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Feeding Behavior of Wild and Captive Oxpeckers (Buphagus Spp.): a Case of Conditional Mutualism Tiffany B

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Feeding Behavior of Wild and Captive Oxpeckers (Buphagus Spp.): a Case of Conditional Mutualism Tiffany B University of Miami Scholarly Repository Open Access Dissertations Electronic Theses and Dissertations 2009-05-15 Feeding Behavior of Wild and Captive Oxpeckers (Buphagus spp.): A Case of Conditional Mutualism Tiffany B. Plantan University of Miami, [email protected] Follow this and additional works at: https://scholarlyrepository.miami.edu/oa_dissertations Recommended Citation Plantan, Tiffany B., "Feeding Behavior of Wild and Captive Oxpeckers (Buphagus spp.): A Case of Conditional Mutualism" (2009). Open Access Dissertations. 239. https://scholarlyrepository.miami.edu/oa_dissertations/239 This Open access is brought to you for free and open access by the Electronic Theses and Dissertations at Scholarly Repository. It has been accepted for inclusion in Open Access Dissertations by an authorized administrator of Scholarly Repository. For more information, please contact [email protected]. UNIVERSITY OF MIAMI FEEDING BEHAVIOR OF WILD AND CAPTIVE OXPECKERS (BUPHAGUS SPP.): A CASE OF CONDITIONAL MUTUALISM By Tiffany B. Plantan A DISSERTATION Submitted to the Faculty of the University of Miami in partial fulfillment of the requirements for the degree of Doctor of Philosophy Coral Gables, Florida May 2009 ©2009 Tiffany B. Plantan All Rights Reserved UNIVERSITY OF MIAMI A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy FEEDING BEHAVIOR OF WILD AND CAPTIVE OXPECKERS (BUPHAGUS SPP.): A CASE OF CONDITIONAL MUTUALISM Tiffany B. Plantan Approved: ________________ _________________ Michael S. Gaines, Ph.D. Terri A. Scandura, Ph.D. Professor of Biology Dean of the Graduate School ________________ _________________ David Janos, Ph.D. William Searcy, Ph.D. Professor of Biology Professor of Biology ________________ Judith Bronstein, Ph.D. Professor of Biology University of Arizona PLANTAN, TIFFANY B. (Ph.D., Biology) Feeding Behavior of Wild and Captive Oxpeckers (May 2009) (Buphagus spp.): A Case of Conditional Mutualism Abstract of a dissertation at the University of Miami. Dissertation supervised by Professor Michael S. Gaines No. of pages in text. (178) Mutualisms are delicately balanced partnerships and are increasingly recognized as being fundamental to patterns and processes within ecological systems. Changes to the ecological setting in which such interactions operate can disrupt this balance. By understanding the context-dependent nature of such associations, researchers can begin to understand how changes in the environment can have cascading effects on the entire community within which they occur. Oxpeckers (Buphagus spp.) feed on the ectoparasites of ungulates in sub-Saharan Africa and from the blood of ungulate wounds. Because of this dichotomy in feeding behavior, the role of oxpeckers as consistently beneficial partners of their hosts has been questioned, and it has been suggested that the concept of conditional mutualism be applied to this interaction. I combined observational studies of oxpeckers in Kruger National Park, South Africa, with experiments on oxpeckers in captivity at the Mokopane Biodiversity Conservation Centre, South Africa, to test the hypothesis that the ectoparasite cleaning service provided by oxpeckers to their hosts is context-dependent. The results of my dissertation research demonstrate that the oxpecker-ungulate association has conditional outcomes. Under certain conditions, the oxpecker-ungulate relationship is a nutritional mutualism where ungulates provide food (ticks) for oxpeckers in exchange for a cleaning service. Under other conditions, oxpeckers exploit their hosts to feed from their blood. My findings suggest that a high abundance of the tick species and tick stages oxpeckers prefer is necessary to maintaining an alignment of interests between oxpeckers and ungulates. When ungulates host few ticks of the species oxpeckers prefer, these birds will wound-feed to meet their nutritional demands. Such wound-feeding threatens the balance of the oxpecker-ungulate mutualism. Although oxpeckers frequently wound-fed in captivity, the frequency of wound-feeding events on wild host species was only 3.1% of feeding events. Whether the relationship between oxpeckers and domesticated hosts differs from that between oxpeckers and wild hosts, or if this observed difference is actually a result of researcher constraints in the wild, needs further exploration. This thesis is dedicated to my family. You provided me with the love and support I needed to pursue my dream in Africa. iii ACKNOWLEDGEMENTS To my advisor, Dr. Michael S. Gaines. You have been an advisor, a teacher, a supporter, a critic, a friend, and a confidant. Thank you for believing in me when I needed it the most. To my Graduate Committee, Dr. Judith Bronstein, Dr. David Janos, and Dr. William Searcy. I express my deepest gratitude to you for believing in this project, challenging my ideas, and helping me develop into a better scientist. To Professor Ivan Horak, whose kindness and tick expertise are unmatched. To my labmates and graduate student colleagues for being amazing friends, listeners, storytellers, and distracters through the years. To all my South African friends who supported me and comforted me during the endless challenges I faced abroad. To the University of Miami, which provided funding for this project through the Tropical Biology Fellowship. iv These acknowledgements would not be complete without recognizing those institutions in South Africa that made the impossible possible: The National Zoological Gardens of South Africa (NZG), particularly Professor Antoinette Kotzé, for not only accepting my research project and advertising it as a flagship project for the NZG’s research initiatives, but for intellectual, logistical, and financial support. The Mokopane Biodiversity Conservation Centre (MBCC), which served as my home for over a year. Special gratitude is extended to Mr. Mark Howitt and his family. Kruger National Park (KNP) where I spent endless days observing the African wildlife I had only imagined as a child, and where Sharon and Dave Thompson and Andre and Stefanie Ganswindt became my family away from home. The Endangered Wildlife Trust, particularly Arnaud le Roux, and the Limpopo Department of Economic Development, Environment and Tourism for shelving their reservations and allowing me to research this magnificent bird. And to Kenny… Thank you for sacrificing the world to make my dream a reality. v McAttee (1944): “The perching of birds upon animals is not altogether an innocent and mutually advantageous arrangement; like so many relations, it has become perverted in some instances and has a sinister side.” vi TABLE OF CONTENTS PAGE LIST OF FIGURES ix LIST OF TABLES xi CHAPTER ONE: INTRODUCTION The Potential for Conditionality in the Oxpecker-Ungulate Interaction 1 Background 2 Study Species 6 Oxpecker Controversy: The Beginnings 9 Conditional Cleaners 15 CHAPTER TWO: The Tick and Wound-Feeding Behavior of Oxpeckers (Buphagus spp.) in Kruger National Park, South Africa 20 Summary 21 Background 23 Methods 30 Results 34 Discussion 41 Conclusion 48 CHAPTER THREE: Population Dynamics of Free-Living Ixodid Ticks Relative to Oxpecker-Ungulate Presence 60 Summary 61 Background 63 Methods 70 Results 74 Discussion 79 Conclusion 84 vii CHAPTER FOUR: Feeding Preferences of the Red-Billed Oxpecker (Buphagus erythrorhynchus): A Bird That Pecked Its Way to Parasitism 98 Summary 99 Background 101 Methods 105 Results 115 Discussion 123 Conclusion 130 CHAPTER FIVE: The Oxpecker (Buphagus spp.) Diet: A Nutritional Analysis of Ticks and Blood 140 Summary 141 Background 142 Methods 143 Results 144 Discussion 144 Conclusion 147 CONCLUSION 151 APPENDICES 156 Appendix A: Bird-Mammal Feeding Associations 157 Appendix B: Comparison of Argasid and Ixodid Ticks 159 Appendix C: Ixodid Ticks of South Africa 160 Appendix D: Blood-Feeding Birds 161 REFERENCES 163 viii FIGURES PAGE CHAPTER TWO Fig. 2.1 Study area in Kruger National Park, South Africa 54 Fig. 2.2 Percentage of total oxpecker utilization (a) of eight host species 55 in Kruger National Park and percentage of total oxpecker utilization of these hosts in the wet (b) and the dry (c) seasons Fig. 2.3 Percentage of red-billed oxpecker observational events per host 56 species (a) and percentage of yellow-billed oxpecker observational events per host species (b) Fig. 2.4 Feeding versus non-feeding events for each oxpecker species 57 Fig. 2.5 Proportions of the observed feeding behaviors of red-billed 57 oxpeckers and yellow-billed oxpeckers Fig. 2.6 Number of red-billed oxpecker and yellow-billed oxpecker 58 feeding events during which an oxpecker only non-wound fed (tick, ear, eye, anogenital, nose, mouth) or only wound-fed Fig. 2.7 Total oxpecker feeding behavior related to season 58 Fig. 2.8 Proportion of host response behaviors to oxpeckers in the wet 59 and the dry season Fig. 2.9 Host response behavior to wound-feeding and non-wound 59 feeding oxpeckers CHAPTER THREE Fig. 3.1 Map of study sites in Kruger National Park, South Africa 89 Fig. 3.2 Tick plots of Kruger National Park, South Africa 90 Fig. 3.3 Tick drag apparatus 91 Fig. 3.4 Percentage of larval, nymphal and adult ticks collected in 92 Makhohlola and Shingwedzi Fig. 3.5 Percentage of ticks of each species collected in Makhohlola and 93 Shingwedzi ix Fig. 3.6 Percentage of ticks belonging to the oxpecker diet that were collected 94 in the high mammal use plot and low mammal use plot of Makhohlola and Shingwedzi Fig. 3.7 Mean number of ticks (±SE) collected in low mammal use (LMU) and 94 high mammal use (HMU) plots of each site (Makhohlola and Shingwedzi) in the wet and the dry season. Fig. 3.8 Number of ticks collected monthly in Makhohlola and Shingwedzi 95 April 2007-March 2008 Fig. 3.9 Percentage of ticks of each species collected at Makhohlola and 96 Shingwedzi in the wet and the dry season Fig. 3.10 Temperature of Makhohlola and Shingwedzi April 2007-March 2008 97 Fig. 3.11 Rainfall of Makhohlola and Shingwedzi April 2007-March 2008 97 CHAPTER FOUR Fig. 4.1 Oxpecker enclosure at the Mokopane Biodiversity Conservation 135 Centre (MBCC), South Africa Fig.
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