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THE PYGMY HIPPOPOTAMUS (Choeropsis Liberiensis)

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THE PYGMY HIPPOPOTAMUS (Choeropsis Liberiensis) THE PYGMY HIPPOPOTAMUS (Choeropsis liberiensis) An Enigmatic Oxymoron How a not-so-small species presents a sizeable conservation challenge Gabriella L Flacke DVM, MVSc This thesis is submitted to fulfill the requirements for the degree of Doctor of Philosophy School of Animal Biology 2017 © jem barratt It is not the critic who counts; not the man who points out how the strong man stumbles, or where the doer of deeds could have done better. The credit belongs to the man who is actually in the arena, whose face is marred by dust and sweat and blood; who strives valiantly; who errs, who comes short again and again, because there is no effort without error and shortcoming; but who does actually strive to do the deeds; who knows great enthusiasms, the great devotions; who spends himself in a worthy cause; who at the best knows in the end the triumph of high achievement, and who at the worst, if he fails, at least he fails while daring greatly. –Theodore Roosevelt DEDICATION Dedicated to the memory of loved ones who accompanied me on this journey in spirit – Phyllis and Ben Johnson; Stephen Johnson; Hildegard and Gerhard Flacke Caminante, no hay camino, se hace camino al andar. Traveler, there is no path; the path must be forged as you walk. –Antonio Machado iii SUMMARY The pygmy hippopotamus (Choeropsis liberiensis) is endangered in the wild and has been exhibited in zoological collections since the early 1900s; however, it remains one of the most little known and poorly understood large mammal species in the world. Studies of its biology, physiology and ecology have been limited, both by the often inhospitable nature of its native West African rainforest habitat and by the common misconception that the husbandry and management of the ex situ population is already optimized. Most of what we know about this species stems from two radio-telemetry studies conducted in Côte d’Ivoire in the 1980s, a handful of camera-trap and footprint tracking surveys, and observations in zoological facilities; very little analytical, prospective research has been conducted. The first Conservation Strategy for the Pygmy Hippopotamus (Mallon et al. 2011) identified several key areas for further research on the ex situ population, including reproductive physiology, polycystic kidney disease (PKD), the female-biased sex ratio, and the potential influence of captivity-associated stress on health and welfare. The overall aim of my PhD research was to address some of these objectives and thereby also provide baseline data essential for further studies. Specifically, I investigated mortality (causes and trends), the demographics of PKD and potential impacts on long-term population viability, reproductive biology of both sexes, and the application of a non-invasive technique for monitoring stress. The first chapter provides background context and outlines the overall scope of the thesis. Chapter 2 reviews historical and recent literature, creating a framework for the thesis. Several specific issues are discussed in detail, including PKD, the female-biased sex ratio, obesity, the high neonatal mortality rate, and failure of many breeding pairs to reproduce. Chapter 3 identifies primary causes of disease and mortality for newborn, juvenile, and adult pygmy hippos and presents recommendations for veterinary care, husbandry and management. The information in this chapter constitutes the first comprehensive review of mortality data (greater than 400 cases) from the managed population since 1982 and significantly expands on previous v analyses. Chapter 4 describes the demographics of PKD, investigates potential inheritance patterns for this condition based on pedigree, and examines effects of PKD on longevity. This chapter also includes an age-based survival analysis to assess long-term viability based on historical data and current population demographics. The data in the third and fourth chapters were generated in collaboration with the International Studbook keeper at Zoo Basel. Chapter 5 is the first investigation of female reproductive parameters for this species and represents a collaborative research effort between the Southeast Zoo Alliance for Reproduction and Conservation (SEZARC), Yulee, Florida; the Department of Biomedical Sciences, Unit of Physiology, Pathophysiology and Experimental Endocrinology, University of Veterinary Medicine (Vetmeduni), Vienna, Austria; the Chester Zoo, UK; and the Institute for Breeding and Reproduction of Endangered African Mammals (IBREAM). Together, we characterize the reproductive biology of the female pygmy hippo during gestation, lactation, and the estrus cycle using enzyme immunoassays (EIAs) to measure fecal hormone metabolites. Chapter 6 was also a collaborative venture between SEZARC, Vetmeduni and IBREAM, and examines androgen metabolite patterns throughout the year for male pygmy hippos. We explore one of the potential pitfalls of EIA analysis and describe a substantial cross-reaction between two assays developed to measure the native hormones corticosterone and testosterone. We also describe an EIA that presents biologically relevant patterns in fecal metabolites of cortisol and thus can be used for quantifying individual stress response in pygmy hippos. The final chapter offers a brief review of overall conclusions and provides recommendations based on research outcomes. Collectively, the information presented in this thesis significantly expands our knowledge base about the pygmy hippo and provides a valuable framework for future studies to further optimize health, reproduction and welfare in the managed population. vi TABLE OF CONTENTS Dedication ............................................................................................................................. iii Summary .................................................................................................................................v Table of Contents .................................................................................................................. vii Acknowledgements .............................................................................................................. xiii Author’s Declaration .............................................................................................................xix Statement of Contributions ..................................................................................................... xx List of Publications .............................................................................................................. xx Author Contributions ..........................................................................................................xxi List of Abbreviations............................................................................................................xxii List of Figures ...................................................................................................................... xxv List of Tables ..................................................................................................................... xxvii Chapter 1 General Introduction ..........................................................................................1 1.1 A Brief Overview of the Pygmy Hippopotamus .................................................1 1.2 Context and Scope .............................................................................................2 1.3 Objectives and Structure ....................................................................................5 Chapter 2 The Pygmy Hippopotamus Choeropsis liberiensis (Morton, 1849): Bringing to Light Research Priorities for the Largely Forgotten, Smaller Hippo Species ....................................................................................................7 2.1 Abstract ........................................................................................................... 10 2.2 Introduction ..................................................................................................... 11 2.3 Ex Situ History ................................................................................................ 12 2.4 Phylogeny and Taxonomy ................................................................................ 13 2.5 Anatomy and Physiology ................................................................................. 14 2.6 Husbandry ....................................................................................................... 18 2.7 Reproduction ................................................................................................... 21 2.8 Female-biased Sex Ratio .................................................................................. 25 2.9 General Health and Medicine ........................................................................... 28 2.10 Polycystic Kidney Disease (PKD) .................................................................... 33 2.11 Obesity ............................................................................................................ 34 2.12 Population Genetics ......................................................................................... 37 2.13 Anesthesia ....................................................................................................... 38 2.14 Conclusions ..................................................................................................... 45 2.15 Acknowledgements .........................................................................................
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