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Opening Pages Investment patterns and kinship cues in a cooperatively breeding bird Nyil Khwaja Thesis submitted for the degree of PhD Department of Animal & Plant Sciences University of Sheffield January 2017 Contents Acknowledgements 7 Statement of intellectual contribution 9 General summary 11 INTRODUCTION TO THE THESIS 13 1. General introduction 15 Parental investment 16 Offspring investment with multiple carers 17 Investment in relation to offspring sex 19 Summary 20 Cooperative breeding in birds 21 Why helpers help 22 Factors creating the conditions for helping 24 Ultimate predictors of cooperative breeding 27 Summary 28 Kin recognition 28 Adaptive basis 29 Mechanism and development 30 Summary 31 Scope of the thesis 32 Riflemen 32 Thesis outline 33 General methods 34 Kowhai Bush 34 Field methods 35 Genotyping 36 Ethical note 36 INVESTMENT PATTERNS OF PARENTS AND HELPERS 39 2. Flexibility but no coordination of visits in provisioning riflemen 41 Introduction 42 Methods 45 Data collection 45 Testing the relationship between visit rate and load size 45 Repeatability analysis 46 Other factors affecting visit rate and load size 47 Testing for alternation by carers 47 Results 48 Relationship between visit rate and load size 48 Repeatability of visit rate and load size 50 Other factors affecting visit rate and load size 50 Alternation of nest visits 53 Discussion 53 SEX ALLOCATION IN COOPERATIVELY BREEDING BIRDS 59 3. Cheaper, more helpful males are not overproduced by breeding riflemen 61 Introduction 62 Methods 64 Data collection 64 Data analysis 65 Results 66 Size dimorphism 66 Adult sex ratio 66 Brood sex allocation 67 Investment in relation to brood sex ratio 70 Discussion 70 4. No cross-species support for the repayment hypothesis in birds 75 Introduction 76 Methods 77 Results 79 Discussion 83 No overall bias to producing the more helpful sex 84 Rarity of sex ratio manipulation 86 Conclusion 88 TESTING POTENTIAL KINSHIP CUES IN RIFLEMEN 89 5. Potential chemical cues to relatedness in cooperative riflemen 91 Introduction 92 Methods 94 Sample collection and processing 94 Statistical analysis of chemical data 95 Experimental design and analysis 96 Results 98 Chemical composition 98 Manipulation of nest odour 102 Discussion 103 6. Playback of calls containing kinship information in cooperative riflemen 107 Introduction 108 Methods 110 Recording calls 110 Call individuality 111 Call similarity and kinship 113 Playback experiment 114 Results 115 Individuality of calls 115 Call similarity and kinship 117 Playback experiment 118 Discussion 119 SYNTHESIS 125 7. Cooperative breeding in riflemen 127 Ecology and life history 128 Helper demography and relatedness 130 Kin discrimination 132 Active kin recognition 132 Potential mechanisms 133 Genetic or learned cues 134 Helper contributions 135 Fitness consequences of help 137 Indirect fitness benefits 137 Direct fitness benefits 140 Costs of help 141 Sex allocation 142 Conclusion 143 8. General discussion 145 Summary of results 146 Implications and future directions 148 Measuring parental investment 148 Development of evolutionary theory 149 Opportunities and challenges in avian sensory ecology 151 APPENDICES 155 A. Supplementary model results from study of rifleman sex allocation 157 B. Tables of data used for comparative analysis and meta-analysis 161 C. Eurasian blackbird nest parasitised by song thrush 166 REFERENCES 173 Acknowledgements This research would not have been possible without financial support from the Natural Environment Research Council and the University of Sheffield, or ethical approval from the University of Canterbury and New Zealand’s Department of Conservation. Thanks to all. Thanks to my supervisor Ben Hatchwell for offering me this opportunity, and for meetings about my work that were always productive, reassuring and interesting. Thanks also for the three months I was allowed to spend working on the sociable weaver project in South Africa, which was a much-appreciated break from working towards this thesis. It’s been a pleasure to work together over the last four years! To Jim Briskie, thanks for your help organising visas, ethical approval, field equipment and sample transport, all of which were essential to three successful seasons. On a personal note, just as appreciated were welcomes at the airport, coffee, Christmas dinners and birding outings around Canterbury. I hope I’ll return to N.Z. and find a rock wren with you soon! I was lucky enough to spend almost a year living in the beautiful town of Kaikoura to carry out research for this thesis, and it’s been sad to hear of the earthquake that afflicted it while I was back in England writing up. Best wishes to all those in Kaikoura who welcomed me during my stays, in particular Ngaire Perrin and Jack van Berkel at the University of Canterbury’s late Edward Percival Field Station, where I was provided a flat and laboratory space each season. Thanks for sorting out everything I needed and making me feel at home. A number of friends and colleagues are owed thanks for their contributions to fieldwork, especially Steph Preston who spent the first three weeks of my first season patiently showing me how to be a rifleman fieldworker and braving my jet-lagged driving. I’m grateful to Lorna Deppe, Justin Rasmussen and Archie Macfarlane for help during that first season, as well as David Thomas who also spent a day helping 7 me mist-net the following season, as did Mia Derhé. Thanks to Robyn White for help with ringing nestlings during my first two seasons and for follow-up fieldwork after I left, and to Laura Azzani who collected preen wax samples with me, and processed them, for which I’m very grateful. Robyn, Laura and Archie deserve special thanks for always making me welcome in Christchurch and at the university. I’ve benefited from being around a fantastic, evolving group of people, who number too many to name in full, over the years I’ve spent in Sheffield. Support from staff in the Molecular Ecology Laboratory was vital to the genotyping work I carried out. Thanks in particular to Rachel Tucker and Andy Krupa for constant support; Gav Horsburgh for training me; Caitriona McInerney for being incredibly helpful when I started to work in the lab; Maria-Elena Mannarelli for letting me follow her around while she extracted DNA, and Debs Dawson for help with multiplex design. To past and present members of our LHB Group, thanks for being such an insightful, supportive and amusing bunch. Jonathan Green and Issie Winney, who worked with me on chapters; Amy Leedale, who helped me with sound analysis, and Elspeth Kenny and John Jackson, who helped me to make nice plots, have all made visible contributions to this thesis. Joel Pick’s simulations course deserves special mention for improving my understanding of statistics and writing R code. But thanks also to the rest of you for all your helpful advice and interesting discussions. To everyone in the department not already covered, thanks for making it a brilliant place to work. Miscellaneous thanks: to the Audacity Team, Robert Lachlan who wrote Luscinia, and of course the R Development Core Team, for making their programs freely available; to anyone who posts and especially those who answer posts about R on Stack Exchange etc.; to two anonymous reviewers whose comments improved Chapter 2, and to James Savage, Steph Preston, Ben Jackson, Laura Azzani, Stuart Sharp, Ki-Baek Nam, Sarah Withers, Pip Gullett, René van Dijk and Mike Dickison, whose excellent PhD theses helped me work out how to get mine onto these pages. 8 Statement of intellectual contribution As well as the assistance mentioned above, the research chapters (2-6) presented in this thesis have benefited from collaboration with a number of colleagues. To reflect this, they are presented in the style of scientific papers, with these collaborators listed as coauthors. As well as supervision from Ben Hatchwell and (for fieldwork) James Briskie, contributions made by the coauthors are detailed here. Other work is my own. Chapter 2. I carried out the repeatability analysis with Isabel Winney, with whom I took the decision of what method to use for calculating R and implemented this method. Stephanie Preston provided provisioning data collected between 2008 and 2011, which were used in the turn-taking analysis. James Savage gave guidance on the turn-taking analysis and provided R code for implementing the runs test. All coauthors made comments that improved the manuscript. Chapter 3. Stephanie Preston provided sex allocation data from 2008-2011. Ben Hatchwell and James Briskie made comments that improved the manuscript. Chapter 4. I conceived this study with Jonathan Green, who suggested a multi- species comparison, and Ben Hatchwell, who suggested using helper sex ratio as the predictor in the comparative analysis. Robert Freckleton provided R code for the custom PGLS model, which I adapted to fit our data with Jonathan and Rob. All coauthors made comments that improved the manuscript. Chapter 5. Laura Azzani used gas chromatography to analyse all preen wax samples, and provided me with standardised per-compound proportions for each sample, which I used in analysis. Ben Hatchwell made comments that improved the manuscript. Chapter 6. Ben Hatchwell made comments that improved the manuscript. In addition, Appendix C reproduces a note written with David Lloyd-Jones, who recorded and transcribed footage, produced Figure C.1 and wrote parts of the text. 9 General summary In cooperatively breeding species, ‘helpers’ provide care for other individuals’ offspring. Research into cooperative breeding, which initially asked the deceptively simple question ‘why?’, has continued to provide insights in behavioural ecology thanks to the opportunities for adaptation and coevolution that are generated in these unusual societies. I explore some of these potential adaptations in detail, mainly through studying a population of riflemen Acanthisitta chloris, which are passerine birds endemic to New Zealand.
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