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FORAGING BEHAVIOR, BEHAVIORAL FLEXIBILITY, AND RANGE SIZE OF AUSTRALIAN HONEYEATERS (MELIPHAGIDAE) by SARAH KATHERINE WAGNER B.A., Earlham College, 2002 M.A., University of Colorado, 2010 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2015 This thesis entitled: Foraging behavior, behavioral flexibility, and range size of Australian Honeyeaters (Meliphagidae) written by Sarah Katherine Wagner has been approved for the Department of Ecology and Evolutionary Biology Alexander Cruz (chair) Kendi Davies (member) 14 July, 2015 The final copy of this thesis has been examined by the signatories, and we Find that both the content and the form meet acceptable presentation standards Of scholarly work in the above mentioned discipline. iii Wagner, Sarah Katherine (Ph.D., Department of Ecology and Evolutionary Biology) Foraging behavior, behavioral flexibility, and range size of Australian Honeyeaters (Meliphagidae) Dissertation directed by Professor Alexander Cruz Anthropogenic disturbance is the leading cause of species extinctions (Vitousek 1997, Pimm and Raven 2000, Ewers and Didham 2006). Modern ecologists are given the task of determining how to predict and then mitigate species’ response to such disturbances. Species with larger niches, and more behaviorally flexible species, are predicted to better succeed in novel environments in the face of large scale habitat changes (Mayr 1965, Ehlrich 1989, Sol 2002, Shultz 2005). Foraging behavior can be a good descriptor of species’ niches, and the variation in these measures can be used to quantify behavioral flexibility (Sol 2002). My dissertation utilizes the interface between animal behavior data and broad-scale ecological patterns. I collected foraging behavior data (~7,300 independent foraging observations) across 74 of 75 Australian honeyeater (Meliphagidae) species to quantify niche size and position. I used functional dispersion (FDis) to quantify niche size. Related species foraged similarly, and foraging behavior showed significant phylogenetic signal. Generalists utilized a variety of resource acquisition strategies, whereas species with small niches were either highly nectarivorous or insectivorous. In order to determine if foraging niche size can be a predictor of extinction risk, I tested whether niche size was correlated with exposure or sensitivity to climate change. I did not find niche size to be a significant predictor of these risks as assessed by others. However, synergistic effects between small niche size and anthropogenic disturbance and climate change may put these species at an elevated risk of extinction. I also found a strong iv positive relationship between species that are highly nectarivorous and species that make attacks to the air for invertebrates. Nectarivorous species supplement their diets with protein, and it appears that these species make costly aerial attacks to acquire protein quickly. Geographic range size was not correlated with foraging niche size, but it was weakly correlated with niche position. Specifically, species that glean and hang from leaves in forests with high canopies were found to have smaller geographic range sizes. This is likely driven by the fact that such forests occur over a limited area in Australia, and occupy only remnants of their former geographic extent. v ACKNOWLEDGEMENTS The completion of this dissertation was very much dependent on the support and help from numerous people. I first want to thank my husband, collaborator and adventure partner, Eliot Miller for his love, support, patience, and enthusiasm. I also want to thank my parents, Pat and Lowell Wagner, for encouraging me to be a bird loving conservation scientist even if it meant spending so many years in school. I am grateful for a shared love of science, natural history and humor with my siblings and their partners, Becky Wagner and Jed Bopp and Jon Wagner and Prairie Hale. I am not sure where I would be without the free counseling and editing, and reminders to keep getting my hands dirty in the garden. I thank my advisor, Alex Cruz for believing in me, giving me the freedom to study a family of birds all the way in Australia, sharing his excitement about avian biogeography and conservation and being an incredibly inspiring educator and mentor. I thank my committee: Sharon Collinge, Kendi Davies, Dan Doak, and Rob Guralnick for the countless ideas, analyses help, editing suggestions and the many hours spent brain storming. The Cruz lab family (Marcus Cohen, Clint Francis, Nathan Kleist, Catherine Ortega, Ty Tuff) have been a comforting examples of how to navigate academia and lots of fun on whitewater rafting and field work adventures. Kelly Ramirez has been a dear friend since day one of my graduate career at CU and is responsible for many of my more stream-lined and well thought out ideas. I am forever indebted to Bill Buskirk, my Ornithology professor at Earlham College, who first opened my eyes to the world of birds and thereafter provided multiple opportunities to further pursue my ornithology interests (he also does one stellar American woodcock display impersonation). My Aunt Janet and Uncle Skip bought me my first Ornithology text book and continued to support other Ornithology May terms and excursions, and I am very grateful for that. I taught during every semester that I was a vi student at CU and I am grateful for the teaching mentorship and guidance from John Basey, Mike Breed and the wonderful people at the Biological Sciences Initiative at CU. Our work in Australia would have been impossible without support for Mark Westoby at Macquarie University and Leo Joseph at the Australian National University. I am also incredibly grateful to Glen Sanders and Hillary Cherry for being our very comfortable and fun loving Sydney home base. I thank our new community of friends in Moscow, Idaho where I finished up the last leg of my PhD with the help of: Denim Jochimsen, Rafael Maia, Amy Worthington, Andy Kraemer, and Anahi Espinola. vii CONTENTS CHAPTER I. INTRODUCTION Foraging behavior, behavioral flexibility, and range size of Australian honeyeaters (Meliphagidae)………………………………………….…………………………………1 Summary of chapters two through four………………………………………………...…2 II. A QUANTITATIVE SUMMARY OF THE FORAGING BEHAVIOR OF A CONTINENTAL RADIATION: AUSTRALIAN MELIPHAGIDAE…………………………………………………………..…………….4 Abstract………………………………...………………………………………………….4 Introduction…………………………………………………...…………………………...4 Methods……………………………………………...…………………………………...10 Results……………………...…………………………………………………………….15 Discussion…………………………...…………………………………………………...62 III. DOES FORAGING NICHE PREDICT EXTINCTION RISK IN THE AUSTRALIAN MELIPHAGIDAE?............................................................................................................68 Abstract…………………………………………………………………………………..68 Introduction…,,,………………………………………………………………………….68 Methods…………………………………………………………………………………..71 Results……………………………………………………………………………………77 Discussion……………………………………………………………………………......82 viii IV. NICHE SIZE AND THEREFORE BEHAVIORAL FLEXIBILITY ARE ASSOCIATED WITH LARGE GEOGRAPHIC RANGES…………………………….........................87 Abstract…………………………………………………………………………………..87 Introduction………………………………………………………………………………87 Methods………………………………………………………………………………......90 Results……………………………………………………………………………………92 Discussion……………………………………………………………………………......99 V. CONCLUSION…………………………………………………………………………104 BIBLIOGRAPHY…………….………………………………………………………………...107 ix TABLES 2.1 Map of foraging behavior data collection sites……………………………...……………….59 2.2 Bar graph of foraging niche size (FDis) scores per species in order of largest to smallest….64 3.1 Common name, species name, IUCN threat status, IUCN population trends and exposure and sensitivity to climate change……………………………………………………………………..79 3.2 ANOVA results for FDis and sensitivity, exposure and IUCN trend, PC1 with sensitivity, exposure, and IUCN trend, and PC2 with sensitivity, exposure, and IUCN population trend….80 x FIGURES 2.1 Hawking (percent of attacks to the air that are not to flowers) and proportion of attacks to flowers (nectarivory) were positively correlated………………………………………………...11 2.2 Bar graph of foraging niche sizes (FDis) scores per species in order of largest to smallest..17 2.3 Plot of foraging niche size (FDis) by species across the phylogeny………………………………………………………………………………………...19 2.4 Plot of nectarivory by species across the phylogeny………………………………………..22 2.5 Plot of proportion of attacks to fruit (frugivory) by species across the phylogeny…………30 2.6 Plot of proportion of attacks to branches by species across the phylogeny…………………36 2.7. Foraging niche size (FDis) and proportion of attacks to flowers (nectarivory) produced a unimodal response which highlights the fact that specialization and small sample size are related ……………………………………………………………………………………………………55 2.8 Hawking (percent of attacks to the air that are not to flowers) and proportion of attacks to flowers (nectarivory) were positively correlated………………………………………………...56 2.9 Meliphagidae phylogeny with position along PC1 mapped in color………………………...58 2.10 Meliphagidae phylogeny with position along PC2 mapped in color……………………….60 3.1 Foraging niche size and IUCN population trend…………………………………………….79 3.2 Niche position on PC2 and IUCN population trends………………………………………...80 4.1 Geographic range sizes per species (occurrence in a 100 x 100 grid cell)…………………..93
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