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Immunity, Life History and Conservation in the Galapagos Sea Lion

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Immunity, Life History and Conservation in the Galapagos Sea Lion Immunity, life history and conservation in the Galapagos sea lion Patrick Michael Brock Submitted in accordance with the requirements for the degree of Doctor of Philosophy University of Leeds, Faculty of Biological Sciences September 2012 2 Declaration The candidate confirms that the work submitted is his own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors of this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given in the thesis where reference has been made to the work of others. Chapter 2 is based on the jointly authored publication: Brock, P.M., Hall, A.J., Goodman, S.J., Cruz, M. & Acevedo-Whitehouse, K. 2012. Applying the tools of ecological immunology to conservation: a test case in the Galapagos sea lion. Animal Conservation. Published online 26th June. DOI: 10.1111/j.1469- 1795.2012.00567.x Chapter 3 is based on the jointly authored manuscript: Brock, P.M., Hall, A.J., Goodman, S.J., Cruz, M. & Acevedo-Whitehouse, K. The cost of immunity is modulated by anthropogenic environmental impacts. Submitted to PLOS One, 11th August 2012, returned on 18th September for ‘major revisions’. In both cases the research was conceived by PMB, KAW, SG and AH. PB and MC carried out fieldwork and laboratory work. PB analysed the data and wrote the first draft of manuscripts. KAW, SG and AH, commented on manuscripts and PB produced the final manuscripts. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgment. © 2012 The University of Leeds and Paddy Brock 3 Acknowledgments I would like to thank the Institute of Zoology, the Natural Environment Research Council, the University of Leeds, the Sea Mammal Research Unit at the University St. Andrew’s and the Universities Federation of Animal Welfare for the funding and support that made this project possible. All the work presented in this thesis was carried out under Galapagos National Park permits PC-18-09, N°046-2009-PNG, N°101-2010-PNG and N°032-2010- PNG, and samples were imported to the UK under Department for Environment Food and Rural Affairs permits POAO/2008/925 and POAO/2010/136. I am extremely grateful to my supervisors Karina Acevedo-Whitehouse and Simon Goodman for all their support and constructive feedback during the course of the project. This research would not have been possible without their help, without Karina’s Nextian determination or without Simon’s humour at crucial moments (30/09/2010). I would also like to thank Ailsa Hall for her help in the laboratory and her excellent advice; Marilyn Cruz for her support in the field and her patient tutelage; Pamela Martinez for her toughness; Jorge Torres for his dedication; and Alberto Velez for his forbearance. I am also grateful to Fritz Trillmich, Elke Hippauf, Tine Meise and the rest of the research group at the University of Bielefeld for welcoming me so warmly; Virna Cedeño, Washington Tapia, Juan Carlos Murillo, Eduardo Espinoza, Judith Denkinger, Pablo Mejia, Ricardo Visaira, Mario and Lutty for their assistance during fieldwork; Rupert Quinnell and Judith Smith for their scientific advice; Bill Holt and Daphne Green for their help in the laboratory; Patricia Brekke and Jinliang Wang for their time and thoughts; and Trent Garner and Guy Cowlishaw for their guidance. Lastly, I would like to thank my family, Kay, George, Ollie, Michael, Eleanor and Helen for their wonderful love and support; Rose, the sister I never had; Mark and Claire for their formative enthusiasm; Jon and Harry for keeping me sane during the ice-cold-indoor- winter; and Jana for being Jana, and for showing me an end of the earth. 4 Abstract Infectious disease threatens health and biodiversity across the globe, and disease emergence may become more common as humans further encroach on habitats and modify environments. To assess the risks of disease emergence in natural populations accurately, we require an understanding of the workings of immunity in the wild. This thesis is about immunity in the context of life history in the endangered Galapagos sea lion, and aims to contribute to understanding of immune dynamics in wild populations, and to evidence-based conservation management. The introduction reviews the development of the discipline of ecological immunology, and discusses the application of its methodological tools to little- known species such as the Galapagos sea lion. The first data chapter uses these tools to describe the ontogeny of Galapagos sea lion immunity in two contrasting ecological contexts. The second data chapter contextualises the immune variation described in the first by assessing the relationship between immune activity and condition. The third data chapter introduces a genetic dimension through the analysis of inbreeding estimates with immune measures. The fourth and final data chapter uses epidemiological models to assess the risk of Galapagos sea lion exposure to canine distemper virus under different management and environmental scenarios. The discussion brings together the results of the data chapters and evaluates emergent themes and limitations in the context of suggestions for future work. The results show that the study of immune variation in species such as the Galapagos sea lion can provide useful insight into the dynamics of immunity in the wild, and information that can have practical application to conservation. They also lay a foundation for integrated epidemiological analyses of disease risk that incorporate physiological and immunological variation, and that have potential for constructive development beyond the Galapagos sea lion. 5 Table of Contents Declaration ..................................................................................................... 2 Acknowledgments ......................................................................................... 3 Abstract .......................................................................................................... 4 List of Tables .................................................................................................. 7 List of Figures ................................................................................................ 9 List of Abbreviations ................................................................................... 11 Chapter 1. General introduction ................................................................. 13 Immunity .......................................................................................................... 13 Ecological immunology .................................................................................... 17 Trade-offs ........................................................................................................ 19 Quantifying immunity ....................................................................................... 22 Wild immunology ............................................................................................. 25 The Galapagos sea lion ................................................................................... 26 Thesis aims ..................................................................................................... 30 Chapter 2. Applying the tools of ecological immunology to the Galapagos sea lion ...................................................................................... 33 Introduction ......................................................................................................... 34 Methods .............................................................................................................. 37 Sampling ......................................................................................................... 37 Haematology ................................................................................................... 40 Serum proteins ................................................................................................ 40 Immunoglobulin G ........................................................................................... 41 Phytohemagglutinin ......................................................................................... 41 Statistical analysis ........................................................................................... 41 Immune measure covariation........................................................................... 44 Results ................................................................................................................ 46 Discussion ........................................................................................................... 64 Immune variation with colony and age ............................................................. 64 Immune measure covariation........................................................................... 70 The ecological context ..................................................................................... 72 Chapter 3. Negative correlation between changes in immune activity and body condition under human influence ..................................................... 76 Abstract ............................................................................................................... 76 Introduction ......................................................................................................... 77
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