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Diceros Bicornis Michaeli) INVESTIGATING POPULATION PERFORMANCE AND FACTORS THAT INFLUENCE REPRODUCTIVE SUCCESS IN THE EASTERN BLACK RHINOCEROS (DICEROS BICORNIS MICHAELI) Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Katie Louise Edwards June 2013 ii ABSTRACT Investigating population performance and factors that influence reproductive success in the eastern black rhinoceros (Diceros bicornis michaeli). Katie L. Edwards With fewer than 5000 black rhinoceros remaining, ex situ populations play a vital role in the conservation of this species. To reinforce in-situ conservation efforts, captive populations must be self-sustaining, both demographically and genetically, to maximise future viability. The aim of this thesis was to determine the sustainability of the European captive population of eastern black rhinoceros, and investigate factors that may influence population performance in this species. Population viability analysis of demographic data from in situ managed black rhinoceros populations were used to establish the variability in population growth rates across reserves. Secondly, these data were used to calculate fecundity, mortality and population structure performance indicators, as a reference for how this species can perform under natural conditions. The same analyses were then applied to the European ex situ population, to determine whether the population is demographically and genetically self-sustaining, and identify areas for potential improvement. The European captive population of eastern black rhinoceros, although currently self- sustaining, is performing sub-optimally both with respect to their in situ counterparts, and to a proposed target of 5% growth per annum. Population performance is primarily limited by sub-optimal reproduction, both in terms of individuals producing fewer calves per annum, and due to a high degree of reproductive skew across the population, leading to a large proportion of individuals failing to produce offspring. A multi-institutional study was conducted on 90% of the European population, to investigate intrinsic differences in faecal reproductive hormone metabolites between breeding and non-breeding individuals. In females, irregular oestrous cyclicity was observed, with longer than average cycles observed more frequently in females that had never bred, and periods of acyclicity more common in females that had not bred for at least seven years. Non-proven females also had higher body condition scores, and were less likely to exhibit regular signs of oestrus. In males, non-breeding males had reduced faecal testosterone compared to males that had previously sired offspring. Extrinsic factors were also investigated, to determine whether differences in reproductive success could be attributed to aspects of the social or physical environment. However, no consistent relationships were observed between breeding and non-breeding males or females. Furthermore, adrenal activity and testosterone concentration were not correlated with environmental factors, indicating that extrinsic factors alone may not explain differences in reproductive success. However, within females, differences in hormone concentration were associated with irregular oestrous cyclicity. Long cycles were associated with increased glucocorticoid metabolite concentration, and oestradiol metabolites were lower during periods of acyclicity. The duration of the preceding luteal phase varied between cycle types, indicating that the occurrence of regular and irregular oestrous cyclicity may be influenced by hormone exposure during the preceding oestrous cycle. In summary, a number of intrinsic differences in reproductive hormones in both males and females have been identified, which may be related to differential reproductive success. A better understanding of the causes of these differences would be beneficial to maximise growth rates and overall population performance of this ex situ population. iii iv ACKNOWLEDGMENTS The work in this thesis would not have been possible without the help and support of a number of people. In particular I would like to thank my supervisors Susanne Shultz, Sue Walker and Jane Hurst. This work would not have been initiated without your vision, and I am eternally grateful for your faith in me, your guidance, understanding, support and patience. Thank you to the University of Liverpool, Natural Environment Research Council (NERC) and Chester Zoo for funding, without which this study could not take place. Also to the Association of British and Irish Wild Animal Keepers (ABWAK) and the Thriplow Trust for research grants that have contributed towards this work. Thank you to Mark Pilgrim, Director General of Chester Zoo, and EEP Coordinator for the black rhinoceros. I am eternally grateful for your on-going support. To Stephanie Sanderson and the Conservation Medicine division at Chester Zoo, thank you for welcoming me as part of the team, I have no doubt my time at Chester Zoo has improved me as a researcher and as a person. All the staff at Chester zoo for making me feel so welcome, and making the zoo such a fun place to work. To all the technicians, interns and volunteers that have worked in the lab and helped with my faecal extractions – 11,000 faecal samples would just not have been possible on my own! I am also extremely grateful to all participating members of the Black rhino EEP, without whom this work could not have taken place. To the curators, veterinarians, assistants and keepers who have assisted with sample collection and provided information. This multi-institution study would not have been possible without your hard work. In particular to Tim Rowlands, Curator of Mammals, and all the keepers and interns on the rhino section past and present; Chas, Helen, Mark, Chris, Clare, Sarah, Shane, Lou and Rosie – thank you for all your hard work over the last five years, and for never complaining when I request yet more samples! Of course, I have to thank the rhinos and calves born during my time here, that have been a constant source of inspiration and motivation! Finally, to my family, I know I have been a nightmare to live with, especially over these last few months, and I will be eternally grateful for your love and support. v vi TABLE OF CONTENTS Abstract .............................................................................................................................................................. iii Acknowledgments ........................................................................................................................................... v List of Figures ................................................................................................................................................ xiii List of Tables ............................................................................................................................................... xviii List of Abbreviations .................................................................................................................................... xx 1. Introduction and literature review ....................................................................................... 25 1.1. Ex situ conservation ..................................................................................................................... 26 1.1.1. The importance of species conservation .............................................................. 26 1.1.2. Captive breeding programs ........................................................................................ 27 1.1.3. Population management ............................................................................................. 28 1.2. Endocrine control of reproduction ........................................................................................ 30 1.2.1. Female mammals: the oestrous cycle .................................................................... 30 1.2.2. Endocrine control of oestrus ..................................................................................... 33 1.2.3. Male mammals: spermatogenesis ........................................................................... 34 1.3. Factors that can lead to disruption of reproduction ...................................................... 35 1.3.1. Adrenal activity ............................................................................................................... 35 1.3.2. Disruption of reproduction due to stress ............................................................. 38 1.3.3. Nutrition and body condition .................................................................................... 41 1.3.4. Health .................................................................................................................................. 41 1.4. The black rhinoceros ................................................................................................................... 42 1.4.1. Species information and distribution .................................................................... 42 1.4.2. Current conservation status ...................................................................................... 43 1.4.3. Rhinoceros reproduction ............................................................................................ 45 1.4.4. Rhinoceros in captivity ................................................................................................ 49 1.5. Aims of this thesis
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