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The Drivers and Consequences of Hookworm Disease in South

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The Drivers and Consequences of Hookworm Disease in South THE DRIVERS AND CONSEQUENCES OF HOOKWORM DISEASE IN SOUTH AMERICAN FUR SEALS by MAURICIO SEGUEL (Under the Direction of Nicole Gottdenker and Elizabeth Howerth) ABSTRACT Hookworms are highly pathogenic hematophagous nematodes that parasitize more than 100 species of wild animals. Hookworms of fur seals and sea lions are particularly virulent, causing high levels of mortality, however little is known about the drivers of these effects. During 10 reproductive seasons, the dynamics of hookworm diseases was studied in the South American fur seals (SAFS, Arctocephalus australis, Otariidae) rookery at Guafo Island, Chilean Patagonia. Fur seal hookworms (Uncinaria sp.) reached 100% prevalence among pups, and in animals with high burdens (>300 nematodes) there was marked hemorrhagic enteritis, sometimes with peritoneal penetration. The life cycle of Uncinaria sp. in SAFS involved brief lactogenic transmission of infective larvae. This hookworm species has a live fast die young life history strategy that translates into aggressive feeding behavior and high rates of extraction of host resources. Therefore, pups with high burdens, a third of pups born each year, suffered significant levels of anemia and up to 60% hookworm-related mortality. These pups contributed disproportionally to parasite fitness, and increases in host mortality (virulence) always paid off in terms of parasite fitness, selecting for higher virulence within the parasite population. Pups that survived hookworm infection developed an efficient immune-mediated parasite clearance where T-lymphocytes, basophils, mast cells and parasite specific IgG were key players. Pups that received higher levels of maternal attendance had better energy balance and a more reactive immune system. These pups cleared hookworm infection earlier, increasing their chances of survival. Maternal attendance decreased in years with high sea surface temperature (SST), probably reflecting less availability of prey in the environment. Therefore, in years with high SST, fur seal pups exhibited a weaker immune response and higher levels of hookworm mortality. Hookworm disease is the most significant cause of death in many otariid populations, and the present study demonstrates that the parasite is selected for higher virulence, especially when a high hookworm burden is favored. The key role of parasite immune clearance in hookworm infection dynamics and the link between environmental conditions and pups immune system present a scenario where global climate change may lead to increased hookworm virulence and mortality of fur seal pups. INDEX WORDS: climate change, ecology, hookworm, immunology, marine mammals, pathology. THE DRIVERS AND CONSEQUENCES OF HOOKWORM DISEASE IN SOUTH AMERICAN FUR SEALS by MAURICIO SEGUEL BVSc, Universidad Austral de Chile, Chile, 2007 DVM, Universidad Austral de Chile, Chile, 2010 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2018 © 2018 MAURICIO SEGUEL All Rights Reserved THE DRIVERS AND CONSEQUENCES OF HOOKWORM DISEASE IN SOUTH AMERICAN FUR SEALS by MAURICIO SEGUEL Major Professor: Nicole Gottdenker Elizabeth Howert Committee: Vanessa Ezenwa Donald Harn Electronic Version Approved: Suzanne Barbour Dean of the Graduate School The University of Georgia August 2018 DEDICATION To those who walked the forests before me, to those who navigated the rivers before me, to those who named the stars. To my Mapuche people, their teachings and values. iv ACKNOWLEDGEMENTS This work could not have been possible without the collaboration and contribution of numerous people and organizations in the United States and Chile. I would like to acknowledge the funding agencies that provided funds for tuition, travel and field research; The Fulbright Commission, CONICYT Chile, Morris Animal Foundation, Universidad Austral de Chile, LACSI at the University of Georgia, Rufford Small Animal Grants, Society for Marine Mammalogy, Mohamed Bin Zayed Species Conservation fund, the Pathology Department at the University of Georgia and the numerous people that contributed with donations in our crowdfunding campaigns. I appreciate very much the logistical support of the Chilean Navy, Artisanal fishermen of Quellon and the numerous crews of the Chilean Navy at Guafo Island lighthouse. I thank tremendously the abnegate field assistance and partnership of Amanda Hooper, Elvira Vergara, Ignacio Silva, Rocio Carrasco, Eugene DeRango, Lorraine Barbosa, Josefina Gutierrez, Diego Perez, Felipe Montalva, Francisco Munoz, Piero Becker, Emily Morris, Sian Tarrant, Emma Milner and Camila Diaz. I would like to thank the scientific collaboration in the Guafo Island science projects of Claudio Verdugo, Daniel Crocker, Maria Jose Navarrete, Hector Paves, Ananda Muller, Enrique Paredes, Shawn Johnson and Claire Simeone. Finally, I would like to thank the continuous and restless support of my friends and family, which through many years have supported my ideas and accepted the long periods of field work. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .............................................................................................................v LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ...................................................................................................................... xii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .....................................................1 Abstract ....................................................................................................................2 Introduction ..............................................................................................................3 Materials and Methods .............................................................................................4 Results ......................................................................................................................6 Discussion and Conclusion ....................................................................................21 References ..............................................................................................................23 Figures....................................................................................................................60 Tables .....................................................................................................................65 2 HOOKWORM INFECTION IN SOUTH AMERICAN FUR SEALS: FACTORS ASSOCIATED WITH HOST TISSUE DAMAGE AND SURVIVAL ......................80 Abstract ..................................................................................................................81 Introduction ............................................................................................................82 Materials and Methods ...........................................................................................84 Results ....................................................................................................................89 vi Discussion ..............................................................................................................94 References ..............................................................................................................99 Figures..................................................................................................................104 Tables ...................................................................................................................108 3 LIVE FAST AND DIE YOUNG LIFE HISTORY STRATEGY DRIVES HIGH VIRULENCE OF PINNIPED HOOKWORMS ........................................................112 Abstract ................................................................................................................113 Introduction ..........................................................................................................114 Materials and Methods .........................................................................................117 Results ..................................................................................................................122 Discussion ............................................................................................................126 References ............................................................................................................131 Figures..................................................................................................................134 Tables ...................................................................................................................140 4 CHANGES IN OCEAN TEMPERATURE AFFECT HOST-PARASITE DYNAMICS IN A MARINE MAMMAL ...............................................................144 Abstract ................................................................................................................145 Introduction ..........................................................................................................146 Materials and Methods .........................................................................................150 Results ..................................................................................................................158 Discussion ............................................................................................................162
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