LINKING MECHANISM TO PATTERN IN COMMUNITY ASSEMBLY: ANT-MEDIATED SEED DISPERSAL IN NEOTROPICAL PIONEER TREE SPECIES BY SELINA ARIEL RUZI DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology, Evolution, and Conservation Biology in the Graduate College of the University of Illinois at Urbana-Champaign, 2019 Urbana, Illinois Doctoral Committee: Professor Andrew V. Suarez, Chair and Director of Research Professor James W. Dalling Professor Adam S. Davis Professor Lawrence M. Hanks ABSTRACT Dispersal is a fundamental process that affects all aspects of an organism’s biology including its distribution, genetic structure, demography, and reproduction. Ant-mediated seed dispersal has evolved multiple times in many biogeographical locations. Most research in this area has focused on myrmecochorous plants that are known to elicit seed dispersal by providing a specialized lipid rich food reward called an elaiosome attached to their seeds. However, seeds that are not known to have this food reward may still be attractive to ants. The aim of my dissertation was to describe the movement of seeds of Neotropical pioneer tree species that are not known to have elaiosomes by ants. For my research, I chose Neotropical pioneer tree species that are commonly found in the soil seed bank of Barro Colorado Island (BCI), Panama. The seeds of these tree species do not provide an elaiosome food reward to their ant removers, but varied in mass, primary dispersal mode (animal or wind), dormancy type (physical, physiological, or quiescent), and ability to persist in the soil in the absence of predators. My dissertation research from BCI had four parts: (1) I quantified seed removal rates among 12 Neotropical pioneer species in two locations of the soil seed bank (soil surface and two cm within the topsoil) to determine which seed characteristics best explained variation in seed removal rates. (2) I identified seed-removing ants and determined whether variation in ant communities / activity correlated with differences in seed removal rates among sites. (3) I determined that chemical cues played a role in mediating some seed-ant interactions for one Neotropical pioneer seed species. (4) Lastly, I estimated where and how far ants moved seed of one pioneer species, Zanthoxylum ekmanii Urb. (Alain) (Rutaceae) and whether the seeds would survive their deposition location. My dissertation research supports that ants will interact with ii seeds of some Neotropical pioneer tree species without any type of food reward on Barro Colorado Island, Panama. This indicates that ants may alter the recruitment dynamics of more plant species than previously thought broadening the impact of this important ecosystem service. iii ACKNOWLEDGMENTS This work would not have been possible without the input of many people throughout my graduate career. I would like to thank my advisor, Andrew Suarez, for his advice, guidance, editing, and support through my research, teaching, and grant writing efforts. Additionally, I would like to thank to other members of my committee Jim Dalling, Adam Davis, and Larry Hanks for their insight and support, as well as for pushing me to grow as a researcher delving into topics such as tropical biology, statistics, and chemical ecology. Without this committee, this thesis would look very different and my PhD process would not have been as rewarding as it has been. Thank you to my labmates, both past and present: Rafael Achury, Andrea Belcher, Kim Drager, Joshua Gibson, Dietrich Gotzek, Jo-anne Holley, Fred Larabee, Michael Rivera, Adrian Smith, and Bill Wills, who have helped create a supportive laboratory culture, giving me advice and comments, and helping me with fieldwork, labwork, and statistical analysis. I have been fortunate to work with many amazing undergraduates including but not limited to: Paul Kang, Marlee Ryerson, Jelena Verkler, Adam Skrzekut, Katelyn Detweiler, Brandan Brew, and Ellen Andrews. I must specifically thank Francisco Juarez, whose help analyzing video interactions and preparing chemical extracts has been invaluable for data collected in my fourth chapter. Additionally, I must thank two wonderful Smithsonian Tropical Research Institute (STRI) – Butler University interns, Abigail Robson and Adam Beswick, who collected data during the wet season for three of my chapters when I was unable to be in Panama. Thank you to the Panamanian researchers and assistants who helped from setting up greenhouses, letting me know where trees were fruiting, and particularly to Ernesto Bonadias for help in the field. Thank you to all my wonderful co-authors, some of which fall under previously mentioned categories, iv but also include Daniel Roche and Camilo Zalamea, for not only their help in idea generation, fieldwork, and writing, but for their friendship. Additionally, I want to thank Bill Wcislo, Owen McMillan, Allen Herre, and Oscar Puebla for their help, guidance, and planning of my first semester visit in Panama and research help through additional field seasons. I thank all the logistical and support staff both at the University of Illinois and at STRI. Within the SIB Business Office, Norma Treakle, Penny Broga, Teresa Acosta, Jessica Katternhenry, James McGrawth, and Ted Hermann among others have provided valuable assistance in budgeting, purchasing various research supplies, and paying for flights and housing for research and conferences in the U.S. and other countries. I would also like to thank all the PEEC and SIB secretaries and support staff, especially Carol Hall, Kim Leigh, Lisa Smith Tara Heiser, and Liz Barnaby for all their help ranging from answering questions, scheduling logistics, and proofreading my dissertation. From STRI, I thank the visitor’s office, the permit’s office, the housing offices for both Gamboa and Barro Colorado Island (BCI), and BCI’s scientific coordinators. Specifically, Orelis Arosemena, Lil Camancho, Zurenayka Alain, Adrianna Bilgray, Taisha Parris, Hilda Castaneda, Norisa Soto, Oris Acevedo, Belkys Jimenez, and Melissa Cano have been invaluable to conducting research in Panama. I would also like to thank the chefs, maintenance crew, boat drivers, and cleaning personnel of Barro Colorado Island. I am indebted to the many friends I have made throughout this PhD process, from those based at my home institution at University of Illinois to those I met during my many field seasons at Barro Colorado Island, Panama, and to the field courses and conferences I have attended. They have not only acted as sounding boards for my research and edited my numerous grants and emails, but have reminded me to maintain a work-life balance. Here I include some of v these friends but know that there are many more that remain unnamed: Kelsey Witt Dillon, Amanda Owings, Carolina Sarmiento, Nicholas Sly, Harriet Downey, Nick Gardner, Alan Ward, Lourdes Hernández, Brian Harvey, Allison Gardner, Jennifer Jones, Halie Rando Robson, Beryl Jones, and Cassidy Martin. This research was made possible through a variety different funding sources coming from the National Science Foundation, STRI, the University of Illinois, and the STRI – Butler Internship. Within the University of Illinois, funding came from the Graduate College, School of Integrative Biology, a U.S. Department of Agriculture grant to Natural Resources and Environmental Sciences, and through the Program of Ecology, Evolution, and Conservation Biology. Additional funds came from the Association for Tropical Biology and Conservation to present work from this dissertation at conferences both within the United States and internationally. Lastly, I must thank my family. My mom, dad, and brother who may not always understand what I was doing during my time in Illinois and Panama, but they constantly encouraged me and supported me all the same. Finally, I thank my fiancée, Timothy Dinh, who has always supported me from afar, pushing me to grow and do more than I thought I was capable of while also reminding me that it is okay to place boundaries and say no. vi Para mi Abuela, Por inculcarme el amor por las plantas y animales vii TABLE OF CONTENTS CHAPTER 1: INTRODUCTION ....................................................................................................1 CHAPTER 2: TREE SPECIES IDENTITY INFLUENCES SECONDARY REMOVAL OF SEEDS OF NEOTROPICAL PIONEER TREE SPECIES .............................................................9 CHAPTER 3: CAN VARIATION IN SEED REMOVAL PATTERNS OF NEOTROPICAL PIONEER TREE SPECIES BE EXPLAINED BY LOCAL ANT COMMUNITY COMPOSITION? ..........................................................................................................................41 CHAPTER 4: PRELIMINARY IDENTIFICATION OF CHEMICAL CUES THAT MEDIATE SEED REMOVAL BY THE ANT ECTATOMMA RUIDUM ROGER IN A NEOTROPICAL PIONEER TREE SPECIES ..............................................................................78 CHAPTER 5: QUANTIFYING SEED FATE IN ANT-MEDIATED DISPERSAL: SEED DISPERSAL EFFECTIVENESS IN THE ECTATOMMA RUIDUM (FORMICIDAE) – ZANTHOXYLUM EKMANII (RUTACEAE) SYSTEM ..............................................................110 CHAPTER 6: CONCLUSIONS ..................................................................................................147 APPENDIX A: SUPPLEMENTARY TABLE FOR CHAPTER 2 .............................................152 APPENDIX B: SUPPLEMENTARY TABLES AND FIGURES FOR CHAPTER 3 ..............153 APPENDIX C: SUPPLEMENTARY TABLES AND FIGURES FOR CHAPTER 4 ..............163