SEED PREDATION ALONG AN ELEVATIONAL GRADIENT IN THE TROPICAL ANDES, PERU By RACHEL HILLYER A Thesis Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY in Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE in the Department of Biology May 2009 Winston-Salem, North Carolina Approved By: Miles R. Silman, Ph.D., Advisor ____________________________________ Examining Committee: Kathleen A. Kron, Ph.D. ____________________________________ William K. Smith, Ph.D. ____________________________________ ii ACKNOWLEDGEMENTS From the start, I’d like to thank my advisor, Dr. Miles Silman, for his patience, thoughtful guidance, and constant enthusiasm throughout this entire process. I’d also like to thank the members of my committee, Dr. Kathleen Kron and Dr. William Smith for lending their time and perspective to this project. I’ve also benefited from the support and insight of the entire Silman lab: Dr. Ken Feeley, Julie Wyatt, Josh Rapp, William Farfan Rios, and Karina García Cabrera. I am also indebted to Mireya Natividad Raurau Quisiyupanqui both for the use of the seed rain data and for being my middleman in Peru. I owe a huge thank you to my field assistants in Peru: Jhoel Delgado Salazar, Guido Vilcahuaman Fernandez, Reyner Tairo Loayza, and Adam Ccahuana Quispe for their many hours of hard work. Funding for this research was provided by the Moore Foundation. I’d like to thank my mom, dad, and brother for the love and support that brought me here. Finally, to my fellow grad students who became my closest allies: Heather Fairfield, Jacquelyn Grace, Paige Roe, and Hugh Bender, thanks for the never ending support when things were difficult and all the laughter when things were fun. iii TABLE OF CONTENTS LIST OF TABLES……………………………………………………………………….v LIST OF FIGURES………………………………………………………………………vi ABSTRACT……………………………………………………………………………..vii INTRODUCTION………………………………………………………………………...1 Differential Seed Predation on Plant Species …………………………………….2 Biotic Interactions along Gradients…………….…………………………………3 Predicting Extinctions Due to Climate Change………………………………..….4 METHODS………………………………………………………………………………..5 Study Site………………………………………………………………………….5 Study Species……………………………………………………………………...5 Seed Predation Experiments………………………………………………………6 Ecosystem Productivity Data..…………………………………………………….7 Analysis……………………………………………………………………………8 RESULTS…..……………………………………………………………………………10 Seed Predation…………………………………………………………………...10 Predictors of Seed Predation…………………………………………………..…11 DISCUSSION………………………………..…………………………………………..11 Species Differences…………………….………………………………………...11 Species-Elevation Interactions…………………………………………………...13 Alternative Hypotheses for Seed Predation Patterns.……………………………15 The Importance of Gradients in Biotic Interactions……………………………..16 LITERATURE CITED…………………………………………………………………..18 iv FIGURE CAPTIONS……………………………………………………………………26 TABLES………………………………………………………………………….……...27 FIGURES………………………………………………………………………………...35 CURRICULUM VITAE…………………………………………………………………45 v LIST OF TABLES TABLES PAGE 1. Species used in seed predation experiments……………………………………..27 2. Elevation midpoints of species and genera……………………………………....28 3. Dates of installation and censuses of seed predation sites……………………….29 4. Cox proportional hazard model of seed survival………………………………...30 5. Generalized linear model of seed mortality vs. seed mass ……………………...31 6. Linear regressions of species seed mortality vs. elevation midpoints of genera...32 7. Linear regression of species seed mortality vs. elevation midpoints of species...33 8. Linear regression of measures of ecosystem productivity vs. elevation…………34 vi LIST OF FIGURES FIGURES PAGE 1. Experimental design………………………………………………………….35 2. Boxplot of species seed mortality …………………………………………...36 3. Seed mortality across the elevation gradient ………..……………………....37 4. Patterns of species seed mortality across elevation …………………...…….38 5. Seed mortality vs. seed mass………………………………………………...39 6. Seed mortality vs. elevation midpoint of genera…………………………….40 7. Seed mortality vs. elevation midpoint of species…………………………….41 8. Seed rain volume vs. elevation………………………………………………42 9. Woody biomass increment vs. elevation…………………...………………..43 10. Elevational ranges of rodents and carnivores in Manu National Park……….44 vii ABSTRACT The study of plant species response to climate change is primarily a study of plant distributions along environmental gradients, on which biotic interactions exert a large impact. Post-dispersal seed predation is a plant animal interaction that affects the population dynamics, community structure, and diversity of plant species through time and space. This thesis presents a comparative seed predation study of 24 species of tropical trees across a 2.5 km elevation gradient in the Peruvian Andes. The following questions were asked (1) does seed predation vary across the elevation gradient? (2) do predation rates vary among species and are those rates predictable from species traits such as seed size or current elevational range? And (3), what may be the underlying cause of variation in seed predation rates in terms of ecosystem productivity and associated animal communities? Species exhibited marked variation in total seed predation and in seed predation across the elevation gradient. For all species combined there was a significant decrease in seed predation at high elevations, resulting in an 5.6 increase in effective fecundity for trees at 3450 m. The overall trend in seed predation across elevation potentially arises due to seed predator regulation via top-down forces in the lowlands giving way to bottom-up (productivity) regulation at mid to high elevations. 1 INTRODUCTION The study of plant species responses to climate change is at its core a study of species distributions along environmental gradients. Most research in this area, both modeling (see Malcom et al. 2002; Thomas et al., 2004 for overviews) and empirical work (e.g. Ibañez et al., 2008) focus on changes in abiotic gradients. However, biotic interactions are central to plant distributional ecology, and changes in biotic interactions can have profound effects on species distributions (Weltzin et al., 1997; Leathwick and Austin, 2001; Webb and Peart, 2001). Indeed in a major empirical study of plant responses to climate change, a treatment intended to “control” for seed predators had effects on plant recruitment that equaled or exceeded climate treatments (Iabñez et al., 2008). How plant-animal interactions change across environmental gradients, even through central in setting plant distributions, is little studied. Post-dispersal seed predation is a quantitatively important plant-animal interaction that can control population dynamics in time and space (Janzen, 1971; Hulme, 1998; Silman et al., 2003). Seed predators affect plant populations through changes in population dynamics (Harper, 1977; Crawley, 2000), community structure (Howe and Brown, 1999), and species diversity (Hubbell 1980). In long-term studies of the population dynamics of tropical trees, Silman et al. (2003) and Wyatt and Silman (2004) found that population fluctuations in a major seed predator (white-lipped peccary) controlled recruitment of the two dominant tropical tree species (Astrocaryum murumuru and Iriartea deltoidea) in Western Amazonia. Rodents as seed predators have been shown to have considerable impact on plant populations (Price and Jenkins, 1986), and 2 this can occur in manifold ways, such as controlling the desert grassland transition (Brown and Heske, 1990), affecting the landscape level abundance of early successional species (Orrock et al., 2006), and reducing seed recruitment in tropical canopy trees (De Steven and Putz, 1984; Schupp, 1990). Seed addition experiments suggest that seed limitation is important in many different terrestrial habitats (Silman, 1996; Svenning and Wright, 2005; but see Hulme, 1998; Crawley, 2000) and when seeds have been protected from herbivores, all protected seeds have ultimately germinated (Wenny, 2000). Changes in seed predation have also been shown to interact with other species interactions to radically alter distance- and frequency-dependent recruitment in tropical trees, a central mechanism maintaining diversity in tropical forests (Janzen, 1970; Connell, 1978; Wright and Duber, 2001; Wyatt and Silman, 2004). Differential Seed Predation on Plant Species Differential seed predation on plant species is reported in many studies (e.g. Wilson and Whelan, 1990; Terborgh et al., 1993; Holl and Lulow, 1997; Blate et al., 1998; Notman and Gorchov, 2001; Xiao et al., 2006), and the relative effects on species can vary widely. In a study of grassland plants the seed predation of different species ranged from 20 to 95% though there was no difference in the percentage of times species were encountered by seed predators (Hulme, 1994). In the Chilean Andes seed removal ranged from 3 % to 78 % across nine species of herbs and shrubs (Muñoz and Cavieres, 2006). The effect of seed predation on the population dynamics of species can also vary. Seed predation significantly reduced seedling populations of two of five Papua New Guinean tree species (Cerbera floribunda K. Schum. and Microcos grandiflora Burret) 3 while the seedling populations of the other three species were only minimally affected (Jones et al., 2008). Multiple suggestions for species differences in predation risk have been proposed. Seed size can have multiple effects, from changing the suite of predators to which a species is exposed, to nutritional return