FUNCTIONAL TRAIT MEDIATION OF PLANT-ANIMAL INTERACTIONS: EFFECTS OF DEFAUNATION ON PLANT FUNCTIONAL DIVERSITY IN A NEOTROPICAL FOREST A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGY AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Erin Leigh Kurten August 2010 © 2010 by Erin Leigh Kurten. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/bb408gp7470 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Rodolfo Dirzo, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Peter Vitousek I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. David Ackerly Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Preface Dissertation Abstract This dissertation examines how terrestrial vertebrates, as seed dispersers, seed predators and herbivores, influence plant functional trait composition in tropical forests and thereby diversity. I conducted this work in the Barro Colorado National Monument (BCNM) in Central Panama, where a long term mammal exclosure experiment has been ongoing, and in neighboring Parque Nacional Soberanía (PNS), which together with the BCNM forms a defaunation gradient driven by hunting. I first comprehensively review what is known about how the loss of vertebrates in tropical forests alters plant-animal interactions, plant demography, and plant diversity. Defaunation consistently lowers primary dispersal and creates a seed shadow that is more dense around the parent tree and less dense at sites farther away. However, it also often lowers seed predation by rodents, and as a consequence, species with rodents as seed predators and dispersers often benefit from defaunation. While demographic and diversity responses tend to be more mixed, a few consistent trends emerge. Community dominance tends to increase in response to defaunation. Often, plants with particular functional traits or abiotic or unhunted dispersal agents are favored by defaunation. I next examined how community-level functional trait composition shifts in seedling communities (Chapter 2) and sapling communities (Chapter 3) which have experienced exclosure from terrestrial mammals. Seedling communities in exclosures had higher median seed mass than paired plots open to the mammal community, but treatments did not differ in their leaf traits (leaf mass per area and laminar toughness) or wood density. In contrast to the seedling community, the sapling community did show significant shifts toward higher specific leaf area and lower leaf toughness in response to herbivore exclosure, primarily due to an increased dominance of species with those traits, and secondarily due to differences in the iv species present in each treatment type. These data, combined with data from PNS, also suggest that hunting results in community mean wood density in seedling communities, due to a disproportionate number of high wood density species relying on hunted animals for their seed dispersal. Finally, I investigated the seed size response to changes in mammal abundance by measuring vertebrate seed predation rates in a protected and hunted forest (Chapter 4). I found that in central Panama, seed mass does not correlate well with either body size of the seed predator, or vertebrate seed predation rates. I suggest that rather than formulate seed predation rates as a linear function of seed predator abundance, these interactions may be better modeled as threshold-dependent processes. This work suggests that terrestrial vertebrates play an underappreciated role in maintaining plant diversity and that pan-tropical levels of unsustainable hunting may indirectly lead to losses of plant biodiversity. v Acknowledgments My deep gratitude goes to my two advisors, Rodolfo Dirzo and David Ackerly, for giving me the flexibility and support to pursue this work. Rodolfo’s generosity as a teacher and advisor, and his tireless contributions to teaching, research and conservation, both at Stanford and internationally, are a great inspiration to me. I am thankful to David for graciously and supportively allowing me to build a network of intellectual support that allowed me to successfully complete this journey. He has also been an excellent intellectual role model for me, challenging me to grapple with complexity and nuance and to confront problems from new perspectives. Joe Wright has been a generous and supportive mentor and collaborator throughout my time at the Smithsonian Tropical Research Institute, and some of this work would not have been possible without his contributions. Peter Vitousek contributed many insightful suggestions throughout the course of this work as a committee member, and his service activities, from facilitating collaboration among scientists in Hawaii, to the First Nations’ Futures Program, have also inspired me. I also thank Fio Micheli for her enthusiasm as a committee member and for helping me frame my work in a broader context. Walter Carson very generously permitted me to work on the long-term mammal exclosure experiment he established in the Barro Colorado National Monument in Panama and shared with me his long-term datasets. The communities at Stanford, Berkeley and STRI were essential in shaping my graduate school experience. At Stanford, Will Cornwell, Nathan Kraft, Virginia Maztek, Steve Allison, Stephen Porder, Katie Amatangelo, Jen Funk, Camila Donatti, and Mauro Galetti provided helpful feedback and support throughout the various stages of my work. Doug Turner was an essential help in analyzing leaf nutrients, both for chapter three, and work not included in this thesis. Alex Royo, Allen Herre, Scott Magnan, Liza Comita, Mike Tobin, vi Patrick Jansen, Noelle Beckman, Roland Kays, Jackie Willis, Stephan Schnitzer generously shared their advice and knowledge of the field site with me, improving the feasibility and execution of this work. Many thanks go to the botanists at BCI. Without their assistance, this work would not have been possible. Andrés Hernández, Oldemar Valdes, David Brassfield, and Osvaldo Calderón were always happy to help me identify whatever leaf, fruit, seed, or flower I brought to their office. Andrés and Oldemar in particular taught me most of what I know about the BCI flora. Many paid and volunteer field and lab assistants helped to make this work possible. Lissie Jiménez helped immensely with the collection and processing of the thousands of leaves collected for Chapter three. Ana Patricia Calderón and Rousmery Bethancourt contributed many early mornings conducting mammal transect surveys. Clare Sherman was such a dedicated help in the lab and fieldwork for chapter 4, that I sometimes had to remind her to take a break and have some fun. Susan Rebellon helped with the pilot studies for chapter four, and also with leaf sample processing at Stanford. Gaspar Bruner, Karen Kapheim, Adam Roddy, and David Bethancourt, helped me recover (most of) my leaf samples after they were destroyed in a freezer accident. I would also like to thank staff at Stanford and STRI who helped make the logistical aspects of this work easier. The competence of Pam Hung, Oris Acevedo, Belkys Jiménez, Orelis Arosemana, and Marcela Paz made them a pleasure to work with. The Falconer library and copy staff, as well as Allen Smith, did their best to get me the literature I needed, despite STRI’s rigorous firewall. Valerie Kiszka and Jennifer Mason helped with countless administrative tasks and advice during my time as a student at Stanford. vii Contents Preface iv Acknowledgements vi List of tables ix List of figures x Introduction………………………………………………………………………... 1 1 Contemporaneous defaunation and cascading effects on tropical forests…...… 3 Introduction…………………………………………………………………. 3 Scope of Review……………………………………………………………. 4 Methodology………………………………………………………………... 5 Plant-animal interactions………………………………………………….... 7 Seed dispersal……………………………………………………….... 7 Seed Predation………………………………………………………… 14 Herbivory & Trampling…………………………………………….… 17 Plant Demography……………………………………………………….…. 17 Recruitment…………………………………………………………… 17 Seedling survival……………………………………………………… 19 Standing abundance……………………………………………….….. 20 Linking Dispersal and Seedling Recruitment………………………… 22 Community Diversity….…………………………………………………… 24 Seedling density………………………………………………………. 24 Diversity……………………………………………………………… 24 Plant Functional Groups……………………………………………… 25 What is defaunation? ………………………………………………………. 27 Heterogeneity Among Studies……………………………………………… 28 Conclusions……………………………………………………………….… 29 Appendix 1.1……………………………………………………………..… 30 2 Reduced seed dispersal as a consequence of hunting lowers community-level wood density in a Neotropical