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Ecological Studies on Seed Dispersal Networks: Insights from a Diverse Tropical Ecosystem a Dissertation Submitted to the Depart ECOLOGICAL STUDIES ON SEED DISPERSAL NETWORKS: INSIGHTS FROM A DIVERSE TROPICAL ECOSYSTEM 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 Camila Iotte Donatti December 2011 © 2011 by Camila Iotte Donatti. 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/jz498cr4469 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. Carol Boggs 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. Fiorenza Micheli 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 ABSTRACT Mutualisms between animals and plants, such as pollination, seed dispersal and ant-plant protection, are key ecological processes in many ecosystems throughout the world. Like any other ecological interaction, plant-animal mutualisms occur in a community context. Therefore, one-to-one interactions are very rare in nature and the majority of species, both animals and plants, have more than one partner. Recently, studies on mutualistic interactions at the community level have used the “network approach” in order to simplify complex interactions and to determine both the pattern of interaction and the properties of species in networks. In this dissertation, I use network theory combined with long-term field work, phylogenetic and multivariate analysis, species extinctions simulations and experimental manipulation to identify the pattern of interaction in a seed dispersal network, to assess the contribution of particular animal species to network stability and robustness, and to address the extent to which seed dispersal interactions can structure plant communities. To do so, I studied a hyper-diverse seed dispersal network sampled in the Brazilian Pantanal, which includes interactions among plant species from 28 families and seed dispersers, both native and exotic species, from 25 families and 4 taxonomic groups. In the first chapter I examine the pattern of interaction in this hyper-diverse seed dispersal network and show that this network has a heterogeneous structure, which is organized around a modular pattern. That is, subsets of species (modules) more frequently interact with each other than with species in other modules. I show that plant and animal trait values are associated with specific modules but phylogenetic signal is limited. I conclude that the observed modularity emerges by a combination of phylogenetic history and trait convergence of phylogenetically unrelated species, shaped by interactions with particular types of dispersal agents. Additionally, my results from this chapter highlight the fact that the absence of large and medium-bodied species may affect the pattern of interaction and, as a consequence, the functioning of this seed dispersal network. In the second chapter I use species extinction simulations to explore how the extinction of large- and medium-bodied species may affect the pattern of interaction in this network and seed dispersal services as a whole. My results show that the removal of large- and medium-bodied species has a large impact on the network pattern and robustness. Although exotic mammalian species usually have negative impacts on native taxa, my results surprisingly show that the exotic feral pig (Sus scrofa) actually plays a critical role in maintaining structural network metrics and in providing seed dispersal services in this community. In the third chapter, I continue to explore the importance of large-bodied species in providing seed dispersal services in the Pantanal plant-animal community. It is well known that defaunation, the contemporary pulse of animal population loss or decline driven by human activities, can compromise the dispersal of large-seeded plants. This is the case because the especially vulnerable large-bodied seed dispersers are extremely important in ingesting and dispersing large-seeded plant species. However, the results from this chapter emphasize the fact that large-bodied animals are also important because v they disperse such species in high frequencies, and also have the ability to disperse large conspecific seeds, which in turn show high germination rates. The three first chapters of my dissertation focus primarily on the seed dispersal process per se. However, in chapters 4 and 5 I expand my study to a broader view and address the importance of seed dispersal in determining the structure of plant communities. In chapter 4, I describe the properties of species in this network and, in chapter 5, I use one of these species properties, the “maximum dependence”, to address this association, taking into account the complexities related to the effect of multiple seed dispersers on the spatial distribution of animal-dispersed plants. I found that seed dispersal was the main important predictor of the aggregation intensity of individual plants, in comparison with several other biotic and abiotic variables. Therefore, I conclude that, although different variables, such as seed size and edaphic characteristics, can operate at different scales in shaping the distribution and structure of plant communities, seed dispersal appears to be the most important in that respect, even when considering the effects of multiple animal species in dispersing plant species. This study contributes novel information on seed dispersal at the community level, especially because I examined a diverse and relatively complete seed dispersal network, which may provide insights for other diverse systems, especially in the tropics. Besides generating information on the ecology and evolution of plant-animal interactions, this study also shows that not all seed disperser species are equal at the community level; and body size of dispersers seem to be a useful proxy of relative importance for dispersal services. Since contemporary defaunation differentially affects species depending on body size, this work illustrates how human activities, such as hunting, land use and climate change, affect not only taxa, but also crucial processes in which animals of different body size play different roles. This study emphasizes that conservation science needs to look at the conservation of ecological processes driven by species interactions. vi ACKNOWLEDGMENTS I could not have completed this work without the help and generosity of several people: My advisor Dr. Rodolfo Dirzo, who has been an incredible source of support and inspiration since the very first day that I arrived at the lab. Dear Rodolfo, you have made me a better person and professional and I will be forever indebted to you. Thank you so much for everything! My committee Dr. Carol Boggs, Dr. Fiorenza Micheli, Dr. Tadashi Fukami and Dr. Lisa Curran My collaborators Dr. Mauro Galetti, Dr. Paulo Guimarães Jr, Dr. Marco Aurélio Pizo, Dr. Alexine Keuroghlian, Ellen Wang, Flávia M. D. Marquitti, Marina Schweizer and Lucas Leuzinger My friends from the Dirzo Lab Rachel Adams, Eben Broadbent, Posy Busby, Oskar Burger, Yolanda Cachu Pavón, Mauro Galetti, Dennis Hansen, Erin Kuerten, Eduardo Mendoza, Doug McCauley, Katherine Mertes, Beth Pringle, Chelsea Wood and Hillary Young My friends from the Palumbi Lab Dr. Steve Palumbi, who generously offered me a space in his lab, Dan Barshis, Pierre De Wit, Alison Haupt, Hannah Jaris, Jason Ladner, Tom Oliver, Marina Oster, Melissa Pespeni, Carolyn Tepolt and Nina Therkildsen Friends from my cohort Aaron Carlisle, Posy Busby, Henri Folse, Nishad Jayasundara, Jason Ladner, Kevin Miklasz, Malin Pinsky, Beth Pringle, Julie Stewart and Shelby Sturgis Stanford University staff Pamela Hung, Monica Bernal, Dan King, Valeria Kiszka, Jennifer Mason and Matt Pinheiro Funding Stanford University Conservation International Zaffaroni Fellowship Fund The State of São Paulo Research Foundation (FAPESP) My family Caroline, Gustavo, Alice, Rodrigo, João, Karin, Jennifer, Julia and Tom My parents Maria José e José Airton And my husband Jason vii TABLE OF CONTENTS LIST OF FIGURES .....................................................................................................XIII LIST OF TABLES ..................................................................................................... XIIII INTRODUCTION............................................................................................................. 1 STATEMENT ON MULTIPLE AUTHORSHIP .......................................................... 6 REFERENCES.................................................................................................................. 7 CHAPTER 1. ANALYSIS OF A HYPER-DIVERSE SEED
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