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University of Florida Thesis Or Dissertation Formatting HIERARCHICAL PROCESSES STRUCTURING CROCODILE POPULATIONS IN CENTRAL AFRICA By MATTHEW HARTON SHIRLEY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2013 1 © 2013 Matthew Harton Shirley 2 In memory of John Thorbjarnarson 3 ACKNOWLEDGMENTS I would like to start by expressing my gratitude to my committee. Jim Austin was the ideal advisor for me because he allowed me to figure things out on my own, trusting that I would not get too lost along the way, while offering steadfast support when needed. John Thorbjarnarson was incredibly instrumental in the vision for and success of this work and his influence on my research and conservation philosophy cannot be understated. Perran Ross was providing opportunities to help me since before I even started my graduate career and that support has never flagged. Paul Reillo has been a constant example in my life for how to live conservation and I thank him for always taking an interest in me. I offer my sincerest gratitude to my other committee members, Charlie Baer and Susan Cameron Devitt, for their enthusiasm, willingness to share resources, and accessibility. Kent Vliet, while not on my committee, was always available as a mentor, friend, colleague and collaborator. I thank the governments of Senegal, Gambia, Cote-d’Ivoire, Ghana, Gabon, and the Democratic Republic of Congo (DRC) for granting me research and export permits. In Gabon I would especially like to recognize ANPN, including conservateurs Brice Meye, Joseph Okouyi, Sosthene Ndong Obiang, Solange Ngouessono, Jean Tondanoye, and CENAREST, particularly Daniel Franck Idiata and Flore Koumba. The Gabonese Division de la Faune et de la Chasse of MINEF was always gracious in providing my CITES export permits. Much logistic and in-kind support was provided by the Wildlife Conservation Society, WWF, Smithsonian, PPG, PROGRAM and the Lukuru Foundation. Special thanks are owed to Ruth Starkey, Malcolm Starkey, Alden Whittaker, Romain Calaque, Bas Huijbrechts, Bas Verhage, Lisa Korte, Marguerite Butler, Nicolas Bout, Koumba Kombila, Zacharie Chifundera, Ashley Vosper, and John 4 and Therese Hart. Victor Mpira was the best boatmen I ever had in Africa. I would also like to give special thanks to Fondation Liambissi and Philippe and Sylvie du Plessis for their logistic and financial support, but most of all their friendship. I thank Steve Rogers and the Carnegie Museum of Natural History, Max Nickerson, Kenny Krysko and the Florida Museum of Natural History, Patrick Campbell and the British Museum, Addison Wynn and the Smithsonian Institute, Allison Murray and the University of Alberta, Jon Woodward, Jose Rosado and the Harvard Museum of Comparative Zoology, David Kizirian, George Amato, Natalia Rossi and the American Museum of Natural History, as well as the Naturkunde Museum – Frankfurt, Seckenberg Museum of Natural History, Royal Belgian Institute for Natural Sciences, and the Royal Museum for Central Africa for providing skeletal specimens and pictures. I thank Jennifer Nestler for providing pictures from the latter European institutions. Loopy Lu Rabanal was kind enough to take photos at the British Museum. Ashley Pearcy helped clarify some of her analytical methods and offered advice. Vicki Villanova extracted tons of DNA greatly simplifying my workload. A very special mention goes to Mandie Carr who did a superb job illustrating the crocodile skulls and is, quite possibly, the best undergraduate research collaborator ever. Labwork was supported by a Doctoral Dissertation Improvement Grant from the National Science Foundation, the Riverbanks Zoo and Gardens Conservation Support Fund, and the Austin Lab. Fieldwork was supported by the USFWS Wildlife Without Borders program, Conservation, Food and Health Foundation, Columbus Zoo, Idea Wild Foundation, St. Augustine Alligator Farm, IUCN/SSC Crocodile Specialist Group, AZA Crocodilian Advisory Group, Minnesota Zoo, Fresno Chaffee Zoo, San Diego Zoological 5 Society, Mohamed bin Zayed Species Conservation Fund, Cleveland Metroparks Zoo, Oklahoma City Zoo, Aspinall Foundation, Wildlife Conservation Society, WWF, Rotary International, and Colin Stevenson. The Rare Species Conservatory Foundation was very gracious in serving as a zero-overhead funding fiduciary for these grants. I would like to thank the University of Florida and the Dept. of Wildlife Ecology & Conservation for providing fellowship, scholarship, assistantship, and travel grant support. Mitch Eaton provided many tissue samples and sequences, and was always available to talk about my work, crocodiles, conservation and Africa. John Brueggen, Kevin Torregrosa, and David Kledzik at the St. Augustine Alligator Farm helped train me to handle and sample crocodilians and I thank them for their continual support and friendship. Monica Lindberg, Caprice McRae, and Claire Williams were wonderfully tolerant in the management of my funds and my absurd travel schedule, and I thank them for always being happy to see me when I came back from the field. Many other friends and colleagues helped make this a success along the way. I’d like to thank the other members of the Austin Lab including Emily Saarinen, John Hargrove, Nate Johnson, Joe Townsend, and Aria Johnson. I thank Erin McClure, Laura Schreeg, Alex Moskalenko, Chris Brochu, John Groves, Peter Brazaitis, Michelle Davis, Lucy Keith, Mike Cherkiss, Frank Mazzotti, Kate Ingenloff, Christine Lippai, Ginger Clark, Richard Oslisly, David Sebag, Christine Lippai, Charlie Manolis, Tom Dacey, and Grahame Webb. Emilie Fairet m’a enseigné que tout est possible et j’ai hâte de réaliser nos rêves ensemble. Finally, I thank my parents – Jim and Barbara Shirley, my sister – Liz Shirley, and my aunt – Diane Keane, for always being supportive of my endeavors… even when that meant disappearing to Africa for months at a time to catch crocodiles! 6 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 9 LIST OF FIGURES ........................................................................................................ 10 ABSTRACT ................................................................................................................... 12 CHAPTER 1 CROSSING THE DIVIDE – POLYMORPHISM AND SPECIATION IN AFRICAN CROCODILES ........................................................................................................ 14 Hierarchical Processes in Ecology and Evolution ................................................... 14 Crocodiles of Central and West Africa .................................................................... 17 Slender-snouted Crocodile (Mecistops cataphractus) ...................................... 18 African Dwarf Crocodile (Osteolaemus tetraspis) ............................................. 19 Integrated Genetic Approach for Studying Central African Crocodiles ................... 20 2 TOTAL EVIDENCE APPROACH REVEALS TWO CRYPTIC SPECIES IN THE SLENDER-SNOUTED CROCODILE ...................................................................... 23 Introduction ............................................................................................................. 23 Methods .................................................................................................................. 26 Taxon and Molecular Character Sampling ....................................................... 26 Data Collection ................................................................................................. 28 Data Analysis ................................................................................................... 29 Results .................................................................................................................... 37 Distance and Population Aggregation Analysis ................................................ 37 Phylogenetic Analysis and Divergence Timing ................................................. 38 Morphological Analysis ..................................................................................... 40 Discussion .............................................................................................................. 40 3 COMPARATIVE SPATIAL STRUCTURE OF MECISTOPS SP. NOV. AND OSTEOLAEMUS TETRASPIS REVEALED BY MITOCHONDRIAL AND NUCLEAR MARKERS ............................................................................................ 66 Introduction ............................................................................................................. 66 Methods .................................................................................................................. 68 Taxon and Character Sampling ........................................................................ 68 Data Analysis ................................................................................................... 70 Results .................................................................................................................... 79 Mitochondrial Sequences and Phylogeographic Analyses ............................... 79 Microsatellite Genotypes and Spatial Clustering Analysis ................................ 83 7 Discussion .............................................................................................................
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