D13ZO-420). On the miniature side of the feline spectrum, special thanks is afforded to the Feral Cat Coalition of Oregon (FCCO), who allowed us to collect feral cat samples alongside their spay- and-neuter efforts; to our funders at the OSU College of Veterinary Medicine (OSU CVM) and the LL-Stewart Foundation; and to the OSU CVM class of 2013 for their efforts in sample processing. Finally, to my lab, feline, canine, and friend family, and to my parents, I would never have been able to achieve these goals without your love and support. Also, special acknowledgement goes out to the felines of all shapes and sizes that made this work possible. CONTRIBUTION OF AUTHORS Chapters 1-4: Dr. Anna Jolles was the principal investigator, and my primary PhD advisor, for all chapters presented in this dissertation. In addition to helping secure grants and funding through Oregon State University, Morris Animal Foundation, and the LL-Stewart Foundation, she also provided countless hours of help and feedback in the lab, the classroom, and the field. Chapters 1-3: For all chapters with Dr. Danny Govender and Purvance Shikwambana as co- authors, Danny served as both a co-principle investigator and a co-advisor for my PhD and research efforts, from project planning and data collection until publication. Purvance Shikwambana was our right-hand woman, serving a primary role in the planning, development, and implementation of all of our laboratory and field methods. Chapter 1: Dr. Patrick Chappell was directly involved in the development of RIA methods used to measure endocrine markers for leptin and ghrelin against which clinical normals could be established and malnutrition evaluated for FIV-positive and negative populations. Chapter 2: Dr. Emmanuel Serrano served as our resident statistical genius for this chapter through his adaptation of a partial least squares structural equation model to our data in order to evaluate causal relationships between FIV, coinfections, immunity, and impaired clinical health. Chapter 3: Dr. Erin Gorsich is a postdoc in our lab and was the brain behind the monopartite network and cluster analysis used in this chapter to evaluate parasite community assemblages and host-parasite connectivity between FIV-positive and FIV-negative lion networks. Chapter 4: Technician Leah Kennon is the primary overseer of all Feral Cat Coalition operations in Portland, Oregon and was the sole reason we were allowed to collect cat samples alongside their spay-and-neuter efforts. Drs. Ling Jin, Kathy O’Reiley, Janelle Bishop-Stewart, and Jana Gordon helped to collect data for this study through their supervision of diagnostic laboratory assays used to detect the various pathogens identified in the study. TABLE OF CONTENTS Page INTRODUCTION .......................................................................................................................... 1 CHAPTER 1: BRIDGING GAPS BETWEEN ZOO AND WILDLIFE MEDICINE: ESTABLISHING REFERENCE INTERVALS FOR FREE-RANGING AFRICAN LIONS (PANTHERA LEO) ........................................................................................................................ 6 1.1 INTRODUCTION ........................................................................................................ 8 1.2 METHODS ................................................................................................................... 9 1.3 RESULTS ................................................................................................................... 15 1.4 DISCUSSION ............................................................................................................. 15 1.5 TABLES AND FIGURES .......................................................................................... 19 CHAPTER 2: EQUAL CONTRIBUTIONS OF FELINE IMMUNODEFICIENCY VIRUS AND
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