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Parasite Ecology and the Conservation Biology of Black Rhinoceros (Diceros Bicornis)

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Parasite Ecology and the Conservation Biology of Black Rhinoceros (Diceros Bicornis) Parasite Ecology and the Conservation Biology of Black Rhinoceros (Diceros bicornis) by Andrew Paul Stringer A thesis submitted to Victoria University of Wellington in fulfilment of the requirement for the degree of Doctor of Philosophy Victoria University of Wellington 2016 ii This thesis was conducted under the supervision of: Dr Wayne L. Linklater Victoria University of Wellington Wellington, New Zealand The animals used in this study were treated ethically and the protocols used were given approval from the Victoria University of Wellington Animal Ethics Committee (ref: 2010R6). iii iv Abstract This thesis combines investigations of parasite ecology and rhinoceros conservation biology to advance our understanding and management of the host-parasite relationship for the critically endangered black rhinoceros (Diceros bicornis). My central aim was to determine the key influences on parasite abundance within black rhinoceros, investigate the effects of parasitism on black rhinoceros and how they can be measured, and to provide a balanced summary of the advantages and disadvantages of interventions to control parasites within threatened host species. Two intestinal helminth parasites were the primary focus of this study; the strongyle nematodes and an Anoplocephala sp. tapeworm. The non-invasive assessment of parasite abundance within black rhinoceros is challenging due to the rhinoceros’s elusive nature and rarity. Hence, protocols for faecal egg counts (FECs) where defecation could not be observed were tested. This included testing for the impacts of time since defecation on FECs, and whether sampling location within a bolus influenced FECs. Also, the optimum sample size needed to reliably capture the variation in parasite abundance on a population level was estimated. To identify the key influences on parasite abundance, the black rhinoceros meta- population in South Africa presented an extraordinary and fortuitous research opportunity. Translocation and reintroduction have created multiple populations from the same two source populations, providing a variety of comparable populations with the same host-parasite relationship. I applied my population-level faecal sampling and egg count protocol to collect 160 samples from 18 black rhinoceros populations over two summer sampling periods between 2010 and 2012. I test hypotheses for the influence of a variety of ecological and abiotic factors on parasite abundance. To test for the influence of individual-level host characteristics on parasite abundance, such as age and sex, I collected rectal faecal samples at the translocation of 39 black rhinoceros. At that time I also investigated the influence of body condition on a variety of measures of host resources, such as the size of sexually selected characteristics. Finally I developed a logical and robust approach to debate whether parasites of threatened host species should be controlled. For faecal egg counts, samples taken from the centre of faecal boluses did not change significantly up to six hours after defecation. The only factor which significantly affected the size of confidence intervals of the mean parasite abundance for a host population for both parasite groups was the level of parasite aggregation. The accuracy of estimates of mean parasite abundance increased with increasing sample size, with >9 samples having little further v effect on accuracy. As host defecation no longer needs to be observed the efficiency of fieldwork for studies investigating elusive host species is greatly increased. On a population level, host density was the leading model explaining the abundance of both a directly and an indirectly transmitted parasite. For instance, doubling host density led to a 47% rise in strongyle parasite abundance. I found no support for competing hypotheses, such as climate-related variables, that were thought to affect the abundance of free-living stages of macroparasites. This result will be useful to conservationists as it will allow them to predict where parasite abundance will be greatest and may also reveal potential avenues for parasite control. On an individual level, younger individuals may have harboured higher levels of parasitism (p = 0.07). This result would be widely supported by the literature, but a larger host age range is needed to verify the result. I identified four sexual dimorphisms, with anterior horn volume and circumference, and body size, all showing a sex difference in both the slope and intercept of regression lines. Although sexually selected traits are implicated as most vulnerable to parasite impacts, I did not find an influence of parasite abundance on the size of these potentially sexually-selected characteristics or other measures of body condition. This may be because of numerous different factors affecting host resources, of which the parasite groups studied are a relatively small proportion. Parasites can be an important cause of population decline in threatened species. However, the conservation of potentially threatened parasites within host species is rarely considered. Here, I debated the potential benefits and pitfalls of parasite control to help identify the principles behind parasite control within threatened species. I rank 11 identified different types of parasite control by their potentially detrimental effects on host populations and ecosystems. I conclude that as the risk a parasite poses to host extinction increases, so does the justification for using parasite control methods with potentially detrimental effects. Also, the extinction risk of the parasite should determine the need for dedicated parasite conservation programs. These principles may be predominantly intuitive, but there are a number of examples in the literature where they have not been used, such as the treatment of parasites with low levels of virulence in host species of ‘least concern’. The principles provide a framework for the adaptive implementation of parasite control strategies in conservation-reliant species, like rhinoceros. I embarked on the first multi-population and comparative study of host-parasite relationships in the critically endangered black rhinoceros. This was made possible by empirically testing and refining field sampling protocols to overcome concerns about sample vi identification, number, and age. Through these well-developed, efficient sampling methodologies I was able to determine that host density was the main influence on parasite abundance within black rhinoceros on a population level – a result not previously proven for macroparasites. Influences on individual level variation need further investigation. In particular genetic factors, such as inbreeding, were not researched as part of this study. I successfully identified a number of sexual dimorphisms, but found no evidence that they were influenced by individual parasite abundance. Finally I use a targeted review of the literature to propose some principles behind whether parasites should be controlled within threatened host species. These principles should allow conservation managers to focus resources on those situations where parasite control is needed, and also help conservation managers avoid the potentially detrimental effects of parasite control. In these ways this thesis has advanced the study and understanding of parasites, their ecology, and their relationship to conservation-reliant hosts. vii Acknowledgements Many thanks to my parents, family, and friends. In particular Tom Hawkins, Paul Fisher, and Roan Plotz. Wayne Linklater for all his help, advice and eating all the pies. All colleagues at Victoria University of Wellington: Rosalyn Anderson-Lederer, Gaius Wilson, Megan English, Doug Eckery, Heiko Wittmer, Nicola Nelson, Graham Le Gros, Simon Davy, Dalice Sim, Anne Wietheger, Shaun Wilkinson, Luke Cooney, Emma Gibbin, Katie Hillyer, Grace Paske, Stefanie Pontasch, Karl Yager, Jennifer Howe, and the rest of the coffee club. Eastern Cape Parks and Tourism Agency and associated staff: Dean Peinke, Brad Fike, and Gav Shaw. Ezemvelo KZN Wildlife and associated staff: Jed Bird, Geoff Clinning, Tarik Bodasing, Dave Druce, Bhom Ndondwe, Joseph, Chris Barichievy, Pete Ruinard, Petros Ngwenya, Catherine Hanekom, Dennis Kelly, Dave Robertson and Suni Raas. Wildlife Act: Chris Kelly, Simon Morgan, and Cathy. A special mention to the ineffable Brendan Whittington-Jones. All friends and colleagues who filled in the online body condition survey. Many thanks for the valuable assistance from Nelson Mandela Metropolitan University including Graham Kerley, Shirley Parker-Nancy, Craig Tambling, Liaan Minnie, Diane Smith, and Marietjie Landman, South African National Parks capture unit including Dave Zimmerman, Cathy Dreyer, Markus Hofmeyr, Tosh Ross, and Hanno Kilian, the South African Weather Service, the Rhino Resource Center, Annemieke van der Goot, WWF and Jacques Flamand. Very special thanks to the owners, staff and black rhinoceros monitors from numerous private reserves who wished to remain anonymous due to the recent upsurge in rhinoceros poaching. Many thanks to Anne La Flamme, Nancy Webber and Stephen Hartley for their very useful comments on final drafts of the manuscript. I would also like to say hello to Jason Isaacs. viii Contents Abstract .................................................................................................................................. v Acknowledgements ............................................................................................................ viii List
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