Toxicology of reptiles

Tai Lieu Chat Luong NEW PERSPECTIVES: TOXICOLOGY AND THE ENVIRONMENT Toxicology of Reptiles Edited by Susan C Gardner Centro de Investigaciones Biológicas del Noroeste La Paz, Mexico Eva Oberdưrster Southern Methodist University Dallas, TX Boca Raton London New York A CRC title, part of the Taylor & Francis imprint, a member of the Taylor & Francis Group, the academic division of T&F Informa plc Copyright © 2006 Taylor & Francis Group, LLC 2715_Discl.fm Page Friday, September 2, 2005 1:29 PM Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 Published in 2006 by CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2006 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group No claim to original U.S Government works Printed in the United States of America on acid-free paper 10 International Standard Book Number-10: 0-8493-2715-6 (Hardcover) International Standard Book Number-13: 978-0-8493-2715-5 (Hardcover) Library of Congress Card Number 2005049107 This book contains information obtained from authentic and highly regarded sources Reprinted material is quoted with permission, and sources are indicated A wide variety of references are listed Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers For permission to photocopy or use material electronically from this work, please access www.copyright.com (http://www.copyright.com/) or contact the Copyright Clearance Center, Inc (CCC) 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400 CCC is a not-for-profit organization that provides licenses and registration for a variety of users For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe Library of Congress Cataloging-in-Publication Data Toxicology of reptiles / edited by Susan C Gardner and Eva Oberdörster p cm (New perspectives) Includes bibliographical references and index ISBN 0-8493-2715-6 Reptiles Effect of pollution on Reptiles Ecophysiology I Gardner, Susan C II Oberdörster, Eva III New perspectives (Taylor & Francis) QL669.8.T69 2005 571.9'5179 dc22 2005049107 Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com Taylor & Francis Group is the Academic Division of T&F Informa plc Copyright © 2006 Taylor & Francis Group, LLC and the CRC Press Web site at http://www.crcpress.com Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 2715_C000.fm Page v Friday, September 9, 2005 11:21 AM Contributors A Alonso Aguirre Wildlife Trust Palisades, New York Kelly Irwin Arkansas Game & Fish Commission Benton, Arkansas Joanna Burger Rutgers University Division of Life Sciences Piscataway, New Jersey Lisa Irwin U.S Fish and Wildlife Service Arkansas Field Office Conway, Arkansas Ian Callard Biology Department Boston University Boston, Massachusetts Jennifer M Keller National Institute of Standards and Technology Hollings Marine Laboratory Charleston, South Carolina Malin Celander Goteborg University Department of Zoo Physiology Goteborg, Sweden Noppadon Kitana Department of Biology Chulalongkorn University Bangkok, Thailand Susan C Gardner Centro de Investigaciones Biológicas del Noroeste, S.C La Paz, Baja California Sur México Emily Marquez Biology Department Boston University Boston, Massachusetts William A Hopkins Department of Fisheries and Wildlife Sciences Virginia Polytechnic and State University Blacksburg, Virginia Patricia McClellan-Green Department of Environmental and Molecular Toxicology Center for Marine Sciences and Technology North Carolina State University Morehead City, North Carolina Copyright © 2006 Taylor & Francis Group, LLC 2715_C000.fm Page vi Friday, September 9, 2005 11:21 AM Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 Linda Meyers-Schöne Blue World Environment Albuquerque, New Mexico Carys L Mitchelmore University of Maryland, Center for Environmental Science, Chesapeake Biological Laboratory Solomons, Maryland Apolonia Novillo Biology Department Boston University Boston, Massachusetts Eva Oberdörster Department of Biology Southern Methodist University Dallas, Texas Margie M Peden-Adams Medical University of South Carolina Department of Pediatrics Marine Biomedicine & Environmental Sciences Center Charleston, South Carolina Copyright © 2006 Taylor & Francis Group, LLC Allen R Place Center of Marine Biology University of Maryland Baltimore, Maryland Christopher L Rowe University of Maryland Center for Environmental Science Chesapeake Biological Laboratory Solomons, Maryland Kyle W Selcer Duquesne University Pittsburgh, Pennsylvania Emily Willingham School of Medicine, Department of Urology University of California San Francisco, California Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 2715_C000.fm Page vii Friday, September 9, 2005 11:21 AM Foreword It is my honor to present the foreword of this book — a book that advances the fields related to reptilian biology, conservation, and ecological risk assessment Historically, most reptilian toxicity information has been associated with tissue concentrations (e.g., MeyersSchöne and Walton, 1994) with little cause-and-effect information available In their book entitled Ecotoxicology of Amphibians and Reptiles, Sparling, Linder, and Bishop (2000) alerted us to the scarcity of relevant contaminant effects information on reptiles compared with other vertebrate taxa The editors and authors of specific chapters stressed the need for research in areas such as the following: • Physiology: to better understand the dynamics of chemical contaminant exposure, uptake, and elimination, with emphasis on reproductive physiology and endocrine modulators • Pathology and disease: to better understand the influence of contaminants on humoral and cell-mediated responses • Ecotoxicology: to better understand critical organ concentrations and regulatory capacities • Population ecology: to better understand potential impacts of contaminants on the ability of reptiles to withstand perturbations that may affect the population This book serves as a very useful text because it cohesively summarizes some of the cutting-edge research that is taking place in areas such as reptilian endocrinology, neurophysiology, immunology, and ecology Conservation needs are also addressed as well as the issues related to complications associated with conducting population studies This information is easily available for synthesis and use in the evaluation and understanding of potential risks of reptiles to environmental contaminants As we know, reptiles are often not included in the ecological risk assessment process When present within an ecosystem, they Copyright © 2006 Taylor & Francis Group, LLC Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 2715_C000.fm Page viii Friday, September 9, 2005 11:21 AM frequently occupy key positions within the food web — one of the primary considerations when considering an ecological receptor The dilemmas faced by risk assessors, however, are the absence of sufficient reptilian toxicity information and the lack of specific exposure information Assumptions can be made with respect to the use of “default” values with uncertainty factors One must determine what level of confidence such information would yield and what level would be acceptable The selection of an appropriate receptor and utilization of technically defensible data to support the estimate of potential risk to that receptor are essential to both the scientific and regulatory management processes The question is likely to be asked whether reptiles are more toxicologically sensitive to chemical contaminants than birds or mammals The few studies that have been conducted indicate metallothioneinmetal metabolic systems in reptiles are similar to those in other vertebrate classes However, the temperature-associated sex determination reproductive strategy in turtles and alligators may make them more susceptible to endocrine disruptors compared with other vertebrates This comparison remains an area of fruitful study Significant progress has also been made in the establishment of at least one model test species, specifically, the Western fence lizard (Sceloporus occidentalis) Suitable wild populations have been located in the California Valley, the species is sexually dimorphic, females lay from to clutches of to 15 eggs each, many assay endpoints have been identified for testing purposes, and the species is easily raised in the lab Historically, the reptilian ecotoxicology database has been extremely limited and has prevented us from sufficiently addressing the question “How similar are all reptiles?” From an evolutionary prospective, traditionally, crocodilians, turtles, snakes, lizards, amphisbaenids, and tuataras were grouped together under the class Reptilia However, recent cladistic analysis proposes a classification system that places turtles and crocodilians in separate classes Although this is not widely accepted among herpetologists, it does provide additional food for thought as we consider issues such as the most appropriate test model species and toxicological data that best represent “reptiles” as a whole This book, and the investigators who have supported the research discussed within it, prove that we are making great strides in the area of reptilian ecotoxicology To the editors and authors — congratulations on a much needed and comprehensive effort To the readers — give reptiles a try if you haven’t already We could use your help! Copyright © 2006 Taylor & Francis Group, LLC 2715_C000.fm Page ix Friday, September 9, 2005 11:21 AM References Meyers-Schöne, L and Walton, B.T 1994 Turtles as monitors of chemical contaminants in the environment Rev Environ Contam Toxicol., 135, 93–153 Sparling, D.W., Linder G., and Bishop C.A., Eds., Ecotoxicology of Amphibians and Reptiles, SETAC Press, Pensacola, FL, 2000 Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 Linda Meyers-Schưne, Ph.D Blue World Environment Copyright © 2006 Taylor & Francis Group, LLC Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 2715_C000.fm Page xi Friday, September 9, 2005 11:21 AM Acknowledgments We are indebted to Drs Donald E Gardner and Günter Oberdörster for the decades of service as scientific role models and for encouraging us to compile this book We would also like to extend personal appreciation to Dr Louis Guillette, Jr., for his contribution to the initial book outline and for his dedication to the study of comparative physiology, which helped initially propel the field of reptile toxicology to the current state of the science We gratefully acknowledge the peer reviewers, including Drs William S Baldwin, Kym Campbell, David Hinton, Gerald LeBlanc, Michael Newman, Charles Rice, Jeffrey Seminoff, and Stacey Weiss, for their thoughtful suggestions for revision of the chapters We would also like to thank the contributing authors for their extensive effort in the writing and revising of these chapters EO and SCG Copyright © 2006 Taylor & Francis Group, LLC Downloaded by [National Taiwan Ocean University] at 07:21 15 December 2014 2715_C000.fm Page xiii Friday, September 9, 2005 11:21 AM Contents Chapter Introduction to Reptilian Toxicology Susan C Gardner Chapter Global Threats Affecting the Status of Reptile Populations Lisa Irwin and Kelly Irwin Chapter Use of Tissue Residues in Reptile Ecotoxicology: A Call for Integration and Experimentalism 35 William A Hopkins Chapter Tools for Assessing Contaminant Exposure and Effects in Reptiles 63 Carys L Mitchelmore, Christopher L Rowe, and Allen R Place Chapter Hepatic, Renal, and Adrenal Toxicology 123 Patricia McClellan-Green, Malin Celander, and Eva Oberdörster Chapter Developmental and Reproductive Effects 149 Emily Willingham Chapter Neurotoxicology and Behavioral Effects in Reptiles 173 Joanna Burger Chapter Immunotoxicology and Implications for Reptilian Health 199 Jennifer M Keller, Margie M Peden-Adams, and A Alonso Aguirre Chapter Reptilian Genotoxicity 241 Apolonia Novillo, Noppadon Kitana, Emily Marquez, and Ian P Callard Chapter 10 Reptile Ecotoxicology: Studying the Effects of Contaminants on Populations 267 Kyle W Selcer Index .299 Copyright © 2006 Taylor & Francis Group, LLC 2715_C010.fm Page 283 Wednesday, August 31, 2005 1:08 PM Downloaded by [National Taiwan Ocean University] at 07:22 15 December 2014 Chapter 10: Reptile Ecotoxicology 283 clutches allow for sampling of contaminants from some eggs and incubation of other eggs from the same nest for assessing effects of contaminants on hatching rates and various hatchling parameters 17,18 Turtles usually have the periodic type of life history strategy that places a premium on adult survivorship Thus, any factor that selectively removes adults from the populations (e.g., pet trade, use as food) can have serious consequences on turtle populations Also, turtle populations may be slow in recovering after a population decline.44,45 Turtles store considerable amounts of body fat that can serve as a reservoir for lipid-soluble contaminants These lipids are used for reproduction and can be passed on to the eggs during the yolking process Adult female turtles have been shown to have lower levels of accumulated contaminants than adult males from the same site, providing indirect evidence that females undergo depuration during reproduction.18 Some turtle species have temperature-dependent sex determination, whereas others have genotypic sex determination Many turtle species exhibit a high degree of site tenure, making them ideal for studies of local contamination Also, some turtles appear to maintain high population densities in known contaminated sites, leading to the suggestion that they may be relatively insensitive to effects of toxins Turtles occupy a variety of habitats, from marine and freshwater to terrestrial Each of these lifestyles results in very different routes and levels of exposure to environmental contaminants; therefore, model species are suggested for each of these groups Freshwater Aquatic Turtles Freshwater aquatic turtles are potentially exposed to aquatic contaminants at both the egg and adult stages The eggs may be exposed to contaminants through maternal deposition and by contaminants in the nesting matrix Adults can be exposed to contaminants through their food and from their aquatic medium because they are known to cycle water through their pharynx and cloaca Freshwater aquatic turtles may be carnivorous, omnivorous, or herbivorous, depending on the species It is likely that the more carnivorous species are at greatest risk of significant exposure to persistent contaminants that biomagnify The ecology of several species of freshwater turtles has been extensively studied,31,35,44–46 resulting in a good demographic framework from which to investigate contaminants Furthermore, compared with other reptiles, a substantial amount of data is available on contaminant levels present in freshwater turtles,8,15,47 and comprehensive attempts have been made to determine the effects of contaminant exposure on population parameters of some species.17–21 Copyright © 2006 Taylor & Francis Group, LLC 2715_C010.fm Page 284 Wednesday, August 31, 2005 1:08 PM 284 Toxicology of Reptiles Downloaded by [National Taiwan Ocean University] at 07:22 15 December 2014 Freshwater turtles as a group are declining worldwide, with exploitation by humans for food and the pet trade being among the major causes.48 However, significant effects of contaminants on turtle populations cannot be ruled out 1.1 Red-Eared Slider Turtle (Trachemys scripta) The red-eared slider turtle — common to lakes, ponds, and streams — is geographically widespread throughout the central and southeastern United States Subspecies extend into Mexico and Central America There is a substantial amount of data available on the life history and ecology of this turtle.46 This species has temperature-dependent sex determination, and studies have investigated contaminant effects on this process.49 This turtle is generally omnivorous, but individuals may shift their diet more toward herbivory as they move from juvenile to adult Red-eared slider turtles are common in the pet trade Hatchlings and small juveniles (