Coevolution between brood-parasitic honeyguides and their hosts Luke Alexander McClean Thesis presented for the degree of Doctor of Philosophy Town FitzPatrick Institute of African Ornithology, DST-NRF Centre of Excellence, Department of Biological Sciences, Faculty of Science, University of Cape Town January 2020Cape Supervised by Professor Claire N. Spottiswoodeof and Dr Nicholas P.C. Horrocks University The copyright of this thesis vests in the author. No quotation from it or information derived fromTown it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non- commercial research purposes only. Cape Published by the University of Cape Town (UCT) in terms of the non-exclusive licenseof granted to UCT by the author. University The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgement of the source. The thesis is to be used for private study or non-commercial research purposes only. Published by the University of Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. Abstract Obligate brood parasites lay their eggs in the nests of other species, foisting the costs of parental care onto the host parents. The success of the parasite and host are then at odds, with both parties evolving defences and countermeasures in an evolutionary arms race. This reciprocal influence of acting upon both species’ evolution — a process known as coevolution — has forged the natural world around us. Avian brood parasites and their hosts are now model systems for studying such coevolutionary interactions between species, providing striking examples of the adaptations that arise when the life histories of two species become entangled. In this thesis I highlight the adaptations that have arisen in response to coevolutionary selection pressures in a group of understudied avian brood parasites, the honeyguides (Indicatoridae), and their hosts. This study focuses on the greater (Indicator indicator) and lesser (I. minor) honeyguides, and their respective primary hosts, the little bee-eater (Merops pusillus) and the black-collared barbet (Lybius torquatus). The interactions between honeyguides and their cavity-nesting hosts of the Old World tropics are evolutionarily ancient, contrasting with the majority of studies of avian brood parasitism which have predominantly focused on temperate brood-parasitic species targeting open cup-nesting hosts. Therefore, honeyguides and their hosts are an ideal study system in which look for novel adaptations that have not evolved in other systems. Using field observations and experimental manipulations at each stage of the parasitic life cycle — before parasitism, during egg-laying, during incubation, and during chick- rearing — I examine how honeyguides and their hosts have evolved in response to the selection pressures they exert on each other. First, in chapter two, I consider whether the nest structure of the little bee-eater – host to the greater honeyguide – can act as a defence against brood parasitism. Experimental manipulation of the size of bee-eater nest tunnels demonstrates that bee-eaters with narrower nest tunnels are less likely to be parasitized by greater honeyguides than those bee-eaters whose nests have wider nest tunnel entrances. This study provides the first experimental evidence of a host nest functioning as a frontline defence against brood parasitism. In chapter three, I take a comparative approach and use a phylogenetic framework to investigate, across multiple avian brood parasite species, the evolutionary drivers of rapid egg- laying. This trait is shared by most brood-parasitic birds, but not by non-parasitic birds. I find strong evidence that the egg-laying speed of avian brood parasites is ecologically and physiologically constrained, but find no evidence that variation in the costs incurred during i parasitism events have driven variation in the rapidity of egg-laying among brood-parasitic species. In chapter four, I examine whether there are costs associated with the virulent egg puncturing behaviour of greater honeyguides, and whether honeyguides can adjust their level of virulence in accordance with these costs. I find strong support for the idea that virulence is costly to honeyguides, as bee-eater hosts are more likely to reject clutches that contained eggs punctured by honeyguides. Such punctured clutches are also more likely to be predated. Honeyguides appear to adjust how much they puncture host eggs in accordance with the severity of these costs, providing the first evidence of an avian brood parasite moderating its virulence in response to the associated costs. In chapter five, I examine egg rejection behaviour in the black-collared barbet, a common host of the lesser honeyguide. I consider whether the (smaller) size of a parasitic egg could be used as a cue for egg rejection inside the dark environment of a cavity nest. Through observations of natural parasitism events, and experimental parasitism of host nests using different sized eggs, I demonstrate that barbets are more likely to reject a clutch of eggs when they detect a small egg within the nest. This seems to be achieved through a process of true recognition, a mechanism that involves a specific innate or learnt template of what size eggs a host should reject. Barbets do not appear to rely on discordancy – comparing all eggs within their clutch in order to reject the odd one out – in order to make rejection decisions. Finally, in chapter six I explore whether honeyguides elicit additional provisioning from their foster parents by using vocal mimicry, and investigate why such extra food would be required. I demonstrate that both greater and lesser honeyguides mimic the sound of a brood of chicks of their respective hosts in order to receive higher levels of provisioning from their foster parents. I establish that greater and lesser honeyguides do this for contrasting reasons. Greater honeyguides require higher levels of provisioning to support their fast growth rate to a size much larger than their host siblings, whereas lesser honeyguides require more food in order to offset a sub-optimal diet provided to them by their foster parents. ii Acknowledgements There are many people that have made this PhD possible. The list of people I am thankful to is much longer than what follows, and I am sure to have left some people out. If by some chance you are reading this and do not find your name, know it is only a mistake of omission. I thank The Leverhulme Trust for their financial support, provided through Study Abroad Scholarship. Particularly, I would like to thank Bridget Kerr, who has been immensely helpful and friendly in all our communications. Thanks to the South African Department of Science and Technology – National Research Foundation Centre of Excellence at the FitzPatrick Institute for providing funding to conduct my research in Zambia each year. Thank you to the University of Cape Town for hosting me these three years. It was an amazing place in which to study and live. I must thank both my supervisors. Claire Spottiswoode for giving me the opportunity to study with her in Africa. I thoroughly appreciate the breadth of her knowledge and skill in conveying it to me. Nick Horrocks, for putting up with me for months at a time in Zambia and his endless and prompt feedback on all my ideas and drafts. I am indebted for their faith in my research ideas, their guidance and understanding. Their endless patience has made the arduous journey of a PhD that much more rewarding. I am hugely thankful to the greater Choma community, who not only made my field work in Zambia possible, but provided me with a home away from home for three months of each year. Thank you to the residents of Musumanene and Semahwa Farms, for the endless assistance conducting fieldwork. In particular, I would like to thank Oliver and Harvest Kashembe, Efte, Oscar, Amos Richards, Callisto Shankwasiya, Gift Mulonda and Tom Hamusikili, for four years of adept nest finding. Thanks to Silky Hamama, Lazaro Hamusikili, Collins Moya, Sanigo Mwanza and Sylvester Munkoko for their expert assistance and friendship during fieldwork. I am grateful to Dr Lackson Chama at the Department of Zoology and Aquatic Sciences at Copperbelt University for his assistance within Zambia. I am grateful to the Department of National Parks and Wildlife for permission to conduct research in Zambia, and in particular to Rhoda Kachali, Jassiel M’Soka and Priscilla Sichone for their kind support to our project. To Molly and Archie Greenshields, for providing a roof over my head in their home in Zambia and for the countless yarns over dinner. To Richard and Vicki Duckett, Troy and Squacky Nicolle, for allowing me to stay and conduct my research on their land. To Ian and iii Emma Bruce-Miller, for their friendship, generosity and hospitality at Muckleneuk Farm. To Annabel Hughes and Chris Aston for their warm support in Livingstone. Thanks to the rest of the amazing Zambian brood parasites team – Tanmay Dixit, Gabriel Jamie, and Jess Lund, for their excitement in both their own research pursuits and in mine. To all my friends at the Fitz, my office-mates Carina Nebel, Anthony Lowney, Diana Bolopo, Petra Sumasgutner and Shane McPherson for being keen procrastinators consisting of coffee breaks and birding trips. Thank you to all the support staff at the Fitz: Rob Little, Denise Scheepers, Carmen Smith, Gonzalo Aguilar, Susan Mvungi. I am particularly thankful to Anthea Links and Hilary Buchanan for their aid in all matters bureaucratic (there were many) throughout my time in South Africa. Also, thanks to those at the University of Cambridge Zoology Department, who hosted me during part of my write-up. Thanks are extended to Will Feeney, Jessie Walton, and Analia Lopez, for providing videos of brood parasites laying their eggs for my analysis in chapter three.