Biology_of_Turtles
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Biology of Turtles
Biology of Turtles
Edited by
Jeanette Wyneken
Florida Atlantic University
Boca Raton, FL, U.S.A.
Matthew H. Godfrey
North Carolina Wildlife Resources Commission
Beaufort, NC, U.S.A.
Vincent Bels
Muséum of National D’ Histoire Naturelle
Paris, France
Cover photos by Stephen L. Barten, D.V.M., Ann C. Burke, and Jeanette Wyneken.
CRC Press
Taylor & Francis Group
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Library of Congress Cataloging in Publication Data
Wyneken, Jeanette, 1956
Biology of turtles / Jeanette Wyneken, Matthew H. Godfrey, Vincent Bels. p. cm.
Includes bibliographical references and index. ISBN 978 0 8493 3339 2 (alk. paper)
1. Turtles. I. Godfrey, Matthew H. II. Bels, V. L. (Vincent L.) III. Title.
QL666.C5W96 2007 |
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597.92 dc22 |
2007024320 |
Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com
and the CRC Press Web site at http://www.crcpress.com
Contents |
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Preface............................................................................................................................................. |
vii |
About the Editors............................................................................................................................ |
ix |
Contributors..................................................................................................................................... |
xi |
Chapter 1 |
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How the Turtle Gets Its Shell............................................................................................................. |
1 |
Scott F. Gilbert, Judith A. Cebra-Thomas, and Ann C. Burke |
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Chapter 2 |
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Comparative Ontogenetic and Phylogenetic Aspects of Chelonian Chondro-Osseous |
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Growth and Skeletochronology........................................................................................................ |
17 |
Melissa L. Snover and Anders G.J. Rhodin |
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Chapter 3 |
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Evolution and Structure of the Turtle Shell...................................................................................... |
45 |
Peter C.H. Pritchard |
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Chapter 4 |
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Long Bone Allometry in Tortoises and Turtles................................................................................ |
85 |
Gustavo A. Llorente, Xavier Ruiz, Adrià Casinos, Ignacio Barandalla, and Carles Viladiu |
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Chapter 5 |
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Evolution of Locomotion in Aquatic Turtles.................................................................................... |
97 |
Sabine Renous, France de Lapparent de Broin, Marion Depecker, John Davenport, |
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and Vincent Bels |
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Chapter 6 |
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Hindlimb Function in Turtle Locomotion: Limb Movements and Muscular Activation across |
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Taxa, Environment, and Ontogeny................................................................................................. |
139 |
Richard W. Blob, Angela R.V. Rivera, and Mark W. Westneat |
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Chapter 7 |
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Cervical Anatomy and Function in Turtles.................................................................................... |
163 |
Anthony Herrel, Johan Van Damme, and Peter Aerts |
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Chapter 8 |
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Functional Evolution of Feeding Behavior in Turtles.................................................................... |
187 |
Vincent Bels, Sabine Baussart, John Davenport, Marc Shorten, Ruth M. O’Riordan, |
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Sabine Renous, and Julia l. Davenport |
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vi |
Contents |
Chapter 9 |
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The Structure of Cardiopulmonary Systems of Turtles: Implications for Behavior |
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and Function ................................................................................................................................... |
213 |
Jeanette Wyneken |
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Chapter 10 |
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Reproductive Structures and Strategies of Turtles......................................................................... |
225 |
Jeffrey D. Miller and Stephen A. Dinkelacker |
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Chapter 11 |
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Mixed and Uniform Brood Sex Ratio Strategy in Turtles: The Facts, the Theory, and Their |
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Consequences................................................................................................................................. |
279 |
Vincent Hulin, Marc Girondot, Matthew H. Godfrey, and Jean-Michel Guillon |
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Chapter 12 |
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The Physiology and Anatomy of Anoxia Tolerance in the Freshwater Turtle Brain..................... |
301 |
Sarah L. Milton |
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Chapter 13 |
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The Relationships of Turtles within Amniotes.............................................................................. |
345 |
Olivier Rieppel |
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Index.............................................................................................................................................. |
355 |
Preface
The first beasts that we identify as turtles emerged abruptly in the Triassic about 220 million years ago. Since then, countless diverse lineages of turtles—terrestrial, marine, freshwater, and in-between— have come and gone, yet many lineages persist for tens of millions to more than 100 million years. All bring with them the suite of traits that are uniquely turtle: a bony shell, usually a retractable neck, lack of trunk musculature, and limb girdles located inside the rib cage (instead of lying outside of it). The reptiles we identify as turtles, or testudines, or chelonians, have captivated many naturalists and other scientists because of these and other unique traits and their consequences.
Some 180 years ago while in Jena, Germany, Ludwig Heinrich Bojanus developed an interest in the anatomy of the European turtle Emys obicularis. By dissecting specimens and illustrating their anatomy over the next decade, Bojanus authored one of the most detailed studies on any single vertebrate species, Anatome Testudinis Europaeae (1819–1821). This unparalleled book on turtle anatomy represents the intersection of his interests as a naturalist, comparative anatomist, veterinary surgeon, and teacher of anatomical art. It was because of this historical backdrop that the biology, particularly the anatomy, of turtles was visited again fittingly at the Sixth International Congress of Vertebrate Morphology, which was held in Jena in 2001. The symposium and its many contributed papers served as the foundation upon which this volume is based. However, this book goes beyond a morphologically based symposium in recognizing that the structures of turtles are particularly interesting and best understood within the context of their formation, their diversity of functions, their novelty, and their evolution. Whereas several areas of interest (e.g., turtle genetics, sensory systems and behavior, and life history evolution) are not included—as these fields continue to progress rapidly without a clear stable point—we have brought together a wide range of discussions on other novel features of turtles.
For the first time anywhere, we have a robust discussion about the origins, development, and diversity of the shell in chapters by Gilbert et al. (Chapter 1) and Pritchard (Chapter 3). Snover and Rhodin (Chapter 2) synthesize the important work on bone growth and aging, while Llorente et al. (Chapter 4) bring forward an understanding of limb bone strength in this unique group. Turtle locomotion is unique in many ways because of the presence of the shell. Renous et al. (Chapter 5) provide a novel synthesis of the field while Blob et al. (Chapter 6) present an experimental and functional perspective on the motor patterns used by turtles during locomotion. The retractable neck is expertly described by Herrel et al. (Chapter 7) and given functional context beyond the simple view of “protecting the head.” Bels et al. (Chapter 8) provide a functional, anatomical, and behavioral overview of feeding in herbivorous versus carnivorous types and aquatic versus terrestrial turtles that has never previously been summarized. Wyneken (Chapter 9) discusses cardiopulmonary anatomy and function from functional perspectives. Reproductive strategies receive a thorough overview by Miller and Dinkelacker (Chapter 10). Hulin et al. (Chapter 11) challenge the reader to think rigorously in their analysis of the consequences of environmental sex determination and turtle sex ratios, and Milton (Chapter 12) reminds us that at least some turtles (particularly the aquatic species that hibernate underwater) have a number of very unique structural and functional adaptations for tolerating low oxygen levels. Rieppel (Chapter 13) examines why the origin of turtles and their relationships to other amniotes is such a great challenge. Despite more than a century of intensive study, our understanding of the phylogenetic origins of turtles remains indefinite. This chapter particularly challenges us to look both inside and outside the shell as we build an understanding of the evolution of turtles. This challenge extends across all fields represented in this volume and those yet to come.
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Preface |
The editors thank the many external referees who responded to our request for a rigorous review of each chapter. We are grateful for the collegial environment in Jena, Germany, and at the Sixth International Congress for Vertebrate Morphology, which stimulated the ideas and topics for this synthesis. Particularly, we acknowledge Matthias Starck for his encouragement and support of the symposium “Turtles: From Structures to Strategies of Life,” and to the late Peter Lutz for a perspective on the history of the science and the many novel integrative approaches that have led to understanding the biology of turtles. John Sulzycki and David Fausel at CRC Press/Taylor & Francis provided essential guidance, superb advice, and good humor as this book progressed at a turtle’s pace.
Jeanette Wyneken
Boca Raton, Florida, USA
Matthew H. Godfrey
Beaufort, North Carolina, USA
Vincent Bels
Paris, France
About the Editors
Jeanette Wyneken, Ph.D., is an associate professor of biological sciences at Florida Atlantic University in Boca Raton. She earned her B.A. from Illinois Wesleyan University and later, her Ph.D. in biology from the University of Illinois in 1988. She was a research associate from 1988 to 1989 at the University of Illinois before taking a research position at Florida Atlantic University in 1990. She later assumed a position as assistant professor, then associate professor of biological sciences at Florida Atlantic University. Dr. Wyneken is a comparative and functional anatomist and a conservation biologist. Her studies are diverse and deal with growth, energetics, migratory behavior, development, including environmental sex determination, and medical imaging of reptiles. In addition to teaching vertebrate anatomy and development, she developed and taught the Biology of Sea Turtles course offered at Harbor Branch Oceanographic Institute in Fort Pierce, Florida, and worked with Selina Heppell and Larry Crowder to develop a similar conservation-based sea turtle biology course at the Duke University Marine Laboratory in Beaufort, North Carolina. She is the former president of the Annual Sea Turtle Symposium (now The International Sea Turtle Society), the convener of the 7th International Congress for Vertebrate Morphology, and has organized several symposia on various aspects of the biology of turtles.
Dr. Wyneken serves on the editorial boards of two professional journals in her field and is active in the peer review process for a number of other journals. She is a member of several professional organizations including the AAAS, Association of Ichthyologists and Herpetologists, Society for the Study of Amphibians and Reptiles, Herpetologists League, Association of Reptilian and Amphibian Veterinarians, the International Sea Turtle Society, Sigma Xi, the Society of Integra-
tive and Comparative Biology, and the IUCN Marine Turtle Specialist Group. Dr. Wyneken has authored more than 30 peer-reviewed papers, four book chapters, one book (The Anatomy of Sea Turtles), and co-edited The Biology of Sea Turtles, Volume 2.
Matthew H. Godfrey, Ph.D., is a biologist with the North Carolina Wildlife Resources Commission and an adjunct assistant professor at the Nicholas School for the Environment and Earth Studies at Duke University, North Carolina. Dr. Godfrey received a B.A. (1991) in history and philosophy from the University of Toronto. He went on to receive a M.Sc. (1994) and Ph.D. (1997) in zoology from the University of Toronto in 1997. Between 1997 and 2002, Dr. Godfrey worked as a research fellow at Projeto TAMAR-IBAMA in Brazil and as a researcher/lecturer at Université Paris, France. His research topics include behavioral and evolutionary ecology of reptiles, with a focus on temperature-dependent sexual differentiation. Dr. Godfrey is also interested in the conservation of protected species and its links to social justice. He has authored or co-authored more than 40 research papers and five chapters in edited books. Dr. Godfrey is currently co-editor of the Marine Turtle Newsletter and serves on the editorial board of two other scientific journals. He is also a member of the IUCN Marine Turtle Specialist Group and serves on three national and two state scientific advisory committees concerned with protected species management and conservation.
Vincent Bels, Ph.D., is professor at the Muséum National d’Histoire Naturelle (Paris, France). He obtained his B.A. and his doctorat d’Etat from the University of Liège (Belgium) in 1989. Dr. Bels began his work in ethology at the University of Liège and cultivated his interest in comparative and functional morphology of vertebrates. He is now associate director of the research team UMR7179 “Mécanismes adaptatifs: des organismes aux communautés” (CNRS – MNHN – Univ. Paris 6
– College de France) at the Department Ecologie et Gestion de la Biodiversité at the Muséum National d’Histoire Naturelle. In addition to teaching vertebrate functional morphology at the Uni-
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