Adaptations of Desert Organisms Edited by J.1. Cloudsley-Thompson Springer Berlin Heidelberg New York Barcelona Budapest Hong Kong London Milan Paris Santa Clara Singapore Tokyo
Volumes already published Ecophysiology of the Camelidae and Desert Ruminants By R.T. Wilson (1989) Ecophysiology of Desert Arthropods and Reptiles By J.L. Cloudsley-Thompson (1991) Plant Nutrients in Desert Environments By A. Day and K. Ludeke (1993) Seed Germination in Desert Plants By Y. Gutterman (1993) Behavioural Adaptations of Desert Animals By G. Costa (1995) Invertebrates in Hot and Cold Arid Environments By L. S0mme (1995) Energetics of Desert Invertebrates By H. Heatwole (1996) Ecophysiology of Desert Birds By G.L. Maclean (1996) Plants of Desert Dunes By A. Danin (1996) Biotic Interactions in Arid Lands By J.L. Cloudsley-Thompson (1996) Structure-Function Relations of Warm Desert Plants By A.C. Gibson (1996) Physiological Ecology of North American Desert plants By S.D. Smith, R.K. Monson, and J.E. Anderson (1997) Ecophysiology of Small Desert Mammals By A.A. Degen (1997) Homeostasis in Desert Reptiles By S.D. Bradshaw (1997) Ecophysiology of Amphibians Inhabiting Xeric Environments By M:R. Warburg (1997) In preparation Avian Desert Predators By W.E. Cook (1997)
S. Donald Bradshaw Homeostasis in Desert Reptiles With 62 Figures and 40 Tables Springer
Prof. Dr. S. DONALD BRADSHAW Professor and Head of the Department of Zoology The University of Western Australia Hackett Drive, Matilda Bay, Perth Western Australia 6907 Front cover illustration: The Ornate dragon lizard (Ctenophorus ornatus) from Western Australia whose ecology and physiology has been extensively studied, both in the field and the laboratory, over a period of three decades. ISSN 1430-9432 ISBN-\3: 978-3-642-64368-2 e-isbn-\3: 978-3-642-60355-6 001: 10.1007/978-3-642-60355-6 Library of Congress Cataloging-in-Publication Data. Bradshaw, S.D. (Sidney Donald) Homeostasis in desert reptiles/s. Donald Bradshaw. p. cm. - (Adaptations of desert organisms) Includes bibliographical references (p. ) and index. 1. Reptiles - Physiology. 2. Reptiles - Adaptation. 3. Desert animals - Physiology. 4. Desert animals - Adaptation. 5. Homeostasis. I. Title. II. Series. QL669.2.B74 1997 597.9'0452652 - dc20 96-43589 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permissions for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer-Verlag Berlin Heidelberg 1997 Soflcover reprint of the hardcover I st edition 1997 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover design: Design & Production GmbH, Heidelberg Typesetting: Best-set Typesetter Ltd., Hong Kong SPIN: 10481842 31/3137/SPS - 5 4 3 2 1 0 - Printed on acid-free paper
To Felicity, for her priceless gift of truth and love... dont la purete rn'aide a vivre
Acknowledgements I should like to thank John Cloudsley-Thompson for his kind invitation to write this book and for giving me the opportunity of extending my thoughts on reptilian ecophysiology. Most of the text of the book was written whilst on study leave in France and I am very grateful to Robert Barbault of the Ecole N ormale Superieure in Paris for the opportunity of sharing the excitement and ferment of his laboratory. One of my greatest regrets is that Michel Lemire, from the Museum d'histoire Naturelle, with whom I shared so many happy and profound experiences, died suddenly at an early age just after I left Paris to return to Australia, as did Marie Charlotte Saint Girons who, with her husband Hubert, nurtured all my herpetological experiences in France over a period of three decades. Many of the ideas in the book have been enriched by discussions with colleagues over the years, including Fran<;:ois Lachiver, Hubert and Marie-Charlotte Saint Girons, Maurice Fontaine, Erik Skadhauge, Greg Rice, Phil Withers, Howard Bern, Claude Grenot, Roland Vernet, John Ball and Carl Gans. I am also very grateful to Roger Avery, Bill Danztler and Charles Peterson for allowing me access to unpublished and original data. I also wish to express my sincere appreciation for the generous funding that I have received over the years from the Australian Research Council (and in its former guises of ARGC and ARGS), without which I should never have been able to carry out fundamental research on desert reptiles. Permission to reproduce a number of figures from my earlier book on Ecophysiology of Desert Reptiles was generously given by Academic Press, whom I wish to acknowledge for permission to reproduce the following tables and figures: Figs. 2.2, 2.6, 2.7, 2.10,2.12,2.13,2.14,2.15,2.16,2.20,2.23,2.26, 2.29, 2.34, 2.35, 2.37, 2.42,5.3,5.10, and 5.15. Academic Press Inc. also approved reproduction of material incorporated in Figs. 2.6, 2.7, 3.1, 3.2, 3.6, 3.8, 3.11, 3.13, 3.16, 3.24 and 4.2 and Tables 2.8, 3.3, 3.7, 3.11, 4.3, and 4.8 in the current text. I also wish to acknowledge Elsevier Science (Fig. 4.10), Munskgaard International Publishers Ltd. (Tables 3.2 and 3.9), University of Chicago Press (Tables 4.1 and 4.6), Princeton University Press
VIII Acknowledgements (Fig. 4.15), The Society for the Study of Amphibians and Reptiles (Fig. 4.16), Springer-Verlag (Figs. 2.9, 3.25, 4.1, 4.7, 4.8, Tables 2.13, 2.14, 4.2 and 4.4 and Plate 3.2), Pergamon Press (Fig. 4.10), John Wiley & Sons, Inc. (Fig. 4.6 and Plates 2.1 and 2.2), E. J. Brill (Fig. 2.14 and Table 2.17), MacMillan (Table 2.3), Masson (Plate 3.1), Herpetologica (Fig. 2.2). Permission has also been requested for the reproduction of Tables 2.2, 2.4, 2.5, 2.10, 2.15, 3.2, 3.6, 3.8 and 3.9. Perth, December 1996 S.D. BRADSHAW
Contents Introduction... 1 1 The Osmotic Anatomy of the Reptiles... 9 1.1 Evidence for Homeostasis... 9 1.2 A Comparative Account... 9 1.3 Water and Electrolytes in Reptiles as a Group... 12 1.4 Conclusions............................... 12 2 Water and Electrolyte Homeostasis... 21 2.1 Basic Concepts... 21 2.2 The Maintenance of Homeostasis... 23 2.2.1 Regulatory Responses... 24 2.2.2 The Concept of Stress... 25 2.3 Effector Systems... 25 2.3.1 Kidney Morphology... 26 2.3.2 Derivation of Renal Parameters... 28 2.3.3 The Cloacal-Colonic Complex in Reptiles... 31 2.3.4 The Cephalic Salt-Secreting Glands... 32 2.4 Osmoregulation in Crocodiles, Alligators and Chelonians... 33 2.4.1 Extent of Environmental Exchange... 33 2.4.2 Kidney and Cloaca... 34 2.4.3 Salt-Excreting Glands... 35 2.4.4 Desert Tortoises... 35 2.5 Osmoregulation in Lizards... 39 2.5.1 Hypernatraemia and Hyperkalaemia in Lizards... 39 2.5.2 Studies of the Agamid Genus Amphibolurus (Ctenophorus and Pogona) in Australia... 40
x Contents 2.5.3 The Desert Iguana (Dipsosaurus dorsalis) in North America............................... 52 2.5.4 The Chuckwallas (Sauromalus obesus and S. hispidus)... 55 2.5.5 Two Saharan Lizards: Le Fouette-Queue (Uromastix acanthinurus) and the Varanid Varanus griseus... 58 2.5.6 The Mountain or Thorny Devil (Moloch horridus)... 65 2.6 Osmoregulation in Snakes... 67 2.7 Conclusions................................... 70 3 Activity and Hormonal Control of Excretory Organs... 73 3.1 Avant Propos.................................. 73 3.2 The Kidney... 74 3.2.1 Renal Clearances and the Handling of Water and Solutes............................ 74 3.2.2 Neurohypophysial Hormones... 79 3.2.3 Adrenocortical Hormones... 88 3.2.4 Localisation of Action of Arginine Vasotocin in Kidney Tubules... 95 3.3 The Cloacal-Colonic Complex... 99 3.4 Cephalic Salt-Secreting Glands... 107 3.5 Conclusion.................................... 120 4 Thermal Homeostasis... 123 4.1 Generalities................................... 123 4.2 The Interpretation of Field Studies... 124 4.3 Physiological Mechanisms...................... 126 4.3.1 Metabolic Characteristics of Ectotherms... 126 4.3.2 Sources of Heat Production in Reptiles... 126 4.3.3 Thermal Hysterisis and Changes in Dermal Vascularity........................... 130 4.3.4 Panting and Evaporative Heat Loss... 136 4.3.5 The Pineal Eye and Photoperiod... 139 4.3.6 Hormonal Influences on Thermoregulation... 141
Contents Xl 4.4 Behavioural Mechanisms....................... 147 4.4.1 The Neuronal Basis for Thermoregulation... 147 4.4.2 Maintenance of Thermal Homeostasis in the Field... " lsi 4.S Conclusion... 163 S Conclusion... 167 References... 17 S Subject Index... 199