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University of Florida Thesis Or Dissertation Formatting TRACE METAL CONCENTRATIONS AND THE PHYSIOLOGICAL ROLE OF ZINC IN THE WEST INDIAN MANATEE (Trichechus manatus) By NOEL YOKO TAKEUCHI 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 2012 1 © 2012 Noel Yoko Takeuchi 2 To my parents, for without them, I would not be where I am today. As first generation Japanese immigrants, they continue to inspire me to live the “American Dream”. 3 ACKNOWLEDGMENTS I want to first, and foremost, thank my amazing advisor, Dr. David Barber, for his dedication to his students, his great insight to science, life and family, and for being encouraging when times were tough. I want to also give a huge thank you to my committee members: Drs. Roger Reep, Robert Bonde, Robert Cousins and Michael Walsh. This could not have been accomplished without their support, advice and expertise. The greatest part of science is working together to answer a common question. As a result, I have a number of collaborators and organizations to thank for being a part of this project. The magnificent United States Geological Survey (Sirenia Project), Florida Fish and Wildlife Commission (Dr. Charles Deutsch), Nicole Auil Gomez and Dr. James Powell (Sea to Shore Alliance), Dr. Ramiro Isaza, Carla Bernal, Natalie Hall (UF) and Dr. Ellen Wiedner (Ringling Brothers) for elephant samples, the Marine Mammal Pathobiology Laboratory (Dr. Martine deWit and staff), Mote Marine Laboratory and Aquarium (Joseph Gaspard), Dr. Dean Bass (Doctor’s Data, Inc.), Dr. Iske Larkin (UF) and Joyce Kleen (Crystal River National Wildlife Refuge) for plant surveys, Dr. Jim Wellehan and Heather Maness for their help with phylogenetic analysis, Drs. David Silverman and Chingkuang Tu for their patience and expertise in carbonic anhydrase kinetics (UF Biochemistry), Joseph Aufmuth, Anthony Lau and Dr. Dan Slone (USGS) for their help with GIS, Melanie Pate (UF), Terry Merano (UF), Sharon Norton and Carolyn Diaz (UF ICBR) for their assistance in protein analysis, Dr. Raymond Bergeron and Elizabeth Nelson (UF Pharmacy) for their years of patience and assistance with the ICP-MS, and Dr. Dean Bass (Doctor’s Data, Inc). Thank you to the University of Florida’s Aquatic Animal Health Program’s graduate and undergraduate students for 4 helping collect samples and to Sally O’Connell and Dr. Charles Courtney for their assistance and support. I would also like to acknowledge the Physiological Sciences department in the College of Veterinary Medicine, both faculty and students, for their support. I also want to thank everyone at the CEHT, especially those in the Barber Lab (Nicholas Doperalski, April Feswick, Erica Anderson, Ley Cody Smith), for sharing their knowledge with me and for all their support throughout the years. A special thank you to Drs. Thomas O’Shea and Francis Gulland, who continue to inspire me through their passion, and collaborative attitude in the field of marine mammal science. I want to thank my friends across the country for listening to my struggles in graduate school, coming to visit, all the late night phone conversations, and the continuous laughter. Thank you to Kai, Sheri and Pingel for putting up with me and willing to share common grounds and Jayson for his patience, support and love. Lastly, thank you to my family for all their support and understanding throughout my years in graduate school. My family has guided me and helped shape the person who I am today. They believed in me when I didn’t even believe in myself and were always there for me through thick and thin. Last, I want to thank my various funding sources: The University of Florida’s College of Veterinary Medicine Team Building Grant, the University of Florida’s Aquatic Animal Health Program, the American Museum of Natural History’s Lerner Gray Fund for Marine Research, and the Graduate Student Council Travel Grants. I also want to thank the National Science Foundation (NSF) and the Australian Academy of Sciences for providing me a great opportunity to begin a career as an international researcher in Australia through the NSF East Asia and Pacific Summer Institute Program in 2009. 5 This research was approved by the University of Florida’s (UF) Institutional Animal Care and Use Committee (IACUC) under study #201105936 and #201101961 and the United States Fish and Wildlife Service (FWS) Federal Research #MA791721-4. Additional permission was obtained from Homosassa Springs Wildlife State Park and Mote Marine Laboratory. A saltwater fishing license (State of Florida Recreational License #395975378) from FWC allowed for a maximum of five gallons of saltwater seagrass and a permit from the Department of Agriculture was approved for freshwater plants (Florida Department of Agriculture and Consumer Services, Certificate of Nursery Registration #48006548). Samples were taken opportunistically from animals and in conjunction with health assessments and were not taken solely for the purpose of this project. 6 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES .......................................................................................................... 12 LIST OF FIGURES ........................................................................................................ 14 LIST OF ABBREVIATIONS ........................................................................................... 16 ABSTRACT ................................................................................................................... 17 CHAPTER 1 INTRODUCTION .................................................................................................... 21 Overview of Metals in Marine Mammals in Relation to Sirenians ........................... 22 Past Studies of Metal Accumulation in Dugongs .............................................. 24 Past Study of Metal Accumulation in Manatees ............................................... 25 Factors Affecting Metal Accumulation .............................................................. 26 Sampling Methods in Marine Mammals ........................................................... 27 Metals in Whole Blood of Marine Mammals ..................................................... 28 Metal Toxicity and the Importance of Baseline Levels ............................................ 29 Metal Detoxification Mechanisms in Marine Mammals ........................................... 32 Mercury and Selenium ..................................................................................... 32 Metallothioneins ............................................................................................... 33 The Physiological Role of Zinc ................................................................................ 35 Zinc and Metallothionein Gene Expression ...................................................... 36 Carbonic Anhydrase ......................................................................................... 37 Manatee Physiology ............................................................................................... 39 Gastrointestinal Tract ....................................................................................... 39 Hindgut Fermentation ....................................................................................... 41 Metabolism ....................................................................................................... 42 Diet and the Environment ....................................................................................... 42 Vegetation Preference and Possible Role in Metal Exposure .......................... 43 Metals in Sediment ........................................................................................... 44 Manatee Evolution .................................................................................................. 45 Fossil Evidence ................................................................................................ 45 Phylogeny Classification................................................................................... 46 Project Objectives ................................................................................................... 48 Chapter 2 Objective .......................................................................................... 49 Chapter 3 Objective .......................................................................................... 50 Chapter 4 Objective .......................................................................................... 50 Chapter 5 Objective .......................................................................................... 51 Chapter 6 Objective .......................................................................................... 51 Chapter 7 Objective .......................................................................................... 52 7 Significance of the Project ...................................................................................... 52 2 BASELINE TRACE METAL LEVELS IN BLOOD OF WILD AND CAPTIVE WEST INDIAN MANATEES (Trichechus manatus) IN FLORIDA AND BELIZE ..... 67 Background ............................................................................................................. 67 Materials and Methods............................................................................................ 69 Wild
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