UNDERSTANDING AMPHIBIAN VULNERABILITY TO EXTINCTION: A PHYLOGENETIC AND SPATIAL APPROACH DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Graduate School of The Ohio State University By Sarah J. Corey, B.S. ***** The Ohio State University 2009 Approved by: Dissertation Committee: Dr. Amanda Rodewald, Advisor _______________________________ Dr. Kendra McSweeney Advisor Evolution, Ecology, & Organismal Dr. Andrea Wolfe Biology Dr. Darla Munroe ABSTRACT In the global extinction crisis currently underway, threats to biodiversity are not simply limited to species with particular risks in particular cases. Biodiversity will be increasingly affected by the wholesale decline of entire clades. In the face of this crisis, with amphibians ranking at the top of all vertebrates in the rate of extinctions, there is a great need for macroecological studies addressing three key areas of species declines. The processes that put species at great risk for extinction may be associated with 1) environmental factors, 2) spatially structured, or geographic effects, and 3) evolutionary predispositions to those processes (phylogenetic structure in vulnerability). I present a collection of work to address primarily the phylogenetic and geographic components of species vulnerability. First, I construct a theoretical foundation for using phylogenetic comparative methods for conservation assessments, emphasizing the importance of evolutionarily specific parameters and trees. I prescribe a greater conservation focus on understanding the severity of clade-level threats and potential data deficient species vulnerability, and identify evolutionary scenarios with the greatest return on resource investments. Second, I identify autocorrelated threats in the amphibian tree of life representing potential evolutionary predispositions to enigmatic rapid declines and Redlist threatened status in the superfamily Hyloidea. Third, I focus in on a family in ii Hyloidea, Hylidae, and use multiple phylogenetic comparative methods to identify phylogenetic signal in processes that selectively threaten lineages in the tree. I find phylogenetic signal (a predisposition to vulnerability) in pollution, habitat loss, species with multiple threatening processes, Redlist threatened status, and enigmatic rapid declines, concentrated in the clade Hylini. Among the comparative methods employed is a new application for conservation of a more flexible measure of phylogenetic signal accounting for selection using an Ornstein-Uhlenbeck model. Fourth, I use a landscape perspective to discover what spatial and environmental factors predict threats to amphibians in Venezuela. I find that traditional measures of human impact (population density and ecological footprint) effectively predict higher numbers of threatened amphibians, but indigenous peoples population density does not predict threats. Accounting for spatial dependence in the landscape reveals that cultural stewardship, i.e., parks on indigenous versus nonindigenous land, cannot predict threatened species distributions, failing to validate typical conservation concerns over indigenous population impacts to parks and biodiversity. Using a local spatial autocorrelation metric, I also find that the northwest region of Venezuela is a hotspot of geographic irreplaceability, for spatially autocorrelated threatened species, endemics and data deficient species. Overall, my collection of work addresses key themes in the amphibian extinction crisis using a macro-analytic approach: evolutionary predisposition to threats, anthropogenic threatening processes and spatial autocorrelation (or clumping) of threatened species. My work supports the emerging consensus that the extinction crisis is widespread, in terms of impact to phylogenetic diversity and geographic regions, but iii my findings also point to advantages for conservation policy and management gained by prioritizing vulnerable clades and geographic regions that stand to lose the most diversity and hold the greatest potential management payoffs. iv DEDICATION For my friend and mentor, Tom Waite, who continually inspires me. Y para Venezuela, tierra de mi madre, tierra de mi esposo, y manatial continuo de mis sueños. v ACKNOWLEDGEMENTS I want to extend my thanks to my advisor, Amanda Rodewald, for her guidance and advice, and for helping me keep my bearings along the way. I owe my gratitude to Kendra McSweeney, who went beyond her duties as a committee member, to being an advisor and mentor to me on all things related to conservation, academia, and professional work. Her refreshing point of view about people and conservation is a key inspiration to me. I also thank my committee members, Andrea Wolfe and Darla Munroe for sharing their diverse perspectives and providing me with support in writing and methods through this research. I also thank Emilia Martins for guidance with methods that were critical to my work. I thank my colleagues who have always offered help, advice, and good times: Katy Greenwald, Julie Mills, Jonathan Hall, Erin Greenley, Miles Spathelf, Jose Diaz, Ian Hamilton, Christine Anderson, and Kristen Mylecraine. I also wanted to thank researchers who have provided enriching research experiences for me: Lisle Gibbs, John Freudenstein, and David Culver. * * * I wish to thank Tom Waite, for inspiring me, advising me with this dissertation work, and for helping me find joy in my work. Thanks Tom. * * * I thank my husband, Jesús Rivas, who has been by my side with advice and encouragement this whole time. I thank him especially for coming to understand my work the best and for tirelessly editing manuscripts and discussing research. I give warm thanks to my family who have maintained a curiosity about my work, and have each given me much needed encouragement. vi VITA 2003 B.S. Zoology, The Ohio State University 2003-2004 Research Assistant, The Ohio State University 2004-2005 University Fellow, The Ohio State University 2005-2008 Graduate Teaching Associate, The Ohio State University 2006 Graduate Research Associate, The Ohio State University 2006-2009 Journal Reviewer, Science Magazine, Evolutionary Ecology, Journal of Herpetology 2008-2009 Presidential Fellow, Mary S. Muellhaupt Fellowship, The Ohio State University PUBLICATIONS T. A. Waite, S. J. Corey, L. G. Campbell, A. K. Chhangani, J. Rice, & Robbins, P. (2009). Satellite sleuthing: Does remotely sensed land-cover change signal ecological degradation in a protected area? Diversity and Distributions, 15, 299-309. Corey, S. J. & Waite, T. A. (2008). Phylogenetic autocorrelation of extinction threat in globally imperiled amphibians. Diversity and Distributions, 14, 614-629. Rivas, J. A. & Corey, S. J. (2008). Natural history note: Eunectes murinus (green anaconda). Longevity. Herpetological Review, 39, 469. Gibbs, H. L., Corey, S., Blouin-Demers, G., Prior, K., & Weatherhead, P. J. (2006). Hybridization between mtDNA-defined phylogeographic lineages of black ratsnakes (Pantherophis sp.). Molecular Ecology, 15, 3755-3767. FIELDS OF STUDY Major Field: Evolution, Ecology, & Organismal Biology vii TABLE OF CONTENTS Abstract ....................................................................................................................... ii Dedication.................................................................................................................... v Acknowledgements..................................................................................................... vi Vita .............................................................................................................................vii List of Tables ................................................................................................................xi List of Figures ..............................................................................................................xii Introduction: Applying phylogenetic and spatial methods in amphibian vulnerability assessments................................................................................................................. 1 Literature Cited ................................................................................................................... 5 Chapter 1. Using phylogenetic signal in vulnerability assesments ................................ 7 Summary............................................................................................................................. 7 Introduction ........................................................................................................................ 8 An incomplete picture of amphibian declines ........................................................................8 Conservation’s standard operating procedures......................................................................9 Phylogenetics as a tool for conservation ..............................................................................10 Part I. What does phylogeny mean for conservation? ........................................................ 11 Part II: The importance of quantifying phylogenetic signal................................................. 12 Common uses and challenges...............................................................................................12 Quantifying phylogenetic signal............................................................................................15 Further considerations: geographic location, scale, and phylogeography