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Toxicology of Reptiles
NEW PERSPECTIVES: TOXICOLOGY AND THE ENVIRONMENT

Toxicology of Reptiles

Edited by

Susan C. Gardner
Centro de Investigaciones Biológicas del Noroeste
La Paz, Mexico

Eva Oberdörster
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.
2715_Discl.fm Page 1 Wednesday, April 20, 2005 9:12 AM

Published in 2005 by
CRC Press
Taylor & Francis Group
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Boca Raton, FL 33487-2742

© 2005 by Taylor & Francis Group, LLC

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Contributors
A. Alonso Aguirre Kelly Irwin
Wildlife Trust Arkansas Game & Fish Commission
Palisades, New York Benton, Arkansas

Joanna Burger Lisa Irwin

Rutgers University U.S. Fish and Wildlife Service
Division of Life Sciences Arkansas Field Office
Piscataway, New Jersey Conway, Arkansas

Ian Callard Jennifer M. Keller

Biology Department National Institute of
Boston University Standards and Technology
Boston, Massachusetts Hollings Marine Laboratory
Charleston, South Carolina
Malin Celander
Noppadon Kitana
Goteborg University
Department of Biology
Department of Zoo Physiology
Chulalongkorn University
Goteborg, Sweden
Bangkok, Thailand

Susan C. Gardner Emily Marquez

Centro de Investigaciones Biology Department
Biológicas del Noroeste, S.C. Boston University
La Paz, Baja California Sur Boston, Massachusetts
México
Patricia McClellan-Green
William A. Hopkins Department of Environmental and
Department of Fisheries and Wildlife Molecular Toxicology
Sciences Center for Marine Sciences and
Virginia Polytechnic and Technology
State University North Carolina State University
Blacksburg, Virginia Morehead City, North Carolina
Linda Meyers-Schöne Allen R. Place
Blue World Environment Center of Marine Biology
Albuquerque, New Mexico University of Maryland
Baltimore, Maryland
Carys L. Mitchelmore
University of Maryland, Christopher L. Rowe
Center for Environmental Science, University of Maryland
Chesapeake Biological Laboratory Center for Environmental Science
Solomons, Maryland Chesapeake Biological Laboratory
Solomons, Maryland
Apolonia Novillo
Biology Department Kyle W. Selcer
Boston University Duquesne University
Boston, Massachusetts Pittsburgh, Pennsylvania

Eva Oberdörster Emily Willingham

Department of Biology School of Medicine,
Southern Methodist University Department of Urology
Dallas, Texas University of California
San Francisco, California
Margie M. Peden-Adams
Medical University of
South Carolina
Department of Pediatrics
Marine Biomedicine &
Environmental Sciences Center
Charleston, South Carolina
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 infor-
mation has been associated with tissue concentrations (e.g., Meyers-
Schöne 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 concentra-
tions and regulatory capacities
• Population ecology: to better understand potential impacts of
contaminants on the ability of reptiles to withstand perturba-
tions that may affect the population

This book serves as a very useful text because it cohesively sum-

marizes 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 stud-
ies. This information is easily available for synthesis and use in the
evaluation and understanding of potential risks of reptiles to environ-
mental contaminants.
As we know, reptiles are often not included in the ecological risk
assessment process. When present within an ecosystem, they
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 suffi-
cient 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 toxi-
cologically sensitive to chemical contaminants than birds or mammals.
The few studies that have been conducted indicate metallothionein-
metal metabolic systems in reptiles are similar to those in other
vertebrate classes. However, the temperature-associated sex determi-
nation reproductive strategy in turtles and alligators may make them
more susceptible to endocrine disruptors compared with other verte-
brates. 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 3 to 6 clutches of 8 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 — congratula-
tions on a much needed and comprehensive effort. To the readers —
give reptiles a try if you haven’t already. We could use your help!
References
Meyers-Schöne, L. and Walton, B.T. 1994. Turtles as monitors of chemical contami-
nants 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.

Linda Meyers-Schöne, Ph.D.

Blue World Environment
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
Contents
Chapter 1 Introduction to Reptilian Toxicology...........................................1
Susan C. Gardner

Chapter 2 Global Threats Affecting the Status of Reptile Populations....9

Lisa Irwin and Kelly Irwin

Chapter 3 Use of Tissue Residues in Reptile Ecotoxicology:

A Call for Integration and Experimentalism .........................................35
William A. Hopkins

Chapter 4 Tools for Assessing Contaminant Exposure and

Effects in Reptiles ........................................................................................63
Carys L. Mitchelmore, Christopher L. Rowe, and Allen R. Place

Chapter 5 Hepatic, Renal, and Adrenal Toxicology ................................123

Patricia McClellan-Green, Malin Celander, and Eva Oberdörster

Chapter 6 Developmental and Reproductive Effects..............................149

Emily Willingham

Chapter 7 Neurotoxicology and Behavioral Effects in Reptiles ...........173

Joanna Burger

Chapter 8 Immunotoxicology and Implications for Reptilian Health...199

Jennifer M. Keller, Margie M. Peden-Adams, and
A. Alonso Aguirre

Chapter 9 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
chapter 1

Introduction to
Reptilian Toxicology
Susan C. Gardner

Table of Contents
I. Book Overview...................................................................................1
II. Reptilian Toxicology ..........................................................................1
III. Summary .............................................................................................7

I. Book Overview
Compared with studies in other taxa, the field of reptilian toxicology
is in its infancy. However, studies in other wildlife (fish and mammals
in particular) have provided the foundation for reptilian studies, and
many modern tools developed for toxicological assessment of other
species have been successfully applied to reptiles. The purpose of this
book is to summarize the information currently available on toxicology
of reptiles within the context of what is known of nonreptilian species.
The effects of contaminants on target organs are described, including
examples of terrestrial, freshwater, and marine species. Major contam-
inant classes are covered within each chapter, with a focus on contam-
inants of greatest concern. Some overlap in the material covered among
chapters is necessary and intentional so that each chapter is complete
in its treatment of the material, whereas references to other chapters are
included to direct the reader to more information on particular topics.

II. Reptilian Toxicology

The current population status of most reptilian species has not been
evaluated. Of the species in which evaluations have been conducted,
1
2 Toxicology of Reptiles

more than half are regarded as threatened. Chapter 2 provides an

overview of the current phylogeny and status of reptile populations
and the major threats to their stability, including examples of both
terrestrial and aquatic species. Although habitat degradation is one
of the most pronounced threats to reptile populations, Irwin and
Irwin (Chapter 2) point out that population declines are generally the
result of a combination of both anthropogenic and natural stressors,
and rarely is one single factor operating in isolation. The response of
a population to environmental stressors will differ according to each
species’ life history characteristics and the cumulative effects of the
different stressors present. Therefore, the effects of natural stressors
(e.g., drought, flood, disease) will be more pronounced when coupled
with anthropogenic factors (e.g., contaminants, habitat destruction,
harvest) and may eventually impede a species’ ability to maintain
stable populations.
In Chapter 2, Irwin and Irwin provide an overview of the life
history characteristics that make many reptilian species difficult to
study using short-term surveys, including long generation times, late
maturation, and cryptic juvenile stages. Detecting declines in such
species is often delayed and may not be possible until decreases in
reproductive size classes are observed years or decades later. There-
fore, the authors stress the importance of long-term herptofaunal
surveys using standardized protocols to ensure the validity of com-
parisons of populations over time and space.
In Chapter 3, Hopkins illustrates the utility of reptiles as indicators
of environmental contamination and emphasizes the potential of
reptiles to serve as models in the study of environmental pollution.
With high population densities and high efficiency of exploiting
resources, reptiles may serve a major role as transporters of contam-
inants through food webs, the importance of which likely has been
underestimated. To date, the majority of toxicological assessments in
reptiles have been made up of tissue residue studies. Measurements
of chemical residues in tissues are valuable because they provide an
indication of the bioavailability of the contaminant in the environ-
ment and the ecologic and physiologic characteristics of the organism.
Whereas the distribution of contaminants among tissues in reptiles
is generally similar to those in other vertebrate wildlife, reptiles pos-
sess unique sets of traits that may influence accumulation patterns.
High conversion efficiencies, a less developed enzymatic detoxifica-
tion system, dietary patterns, and behavioral traits (as described in
Chapter 7) are all factors that may influence uptake and accumulation
of contaminants in reptiles. Likewise, Hopkins (Chapter 3) points out
Chapter 1: Introduction to Reptilian Toxicology 3

that differences exist in contaminant accumulation among individuals

of the same species. For example, male–female differences in tissue
residues observed in reptilian field surveys can be attributed to behav-
ior, feeding ecology, reproductive state, or gender-based differences
in physiology. Additionally, ontogenetic shifts in enzymatic metabo-
lism and feeding strategies have also been observed in reptiles and
could result in variation in the accumulation of contaminants
throughout an individual’s lifetime.
Despite a large body of literature reporting contaminant concen-
trations in reptilian tissues, interpretation of this information is diffi-
cult because of the lack of data on the corresponding concentrations
of contaminants in the environment and their effects. In Chapter 3,
Hopkins offers recommendations on where efforts in reptile tissue
residue analyses should be focused to maximize the application of
these results toward conservation initiatives. He proposes that field
surveys be coupled with laboratory and field experiments and be
designed to test well-conceived hypotheses to provide much needed
information to improve understanding of contaminant effects on rep-
tile populations.
Establishing relationships between contaminant exposure and
biological effects in reptiles will likely involve an increased use of
biomarkers. Biomarker research on fish has formed the basis for
biomarker development in reptile species with the consequence that
these tools have been applied in a similar fashion in both groups.
Mitchelmore and coauthors (Chapter 4) describe the current state of
reptilian biomarker research and the application of various tools
ranging from the molecular level to the individual level. These tools
are particularly valuable as compared with pure residue studies
because they provide indications of synergistic effects among com-
plex mixtures as well as the effects of contaminant metabolites not
detected in routine analyses.
Measurements of xenobiotic induction or inhibition of enzymes
are particularly useful as tools for biomonitoring. As in mammals,
hepatic phase I enzymes in reptiles have been induced after contam-
inant exposure (e.g., polyaromatic hydrocarbon treatment in snakes
and turtles), but much less work has been done on reptilian enzymes
involved in phase II metabolism, which to date has consisted only of
glutathione conjugation. Chapter 5 covers the basic anatomy of rep-
tilian liver and kidney and their roles in metabolism and elimination
of xenobiotics as compared with other vertebrates. Numerous cyto-
chrome P450 isozymes known in mammals have been found in the
reptile liver, whereas other mammalian isozymes may be completely
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