VERTEBRATE COMMUNITY CHANGES ACROSS A 3200M AMAZON-TO- ANDES GRADIENT: COMPOSITION, STRUCTURE, AND OCCUPANCY BY DANIEL A. LOUGH A Thesis Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES in Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE Biology December, 2017 Winston Salem, North Carolina Approved By: Miles R. Silman, Ph.D., Advisor William E. Conner, Ph.D., Chair Todd M. Anderson, Ph.D. ii ACKNOWLEDGEMENTS From the start, I would like to thank my advisor, Dr. Miles Silman, for his insightful guidance and constant enthusiasm throughout this process. I’d also like to thank the members of my committee, Dr. William Conner and Dr. Michael Anderson, for lending their time and perspective to this project. I’ve also benefited from the guidance and support of the entire Silman Lab: William Farfan Rios, Cassie Freund, Rachel Hillyer, Jorge Cabellero Espejo, Max Messinger, and Jared Beaver. I am indebted to Dr. Russell Van Horn, Dr. Nicholas Pilfold, and Dr. Mathias Tobler at San Diego Zoo Global’s Institute for Conservation Research for their logistical and methodological support throughout this project. I owe a great deal of gratitude to Leydi Vanessa Aucacusi Choque, Ricardo Vivanco, and Fredy Martin Guizado for their assistance in the field and their many hours of hard work. I would like to thank my undergraduate researchers that assisted me in classifying the thousands of camera trap photos: Rebecca Wiebki, Kimiko Morris, Zachary Taylor, Kyla Mathon, Kristin Lanier, Nicholas Mouser, and Kiley Price. I would also like to thank SERNANP-Manu and the staff at Manu National park, for permitting this project. Funding for this research came through the North Carolina Academy of Science’s Bryden Grant, Wake Forest University’s Vecellio Grant, and the Paul K. and Elizabeth Cook Richter Memorial Fund. I am gracious to the researchers at the Amazon Conservation Association and the Andes Biodiversity and Ecosystem Research Group for their logistical support throughout this project. I would also like to thank my family and my fiancée for their constant love and support throughout this process. Finally, I would like to thank the faculty, staff, and graduate students of the Wake Forest Biology Department for their support throughout this degree. iii TABLE OF CONTENTS CHAPTER 1 MAMMAL AND BIRD DISTRIBUTIONS ALONG A 3200M ANDES-TO-AMAZON GRADIENT IN MANU NATIONAL PARK, PERU ABSTRACT……………………………………………………………………………....1 INTRODUCTION………………………………………………………………………...2 METHODS……………………………………………………………………………….4 Study Area………………………………………………………………………..4 Camera Deployment………………………………………………………………6 Elevational Range Data and Photographs…………………………………………7 Analysis……………………………………………………………………………9 RESULTS…………………………………………………………………………………9 Birds……………………………………………………………………………...9 Mammals…………………………………………………………………………17 DISCUSSION……………………………………………………………………………24 Birds……………………………………………………………………………...24 Mammals…………………………………………………………………………25 Conservation Implications……………………………………………………….31 iv LITERATURE CITED…………………………………………………………………..34 CHAPTER 2 SEED SURVIVAL AND GRANIVORE COMMUNITY CHANGES ALONG A 3.9KM TROPICAL ELEVATIONAL GRADIENT ABSTRACT……………………………………………………………………………...43 INTRODUCTION……………………………………………………………………….44 Vertebrate Functional Traits and Changes in Plant-Animal Interactions………..46 Camera Traps: Novel Approach to Documenting Seed Mortality….……………47 METHODS………………………………………………………………………………48 Study Area……………………………………………………………………….48 Study Species…………………………………………………………………….49 Camera Design and Seed Arrays………………………………………………...51 Analysis…………….……………………………………………………………55 RESULTS………………………………………………………………………………..57 Seed Predator Community and Diversity………….…………………………….57 Seed Survival…………………………………………………………………….59 Occupancy of Granivores………………………………………………………..69 DISCUSSION……………………………………………………………………………80 v Granivore Species Richness, Seed Survival and Occupancy across the Elevational Gradient……………………………………….……………..…………………...80 Seed Survival and Seed Defenses………..………………………………………81 Occupancy of Granivores and Seed Survival……………………………...…….83 Further Studies…………………………………………………………………...86 LITERATURE CITED…………………………………………………………………..89 APPENDIX 1…………………………………………………………………………...100 CURRICULUM VITAE………………………………………………………………..107 vi LIST OF FIGURES FIGURES Chapter 1 1. Map of camera stations in Manu National Park, Peru………………………….....5 2. Elevational distribution shifts of birds…………………………………………...13 3. Differences in avian species richness across elevational gradient……………….15 4. Differences in terrestrial-foraging avian species richness across the elevational gradient……………………………………………..……………………………16 5. Elevational distribution shifts of mammals……………………..……………….20 6. Differences in mammalian species richness across elevational gradient ……….23 7. Photograph of Andean white-eared opossum (Didelphis pernigra)….………….27 8. Photographs of mountain coatis (Nasuella sp.)………………………………….28 9. Differences in mammalian predator richness ………………………….……......30 10. Differences in mammalian seed disperser richness ……………………………..32 Chapter 2 1. Granivore species richness across the elevational gradient……………………...50 2. Camera station design..…………………………………………..........................52 3. Seed array design………………………………………………………………...54 4. Granivore detections……………………………………..………………………58 5. Granivore elevation distributions…………………………………..…………….60 6. Proportion of seeds removed over the elevational gradient……………………...61 7. Proportion of seeds removed per granivore taxa………………………………...63 vii 8. Seed survival over the elevational gradient…..……..….………………………..64 9. Time to removal of all three seed species per elevation…………………….......67 10. Detection probabilities of granivore taxa over the elevational gradient………...70 11. Detection probabilities of granivore guilds over elevational gradient…………..72 12. Detection probabilities of granivore guilds with slope………………………….77 13. Detection probabilities of granivore guilds with aspect…………………………78 14. Detection probabilities of granivore guilds with habitat…………………………79 15. Mammalian predator detection probabilities over the elevational gradient……...85 16. Proportion of all removed seeds by granivores………………………………….88 viii LIST OF TABLES TABLES Chapter 1 I. Bird species documented outside their previous range………………………11 II. Birds with range extensions broken into guilds……………………………...14 III. Mammal species documented outside previous range……………………….18 IV. Detected mammals and their guilds and body sizes…………………………21 Chapter 2 I. Covariates for Cox Proportional Hazard Model……...………………………65 II. Best Cox Proportional Hazard Models……...………..……………………...66 III. Granivore occupancy and detection probability…………………………….71 IV. Best occupancy models per granivore………………………………………73 V. Effects of individual covariates on occupancy of granivores……………….75 1 CHAPTER 1 MAMMAL AND BIRD DISTRIBUTIONS ALONG A 3200M ANDES-TO-AMAZON GRADIENT IN MANU NATIONAL PARK, PERU ABSTRACT Conservation planning depends heavily on understanding current species distributions. However, most Neotropical vertebrate distributions are poorly known and depend on field survey techniques which may not capture the full extent of an animals’ range. Here we present findings from two camera surveys in 2013 and 2016 conducted in and near Manu National Park, Peru. In 2013, 53 camera traps were installed between 3693 -1271 m a.s.l to identify both mammal and bird species along two parallel elevational transects composed of tropical montane cloud forest. In 2016, we replicated and extended the survey along one transect, setting 80 cameras from 3578 to 519 m a.s.l. We use these findings in conjunction with existing range hypotheses to assess (1) if there are major distribution changes (≥100 m, ~0.5 deg C) for mammal and bird species and whether there is a pattern among guilds and (2) quantify whether species richness across the elevational gradient changes as a result of new range estimates. Of the 83 taxa of identifiable birds, 18% had their distributions increased by ≥100 m with an average of two novel species per elevation. In contrast, of the 54 taxa of mammals detected, 44% had their distributions extended by ≥100 m, with most taxa acting as either predators or seed dispersers, with an average of six novel species per elevation sampled. These findings are crucial for expanding our understanding of tropical communities and what is needed to better conserve them. 2 INTRODUCTION Understanding current species distributions is crucial for biodiversity conservation and predicting community responses to anthropogenic climate change (Feeley and Silman, 2011). It has been well documented that temperate species will move latitudinally in response to dramatic variation in climate to find more suitable climates in which to survive (von Post 1916; Davis 1969). However, because of shallow temperature gradients at low latitudes, tropical species tend to move altitudinally, rather than latitudinally, to find more suitable climates in which to survive (Janzen 1969; Forero- Medina et al. 2006; Colwell et al. 2008; Lutz et al. 2013). Therefore, knowledge of the current elevational ranges of tropical species is vital to predicting future community shifts and creating adaptive conservation management plans (Ahumada et al. 2013; Fleming et al. 2014). Though understanding elevational distributions is central to conservation and basic understanding of ecosystem function, little is known about the current elevation and geographic ranges of many Neotropical animals, especially