Behavior of lizards: evolutionary and mechanistic perspectives 9781498782722, 1498782728, 9781498782739

Table of contents :
Content: Introduction: The characterization and evolution of lizard behavior / Vincent L. Bels and Anthony P. Russell --
Part I. "Everyday" behavior. Chapter 1. Behavioral thermoregulation in lizards : strategies for achieving preferred temperature / Ian R.G. Black, Jacob M. Berman, Viviana Cadena, and Glenn J. Tattersall
Chapter 2. Lizard locomotion : relationships between behavior, performance, and function / Timothy E. Higham
Chapter 3. Lizard foraging : a perspective integrating sensory ecology and life histories / Chi-Yun Kuo, Martha M. Muñoz, and Duncan J. Irschick
Chapter 4. Predatory behavior in lizards : strategies and mechanisms for catching prey / Vincent L. Bels, Jean-Pierre Pallandre, Sébastien Charlier, Aurélie Maillard, Pierre Legreneur, Anthony P. Russell, Anne-Sophie Paindavoine, Leïla-Nastasia Zghikh, Emeline Paulet, Emilie Van Gysel, Christophe Rémy, and Stéphane Montuelle
Chapter 5. Antipredator behavioral mechanisms : avoidance, deterrence, escape and encounter / Eric J. McElroy --
Part II. Social behavior and communication. Chapter 6. The physiological control of social behavior in lizards / Rachel E. Cohen and Juli Wade
Chapter 7. Sensory processing in relation to signaling behavior / Leo J. Fleishman and Enrique Font
Chapter 8. Phylogeny and ontogeny of display behavior / Michele A. Johnson, Ellee G. Cook, and Bonnie K. Kircher
Chapter 9. Behavioral ecology of aggressive behavior in lizards / Martin J. Whiting and Donald B. Miles
Chapter 10. Stable social grouping in lizards / Geoffrey M. While, Michael G. Gardner, David G. Chapple, and Martin J. Whiting --
Part III. Environmental impact, global change and behavior. Chapter 11. Hydroregulation : a neglected behavioral response of lizards to climate change? / Elia I. Pirtle, Christopher R. Tracy, and Michael Ray Kearney
Chapter 12. Impact of human-induced environmental changes on lizard behavior : insights from urbanization / Breanna J. Putman, Diogo S.M. Samia, William E. Cooper Jr., and Daniel T. Blumstein.

Citation preview

Behavior of Lizards

Behavior of Lizards

Evolutionary and Mechanistic Perspectives

Edited by

Vincent L. Bels and Anthony P. Russell

CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2019 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed on acid-free paper International Standard Book Number-13: 978-1-4987-8272-2 (Hardback) This book contains information obtained from authentic and highly regarded sources. Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the consequences of their use. The authors and publishers have attempted to trace the copyright holders of all material reproduced in this publication and apologize to copyright holders if permission to publish in this form has not been obtained. If any copyright material has not been acknowledged please write and let us know so we may rectify in any future reprint. Except as permitted under U.S. Copyright Law, 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 Names: Bels, V. L. (Vincent L.), editor. Title: Behavior of lizards : evolutionary and mechanistic perspectives / edited by Vincent L. Bels, Institut de Systematique Evolution Biodiversite (ISYEB), Museum national d’Histoire naturelle, CNRS, Sorbonne Universite, Paris, France, Anthony P. Russell, Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada. Description: Boca Raton, Florida : CRC Press, [2019] | Includes bibliographical references and index. Identifiers: LCCN 2018049024 | ISBN 9781498782722 (hardback : alk. paper) | ISBN 9781498782739 (e-book) Subjects: LCSH: Lizards--Behavior--Evolution. | Lizards--Adaptation. Classification: LCC QL666.L2 B46 2019 | DDC 597.95—dc23 LC record available at https://lccn.loc.gov/2018049024 Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com

The Editors wish to dedicate this volume to the memory of their friend and colleague Kenneth Victor Kardong (February 7, 1943–December 2, 2018). Ken was a source of inspiration to both of us through his studies of squamate morphology and behavior.

Contents Acknowledgments..............................................................................................................................ix Editors................................................................................................................................................xi Contributors.................................................................................................................................... xiii Introduction: The Characterization and Evolution of Lizard Behavior..............................................1 Vincent L. Bels and Anthony P. Russell Part I “Everyday” Behavior Chapter 1 Behavioral Thermoregulation in Lizards: Strategies for Achieving Preferred Temperature........... 13 Ian R. G. Black, Jacob M. Berman, Viviana Cadena, and Glenn J. Tattersall Chapter 2 Lizard Locomotion: Relationships between Behavior, Performance, and Function........................ 47 Timothy E. Higham Chapter 3 Lizard Foraging: A Perspective Integrating Sensory Ecology and Life Histories........................... 87 Chi-Yun Kuo, Martha M. Muñoz, and Duncan J. Irschick Chapter 4 Predatory Behavior in Lizards: Strategies and Mechanisms for Catching Prey............................ 107 Vincent L. Bels, Jean-Pierre Pallandre, Sébastien Charlier, Aurélie Maillard, Pierre Legreneur, Anthony P. Russell, Anne-Sophie Paindavoine, Leïla-Nastasia Zghikh, Emeline Paulet, Emilie Van Gysel, Christophe Rémy, and Stéphane Montuelle Chapter 5 Antipredator Behavioral Mechanisms: Avoidance, Deterrence, Escape, and Encounter............... 143 Eric J. McElroy Part II Social Behavior and Communication Chapter 6 The Physiological Control of Social Behavior in Lizards.............................................................. 191 Rachel E. Cohen and Juli Wade

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Chapter 7 Sensory Processing in Relation to Signaling Behavior..................................................................207 Leo J. Fleishman and Enrique Font Chapter 8 Phylogeny and Ontogeny of Display Behavior............................................................................... 259 Michele A. Johnson, Ellee G. Cook, and Bonnie K. Kircher Chapter 9 Behavioral Ecology of Aggressive Behavior in Lizards................................................................. 289 Martin J. Whiting and Donald B. Miles Chapter 10 Stable Social Grouping in Lizards.................................................................................................. 321 Geoffrey M. While, Michael G. Gardner, David G. Chapple, and Martin J. Whiting Part III Environmental Impact, Global Change, and Behavior Chapter 11 Hydroregulation: A Neglected Behavioral Response of Lizards to Climate Change?................... 343 Elia I. Pirtle, Christopher R. Tracy, and Michael Ray Kearney Chapter 12 Impact of Human-Induced Environmental Changes on Lizard Behavior: Insights from Urbanization���������������������������������������������������������������������������������������������������������������������������������� 375 Breanna J. Putman, Diogo S. M. Samia, William E. Cooper Jr., and Daniel T. Blumstein Taxonomic Index��������������������������������������������������������������������������������������������������������������������������� 397 Subject Index���������������������������������������������������������������������������������������������������������������������������������� 401

Acknowledgments This book is the result of contributions from experts in the field of lizard behavior. It covers a broad range of “everyday” and social behavior of these vertebrates. The chapters cover many, but not all, of the behavior of these animals. Throughout the book, attention is given to the impact of anthropogenically induced environmental challenges—from the effects of climate modification to habitat perturbation—on lizard behavior. The book was conceptualized by Vincent L. Bels (Muséum national d’Histoire naturelle, Paris, France), who then asked Anthony P. Russell (University of Calgary, Calgary, Alberta, Canada) to join him as coeditor, providing them with an excellent opportunity to work together on this project devoted to the understanding of lizard behavior. This volume would not have been possible without the work of all of its contributors and reviewers. We are indebted to all of them and acknowledge their dedication, patience, understanding, and comprehension. Our greatest thanks go to all the authors. We express further gratitude to the following colleagues who reviewed one or more of the ­chapters, providing excellent insights and contributing to substantial improvement of all of the ­contributions: Michel Baguette, Muséum national d’Histoire naturelle, Paris, France; Aaron Bauer, Villanova University, Villanova, Pennsylvania, United States; Philip Bergmann, Clark University, Worcester, Massachusetts, United States; William E. Cooper, Indiana University–Purdue University Fort Wayne, Fort Wayne, Indiana, United States; Dale DeNardo, Arizona State University, Tempe, Arizona, United States; Stanley Fox, Oklahoma State University, Stillwater, Oklahoma, United States; Robert Heathcote, University of Exeter, Exeter, Devonshire, UK; Anthony Herrel, Muséum national d’Histoire naturelle, Paris, France; Timothy E. Higham, University of California, Riverside, California, United States; Jerry Husack, University of St. Thomas, St. Paul, Minnesota, United States; Michele A. Johnson, Trinity University, San Antonio, Texas, United States; Michael Ray Kearney, University of Melbourne, Melbourne, Victoria, Australia; Tiana Kohlsdorf, Universidade de São Paulo, São Paulo, Brazil; John Lewellyn, James Cook University, Townsville, Queensland, Australia; Eric J. McElroy, College of Charleston, Charleston, South Carolina, United States; Martha M. Muñoz, Virginia Tech, Blacksburg, Virginia, United States; George Lawrence Powell, University of Calgary, Calgary, Alberta, Canada; Anthony P. Russell, University of Calgary, Calgary, Alberta, Canada; Glenn J. Tattersall, Brock University, St. Catharines, Ontario, Canada; Juli Wade, Minnesota State University, Mankato, Minnesota, United States; and Geoffrey M. While, University of Tasmania, Sandy Bay, Tasmania, Australia. We are also grateful to Dr. Jean-Pierre Pallandre who provided the images for the cover. Finally, we are pleased to thank John Sulzycki for his support and help through the approval process at Taylor & Francis and are also very grateful to Alice Oven, Jennifer Blaise, and Lara Spieker for their invaluable help in the editorial and production processes of the book.

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Editors Vincent L. Bels was born in Verviers, Belgium. He completed his PhD at the University of Liège (Liège, Belgium) using the combined approaches of classical ethology and functional morphology. He used lizards as a key model to investigate the process of behavioral ritualization. He was research fellow and then assistant at the University of Liège for more than 10 years following which he taught biology, zoology, and ecology for more than 10 years, and developed an applied research program on feeding behavior in domestic animals at the Hautes Ecoles (Hainaut, Belgium) and its associated Agronomic Centre. He became professor at the Muséum national d’Histoire naturelle (Paris, France) in 2005 and in this capacity served as joint director of a Mixed Research Unit (Centre National de Recherche Scientifique [CNRS]/Muséum national d’Histoire naturelle, France) for over 7 years. He has been serving as a member of the Scientific Committee of the Muséum national d’Histoire naturelle for 8 years and currently serves as a member of the Scientific Sections of the CNRS for the same period. He has authored more than 80 peer-reviewed articles, ten chapters, and six books. The major theme of his research publications is the study of feeding, drinking, and displaying in lizards, although he has also published some papers on feeding and locomotion in fishes, lizards, and birds. His main objective is the integration of behavioral and morphological studies into a comprehensive understanding of the “form–function” complex as it relates to the evolution of the trophic system of vertebrates. Anthony P. Russell was born in London. He completed his BSc at the University of Exeter, and his PhD at the University of London, UK. Upon completion of his PhD, he took up a short teaching appointment at the University of Botswana, Lesotho and Swaziland, Roma, Lesotho before beginning his work at the University of Calgary, Calgary, Alberta, Canada, during which time he served for 6 years as head of the department of biological sciences. After 40 years of teaching various aspects of vertebrate biology and evolutionary biology, he retired from his faculty position in 2013 but continues with his research. He has authored more than 300 peer-reviewed scientific articles, 19 chapters, and three books. Although he has published on many groups of vertebrates, the continuing focus of his research has been the structure, function, and evolution of geckos. His field work has taken him to Australia, New Zealand, many islands in the Eastern Caribbean, Namibia, and, most recently, Trinidad and Tobago. He has received recognition for his contributions including the Natural Sciences and Engineering Research Council (NSERC) 25 Years of Excellence Award, the Alberta Foundation for Environmental Excellence Award, and the University of Calgary Distinguished Faculty Award. Outside the University, he has served as president of the Canadian Society of Zoologists and president of the International Society of Vertebrate Morphologists.

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Contributors Vincent L. Bels Institut de Systématique Evolution Biodiversité (ISYEB–UMR 7205) Département Origin and Evolution Muséum national d’Histoire naturelle, Sorbonne Université Paris, France Jacob M. Berman Department of Biological Sciences Brock University St. Catharines, Ontario, Canada Ian R. G. Black Department of Biological Sciences Brock University St. Catharines, Ontario, Canada Daniel T. Blumstein Department of Ecology and Evolutionary Biology University of California, Los Angeles Los Angeles, California Viviana Cadena Department of Biological Sciences Brock University St. Catharines, Ontario, Canada David G. Chapple School of Biological Sciences Monash University Melbourne, Victoria, Australia Sébastien Charlier Institut de Systématique Evolution Biodiversité (ISYEB–UMR 7205) Sorbonne Université Paris, France

William E. Cooper Jr. Department of Biology Indiana University–Purdue University Fort Wayne Fort Wayne, Indiana Leo J. Fleishman Department of Biology Union College Schenectady, New York Enrique Font Instituto Cavanilles de Biodiversidad i Biologia Evolutiva Universitat de Valencia Valencia, Spain Michael G. Gardner School of Biological Sciences Flinders University Adelaide, South Australia, Australia and Evolutionary Biology Unit South Australian Museum Adelaide, South Australia, Australia Emilie Van Gysel Laboratoire d’Histologie Institut des BioSciences Université de Mons Mons, Belgium Timothy E. Higham Department of Evolution, Ecology, and Organismal Biology University of California, Riverside Riverside, California

Rachel E. Cohen Department of Biological Sciences Minnesota State University, Mankato Mankato, Minnesota

Duncan J. Irschick Department of Biology University of Massachusetts Amherst Amherst, Massachusetts

Ellee G. Cook Division of Biological Sciences University of Missouri Columbia, Missouri

Michele A. Johnson Department of Biology Trinity University San Antonio, Texas xiii

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Contributors

Michael Ray Kearney School of BioSciences The University of Melbourne Parkville, Victoria, Australia

Martha M. Muñoz Department of Biological Sciences Virginia Tech Blacksburg, Virginia

Bonnie K. Kircher Department of Biology University of Florida Gainesville, Florida

Anne-Sophie Paindavoine Laboratoire d’Histologie Institut des BioSciences Université de Mons Mons, Belgium

Chi-Yun Kuo Department of Biology Ludwig Maximilian University of Munich Munich, Germany Pierre Legreneur Laboratoire Inter-universitaire de la Biologie de la Motricité (LIBM) Université de Lyon Villeurbanne Cedex, France Aurélie Maillard Muséum national d’Histoire naturelle Institut de Systématique Sorbonne Université Paris, France and Laboratoire d’Histologie Institut des Biosciences Université de Mons Mons, Belgium Eric J. McElroy Department of Biology College of Charleston Charleston, South Carolina Donald B. Miles Department of Biological Sciences Ohio University Athens, Ohio Stéphane Montuelle Department of Biomedical Sciences Ohio University Athens, Ohio

Jean-Pierre Pallandre Institut de Systématique Evolution Biodiversité (ISYEB–UMR 7205) Département Origin and Evolution Muséum national d’Histoire naturelle, Sorbonne Université Sorbonne Université Paris, France Emeline Paulet Laboratoire de Zoologie Institut des BioSciences Université de Mons Mons, Belgium Elia I. Pirtle School of BioSciences The University of Melbourne Melbourne, Victoria, Australia Breanna J. Putman Department of Ecology and Evolutionary Biology University of California, Los Angeles Los Angeles, California and Section of Herpetology The Natural History Museum of Los Angeles County Los Angeles, California Christophe Rémy Musée d’Histoire Naturelle de Tournai Tournai, Belgium

Contributors

Anthony P. Russell Department of Biological Sciences University of Calgary Calgary, Alberta, Canada

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Juli Wade Departments of Psychology and Integrative Biology Michigan State University East Lansing, Michigan

Diogo S. M. Samia Department of Ecology Bioscience Institute University of São Paulo São Paulo, Brazil

Geoffrey M. While School of Biological Sciences University of Tasmania Sandy Bay, Tasmania, Australia

Glenn J. Tattersall Department of Biological Sciences Brock University St. Catharines, Ontario, Canada

Martin J. Whiting Department of Biological Sciences Macquarie University Sydney, New South Wales, Australia

Christopher R. Tracy Department of Biological Science California State University Fullerton Fullerton, California

Leïla-Nastasia Zghikh Laboratoire d’Histologie Institut des BioSciences Université de Mons Mons, Belgium

Introduction The Characterization and Evolution of Lizard Behavior Vincent L. Bels Muséum national d’Histoire naturelle

Anthony P. Russell University of Calgary

CONTENTS References...........................................................................................................................................6 Effective behavioral traits are crucial to the survival and reproduction of animals. Understanding the behavior of a given group of organisms allows us to gain insights into the ways in which species arise, change, and multiply. As stated by Irschick and Higham (2016), “…Animals exhibit behaviors and functional capacities that are “emergent” properties at the organism level….” Empirical approaches to the understanding of the proximate and ultimate causes of behavior help us to gain a deeper understanding of the ecological relationships and evolutionary patterns exhibited by a given group of animals. Behavior as a term encompasses everything from the responses of any animal to the ­totality of all the ecological circumstances it encounters (that is, Basic Ethology) to the responses to the entirety of evolutionary processes that impinge upon it throughout its life (that is, Behavioral Ecology). Behavior has been defined as “…The manner in which a person, … acts under specified conditions, or circumstances, or in relation to other things…” (Barrows, 2017). Tinbergen (1952), one of the founders of Ethology, defined behavior as “…The total movements made by an intact animal….” His credo of exploring the questions How? and Why? animals behave constitutes the basis for understanding the responses that play important roles in the adjustment of animals to changing environments. Collocot and Dobson (1974) characterize behavior as “…all observable, recordable or measurable activities of a living animal…due to the animal’s interactions with, or reactions to, its environment….” From the very beginning of studies of animal behavior, there has been extensive investigation of the central role that it plays in adaptability versus adaptation of animals in response to the influences of natural and sexual selection (Tinbergen, 1952; Lorenz, 1965; Nordell and Valone, 2014). Many studies have demonstrated that morphological and physiological systems play key roles in the ways in which behavior is carried out. Lizards represent one of the key focal groups for such ­studies (Pianka, 1973; Losos and Sinervo, 1989; Losos, 1990, 2011; Kardong et al., 1996; Bels, 2003; Pianka and Vitt, 2003; Schulte et al., 2004; Goodman et al., 2008; Johnson et al., 2008; Vitt and Pianka, 2014; Evans et al., 2017; Garland and Albuquerque, 2017; Hagey et al., 2017). 1

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BEHAVIOR OF LIZARDS

Although lizards are a paraphyletic assemblage (when snakes are excluded, which they are for the most part here), their diversity, disparity, and broad geographic and ecological distributions make them excellent subjects for comparative investigations. They have been employed to study a broad range of biological questions related to evolution, ecology, physiology, and morphology, and have been investigated with regard to these at a variety of spatial and temporal scales, from the individual to the community. This volume illustrates why lizards have become an important assemblage for enhancing our general understanding of evolutionary and adaptive behavioral mechanisms. Their behavior has been the subject of many studies and has been reviewed in various books, many of which focus either on specific groups of lizards (see, e.g., Auffenberg, 1988, 1994; King et al., 1999; Alberts et al., 2004; Losos, 2011; Tolley and Herrel, 2013) or on specific questions relating to their behavioral biology and ecology (see, e.g., Huey et al., 1983; Schwenk, 2000; Cooper, 2004, 2015; Bels et al., 2003; Reilly et al., 2007, 2015). In developing their understanding of the evolution of behavior (particularly that related to the origin of communication), ethologists in the 1960s divided behavior into two main categories: “everyday” behavior and behavior associated with communication. Such a division is still largely evident (whether clearly indicated or not) in studies of lizard behavior, and these categories tend to be investigated in quite different ways. “Everyday” activities relate to survival in the ­context of the management of physiological functions, such as thermoregulation and hydroregulation, and ­predator–prey interactions (involving escape, locomotion, exploration, foraging, and feeding) (Barrows, 2017). The evolution of communication and social behavior, and their neuromotor control, form the basis of studies exploring how intraspecifically important aspects of behavior impact the lives of lizards (Carpenter, 1969, 1982; Crews, 1975; Greenberg, 1977; Jenssen, 1977; Greenberg et al., 1984; Fleishman, 1988, 2000; Font and Kramer, 1989; Wade, 1997, 2011; Fox et al., 2003; Ord and Martins, 2006; Johnson et al., 2008; Johnson and Wade, 2010). In this book, we address the entire gamut of lizard behavioral responses. Lauder (1986) stated that “… the behavioral level (viewed as movements and movement sequences) is perhaps the most general level at which one might study form and function….” Since the 1980s, one of the more common paradigms underlying studies of how natural and sexual selection mold the responses of animals to the constraints imposed by their environment has been that involving the integration of morphology, performance, behavior, and fitness (Arnold, 1983; Garland and Losos, 1994; Irschick and Higham, 2016). For example, among vertebrates, Anolis lizards constitute one of the most intensively studied clades of tetrapods for which ­morphology, physiology, and behavior have been integrated in order to gain a deeper understanding of the mechanisms of diversification (Williams, 1972, 1983; Jenssen, 1977; Moermond, 1979; Ord and Martins, 2006; Harrison et al., 2015; Sathe and Husak, 2015; Baeckens et al., 2018). Natural selection acts directly upon how an animal or a group of animals behaves. For example, individual predators impact their intended prey by detecting, pursuing, catching, and, ultimately, killing them. If the prey individual does not perform effectively enough to escape from, or defend against, the predator, it will be caught and consumed. Thus, potential prey cannot survive if they do not carry out a complex array of behavioral responses such as either being able to accelerate rapidly and attain high escape speed (permitting them to flee) or, contrastingly, to avoid movement and express particular colors and hues (enabling them to blend with their environmental circumstances so as to avoid detection). Sexual selection on males is based on competition, and on females is based on the selection of the more attractive partners with which to mate and produce offspring. The behavioral repertoires of sexual competitors and partners often incorporate a wide array of performances expressed as stereotyped, ritualized actions (Carpenter and Grubitz, 1961; Carpenter, 1969, 1982; Jenssen, 1977; Bels, 1992; Ord and Blumstein, 2002; Ord et al., 2002; Ord and Martins, 2006), such as the push-ups and dewlap erection of some lizards, which may or may not be associated with particular morphological features (such as a highly modified hyoid apparatus).

Introduction

3

Behavior relating to survival and reproduction can be characterized by performances that can be explored “… operationally by laboratory measurements, generally index[ing] an animal’s ability to do something when pushed to its morphological, physiological, or biochemical limits. (Whether animals routinely behave at or near physiological limits under natural conditions is an important empirical issue for which precious few data exist…)” (Garland and Losos, 1994). Such performances are constrained by a combination of historical (phylogenetic) and ecological factors, as emphasized by Wainwright (2007) who states: “… It is generally accepted that organismal performance traits are a major target of natural selection (performance being the ability of individuals to do the tasks that fill their lives).” In such conceptual approach, all aspects of behavior play a role in determining fitness through their roles as a potential “filter” at determined moments and places for both natural and sexual selection, on the one hand, and measurable performance, on the other (Garland and Losos, 1994). This not only concerns the behavior of individual organisms, but also groups of them (such as lizards feeding in social groups). The nature and effectiveness of group behavior, like the behavior of individuals, can be assessed by its performance at particular moments and places. This deterministic approach to behavior is evident in all of the chapters in this book. A typical day in the life of a lizard may involve achieving optimal thermoregulation, finding food and feeding, engaging in various social activities such as courtship, mating, and territory defense, while at all times attempting to avoid falling victim to predators. All behavior is based upon actions driven by complex neuromotor control (Katz, 2016) that bring about thermoregulatory, locomotor, foraging, feeding, and escape activities. Communication-focused behavior is often associated with “ritualized” modal or fixed action patterns (MAPs/FAPs) that are triggered by input received by dedicated sensory pathways such as vision, and vomerolfaction in lizards (Carpenter, 1982; Bels et al., 1995; Bels, 2000; Fleishman, 2000; Vicente and Halloy, 2017). Both “everyday” and social behaviors rely on complex sensory input and motor patterns that may be modulated through cognition. Some aspects of behavior can be altered during the life of the individual and some are under strict physiological (e.g., hormonal) control and depend upon aspects of basic p­ hysiology (such as temperature and water balance). The integration of the study of everyday and social behavior of lizards will enhance our ­understanding of mechanisms of evolution and adaptation. Pioneering work of this sort has been conducted on anoles (see above), and these have become a major model for investigating evolutionary mechanisms of organisms. Such integrative approaches are now being adopted for the study of other branches of the lizard radiation, as is evidenced by work published in the last ten years. This volume provides a contemporary overview of our knowledge of advances in behavioral studies of lizards. We hope that it will encourage discussion of the conceptual and methodological approaches employed in their pursuit. The various chapters include the exploration of key questions that have arisen in the last ten years, these studies often being facilitated by newly available technical approaches and emergent novel conceptual frameworks. New insights from comparative studies in relation to various other biological disciplines have permitted an integration of questions about adaptive and evolutionary mechanisms of behavior that enhance our understanding of the behavior of lizards in relation to changing environments. The included chapters are arranged such that the fundamental everyday behaviors are covered first, followed by aspects of social behavior and communication. The final section of the book explores some of the challenges that lizards face as a result of environmental change at both local and global scales. The following outlines the general content and emphasis of the book’s chapters and points out some of the ways in which they interrelate. Because they are poikilothermic ectotherms, lizards are dependent upon a suite of behavioral attributes that allow them to attain and maintain body temperature within a well-circumscribed preferred range. Because of this, thermoregulatory behavior underpins the effectiveness of all other behavioral activities. Chapter 1 considers the means by which lizards go about achieving and regulating their preferred body temperature, and how such behavior influences other aspects of their

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BEHAVIOR OF LIZARDS

behavioral repertoire. Consideration is given to the methodological challenges involved in studying behavioral thermoregulation in the laboratory, and the even greater challenges that are evident when studying it in the field. As with other aspects of behavior (considered in other chapters), changes in thermoregulatory behavior may be induced as a result of growth, reproductive state, the degree of hydration, and the influence of metabolic stress. Thus, thermoregulatory behavior is plastic and adaptable throughout the life of the individual. Such plasticity and adaptability to changing circumstance is a theme evident in almost all of the included chapters. The long-term adaptability of thermoregulatory behavior is explored in relation to rapid global climate change. Building upon aspects governed by thermoregulatory behavior, Chapter 2 considers locomotor behavior and performance in lizards, with an emphasis on foraging, predator escape, and social interactions, topics that form the substance of subsequent chapters. Performance measures relating to speed, acceleration, endurance, and maneuverability are dependent upon body temperature and are issues thought to be critical to the determination of fitness, because they relate to the ability to avoid being preyed upon by other organisms, and to the effectiveness of foraging. Various morphological specializations are known to permit the exploitation of particular habitats and substrata, and the relationship between these and specializations of locomotor behavior are discussed, and compromises and trade-offs that result from locomotor specialization are examined in the context of locomotor behavior. The influence of habitat structure on locomotor behavior is extensive, and Chapter 2 considers how the physical environment affects movement and distribution patterns, including that of dispersion across the landscape. The defensive strategy of caudal autotomy is widespread among lizards, and its impacts (and those of tail regeneration) on locomotor behavior and survival potential are explored. Consideration of locomotor behavior provides the backdrop for exploring the behavioral patterns exhibited during foraging, which is the subject of Chapter 3. Sensory modalities (visual, auditory, chemical, and thermal) are examined in terms of the ways in which foraging is carried out along the behavioral continuum between, at the extremes, sit-and-wait and active foragers. Aspects of the structure of the physical habitat impact sensory input during foraging. Life history aspects, such as the influence of ontogenetic change, and more transient factors affecting body mass, such as water retention and caudal autotomy, are addressed in terms of how they affect foraging effectiveness. The behavioral associations of prey capture are the subject of Chapter 4, which considers the link between locomotion and foraging and the behavior associated with the deployment of the trophic apparatus (the jaws and tongue). The approach, adjustment, and capture phases of prey acquisition involve the coordination of locomotor and jaw/tongue actions, the integration of which is mediated by information received through sensory input. When seeking prey, vigilance regarding the possibility of being preyed upon must be maintained, so additional behavioral coordination is evident, the consequences of which are considered further in Chapter 5. Prey detection and identification via visual and/or chemical inputs compliments the behavioral cascade evident in foraging presented in Chapter 3. The means of physically contacting the prey and drawing it into the mouth are integrated with whole body movements brought about by the locomotor system and the head/ neck complex, which collectively maneuver the trophic apparatus into a position that enables successful food capture and consumption. The means by which lizards avoid being captured, and ultimately dispatched and consumed, while carrying out their everyday and social activities is the subject of Chapter 5. A decision-tree framework is used to indicate the behavioral options open at each stage of a potential predator–prey interaction, with different responses being invoked as the interaction between predator and prey intensifies. This behavior is counterpoint to that considered in Chapters 3 and 4, in which the lizard is the predator, not the intended prey; thus, the sensory modalities used to detect predators are influenced by habitat structure, and escape tactics are related to locomotor capabilities. The energetic costs of various behavioral responses contribute to the choice of response adopted. Linkages to the locomotor attributes considered in Chapter 2 are evident, and aspects of aggressive response (should

Introduction

5

close encounter or capture occur and escape is attempted) provide connections to the subject matter of Chapter 9. Chapter 6 marks the transition between the cluster of five chapters (Part I of the book) that deal largely with behavior related to “everyday” activities, and a cluster of five chapters (Part II) that deal more with social behavior and communication, which may be employed frequently or only occasionally, depending upon species-specific characteristics and ecological circumstances. The everyday behavioral responses considered in the first five chapters are often co-opted into aspects of these social and signaling behavioral patterns. The importance of studying lizards to gain a more complete understanding of the physiological control of social behavior is explored in Chapter 6, with the case being made that the wide array of distinctive social behavior, sex-determining mechanisms, and prevalence of unisexual species that they display provide excellent opportunities for characterizing critical behavioral processes. Both reproductive and signaling behaviors are underpinned by hormonal control. The location of the hormone receptor sites in the brain has provided insights into the regulation and ontogeny of sexual behavior through physiological means. Relatively few lizard species have been investigated in detail in this regard, and an increased representation of examples from across the lizard tree holds great promise for adding to our understanding of this area. The relatively poor representation of lizard species studied from the perspective of the ­physiological control of social behavior stands in stark contrast to the phylogenetically rich and diverse coverage of their display behavior, which is considered in Chapter 7. Complex and diverse behavioral patterns are evident across the lizard radiation. Display behavior in lizards involves ­signaling via stereotyped body movements, called ritualized behavior (Carpenter, 1982), the employment of ornaments of various kinds, and the use of vocalizations and chemical secretions. Ecological context is important in the shaping of patterns of display. The sensory modalities involved in receipt and processing of the signals transmitted during display behavior are the subject matter of Chapter 8. The ontogenetic development of signaling and response, and the signaling behavior employed by females and juveniles have received much less attention than the often-flamboyant signals that characterize males. The diversity and complexity of signaling behavior (Chapter 7) is examined in Chapter 8 from the perspective of the receipt of those signals and the behavior triggered by them. The manner in which incoming signals are perceived has influenced their evolution. The sensory modalities mentioned in earlier chapters (in relation to locomotion and foraging) are further explored with regard to how the messages contained in incoming signals are decoded and interpreted. The role of aggressive behavior is presented in Chapter 9, and its influences on the ­establishment of social systems and the structuring of populations are explored. Whereas Chapters 7 and 8 deal with signaling largely from the perspective of the cohesive aspects of social behavior, Chapter 9 explains how negative behavior plays an important role in the lives of lizards. Aggressive signals can be directed at conspecifics, as in territory defense, or at members of other species as, for example, when attempting to ward off a predator (as described in Chapter 5). Signals of aggression may be visual, chemical, or auditory, and their intensity can vary according to the magnitude of the perceived threat. There is an ontogenetic trajectory to the expression of aggressive behavior, and within populations, the degree of aggressiveness may also be a personality trait. Evolutionarily aggressive behavior plays roles in accessing various resources, in sexual selection, and in social selection. With regard to the latter, it plays a significant role in the establishment of parental care and social grouping, which are explored in Chapter 10. As social groupings become established, the mutual dependence of individuals on each other becomes important. Although lizards are generally regarded as not exhibiting much in the way of stable complex social grouping, Chapter 10 establishes that research conducted over the last 30 years has revealed that such aggregations are both functionally and phylogenetically diverse among them. The behavioral shifts that lead to and maintain stable social groupings involve a diminution of

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intraspecific aggression and home range defense, a general absence of the bright colors typical of territorial species, and the development of chiefly chemical signals, perceived through vomerolfaction, that serve to support group cohesion. Benefits of cooperating rather than competing accrue in association with particular life history traits, such as increased longevity, delayed maturity, and extensive reproductive investment in relatively few offspring. Stable social groupings are stabilized through relatedness, and particular ecological factors, such as resource availability, the increased probabilities of contact, and the collective use of permanent shelter sites also favor their evolution. Part III of this book consists of two chapters that address how global climate change and human environmental impact affect lizard behavior. Most of the preceding chapters consider some of the ways in which these phenomena are impacting the behavior of lizards, and all of the areas covered by them could have been elaborated upon in the context of Part III. We have chosen, however, to explore such issues through two avenues of inquiry. The first explores an emergent physiological challenge that is likely to be manifested worldwide as a result of global warming. This concerns water availability and water relations (Chapter 11). The second relates to how the built environment and human activities make incursions into lizard habitat (Chapter 12). It examines challenges associated with environmental change that is more directly human-mediated. The effects of these may be localized, but may also be repeated from place to place. Water is a fundamental necessity of life, and must be physiologically regulated to ensure survival. This entails the employment of behavior consistent with effective water conservation. The authors of Chapter 12 adopt a quantitative and qualitative modeling approach to the projected impacts of global temperature increases, their effects on water balance, and how these affects may be buffered through physiological and behavioral mechanisms. Various scenarios for such ­adjustments are examined in relation to their potential effectiveness in achieving these ends, and potential trade-offs between behavioral regimes to bring them about are explored. Hydroregulation is assessed in relation to associated physiological and ecological challenges. The resulting prediction is that different lizard species may be affected in quite different ways by the same broad-scale environmental challenges because of their current ecological adaptations. Human-induced rapid environmental change and its impacts on lizards and lizard populations is the subject of Chapter 12. Behavioral responses to altered predator regimes, human activity, habitat fragmentation/loss, non-native competitors, changes in food resources, noise and light pollution, and altered thermal environments are examined in relation to the potential persistence of lizards in a given area. Mechanisms of adjustment that might promote persistence are advanced. The behavioral resources available to lizards are assessed in the context of these various challenges, leading to the recognition that some species may adapt locally, some may respond by way of phenotypic plasticity, and some may show differential sorting among personality types. In this book, we have attempt to provide a broad overview of how lizard behavior relates to the conduct of the demands of everyday life and to the complex social interactions that are necessary for species survival, persistence, and adaptability. Our coverage is not exhaustive and certain aspects of lizard behavior that could be the subject matter of complete chapters in their own right (such as dispersion, learning processes, and the genetic basis of behavior) have received only relatively brief mention in one or more of the chapters. Nonetheless, the included chapters serve as up-to-date reviews of important and exciting areas of intense research activity on this widespread and diverse “group” of animals. As the authors of the various chapters indicate, lizards have a great deal to offer as potential models for the understanding of the evolution of behavior.

REFERENCES Alberts, A.C., Carter, R.L., Hayes, W.K., and Martins, E.P. 2004. Iguanas: Biology and Conservation. Berkeley, CA: University of California Press.

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Arnold, S.J. 1983. Morphology, performance and fitness. American Zoologist 23(2): 347–361. Auffenberg, W. 1988. Gray’s Monitor Lizard. Gainesville, FL: University Press of Florida. Auffenberg, W. 1994. The Bengal Monitor. Gainesville, FL: University Press of Florida. Baeckens, S., Driessens, T., Huyghe, K., Vanhooydonck, B., and Van Damme, R. 2018. Intraspecific variation in the information content of an ornament: Why relative dewlap size signals bite force in some, but not all island populations of Anolis sagrei. Integrative and Comparative Biology, 58: 25–37. Barrows, E.M. 2017. Animal Behavior Desk Reference: A Dictionary of Animal Behavior, Ecology, and Evolution. Boca Raton, FL: CRC Press. Bels, V.L. 1992. Functional analysis of the ritualized behavioural motor pattern in lizards: Evolution of behaviour and the concept of ritualization. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 122: 141–159. Bels, V.L. 2000. Biomechanics of display behavior in Tetrapods: Throat Display in Squamates. In Biomechanics in Animal Behaviour, eds. R. Blake and P. Domenici, 125–140. Oxford: BIOS. Bels, V.L. 2003. Evaluating the complexity of the trophic system in Reptilia. In Vertebrate Biomechanics and Evolution, eds. V.L. Bels, J.-P. Gasc, and A. Casinos, 185–202. Oxford: BIOS. Bels, V.L., Gasc, J.-P., Goosse, V., Renous, S. and Vernet, R. 1995. Functional analysis of the throat display in the sand goanna Varanus griseus (Reptilia: Squamata: Varanidae). Journal of Zoology 236: 95–116. Carpenter, C.C. 1969. Behavioral and ecological notes on the Galápagos land iguanas. Herpetologica 25: 155–164. Carpenter, C.C. 1982. The aggressive displays of iguanine lizards. In Iguanas of the World: Their Behavior, Ecology and Conservation, eds. G.M. Burghardt and A.S. Rand, 215–231. Park Ridge, NJ: Noyes Publications. Carpenter, C.C., and Grubitz, G. 1961. Time-motion study of a lizard. Ecology 42: 199–200. Collocot, T.C., and Dobson, A.B. 1974. Chambers Dictionary of Sciences and Technology. London: Chambers. Cooper Jr, W.E. 2015. Escape behavior in reptiles. In Escaping from Predators: An Integrative View of Escape Decisions, eds. W.E. Cooper Jr, and D.T. Blumstein, 113–151. Cambridge: Cambridge University Press. Cooper Jr, W.E. 2004. Adaptive chemosensory behavior by lacertid lizards. In The Biology of Lacertid lizards. Evolutionary and Ecological Perspectives, eds. V. Pérez-Mellado, N. Riera, and A. Perera, 83–118. Menorca: Institut Menorquı d’Estudis, Recerca. Crews, D. 1975. Inter-and intraindividual variation in display patterns in the lizard, Anolis carolinensis. Herpetologica, 31: 37–47. Evans, J.S., Eifler, D.A., and Eifler, M.A. 2017. Sand-diving as an escape tactic in the lizard Meroles anchietae. Journal of Arid Environments 140: 1–5. Fleishman, L.J. 1988. Sensory influences on physical design of a visual display. Animal Behaviour 36: 1420–1424. Fleishman, L.J., 2000. Signal function, signal efficiency and the evolution of anoline lizard dewlap color. In Animal Signals: Signalling and Signal Design in Animal Communication, eds. Y. Epsmark, T. Amundsen, and G. Rosenqvist, 209–236. Trondheim: The Royal Norwegian Society of Sciences and Letters. Font, E., and Kramer, M. 1989. A multivariate clustering approach to display repertoire analysis: Headbobbing in Anolis equestris. Amphibia-Reptilia 10: 331–344. Fox, S.F., McCoy, J.K., and Baird. T.A. 2003. Lizard Social Behavior. Baltimore, MD: JHU Press. Garland Jr, T., and Losos, J.B. 1994. Ecological morphology of locomotor performance in squamate ­reptiles. In Ecological Morphology: Integrative Organismal Biology, ed P.C. Wainwright and S. Reilly, 240–302. Chicago, IL: Chicago University Press. Garland Jr, T., and Albuquerque, R.L. 2017. Locomotion, energetics, performance, and behavior: A mammalian perspective on lizards, and vice versa. Integrative and Comparative Biology 57: 252–266. Goodman, B.A., Miles, D.B., and Schwarzkopf, L. 2008. Life on the rocks: Habitat use drives morphological and performance evolution in lizards. Ecology 89: 3462–3471. Greenberg, N. 1977. A neuroethological study of display behavior in the lizard Anolis carolinensis (Reptilia, Lacertilia, Iguanidae). American Zoologist 17: 191–201. Greenberg, N., Chen, T., and Crews, D. 1984. Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis. Hormones and Behavior 18: 1–11. Hagey, T.J., Uyeda, J.C., Crandell, K.E., Cheney, J.A., Autumn, K., and Harmon, L.J. 2017. Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards. Evolution 71: 2344–2358.

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Harrison, A.S., Revell, L.J., and Losos, J.B. 2015. Correlated evolution of microhabitat, morphology, and behavior in West Indian Anolis lizards: A test of the habitat matrix model. Behaviour 152, 1187–1207. Huey, R.B., Pianka, E.R., and Schoener, T. 1983. Lizard Ecology, Studies of a Model Organism. Cambridge: Harvard University Press. Irschick, D.J., and Higham, T.E. eds. 2016. Animal Athletes: An Ecological and Evolutionary Approach. Oxford: Oxford University Press. Jenssen, T.A. 1977. Evolution of anoline lizard display behavior. American Zoologist 17: 203–215. Johnson, M.A., and Wade, J. 2010. Behavioural display systems across nine Anolis lizard species: Sexual dimorphisms in structure and function. Proceedings of the Royal Society of London B: Biological Sciences 277: 1711–1719. Johnson, M.A., Leal, M., Schettino, L.R. Lara, A.C., Revell, L.J., and Losos, J.B. 2008. A phylogenetic ­perspective on foraging mode evolution and habitat use in West Indian Anolis lizards. Animal Behaviour 75: 555–563. Katz, P.S. 2016. Evolution of central pattern generators and rhythmic behaviours. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 1–12. Kardong, K., Kiene, T., and Bels V. 1996. Evolution of trophic systems in squamates. Netherlands Journal of Zoology 47: 411–427. King, D., Green, B., and Knight, F. 1999. Monitors: The Biology of Varanid Lizards. Malabar, FL: Krieger Publishing Company. Lauder, G.V. 1986. Homology, analogy, and the evolution of behavior. Evolution of Animal Behavior: 9–40. Lorenz, K. 1965. Evolution and Modification of Behavior. Chicago: University of Chicago Press. Losos, J.B. 1990. Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs 60: 369–388. Losos, J.B. 2011. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. Berkeley, CA: University of California Press. Losos, J.B., and Sinervo, B. 1989. The effects of morphology and perch diameter on sprint performance of Anolis lizards. Journal of Experimental Biology 145: 23–30. Moermond, T.C. 1979. Habitat constraints on the behavior, morphology, and community structure of Anolis lizards. Ecology 60: 152–164. Nordell, S.E., and Valone, T.J. 2014. Animal Behavior: Concepts, Methods, and Applications. Oxford: Oxford University Press. Ord, T.J., and Blumstein, D.T. 2002. Size constraints and the evolution of display complexity: why do large lizards have simple displays? Biological Journal of the Linnean Society 76: 145–161. Ord, T.J., Blumstein, D.T., and Evans, C.S. 2002. Ecology and signal evolution in lizards. Biological Journal of the Linnean Society 77: 127–148. Ord, T.J., and Martins, E.P. 2006. Tracing the origins of signal diversity in anole lizards: Phylogenetic approaches to inferring the evolution of complex behaviour. Animal Behaviour 71: 1411–1429. Pianka, E.R. 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4: 53–74. Pianka, E.R., and Vitt, L.J. 2003. Lizards: Windows to the Evolution of Diversity. Berkeley, CA: University of California Press. Reilly, S.M., McBrayer, L.B., and Miles, D.B. 2007. Lizard Ecology. Cambridge: Cambridge University Press. Sathe, E.A., and Husak, J.F. 2015. Sprint sensitivity and locomotor trade-offs in green anole (Anolis carolinensis) lizards. Journal of Experimental Biology 218: 2174–2179. Schulte, J., Losos, J., Cruz, F., and Nunez, H. 2004. The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini). Journal of evolutionary biology 17: 408–420. Schwenk, K. 2000. Feeding in lepidosaurs. In Feeding. Form, function and Evolution in Tetrapod Vertebrates, ed. K. Schwenk, 175–291. San Diego: Academic Press. Tinbergen, N. 1952. The Study of Instinct. Oxford: Oxford University Press. Tolley, K.A., and Herrel, A. 2013. The Biology of Chameleons. Berkeley, CA: University of California Press. Vicente, N.S., and Halloy, M. 2017. Interaction between visual and chemical cues in a Liolaemus lizard: A multimodal approach. Zoology, 125: 24–28. Vitt, L.J., and Pianka, E.R. 2014. Lizard Ecology: Historical and Experimental Perspectives. Princeton, NJ: Princeton University Press.

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Wade, J. 1997. Androgen metabolism in the brain of the green anole lizard (Anolis carolinensis). General and Comparative Endocrinology 106: 127–137. Wade, J. 2011. Relationships among hormones, brain and motivated behaviors in lizards. Hormones and Behavior 59: 637–644. Wainwright, P.C. 2007. Functional versus morphological diversity in macroevolution. Annual Review of Ecology, Evolution, and Systematics, 38: 381–401. Williams, E.E. 1972. The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. Evolutionary Biology 6: 47–89. Williams, E.E. 1983. Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. In Lizard Ecology, Studies of a Model Organism, eds. R.B. Huey, E.R. Pianka, and T. Schoener, 326–370. Cambridge: Harvard University Press.

Part  I

“Everyday” Behavior

Chapter  1

Behavioral Thermoregulation in Lizards Strategies for Achieving Preferred Temperature Ian R. G. Black, Jacob M. Berman, Viviana Cadena, and Glenn J. Tattersall Brock University

CONTENTS Introduction....................................................................................................................................... 14 Background....................................................................................................................................... 14 The Thermal Environment........................................................................................................... 14 Biological Effects of Temperature............................................................................................... 15 Fundamentals of Thermoregulation.................................................................................................. 16 What Is Thermoregulation?.......................................................................................................... 16 Neurophysiological Control and the Characterization of Behavioral Thermoregulation............ 17 Behavioral Thermoregulation in Lizards.......................................................................................... 19 Overview...................................................................................................................................... 19 Microhabitat Selection and Shuttling........................................................................................... 19 Basking.........................................................................................................................................20 Orientation and Posture................................................................................................................20 Ventilatory Behaviors................................................................................................................... 21 Physiological Thermoregulatory Responses..................................................................................... 23 Cardiovascular Adjustments......................................................................................................... 23 Cutaneous Reflectance Adjustments............................................................................................24 Methods for Examining Behavioral Thermoregulation in the Laboratory.......................................25 Shuttle Boxes...............................................................................................................................25 Thermal Gradients........................................................................................................................28 Methodological Considerations................................................................................................... 29 Changes to Thermoregulatory Set Points.......................................................................................... 30 Overview...................................................................................................................................... 30 Physiological States: Reproduction............................................................................................. 30 Physiological States: Feeding and Digestion............................................................................... 30 Physiological States: Hydration................................................................................................... 31 Physiological States: Infection and Immunological Responses................................................... 31 Physiological States: Metabolic Stressors.................................................................................... 32 Effectiveness of Thermoregulatory Responses: Thermoregulatory Precision.................................. 32 Behavioral Thermoregulation in Nature: Placing Thermal Preference into Context........................ 35

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Conclusions and Perspectives........................................................................................................... 37 Acknowledgments............................................................................................................................. 39 References......................................................................................................................................... 39 INTRODUCTION Body temperature (Tb) is one of the most important variables in an animal’s biology because physiological processes only exhibit peak performance within a narrow thermal range (Peterson, Gibson, and Dorcas 1993; Hutchison and Dupré 1992). Body temperature itself has important implications for different aspects of an animal’s ecology and behavior, such as the ability to escape from predators and to forage (Christian and Tracy 1981; Vandamme, Bauwens, and Verheyen 1991), to digest and absorb nutrients (Pafilis et al. 2007; Secor 2009; Miller, Erasmus, and Alexander 2014), to reproduce (Luo, Ding, and Ji 2010), to compete for mates or territory (Kondo and Downes 2007), and to maintain homeostasis (Angilletta 2009). As a result, the ability to maintain a relatively constant body temperature may have direct effects on an individual’s fitness (Warner 2014). Although many of these constraints apply generally to animals with variable body temperatures, as terrestrial ectotherms, lizards live in a thermally heterogeneous environment, so temperature regulation through behavior has become an important feature. As ectotherms, lizards do not generally rely on metabolically generated heat to maintain a high body temperature, but instead depend primarily on external heat sources such as solar radiation or conductive heat transfer from the substrate for temperature regulation. As a result, lizards thermoregulate primarily through behaviors such as basking, postural changes, and shuttling (Cowles and Bogert 1944; Bennett and Ruben 1979), which alter heat transfer from or to the environment. Physiological adaptations can also aid thermoregulation, especially in lizards of large body size. The most prominent physiological mechanism is the ability to control rates of heating and cooling through cardiovascular adjustments and alterations of peripheral blood flow (see Section “Physiological Thermoregulatory Adjustments”). Furthermore, some reptiles have the capacity for modest amounts of thermogenesis (Cowles 1958; Bartholomew and Tucker 1963; Seebacher 2000; Dzialowski and O’Connor 2001; Seebacher and Franklin 2005; Tattersall et al. 2016). For example, enhanced and sustained thermogenesis has been demonstrated in the Argentine Black and White Tegu (Salvator merianae) (Tattersall et al. 2016), suggesting that behavioral thermoregulation may often be accompanied by additional features that augment thermoregulatory capacity. These physiological adaptations may allow lizards in thermally variable habitats to maintain their body temperature within their preferred range for longer periods of time, reducing the requirement for the employment of costly (in terms of predation risk and energy expenditure) behavioral thermoregulatory mechanisms (i.e., shuttling and basking) (Bartholomew and Tucker 1963; Heath 1970; Seebacher 2000; Seebacher and Grigg 2001). In this chapter, we focus primarily on the ethological aspects and proximate mechanisms of thermoregulatory behavior of lizards, occasionally drawing from research on other reptiles. BACKGROUND The Thermal Environment All animals are influenced by their environment. Influential factors range from the abiotic, such as temperature and humidity, to the biotic, such as predator and prey abundance. The type and ­magnitude of an animal’s response to environmental factors can vary between species. As the external environment fluctuates and influences an organism’s internal environment, animals either make homeostatic adjustments to keep their internal environment relatively constant or allow their

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internal environment to shift with the external environment (Hertz, Huey, and Stevenson 1993; Huey and Slatkin 1976; Huey and Stevenson 1979). Animals adopting these contrasting strategies are often referred to, respectively, as regulators and conformers. Regulators react to changes in their external and internal environments, whereas conformers either do not regulate their internal conditions or only do so under exceptional circumstances. There are no perfect conformers or regulators in the animal kingdom; instead, most species lie on a spectrum between the two extremes. Changes in external environmental factors may alter peripheral or internal states, with the changes subsequently being perceived by sensory receptors. A behavioral and/or physiological response is then evoked, which acts upon the internal environment in the opposite direction to the deviation and reestablishes homeostasis of the internal environment. From a thermal perspective, either animals will regulate their internal temperature with respect to their external environment and maintain a relatively stable body temperature (homeotherms), or their body temperature will conform with that of their environment (poikilotherms). Biological Effects of Temperature There is typically a narrow range of temperatures within which biochemical processes operate at their highest rates and efficiency. Specifically, temperature affects the kinetic energy of biochemical reactions, causing their rates to change. For this reason, remaining within a thermally optimal range is important enough for most animals to invest energy into some form of thermoregulation. Additionally, hot or cold extremes can have immediate negative consequences (i.e., freezing or protein denaturation) on an animal’s survival. Biological processes generally have critical maximum (CTmax) and minimum (CTmin) temperature thresholds, above and below which they do not function. There is also usually a particular temperature at which any given metabolic or physiological process yields maximum performance (Pmax), or a range of temperatures where the performance is nearly maximal (conventionally 95% or 80%, depending on the study; see Angilletta 2009). The Pmax combined with the CTmax and CTmin broadly defines a response curve (Figure 1.1) with maximum performance at the optimal temperature (Topt) and decreasing performance at lower and higher temperatures until the CTmax or CTmin is reached. Lower temperatures limit the energy available for chemical reactions to occur, leading to a response curve based on the “Q10 effect,” where reaction rates change two to three times for every 10°C change in temperature (Tattersall et al. 2012). Above the CTmin value, the molecular kinetic energy rises, making the likelihood of interactions between molecules and structures of the pathway higher. The decline in performance at temperatures above Topt is due to multiple causes. For example, alterations in the ionization state for critical amino acids or an alteration in an enzyme’s ability to undergo conformational changes usually occurs at elevated temperatures. Furthermore, as temperature continues to increase, protein denaturation (Somero 1995) and changes in membrane viscosity and permeability also contribute to a decline in function (Angilletta 2009). Optimal temperature can be quantified for processes at the cellular (e.g., enzyme reaction speed, membrane viscosity), systemic (e.g., digestion, reproduction, sprint speed), or whole animal (e.g., survivorship, growth rate, fecundity) level (Angilletta 2009). In the case of a thermal generalist, performance breadth can be relatively wide, with the trade-off being a relatively low maximum performance (Levins 1968). Alternatively, performance breadth can be narrow, with a relatively high maximum performance, as seen in thermal specialists (Levins 1968). The breadth of thermal environments over which life exists has led, in different species, to evolutionary adaptations of different optimal temperatures for essential life processes. For example, the level of performance in animals living at low or high temperatures is maximal at those temperatures but lower outside these ranges (Van Berkum 1988; Franklin 1998; Wilson 2001). Likewise, many studies have shown a trend in survivorship between populations of the same species living at different latitudes or altitudes, whereby survivorship is maximal at the optimal temperature of the particular population of the species (Angilletta, Steury, and Sears 2004).

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Figure 1.1  Generalized optimality curve that can be used to describe any temperature-sensitive biological process. Topt (optimal temperature) is the temperature at which Pmax (maximum performance) occurs. Performance breadth is the temperature range across which a certain percentage of maximal performance occurs. Performance breadth can be defined as anywhere from 80% to 95% of maximal performance depending on the study. CTmax (critical thermal maximum) is the maximum temperature at which a physiological trait’s performance is possible. CTmin (critical thermal minimum) is the minimum temperature at which any performance occurs.

Survivorship is, however, only one variable over which temperature shows influence. In ­contrast to survivorship, thermal optima of sprint speeds, specifically in lizards, correspond directly with operative temperatures measured in the field (Huey and Kingsolver 1993). Additionally, CTmax changes proportionately with optimal temperature in lizards, whereas CTmin can remain relatively constant across species (Huey and Kingsolver 1993). This correlation s­ uggests that the lower threshold for sprinting is limited by the energy required for muscle contraction. In contrast, the optimal temperature and upper threshold for sprinting have room for evolutionary modification or specific acclimation within a species. High- and low-temperature specialists, compared to generalists, have higher performance around a smaller range of temperatures. The benefit of being a specialist is that a relatively higher Pmax can be achieved, but body temperature must remain closer to the Topt in comparison with generalists. Specialists are, therefore, likely to thermoregulate more precisely than generalists to maintain body temperature within this narrower range. FUNDAMENTALS OF THERMOREGULATION What Is Thermoregulation? Thermoregulation is the process by which an organism maintains internal temperature homeostasis (Angilletta 2009). An organism must maintain its body within a restricted temperature range

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for optimal function, and it is through the process of thermoregulation that the required range of temperatures is achieved. Physiological thermoregulatory mechanisms are beneficial as they can be recruited regardless of the external environment; however, the trade-off is typically the high metabolic cost associated with heat production. Behavioral thermoregulation has lower ­metabolic costs than metabolic heat production (Bennett and Ruben 1979) but is constrained by an animal’s need to perform other tasks (e.g., feeding, predator avoidance, and reproductive behaviors), which limits its ability to focus solely on thermoregulation (Huey and Slatkin 1976). Endotherms often rely on behavioral thermoregulation as a result of these trade-offs, as it reduces metabolic costs and can mitigate metabolic heat production (Bennett and Ruben 1979). Regardless of the ­mechanisms, all organisms still rely on their physiological abilities to sense temperature (i.e., thermosensation), ­monitor internal and peripheral temperatures, and use the thermal information to recruit the ­appropriate thermoeffector response (Bicego, Barros, and Branco 2007). Organisms use ­thermosensation to assess their environment and seek out favorable environmental temperatures while avoiding unfavorable ones (Angilletta 2009). Neurophysiological Control and the Characterization of Behavioral Thermoregulation For historical reasons, and due to the disciplines of those who were the first to study these questions (Cowles and Bogert 1944; Cabanac, Hammel, and Hardy 1967; Hammel, Caldwell, and Abrams 1967; Heath 1970; Bogert 1949), thermoregulation in lizards has been viewed through either an ecological or a physiological lens. As a result, the literature on behavioral thermoregulation in lizards is divided between the neurophysiological and ecological realms, with investigators examining, often in isolation, proximate and ultimate contributors to behavior (Tinbergen 1963). Thermoregulatory behaviors have typically been divided into two categories: voluntary and involuntary (Heath 1970). When an animal actively tries to remain within an optimal thermal range, by moving from one thermal environment to another, it is voluntarily thermoregulating. Heath (1970) referred to voluntary thermoregulation as activity that involves directed movements and recognized this as a complex suite of behaviors related to moving between available, yet varying, thermal environments. In contrast, involuntary behaviors are those that are considered autonomic responses (Jessen 2001). One implication of this strict delineation between voluntary and involuntary thermoregulatory behaviors, however, is that ectothermic animals have little choice over certain aspects of their behavioral thermoregulatory responses, which may make laboratory measurement of behavioral thermoregulation difficult to reconcile with ecological studies of lizard thermal behavior. The simplest form of thermoregulatory control can be understood in the context of control theory (Mrosovsky 1990), which states that homeostatic responses can be regulated with either a feedback or a feedforward loop. A feedback loop is a pathway wherein a stimulus leads to a corresponding response. Essentially, a stimulus evokes a sensory response that sends a signal to the system’s controller. In the case of negative feedback, the sensory stimulus evokes an opposing regulatory response, which counters the strength of the stimulus and reduces the sensory response. In the case of vertebrate temperature regulation, the sensor is a thermoreceptor, which signals to the central neural controller the direction of the error signal and then activates a thermoregulatory response. There is extensive evidence indicating that neural centers in the hypothalamus are responsible for controlling body temperature in vertebrates (Berk and Heath 1975; Cabanac, Hammel, and Hardy 1967; Hammel, Caldwell, and Abrams 1967; Myhre and Hammel 1969). Work on Blue-tongued Lizards (Tiliqua scincoides) demonstrated that warming or cooling the hypothalamus induced the corresponding changes (i.e., behaviors in opposition to the direction of temperature change) in shuttling behavior (Hammel, Caldwell, and Abrams 1967). Berk and Heath (1975) further observed that

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lesions in the nucleus of the anterior hypothalamus of Dipsosaurus dorsalis caused a significant drop in mean exit body temperature when the animals were shuttling from a cold chamber to a hot chamber, lending support to the importance of hypothalamic centers with regard to thermoregulation and thermoregulatory behavior. Fitting within the context of neurophysiological control, there are two principal control mechanisms for behavioral thermoregulation: proportional control, used for fine-tuning body temperature, and on–off control, used for overt thermoregulation (Heath 1970). Proportional control involves subtle thermoregulatory behaviors that address relatively small deviations from the regulated T b and may occur over a wide range of Tb’s. It applies to behaviors whose intensity is determined by the level of thermal strain an individual can endure; the level of the thermoregulatory response is proportional to the deviation in the body temperature from the presumed T b set point (Heath 1970). Behaviors such as gaping, orientation changes, and postural adjustments all appear to be regulated by proportional control mechanisms (Heath 1970). Depending on the relative need, specific thermolytic, or heat-seeking, behaviors will be expressed at different levels. In the case of gaping, this is represented by how widely the mouth is opened and the time spent gaping. Central Bearded Dragons (Pogona vitticeps) have been shown to gape more widely at higher temperatures compared to lower ones, and to increase the amount of time spent gaping with the intensity of thermal stimulus (Tattersall and Gerlach 2005), suggesting that the effort involved in gaping produces a proportional degree of evaporative cooling at elevated temperatures. More overt behaviors, such as shuttling, operate using an on–off control system, leading to an all-or-nothing behavioral reaction. In the shuttling model, lizards will alternate between two responses to maintain a relatively narrow T b range. They will move into either a warm region to heat up or a cooler region to cool off. A typical example of this is a lizard shuttling between shade and sunlight (Heath 1970); when the lizard warms up too much and reaches its upper T b set point (USP), it moves to a cooler location and stays there until it reaches its lower Tb set point (LSP), subsequently returning to the warmer environment. The temperature that stimulates the animal to move from one environment to another is called the escape temperature (Barber and Crawford 1979), usually with respect to air or skin temperature. The upper escape temperature (UET) is typically the highest temperature reached by the lizard before moving from a warm to a colder environment. Conversely, the lower escape temperature (LET) is the lowest temperature reached by a lizard before moving from a colder to a warmer environment. At present, it is not known to what extent peripheral versus core temperature sensation drives shuttling behaviors. Such control mechanisms do not precisely allow the animal to reach its desired temperature per  se, but rather allow its temperature to fluctuate around its preferred Tb, imparting a certain degree of variation to behavioral thermoregulation. This means that lizards will strive to prevent their Tb from rising above the USP or falling below the LSP, thereby keeping them within an optimal Tb range. This allows them to take advantage of other thermoregulatory responses, such as gaping or ­orientation, whose associated costs are lower (see Section “Effectiveness of Thermoregulatory Responses: Thermoregulatory Precision”). By remaining within the zone between the USP and the LSP, called the refractory zone, lizards need not dedicate as much time to costly shuttling thermoregulatory behaviors (Heath 1970). A model proposed by Mitchell, Snellen, and Atkins (1970) integrates well with the dual threshold system involved in behavioral thermoregulation in reptiles and lizards in particular. This model suggests that a balance of incoming warm and cold sensory signals determines the appropriate thermoregulatory action. Research on lizards has already shown that artificial manipulation of one group of thermosensors (i.e., by warming or cooling the hypothalamus) does not have an immediate behavioral effect but rather shifts the threshold at which other sensors induce thermoregulatory behaviors (Hammel, Caldwell, and Abrams 1967). This model also serves as an alternative to the concept of one, central, fixed set point. However, the concept of a single set point has emerged more

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as an analogy, especially in reptiles where body temperatures fluctuate over a wide range, leading to lizard shuttling behavior being modelled as a dual threshold thermoregulatory system (Barber and Crawford 1977). Such a system has been described for a number of lizard species (Barber and Crawford 1979; Van Berkum, Huey, and Adams 1986; Cadena and Tattersall 2009), where ­shuttling is characterized by an upper and a lower temperature threshold, above and below which thermosensory information signals thermoeffectors (e.g., escape behaviors) to elicit thermoregulatory ­behavior which entails changing Tb in the opposite direction to the signal (Barber and Crawford 1977). These two thresholds can be linked to the relevant cold and warm sensors in the periphery and core, which are responsible for detecting the lower and upper thresholds, respectively. Since lizards do not generally produce endogenous heat, and since Tb is dependent on environmental conditions, these two thresholds can be described in terms of skin, body, or brain temperature (Barber and Crawford 1979; Berk and Heath 1975). One primary mechanism used in peripheral and internal temperature sensation, which appears relatively conserved across many taxa, involves transient receptor potential (TRP) ion channels (Caterina 2006). These TRP channels, which are abundantly expressed in sensory nerves and often in adjacent skin cells (e.g., keratinocytes), have been shown to respond strongly (Q10 values are vastly different from those of other ion channels) and predictably to temperature, with different TRP channels responding to different temperature ranges (Caterina 2006; Romanovsky 2007). The TRP channels also respond to a wide range of temperatures, both noxious and innocuous (Romanovsky 2007). Little research into their role in reptiles has been conducted, although Seebacher and Murray (2007) identified the expression of TRPV1 in numerous ectotherms including the Saltwater Crocodile (Crocodylus porosus) and provided evidence to suggest that TRPV1 and TRPM8 are used as both internal and peripheral temperature sensors that can influence behavioral thermoregulation.

BEHAVIORAL THERMOREGULATION IN LIZARDS Overview Thermoregulation in lizards is primarily achieved through careful exploitation of temporal and spatial gradients in environmental temperature (Bogert 1949; Seebacher and Franklin 2005). Selection of an appropriate habitat (living in a thermally favorable environment) is an important first step to maintain an optimal temperature. Other mechanisms include postural changes and regulation of activity times. Posture allows animals to alter the amount of heat absorbed from the sun (i.e., heliothermy) or the substrate (i.e., thigmothermy), while regulating activity restricts this to certain times of day when they are more likely to encounter optimal temperatures in the environment. Ectothermy, in general, entails reliance upon a repertoire of behavioral strategies to maintain an optimal body temperature. In this section, we discuss the variety of thermoregulatory behaviors exhibited by lizards. Microhabitat Selection and Shuttling The behavior that usually has the greatest impact on Tb is microhabitat selection. Finding an area with an ideal, unchanging operative temperature is unlikely; however, so many lizards that are active thermoregulators will shuttle between multiple microhabitats (Dreisig 1984; Bennett 2004; Cowles and Bogert 1944). If a microhabitat becomes too warm or too cold, the individual may shuttle to a more desirable environment. Shuttling can also occur between a large

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variety of microenvironments, such as aboveground and underground, across a gradient of several ­temperatures, or between aquatic and terrestrial situations (Bartholomew 1966; Cowles and Bogert 1944; Smith 1979). In controlled laboratory experiments on lizards, shuttling behavior is clearly defined, with animals moving back and forth regularly between areas of high and low temperatures to maintain body temperature at a moderate value between both extremes (Berk and Heath 1975; Barber and Crawford 1977, 1979; Cadena and Tattersall 2009). There is a relatively high degree of predictability within species in terms of threshold temperatures (ambient, body, skin, and brain) that elicit movement from one thermal environment to another. Quantifying shuttling behavior in the field is more problematic, as it is difficult to differentiate between thermoregulatory and other behaviors (e.g., predator avoidance and hunting) (Heath 1964b; Ribeiro et al. 2007). Basking Basking is a process by which an animal exposes itself to a heat source, like the sun, for extended periods to absorb heat energy (Bartholomew 1966; Cowles and Bogert 1944). It can be conceived of as a subset of the shuttling behaviors described above. Many lizards bask in open regions or on warm rocks or similar structures (Ben-Ezra, Bulte, and Blouin-Demers 2008; Bennett 2004; Martin et al. 1995; Shine 2006; Corbalan and Debandi 2013; Heathcote et al. 2014; Munoz et al. 2016; Patterson 1991; Werner and Goldblatt 1978). By remaining on a warm substrate, additional heat can be absorbed from the ground through conduction. It is common to see lizards basking extensively during different parts of the day, depending on their needs. Many desert lizards take advantage of the early morning sun to warm up and then avoid the sun, often by retreating to subterranean burrows during the middle of the day to avoid overheating (Buckley, Hurlbert, and Jetz 2012; Cowles and Bogert 1944). Others bask extensively before entering cooler foraging regions (Bartholomew 1966). Female Raukawa Geckos (Woodworthia maculata) exhibit basking behavior approximately 40% more frequently than males during the spring and summer months, and select higher temperatures on average (approximately 5°C higher) when gravid. Despite this, Gibson, Penniket, and Cree (2015) saw no impact of reproductive condition on the frequency of basking in these geckos. Orientation and Posture While basking and shuttling are the most effective methods for inducing a relatively large change in core temperature, other behaviors allow for finer temperature control. Preferential orientation to the sun allows lizards to make slight adjustments to body temperature while remaining within a single microhabitat. The best-documented example is that of the Marine Iguana (Amblyrhynchus cristatus) (Bartholomew 1966). By facing the sun while basking, it minimizes the amount of its surface area exposed to direct solar radiation. The surface temperatures of the barren lava rocks upon which it is often found basking can exceed 50°C, yet the iguana’s core temperature is usually below 40°C. Marine iguanas also maintain a lower T b relative to their substrate with the aid of posture and orientation. By limiting their surface area exposed to the sun and maximizing exposure to cooler winds, marine iguanas can prevent overheating while they bask on land (Bartholomew 1966). Lizards also use postural changes to aid in body temperature manipulation, in much the same way they use orientation. By choosing which body parts are in contact with hot surfaces, they can exert some control over rates of heat exchange (Bartholomew 1966). For example, by lifting body parts, such as the head or foot, off extremely hot substrates or away from warm air within the boundary layer close to the ground, lizards can cool sections that are overheating, a behavior seen in some desert species such as Anchieta’s Shovel-snouted Lizard (Meroles anchietae) of the Namib Desert (Brain 1962). The use of posture as a thermoregulatory

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strategy has also been encountered in the nocturnal Marbled Gecko (Christinus marmoratus), enabling it to thermoregulate within its retreat site during its “inactive” phase, to an extent comparable to that of diurnal animals (Kearney and Predavec 2000). In contrast, by flattening their bodies, many lizards, such as the Marine Iguana, the Bearded Dragons, and horned lizards, can expose more surface area to the sun, increasing the rate at which they absorb heat (Bartholomew 1966; Cowles and Bogert 1944; Heath 1965). Recent laboratory measurements of the Central Bearded Dragon (P. vitticeps) demonstrate a preference for orientating the head toward warm environments and the tail toward cooler environments, suggesting that these behaviors occur in the absence of solar heating and may be innate (Black and Tattersall 2017). Postural thermoregulatory behaviors have also been recorded for the Raukawa Gecko (Woodworthia maculata) of New Zealand and for two phrynosomatid lizards (Uta stansburiana and Sceloporus arenicolus) (Gibson, Penniket, and Cree 2015; Sartorius et al. 2002). W. maculata basks by exposing either the entirety or one side of its abdomen to the sun, or occasionally may bask “on-toes” or with its abdomen raised off the substrate, depending on thermoregulatory needs (Gibson, Penniket, and Cree 2015). Ventilatory Behaviors Head–body temperature differences have been known for snakes, lizards, and turtles since the 1960s (Heath 1964a; Dewitt 1967), but it was not until the 1970s that the physiological mechanisms underlying this phenomenon were studied (Webb, Firth, and Johnson 1972; Webb and Johnson 1972; Johnson 1973). These differences were shown to be due to active measures taken by the animals themselves using evaporative cooling evoked through respiratory mechanisms and were not purely due to environmental factors (Pough and McFarland 1976). Crawford et al. (1977) compared panting and non-panting lizards and provided evidence that evaporative cooling was, in fact, the primary means of establishing these head–body temperature differences. Indeed, such differences in reptiles have often been cited as examples of the precision by which ectotherms can thermoregulate (Borrell, LaDuc, and Dudley 2005; Tattersall, Cadena, and Skinner 2006), and eventually led to the conclusion that many reptiles have what can be described as “ventilatory behavioral responses.” The main respiratory patterns related to cooling are relaxed breathing through the nares, more rapid breathing through the nares (similar to panting), and breathing with an open-mouthed gape (Tattersall, Cadena, and Skinner 2006). Typically, the first two mechanisms allow for very limited heat and water loss, and reptiles use these responses the most. The openmouthed response has alternatively been referred to as panting or gaping, depending on whether or not increased ventilatory effort (i.e., breathing frequency) is readily observed. Ultimately, gaping is similar to panting in that the cooling is imparted to the animal by the evaporation of water from the mucous membranes exposed in the opened mouth. This is a relatively energetically effective way of thermoregulating, although it requires the animal to be hydrated (Parmenter and Heatwole 1975). Many lizards begin panting at temperatures at or very close to their upper critical body temperature (Heatwole, Firth, and Webb 1973), suggesting it may be employed only as a last resort against overheating; nevertheless, it could have ecological significance by increasing the tolerable exposure time in hot sun. Gaping for the purpose of thermoregulation occurs in certain lizards but is also observed in crocodilians (Tattersall, Cadena, and Skinner 2006). By opening the mouth at high temperatures, evaporative heat loss within the upper airways leads to cooling of the head, potentially preventing the brain from reaching lethal temperatures (Tattersall, Cadena, and Skinner 2006; Spotila, Terpin, and Dodson 1977; Crawford 1972). The added cooling allows lizards to spend longer periods basking before needing to move to shaded areas—a potentially more costly behavior. Tattersall and Gerlach (2005) showed that as the bearded dragon lizard increased gaping at high ambient temperatures, it decreased its head surface temperature (a proxy measure for cranial temperature) compared to

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Figure 1.2  G  raphical representation of the change in body temperature and brain temperature over time in the common chuckwalla (Sauromalus ater). Animals showed a significantly lower brain t­emperature in comparison with body temperature, and both temperatures were lower than the ambient ­temperature. This is in contrast to a model lizard, which approached the ambient temperature asymptote in both cases. (Adapted from Crawford 1972.)

body surface temperature, supporting a role for ventilatory behavior as a thermoregulatory response (Tattersall, Cadena, and Skinner 2006). Crawford (1972) also found that gaping allows the brain temperature of the chuckwalla (Sauromalus ater) to be 2.7°C lower than the ­ambient temperature (Figure 1.2). During periods of panting, brain temperature also drops far below body temperature in many other lizards (Crawford 1972; Webb, Firth, and Johnson 1972). Indeed, at lower ambient temperatures, head temperature tends to be higher than T b. This holds true until body temperature rises to a critical panting threshold, after which breathing becomes more rapid and head temperature drops down to or below Tb (Webb, Firth, and Johnson 1972). While head–body temperature differences have been observed both in the laboratory and in the field, Webb, Firth, and Johnson (1972) noted that the differences are much smaller outside of the laboratory environment. Nevertheless, it does appear that respiratory cooling could have evolved to aid in preventing high brain temperatures in reptiles (Tattersall, Cadena, and Skinner 2006). One challenge associated with interpreting thermoregulatory behaviors is that temperature is not the only factor that influences it. For example, during gaping, heat is exchanged with the environment through evaporative heat loss and, much like panting in mammals (Jessen 2001), can lead to a trade-off between thermoregulatory and osmoregulatory needs (Wolf and Walsberg 1996). Recent work by Scarpellini, Bicego, and Tattersall (2015) used salt loading to mimic the increased plasma osmolality that would accompany dehydration and, by examining the ratio of evaporative water loss to metabolic rate, found evidence that gaping contributes to total body water loss, albeit rather modestly. However, lizards that had been injected with hypertonic saline solutions spent less time gaping, the decrease in time being directly dependent upon the saline concentration. The notable drop in time spent gaping suggests that thermoregulatory behaviors that rely on water loss (Figure 1.3), such as gaping, show high sensitivity to dehydration stress (Scarpellini, Bicego, and Tattersall 2015).

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Figure 1.3  T  hermal images of bearded dragons (Pogona vitticeps) while gaping (a and c) and following suppression of gaping (b and d) with hypertonic injection of saline. Salt loading suppresses gaping behavior, reducing evaporative cooling, and results in a rise in surface temperatures of the head and body. (Data and images derived from Scarpellini, Bicego, and Tattersall 2015.)

PHYSIOLOGICAL THERMOREGULATORY RESPONSES Cardiovascular Adjustments All the behaviors mentioned above are used to facilitate thermoregulation in reptiles; however, autonomic responses also contribute. During an animal’s active and inactive periods of the day, autonomic responses increase peripheral blood flow while the animal is in warmer situations to speed up heating and decrease peripheral blood flow while the animal is in cooler situations to slow heat loss (Bartholomew and Lasiewski 1965; Dzialowski and O’Connor 2001). In other words, the rate at which a lizard warms its body may not be the same as the rate at which it cools its body (Bartholomew and Tucker 1963; Cowles 1958), leading to a hysteresis in whole-body temperature changes. These changes allow for a rapid rise in body temperature in the morning, while facilitating prolonged absorption of body heat into the later, cooler periods of the afternoon (Tattersall et al. 2016; Sanders et al. 2015). In reptiles, these changes are followed by increasing and decreasing the heart rate, referred to as heart rate hysteresis (Seebacher and Franklin 2005). This hysteresis in the heart rate–temperature relationship is often incorrectly interpreted as an initial response to temperature change, as pointed out by Seebacher and Franklin (2005), when in reality the change in heart rate is secondary to the circulatory adjustments. Nevertheless, experimental evidence suggests that these processes contribute directly to the rate of heating and cooling in lizards (Bartholomew and Tucker 1963; Grigg, Drane, and Coutice 1979; Seebacher 2000; Seebacher and Franklin 2005). Heat retention is especially important in the absence of any capacity for producing heat endogenously

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(Seebacher and Franklin 2005). Indeed, the thermal inertia observed in basking lizards can be traced to the capacity for the animals to retain body heat during cooling (Bartholomew and Tucker 1963; Seebacher 2000). The thermal hysteresis effect is often used to infer whether cardiovascular adjustments are affecting heat exchange. It can be influenced by several factors, with body size being of primary importance. A study conducted on five species of small scincid lizards by Fraser and Grigg (1984) found that physiological control over thermal conductance is essentially insignificant in small reptiles (5 kg) should also be unable to use heart rate and blood flow to control heat exchange unless they are exposed to certain environmental conditions, such as immersion in water or exposure to high winds or extensive heat radiation (Turner 1987). There should be an optimal body size for the usefulness of blood flow in heat exchange (Turner 1987). Dzialowski and O’Connor (2001) noted a similar impact of size on the effectiveness of blood flow with regard to warming and cooling, but they also observed that heat exchange rates were only noticeably changed during periods of simulated basking, as opposed to shuttling. While working with the Saltwater Crocodile (Crocodylus porosus), Franklin and Seebacker (2003) observed a clear hysteresis effect on both Tb and heart rate during the later stages of heating and cooling. However, they also saw large changes in heart rate with little to no changes in body temperature during initial stages of heating or cooling. Dzialowski and O’Connor (2001) and Franklin and Seebacker (2003) indicated that changes in heart rate represent a thermoregulatory mechanism in these animals in response to their thermal environment, but that heart rate is also partially controlled independently of Tb during heating and cooling. Finally, once reptiles reach a certain temperature threshold, they may undergo a reverse hysteresis pattern. A study of the Eastern Bearded Dragon (Pogona barbata) found that when placed in an environment that put them at risk of overheating due to excessive solar heat gain, their heart rates dropped significantly above a critical T b (>40°C), rather than continuing to rise. In contrast, the heart rate rose significantly during the cooling phase, facilitating heat loss, until Tb had fallen below the critical temperature (Grigg and Seebacher 1999). This decline in heart rate at high temperatures was argued to be a protective response to prevent further heating, which would have been exacerbated by enhancing peripheral blood flow. Clearly, some lizards employ cardiovascular adjustments to supplement their behavioral thermoregulatory responses. Cutaneous Reflectance Adjustments A visible reaction to temperature has often been observed in the skin of reptiles. The phenomenon of changing pigment density usually occurs over a longer timescale in comparison with other thermoregulatory changes but may have a noticeable impact on thermal balance. Certain species of lizard, when cooled, will adopt a darker skin tone within minutes, which allows for higher rates of solar heat absorption (Carey 1978; Cole 1943; Cowles 1958; King, Hauff, and Phillips 1994; Smith et al. 2016a, b). Conversely, upon reaching or surpassing the desired Tb, these same animals can adopt a lighter shade, thus becoming more reflective to solar heat radiation (Cole 1943; Cowles and Bogert 1944; Smith et al. 2016a, b; De Velasco and Tattersall 2008). The role of melanism in heat absorption has given rise to the thermal melanism hypothesis (TMH), which predicts that darker individuals are at greater advantage in cooler climates, as they absorb heat faster than more lightly colored individuals. Work on TMH has yielded mixed results, but there seems to be support for this hypothesis at a larger geographic scale (Clusella-Trullas et al. 2008). Changing pigment density, however, is not exclusively a thermoregulatory response and is often associated with defense, social interaction, or other necessities (King, Hauff, and Phillips 1994; Fan, Stuart-Fox, and Cadena 2014; Smith et al. 2016b).

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METHODS FOR EXAMINING BEHAVIORAL THERMOREGULATION IN THE LABORATORY Much of the evidence for behavioral thermoregulation in lizards has been derived from laboratory studies, and one of the most common metrics is preferred temperature (Tp). The Tp refers to the temperature an animal chooses when allowed to select from a wide range of temperatures. For most species, under ideal laboratory conditions, Tp is at or near the optimal physiological temperature, is equivalent to the temperature set point of the animal (Kingsolver and Huey 2008; Angilletta, Niewiarowski, and Navas 2002), and generally corresponds well to average Tb values in the field (Clusella-Trullas and Chown 2014). Tp is generally expressed as either the mean or the median of all observed body temperatures (Tb) during a determined time period. It is usually obtained through cloacal temperature probes, temperature telemeters, or data loggers implanted in the peritoneal cavity (Hertz, Huey, and Stevenson 1993). Because lizards do not thermoregulate precisely toward at one particular Tb, but instead operate effectively within a range of Tb’s (Heath 1970; Barber and Crawford 1977), the measurement of the “preferred temperature range” is also important (see Section “Neurophysiological Control and the Characterization of Behavioral Thermoregulation”). This works particularly well for larger animals that warm or cool slowly when occupying the alternating chambers of a shuttle box (see Section “Shuttle Boxes”), thus providing a chance for body temperature to remain reasonably constant, but under the behavioral control of the animal. Furthermore, shuttle boxes allow for the measurement of these escape responses repeatedly throughout a trial, thus providing, along with Tp, useful and accurate information on upper and lower temperature thresholds of individual species. Shuttle Boxes Different methodologies are available for the measurement of these temperature variables in the laboratory. One technique used to determine the thermoregulatory preference of an animal is the shuttle box (Berk and Heath 1975; Blumberg, Lewis, and Sokoloff 2002; Hicks and Wood 1985; Cadena and Tattersall 2008, 2009). In a typical shuttle box experiment, the animal is placed inside a chamber where it is given access to two adjacent compartments separated by an opening providing access to two ambient temperature choices (hot and cold in each respective compartment), with the temperature difference set empirically to the needs of the species (Figure 1.4). To maintain Tb within the limits of its preferred range, the animal must shuttle back and forth between the two chambers. By measuring the air or body temperature continuously, the shuttle box approach assesses the upper and lower temperatures at the point of exiting a chamber, which, respectively, are referred to as the UET and LET. This works particularly well for larger animals that warm or cool slowly when occupying the alternating chambers, thus allowing body temperature to remain under their behavioral control (Figure 1.5). Furthermore, shuttle boxes allow for the measurement of these escape responses repeatedly throughout a trial, thus providing useful and accurate information on upper and lower temperature thresholds of individual species, as well as Tp. In the shuttle boxes traditionally used to study temperature preferences of ectotherms, a choice of two extreme temperatures is provided to the animals (Hicks and Wood 1985; Blumberg, Lewis, and Sokoloff 2002; Myhre and Hammel 1969; Berk and Heath 1975). A problem with this design is that the requirement that the temperatures inside the compartments of the shuttle box be well above and below the animal’s normal range of preferred temperatures, and thus movement between compartments may represent distress responses rather than thermoregulatory ones. A second problem is that animals will often straddle the gap between the two compartments (Cadena and Tattersall 2009) allowing them to achieve a relatively constant Tb typically halfway between the two extremes, without exhibiting overt behavioral responses (i.e., movements or escape responses) that indicate active thermoregulation. Thus, although the animal may be effectively thermoregulating (i.e., achieving

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Figure 1.4  Photograph (a) and schematic drawing (b) of an electronic shuttle box (Cadena and Tattersall 2009). The box consists of a chamber divided into two identical compartments separated by a partition. A hole at the bottom of the partition connects the two compartments allowing for shuttling behavior. Internal walls in each of the compartments are angled to create a “funnelling” effect, which facilitates shuttling behavior. A treadle switch located on the floor between the two ­compartments detects the location of the lizard inside the box (heating or cooling ­compartment) activating ­accordingly the heating or cooling sources positioned at each end of the box. Thermometers inside each compartment allow for continuous air temperature monitoring which is fed back to the computerized control system. One compartment is kept continuously warmer than the other. Both compartments can be controlled to ramp temperature at a constant rate, slowly exposing the animal to a range of temperatures, which lead to the animal escaping (e.g., shuttling) to the adjacent compartment.

a stable Tb), assessment of this response is less obvious from the behavior, and not as easily automated. Moreover, it is possible that the animal is not thermoregulating, and the stable T b observed is merely the result of an average between the temperatures in the two compartments of the shuttle box. Lastly, it is important to consider the effect of low temperatures on lizard locomotion when using this type of shuttle box; if an animal stays in the cold chamber of the shuttle box long enough to induce lethargy, the cold chamber becomes a “cold trap” from which the animal may not be able to escape (Cadena and Tattersall 2009). A more complex type of shuttle box design is the electronically controlled ramping temperature shuttle box, commonly used in thermoregulatory studies of fish (Neill, Chipman, and Magnuson 1972; Petersen and Steffensen 2003; Staaks, Kirschbaum, and Williot 1999; McCauley 1977; Schurmann, Steffensen, and Lomholt 1991; Reynolds and Casterlin 1979), but also used in the study of lizards (Cadena and Tattersall 2009). This type of shuttle box better simulates a natural environment since it produces slow changes in temperature over time, in addition to distinct spatial differences of temperature distribution which mimic thermal refuges. Ramping temperature shuttle boxes

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Figure 1.5  R  epresentative trace (top trace) of body temperature (Tb) and selected air temperature (Ta) of a Central Bearded Dragon (Pogona vitticeps) allowed to thermoregulate inside an electronic shuttle box. Traces are plotted for a 4 h exploration period and a subsequent 8 h of experimental measurement. The exploration period is non-thermoregulatory and cannot be used to assess behavioral thermoregulation, since high rates of shuttling occur when temperatures are held at Tp. To determine an objective criterion for the exploratory, non-thermoregulatory period, lizards were provided the same opportunity to shuttle between compartments held at a constant temperature. In the bottom trace, the frequency of shuttling is depicted for 12 individuals throughout 12 h of activity inside a shuttle box, broken into two phases based on their relative activity: where 90% and 10% of shuttling occur. Air temperature was set at a constant temperature of 34.5°C (equal to previously measured Tp). Values are plotted as the averaged values for 12 individuals (+SE) for every 30 min interval during a 12 h period. (Derived from Cadena and Tattersall 2009, 2008.)

evoke shuttling behavior between warmer and cooler temperatures and simulate the continuous warming and cooling associated with basking or retreating to a shaded area evident in lizards thermoregulating in their natural habitats (Heath 1970; Cowles and Bogert 1944). The temperature of the environment is controlled by the movements of the animal between the two chambers, heating at

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a steady rate when the animal moves to one compartment and cooling at the same rate when it enters the other. Meanwhile, a constant temperature differential, maintained through electronic feedback, between the two chambers guides the animal toward a preferred temperature (Neill, Chipman, and Magnuson 1972). Therefore, by moving back and forth between the two chambers, through operant conditioning, the animal controls the temperature of its environment and, as a result, its own Tb. One of the advantages of this system is that upper and lower escape ambient temperatures can be measured (ambient temperature at which the animal exits the hot or cold chamber of a shuttle box, respectively) along with core Tb. This allows for the study of the possible role of peripheral thermal sensors (assessed via the ambient escape temperatures) in the central control of temperature regulation. Shuttle boxes are limited to studies that monitor overt shuttling behaviors. Subtle behaviors, such as orientation or gaping, are often not as readily observed within a shuttle box. In addition, shuttle boxes do not allow an animal the choice of a constant preferred Ta, limiting this technique to the collection of data on active or locomotory behaviors. Furthermore, some simple learning is required for animals to be able to thermoregulate effectively in a shuttle box, such that inactive, reclusive, or unmotivated animals may be difficult to study. While preferred temperature can be accurately estimated with a shuttle box, precision of thermoregulatory behavior is also influenced by the amount of locomotory activity required of the animals (Cadena and Tattersall 2009), such that a trade-off between movement and thermoregulation ultimately results in lizards lowering their Tp and decreasing the precision of thermoregulation. For analyzing other thermoregulatory responses, the use of thermal gradients is generally more useful. Thermal Gradients Linear thermal gradients are some of the most commonly used methods for studying temperature preferences of ectotherms (Arad, Raber, and Werner 1989; Hicks and Wood 1985; Jarling, Scarperi, and Bleichert 1989; Bennett 2004; Branco and Steiner 1999; Branco et al. 2000) and have been used since the early 1920s (Deal 1941) with little modification since then (Figure 1.6). Thermal gradients have the advantage of being straightforward and easy to construct by heating one end and cooling the other end of a highly conductive surface, such as a copper or aluminum plate or tube, which serves as the floor of the test environment. A radiant lamp can also be used to heat a region of a cage, while leaving other parts of the cage unheated, although this introduces the confounding effects of light attraction versus heat attraction. This requires consideration in experimental design (Khan, Richardson, and Tattersall 2010). When desirable, an air temperature gradient can also be achieved by using fans that direct warm and cold air at each end of the gradient. In a thermal gradient apparatus, a gradient (typically linear) of temperatures is available to the animal, allowing it to position itself in a “comfortable” environmental temperature within the chamber. Other devices, such as circular or vertical gradients, are modifications of this basic linear gradient design (Dillon et al. 2009; Flinn and Hagstrum 1998). Tp of the animal is determined by some measure of central tendency (i.e., mode, median, mean) of the T b measurements obtained over time. In contrast to dynamic shuttle boxes, temperature profiles of thermal gradients are static in nature and do not readily allow for the measurement of upper and lower temperature thresholds, unless the animals

Figure 1.6  T  hermal image of a thermal gradient chamber used to assess thermal preference in the bearded dragon (Pogona vitticeps). (Image of gradient used in Cadena and Tattersall 2009.)

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are naturally very active and explore the temperature gradient often enough to allow an objective determination of these thresholds. The thermal gradient is usually the method of choice when studying temperature preferences in small invertebrate animals (Dillon et al. 2009; Campbell 1937; Chapman 1965; Deal 1941; Yamamoto and Ohba 1984). Preferred temperature is usually evaluated by recording the location of multiple animals within the gradient at preset time intervals or after a certain length of time, from which a distribution of preferred temperatures can be derived. The general assumption in these experiments is that animals will distribute themselves evenly along the gradient if they exhibit no thermal preference and that they will congregate around a location in the gradient if a thermal preference exists. This assumption, however, implies that, in the absence of a temperature gradient, animals will not exhibit a preference for any one location within the chamber. This may not necessarily be the case, since animals may aggregate at edges of the chamber instead of distributing themselves uniformly along the apparatus when a temperature gradient is not present (Murphy and Heath 1983; Dillon et al. 2009). Further complications arise due to the very low thermal inertia of small animals, which, when they wander into the cooler section of a thermal gradient, quickly become immobilized. In cases such as this, it could be falsely concluded that this low temperature is what the animal prefers. These problems can be circumvented by testing for location biases within the testing chamber in the absence of a temperature gradient and by generating a null mathematical model for the spatial distribution of the animals within the thermal gradient apparatus. Anderson et  al. (2007) suggest developing a mathematical model that predicts the distribution of animals within the test chamber in the absence of a thermal gradient. In other words, the model takes into account the effect of temperature on locomotion and, therefore, on the final distribution of the animals within the chamber. The null model can then be compared to the actual distribution of the animals in the presence of a thermal gradient to determine if they are actively thermoregulating (Anderson et al. 2007). In general, thermal gradients are advantageous due to their simplicity, and because they allow for observation of positioning and other thermoregulatory behaviors that may influence temperature selection. However, only preferred ambient temperature, not body temperature, can be inferred by the locations of the reptiles within the gradient itself. Inferring preferred temperature in this way can be complicated if the animal in question is large enough to occupy a large range of different temperatures along the chamber. A final concern arises when trying to estimate T b using this method. Due to the existence of a refractory zone in ectotherms (a range of temperatures within which no attempts to correct Tb are made), Tb estimates obtained from thermal gradient data can be less precise compared to other Tb estimation techniques. In a thermal gradient, the lizard would cease most voluntary thermoregulation upon reaching the refractory zone (Heath 1970), and since the zone can span up to several degrees, this makes estimating the specific desired Ta and Tb more difficult. Methodological Considerations When selecting a method for studying thermal preference, it is important to consider the energetic costs associated with each of those available. This will influence the accuracy and precision to which an animal will thermoregulate both in the laboratory (Cadena and Tattersall 2009; Campbell 1985; Withers and Campbell 1985) and in the field (Huey and Slatkin 1976; Huey 1974). For example, lizards will thermoregulate more precisely and select higher temperatures in a thermal gradient or an electronic ramping temperature shuttle box than in an extreme fixed temperature shuttle box, which requires regular locomotory efforts to maintain a constant body temperature (Cadena and Tattersall 2009). Furthermore, the rate of temperature change in electronic shuttle boxes also influences thermoregulatory precision, so that, for instance, faster rates of ambient temperature change induce a decrease in thermoregulatory precision, as was found for Pogona vitticeps (Cadena and Tattersall 2009).

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CHANGES TO THERMOREGULATORY SET POINTS Overview Preferred temperature is operationally defined as the temperature at which an animal spends the majority of its time when provided a range of temperatures from which it can select freely. Although the term “preferred” implies knowledge of the animal’s cognitive state, the use of the term is so pervasive that it is generally accepted in reference to the thermal condition to which an animal will naturally return if given a choice. Nevertheless, the Tp is argued to represent the temperature at which numerous processes function at peak performance (Reynolds and Casterlin 1979; Stevenson, Peterson, and Tsuji 1985). This criterion is physiologically relevant to ectotherms. Because they are limited primarily to behavioral thermoregulation, availability of ambient temperature choices is vital to their survival. Also, while preferred temperature is generally physiologically relevant to an individual, what is optimal is not always a constant. Preferred temperature can change significantly from one season to the next (Patterson and Davies 1978; Christian, Tracy, and Porter 1983), show a large degree of plasticity within a population, and be dependent on the prenatal temperature of incubated eggs in oviparous (egg-laying) species or the temperature of the mother during gravidity in viviparous species (Shine and Harlow 1993; Alberts et al. 1997; Shine et al. 1997). There also exist many situations (toxicological, physiological, pathological, and environmental) in which preferred temperature can be altered. These are discussed in the sections that follow. Physiological States: Reproduction Temperature is a driving force in many physiological processes such as reproduction, gestation, digestion, survival, and growth (Stevenson, Peterson, and Tsuji 1985). Changes in preferred temperature occur in several situations associated with reproduction. In certain viviparous lizards, females will bask more when gravid and prefer warmer temperatures in general (Tu and Hutchison 1994; Shine 2004, 2006). Some species, however, exhibit lowered body temperature when gravid, which is believed to be due to a sensitivity of the young to higher temperatures within the female’s normal physiological range (Mathies and Andrews 1997). The Viviparous Lizard (Zootoca vivipara) shows a complex relationship between preferred temperature and locomotion throughout its period of gravidity. In the last month of gestation, activity becomes significantly diminished and preferred temperature is at its lowest. However, in the final days before birth, preferred temperature increases markedly (Le Galliard, Le Bris, and Clobert 2003). Shifts in preferred temperature are thought to provide optimal temperatures for offspring development in species with live birth and those that retain eggs through part of development (Beuchat 1988). The assumption is that thermal optima must shift depending on the point in gestation. Other stages of reproduction, such as the act of courting and mating, can also influence preferred temperature. Male garter snakes forego normal preferred temperature during courtship, resulting in a more variable body temperature than during non-mating seasons (Shine et al. 2000). Physiological States: Feeding and Digestion Feeding is another well-documented physiological function that induces a change in preferred temperature, specifically during the period of digestion. All the major ectothermic vertebrate groups (reptiles, amphibians, and fish) show altered thermal preference with changes in feeding status (i.e., fed vs. starved). Routinely, these animals seek to raise body temperature following feeding, a phenomenon known as the postprandial thermophilic response (Regal 1966; Slip and Shine 1988), which is thought to help with digestion by increasing metabolism and gut turnover rate, and significantly reducing digestion time (Secor 2009). Animals that have recently fed will raise their

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body temperature by basking more than unfed animals (Witten and Heatwole 1978; Parmenter 1981; Hammond, Spotila, and Standora 1988). Physiological States: Hydration Hydration status has a strong influence on the preferred temperature of terrestrial ectotherms. Snakes (Ladyman and Bradshaw 2003), toads (Malvin and Wood 1991), and lizards (Crowley 1987) have been shown to lower preferred temperature when faced with dehydration. This is argued to be an adaptive behavior because reduced temperature lowers metabolic rate, and consequently metabolic water loss, helping to limit water loss as much as possible. Lower temperatures also lower the water vapor pressure adjacent to the skin, thereby reducing the gradient for evaporative water loss from the skin to the (typically) drier environment. Acclimation and adaptation also play an important role in this response. Desert-dwelling animals such as the Desert Iguana (Dipsosaurus dorsalis) show a capacity to survive relatively severe dehydration without undergoing a change in preferred temperature (Dupré and Crawford 1985; Lorenzon et al. 1999). Additionally, environmental variability across the range of the Viviparous Lizard (Zootoca vivipara) results in areas of differential water availability, where individuals from more arid environments prefer warmer temperatures than those from more humid ones (Lorenzon et al. 1999). Plasma or cellular osmolarity can also affect behaviors and preferred T b (Harrison, Edwards, and Fennessy 1978; Ladyman and Bradshaw 2003; Malvin and Wood 1991). The anuran Rhinella marina has been shown to select lower ambient temperatures, and thus have lower T b, when placed in dry conditions (Malvin and Wood 1991). Selecting a lower temperature reduces the water lost due to evaporation by 42% in these animals. A similar situation is seen in the Western Tiger Snake (Notechis scutatus). When these snakes are dehydrated, they have a lower preferred T b (around 19.7°C) than their hydrated counterparts (around 26°C) (Ladyman and Bradshaw 2003). Dehydration is an important concern since many reptiles live in deserts or dry environments, in which water conservation is critical. Despite this, loss of water through evaporation can be an effective means of cooling, and evaporative heat loss, through the tongue or skin, is an integral part of an animal’s thermoregulatory strategy (DeNardo et al. 2004). The work done by Scarpellini, Bicego, and Tattersall (2015) on the desert-dwelling lizard, the Central Bearded Dragon (Pogona vitticeps), showed that when injected with hypertonic saline (to rapidly mimic dehydration without incurring the debilitating effects on condition), lizards spent proportionally less time gaping as saline concentration increased. Bearded dragons also showed altered UET and LET after being injected with the highest saline concentration, which was attributed to a decrease in the animals’ propensity to move, and a suppression of the normal thermoregulatory response (Scarpellini, Bicego, and Tattersall 2015). By gaping less, dehydrated animals avoid water loss through evaporation (Figure 1.3). The consequence of this is that head temperature rises with increasing dehydration, which suggests that cranial tissue temperature would be compromised in the face of dehydration stress. Ultimately, for lizards, hydration status and temperature regulation appear to represent a case of homeostatic systems with conflicting requirements and suggest that these traits represent a trade-off that may be resolved differently in different groups, depending on their environmental conditions. Physiological States: Infection and Immunological Responses An animal’s pathology can also contribute significantly to its preferred temperature. This is most apparent when an infection occurs. An organism can react to this with fever, resulting in a controlled rise in body temperature. In the case of ectotherms, these conditions cannot be evoked simply by physiological means, but instead manifest as a behavioral fever. Indeed, a rise in preferred temperature following bacterial infection or lipopolysaccharide injection has been observed in all

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major ectothermic vertebrate groups (Kluger 1979). Many experiments have shown that such a response increases host survival (Covert and Reynolds 1977; Casterlin and Reynolds 1977), including reptiles (Kluger, Ringler, and Anver 1975; Bernheim and Kluger 1976a, b). This may result from impairment of bacterial growth and potentially by increasing the immune response capabilities (Covert and Reynolds 1977). It is also noteworthy that some reptiles have been shown to exhibit a “hypothermic” response to bacterial infection (Burns, Ramos, and Muchlinski 1996; Do Amaral, Marvin, and Hutchison 2002; Merchant et al. 2008), which may also have a debilitating effect on the bacteria within the host, similar to that of fever (Merchant et al. 2008). Physiological States: Metabolic Stressors Metabolism and most physiological processes are not only impacted by temperature and temperature regulation but also can, in their turn, impact thermoregulatory behaviors. While it is true that changing Tb has an impact on metabolism and physiology, the relationship is more complex. A ­deficiency of circulating glucose (i.e., hypoglycemia) can reduce preferred temperature (Branco 1997; Rocha and Branco 1998). The benefits of this are related to metabolism; reducing body ­temperature decreases oxygen consumption, and in turn glucose requirements (Rocha and Branco 1998). Similarly, in situations where oxygen availability is lower than ordinarily expected, the majority of species show a decrease in Tb (Wood 1995, 1991; Wood and Gonzales 1996). This behavioral response has been demonstrated for terrestrial amphibians and reptiles (Wood and Malvin 1991; Branco, Portner, and Wood 1993; Bícego, Gargaglioni, and Branco 2001; Cadena and Tattersall 2008), as well as aquatic amphibians and fish (Dupré, Romero, and Wood 1988; Schurmann, Steffensen, and Lomholt 1991; Petersen and Steffensen 2003). The response of adopting a lower regulated temperature has been referred to as anapyrexia (the opposite of fever), to reflect the fact that thermoregulatory defenses are still functional but are reset to a lower value. Lizards also show a lower preferred T b in hypoxic conditions (Cadena and Tattersall 2008), although usually at inspired oxygen levels much lower than normally encountered. Nevertheless, hypoxemia can be brought about by exercise or parasitic infections, and it is suggested that by lowering body temperature, animals protect themselves from oxygen depletion in critical organs. Indeed, following intense activity in some species of lizards, a decline in preferred body temperatures occurs (Wagner and Gleeson 1997; Wagner, Scholnick, and Gleeson 1999), a response shared by other taxa (Tattersall and Boutilier 1999). The potential significance of lowering Tp is lowering metabolic rate, reducing the need for ­oxygen, and increasing blood oxygen affinity, all of which protect vital organs and the brain from damage (Hicks and Wood 1985; Dupré, Romero, and Wood 1988; Schurmann, Steffensen, and Lomholt 1991). For example, Hicks and Wood (1985) found that a lower T b (by about 6°C–8°C) can lower oxygen demand by around 50%. Lizards that are allowed to cool down below their normal preferred Tb show a survival rate of 100% during hypoxia, as opposed to exhibiting a mortality rate of 100% in those that are forced to remain at their normal preferred T b during hypoxia (Hicks and Wood 1985). These observations have led to the suggestion that thermoregulatory control is malleable and that, during times of metabolic compromise (i.e., states that would inhibit the rate of aerobic metabolism), animals that normally regulate Tb at higher temperatures will switch to a lower, but still regulated temperature. EFFECTIVENESS OF THERMOREGULATORY RESPONSES: THERMOREGULATORY PRECISION In an ideal scenario, preferred temperature would match the optimal physiological temperature of that organism, and indeed good evidence exists that Tp correlates with field body temperatures (Figure 1.7). In reality, however, there is often variability in Tp, showing that animals have differing

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Figure 1.7  In (a), preferred temperatures (Tp) measured in the laboratory are strongly associated with mean body temperatures (Tb) measured in the field active period. The thin line and shaded region represents an ordinary least squares (OLS) regression line (slope = 0.702) ± 95% confidence limits, and the thick line represents the phylogenetically independent regression line (slope = 0.719; Pagel’s λ = 0.635, P0 = 0.31, P1 = 0.49) estimated with PGLS (Symonds and Blomberg 2014), showing little evidence of phylogenetic signal in the residual structure. Since the slope is less than 1 (dotted line represents the slope = 1 isopleth), there is a trend for Tp to be higher in lizards that are found at lower Tb values in the field, suggesting higher costs of thermoregulation in the field. In (b), the standard deviations for Tp and Tb are depicted for a subset of lizard families (N = 18), showing the OLS regression line (slope = 0.384, P = 0.02) ± 95% confidence (in shading) and PGLS regression lines as overlapping (slope = 0.384, P = 0.02; Pagel’s λ = 0, P0 = 1, P1 = 0.024), showing no evidence of phylogenetic signal in the residual structure. Data are derived from those summarized by Clusella-Trullas and Chown (2014) and represent family mean values, where symbol size represents the number of species used to estimate values. Symbol color refers to the heat map scale. Mean values are depicted in the top panel (a), and within-family variation (SD) values are depicted in the bottom panel (b).

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Figure 1.8  Inverse relationship between Tp and precision of Tp (SD) within individual bearded dragons (Pogona vitticeps) from two separate studies (a and b). Regression lines (solid lines and shaded regions represent model fits and 95% confidence limits) were fitted to the data for visualization purposes. Linear mixed models (with individual for a and b) were fit from SD vs. Tp. In all cases, a significant (P < 0.05) trend was observed. In panel (a), data represent thermal preferences of individual lizards tested at a range of oxygen concentrations. (Data from Cadena and Tattersall 2008.) In panel (b),  data represent thermal preferences of lizards tested using a variety chambers designed to enforce locomotory costs (shuttle box: 1, 4, 7°C/min, extreme temperatures, and thermal gradient). (Data from Cadena and Tattersall 2009.)

levels of precision in preferred temperature (Dewitt 1967). Indeed, at least in measurements of behavioral thermoregulation in Central Bearded Dragons (Pogona vitticeps), an inverse relationship between the mean Tp and the variance (Figure 1.8) exists. This is a pattern that appears to hold up when exposed to different stressors. The implication is that elevated thermal preferences are associated with a higher precision of thermoregulation; proximate reasons for this may simply reflect the tendency for Tp to approach the CTmax in magnitude (Clusella-Trullas and Chown 2014), and thus, thermoregulatory decisions are influenced strongly by the risks of overheating (Cadena and Tattersall 2008, 2009). Thermal optimality and precision have been further explained with the aid of mathematical models, a prominent one of which assumes that thermoregulation is only favorable when its costs are lower than the benefits it confers (Huey and Slatkin 1976). In an ideal environment, one would

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expect the cost of thermoregulating to be low or nonexistent, and therefore, one would anticipate that a lizard would attempt to reach its thermally optimal Tb. However, ideal environments do not exist naturally, and costs of thermoregulation must be taken into account. Huey and Slatkin (1976) predicted that when associated costs are low, reptiles will be thermoregulators, but if costs are high, they will instead conform to the ambient temperature (thermoconformers). The model put forth by Huey and Slatkin (1976) predicted that reptiles living in environmental extremes, where ­precise thermoregulation is costly, will be thermoconformers. Subsequent work has found this prediction to be unsatisfactory in certain situations and has sought to clarify the cost–benefit model. For example, a study conducted on the Black Rat snake (Pantherophis obsoletus) found that despite the study population being located in the coldest region of the species’ distribution, its members were moderate thermoregulators and similar in this regard to other species in less costly environments (Blouin-Demers and Weatherhead 2001). Further work has supported this, showing that the costs of thermoconformity are higher than the costs of thermoregulation in regions of poor thermal quality (Blouin-Demers and Nadeau 2005). Thermoconformity can be beneficial in tropical regions where more active thermoregulation may be unnecessary, since the thermal environment is relatively benign (Blouin-Demers and Weatherhead 2001; Huey and Slatkin 1976). There are also numerous concerns a lizard may face that will increase the cost of thermoregulation, not the least of which is the energetic cost of shuttling, or balancing the need to thermoregulate and the need to eat, mate, or engage in social interactions. Precision is also affected by physical factors, such as temperature distribution within the environment (Huey and Webster 1976; Dewitt 1967). Dewitt’s (1967) work examined the impacts of biological factors, such as predation and competition, on Dipsosaurus dorsalis, during warmer months of the year; D. dorsalis exhibits body temperatures higher than Tset during active periods away from shelter. Typically, the ambient temperature at or above ground level never drops to the desired ambient temperature of the animal during warmer months. For this reason, despite thermoregulatory behaviors, the lizards are forced to maintain a Tb of 3°C–4°C higher than their preferred Tb when they are above ground. Therefore, individuals of D. dorsalis usually tend to remain in their burrows where it is cooler, although this is not always possible. The biological and behavioral factors that most strongly impacted thermoregulation and forced these animals from their cooler dwellings were territorial behaviors and antipredator responses. Smaller changes to precision were caused by feeding demands, while courtship behaviors had no significant impact. During territorial disputes in D. dorsalis, lengthy periods of threat display often ensue, and occasional fights between lizards occur. These displays and fights often last several minutes and commonly take place above ground in exposed areas. Dewitt (1967) observed that, in several cases, the animals’ Tb immediately after a fight was, on average, 6°C–8°C higher than their preferred Tb. The high body temperature suggests that these animals compromise thermoregulation for territorial protection and engagement in intra-specific competition. During periods of predation threat, these animals often remain as still as possible to avoid detection. Overheating can occur when this happens in exposed areas during warm periods. This behavior is more common when a potential predator is situated between the organism and its burrow (Dewitt 1967). Changes to thermoregulatory precision caused by physical or biological factors are evident among many species (Dewitt 1967; Cadena and Tattersall 2009; Huey and Webster 1976). BEHAVIORAL THERMOREGULATION IN NATURE: PLACING THERMAL PREFERENCE INTO CONTEXT According to Huey and Slatkin’s (1976) cost–benefit model of lizard thermoregulation, ectotherms should alter their thermoregulatory strategy with respect to the costs associated with the behavior, the benefits of the achieved body temperature, and the thermal quality of the environment (Herczeg et al. 2006). The associated costs are the time and energy devoted to the thermoregulatory behavior that are

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consequently not available for other fitness-related activities, such as foraging and mate-searching, and those leading to an increased risk of predation (Huey and Slatkin 1976). This is important for research on basking, as it has been shown experimentally that lizards bask less when there is a high risk of predation (Downes and Shine 1998; Downes 2001). Furthermore, different sexes respond differently to such costs (Shine 1980; Madsen and Shine 1992), because females bear the costs of reproduction. One of the major challenges when attempting to determine temperature preference of an animal in the field is that measuring Tb is not equivalent to measuring the animal’s Tp, nor does it provide a guarantee that the animal is indeed thermoregulating. As in the laboratory, to demonstrate that an ectotherm is actively thermoregulating in the field, one needs to demonstrate that its Tb diverges significantly from that of a null model, that is, from the temperature of a non-thermoregulating animal or “thermoconformer” in the environment, and that this Tb distribution is as close to the animal’s Tset as its environment will allow. The research protocol proposed by Hertz, Huey, and Stevenson (1993) set the standards and parameters necessary for studying behavioral thermoregulation in the field and helped to answer the question: “How carefully do ectotherms regulate their body temperatures?” Three main types of data are necessary for answering this question. First, it is necessary to collect the Tb of free ranging animals; as with experiments performed in the laboratory, this can be done through implantation of temperature data loggers or radio telemeters or by using cloacal temperature probes. Second, it is necessary to record the distribution of operative environmental temperatures (Te), that is, the null distribution of Tb that a thermoconformer would experience in its natural environment. Te can be obtained by measuring the core temperatures of artificial models of the study animal placed randomly throughout the study area. These models should have similar thermal properties to the real animal, without the ability to thermoregulate either behaviorally or physiologically. Metal or plastic models of similar size and shape to the species in question are commonly used for this purpose (Bakken 1992). Tb and Te should ideally be recorded simultaneously or, at the very least, when environmental conditions at the field site are similar. Lastly, it is important to determine the preferred temperature or set-point temperature range, which can be done using a thermal gradient, shuttle box, or other method of Tp determination in the laboratory (see Section “Methods for Examining Behavioral Thermoregulation in the Laboratory”). Having obtained these three variables, one can calculate different parameters that describe the animal’s thermoregulatory behavior in the field. The accuracy of thermoregulation is the degree to which field Tb approximates Tset, independent of whether the animal is actively thermoregulating. Thermoregulatory accuracy can be estimated by calculating the mean of the absolute values of the deviations of Tb from the upper and lower limits of Tset (db); the larger the db, the lower the accuracy of thermoregulation (Hertz, Huey, and Stevenson 1993). Similarly, one can obtain a measure of the thermal quality of the habitat by calculating the mean of the absolute values of the deviations of the upper and lower limits of Tset from Te (de). As with db, a low de indicates a close match between the animal’s Tset and the temperatures the animal is able to achieve within its environment (Hertz, Huey, and Stevenson 1993). From these two basic parameters, db and de, one can determine whether an ectotherm is actively thermoregulating as well as the degree of effectiveness of said thermoregulation. Hertz, Huey, and Stevenson (1993) proposed an index for the effectiveness of thermoregulation (E) which can be calculated as E = 1 − (db /de), which generally ranges in value between 0 and 1. A value of 0 indicates no thermoregulation and a value of 1 indicates a perfect thermoregulator; negative values can occur if an animal is actively avoiding Tset temperatures. Unfortunately, the index E presents a problem, since a given E value can be obtained through different combinations of db and de because E depends upon the ratio db:de. This means that in some cases, animals with very different thermoregulatory strategies occupying habitats of different thermal quality will have similar E values (Blouin-Demers and Weatherhead 2001). This makes it imperative to also consider the magnitudes of db and de individually. In addition, ratios are sensitive to extreme values in the numerator and the denominator, creating skewed distributions (BlouinDemers and Weatherhead 2001). To circumvent these problems, Blouin-Demers and Weatherhead

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(2001) proposed a simplification of E, whereby the effectiveness of thermoregulation is described by de − db. Negative values of this index indicate animals that avoid Tset temperatures, whereas positive values are indicative of active thermoregulation. A value of 0 represents thermoconformity. Lastly, another helpful parameter is the index of thermal exploitation (Ex) proposed by Christian and Weavers (1996), which provides an indication of the extent to which an animal exploits its thermal environment. It is expressed as the time in which Tb’s are within Tset, divided by the time available for the animal to have its Tb within Tset. Although the focus of our review has been on proximate, ethological aspects of thermoregulation, phylogenetic signal in thermoregulatory behaviors should exist, which has not been extensively studied. Behavioral traits are often more labile and show less phylogenetic signal than morphological and physiological ones (Blomberg, Garland, and Ives 2003). Examining the available data on fieldmeasured Tb and laboratory-measured Tp, as collated by Clusella-Trullas and Chown (2014), we found evidence for strong phylogenetic signal in both Tb (Pagel’s λ = 1.048, P = 0.023; Blomberg’s K = 1.075, P = 0.008) and Tp (Pagel’s λ = 1.064, P = 0.064; Blomberg’s K = 0.99, P = 0.008) when analyzed using phylogenetic generalised least squares (PGLS) analysis for each trait separately (see Figure 1.9 for traits mapped onto phylogenies). Particular families that stand out are the Xantusiidae, Trogonophidae, and Amphisbaenidae. The latter two reside in the Clade Amphisbaenia, along with the Anguidae and Anniellidae, and all of these demonstrate a cool Tb relative to their phylogenetic position. In this case, the Xantusiidae is represented by the Desert Night Lizard (Xantusia vigilis), which does not bask, is active at night and is effectively a thermoconformer (Kaufmann and Bennett 1989). The remaining families are burrowing, legless squamates, constrained by their fossorial microhabitat choice from experiencing temperatures different from ground temperature and overall appear less prone to overt basking behaviors (Civantos, Martin, and Lopez 2003; Abe 1984; Meek 2005; Bury and Balgooyen 1976). Clearly, a more comprehensive phylogenetic approach is warranted, where an examination of species-level differences in both Tb and Tp can be explored in order to interpret the relative role of natural selection on behavioral thermoregulatory processes. Given the array of thermoregulatory behaviors discussed in this chapter, future research areas could incorporate a phylogenetic approach to analyze the adaptive significance of specific thermoregulatory behaviors in lizards. CONCLUSIONS AND PERSPECTIVES Most lizards must use behavioral thermoregulation to maintain body temperature within a range that permits normal, or optimal, activity (Avery 1982; Huey 1982; Ben-Ezra, Bulte, and BlouinDemers 2008). Within this range, and between presumed upper and lower threshold temperatures, little additional energy is expended for thermoregulatory behavior, resulting in a refractory zone (Heath 1970). The existence of this zone allows lizards to perform vital life functions (feeding, reproduction, predator avoidance) without the need to thermoregulate constantly. In general, it is expected that this refractory zone corresponds to the animal’s optimal temperature range, as described by Angilletta (2009), although this has not often been explicitly tested. Nevertheless, most lizards can regulate a relatively constant body temperature, typically higher than their surrounding environment. In nature, this can be observed as lizards move between shaded and sunny areas throughout the day, in a manner dependent on the thermal quality of their habitat (Bennett 2004; Cowles and Bogert 1944). The complex interplay between physiological thermal optimalities, thermoregulation, and the requirement for fine-scale adjustments in thermosensation suggest the coevolution of these traits. Fruitful future areas of research will range from examinations of the evolution and mechanisms of temperature sensation and its role in behavioral thermoregulation, to the adaptive significance of specific thermoregulatory behaviors, and finally, to the potential for behavioral thermoregulation to evolve in the face of rapidly changing climates.

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Figure 1.9  P  hylogeny of field measured body temperatures (Tb) and thermal preferences (Tp) in lizard families (Clusella-Trullas and Chown 2014), with Sphenodontidae included for comparison where data were available. Data for Tb were more comprehensive (24 taxa) than those for Tp (18 taxa). Evidence for strong phylogenetic signal is detected for both Tb (Pagel’s λ = 1.048, P = 0.023; Blomberg’s K = 1.075, P = 0.008) and Tp (Pagel’s λ = 1.064, P = 0.064; Blomberg’s K = 0.99, P = 0.008). Trait values are mapped onto the respective phylogenies derived from Kumar et al. (2017). The scale bar refers to branch length, estimated as millions of years ago (mya).

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Sartorius, S. S., J. P. S. do Amaral, R. D. Durtsche, C. M. Deen, and W. I. Lutterschmidt. 2002. Thermoregulatory accuracy, precision, and effectiveness in two sand-dwelling lizards under mild environmental conditions. Canadian Journal of Zoology 80:1966–1976. doi: 10.1139/z02-191. Scarpellini, C. D., K. C. Bicego, and G. J. Tattersall. 2015. Thermoregulatory consequences of salt loading in the lizard Pogona vitticeps. Journal of Experimental Biology 218:1166–1174. Schurmann, H., J. F. Steffensen, and J. P. Lomholt. 1991. The influence of hypoxia on the preferred temperature of rainbow-trout Oncorhynchus mykiss. Journal of Experimental Biology 157:75–86. Secor, S. M. 2009. Specific dynamic action: A review of the postprandial metabolic response. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 179:1–56. doi: 10.1007/s00360-008-0283-7. Seebacher, F. 2000. Heat transfer in a microvascular network: The effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius). Journal of Theoretical Biology 203:97–109. Seebacher, F., and C. E. Franklin. 2005. Physiological mechanisms of thermoregulation in reptiles: A review. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 175:533–541. Seebacher, F., and G. C. Grigg. 2001. Changes in heart rate are important for thermoregulation in the varanid lizard Varanus varius. Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 171:395–400. Seebacher, F., and S. A. Murray. 2007. Transient receptor potential ion channels control thermoregulatory behaviour in reptiles. PLoS One 2:e281. doi: 10.1371/journal.pone.0000281. Shine, R. 1980. Costs of reproduction in reptiles. Oecologia 46:92–100. Shine, R. 2004. Incubation regimes of cold-climate reptiles: The thermal consequences of nest-site choice, viviparity and maternal basking. Biological Journal of the Linnean Society 83:145–155. Shine, R. 2006. Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards? Journal of Experimental Zoology Part A: Comparative Experimental Biology 305a:524–535. Shine, R., and P. Harlow. 1993. Maternal thermoregulation influences offspring viability in a viviparous lizard. Oecologia 96:122–127. Shine, R., P. S. Harlow, M. J. Elphick, M. M. Olsson, and R. T. Mason. 2000. Conflicts between courtship and thermoregulation: The thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, Colubridae). Physiological and Biochemical Zoology 73:508–516. Shine, R., T. R. L. Madsen, M. J. Elphick, and P. S. Harlow. 1997. The influence of nest temperatures and maternal brooding on hatchling phenotypes in water pythons. Ecology 78:1713–1721. Slip, D. J., and R. Shine. 1988. Thermophilic response to feeding of the diamond python, Morelia s. spilota (Serpentes, Boidae). Comparative Biochemistry and Physiology A: Physiology 89:645–650. Smith, E. N. 1979. Behavioral and physiological thermoregulation of crocodilians. American Zoologist 19:239–247. Smith, K. R., V. Cadena, J. A. Endler, M. R. Kearney, W. P. Porter, and D. Stuart-Fox. 2016a. Color change for thermoregulation versus camouflage in free-ranging lizards. American Naturalist 188:668–678. doi: 10.1086/688765. Smith, K. R., V. Cadena, J. A. Endler, W. P. Porter, M. R. Kearney, and D. Stuart-Fox. 2016b. Colour change on different body regions provides thermal and signalling advantages in bearded dragon lizards. Proceedings of the Royal Society B: Biological Sciences 283:20160626. Somero, G. N. 1995. Proteins and temperature. Annual Review of Physiology 57:43–68. Spotila, J. R., K. M. Terpin, and P. Dodson. 1977. Mouth gaping as an effective thermoregulatory device in alligators. Nature 265:235–236. Staaks, G., F. Kirschbaum, and P. Williot. 1999. Experimental studies on thermal behaviour and diurnal activity rhythms of juvenile European sturgeon (Acipenser sturio). Journal of Applied IchthyologyZeitschrift Fur Angewandte Ichthyologie 15:243–247. Stevenson, R. D., C. R. Peterson, and J. S. Tsuji. 1985. The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiological Zoology 58:46–57. Symonds, M. R. E., and S. P. Blomberg. 2014. A primer on phylogenetic generalised least squares. In Modern Phylogenetic Comparative Methods and their Application in Evolutionary Biology Concepts and Practice, edited by L. Z. Garamszegi, 105–130. Berlin, Heidelberg: Springer, Berlin, Heidelberg: Imprint, Springer. Tattersall, G. J., and R. G. Boutilier. 1999. Does behavioural hypothermia promote post-exercise recovery in cold- submerged frogs? Journal of Experimental Biology 202:609–622.

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Chapter  2

Lizard Locomotion Relationships between Behavior, Performance, and Function Timothy E. Higham University of California, Riverside

CONTENTS General Introduction......................................................................................................................... 48 Introduction to Locomotion in Lizards............................................................................................. 50 Sprawling Posture and Its Implications for Locomotor Behavior................................................ 50 Locomotor Kinematics and Mechanics........................................................................................ 50 Performance: Speed, Acceleration, Endurance, and Maneuverability......................................... 51 Speed....................................................................................................................................... 52 Sprint Speed in Nature............................................................................................................ 53 Acceleration............................................................................................................................ 54 Turning Maneuvers................................................................................................................. 55 Running Performance, Defense Strategy, and Foraging......................................................... 56 Locomotor Performance in Relation to Home Range, Territorial Defense, and Mating........ 57 Body Size, Performance, and Behavior................................................................................... 57 Summary: Performance and Behavior.................................................................................... 58 Habitat Structure in Relation to Locomotor Behavior...................................................................... 59 Locomotion in Arboreal Habitats................................................................................................. 59 Running on Sand and Water.........................................................................................................60 Rocky Habitats............................................................................................................................. 61 Obstacles...................................................................................................................................... 61 Exploitation of Features of the Habitat to Escape from Predators............................................... 62 The Utility of Classifying Habitat Based upon Perceived Functional Demand........................... 62 Other Ecological Factors Important for Locomotion........................................................................ 63 Ambient Light.............................................................................................................................. 63 Temperature.................................................................................................................................. 63 Dispersion.........................................................................................................................................64 Morphological Specializations/Innovations...................................................................................... 65 Adhesion...................................................................................................................................... 65 Toe Fringes...................................................................................................................................66 Webbing....................................................................................................................................... 67 Patagia and Other Modifications for Gliding............................................................................... 67 47

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Prehensility................................................................................................................................... 68 Grasping Feet............................................................................................................................... 68 Tail Autotomy, Locomotion, and Behavior.................................................................................. 69 Evolutionary Limb Loss and Simplification................................................................................ 70 Evolution of Locomotor Behavior.................................................................................................... 71 Ecomorphology............................................................................................................................ 71 Trade-offs..................................................................................................................................... 72 Intraspecific Variation.................................................................................................................. 73 Future Directions.............................................................................................................................. 73 Climate Change............................................................................................................................ 73 Combined Field and Laboratory Studies..................................................................................... 74 Individual Variation...................................................................................................................... 74 References......................................................................................................................................... 75 GENERAL INTRODUCTION Lizards are a remarkable structural grade of squamate reptiles that have diversified in many habitats on earth. They are predominantly terrestrial but currently, and especially historically, make incursions into aquatic habitats. The latter is exemplified by the large marine mososaurs (Simões et al., 2017). Lizards are abundant in tropical rain forests and seemingly inhospitable deserts (Figure 2.1). Their total body length ranges from 16 mm (dwarf chameleons and dwarf geckos) to 3 m (Komodo dragon), and collectively they exhibit a wide variety of locomotor specializations, including the ability to swim, glide, climb, burrow, slither without legs, sprint bipedally over soft dune sand, and sprint across the water’s surface. These remarkable specializations result in novel ways to accomplish key behaviors, such as escaping from predators, capturing prey, interacting socially, and dispersing. This chapter is certainly not the first review of lizard locomotion (Foster et al., 2015; Higham, 2015; Russell and Bels, 2001; Van Damme et al., 2003) and is certainly not an exhaustive overview. Instead, I build upon previous research and address key advancements in our understanding of lizard locomotion during ecologically relevant behaviors. In addition to stimulating others to focus their attention on lizard locomotor behavior, I attempt to provide a concise summary of the state of the field. An overarching theme of this chapter is convergence, which is prominent among lizards and provides insights into behavioral adaptation in response to particular environmental challenges, and opens a variety of interesting avenues for future research. Lizard locomotion can be characterized in a number of ways, from the ability to perform a specific task critical for survival (locomotor performance) to the morphological signature of a specific mode of locomotion. Regardless, locomotion in lizards emerges from the integration of multiple hierarchical levels, coupled with constant feedback from the environment. Locomotor performance is an emergent property that reflects how good a lizard is at accomplishing a task, whether it is capturing prey, escaping from a predator, or even displaying to a potential mate (Irschick and Higham, 2016). Different tasks may favor different locomotor traits. For example, locomotion that requires stability may benefit from a prehensile tail, a convergent feature found in multiple arboreal lineages of lizard (Bauer, 1998; Good, 1988; Hardy, 1958; Herrel et al., 2012; Higham and Anderson, 2013; Zippel et al., 1999). Additionally, moving quickly across compliant surfaces may benefit from features that increase the contact area of the feet, such as toe fringes (Carothers, 1986; Luke, 1986). These examples highlight specializations that have emerged that indicate enhanced performance in specific situations. The interplay between these specializations and key behaviors is explored. In this chapter, I provide an in-depth assessment of how lizard behavior, especially escaping from predators and foraging, relies on locomotor movements and performance. All movement depends on the forces (kinetics) and kinematics (motions) of the lizard, and these depend on underlying

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Figure 2.1  Photographs of lizards in different habitats. The Western Dwarf Chameleon (Bradypodion occidentale on a branch in South Africa (a); the Namib Web-footed Gecko (Pachydactylus rangei) on dune sand at Gobabeb, Namibia (b); the Trinidad Gecko (Gonatodes humeralis) on a tree trunk at Nouragues, French Guiana (c); the arboreal Brazilian Anole (Anolis brasiliensis) on a tree trunk at Nouragues, French Guiana (d); the day gecko (Rhoptropus bradfieldi) on a vertical rock in Namibia (e); and the Namib Day Gecko (Rhoptropus afer) on the ground in Namibia (f). (All photos were taken by the author.)

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morphology and physiology. These features, combined with feedback from the environment, whether it is habitat structure, temperature, or some other factor, will then influence foraging, social, and escape behavior. Performance is a measure of how good a lizard is performing an ecologically relevant task and can be measured as sprint speed, acceleration, endurance, or maneuverability. To overcome some challenges of an environment, many lizards exhibit morphological specializations and innovations, such as the adhesive system of geckos. These will then influence behavior in a number of ways, by both facilitating and constraining what a lizard can do. Finally, all of the factors that shape lizard locomotion will influence larger scale ecological factors, such as dispersion. Given that many demands imposed on lizards by their environment are comparable in different regions of the world, evolutionary convergence is common. In addition, convergence provides a valuable way of assessing responses to ecological challenges and how these change through evolution. Finally, I will identify key future directions that will deepen our understanding of lizard locomotion and behavior. INTRODUCTION TO LOCOMOTION IN LIZARDS Sprawling Posture and Its Implications for Locomotor Behavior Most lizards routinely move quadrupedally, with their femora and humeri directed laterally from the body. This abduction of the knees and elbows provides a wide base of support, defined as the area within the four contact points (feet). The sprawling posture, therefore, involves the movement of limb segments in different planes [reviewed by Russell and Bels (2001)]. Although this endows lizards with a stable locomotor gait, it comes at an energetic cost (Reilly et al., 2007). Because the feet contact the ground markedly laterally to the center of mass, the joint moments are greater, requiring greater muscle force to balance them and prevent collapse between the supporting feet. This contrasts with the more upright posture common among mammals, which involves a closer vertical alignment of the contact points (feet) with the substrate and the center of mass (Biewener, 1989). It is, therefore, not surprising that lizards tend not to run for long periods of time. Finally, given the importance of the hind limbs for generating propulsive forces during locomotion, most studies have focused solely on hind limb function. Locomotor Kinematics and Mechanics Kinematics involves the study of animal motion, and many studies have examined this for lizards. Due to the complexity of motion associated with the sprawling posture, a three-dimensional approach is often necessary (Russell and Bels, 2001). Also, the high speeds that are typical of cursorial lizards necessitate the use of high-speed videography to effectively capture and document motion. With only a two-dimensional approach, a limited set of measures of locomotion can be quantified, including duty factor (portion of the stride in which the limbs are in contact with the substrate), stride frequency (number of strides per second), stride length (distance that the center of mass travels during one stride), step length (distance that the center of mass travels while limbs are in contact with the substrate), and vertical girdle height. Of course, locomotor speed and acceleration along the x-axis (fore-and-aft) can also be quantified. When three dimensions are included, it is possible to understand limb segment motions that are important for propelling a lizard that uses a sprawling posture. For example, long-axis femoral rotation, which is driven by the activation of the caudofemoralis muscle (Nelson and Jayne, 2001), occurs in the horizontal plane and increases with increased running speed, as exemplified by the Desert Iguana (Dipsosaurus dorsalis) (Jayne and Irschick, 1999). Almost all terrestrial animals employ two patterns of locomotor mechanics: an inverted pendulum gait when moving slowly and a spring-mass gait at higher speeds (Farley and Ko, 1997). The inverted pendulum gait involves the exchange of gravitational potential and kinetic energy (out of

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phase) with regard to the center of mass (Dickinson et al., 2000). This contrasts with the spring-mass model of locomotion, which involves the legs acting as springs that exchange gravitational potential energy and kinetic energy (in phase) with stored elastic energy (Dickinson et al., 2000). Lizards, unlike most other terrestrial vertebrates, bend their trunk laterally during the locomotor cycle, which raises questions about whether they utilize these two general forms of locomotion. Indeed, the two species that have been examined in this regard (the Western Skink [Plestiodon skiltonianus; cited as Eumeces skiltonianus] and the Western Banded Gecko [Coleonyx variegatus]) exhibit both, with the mechanical power required to accelerate the body laterally during each step representing only 5% of the total mechanical power needed for locomotion (Farley and Ko, 1997). Lateral bending of the body plays a significant role in the locomotion of lizards (Ritter, 1992). Unlike fishes, lizards can exhibit either a standing or a traveling wave of lateral bending during locomotion. In the former, there is always a point (or points) that does (do) not move laterally. Traveling waves, characteristic of fishes, involve all points moving laterally, with the maximum lateral displacement moving caudally over time (Ritter, 1992). Aspidoscelis tigris (the Western Whiptail) and Dipsosaurus dorsalis, both species with strong limb-based locomotion, exhibit a standing wave at slow speeds and a traveling wave as speed increases. In contrast, Elgaria kingii (the Madrean Alligator Lizard) and Plestiodon multivirgatus (cited as Eumeces multivirgatus) (the Northern Many-lined Skink), both species with reduced limbs, exhibit a traveling wave at all speeds of locomotion (Ritter, 1992). It is postulated that both forms of waves will increase stride length, but traveling waves may also contribute propulsive force (Ritter, 1992). A key feature of lizard locomotion employing a sprawling posture is the significant contribution of girdle rotation to forward movement (Jagnandan and Higham, 2017). Like aforementioned waves along the body, girdle rotation will also contribute to an increase in stride length. The side-to-side rotation of the pelvic girdle, which is coupled with the side-to-side motion of the tail (which can represent a significant portion of body mass), allows the hind limbs to protract to a greater degree, resulting in an increase in step length. In some lizards, such as chameleons, the pectoral girdle can displace anteriorly relative to the body wall, thereby substituting for lateral undulation (Peterson, 1984) in a lizard body plan in which the limbs are held beneath the body and the trackway is narrow. This sliding of the girdle can account for up to 40% of step length. In a study of 15 species of lizard, McElroy et al. (2008) tested the hypothesis that the locomotor gait of lizards is correlated with foraging behavior. Although all lizards in the study employed a trotting gait while running, it was found that they segregated into two distinct clusters according to differences in duty factor. By using maximum likelihood ancestral state reconstruction, they found that locomotor mechanics typical of running are ancestral among lizards, and that sit-and-wait is the ancestral mode of seeking food. There have been multiple transitions to the more active, wide foraging mode, and each transition is being associated with the appearance of walking mechanics (McElroy et al., 2008), comparable to walking in mammals. The tight correlation between locomotor mechanics and foraging mode suggests that walking mechanics constitute a key innovation among widely foraging lizards, with this potentially being beneficial by decreasing the total mechanical energy needed to move the animal using the inverted pendulum mode of locomotion (McElroy et al., 2008). Interestingly, the differential modes of foraging observed among lizards may have strong impacts on escape behavior. For example, it is possible that those lizards employing walking mechanics as they forage widely might lack the acceleration capacity to burst away from an oncoming predator. Thus, these species may rely more on refugia and camouflage to avoid encounters. In contrast, those species that employ a sit-and-wait strategy are likely well equipped for rapid escape maneuvers. Performance: Speed, Acceleration, Endurance, and Maneuverability Maximum performance is the ability to perform an ecologically relevant task to its greatest effect (Irschick and Higham, 2016), and thus depends heavily on the ecological context of the behavior.

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Figure 2.2  A  path diagram showing the relationships among lower level traits (morphology, physiology, biochemistry, gray ellipse) and fitness (pink ellipse), and the intervening factors that influence them. The green ellipses indicate locomotor traits and constraints, and the light blue ellipses indicate habitat structure factors. Performance impacts fitness, but many factors contribute to performance, creating a hierarchical thread of factors that will ultimately dictate survival. This is based partly on the work of Aerts et al. (2000), Arnold (1983) and Garland and Losos (1994).

In the paradigm outlined in Figure 2.2, locomotor performance bridges the morphology and biomechanics of a lizard to its locomotor behavior. Locomotor biomechanics, in this case, includes what has been termed integrated dynamic design traits by Aerts et al. (2000), which includes kinematics and mechanics. Although this generally builds on the morphology–performance–fitness paradigm outlined by Arnold (1983), it also includes constraints (Aerts et al., 2000) and behavior (Garland and Losos, 1994), both critical components for the prediction of fitness consequences of variation. The main behaviors of interest when it comes to performance are those involving endurance (e.g., ­foraging) and rapid movements (e.g., predator escape and attacks on prey). Therefore, the variables, discussed in the following sections, are described in the context of predator–prey interactions. Speed Maximum locomotor speed, one measure of maximum performance, is often thought to reflect the ability to escape from a predator, and thus plays a critical role in determining fitness (Higham et al., 2016; Irschick and Garland, 2001). Given the importance of this behavior, the majority of studies of lizard locomotor performance have focused on maximum escape sprint speed. Examining this is a fruitful way of elucidating the outcome of variation in morphology, physiology, and ecology of lizards, and has thus been quantified in numerous studies (Bauwens et al., 1995; Bonine

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and Garland, 1999; Garland and Losos, 1994; Goodman et al., 2008; Hertz et al., 1988; Higham et al., 2011a; Higham et al., 2011b; Higham and Russell, 2010a; Huey et al., 1989; Kohlsdorf and Navas, 2012; Losos, 1990a; Losos and Sinervo, 1989; Macrini and Irschick, 1998; O‘Connor et al., 2011; Olberding et al., 2012; Sinervo and Losos, 1991; Van Damme et al., 1998; Vanhooydonck and Van Damme, 2003; Vanhooydonck et al., 2001). Laboratory sprint speed is commonly measured using a trackway and photocells placed at intervals along the track (Bauwens et al., 1995). The shortest elapsed time between two photocells is then interpreted as the maximum sprint speed. Methods can differ to some degree, as the spacing between the photocells can be different. In addition, some studies have quantified maximum sprint speed using high-speed video (Higham and Russell, 2010a), thereby avoiding the issue of speed modulation between the intervals within which data are obtained. Finally, studies can differ in the way they account for body size, with some comparing absolute speeds, some presenting data in snout vent lengths (SVLs) per second, and others simply including body size as a covariate in the analyses. Future studies should aim to standardize both speed measurement and size correction methods. Sprint Speed in Nature The ecological relevance of maximum sprint speed (as measured in the laboratory) depends, in part, on the relative use of maximum performance in nature. However, few studies have compared escape sprint performance in the laboratory and the field (but see Braña, 2003; Higham and Russell, 2010a; Husak and Fox, 2006; Irschick and Jayne, 1999; Irschick and Losos, 1998; Muñiz Pagan et al., 2012; Stiller and McBrayer, 2013). I combined the data from existing studies, representing 19 ­species that are regarded as being either rock-dwelling, arboreal, or cursorial, to determine if the average maximum sprint speeds measured in the field and laboratory are comparable (Figure 2.3). One study of Urosaurus ornatus (the Tree Lizard) incorporated only a single escape in the field (McElroy et al., 2007) and was therefore not included. It is also important to note that each point represents a species average, but there is likely considerable individual variation within a population. Indeed, Stiller and McBrayer (2013) found that individuals of Sceloporus woodi (the Florida Scrub Lizard) that exhibit the same maximum sprint speed in the laboratory exhibit a wide range of escape speeds in nature, from approximately 0.4 of maximum to 1.3 of maximum. The arboreal and saxicolous species exhibit the lowest sprint speeds in both the field and the laboratory, and speeds tend to be lower in the field compared to the laboratory (Figure 2.3). In contrast, the ground-dwelling species exhibit much higher speeds, and three of the four species run faster in the field compared to the laboratory (Figure 2.3). There are several reasons that can explain this result. First, laboratory measures of sprint speed might fall short due to the constraints of laboratory settings, such as the restriction of trackway length. Indeed, Rhoptropus afer (the Namib Day Gecko), one of the faster species in Figure 2.3, can run many meters at a time (Odendaal, 1979; pers. obs.), beyond what is possible to observe and record in a normal laboratory. Second, ground-dwelling cursorial lizards may simply utilize their maximum capability in the field more frequently than do rock and tree-dwelling species. Most species that have been studied appear to use maximum running speed only during escape (real or simulated), whereas foraging and capturing prey typically occurs using submaximal running speeds in lizards (Cooper Jr. et al., 2005; McElroy et al., 2011; McElroy et al., 2007). For example, the Marine Iguana (Amblyrhynchus cristatus) exhibits maximum running speed only when chased in nature, reaching speeds of approximately 2.5 m/s (Gleeson, 1979). Interestingly, males of Crotaphytus collaris (the Collared Lizard) employ near maximum sprint capacity in the field only when fleeing from a rival male (Husak and Fox, 2006). In contrast, females were not observed to use their maximum sprint capacity in nature. The locomotor performance differences between sexes in the field are poorly understood and should be a focus of future research. Regardless, this indicates that behavior has the potential to override physiological capacity. Therefore, behavior is an essential component when attempting to understand locomotor patterns among lizards.

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Figure 2.3  A linear regression of average maximum laboratory sprint speeds versus average field escape sprint speeds for 19 species of lizard. The red triangles represent eight arboreal species of anole: Anolis sagrei (the Brown Anole), A. lineatopus (the Stripefoot Anole), A. gundlachi (the Yellowchinned Anole), A. carolinensis (the Green Anole), A. grahami (Graham’s Anole), A. evermanni (the Emerald Anole), A. valencienni (the Short-tail Anole), and A. angusticeps (the Cuban Twig Anole). Data for these are taken from Irschick and Losos (1998). The blue squares represent five saxicolous species of lizard: Dalmatolacerta oxycephala (the Sharp-snouted Rock Lizard), Rhoptropus bradfieldi, Podarcis melisellensis (the Dalmatian Wall Lizard), P. siculus (the Italian Wall Lizard), and P. muralis (the Common Wall Lizard). The data for R. bradfieldi are taken from Higham and Russell (2010a) and the lacertid data from Braña (2003) and Irschick et al. (2005). The black circles represent six species of ground-dwelling cursorial lizard: Rhoptropus afer (the Namib Day Gecko)—data taken from Higham and Russell (2010a); Uma scoparia (the Mojave Fringetoed Lizard) and Callisaurus draconoides (the Zebra-tailed Lizard)—data taken from Irschick and Jayne (1999): Sceloporus woodi (the Florida Scrub Lizard)—data taken from Stiller and McBrayer (2013); Ameiva ameiva (the Giant Ameiva)—data taken from Muñiz Pagan et al. (2012); and Crotaphytus collaris (the Collared Lizard)—data taken from Husak and Fox (2006). The photos (from left to right) are of R. afer, U. scoparia, and C. draconoides. The first two were taken by the author, and that of C. draconoides is sourced from Wikimedia Commons. Note that the dashed line represents a slope of 1, where field and laboratory speeds would equal one another. The actual slope of the linear regression is slightly higher at 1.06 (R2 = 0.73, P < 0.01).

Acceleration Although sprint speed is often used as the metric for locomotor performance among lizards, it is likely not the only determining factor of survival during a predator–prey interaction. Acceleration defines how quickly an animal separates itself from a predator and is possibly more important for

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predator avoidance than for speed for a range of animals (Huey and Hertz, 1984; Webb, 1976). When escaping from a predator that adopts a sit-and-wait strategy, this initial acceleration is likely even more important since there is not likely to be a long pursuit. More generally, small lizards typically move in short bursts with frequent pauses (Gleeson, 1979; Higham et al., 2011b; Irschick, 2000; McElroy and McBrayer, 2010), providing additional support for the importance of acceleration as a defensive behavior in its own right. Although not fully explored, it is likely that those lizards executing escape behaviors with maximum acceleration will exhibit a relatively shorter flight distance. This is simply due to the use of highly fatigable muscle fibers, which are necessary for achieving high acceleration. A recent study found that Sceloporus woodi reached a maximum velocity at approximately 0.4 m from its starting position, and that the first two steps were the primary determinants of maximum velocity (McElroy and McBrayer, 2010). Using this same species, another study found that the magnitude of acceleration and the frequency of pausing throughout a locomotor bout depend on the incline of the substrate, with vertical surfaces eliciting greater acceleration and more pausing (Higham et al., 2011b). It appears that the average diameter of fast glycolytic muscle fibers of the gastrocnemius, a stance phase propulsive muscle, positively correlates with maximum acceleration in S. woodi, whereas no correlation was observed between this attribute of the iliofibularis, a swing phase muscle (Higham et al., 2011a). That said, the duration of the swing phase of the stride cycle drops rapidly with increase in running speed in the Savannah Monitor (Varanus exanthematicus), and the burst activity of the iliofibularis increases with increase in speed (Jayne et al., 1990). The ultimate limits to sprint speed and behavior are likely a combination of swing and stance phase parameters. Turning Maneuvers Common maneuvers in terrestrial escape trajectories include changes in direction by turning or changes in velocity by accelerating or decelerating (Higham et al., 2001; Jindrich and Full, 1999). The former involves a change in heading, and can be preceded by a rapid deceleration and followed by a rapid acceleration, thus indicating behavioral modulation of the escape pathway. Turning maneuvers can be challenging to elicit in a controlled way in a laboratory setting, rendering this behavior a poorly understood aspect of lizard locomotor performance. One study was able to elicit turning maneuvers in three Jamaican species of Anolis (A. valencienni [the Short-tail Anole], A. ­lineatopus [the Stripefoot Anole], and A. grahami [Graham’s Anole]) by introducing a turn in the arboreal perch on which they were running (Higham et al., 2001). An increase in turning angle (from 30° to 90°) resulted in both a decrease in velocity and an increase in the frequency of pausing. Such responses were ecomorph dependent, with both A. valencienni (twig ecomorph) and A. lineatopus (trunk-ground ecomorph) exhibiting the greatest decrease in speed. This is in contrast to A. grahami (trunk-crown ecomorph), which showed velocities of 99% (30° turn) and 79% (90° turn) relative to maximum. Approximately half the individuals of each species jumped to bridge the 90° turn, and the potential increase in their overall running speed was likely cancelled out by the increase in time resulting from pausing following the jump (Higham et al., 2001). The variability in the means of navigating the turn might ultimately reflect the ability to modulate behavior depending on the perceived predation threat. The tail appeared to be important for mid-air maneuvers during the jump, but future work is necessary for determining its role during running in an arboreal habitat. Lizards can also execute maneuvers mid-air during jumps or falls (see below). The ability to turn is likely related to vertebral number, where lizards with more vertebrae are able to execute turns more effectively (Van Damme and Vanhooydonck, 2002). It is predicted that those species living in more cluttered habitats will have more vertebrae in order to enhance maneuverability. In contrast, those lizards living in more open spaces will have fewer vertebrate and will be able to run at faster burst speeds. Indeed, lacertids that live in cluttered and arboreal

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habitats exhibit a greater number of vertebrae than those living in open areas (Van Damme and Vanhooydonck, 2002). The lizards living in open areas would require stiffer vertebral columns that favor speed and acceleration capacity, and fewer vertebrate would contribute to this. Running Performance, Defense Strategy, and Foraging In addition to sprinting, jumping, and turning, some lizards often move for longer periods of time and cover long distances in seeking food. Therefore, it is not surprising that endurance performance is correlated with foraging behavior. Closely related lacertid lizards in the Kalahari Desert of Africa exhibit considerable diversity in their foraging behavior (Huey and Pianka, 1981). Some are sit-and-wait predators that move 10%–15% of the time, whereas others are wide-ranging foragers and move 50%–70% of the time. In general, the endurance capacity (measured on a treadmill) was greater for the widely foraging species, whereas sprint performance (measured on a 2.45 m racetrack) was greatest for the sit-and-wait predators (Huey et al., 1984). Thus, it appears that foraging behavior and locomotor performance are tightly linked. That said, locomotor performance during predator escape is likely under greater selection than locomotor performance during foraging, as noted by Muñiz Pagan et al. (2012) who studied Ameiva ameiva (the Giant Ameiva) and found that these lizards used speeds control M=F BS > NBS BS = NBS M=F BS < NBS M>F BS > NBS T > control M>F M=F BS > NBS M=F BS = NBS F>M M=F BS > NBS M=F BS = NBS

Anolis carolinensis A. carolinensis A. carolinensis Urosaurus ornatus A. carolinensis A. carolinensis A. carolinensis A. carolinensis, Aspidoscelis inornatus, U. ornatus A. carolinensis A. carolinensis A. carolinensis, As. inornatus, U. ornatus Eublepharis macularius A. carolinensis A. carolinensis A. carolinensis As. inornatus A. carolinensis, E. macularius A. carolinensis A. carolinensis A. carolinensis

References are cited in the text. BS, breeding season; NBS, nonbreeding season; M, male; F, female.

Preoptic Area Similar to other vertebrates, lesions to the POA and the anterior hypothalamus (AH) in Anolis carolinensis, Eublepharis macularius, Aspidoscelis inornatus, and Aspidoscelis uniparens decrease the display of male reproductive behaviors compared to sham controls (Wheeler and Crews, 1978; Kingston and Crews, 1994; Edwards et al., 2004). This region is also larger overall and has larger soma sizes in male compared to female As. inornatus and Urosaurus ornatus (Crews et al., 1990; Wade and Crews, 1992; Kabelik et al., 2006). In A. carolinensis, breeding lizards have a larger soma size than nonbreeding lizards in the POA (O’Bryant and Wade, 2002). Interestingly, the ­volume of the AH-POA in As. inornatus and POA in U. ornatus is larger in breeding males compared to females (Wade and Crews, 1991a; Kabelik et al., 2006). Similarly, the POA volume is larger in breeding A. carolinensis males compared to nonbreeding males and females (Beck et al., 2008). In contrast, this measure is not sexually dimorphic in leopard geckos (E. macularius), although it does depend on incubation temperature, such that animals incubated at female-biased temperatures have a smaller POAs than those incubated at male-biased temperatures (Coomber et al., 1997). These types of parallels between morphology and function are consistent with the idea that the POA is important for male sexual behavior. Intracranial implantation of T, DHT, or E2 in or near the AH-POA increases courtship behaviors in castrated A. carolinensis males (Crews and Morgentaler, 1979) and systemic T increases soma size in the POA (Neal and Wade, 2007c), suggesting that direct hormone action modulates the morphology of neural structures critical to the display of male sexual behaviors. In support of this idea, intracranial implantation of DHT near the AH-POA of the all-female As. uniparens ­facilitates male-like copulatory behaviors (Mayo and Crews, 1987), indicating that the neuroendocrine

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mechanism regulating masculine sexual behavior in these unisexual animals is similar to that of males in the related gonochoristic species. Ventromedial Hypothalamus Lesions to the basal hypothalamus, which included the VMH, abolished male courtship b­ ehavior in Anolis carolinensis (Farragher and Crews, 1979), suggesting a potential role for this region in the control of male reproduction. Similar to work in rats (La Vaque and Rodgers, 1975; Emery and Moss, 1984), lesions of the VMH in female Aspidoscelis inornatus abolished female receptivity (Kendrick et al., 1995), further indicating that this region specifically is critical for this female reproductive behavior in lizards. Furthermore, E2 administered directly to the VMH of o­ variectomized female As. inornatus and As. uniparens elicits receptivity, whereas E2 in the AH-POA does not (Wade and Crews, 1991b). In Aspidoscelis inornatus, the VMH is larger in females compared to males, an effect due at least in part to increased soma sizes (Crews et al., 1990). The sex difference in volume disappears outside of the breeding season (Wade and Crews, 1991a). Collectively, these results suggest a potential relationship between morphology of the VMH and the display of reproductive behavior within females of this sexually reproducing species. In contrast, VMH soma size in the all-female As.  uniparens does not differ between animals in stages of the ovulatory cycles in which they ­primarily display female- versus male-like behaviors (Wade and Crews, 1992), which indicates that the brains of these species may be less plastic and that specific changes in brain morphology may not be required for this type of switch in behavioral phenotype. Similarly, VMH volume does not different between the sexes in Anolis carolinensis and Eublepharis macularius (Coomber et al., 1997; Beck et al., 2008), but is larger in breeding compared to nonbreeding A. carolinensis (Beck et al., 2008). Relationships between the morphology and the display of social behaviors should be studied in more depth and across more lizard species in an evolutionary context, if we are to be able to draw strong conclusions about the impact these types of variables may have on each other (see Johnson and Wade, 2010). Steroid Hormone Receptors in the Brain While membrane receptors exist (Heinlein and Chang, 2002; Wang et al., 2014), steroid hormones commonly function through genomic actions via intracellular receptors. These receptors bind specific hormones and form homodimers that translocate into the nucleus (Micevych and Dominguez, 2009; Pihlajamaa et al., 2015). Once there, hormone-receptor complexes function as transcription factors and bind to specific response elements in the promoter region of various genes to regulate gene expression. Specifically, T and DHT both bind to androgen receptors (AR) and E2 binds to estrogen receptors (ER). Differences in steroid hormone receptor expression could alter the ability of the brain to respond to steroid hormones. For example, differences in neural AR expression could mediate the seasonal changes in T’s ability to facilitate male sexual behavior in lizards described above. AR is expressed in a range of nuclei in the lizard brain, including various limbic areas such as the POA, VMH, and AMY in Anolis carolinensis, Aspidoscelis inornatus, Aspidoscelis uniparens, Eublepharis macularius, and eastern fence lizards (Sceloporus undulatus) (Young et al., 1994; Moga et al., 2000; Rhen and Crews, 2001; Rosen et al., 2002). Experiments on whole brain homogenates revealed that AR mRNA levels are higher in nonbreeding male A. carolinensis brains compared to breeding males and females (Kerver and Wade, 2013). While on the surface inconsistent with the idea that increased AR enhances T’s ability to activate behavior, it is important to consider local differences in AR expression. Experiments examining regional expression of AR found no sex or seasonal differences in the number of cells expressing AR in the POA, AMY, and VMH of A. carolinensis

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(Kerver and Wade, 2014). However, among gonadectomized animals, more AR positive cells are detected in the AMY of female A. carolinensis compared to males, which may be due to a decrease in endogenous E2 (Kerver and Wade, 2014). In parallel, castration of breeding male As. inornatus increases AR mRNA expression in the POA, and androgen (T or DHT) treatment reduces the expression of AR to control levels, with no effect of treatment in breeding females of this species or the unisexual As. uniparens (Godwin et al., 2000). These data suggest that AR mRNA is present in the brain regions important in controlling reproductive behavior and may be somewhat regulated by steroid hormone levels. In addition to receptors themselves, AR coactivators are potential candidates for seasonal ­regulation of reproductive behaviors. Steroid coactivator-1 (SRC-1) and CREB binding protein (CBP) are the main coactivators of AR and facilitate gene expression in response to AR (Culig et al., 2004). However, no effect of sex or season have been detected on SRC-1 and CBP mRNA expression in green anole whole brain homogenates (Kerver and Wade, 2013). Anolis carolinensis males have more SRC-1 expressing cells in the POA and VMH than females, and females have more CBP expressing cells in the AMY than males (Kerver and Wade, 2015, 2016). T treatment increases the number of SRC-1 expressing cells in the POA and AMY of both male and female A. ­carolinensis (Kerver and Wade, 2015). Similar to the patterns of AR expression, sex differences in the expression of both AR coactivators have been detected without seasonal effects (Kerver and Wade, 2013, 2015, 2016). Thus, the seasonal change of the neural responsiveness to steroid hormones is likely not mediated through relative levels of AR receptors and the coactivators investigated to date. Additional mechanisms should be considered, as well as the possibility that the levels of analysis do not adequately evaluate differential function of availability of the molecules under investigation. There are two intracellular ERs in most vertebrates, ERα and ERβ, with a third ER found in fish (ERγ; Hawkins et al., 2000). Additionally, several membrane bound ERs exist, which are largely g-protein coupled receptors that activate cell signaling pathways (Qiu et al., 2003; Wang et al., 2014). One of the membrane ERs, GPR30, is responsible for rapid effects of E2 and is important in promoting female reproductive behavior in mice (Prossnitz et al., 2008; Micevych and Dominguez, 2009; Anchan et al., 2014). Although it has not been examined in a reptile yet, GPR30 is present in the green anole genome (NCBI gene ID 100554247). Future work should examine whether this ER has a role in lizard reproduction. In rodents, ERα and ERβ are both important for reproductive behavior in the two sexes, although each receptor appears to affect behaviors differently (reviewed in Rissman, 2008). ERα and ERβ have not been functionally characterized in reptiles, but the mRNAs for both receptors are expressed in whole brain homogenates of Eublepharis macularius (Endo et al., 2008). ERα mRNA is widely distributed in specific regions throughout the Anolis carolinensis, Aspidoscelis inornatus, and the parthenogenic Aspidoscelis uniparens brain, but is found in fewer regions in the E. macularius brain (Young et al., 1994; Rhen and Crews, 2001; Beck and Wade, 2009b). ERα mRNA expression in the VMH and POA of A. carolinensis is greater in females compared to males and appears consistent across the breeding and nonbreeding seasons (Beck and Wade, 2009b). Additionally, systemic E2 treatment in castrated male A. carolinensis decreases ERα mRNA expression in the VMH and POA in males but not females (Beck and Wade, 2009a). In contrast, E2 treatment in As. inornatus increases the ERα mRNA expression in the VMH of females but not males (Crews et al., 2004). The reasons behind this inconsistency are unclear. ERβ mRNA is distributed in a similar pattern as ERα in the A. carolinensis brain, but expression has only been examined in the breeding season in this species (Cohen et al., 2012). A higher density of ERβ mRNA expressing cells exists in the AMY and VMH of females compared to males, with no difference in the POA (Cohen et al., 2012). Increased ERα and ERβ levels in specific regions of female compared to male brains parallels behavioral data showing that E2 is critical for female reproductive behaviors, whereas androgenic action is more important for male lizard sexual behaviors. However, the presence of ERs across areas in the social behavior network in both

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sexes is consistent with direct action of this hormone in some functions related to male as well as female behaviors, including the motivation to copulate (see above). Finally, seasonal changes in ERα expression have not been detected, suggesting that seasonal changes in plasma E2 levels alone could be responsible for changes in E2-mediated behaviors. At present, we do not have evidence for seasonal changes in responsiveness to E2 in a manner that parallels the differences associated with equivalent levels of T administered in the breeding and nonbreeding season. However, this issue remains to be investigated, with consideration of both ERβ and membrane ERs as candidates for mediating such potential changes in the response to E2. Steroid Hormone Metabolism Steroid hormone availability in the brain can be altered through metabolism. Specifically, T can be metabolized into DHT through the action of two 5α-reductase isozymes (5αR1 and 5αR2) (Poletti and Martini, 1999) or metabolized into E2 through the action of aromatase (Balthazart and Foidart, 1993). These enzymes play a role in regulating the availability of T, E2, and/or DHT within specific brain regions to regulate reproductive behaviors. Aromatase activity is critical for male reproductive behaviors in birds (Balthazart and Foidart, 1993), while 5αR is critical for ­development of the male brain in birds and mammals (Grisham et al., 1997; Ribeiro and Pereira, 2005) and is present in the adult brain in birds and mammals (Callard et al., 1983; Soma et al., 2003). Aromatase Aromatase may be important for regulating reproductive behaviors in lizards. In Anolis carolinensis, gonadectomy and systemic treatment with T and either saline or an aromatase inhibitor revealed that while T increases female receptivity, aromatase inhibition blocks this effect (Winkler and Wade, 1998). In support of the idea that aromatase may play a role in regulating lizard sexual behaviors, aromatase mRNA is expressed in regions of the brain responsible for these displays, including in the POA, AMY, and VMH of A. carolinensis and Aspidoscelis uniparens (Dias et al., 2009; Cohen and Wade, 2011). The aromatase mRNA levels do not differ between preovulatory and ­postovulatory As. uniparens in the POA or AMY (Dias et al., 2009), indicating that this enzyme may not specifically regulate the changes in expression of female-like versus male-like pseudosexual behaviors that tend to occur across these two stages. However, when comparing male and female A. carolinensis aromatase expression across individuals from the breeding and nonbreeding seasons, males have a greater number of aromatase mRNA expressing cells in the POA regardless of season, whereas females exhibit a greater density of aromatase mRNA expressing cells in the AMY and VMH (Cohen and Wade, 2011). Gonadectomy and T treatment in A. ­carolinensis has no effect on aromatase mRNA expression in either sex, but reveals a female-biased increase in the density of aromatase mRNA expressing cells in the POA and AMY (Cohen and Wade, 2012a), which suggests that E2 production within the POA and AMY may be important for female reproductive behaviors. In a­ ddition to assessing these types of patterns, it is useful to quantify relative levels of aromatase activity in vivo. Due to the small size of lizard brains, whole organ homogenates are often needed for sufficient sensitivity. In A. carolinensis, aromatase activity is higher in breeding males compared to breeding females and ­nonbreeding males, with no seasonal difference in females (Rosen and Wade, 2001). Furthermore, T treatment increases aromatase activity in whole brain homogenates of ­breeding males compared to females and nonbreeding males (Cohen and Wade, 2010a). Thus, a variety of mechanisms exist to modulate levels of aromatase in a manner that could influence the display of sexual behaviors in male and female lizards.

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5α-Reductase 5α-reductase (5αR) may also play a role in regulating reproductive behaviors in lizards. The T-induced increase in sexual behaviors in gonadectomized male Anolis carolinensis is diminished by a 5αR inhibitor (Rosen and Wade, 2000), suggesting that the conversion of T to DHT is important for the full expression of male courtship behaviors. In adult A. carolinensis, 5αR2 mRNA is expressed in the forebrain; it is present in areas including the POA, AMY, and VMH (Cohen and Wade, 2010b). 5αR1 mRNA is detected in the developing but not adult forebrain (Cohen and Wade, 2012b). Interestingly, 5αR1 and 5αR2 show an opposite pattern in mammals, such that 5αR1 is expressed in the adult forebrain and 5αR2 is only expressed in the developing forebrain (Poletti et al., 1998). The functional implications of this difference are unclear. A greater density of 5αR2 mRNA expressing cells is present in the AMY of female compared to male A. carolinensis with no effects of sex or season on 5αR2 expression in the POA and VMH (Cohen and Wade, 2010b). 5αR activity assays in whole brain homogenates revealed that conversion of T to DHT is not different between the sexes or seasons (Rosen and Wade, 2001), although T treatment increases 5αR activity in males alone regardless of season (Cohen and Wade, 2010a). Collectively, the data suggest that the conversion of T to DHT in the brain is somewhat involved in male lizard reproductive behavior and is upregulated by T. However, the lack of seasonal differences in 5αR supports the notion that DHT production in the brain may be less important for male reproductive behaviors than T itself. It is unclear what this enzyme might be doing in females, but perhaps it functions to break down excess T to inhibit potential effects of this potent androgen. STEROID HORMONES AND THE CONTROL OF AGGRESSIVE BEHAVIORS Steroid hormones are important in regulating aggressive behavior in lizards, although the p­ atterns of activation are not always consistent. Aggressive behavior is associated with an increase in circulating T in Anolis carolinensis (Yang and Wilczynski, 2002), although aggressive encounters decrease T levels in water dragons (Intellegama lesueurii) and jacky dragons (Amphibolurus muricatus) (Watt et al., 2003; Baird et al., 2014). Interestingly, T levels are higher in the ­territorial male Sceloporus undulatus and lower in the non-territorial S. virgatus (Hews et al., 2012). In ­parallel, T levels are higher in more territorial compared to less territorial Anolis species endemic to Puerto Rico, but Anolis species on other Caribbean islands have the opposite pattern, such that more aggressive species have lower T levels than less aggressive species (Husak and Lovern, 2014). Collared lizards (Crotaphytus collaris) that are highly territorial also have lower levels of T ­compared to non-territorial males (Baird and Hews, 2007). In species with positive relationships between circulating T and aggressive behavior, experimental manipulations are required to determine causal relationships. T treatment does not affect the overall frequency of bouts of aggression in A. carolinensis compared to gonadectomized controls, but this manipulation increases the number of throat fan (dewlap) extensions in aggressive contexts (Winkler and Wade, 1998), suggesting that T does regulate some aspects of aggressive displays in this species. T administration in gonadectomized male and female Eublepharis macularius increases aggression toward conspecifics (Rhen and Crews, 1999, 2000). T treatment in male Anolis sagrei and White’s skink (Egernia whitii) does not impact territorial behavior displays (Cox  et al., 2009; McEvoy et al., 2015), while both T and progesterone treatment in Urosaurus ornatus increase aggressive behavior (Weiss and Moore, 2004; Kabelik et al., 2008a). Together, these data suggest that increased T is generally associated with higher levels of aggressive behavior in lizards, but interesting exceptions exist. For these exceptions in which T levels are not correlated to aggression, it is possible that other physiological changes may be important, such as changes in T ­responsiveness within specific brain areas controlling aggressive behaviors.

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BRAIN AREAS INVOLVED IN AGGRESSIVE BEHAVIORS In addition to their involvement in reproductive behaviors, the AMY and VMH are also critical for controlling aggression in a variety of vertebrates (Goodson, 2005). Other areas, such as the lateral septum (LS), AH, and regions of the midbrain, are also important in controlling aggressive behaviors (Goodson, 2005). In lizards, aggressive displays by conspecifics can activate brain areas involved in visual processing, such as the anterior dorsal ventricular ridge, basal ganglia, and nucleus rotundus in Anolis carolinensis males (Baxter, 2001; Baxter et al., 2001; reviewed in Greenberg, 2003). Engaging in aggressive behavior triggers neural activation (measured by phosphorylated CREB levels) within the VMH in Urosaurus ornatus (Kabelik et al., 2008b), suggesting that this region is active during aggressive encounters. Additionally, A. carolinensis males watching videos of other males causes an increase in cytochrome oxidase activity in the AMY, LS, medial cortex (reptilian homologue of the hippocampus), visual thalamic region, and nucleus rotundus (Yang and Wilczynski, 2007), lending support to the involvement of these regions in aggressive encounters. Many of the regions activated during aggressive encounters express AR, which could mediate aggressive behavior. Anolis carolinensis males winning aggressive encounters show an upregulation of AR mRNA in the POA and AH compared to losers, with no effect in the AMY and LS (Hattori and Wilczynski, 2014), supporting the notion that specific regions of the brain may change responsiveness to T after aggressive encounters. Similarly, Sceloporus undulatus males (more ­territorial) have higher AR mRNA levels in the POA and VMH than S. virgatus males (non-territorial) (Hews et al., 2012). More work is needed to characterize brain sensitivity to androgens in species that do not increase T levels during aggression. OTHER HORMONES INVOLVED IN THE CONTROL OF AGGRESSIVE AND REPRODUCTIVE BEHAVIORS In addition to steroid hormones, other neuromodulators are involved in regulation of aggressive and reproductive behaviors. In mammals, dopamine (DA) and serotonin (5HT) are implicated in controlling aggressive behaviors (de Almeida et al., 2005), and arginine vasopressin/vasotocin (AVT) is involved in social interactions (Albers, 2012). Similarly, there is growing evidence that DA and 5HT are involved in controlling aggression in lizards. l-DOPA (3,4-dihydroxyphénylalanine) systemically administered to Anolis carolinensis males elevates DA levels throughout the brain and causes a decrease in aggressive behaviors (Hoglund et al., 2005). Dissections of dominant and submissive A. carolinensis males revealed higher DA and 5HT levels in the AMY of subordinate lizards, whereas dominant lizards had higher DA and 5HT levels in the nucleus accumbens, among other regions (Korzan and Summers, 2004; Korzan et al., 2006). Tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine production (DA, epinephrine, and norepinephrine), is expressed in many of the brain areas involved in aggressive and reproductive behaviors in Anolis sagrei, including the POA, AMY, AH, and others (Kabelik et al., 2014). Furthermore, aggressive behavior in male A. sagrei increases colocalization of TH and immediate early gene expression (cFos) in the POA and AH (Kabelik et al., 2014), suggesting that TH-expressing cells in these regions may be important for aggressive encounters. AVT is expressed in the AMY, POA, LS, nucleus accumbens, and other regions in Urosaurus ornatus, and AVT expression increases with T treatment in the AMY and LS (Kabelik et al., 2008c). More active AVT neurons (co-localized with cFos) are detected in the superoptic nucleus (SON) ­following aggressive encounters compared to no social interaction, and in the POA and SON following sexual encounters in Anolis sagrei (Kabelik et al., 2013), consistent with the idea that AVT in these regions is involved in both types of social behaviors in lizards. Similarly, there

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were more AVT positive cells in the POA of dominant compared to subordinate A. carolinensis (Hattori and Wilczynski, 2009), suggesting a role for AVT in dominant–subordinate relationships. Systemic administration of AVT in A. carolinensis had diverse effects on social behaviors, including decreased aggression in mirror-stimulated males, no effect in male–male interactions, and increased female courtship behavior towards AVT-treated males (Dunham and Wilczynski, 2014), suggesting that AVT has a range of direct roles in mediating social behaviors. Finally, numbers of activated neurons expressing mesotocin, the reptilian homologue of oxytocin (involved in reproductive behaviors in mammals; Insel et al., 1997), are correlated with reproductive behaviors in the periventricular nucleus (PVN) in A. sagrei (Kabelik and Magruder, 2014).

CONCLUSIONS Lizards are important models for the study of the physiological control of social behavior. While many parallels in the neuroendocrine regulation of these behaviors exist across vertebrates, the differences can inform conclusions regarding mechanism. For example, across lizards, birds, and mammals, reproductive behaviors are controlled by the POA, AMY, and VMH, and aggressive behaviors involve the AMY, VMH, and LS, among other regions. Steroid hormones are important for reproductive behavior in lizards, although different from mammalian and avian systems, T appears to be the most potent steroid in eliciting these behaviors in male lizards. E2 is important in female lizard reproductive behaviors, which parallels data from mammals and birds. Aggression is likely controlled at least partially by T levels in lizards, but data are conflicting across lizard ­species. Other hormones, such as AVT, DA, 5HT, and mesotocin, likely play a role in regulating aggressive and reproductive behaviors as well. The variety of distinct social behaviors, sex ­determining ­mechanisms, and existence of unisexual species provide unique opportunities to ­characterize ­critical processes. The field of behavioral neuroendocrinology would benefit from additional, evolutionarily informed work that takes advantage of the diversity among lizards.

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Chapter  7

Sensory Processing in Relation to Signaling Behavior Leo J. Fleishman Union College

Enrique Font Universidad de Valencia

CONTENTS Introduction.....................................................................................................................................208 Visual Communication 1: Pattern and Color..................................................................................209 The Eye and Visual Acuity.........................................................................................................209 Color Vision and Color Signals.................................................................................................. 211 Models of Color Perception....................................................................................................... 213 How Colors Are Produced......................................................................................................... 215 Some Functions of Signal Color and Their Influence on Signal Design................................... 216 Elicitation of Attention.......................................................................................................... 216 Categorical Identification...................................................................................................... 220 Individual Comparison and Assessment................................................................................ 221 Visual Communication 2: Motion Signaling.................................................................................. 225 Form, Function, and Constraints on Motion Signals................................................................. 227 Quantifying and Modeling Motion Signals............................................................................... 228 Some Functions of Motion Patterns and Their Influence on Signal Design.............................. 231 Elicitation of Attention.......................................................................................................... 231 Signaling Species Identity..................................................................................................... 232 Signaling Motivation and Condition..................................................................................... 232 An Example of How Different Functions and Contexts Can Influence the Design of Signal Motion Components....................................................................................................... 233 Chemical Communication.............................................................................................................. 234 Terminology: Pheromones and Signature Mixtures................................................................... 235 Chemosensory Perception: Overview of the Main Olfactory System and the Vomeronasal System........................................................................................................................................ 235 Differences between Olfactory and Vomeronasal Chemoreception........................................... 236 Tongue-Flicking......................................................................................................................... 236 Sources of Chemical Signals...................................................................................................... 238 Signal Chemistry: Functional Groups........................................................................................ 239

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Physical Properties of Lizard Chemical Signals........................................................................ 239 Environmental Influences on Chemical Signal Design.............................................................. 241 Functions of Lizard Scent Marks: What Do Lizards Use Scent Marks For?............................. 242 Auditory Communication............................................................................................................... 243 Anatomy and Mechanism of Lizard Ears..................................................................................244 Frequency Response................................................................................................................... 245 What Do Lizards Use Hearing For?........................................................................................... 245 Sound Production and Communication.....................................................................................246 Communication by Substrate Vibration..................................................................................... 247 Summary......................................................................................................................................... 247 References.......................................................................................................................................248

INTRODUCTION In this chapter, we examine communication in lizards, with a special focus on the role that sensory systems have played in shaping the evolution of signal physical properties (sometimes referred to as “signal design”). Communication can be thought of as a process in which a sender produces a “signal” that is detected by a receiver, this signal potentially influencing the behavior of the receiver and evolving as a result of the benefits arising from the receiver’s response (Hailman 1977). The signal may be any act or structure that affects the behavior of the receiver, that evolved (or is maintained by selection) because of these effects, and that is effective because it makes available to the receiver information about the sender or its environment (Font and Carazo 2010). Here, we use the term “information” in its colloquial (i.e., semantic) sense, referring broadly to acquisition of knowledge about the sender or about the environment (for example, another animal), rather than the technical sense of information as “reduction of uncertainty” (Carazo and Font 2010; Font and Carazo 2010). Evolutionarily stable signaling systems will tend to evolve when the response of the signal receiver is, on average, beneficial to both the sender and the receiver. If this is not the case, senders will stop ­signaling and/or receivers will be under selection to ignore the signal (Bradbury and Vehrencamp 2011). The sensory system can exert evolutionary pressures on signal properties in two distinct ways: (1) by determining whether or not a signal is initially detected and (2) through the process by which it extracts information contained within the signal. Sensory systems generally sample the ­environment very broadly and receive a great deal of peripheral sensory stimulation. Central ­awareness, or attention, is limited to only a small subset of the total sensory input. There must, therefore, be attentional mechanisms: rules or filters that determine which environmental stimuli are of s­ ufficient potential importance to elicit central attention. Thus, one key property of an effective signal (or signal component) is that it should stimulate the peripheral sensory system in a way that elicits attention, thus making it detectable. Once detected, the sensory system must extract some information from the signal. The nature of the information, or class of information, extracted and the way that the sensory system encodes and analyzes the information can have a major evolutionary impact on the signal properties. For example, if a signal has evolved because it conveys information about the reproductive status of the signaling individual, the signal must possess physical features that allow the receiver’s sensory systems to discriminate different variants of the signal found within the population. The effectiveness of a signal depends, to a large degree, on how well the sensory system can extract the information that the signal provides. A useful concept in the analysis of sensory influences on signal properties is the concept of signal “function”. This is not meant to imply that the signal is somehow intentionally planned, or that signals evolve for a specific purpose. Here, we use “function” as a shorthand term to characterize the class of responses that the signal elicits from receivers, thereby forming the basis of selection on the signal’s properties. Elicitation of attention is one important signal function. Other signal functions

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can often be defined by the nature of the information they communicate. If we can identify (or reasonably hypothesize) a function (or functions) for a signal or signal component, we can then ask whether it stimulates the sensory system in a way that efficiently supports that function. We refer to this property as the signal’s “effectiveness” (Fleishman 2000; Bradbury and Vehrencamp 2011). Studies of signal evolution often use the term signal “efficacy,” which has a very similar meaning to our term “effectiveness.” However, “efficacy” usually refers to general properties that make a signal, overall, easy to detect. The term “effectiveness” indicates how well a signal stimulates the sensory system so as to support an identified signal function. Natural selection will normally favor effective (and efficient) signaling because (1) signaling is usually costly (both energetically and in terms of risks associated with predation) and (2) signaling animals are often in competition for attention from, and access to, receivers (Bradbury and Vehrencamp 2011). A signal is often made up of a number of distinctly different components: for example, a push-up display may utilize different motion patterns, as well as colorful display patches. Selection can act on each of these signal components independently, and each component may influence the behavior of the receiver in a different way or even serve a different function. Alternatively, selection may act simultaneously on multiple signal components (e.g., two or more signal components might interact to produce a synergistic effect). Furthermore, different selective forces may act simultaneously on any signal component. Since both receivers and senders tend to benefit, on average, from signaling behavior, it is conceivable that a match between signal design and sensory responses could occur through a process of coevolution of signal design and sensory system response. However, comparative studies of animal sensory systems have, for the most part, shown that sensory systems are rather conservative over evolutionary time, with signals generally evolving much more rapidly than the sensory systems that detect them (Fleishman 1992; Martins et al. 2004; Nicholson et al. 2007). For lizards (and most vertebrates) phylogenetic comparisons usually reveal broadly shared patterns of sensory response, although there are exceptions. Since sensory system response patterns are usually ancestral to the signal properties, we can typically view the sensory systems as manifesting as a set of selective forces influencing the evolution of signal design (e.g., Fleishman 1992; Nicholson et al. 2007). Additional factors governing the interaction between signal properties and the effectiveness of sensory stimulation include the signaling context and the signaling environment. Examples of context include the distance from sender to receiver and the time of day. Signals must transmit through the environment and be detected against background noise, making the signaling environment an important factor shaping signal properties. In this chapter, we review signal evolution as it relates to sensory response in a number of important sensory modalities. We begin each section by describing the basic response properties and their physiological underpinnings. We then describe the mechanisms of signal production in that modality. From there we explore how sensory response properties have shaped the evolution of signal design and signal diversity. We include in this analysis considerations of the interacting effects of sensory response and signal context, signaling environment, and signal function. Different sensory modalities tend to favor different signal functions, and these differences have shaped research approaches to the different modalities. For this reason, as we review the different modalities, we focus on different combinations of signal functions, contexts, and methods of analysis.

VISUAL COMMUNICATION 1: PATTERN AND COLOR The Eye and Visual Acuity The lizard eye focuses light as it passes through the lens and cornea and forms an image on the retina. Photoreceptor cells in the retina capture the light and pass the information onto the

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neural layers of the retina. The photoreceptor cells in lizard eyes are believed to be entirely cones (Walls 1942). Each cone contains pigment in its outer segment that captures light and defines the spectral sensitivity of the cone. In diurnal lizards, the cones also usually contain a colored oil droplet, or dispersed pigment, that filters the incoming light before it reaches the photoactive pigment. In nocturnal species, such as geckos, the cones have become larger and often lack oil droplets (Röll 2000). Much of the processing of the spatiotemporal and spectral properties of the image occurs within the retinal layers, and the information is passed via retinal ganglion cells to the brain. One very important eye-to-brain pathway is from the retina to the optic tectum, where connections with motor neurons drive reflexive eye movements that direct visual attention toward relevant images (Ulinski et al. 1992). This attention reflex, referred to as the “visual grasp reflex” (Hess et al. 1946; Ingle 1982; Fleishman 1992), can be easily observed as an abrupt shift of the direction of gaze. The reflex has been used in a number of different experiments as a behavioral assay for elicitation of attention. Visual resolution depends on the size and shape of the eye (which determines the size of the image on the retina), the density of retinal photoreceptors, and the extent of neural convergence of photoreceptors onto ganglion cells. The eye shape of most diurnal lizards is similar, with a relatively small pupil and a fairly large focal length, which results in a large image that falls on a high density of cone photoreceptors. Nocturnal species typically possess an eye with a very large cornea and pupil and a short focal length, resulting in a relatively small, bright image, on the retina, that favors sensitivity in low light over high resolving power. The retinas of nocturnal species contain cones that have modified shape and properties that give them some rodlike properties. They are longer and, in some cases, larger in diameter than those of diurnal lizards. This, combined with a higher degree of neural convergence, improves the sensitivity of the eye (Underwood and Menaker 1970). Although the eyes of nocturnal lizards are specialized for high sensitivity, they exhibit a reasonably high degree of spatial resolution, and some species make use of visual signals in their communication (Marcellini 1977). In most lizards, the density of photoreceptors varies across the retina, with most species exhibiting a region of the retina, associated with direct attention, of much higher photoreceptor density (New and Bull 2011). Where this region is small and approximately circular, it is referred to as a fovea. Anolis lizards are unique among lizards in possessing two foveal regions: a central one associated with monocular gaze and a smaller, temporal one, associated with binocular fixation (Fite and Lister 1981). Attempts to measure visual resolution in lizards are rare. Makaretz and Levine (1980) measured cone and ganglion cell density in the retina of Anolis carolinensis (the Green Anole). The convergence ratio of cones to ganglion cells is close to one throughout the retina, and it is therefore possible to estimate the upper limit of resolution based on photoreceptor densities. Resolution limits are usually quantified in terms of “grating acuity,” which is typically quantified as the number of cycles of repeating black and white stripes that can occur within one degree of visual angle, and still be discriminated as individual lines (= cycles per degree). Fleishman et al. (2017) used the data from Makaretz and Levine (1980) to calculate an acuity limit of 1.25 cycles/deg in the visual periphery and 12 cycles/deg in the central foveal region, indicating a tenfold difference between the fovea and the periphery. A behavioral estimate for the visual periphery of Anolis sagrei (the Brown Anole) was found to be 1.35 cycles/deg, which agrees well with the previous estimate. The only other acuity estimate for a lizard comes from New and Bull (2011) who found a peak value of 6.8 cycles/deg for the Sleepy Lizard (Tiliqua rugosa), a fairly slow moving diurnal animal. By comparison, human visual acuity, because of our large eyes, is much greater. For example, 20/20 vision is equivalent to a foveal acuity of 30 cycles/deg. Thus, the detail that a lizard can see, particularly from a distance, is much less than what a human can see. Fleishman et al. (2017) showed that in A. sagrei, the finer details of patterning of the dewlap (spots and a rim of color around the edge) are not visible to another individual 0.5 m or more away, if the dewlap is viewed in the visual periphery.

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However, viewed with the central fovea, these details are visible from a meter away. Minimum acuity for moving stimuli—the minimum motion distance of an object that can be detected—is considerably smaller than stationary pattern acuity. The minimum motion amplitude that can be detected in several different Anolis species is approximately two to four times smaller than the smallest nonmoving pattern element (Steinberg and Leal 2016; Fleishman et al. 2017). Another interesting case is the chameleon eye, which has been shown to have a lens that enlarges the visual image projected onto the retina. This has the effect of greatly increasing the animal’s visual acuity and also enhancing their ability to use retinal focus as a distance estimation mechanism (Ott and Schaeffel 1995). What does this tell us about signal design? Signal components designed to elicit attention must be considerably larger—in terms of angular extent of pattern elements and/or in terms of amplitude of motion—than components serving other functions, because the acuity in the visual periphery is much less than the foveal acuity associated with direct attention. Finely detailed color patterns, such as dots on the dewlaps of some anoline species, will be detected only at close range by attentive viewers. They are unlikely to serve a role in elicitation of attention but may play a role in species identification or discrimination, when this takes place at close range using foveal vision. Color Vision and Color Signals In the perception of light, the spectral distribution of the stimulus plays a critical role in two aspects of visual perception. Nearly all animal visual systems possess two distinct neural processing channels: achromatic and chromatic. The achromatic channel is based on a sum, weighted by spectral sensitivity, of all the visible wavelengths in the stimulus. This results in a sensation often referred to as “brightness” or “luminance,” which depends on the total intensity and spectral distribution of the source (Kemp et al. 2015). In lizards, the available evidence strongly suggests that luminance is encoded by a class of long-wavelength-sensitive double cones, which are the most common cones in most lizard retinas (Loew et al. 2002; Olsson et al. 2013). The spectral absorption curve of these cones matches the overall behaviorally or physiologically measured luminance sensitivity of the animals (Fleishman et al. 1997; Fleishman and Persons 2001). The achromatic channel is largely responsible for perception of motion and physical form. The chromatic channel is primarily sensitive to the shape of the stimulus spectrum, and not the total intensity. Chromatic sensation is based on comparisons of the strength of stimulation of photoreceptor classes that differ in their spectral sensitivity. These comparisons generally occur in a manner that makes the sensation independent of intensity over a broad range, so that a given color will tend to appear the same over a wide range of intensities. If an animal can discriminate among different stimuli based on their wavelength distribution, independent of intensity, it is said to have color vision. Any attempt to demonstrate animal color vision requires a correction for changes in luminance that occur with changes in stimulus wavelength composition, which greatly complicates the task of demonstrating and analyzing color vision in animals. The most effective approach involves extensive training and testing in experiments that carefully control for luminance effects (Jacobs 1981), for which lizards are not particularly well suited. To our knowledge, there are only two clear reports of using behavioral conditioning (and correction for luminance differences) to demonstrate the capacity for color vision. Wagner (1932) demonstrated color discrimination capability in Lacerta agilis (the Sand Lizard), and Roth and Kelber (2004) demonstrated color vision in the nocturnal Helmethead Gecko, Tarentola chazaliae. Fleishman and Persons (2001) studied Anolis cristatellus (the Crested Anole) and showed that when presented with a novel, moving stimulus in the visual periphery, the lizards would shift their gaze toward it. The probability of gaze shift was an additive function of chromatic and luminance contrast with the background. By systematically varying luminance for every color combination tested, they showed that there is a strong effect of color difference independent of luminance, demonstrating that this species is also capable of color vision.

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Color perception is based on a comparison of the output of two or more different classes of cone photoreceptors that differ in their spectral tuning (Kemp et al. 2015). Thus, a necessary condition for an animal to possess color vision is the existence of at least two different spectral classes of photoreceptors in its retina. All lizards that have been examined possess three or four classes of cones, and this suggests that almost all lizards likely have color vision. The neural pathways in the retina of vertebrates produce an output in the brain that is approximately log-linearly related to the rate of photon capture by the cones. Outputs from different photoreceptor classes are then compared by subtraction. The subtraction of two log-transformed values is equivalent to a division of one stimulus by the other. Thus, color perception is largely equivalent to computing the ratio of stimulation of the different cone classes (Kemp et al. 2015). This means that colors are perceived largely independent of their intensity (although there are some nonlinearities at very high and low values). The nature of the processing of color stimuli by cones makes it possible to represent color perception in a convenient manner, in a graph of the relative stimulation of each cone type (see below). The cones of a number of lizard species over a fairly broad phylogenetic range have been studied using microspectrophometry (MSP), which is the measurement of the spectral absorption properties of the pigment-containing outer segments of individual cones as well as any optical filters such as colored lens or cornea or colored oil droplets within the cones. To a limited extent, gene expression has also been utilized to identify some pigment types (e.g., Pérez i de Lanuza and Font 2014a; Yewers et al. 2015). MSP analysis of cone photoreceptors has been carried out on lizards from the following clades (Suborder, Family (genus): Iguania, Iguanidae (Polychrus, Crotaphytus, Anolis); Iguania, Agamidae (Ctenophorus); Iguania, Chamaeleonidae (Chamaeleo, Furcifer); Lacertoidea, Lacertidae (Podarcis, Zootoca); Scincomorpha, Cordylidae (Platysaurus); Gekkota, Gekkonidae (Gekko, Hemidactylus); Gekkota, Sphaerodactylidae (Gonatodes, Teratoscincus) (Loew 1994; Ellingson et al. 1995; Loew et al. 1996; Barbour et al. 2002; Bowmaker et al. 2005; Macedonia et al. 2009; Fleishman et al. 2011; Martin et al. 2015; Yewers et al. 2015; phylogenetic classifications based on Pough et al. 2016). While this represents a fairly small number of total species studied, the phylogenetic spread is fairly broad and includes both diurnal and nocturnal forms from four major suborders. The most striking outcome is the overall similarity of the findings. Only two basic patterns emerge: geckos and all others. All the non-gekkotan groups studied (all primarily diurnal) exhibit one class of double cones, with pigment in both the main and accessory cones peaking at approximately 560 nm, and four classes of single cones with peak sensitivities of approximately 365, 450, 500, and 560 nm. The cones are referred to by the relative position of their peaks as UVS (ultraviolet sensitive), SWS (short wavelength sensitive), MWS (middle wavelength sensitive), and LWS (long wavelength sensitive). Each of the cone classes in the non-gekkotan species also contains an oil droplet, or a dispersed filtering pigment, that acts as a long-pass filter narrowing the wavelengths of light that reach the pigment in the outer segment. With a few exceptions, the sensitivity peaks of the different cone classes are quite similar across taxa. The wavelength-filtering properties of oil droplets are more variable across species, but they are still broadly similar, such that the similarity of the cone-plus-oil droplet spectral sensitivities across species and taxa is fairly remarkable. The only major exceptions are found in a few species that have visual pigments based entirely, or in part, on vitamin A2-aldehyde rather than the much more common A1, which results in a shift toward longer wavelengths for all pigments. The only pure A2 species measured to date is Anolis carolinensis (Provencio et al. 1992; Loew et al. 2002), and its photoreceptor peaks are indeed shifted to longer wavelengths, as is the overall spectral sensitivity (Fleishman 2000). Three other species appear to have mixtures of A1 and A2 pigments, with a partial shift to longer wavelength peaks (Provencio et al. 1992; Bowmaker et al. 2005; Martin et al. 2015). The gekkotan species exhibit a different pattern. Four primarily nocturnal and one diurnal species have been studied carefully, and the patterns are nearly the same. All possess one morphological class of single cones (type A) and two classes of double cones (types B and C). A long wavelength

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pigment with peak sensitivity 520–540 nm was found in all type A single cones, in both members of type B double cones, and in the principal member of the type C double cones. The accessory member of the type C double cones contained either a pigment peaking in the blue (452–475 nm) or one peaking in the UV (362–365 nm) (Loew 1994; Loew et al.1996; Ellingson et al. 1995). Ellingson et al. (1995) used electroretinography and chromatic adaptation to demonstrate that there are three independent chromatic channels whose peaks approximately match the three cone photopigment classes in Gonatodes albogularis (the Yellow-headed Gecko). This broad picture is somewhat oversimplified, and there are some complexities within individual species, and notable differences between species. For example, oil droplet/cone pigment combinations are variable within some species, which raises the possibility that there may be more than four chromatic channels (Loew et al. 2002). Some species exhibit subclasses of cones with different sensitivity peaks, again raising the possibility of more than four channels (Martin et al. 2015). However, visual modeling of color perception in anoles using four chromatic channels, based on the most common cone–oil droplet combinations and the most common visual pigment peak values, has been used to accurately predict behavioral responses to stimulus versus background color differences in two different species (Fleishman and Persons 2001; Fleishman et al. 2016a). In studying lizard retinal pigments, scientists have looked for a relationship between the animals’ important visual tasks and the design of the retina. Loew et al. (2002) examined 17 species of Anolis and one species of Polychrus, and considered their light habitat as well as the color of their dewlaps. Overall, all species had very similar complements of cone classes. There was some interspecific variation in peak sensitivities, and there was considerable variation in oil droplet transmission, but in no case could the variation be meaningfully related to the typical habitat, or the color of the body or dewlap, of different species. Another possible source of variability in visual response is the relative abundance of different cone classes. Fleishman et al. (1997) considered this indirectly by comparing electroretinographically determined spectral sensitivities of six Anolis species occupying habitats ranging from unshaded grasslands to densely shaded forest. Differences in relative cone abundance will alter the shape of this spectral sensitivity curve. It was found, however, that curves were very similar across all species. Other attempts, for other species, to relate habitat light differences to cone complements have similarly failed to find a connection (Yewers et al. 2015), although Martin et al. (2015) identified some differences among species that might relate to the detection and discrimination of certain color signals. Overall, the most dramatic conclusion from studies of cone sensitivities is that diurnal lizards have inherited a broadly effective and highly conserved ancestral pattern that works well for multiple tasks in multiple conditions, and that this basic pattern has been maintained throughout the group’s diversification (Loew et al. 2002; Fleishman et al. 2011; Olsson et al. 2013; Martin et al. 2015; Yewers et al. 2015). The visual pigments in the gecko eye are different, presumably because of the group’s nocturnal origin. The diurnal geckos have retained the same basic pattern as their nocturnal ancestors (Ellingson et al. 1995). Models of Color Perception Since behavioral tests of color perception are very difficult to conduct for lizards, progress in understanding the role of sensory perception in the evolution of behavior has depended upon the ability to model the perception of color. A question that is fundamental to the study of the evolution of signal colors, is how different two colors appear to a lizard viewer? Fortunately, two rather effective methods for modeling such differences, based on cone spectral sensitivities, have been developed, and both have been shown to predict the outcomes of behavioral experiments (Fleishman and Persons 2001; Fleishman et al. 2016a). A useful way to characterize a color stimulus as perceived by an animal is to depict the ratio of stimulation of the different cones in a graphical manner. Figure 7.1 illustrates how any spectrum

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Figure 7.1  Plotting colors in lizard tetrahedral perceptual color space. The upper left graph illustrates two sample spectra, labeled A and B. The graph on the lower left shows spectral absorption functions for four cone photoreceptors from a typical diurnal lizard retina. In order to create a plot of these spectra in lizard perceptual space, each spectrum is first multiplied by each of the four cone absorption functions. The result for each cone type is then divided by the total from all four, to yield a value from 0–1 for each cone type. The graph on the right depicts lizard perceptual color space as a tetrahedron. Each apex of the tetrahedron represents one of the four classes of cones. The apex for each photoreceptor represents a value of 1, while the opposite face equals 0. Each color spectrum can be plotted as a point in the tetrahedron. The more strongly a color stimulates a given photoreceptor type the closer it plots to the apex for that photoreceptor. Here, the spectra labeled A and B from the first graph are plotted within the color tetrahedron. The difference in appearance of the two spectra A and B, referred to as the “perceptual distance,” can be approximated by calculating the Euclidean distance between the two points.

can be represented as a point in a tetrahedral color space, where each location represents the relative stimulation of the four different cone classes. If two different colors are plotted in this way, a Euclidean distance between them can be calculated, and this distance has been shown, with behavior experiments, to approximate the perceptual distance between pairs of colors (Fleishman and Persons 2001; Fleishman et al. 2016a). The second widely used model is based on estimates of noise in photoreceptor channels. Vorobyev and Osorio (1998) showed that approximations of photoreceptor noise could be used to estimate perceptual distances. They reasoned that color sensation arises from comparisons between pairs of photoreceptor channels, and the accuracy of these comparisons is limited by noise in the spectral signal (quantum noise) in each channel plus the noise within the neural channels in which the comparison occurs. If a change in color creates a change in the output in this comparison channel, but this change is smaller in magnitude than the noise, then the brain will not able to detect any change. When two color signals are just different enough to allow for a reliable discrimination they are said to be one “just noticeable difference” (1 JND) apart in perceptual space. Vorobyev and Osorio (1998) introduced a mathematical model to estimate how different any pair of color stimuli would appear in units of JND. These distances can be calculated based on a knowledge of cone spectral absorption functions, relative abundance of

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different cone classes (which impacts noise), and an estimate of the noise inherent in each photoreceptor channel. They then demonstrated that the calculated limits of spectral differences were a good match for behavioral tests of discrimination limits. Since that time, the model has been modified in several ways, including the addition of a means of estimating the impact of low overall light conditions, which elevates the baseline photon noise within photoreceptors (Vorobyev 2003). The photoreceptor noise model was introduced as a method for determining the limits (i.e., the threshold) of the ability to discriminate very similar colors. However, it has since been argued, on theoretical grounds, that perceptual distance—how different two colors will appear to an animal well beyond threshold—should scale with JND (Pike 2012). Experiments with anoles have shown that perceptual distances between colors can be accurately estimated with either JND or Euclidian distances (Fleishman et al. 2016a). How Colors Are Produced Animal colors typically result from the interaction between light and pigments and/or surface structures present in the integument. Pigments selectively absorb certain light wavelengths, whereas surface structures produce so-called structural colors through selective reflection and/or scattering of certain light wavelengths. In nonavian reptiles, pigments and structures responsible for structural colors are contained in specialized cells known as dermal chromatophores. There are three main types of these: xanthophores, iridophores, and melanophores (Bagnara and Hadley 1973; Cooper and Greenberg 1992). The overall reflectance (and sometimes transmittance) of a patch of skin is ultimately determined by the relative abundance, distribution, and layering of the three chromatophore types (Grether et al. 2004; Kuriyama et al. 2006; Saenko et al. 2013; Haisten et al. 2015). Xanthophores contain carotenoids and pteridines, which act as colored filters, preferentially absorbing short wavelengths. A range of colors, including yellow, orange, and red, are produced by carotenoids (Fitze et al. 2009), by pteridines (Kikuchi and Pfennig 2012), or by a combination of the two (Weiss et al. 2012). Iridophores contain arrays of reflecting crystalline guanine platelets that produce structural colors through a combination of reflection, incoherent and coherent scattering (mainly thin-layer interference) (Bagnara et al. 2007). Disorganized arrays of platelets generate white (i.e., broadband) reflectance, while highly organized and regularly spaced platelets give rise to monochromatic reflectance (Saenko et al. 2013). Iridophores are also responsible for the production of short wavelength colors (blue, violet, or ultraviolet) found in some taxa. Melanophores contain melanin, which absorbs most wavelengths of light, including light in the UV range. In general, the spectral purity of structural colors is increased by increasing melanin within the melanophore layer (Quinn and Hews 2003). Other structures found in the integument, such as collagen fibers and the layer of connective tissue (fascia) separating the skin and muscle, may also contribute to color production (Macedonia et al. 2000). Although lizard colors are often dichotomously categorized as pigment-based or structural, this is an oversimplification because most lizard colors result from an interaction between pigmentary and structural elements (Shawkey and Hill 2005; San-José et al. 2013). Color patches should be thought of as complex phenotypic traits, the components of which may evolve independently and function as truly multicomponent signals (Grether et al. 2004). The mechanisms of color production have important implications for our understanding of the mechanisms that allow color patches to effectively signal differences in individual quality (see below). For example, the content of carotenoids within the xanthophores may arise from a physiological trade-off between carotenoid-based coloration and immune or antioxidant functions (Olsson et al. 2013). Similarly, the regularity and spacing between guanine platelets within the iridophores may be affected by various stressors, by testosterone-dependent melanin expression, or a combination of both (Quinn and Hews 2003; Cox et al. 2008; Fitze et al. 2009; San-José et al. 2013).

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Two detailed phylogenetic comparative analyses of signal color in dwarf chameleons (StuartFox et al. 2007) and anoles (Nicholson et al. 2007) concluded that there is little or no phylogenetic signal for signal color. This means that colors evolve relatively rapidly, without strong phylogenetic constraint, so that relatedness of species generally is not predictive of color similarity. We thus expect colors to evolve in response to selective pressures for signal effectiveness. Some Functions of Signal Color and Their Influence on Signal Design Elicitation of Attention Fleishman and Persons (2001) experimentally quantified the relationship between signal color and attention elicitation in Anolis cristatellus. Given the overall similarity of visual processing of color among lizards, the conclusions from this study can be generalized to other species. In the experiments, the visual periphery of lizards was stimulated by a small flag moving against a colored background. If the lizard noticed the stimulus flag, it would shift its gaze abruptly toward it (the visual grasp reflex), to view it with the fovea. The probability of detection was determined as a function of the contrast between the stimulus and its background. They found that detection probability was a simple additive linear function of two factors, with nearly equal weight: the luminance contrast (CL) and the chromatic contrast, (CC) between the stimulus flag and the background. These variables were defined as

CL =

( Ls − Lb ) , ( Ls + Lb )

where Ls is the stimulus luminance and Lb is the background luminance. Luminance is equal to the stimulus (or background) spectrum times the spectral sensitivity function. CC is defined as the Euclidean distance between the stimulus and the background in the tetrahedral color space of A. cristatellus. Fleishman et al. (2016a) later showed that Euclidean distance could be adequately replaced with distance in JND units derived from photoreceptor noise modeling (see above). For nearly all lizard species, luminance is equal to the spectral response of the double LWS cones (Fleishman et al. 1997). This makes it possible to estimate the effectiveness of any stimulus color for attention elicitation if one knows its spectral reflectance (and, in some cases, transmittance), the typical background color and the light conditions under which it is viewed. These results can be used to compare different signal colors under different habitat light conditions to look for evidence of the role of selection for attention elicitation on the evolution of color signals. Several studies have used this approach to compare the signals of closely related species, or populations that occupy different light environments whose signal colors have diverged. The logic is that if different light environments favor different colors for optimal sensory stimulation, we expect to see divergence in signal color that favors high detectability (i.e., high likelihood of eliciting attention) in each habitat. The idea that animal signals will diverge in physical form due to differences in effectiveness in different habitats is known as the “sensory drive hypothesis” (Endler 1992). Two habitat variables are particularly important for making these estimates. The spectral irradiance (Irrad) refers to all of the light striking a surface from a full hemisphere normal to the surface. Spectral radiance (Rad) is the light intensity and spectrum emanating from a finite area of the surface (typically about 4° of solid angle). If the surface of interest reflects diffusely, then Rad = (Irrad × Ref)/π, where Ref is the the spectral reflectance (Fleishman et al. 2006). Surfaces with directional reflection properties, such as iridescence, have to be measured under natural illumination and viewing geometry in order to determine their radiance (Fleishman et al. 2006). In lizards that signal with thin dewlaps or frills, spectral transmittance must also be accounted for (Fleishman et al. 2006; Klomp et al. 2017a). In order to assess backgrounds against which signals are presented,

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one can sample radiance patches directly in the field, or use the reflectance of known background objects and habitat irradiance to calculate background radiance. However, this latter approach does not account for the presence of natural patches of light from the sky or sun, or the effects of glare from smooth surfaces as natural background radiance elements (see Fleishman et al. 2016b), which are among the most common background radiance patches in most habitats on a sunny day. One can measure or calculate the spectral radiance of the signal of interest—typically by measuring reflectance and transmittance in the laboratory and using field-measured irradiance values—and compare signal to background radiance to determine a relative detectability. One additional factor that has to be taken into account is that nearly all color vision systems have some mechanism to correct for the spectral quality of the ambient light, so that the perceived colors of objects do not change completely when the illuminating spectrum changes (= color constancy). This process is known as chromatic adaptation. In most models, this is calculated by measuring the average light striking the eye and assuming that all cone classes give equal output for that spectral stimulus. Leal and Fleishman (2004) compared dewlap visibility of four allopatric populations of Anolis cristatellus in Puerto Rico. They measured spectral irradiance striking the dewlap from front and back, as well as background spectral radiance at each display location in the field. Reflectance and transmittance data for dewlaps from all four populations were used to estimate signal effectiveness at each display location. It was found that dewlaps from the dry habitats were most detectable in the dry habitats, whereas the dewlaps from the moist habitats were most detectable in the moist habitats. Thus, dewlap coloration among populations diverged in the direction of increased effectiveness in each lizard’s own natural habitat. Stuart-Fox et al. (2007) studied aggressive signaling in 21 species of dwarf chameleons that occupy a range of habitat types with differing light conditions. Signal color pattern covaried significantly with habitat type, but only in the UV portion of the spectrum. Lizards from darker habitats exhibited relatively greater UV reflectance, and modeling showed that the difference resulted in increased effectiveness for attention elicitation in each habitat type. Luminance contrast appeared to evolve toward a common, moderate level across habitats, and it was suggested that selection for luminance might be favoring a balance between detectability by conspecifics and reduced visibility to predators. McLean et al. (2014) studied throat-color conspicuousness in two distinct populations of Ctenophorus decresii (the Tawny Dragon) in South Australia, which exhibit differences in color. Chromatic and luminance contrast was tested for typical bare rock backgrounds, and typical lichencovered rocks from each habitat. Chromatic and luminance contrast against bare rocks was similar for each native population. However, the predominant lichen variety differed from north to south. The northern lichens tended to be blue in color, resulting in greater visibility of the northern orange throat colors. The southern lichens tended to be orange in color, which made the blue throat colors of the southern males more detectable, supporting the hypothesis that signal color divergence was, in part, due to selection for increased visibility under local light conditions. The three studies described above suggest that, at least in certain cases, selection for greater signal visibility (i.e., greater effectiveness at attention elicitation) has resulted in signal color divergence. However, results from some other studies have come to different conclusions. Two detailed studies have been carried out on multispecies sympatric communities of Anolis lizards in Puerto Rico and Jamaica. Fleishman et al. (2009) measured dewlap color and habitat light at display locations of four Puerto Rican species, while Macedonia et al. (2014) did the same for five Jamaican species. In both studies, the authors ranked the dewlap detectability of each study species in each set of habitat light conditions. Although on both islands the species’ habitats ranged from direct sun to heavy shade, and light measurements were taken at times and locations when the lizards displayed their dewlaps, the prediction that each species would exhibit the most effective signal color in its own habitat failed. Instead, it was found that dewlaps that were red or orange in color, and of relatively low luminance, were the most visible in all of the habitats, and the rank order of the different species did not change from one habitat to another.

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The reasons for this result are straightforward. First, the spectral quality of the backgrounds was nearly the same across all of these moist tropical habitats: all were dominated by green vegetation, as well as some bright patches from sun and sky. The irradiance that illuminated the dewlaps varied due to the large differences in canopy cover, but chromatic adaptation of the color vision system removed the effects of this difference. As a result, the chromatic contrast for a given dewlap against the background differed very little from one habitat to the next. Dewlaps that were red or orange exhibited higher chromatic contrast, in all habitat types, than did yellow, white or brown dewlaps. Luminance contrast effects also proved to be relatively unimportant even though some dewlaps were dark (and red) and others were very light (white or yellowish). In each of these habitats, the background radiance consisted of discrete colored patches: some very dark (e.g., shadows, bark, and soil), some medium (green vegetation), and some very bright (glare due to specular reflectance of sunlight off smooth leaves, and small patches of blue sky or sunlight visible through the vegetation). Given this array of light and dark patches, low-luminance dewlaps had high contrast against the high-luminance background patches, and low contrast against the low luminance patches, while the opposite was true for high-luminance dewlaps. The overall result was that dewlap luminance contrast with background luminance patches had little impact on dewlap visibility (also see Fleishman et al. 2016b). We can ask, then, whether habitat light has had any impact on the evolution of these anoline dewlap colors. Figure 7.2 shows plots of dewlap, body, and background spectral radiance in lizard perceptual space for six sympatric species from Puerto Rico (Fleishman and Leal, unpublished). The spectral quality of backgrounds for the different species overlaps extensively. None of the six species have dewlap colors that overlap with the background. However, there are differences in chromatic contrast with the background among the species that are consistent across all of the habitat types. Thus, although the habitats differed greatly in shade level, total intensity, and spectral

Figure 7.2  A  plot of color measurements (spectral radiance) of dewlaps, bodies, and background patches for six species of Puerto Rican Anolis lizards. Each species is represented by a different color. The four apices of the tetrahedron represent the relative stimulation of the UVS (top, purple), SWS (blue), MWS (green), and LWS (red) single cone types as illustrated in Figure 7.1. Each sample represents the appearance of a color to the relevant species after chromatic adaptation to the light striking the eye. (a) Samples of background radiances measured at display locations for six species. Note the high degree of overlap among the different backgrounds. (b) Mid flank body colors of the same six species. Note that body colors and background colors occupy approximately the same, overlapping region in color space. (c) Dewlap colors (each color is a different species) and background colors (all species are summed, and the background colors from all species are shown in gray). Dewlap colors do not overlap with background colors. For the most part dewlap colors of the different species do not overlap, but there is some partial overlap among three of the species shown in brown, yellow, and black. Dewlap and body colors cover a volume of space rather than a single point, because local differences in illumination and imperfect color constancy mechanisms result in slightly different perceived colors for the same dewlap and under different viewing conditions. The colors shown in red and orange (which are in fact red and orange dewlaps) are more distant in color space from the background colors and are expected to be more detectable than the other dewlap colors.

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and relative luminance (i.e., the background luminance relative to the habitat irradiance), their chromatic properties were not actually very different. The relative lack of difference in certain critical features of the light environment seems to account for the fact that the same dewlap colors were most visible in all habitats. However, there is another more difficult question. In both of these studies with Anolis, red and/ or orange dewlaps were consistently found to have the highest calculated visibility, and indeed it can be shown that these colors are the most distant in perceptual color space from the typical background colors. In both of these studies, only two of the species had dewlaps with these red or orange colors, while others possessed yellow or white dewlaps. Nicholson et al. (2007) surveyed the dewlaps of 140 Anolis species and showed that yellow is by far the most common dewlap color, and white is a fairly common color as well, even though red or orange appear to be the most detectable colors in most anoline habitats. Studies of some other taxa have led to similar conclusions. Pérez i de Lanuza and Font (2015) compared the detectability of ventral body colors of the Common Wall Lizard (Podarcis muralis). Multiple color morphs are found sympatrically in the species, and males possess white, yellow, or orange ventral color patterns. They found that orange was consistently the most visible color against natural backgrounds, followed by yellow, and then white. All morphs also possessed highly detectable UV-blue scales positioned laterally along the body. There was no evidence that different morphs were signaling against different backgrounds. The existence of stable morphs that differ in detectability suggests that these lizards are not necessarily evolving toward the signal with the highest visibility. Teasdale et al. (2013) reached a very similar conclusion in their study of polymorphic throat colors of Ctenophorus decresii in Australia. Taking these results together, we find that in most cases orange and red are the colors that are predicted to be most effective at eliciting attention in most natural habitat light conditions and backgrounds. Why then are other colors—particularly yellow and white—also commonly found as signal colors in many different lizard groups? We offer three non-mutually exclusive hypotheses to explain this phenomenon. First, selection for visibility may only act as a broad constraint, rather than a strong directional selective force. Selection for other signal color functions (e.g., species discrimination), might result in the evolution of colors that are sufficient, but not optimal, for attention elicitation. A second hypothesis is that increased visibility adds a cost of increased detection by predators, and that many species evolve colors that balance the advantages of high visibility to conspecifics against the cost of high visibility to predators. Where polymorphic colors appear, this cost–benefit balance might result in distinctly different evolutionarily stable color polymorphisms within a population (Teasdale et al. 2013; Pérez i de Lanuza and Font 2015). A third hypothesis for the observed prevalence of signal colors that are not optimally detectable is that there is an effect of total habitat light intensity, that has not been accounted for by the models described above. It is known that over a large range of light intensities color perception is independent of total light intensity and the perceptual models described above for dewlap detectability assumed, as do most models of animal color perception, that color perception is independent of light intensity. However, we know from human studies and photoreceptor noise models of perception, that in low total light color discrimination becomes more difficult, and darker colors that reflect (or transmit) fewer total photons become harder to identify and distinguish from other colors (Vorobyev 2003; Osorio et al. 2004; Fleishman et al. 2016b). The ambient light intensity at which this reduction in discrimination occurs is not well established. However, since lizards usually have small eyes (and therefore small pupils) it is quite possible that in shaded conditions the total photon flux from the body or dewlap becomes small enough to limit color discrimination. Shady habitats not only have lower total irradiance, they also have proportionally less long wavelength light (Endler 1993). This suggests that red and orange colors, which are highly visible in well-lit habitats, may be difficult to discriminate from other colors in heavily shaded habitats. This might reduce their visible contrast against some backgrounds, or might interfere with their effectiveness for other functions, such as species

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recognition (Fleishman et al. 2016b). While this idea might explain some of the puzzling results described above—in particular the widespread presence of white and yellow in shaded habitats, and the prevalence of red, orange, and blue in open habitats (see Fleishman 1992)—it remains to be tested empirically. Some additional signal properties have been suggested that may have evolved in response to selection for effectiveness at drawing and maintaining attention. Pérez i de Lanuza and Font (2016) demonstrated that at the border of the ventral and lateral body region many lacertid species juxtapose a predominately short wavelength signal against a predominately long-wavelength color signal, producing a strong chromatic contrast stimulus that is likely to enhance signal visibility. A similar juxtaposition of short- and long-wavelength-reflecting color patches is found in the dewlaps of some Anolis species (Nicholson et al. 2007). Another interesting signaling strategy was described by Pérez i de Lanuza and Font (2014b): iridescent head coloration in the Iberian Emerald Lizard (Lacerta schreiberi). Iridescent colors change spectral quality and/or intensity with changes in viewing angle. By measuring from different view angles and using visual detectability models for the lizard visual system and that of a predatory bird, they showed that when viewed from above, with the sun behind the viewer (typical of a predatory bird in midday) by a typical bird visual system, the head color is significantly less visible than it is when viewed through a lizard visual system on the ground (with the light source at approximately 90o). This difference results from a combined effect of viewing angle and visual system differences. Thus, the use of iridescent signaling can potentially enhance signal visibility without strongly increasing predation risk. Categorical Identification Color signals are often used to identify individuals as belonging to some larger group of individuals. Examples include species recognition, sex identification, or divisions of populations into distinct behavioral groups. The mechanisms controlling and producing these discrete color categories can be quite different, ranging from straight genetic control (e.g., species identification) to hormonal effects that may be organizational (operating during development) or activational (responding to seasonal or other more immediate cues) (Sinervo et al. 2000). From the sensory perspective, signals of this type must be sufficiently distant in perceptual space from potential confusing stimuli to allow each category to be easily and reliably recognized. This function will be supported if the spectra of the colors are designed such that small changes in their properties elicit little or no change in sensory output. The achromatic channel (luminance) is usually not useful for this kind of signaling, because apparent brightness changes dramatically with lighting conditions and with the luminance of nearby objects. In general, the chromatic signal is much more useful because, in combination with chromatic adaptation, chromatic stimuli tend to produce nearly the same sensation under a wide range of environmental light conditions. It is widely hypothesized that color patterns play an important role in species recognition (Rand and Williams 1970; Williams and Rand 1977; Losos 2009), which is important in the context of mating, to prevent hybridization. It can also play an important role in interactions between members of the same sex in preventing wasted energy and the risk of engaging in agonistic interactions with other species (Korner et al. 2000). Losos (1985) experimentally demonstrated a role of dewlap color in species recognition in Anolis marcanoi (the Red-fanned Stout Anole) by manipulating dewlap colors with paints. Robotic lizards have been used to demonstrate the importance of dewlap color and/or pattern for species recognition in Anolis grahami (Graham’s Anole) (Macedonia et al. 2013) and Draco melanopogon (the Black-bearded Gliding Lizard) (Klomp et al. 2017b). From the sensory system perspective, species recognition can occur in two distinctly different contexts: close range or long distance. In typical courtship or agonistic interactions, the individuals involved will be viewing one another with the highest acuity part of the retina (i.e., attention has

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been gained) at very close range. The animals will be able to perceive a full array of colors and patterns present on each individual’s body. All that is required is that the patterns and colors can be perceived, and that they can reliably be distinguished from patterns of other sympatric species. In an elegant series of papers, Williams and Rand (Rand and Williams 1970; Williams and Rand 1977) showed that if one considers dewlap color, pattern, and size together, there is more than enough unique information for each species to allow species in complex anoline communities to reliably identify and distinguish one another. Male territorial lizards frequently produce long-range displays that function to attract females to, or keep females within, the territory and to discourage conspecific males from approaching (Carpenter 1965; Stamps 1977; Fleishman 1992). The intended viewers in this case are fairly distant and will often be inattentive, and therefore may receive the signal in their visual periphery. In this case, the effectiveness of the signal will be greatly enhanced if it provides a rapid, unambiguous cue that a lizard of the same species is present. Under these viewing conditions, much less color and pattern detail will be visible (see Section “The Eye and Visual Acuity”). Fleishman et al. (2017) showed that for the dewlaps of Anolis under these conditions, all that is likely to be visible is a patch that is perceived as the average of all colors or patterns present on the dewlap. This suggests that the base color that covers most of the dewlap is an important signal. Thus, signals are expected to evolve such that a simple flash of uniform color detected in the visual periphery is sufficient to inform viewers of the presence of a conspecific. If the signal is ambiguous (that is, if it may be confused with that of another species or a random color patch in the environment) potential mates might wander away or potential rivals might move closer in order to further investigate the area as a potential new territory. We would predict that lizards living in sympatric communities would evolve colors that are easily discernible from other color patterns (conspecific dewlaps and background colors) in the environment. Figure 7.2 summarizes dewlap colors of six sympatric species of anoles in Puerto Rico. The prediction holds up to some extent, but not completely. The dewlap colors are dispersed over visual space and do not overlap with habitat radiance patches. However, in each Anolis community that has been studied, there are a few species whose dewlap colors overlap in visual space (e.g., see Figure 7.2 and Macedonia et al. 2014). This suggests that in some cases other signal components, such as motion patterns (below), may play an important role where color signal information alone is insufficient to clearly identify the species. There are a number of cases where dramatic color differences occur within species or populations, often behaviorally defining subsets of the population. One well-known example has been described for Uta stansburiana (the Side-blotched Lizard), in which three male color phenotypes are found within a single population, and a different behavioral phenotype is associated with each color (Sinervo and Lively 1996). In this example, the color of each population is distinct and discrete in both spectral quality (blue vs. orange vs. yellow) and patterning. Individual Comparison and Assessment Here we consider a diverse set of roles for color that can be grouped under the heading of comparison and assessment among individuals in the same population. While many different kinds of information may be signaled, from the sensory system point of view, the problem is similar. To be effective, there must be detectable among individual variation in signal colors or patterns that correlates with biologically meaningful differences. In these cases, rather than there being a small number of discrete, easily recognized colors, there is essentially continuous variation in the color pattern. Several studies of lizards have documented that biologically relevant differences among individuals result in differences in color. Examples include effects of parasites, disease and immune system function (Molnár et al. 2013; Megía-Palma et al. 2016), overall body condition and/or performance (Olsson 1994; Pérez i de Lanuza et al. 2014; Plasman et al. 2015), reproductive status

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(Cuadrado 2000; Baird 2004; Chan et al. 2009), age (Ellingson et al. 1995; Olsson et al. 2012), and stress level (Fitze et al. 2009). Demonstration that some biological feature correlates with color variation does not necessarily mean that the information is utilized by conspecifics. Demonstrating that color differences are perceived and utilized by conspecifics is quite challenging. The most commonly demonstrated impact of color variation is its influence on the outcome of intra-sexual agonistic encounters (Thompson and Moore 1991; Whiting et al. 2003; Stapley and Whiting 2006; Whiting et al. 2006; Bajer et al. 2011; Hamilton et al. 2013; Baird 2014; Steffen and Guyer 2014; Martin et al. 2016; Abalos et al. 2016). Precopulatory female mate choice in lizards is notoriously difficult to demonstrate (Tokarz 1995; Olsson et al. 2013), but in a few cases, it has been shown that male coloration influences association or mating preference of females (Kwiatkowski and Sullivan 2002; Bajer et al. 2010) and color-assortative mating has been demonstrated for Podarcis muralis (Pérez i de Lanuza et al. 2013, 2016). In order to influence the behavior of signal receivers, there must be some evolutionary constraint that links variation in color to the relevant biological variation, that is, the expression of the color signal should be “condition dependent.” The relationship between color and biological characteristics is currently a subject of intense scrutiny. In most cases, there seems to be some mechanistic connection involving the complex interactions of energetics, hormonal expression, and development (and/or maintenance) of chromatic mechanisms (Olsson et al. 2013). Interestingly, the most intensively studied link in other taxa—a link between diet and carotenoid-based colors—appears to be very rare in reptiles (Olsson et al. 2013). In addition to direct physiological trade-offs, it is also possible that the possession of conspicuous colors could result in indirect costs—through retaliation during agonistic interactions, or from increased need for predator avoidance—that serve as an honesty constraint (Martín et al. 2016). For example, Baird (2008) showed that artificial addition of conspicuous coloration in collared lizards slowed their growth by increasing their need to avoid predators. Ligon and McGraw (2016) showed that artificially adding aggressive coloration to male Veiled Chameleons (Chamaeleo calyptratus) caused them to be physically attacked more often during agonistic interactions. The nature of the costs and developmental stresses associated with production of different classes of coloration (e.g., structural vs. pigment-based) is a complex topic beyond the scope of this chapter (see Olsson et al. 2013 for an excellent review), but the mechanistic factors that determine signal honesty and reliability in this case may be as important for understanding signal design as sensory factors. From the sensory system perspective, the critical feature of signals that provide information about subtle continuous variation among individuals is the extent to which these differences can be reliably discriminated. Condition-dependent color variations are inevitable, but we can only expect them to evolve into signals if these color variations can be detected and discriminated. Small differences in spectral shape will be much more effective as signals of individual quality than differences in overall intensity (or luminance), because luminance varies greatly with specific local lighting conditions, whereas perceived color is much less variable due to perceptual color constancy mechanisms. Figure 7.3 shows a typical example of a color spectrum, such as might be seen on a lizard’s body, and illustrates key descriptive attributes. Most spectra have distinct wavelength regions of high and low reflectance, with fairly sharp transitions between them. The transitions from high intensity to low intensity are often characterized by the wavelength of steepest negative change (the cut-off wavelength, λ cut-off ). The change from low to high reflectance is often characterized by the wavelength where the steepest positive change occurs (the cut-on wavelength, λcut-on). Two similar spectra will be most reliably discernible when their regions of most rapid change occur over a spectral region where spectral absorption of photoreceptors is changing rapidly and where two photoreceptor absorption spectra overlap. In these spectral regions, small changes in the shape

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Figure 7.3  S  ome features of a typical natural color spectrum. In many natural colors, spectral reflectance shifts rapidly between high and low values over a relatively small range of wavelengths. A rapid decrease in reflectance is characterized by the wavelength value, λcut-off, while a rapid increase in reflectance with wavelength is characterized by the wavelength λcut-on.

or position of the spectral stimuli will result in the relatively large changes in sensory output (and the ratio of output) from the photoreceptor cells. For example, Ellingson et al. (1995) showed that male head colors in the diurnal gecko Gonatodes albogularis range from orange to yellow, based on the position of the cut-on wavelength (Figure 7.4). Male heads turn more yellow as they age, and yellow-headed males tend to be larger, more dominant, and preferred by females. The position of the cut-on wavelength of male heads ranges from approximately 525 to 575 nm, which corresponds well with a region of overlap and rapid change in spectral absorption of the two long-wavelength photoreceptors. This means that even small differences in head color should be reliably detected because of the high spectral resolution in this portion of the spectrum (Figure 7.4). In general, we expect to see signals with cut-on (or cut-off) wavelengths with variation that is centered around a wavelength region where different photoreceptor classes overlap and are changing steeply, and these regions will tend to be similar across species. Saturated orange and orange-red are fairly common in lizard chromatic signals (e.g., Hamilton et al. 2013), and such colors tend to have a cuton wavelength in the 540–560 nm range, which is where MWS and LWS photoreceptors typically overlap. The UV-blue part of the visible spectrum has been shown to be important for communicating individual quality in several species. For example, Pérez i de Lanuza et al. (2014) found that in Common Wall Lizards (Podarcis muralis), which have physically separated UV-blue and long wavelength (orange, yellow, and white) signals, it is the UV-blue signals that vary with measures of individual male fighting ability (size-independent bite force) and condition. A number of other studies have found correlations between individual quality and/or fighting success and short-wavelength signal variations (Stapley and Whiting 2006; Bajer et al. 2010, 2011; Martín et al. 2016). In some cases, the method of effectively signaling quality variation with short wavelength signals is similar to that described above: the different UV-blue color variants have a cut-off wavelength that varies over a spectral range where the UV and blue photoreceptors overlap. Such a pattern is observed in Platysaurus broadleyi (Broadley’s Flat Lizard) (Stapley and Whiting 2006; Fleishman et al. 2011) (see Figure 7.5). Throat colors of males vary in the UV-blue range, and these variations correlate with fighting ability. Moreover, Fleishman et al. (2011) demonstrated that P. broadleyi has an unusually high level of sensitivity in the UV that is probably due to an unusually high density of UV-sensitive photoreceptors. Modeling showed that the high density of UV photoreceptors reduces noise in the UV-blue chromatic channel, making it possible for animals to discriminate nearly twice as many individual throat colors. An alternative mechanism is seen in several other species, where signal colors consist of a broad spectral pattern in which the height of the peak in the UV region varies, and this is combined with another, long-wavelength spectral element that is much less variable. This pattern is

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Figure 7.4  T  he upper plot shows the spectral reflectance (relative to a white standard) of the head of two different individuals of Gonatodes albogularis that represent two ends of the range of head coloration observed in this population. The lower plot shows the spectral absorbance of the three cone photoreceptors from the Gonatodes retina. Note the range of different colors spans the wavelength range where the middle- and long-wavelength photoreceptor pigments overlap and change most steeply, which will enhance the ability of conspecifics to distinguish among the different head colors. (From Ellingson et al. 1995.)

seen, for example, in the European Green Lizard (Lacerta viridis) (Bajer et al. 2011) and Podarcis muralis (Pérez i de Lanuza et al. 2014), and is illustrated in Figure 7.6. The variation in height of the UV peak, relative to the less variable long wavelength element, presumably allows for effective discrimination among the different colors because the color sensation is based on the ratio of long wavelength:short wavelength stimulation.

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Figure 7.5  T  he upper graph shows spectral absorption of the four cone/oil droplet combinations in the retina of the lizard Platysaurus broadleyi. The bottom graph shows some typical variants of male head color. Notice that the variation is centered on a spectral region where the UVS and SWS photoreceptors overlap. (From Fleishman et al. 2011.)

Figure 7.6  V  ariation in reflectance of male UV-blue coloration in Podarcis muralis. Bite force correlates with peak total reflectance in this range and wavelength of peak reflectance. The combination of a variable short wavelength intensity with a much less variable long wavelength reflection provides a mechanism for discrimination of color by comparing peaks in short wavelength to long wavelength regions. (From Pérez i de Lanuza, unpublished.)

VISUAL COMMUNICATION 2: MOTION SIGNALING Lizards of nearly all families rely extensively on visual motion perception for survival (Fleishman 1992; Nava et al. 2012). Motion stimuli are used to detect and identify suitable living prey, detect approaching predators and for communication (Fleishman 1992). Lizards are not unique in this dependence on visual motion, and the basic neural principles of visual motion perception appear to be widely shared among visually oriented animals (Stein and Gaither 1983; Borst and Egelhaaf 1989).

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The only published studies of the response of individual neurons to visual motion in lizards described visually responsive cells in the optic tectum of Iguana iguana (the Common Green Iguana) (Gaither and Stein 1979; Stein and Gaither 1983). The optic tectum is the most important brain target for visual motion perception in lizards, because it is where neurons that respond to motion in the visual periphery connect to motor neurons that cause shifts of attention and gaze toward the moving target (Ulinski et al. 1992). A number of important generalizations have emerged from these studies. First, the basic response properties of the tectal neurons are very similar to responses from homologous brain areas in other vertebrates. This suggests that the neural basis for motion processing is, to a large extent, evolutionarily conservative across vertebrates. The majority of the motionsensitive cells exhibit a directionally- selective response and most cells exhibit velocity tuning. The cells fall into three velocity-tuned categories: high, middle, and low. The receptive fields of the motion-sensitive cells mapped to different regions of visual space are circular or elliptical in shape and are larger at a greater distance from the fovea. Tectal neurons typically respond with a strong burst of increased activity to motion onsets and offsets, or to a flash of light. Most of the cells habituate rapidly to a moving or flashing stimulus, but regain sensitivity after 20–30 s (Stein and Gaither 1983). These results suggest that three attributes of visually moving stimuli that influence neural response are critical: the location of the moving stimulus in visual space, the direction of movement, and angular speed across the retina. Because of their directional selectivity and their tendency to fire strongly at the onset of motion, populations of tectal cells are well designed to encode changes of motion direction, and stops and starts. With each shift in stimulus direction, stop, or start, a new population of cells will fire in unison, precisely marking the timing of these transitions. Persons et al. (1999) recorded tectal-evoked potentials from four species of Puerto Rican Anolis. Although this method yields much less detail than single-cell recordings, the results are in general agreement with those of Stein and Gaither (1983). Tectal potentials are evoked by stimulus motion onset and by flashing lights on and off. The potentials exhibited velocity tuning, and showed rapid habituation. Response amplitudes are directly proportional to the stimulus- versus backgroundluminance contrast, which is also seen in behavioral responses. These neurophysiological results have been supplemented by behavioral studies, which have utilized the visual grasp reflex to investigate the relative effectiveness of different patterns of motion in eliciting attention. Fleishman (1986, 1992) stimulated Anolis auratus (the Grass Anole) with stimulus lures presented in the visual periphery, which moved up and down in different motion patterns. The response was strongest to motion amplitudes of 0.2°–0.3° of visual angle for all patterns of motion. By far the strongest motion stimulus pattern was a low-frequency (~1.5 Hz) square wave. This can best be thought of as a step function: a movement in which a stimulus object abruptly jumps to a new position and stops. Fleishman (1986) also presented a variety of smoothly varying, sinusoidal, up and down stimuli, of frequencies ranging from 0.5 to 10 Hz. The response probability was significantly lower than to step functions. Among the different sinusoidal stimuli, it was found that response probability remained the same for frequencies up to 4.5 Hz and then declined rapidly at higher frequencies of motion. Additional studies of five other Anolis species yielded similar results (Pallus et al. 2010; Steinberg and Leal 2013, 2016), but also found a second response peak to step stimuli of higher amplitude: approximately 1.5° of visual angle. Pallus et al. (2010) compared detection probability to the velocity of motion of a computer-­ generated stimulus dot moving linearly across a small screen. Similar to results from tectal recordings, they found that the behavioral motion-detection reflex exhibited velocity tuning. They also showed that a slow moving, habituating pre-stimulus motion stimulus reduced response to slower moving stimuli, but not faster ones. They concluded that there might be at least two different motion channels, with different velocity tuning underlying the response. Peters and Evans (2003a) studied the visual orientation responses of the Jacky Lizard (Amphibolurus muricatus) in response to computer-generated tail-flick displays (the opening movement of their natural display). By creating realistic animations of the motion of lizard tails, they

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were able to explore the impact of different parameters—timing, amplitude, and motion speed— on the effectiveness of the display in eliciting visual attention. Neither amplitude nor speed of the motion significantly influenced response probability, whereas a longer duration display significantly increased response probability. Interestingly, the strongest stimulus was a series of fast up and down movements presented intermittently over a long total duration. This pattern might be particularly effective because it would tend to repeatedly trigger motion onset responses in neurons of the optic tectum. Nava et al. (2009) tested for sex differences in the visual grasp reflex response in Sceloporus graciosus (the Sagebrush Lizard) in response to a black and white spinning disk. They found that females responded more rapidly than males. Nava et al. (2012) presented Sceloporus undulatus (the Fence Lizard) with motion by employing robotic lizards and found that males responded more quickly to slow up and down movements typical of territorial displays, while females responded with shorter latency to rapid up and down movements, typical of male courtship displays. These sex differences in response probably arise from higher order sensory processing, since studies of visual physiology in other species have not revealed any male–female differences in peripheral visual system response (e.g., Fleishman et al. 1997; Persons et al. 1999; Loew et al. 2002). Two sets of studies have examined the effects of visual noise, in the form of windblown vegetation, on the behavioral response to visual motion stimuli. Fleishman (1986) used the visual grasp reflex assay described above to test the impact of background motion on response to various different motion patterns in Anolis auratus. Prior to and/or during the motion stimulus presentation, a piece of artificial vegetation was set in motion in a sinusoidal pattern typical of windblown plant motion. When stimulus motion was similar in waveform to the background movement, response probability was significantly reduced. However, when the stimulus was a step pattern (i.e., a square wave rather than a sine wave), or when the stimulus pattern was sinusoidal at a higher frequency than the background (but less than 7 Hz), response probability was not reduced by the moving background. The effects of differences in velocity and acceleration between background and stimulus motion were also tested. When the stimulus moved with only a higher velocity, or with only higher acceleration, relative to the background motion, response probability was significantly reduced. However, when the stimulus accelerated more rapidly than, and moved more quickly at peak velocity than the background, the background movement did not reduce the response. Thus, background vegetation movement significantly reduced response unless the stimulus motion pattern moved at a higher frequency or with abrupt step patterns that included high acceleration and high velocity. Peters (2008) tested the effects of windblown vegetation on detection response latency in Amphibolurus, using captive individuals in a large arena and presenting them with the motion of a radio-controlled robotic tail. The visual background consisted of a dense collection of typical native plants. He tested the latency until the occurrence of a visual orientation response toward the moving tail in two conditions: with no wind, and with moderate wind generated by fans. The presence of windblown plant motion significantly delayed the time it took to orient toward the flicking robotic tail. Form, Function, and Constraints on Motion Signals Lizards regularly use body motion patterns in visual signaling. There are a relatively small number of possible ways a lizard can create a moving signal, and all seem to be used by some species. Most common are the up and down motion patterns of the body created by extending one or two pairs of limbs (Jenssen 1977), or bending of the neck. Asynchronous movement of rear and front limb pairs can also produce a smaller amplitude of horizontal motion. Motion signals can also be produced by the arms that can be waved forward or back (Peters et al. 2002; Font et al. 2012a) or the tail that can be moved in a variety of patterns. Many species possess an expandable throat fan that can be extended and retracted (a dewlap) either alone or in combination with motion of the head

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and body. The main physical limitation on these movements is the amplitude of their extent. Up and down movements are limited by limb dimensions. Tail movements are less limited, although the slenderness of the tail can limit its visibility from distance. Lizards are capable of completing individual movements in 30–35 ms (Fleishman and Pallus 2010), which is faster than the temporal resolving power of the eye, and thus the rapidity of up and down motion is not a constraint, although highly repeated high-frequency motion may be energetically constrained. It is interesting to consider what constrains some motion patterns to be, at least to some extent, honest signals. Lizard often display several times a minute for many hours of the day, suggesting that there is not high energy cost to each display. It is possible that for some very abrupt display movements, the maximum angular velocity of the display depends on sender quality, but it does not appear that lizards have any difficulty making abrupt movements that are faster than the eye can resolve (Fleishman and Pallus 2010). The most likely general and widespread cost to motion signals is the risk of attracting predators. Since many predators of lizards are themselves very motion sensitive (e.g., snakes and birds), there may be a strong selective pressure to minimize the use of motion displays and to evolve signal movements that are highly effective but that do not need to be repeated more often than necessary. Steinberg et al. (2014) studied the territorial displays of Anolis sagrei on small islands in the Bahamas. They compared display motion pattern and frequency on islands that lacked major predators to islands where predatory Northern Curly-tailed Lizards (Liocephalus carinatus) had been experimentally introduced. Anoles on the islands with predators exhibited significantly reduced amplitude of movements in their displays, which resulted in a smaller active space (area over which displays would be detected) for both conspecifics and predators. Quantifying and Modeling Motion Signals In order to study motion signals and motion noise caused by windblown vegetation, it is necessary to quantify them. The motion in many lizard visual displays consists primarily of vertical axis movement (e.g., push-up displays and foot shakes). For this reason, the most common way of measuring lizard display movements has been to record motion with film or video, and measure the motion, through time, of a few points on the animal’s head, body, and/or dewlap. These plots of position versus time are known as display action patterns (Carpenter 1965; Jenssen 1977). Similar plots can also be made of identified locations on plants, in order to compare the aspects of motion of lizards and that of background vegetation. Fleishman (1988) used this approach to demonstrate that display motion patterns of the Anolis auratus advertisement display are distinct from those of windblown plants in temporal frequency structure. The plant motion is largely sinusoidal (with some harmonics), whereas the introductory portion of the lizard displays is similar to a square wave. In the natural world, background motion is rarely limited to single objects or a single motion axis. Natural visual scenes consist of a three-dimensional array of moving vegetation and other stimuli, at many distances from the viewer. This entire complex scene is projected onto the retina as a two-dimensional image. In order to try to understand visual responses to such complex moving natural scenes, Peters et al. (2002) developed a computer algorithm to measure two-dimensional optic flow (the distribution of motion patterns over time across the entire retina) from video recordings of natural scenes. They applied this approach to a detailed analysis of the signaling behavior of Amphibolurus muricatus. Based on the neural and behavioral results described above, they argued that two critical features of visual motion are local direction and angular speed. They developed a computer algorithm, referred to as the “gradient detector algorithm” (Peters et al. 2002) that operates on sequential frames of video input and uses changes in local spatiotemporal intensity gradients to calculate spatially localized velocity vectors. They have used this approach, for example, to compare retinal motion created by windblown vegetation to motion patterns of different components of stereotyped visual displays (Figure 7.7). They found that most of the movements in the aggressive

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Figure 7.7  Velocity estimates obtained from a random 25-frame window of the tail-flick display of Amphibolorus muricatus overlaid on natural foliage movement in the wind. Dominant direction and speed of motion is shown by intensity and color. The left-hand plot shows the spatial location of movements. The motion from the tail flick is dominated by red and green colors. The graph on the right shows only direction and speed of movement. The red dots arise from the motion of the tail, while the blue dots show the movement of background vegetation. The graph illustrates that the lizard tail-flick display has dominant motion in a different direction than the plant motion. (From Peters et al. 2002.)

display of A. muricatus create directional motion velocities that are distinct from those created by natural vegetation, as long as the vegetation is viewed at the same distance from the viewer as the lizards’ displays (Peters et al. 2002; Peters and Evans 2003b). An extremely useful feature of this analytical approach is that the algorithm describes motion in terms of velocity vectors independent of the intensity contrast of the elements in the scene, and this greatly facilitates comparisons of displays and scenes recorded under varied light conditions (Peters 2008). Another approach that has been developed to model visual motion perception and optical flow of natural scenes attempts to more closely mimic the neural processing underlying this process (Borst and Egelhaaf 1989; Borst 2000; Zanker and Zeil 2005; Fleishman and Pallus 2010; Pallus et al. 2010). This model uses simple spatially localized, biologically plausible neural networks, referred to as “elementary motion detector” (EMD) units. These units are modeled as “correlation detectors,” which compare intensity on the retina at two displaced locations and times (Reichardt 1987; Borst and Egelhaaf 1989). The simplified EMD model is described in Figure 7.8a. Pallus et al. (2010) developed a computer model that analyzed video sequences with a perpendicular array of these EMD units, referred to as a “two-dimensional motion detector” (2DMD) model (Figure 7.8b). Behavioral experiments on Anolis sagrei were used to identify realistic model parameters, which include the distance between the interacting receptive fields (= the space constant), and the temporal property of the time-delayed signal from one receptive field to the other (= the time constant) (see Figure 7.8b). The artificial 2DMD network exhibits directional sensitivity, velocity tuning and is sensitive to luminance contrast between stimuli and backgrounds, and is thus consistent with behavioral and physiological results. Fleishman and Pallus (2010) tested the 2DMD model with videos of artificial computer-generated movement in order to determine the strongest motion stimuli for this model. An example is shown in Figure 7.8c, which shows a frame of video of a displaying male Anolis pulchellus, immediately after an abrupt upward movement of its head and body. Figure 7.8d shows the output of 2DMD network for this movement. Magnitude of motion model stimulation is plotted in the z-axis, while the video frame is plotted in the x- and

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Figure 7.8  (a) A correlation detector model of the neural basis of motion detection. Two receptive fields on the retina, labeled 1 and 2, are separated by a space constant Δø. Δø can also represent a distance in pixels of a natural scene captured on video for modeling purposes. Each receptive field responds to local brightness changes. The output from each receptive field is sent to two nodes, one of which is delayed by a low-pass filter with a time constant τ. The outputs from the two receptive fields are multiplied together as shown at node x. The output from the reciprocally connected units is subtracted. The final output produces a signal whose sign indicates direction and whose amplitude strength of the motion signal. The strength of the signal depends on the velocity and amplitude of the motion as well as its direction. (b) To describe motion in natural scenes, a two-dimensional array of these detectors is used to computer-model response over space. It is referred to as a 2-dimensional motion detector or 2DMD. The spatial and temporal response properties of the model were determined from behavioral experiments. (c) The input to the model is a series of sequential still video images. The lizard shown in the picture has just abruptly moved its body upwards. (d) The model output shows the x–y spatial map of the video input. The z-axis indicates the strength of the motion signal, which is the output from the motion detector circuit in arbitrary units. This example shows output from the video immediately after the lizard has competed one abrupt movement. (e) Examples of display action patterns (DAPs of introductory portions of displays of three species of Puerto Rican Anolis lizards in low wind (left) and moderate to high wind (right): (row 1) A. gundlachi, (row 2) A. cristatellus, and (row 3) A. pulchellus). The black lines show eye position versus time along the axis of greatest motion. The red line shows the peak response amplitude of the 2DMD model for each video frame. The lizard display motion consistently exceeds motion produced by windblown vegetation for both low and moderately high wind conditions. (From Fleishman and Pallus 2010).

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y-axes. Figure 7.8e illustrates the maximum output from the motion detector in each video frame through time. A step function of amplitude close to the space constant always elicited the strongest possible motion detector response, regardless of the time constant. Consistent with this result, behavioral tests using the visual grasp reflex of Anolis have shown that such a step function elicits the strongest response in all conditions. The model predicts that optimal motion amplitude (in degrees of visual angle) should be similar to the spacing between EMD units. Behavioral experiments relating the amplitude of motion to visual attention suggest the existence of at least two classes of EMDs with different spatial and/or temporal properties (Pallus et al. 2010; Steinberg and Leal 2013), which would be consistent with the presence of neurons with different velocity tuning as found by Stein and Gaither (1983). Fleishman and Pallus (2010) ran the 2DMD model on videos of anoline lizards displaying in moderately windy and still conditions in natural field situations. As shown in Figure 7.8e, the initial movements in these displays consist of abrupt step patterns that strongly trigger the EMD motion detector and produce a signal that greatly exceeds that produced by windblown vegetation. Some Functions of Motion Patterns and Their Influence on Signal Design Elicitation of Attention Motion is the strongest stimulus for elicitation of visual attention. We would expect to see movements that are extremely effective at eliciting attention to occur early in most visual signals, and particularly in signals directed at inattentive receivers that are some distance away. As described above, neural network modeling and behavior experiments suggest that abrupt stepwise movements are very strong attention-eliciting stimulus. Fleishman and Pallus (2010) showed that spontaneous territorial displays (typically viewed by inattentive viewers more than a meter away) of four different species of Puerto Rican Anolis begin with a series of abrupt square-wavelike movements (Figure 7.8d). A similar pattern is described (see page 233) for Anolis auratus (Fleishman 1992). Stamps and Barlow (1973) showed that males of Anolis aeneus (the Bronze Anole) add several high amplitude step movements at the beginning of threat displays when their rival is a considerable distance away. Ord and Stamps (2008) showed that Anolis gundlachi (the Yellow-chinned Anole) preferentially adds high amplitude step motion to the beginning of displays directed at distant conspecifics. In contrast, the Jacky Lizard (Amphibolurus muricatus) appears to use a different strategy. Rather than initiating its displays with abrupt high amplitude movements, it begins its displays with an up and down smooth waving motion of the tail, which is of long duration (Peters and Evans 2003b). This extended duration of motion was shown to increase the probability of detection (Peters and Evans 2003a) and this appears to be an alternative solution to the challenge of eliciting attention. As described above, the presence of windblown vegetation has been shown to influence ­detection probability, and this effect would be expected to be particularly important for display components designed to elicit attention. Several strategies have been reported addressing how lizards reduce the impact of this visual noise. Ord et al. (2011) showed that Puerto Rican anoline lizards simply do not display if wind speeds exceed a moderate level, and wait for less windy condition. Interestingly, Jamaican species, that rely primarily on a flash of their colorful dewlap to initiate detection (a signal that stimulates color rather than motion vision channels) do not display less often in higher wind conditions (Ord et al. 2011). As shown in Figure 7.8, some species utilize step functions in the introductory portion of the display, which is effective in the presence of moderate wind. Ord and Stamps (2008) demonstrated that in Anolis gundlachi these step-function signal ­movements are more frequently employed under difficult viewing conditions, including elevated windblown vegetation movement. The Jacky Lizard Amphibolurus muricatus alters its initial display movements

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(repeating tail flicks) in a different way in the presence of wind. It uses a longer duration display and produces the flicks intermittently rather than continuously. This presumably increases the probability that one or more tail flicks will occur during a moment of low background motion (Peters et al. 2007). There is also evidence that some species adjust their signal motion patterns based on the distance to the receiver in a manner that maintains effectiveness as an attention-eliciting signal. Steinberg and Leal (2013) found that males of Anolis gundlachi adjust the amplitude of the initial movements of their displays depending on the distance to the viewer. The amplitude is highest when the viewer is distant, and becomes smaller as the distance to the viewer decreases. This change in amplitude keeps the signal within the range of viewer amplitudes that have been found to elicit the greatest responses in behavioral experiments. In contrast to this result, Peters and Allen (2009) found that Amphibolurus muricatus does not change the amplitude of its introductory tail flicks with changes in distance to the receiver. Signaling Species Identity Stereotyped movements are important for the rapid and unambiguous broadcast of species identity. The displays (advertisement, courtship, and agonistic) of many lizard species include, as part of the signal, a temporal pattern of motion direction changes that is unique to each species (Carpenter 1965, 1967; Jenssen 1977), called a “signature bob.” Signaling species identity is most effectively carried out by utilizing a reliable temporal pattern of motion direction shifts, or with a recognizable sequence of distinctly different display movements (Peters and Evans 2003a). Recall that motion-sensitive neurons are directionally tuned and respond strongly to motion onset. Thus, each reversal of direction of movement stimulus will elicit a burst of new neural responses. If the species-identity information is contained in the time between reversals, the signal will provide the same information when viewed from different distances and from different viewing angles, and will still be recognizable if the view is partially blocked. Amplitude or speed of movements, in contrast, does not carry useful information for this function, because these parameters are altered by changes in the viewer’s angle of view or distance from the signal. And indeed, temporal patterns are much more stereotyped than motion amplitudes in many species (Jenssen 1977). Some species employ other types of movements, such as foot or tail shaking, or sequences of distinct body movements to create the same kind of discrete and recognizable sequence that is seen in signature bobs. The key to all such movements is that they be fairly reliable in temporal sequence, and of sufficient amplitude to be detectable by an attentive viewer, since they often follow an initial attention-eliciting signal (Fleishman 1992; Peters and Evans 2003a). Signaling Motivation and Condition Motion signals and associated postures can be used to signal a variety of differences among individuals. Agonistic interactions are often mediated by graded patterns of display that may include special patterns of movement (such as rocking back and forth, four-legged push-up displays, or tail twitching) to indicate different levels of aggressive intensity. Postural modifications such as body flattening or opening of the jaws in combination with signature displays often accompany movements in order to signal intention or motivation (Jenssen 1977; Jenssen et al. 2005). Steffen and Guyer (2014) demonstrated that the rate of display of Anolis sagrei is a signal of aggressive motivation. The key point about these patterns is that, unlike signals of species or individual identity, they are changeable. They usually consist of discrete postures or kinds of movement, because other changes in motion (such as amplitude or motion velocity) are difficult to discern reliably because they are perceived differently with changes in distance or viewing angle. Motion displays are also used as predator-deterrent signals. Leal and Rodríguez-Robles (1997) showed that Anolis cristatellus directs push-up displays at snakes, and further that the rate of

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repetition of complete display sequences correlates with physical condition. Font et al. (2012a) showed that Podarcis muralis employs one of its foot-shake signals for the same purpose. An Example of How Different Functions and Contexts Can Influence the Design of Signal Motion Components The display patterns of Anolis auratus offer a useful illustration of this (Fleishman 1992). In this study, male lizards were maintained singly in large outdoor enclosures. Males of this species move about their territories and give spontaneous displays from elevated perches. In natural conditions, the viewers of these displays are typically several meters away and inattentive. These long-range displays were recorded on film. Each individual was then captured and brought into the laboratory. A second male was then introduced into the cage and the resulting close-range agonistic displays (directed at individuals within a few cm) were filmed. Display motion patterns were then measured from the filmed behaviors. The results are summarized in Figure 7.9. First, for each individual the temporal motion pattern (i.e., the timing of direction reversals) of both display types was the same. Each individual, however, had its own, unique display motion pattern. The displays consisted of two parts. The motion pattern of Part I of the display was different for each individual, whereas Part II

Figure 7.9  Display action patterns of assertion displays and challenge displays by two individual (a and b) male Anolis auratus. The upper line in each graph shows the position of the head along a line perpendicular to the body axis versus time. The lower hatched area shows the extent of extension of the dewlap below the head. As can be seen, the assertion and challenge display of each individual is unique. The temporal pattern of the two display types by one individual is the same, but the amplitude of the initial portion of the assertion display (part I) is greatly increased relative to the close-range challenge display.

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displays were identical. Part II of the display can be considered a signature bob and probably serves as a species recognition signal. Part I of the display consisted of abrupt up and down step movements with the dewlap fully extended. In the long-range displays, the amplitude of this portion of the display was approximately ten times greater than Part I of the short-range agonistic displays. These large step movements form an extremely effective attention elicitation signal for animals a few meters away. In the long-distance displays, the amplitude of Part II was much lower than that of Part I, presumably because any viewers would already have shifted their gaze toward the viewer where they would see the remainder of the signal with the high acuity part of the retina. Part II of the long-range display was always significantly greater in amplitude than Part II of the close-range display, although this difference was much less than for Part I. This difference presumably makes Part II detectable from a greater distance for the long-distance function. Fleishman (1992) suggested two possible hypotheses for the role of the individual variation of Part I of the display. Since the temporal pattern is consistent from display to display, but different for each individual, it might serve as a signal of individual identity. Alternatively, having different individuals use different display motions might reduce habituation to the attention-eliciting signals. Territorial males display frequently, and using displays that differ might maintain the effectiveness of this signal for individuals, such as females, that would view many males displaying repeatedly. Thus, it is apparent how different functions can favor the evolution of different motion components within the display of a single species. CHEMICAL COMMUNICATION Chemical senses allow lizards to locate potential food sources, detect and avoid predators, and communicate with others of their own species. The literature on chemoreception and ­chemical communication in reptiles is immense, and several detailed reviews of the field are available (Burghardt 1970; Mason 1992; Halpern 1992; Mason and Parker 2010), including those specific to lizards (Cooper 1994a; Martín and López 2011, 2014). Progress in the study of lizard chemical communication has largely proceeded along two routes. Many studies have used the swab/applicator technique, or a variant thereof, to probe the ability of males and females of several species to discriminate among exudates or scent marks of animals differing in species/population identity, sex, age, reproductive condition, hormone levels, diet, health, and so forth, or between different chemical compounds. Other studies have analyzed the chemical composition of lipids in epidermal gland secretions (Figure 7.10) or, more rarely, skin lipids.

Figure 7.10  Femoral pores and femoral gland secretion are clearly visible on the thighs of this male of Podarcis muralis. The yellowish plugs of solid, waxlike secretion have fallen off in the pores located closer to the trunk. (Photograph by E. Font.)

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Much recent work on lizard chemoreception and chemical communication has focused on European lacertids. This research has emphasized the potential role of epidermal gland secretions as signals of individual quality in mate assessment and has produced results suggesting that the chemical senses of lizards can glean sophisticated information about attributes of potential ­partners, ­consistent with the idea that the costs associated with signaling can constrain the ­relationship between signal design and unobservable qualities of senders (e.g., Martín and López 2015). However, this emerging paradigm is inconsistent with laboratory and field observations, and caveats and alternative interpretations that we describe below have been proposed (Font et al. 2012b; Heathcote et al. 2016). Terminology: Pheromones and Signature Mixtures The chemicals used in intraspecific interactions include both pheromones and signature mixtures (Wyatt 2014). Pheromones are species-wide signals and can be a single molecule or a combination of multiple compounds (multicomponent pheromones or pheromone blends), usually in a particular ratio, that elicit a behavioral or physiological response in the receiver. Signature mixtures are subsets of molecules from the animal’s chemical profile that are detected by others, allowing them to recognize an animal as an individual or a member of a particular social group. In contrast to pheromones, many signature mixtures are not signals, but cues (i.e., stimuli that incidentally provide information to an unintended receiver but that have not been selected for that function). Signature mixtures are characterized by variability and the requirement for learning; in contrast, pheromones share the same composition in individuals of the same species (or the same sex-age class) and the response to them is often innate (Wyatt 2014). Most published studies of lizard chemical communication conflate pheromones with signature mixtures and use the term pheromone to refer to compounds or mixtures of compounds in contexts where signature mixture might be more appropriate. The distinction is important because we know that, at least in mammals, pheromones and signature mixtures can interact with each other in complex ways (Wyatt 2014). Scent marks (also known as range marks) are chemical signals released to the environment and later detected by a receiver in the absence of the sender. In lizards, scent marks consist of secretions from epidermal glands or compounds added to the feces (see below). As many studies of scent-mark function have examined the response of lizards to whole secretions rather than to isolated, chemically identified signal compounds, the results may be confounded due to the presence of both pheromones and signature mixtures in the secretions. Chemosensory Perception: Overview of the Main Olfactory System and the Vomeronasal System Lizards have two major chemosensory systems capable of detecting pheromones and signature mixtures: the main olfactory system and the vomeronasal system, which together are termed the olfactory systems. The vomeronasal system has traditionally been considered a system specialized for pheromone detection. However, pheromones and signature mixtures can be detected by both the olfactory and the vomeronasal systems, and the latter is also involved in the detection of odorants that are not chemical signals (e.g., prey chemical stimuli). The nasal cavities of the main olfactory system are lined with a pseudostratified sensory epithelium bearing ciliated olfactory sensory neurons that project to the main olfactory bulb. The vomeronasal system consists of paired vomeronasal organs located in the roof of the mouth and separated from the nasal cavity by the secondary palate. They are connected with the oral cavity by narrow vomeronasal ducts. The openings of the ducts are visible in the roof of the mouth as two slits known as vomeronasal fenestrae. Dorsally, the vomeronasal organ has a sensory epithelium with microvillar sensory neurons that project to the accessory olfactory bulb. Electrophysiological

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responses of isolated vomeronasal sensory neurons to natural odorants have been studied in only one non-ophidian lizard species, Liolaemus bellii, and these exhibited outwardly and inwardly evoked currents in response to stimulation with extracts from conspecific skin, feces, and precloacal epidermal gland secretions (Labra et al. 2005). The main and accessory olfactory bulbs project through separate neural pathways to telencephalic targets, but their secondary and tertiary projections overlap in several telencephalic areas (e.g., lateral cortex and amygdala), providing a neural substrate for interaction of olfactory and vomeronasal information (Halpern and MartínezMarcos 2003). Although data specific to lizards are almost nonexistent, the mechanisms of chemosensory transduction seem to be highly conserved across vertebrates (Wyatt 2014). Chemicals brought in from the environment bind to olfactory receptor proteins (belong to the G-protein-coupled receptor superfamily) embedded in the membranes of receptor cells in the main olfactory and vomeronasal epithelia. Each receptor cell expresses a single receptor protein that triggers a G-protein-based signaling cascade when activated by its ligands. The genes encoding the olfactory receptor proteins belong to large multigene families, those of the main olfactory system having evolved independently from those of the vomeronasal system (Brennan and Zufall 2006). The olfactory systems have the ability to detect and discriminate an enormous diversity of odorants. Olfactory receptors have broad but overlapping specificities, and most odorants are identified not by the activation of a single receptor type but by the activation of a subset of receptors in a combinatorial manner. Olfactory receptor genes have been characterized for a single lizard species, the green anole Anolis carolinensis. Anoles in general have traditionally been considered microsmatic, but recent evidence has challenged this notion (Baeckens et al. 2016). Using a data-mining approach, Dehara et al. (2012) identified 108 putatively functional olfactory receptor genes in the genome of the green anole, A. carolinensis. However, this is probably an underestimate of the real number of functional olfactory receptor genes and does not include genes coding for receptor proteins in the vomeronasal epithelia. For comparison, humans have 350 functional olfactory receptor genes and can discriminate the odors of over one trillion chemical mixtures. Differences between Olfactory and Vomeronasal Chemoreception The main olfactory system is chiefly a distance-sensing system that detects small, highly volatile molecules, whereas the vomeronasal system is best suited for collecting relatively nonvolatile, high-molecular-weight chemicals (see Apps et al. 2015). However, this is not a strict dichotomy, as there is evidence that the vomeronasal system of lizards and snakes is also involved in the perception of relatively volatile chemicals (e.g., air-licks, see below). According to the Cowles and Phelan (1958) hypothesis, olfactory detection of volatile compounds triggers further exploration by means of the tongue–vomeronasal system, which allows for finer discriminations. Volatiles could thus act as attention-eliciting components that function to trigger tongue-flicking and examination by the vomeronasal system. Tongue-Flicking The main olfactory system is well suited for the detection of volatile odorants inhaled or exhaled during respiration. In contrast, vomeronasal system responses present an additional level of complexity as chemicals do not reach the liquid-filled vomeronasal organs directly and require the participation of the tongue. During tongue-flicking, the quintessential squamate behavior (Cooper 1994b), the tongue is extruded from the mouth and collects chemical stimuli from the environment for delivery to the vomeronasal organs located in the roof of the mouth (Halpern 1992; Schwenk 1995). Chemical sampling involves diffusion of environmental chemicals into the thin fluid layer covering the surfaces of the tongue tips. There is some controversy regarding the

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detailed mechanism that allows transfer of stimulus particles from the chemical-laden tongue tips to the vomeronasal organs, but it probably involves additional structures in the floor of the mouth (Filoramo and Schwenk 2009). Distel (1978) conducted an extensive study of the effects of electrical brain stimulation in awake, freely moving Iguana iguana. Tongue-flicking was elicited by stimulation of several olfactory and vomeronasal recipient zones in the telencephalon, including the olfactory tubercle and the nucleus sphericus. The latter is the main recipient of projections from the ipsilateral accessory olfactory bulb and, at least in snakes, projects to hypothalamic areas which in turn project to the hypoglossal nucleus which controls the tongue musculature, thus providing a candidate neural pathway for mediating chemosensory influences on tongue-flicking behavior (Halpern and Martínez-Marcos 2003). Two broad types of tongue-flicks have been described for lizards, sometimes termed air-licks (or air tongue-flicks) and tongue-touches. During air licks the tongue is protruded from the mouth but does not touch the substrate; this suggests that this type of tongue-flick may be an adaptation for collection of volatile odorants. Tongue-touches, on the other hand, bring the tongue (usually its ventral surface) into contact with chemical-laden substrates and are thus better suited for collection of nonvolatile chemicals (Figure 7.11). There is little information on variation in the structure of the vomeronasal organ. In contrast, variation in tongue size and shape is extensive and has been well documented. In a comparative study involving 18 species representing the major lizard families, Cooper (1995) concluded that chemical sampling efficiency is enhanced by tongues that are forked, elongate so that they can be extended beyond the mouth, and narrow at the base, as in varanids and teiids. Lingual shape shows more interfamilial than intrafamilial variation, suggesting a strong phylogenetic signal. However, the squamate tongue has many uses besides those implying chemoreception (e.g., prey prehension, prey transport, tamping food into the esophagus, grooming, drinking; Cooper 1994b), which complicates interpretation of interspecific variation in lingual design. A recent study investigated whether the morphology of the tongue and the vomeronasal organ reveal patterns of concerted evolution in a sample of lacertid lizards (Baeckens et al. 2017a). Although in general the study found little support for the coevolution of the tongue and the vomeronasal organ, some aspects of lingual morphology were found to covary with vomeronasal organ morphology in ways that suggest optimization for efficient chemoreception. In particular, species with deeply forked tongues tend to have relatively thick vomeronasal epithelia carrying more sensory neurons (see also Cooper 1997). Interestingly, the study of Baeckens et al. (2017a) also found that the degree of investment in chemical signaling (measured as the number

Figure 7.11  T  ongue-flicking in Podarcis liolepis (the Iberian Brown Wall Lizard). Note forked tongue tip and contact of the ventral surface of the foretongue with the substrate. (Photograph by E. Font.)

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Figure 7.12  G  allotia stehlini (the Gran Canaria Giant Lizard) biting a cotton swab impregnated with chemical stimuli. The interpretation of bites directed to swabs in chemical discrimination experiments is controversial (see text). (Photograph by E. Font.)

of femoral pores, see below), is a leading factor driving the diversity in vomeronasal-lingual morphology in lacertid lizards. As tongue-flicks are easily counted, tongue-flicking provides a convenient assay of the ability to respond differentially to biologically relevant stimuli and has been extensively used in the study of chemoreception in squamates (Cooper and Burghardt 1990; Halpern 1992; Cooper 1994a). However, the interpretation of the results of experiments using tongue-flicks as a dependent variable may not always be straightforward. In a thoughtful review of methodological issues relating to the study of squamate chemoreception, Cooper (1998) argued that while differential tongue-flick rates may indicate discrimination, their absence does not necessarily indicate lack of discriminatory ability (see also Font and Desfilis 2002). There is no general agreement as to what variation in tongue-flicking rate might represent, with different authors favoring interpretations in terms of interest, preference, detection (i.e., statistically significant difference from control), discrimination (i.e., statistically significant difference between treatments), or recognition. In experiments using chemicals presented on cotton swabs, lizards sometimes bite the swab, a behavior that different authors interpret as an aggressive, a defensive, a feeding, or even a mating response (Figure 7.12). Such inconsistencies highlight the lack of a theoretical framework that allows unambiguous interpretation of experimental results. Sources of Chemical Signals The main sources of chemical signals in lizards are the skin and epidermal holocrine glands (Mason 1992). Two types of epidermal glands are recognized: follicular glands and generation glands (Mayerl et al. 2015). Follicular glands are located in the inner thighs or in the pericloacal region and are variously referred to, depending on their anatomical position, as femoral, precloacal, or preanal glands (Imparato et al. 2007; Khannoon et al. 2013; Valdecantos et al. 2014). Follicular glands secrete a waxy substance through modified pore-bearing scales. The secretion protrudes through the pores as a solid plug (Figure 7.10). There is sexual dimorphism in the size and number of epidermal glands/pores, which are entirely lacking in females of some species. More often, females have pores but those of males are larger and more numerous. There is also extensive interspecific variation in the number of epidermal pores, which is often used as a proxy for the degree of investment in chemical signaling by different species (Van Wyk et al. 1992; Baeckens et al. 2015).

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The secretory activity of follicular glands peaks during the reproductive season and is under androgenic control. In some species, the amount of secretion produced may be related to the size, physiological condition, and reproductive state of the individual. In Sceloporus graciosus, increased secretion during the reproductive season enables males to scent mark more sites rather than to mark any single site more heavily, which may facilitate territorial expansion (Martins et al. 2006). Seasonal variation in the composition of the femoral gland secretions has also been observed (García-Roa et al. 2017). In addition to follicular glands, some cordylids and some geckos also have generation glands (e.g., Van Wyk et al. 1992; Mouton et al. 2010), which are patches of glandular scales that occur in different anatomical locations. Other potential sources of socially relevant chemical stimuli in lizards include several cloacal glandular secretions (e.g., urodeal glands and cloacal glands) and feces. Epidermal gland secretions are assumed to be deposited passively onto the substrate as lizards move about their home ranges, but active scent-mark deposition has also been described. For example, Desert Iguana (Dipsosaurus dorsalis) have been observed pressing their abdomen against the substrate while rhythmically moving their body and tail sideways (Alberts 1989). Similarly, male Common Wall Lizards (Podarcis muralis) often adopt a sprawling gait while patrolling their territories which may increase contact between the femoral pores and the substrate and thereby facilitate the deposition of scent marks. Signal Chemistry: Functional Groups Lizard skin contains many different compounds, including hydrocarbons, alcohols, aldehydes, steroids, fatty acids, and their derivatives (Weldon et al. 2008). Many of these compounds contribute to the transepidermal water barrier, but there is abundant evidence that some also play a role as chemosignals (Weldon and Bagnall 1987; Mason and Gutzke 1990; Font et al. 2012b). Epidermal gland secretions contain lipids and proteins. Typical major components of lipophilic compounds in femoral or precloacal gland secretions of lizards are steroids and fatty acids, and these secretions also contain minor amounts of alcohols, wax esters, squalene, tocopherol, ketones, aldehydes, furanones, alkanes, amides, and other compounds (reviewed by Weldon et al. 2008). Steroids and fatty acids have been reported in the lipophilic fraction of all lizard families studied, whereas other components have a more restricted phylogenetic distribution (e.g., alcohols have not been reported in the family Liolaemidae). Cholesterol is the most abundant steroid in the femoral secretions of some (but not all) lizards, and it is also a major component of skin lipids. Proteins can make up a large proportion of the gland’s secretion (e.g., 80% by weight in Iguana iguana, Alberts 1990), but their potential role as chemosignals has been largely ignored. The almost exclusive focus on the lipophilic compounds present in femoral gland secretions is based on erroneous assumptions regarding the species-specificity and potential information content of proteins versus lipids (Apps et al. 2015; Mayerl et al. 2015). Physical Properties of Lizard Chemical Signals The chemical composition of a chemical signal determines its physical properties, which in turn affect the signal’s detectability, durability (fade-out time), the distance it disperses (active space), and the information it contains (Wyatt 2014). As with signals in other sensory modalities, we ask whether there are predictable ways that selection can enhance the communicative function of chemicals and whether selection imposed by sensory systems results in distinct evolutionary trajectories of chemical signal evolution. Many chemicals used for communication have evolved from chemicals released for noncommunicative functions that incidentally provide information to receivers (Steiger et al. 2011; Wyatt 2014). Initially, it is possible that only receivers benefit from this type of interaction, and therefore, the released chemicals are best seen as cues, not signals. But

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if senders also benefit, on average, from the response of receivers, we expect selection to fine-tune the chemical cue for a communicative function. The process whereby chemical cues evolve into chemical signals has been termed chemical ritualization (Steiger et al. 2011), which entails changes to the chemicals themselves, or to the ways they are released that increase their effectiveness in communication. Chemical signals can also evolve from receiver precursors (i.e., preexisting sensory biases). For example, it has been proposed that some compounds in male femoral secretions may attract females by mimicking food (Martín and López 2008). Although the argument is plausible, it fails because the compound that the authors suggest might have evolved through sensory exploitation (cholesta-5,7-dien-3-ol) is not generally found in insect integument and is, therefore, irrelevant as a stimulus allowing the detection of intact prey. A widespread strategy for enhancing the effectiveness of chemical communication consists of adding signal components that make signals more conspicuous to receivers (Steiger et al. 2011). The added signal components can belong to the same or a different sensory modality than the original signal. For example, scent marks often consist of high-molecular-weight, relatively nonvolatile compounds, possibly because they must remain active long after being emitted by the sender, but those same qualities that make them long lasting and stable also make them less conspicuous to receivers. The trade-off between durability/stability and conspicuousness can be solved by emitting a blend that comprises one or more volatile, attention-getting chemicals together with the less volatile compounds. The former would not provide information to receivers and would thus act as an attention-eliciting component selected for its role in attracting the receiver’s attention. This could explain why the scent marks of lizards consist of a complex blend of volatile and nonvolatile compounds (Weldon et al. 2008). Another way of enhancing the detectability of a chemical signal is to make it visually conspicuous. Femoral gland secretions of some lizards strongly absorb UV radiation (Alberts 1989; Martins et al. 2006). This probably makes them visually conspicuous against natural substrates such as desert sand, which is highly UV-reflective. Alberts (1989) showed that Desert Iguanas (Dipsosaurus dorsalis) are more likely to find femoral gland secretions deposited on the substrate when provided with UV illumination, suggesting that visual cues are important for their long-range detection. Do the receiver’s sensory capabilities predict design features of chemical signals? Answering this question is a challenge given the scarcity of relevant data for lizards. Although many different compounds have been identified in the skin and epidermal gland secretions of lizards, it is unclear which of them qualify as pheromones. In order to qualify as a pheromone, a compound (or a combination of several compounds in defined ratios) must be chemically characterized, and the isolated/ synthesized compound (or combination) must elicit the same response as the natural chemical signal when presented at similar concentrations (Wyatt 2014). This operational definition excludes many, possibly most, candidate pheromones reported in the literature. In fact, a recent review (Apps et al. 2015) identified only two lizard pheromones that fulfill the requisite criteria. Squalene is a major component in the precloacal secretions of the Mediterranean Worm Lizard (Blanus cinereus). It is more abundant in male than in female secretions, and when presented on cotton swabs, elicits chemosensory and aggressive responses similar to those elicited by whole precloacal secretions (López and Martín 2009). Similarly, in Bosk’s Fringe-fingered Lizard, Acanthodactylus boskianus, cholesterol and long-chain alcohols presented in a Y maze elicit avoidance and agonistic behavior in males but not females (Khannoon et al. 2011). In both studies, the conclusion that the candidate pheromones trigger aggressive responses is based on the observation that lizards directed bites to cotton swabs or to the substrate. While bites (Figure 7.12) may indeed reflect an aggressive response, alternative interpretations (e.g., defensive and predatory) cannot be discarded. Until more species are examined, all we can do is speculate on the relationship between signal design and sensory system response properties based on data from other taxa. Apps et al. (2015) reviewed the evidence available for terrestrial vertebrates and found a few small-scale patterns, but few links between signal chemistry and biology and no extensive patterns of chemical signal design.

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It thus appears that ritualization has not had marked effects on the structure of chemical signals. Apps et al. (2015) further concluded that signal detection imposes no practical constraints on the structures of chemicals used for communication. Perhaps more than with other sensory modalities, the response to chemical signals has evolved from a preexisting ability to respond to chemical stimuli generally. The high sensitivity, broad scope, and narrow resolution of the olfactory systems of terrestrial vertebrates, including lizards, have probably allowed for a relaxation of the selection pressures that might have otherwise generated patterned relationships between signal chemistry and chemoreception (Apps et al. 2015). Environmental Influences on Chemical Signal Design In mammals, variation in the chemical composition of chemical signals reflects, at least in part, adaptations to specific ecological conditions. In particular, chemicals used in scent marks from hotter and more humid environments, which increase evaporation and reduce signal life, tend to have stable compounds containing aromatic rings and larger molecular weights (Alberts 1992). Temperature and humidity may also affect the composition of lizard chemical signals. For example, Iberian Wall Lizards (Podarcis hispanicus) from warmer and dryer southern habitats where evaporation rates are higher have a higher proportion of stable and less volatile lipophilic compounds in their femoral gland secretions (Gabirot et al. 2012). Baeckens et al. (2017b) used a phylogenetic comparative approach to examine the relationship between signal chemistry and environmental conditions in a sample of 64 lacertid species from Europe, Africa, and Asia. They found a relatively weak phylogenetic signal, suggesting that chemical signal composition evolves rapidly and is relatively independent of phylogenetic relatedness. Baeckens et al. (2017b) also found a relationship between the lipophilic composition of femoral gland secretions and aspects of the thermal and hydric environment inhabited by different species. Femoral gland secretions of species from xeric environments, characterized by high temperatures and arid conditions, contain high proportions of stable fatty acid esters and high molecular weight alcohols, which likely increase the persistence of scent marks. In contrast, species inhabiting mesic environments, with high levels of precipitation, radiation and wind, produce secretions with many lipophilic compounds and high levels of aldehydes and low molecular weight alcohols, which make them well suited for longdistance airborne communication. There is also evidence that the composition of femoral gland secretions may change with an individual’s basking experience. In male wall lizards (Podarcis muralis), the amount of time spent basking significantly alters the chemical composition of their femoral gland secretions. Further, the direction of the change is consistent with adaptive plasticity to maintain signaling efficacy under warm conditions that increase evaporation of femoral gland secretions (Heathcote et al. 2014). Several studies have examined variation in epidermal pore number in relationship to ecological conditions. In these studies, the number of pores is used as a proxy for the amount of secretion produced by the epidermal glands, reflective of how much a given species or population relies on chemical communication. Escobar et al. (2001) found that species of Liolaemus living in warm, windy, and low-atmospheric pressure conditions (high-altitude and low-latitude habitats) have more precloacal pores than species that live in less harsh habitats, but the results of this study may have been confounded due to phylogenetic effects (see Pincheira-Donoso et al. 2008). In a comparison between two populations of the Algerian Psammodromus (Psammodromus algirus) living at different elevations, Iraeta et al. (2011) found that males have more femoral pores at lower elevations, which the authors attributed to selection for increased effectiveness of chemical communication in the dry and warm low elevation habitats where chemicals become volatile rapidly. In a comparative phylogenetic analysis using 39 species of Sceloporus, Ossip-Klein et al. (2013) found that variation in the number of femoral pores is tightly linked to phylogeny, but arboreal species have fewer femoral pores than do terrestrial ones. Baeckens et al. (2015), in a study of 162 species of lacertid

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lizards, found no effect of climate conditions or latitude on pore numbers but, similar to the situation in Sceloporus, shrub-climbing species tend to have fewer femoral pores than species inhabiting other substrates. There is also evidence for adaptive variation in the number of generation glands. In cordylid lizards, females from species living in cooler environments have fewer generation glands than do females from warmer environments. In males, species from high-altitude habitats have more glands than males from lower altitudes (Mouton et al. 2010). In lacertid lizards, species with a partly herbivorous diet tend to have more compounds in their femoral gland secretions than do species that are strictly insectivorous, presumably because the former can incorporate into their secretions compounds of plant origin that are unavailable in animal prey. However, diet appears to be a relatively poor predictor of interspecific differences in the broad chemical profiles of secretions in this group of lizards (Baeckens et al. 2017c). What little evidence is available therefore suggests that environmental variables may influence the amount and types of chemicals used as pheromones by lizards, but the taxonomic coverage is uneven and there are no clear, extensive patterns. Taken together, these results suggest that dry, windy, and warm habitats pose a special challenge to chemical communication in lizards. Functions of Lizard Scent Marks: What Do Lizards Use Scent Marks For? Putative pheromones and signature mixtures contained in lizard epidermal gland secretions have been attributed a variety of functions, including interspecific recognition, intraspecific ­recognition, social dominance, territoriality, and rival/mate assessment. In the context of intraspecific recognition, different experiments have shown that epidermal gland secretions are involved in the ­recognition of familiar conspecifics, population recognition, color morph recognition, sex recognition, and self-recognition (Halpern 1992; Mason and Parker 2010; Mayerl et al. 2015). As most studies have relied on an evaluation of responses to whole epidermal gland secretions rather than to properly identified pheromones, it is difficult to establish a correspondence between specific signal compounds and their functional consequences. Many studies may also be compromised by a failure to distinguish between pheromones and signature mixtures. Several studies of European lacertids have emphasized the role of scent marks in mate assessment. Females are reported to discriminate between males differing in body size, age, hormonal levels, immune response, diet, symmetry, parasite load, social dominance, and fighting ability, and they associate preferentially with areas scent marked by males with better health, body condition, higher quality, or greater genetic compatibility (Martín and López 2014, 2015). For example, females of Cyren’s Rock Lizard (Iberolacerta cyreni) are attracted to rock substrates to which ergosterol (provitamin D2) has been added experimentally. Ergosterol is found in the femoral gland secretions of male I. cyreni, and its relative abundance may act as an honest indicator of the male’s quality as a mate because the allocation of ergosterol to scent marks diverts it from other important metabolic pathways (Martín and López 2012). Similarly, in the European green lizard (Lacerta viridis), a dietary supplement of α-tocopherol (vitamin E) increases the amount of this compound available in femoral gland secretions, and females prefer to use areas scent marked by males with artificially increased levels of α-tocopherol in their secretions (Kopena et al. 2011). Males of several lacertid species can discriminate between chemicals left on substrates by females of their own or a different species, suggesting that differences in female chemical cues may underlie species recognition in this group. Females, on the other hand, do not respond differentially to conspecific and congeneric male scent marks (Barbosa et al. 2005, 2006; Heathcote et al. 2016). It seems paradoxical that females fail to discriminate between males of their own or a different species based on chemical stimuli alone, yet they are apparently capable of extremely fine intraspecific discriminations. Another point of contention is the relevance of such discriminatory

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abilities to mating patterns in the wild, particularly considering the lack of evidence that supports precopulatory female mate choice based on male phenotypic traits in most lizards. In fact, it has been suggested that many candidate pheromones are probably functional in the context of male– male rather than male–female interactions and have, therefore, likely evolved through intrasexual selection (Font et al. 2012b; Heathcote et al. 2016). In many lizards, scent marks seem particularly important as social signals mediating territorial interactions between males. For example, males of Iberolacerta cyreni rubbed with sunflower oil to which cholesterol had been added won more fights than did males rubbed with plain sunflower oil. This suggests that the relative amount of cholesterol in scent marks may reliably signal fighting ability in this species (Martín and López 2007). For decades, territorial scent marks have been depicted as “no trespass” signals, as mere chemical signposts for intruders. However, recent studies reveal a much more complex picture of scentmark function. To investigate the functional significance of male scent marks in Podarcis liolepis (the Iberian Brown Wall Lizard), Carazo et al. (2007) used scent-marked terraria to simulate the situation faced by a male when intruding into the territories of rival males. This allowed them to examine the role of scent marks in the context of territorial interactions, from the perspective of both the receiver (the intruding male) and the sender (the territory owner). From the perspective of the intruding male, the results of these experiments indicate that scent marks do not function as “keep out” signals. In fact, early in the reproductive season intruding lizards spend more time in areas scent marked by other males of the same size or larger than themselves than in control, unmarked areas. This suggests that scent marks may convey information about the competitive potential (i.e., size) of territory holders. From the perspective of the territory owner, on the other hand, scent marks allow males to recognize potential rivals (i.e., intruding males) individually (Carazo et al. 2007). This is the first conclusive demonstration of true individual recognition in any reptile, and confirms that at least some compounds in the scent marks of male lizards function as signature mixtures rather than pheromones. Traditional interpretations of the function of territorial scent marks were framed in the context of the “dear enemy” hypothesis, which posits that the crucial variable affecting response to social signals is familiarity. However, results for Podarcis liolepis suggest that males are capable of much more complex discriminations. They allocate their aggressive behavior to intruders not on the basis of familiarity but according to the degree of threat posed by the intruder. They use scent marks to identify the potential threat posed by each individual neighbor (i.e., degree of territorial overlap), allowing them to allocate their aggressive behavior accordingly and to adjust it to changes in the territorial status of rival males. Therefore, scent marks can be broadly depicted as complex social signals that reduce the costs of territoriality, allowing males to strategically allocate their investment in territorial defense (Carazo et al. 2007). AUDITORY COMMUNICATION Sound consists of molecular vibrations propagated through some medium—most often air. The use of sound for communication by lizards presents an evolutionary puzzle. As we describe below, lizards have sophisticated ears with a wide frequency range and good sensitivity, in some species being almost as good as that of the average bird or mammal (Brittan-Powell et al. 2010; Manley 2011). Lizard ears also exhibit superb localization capabilities (Christensen-Dalsgaard and Manley 2005). With such a refined and high quality hearing apparatus, one would expect to find that auditory communication would be widespread and complex. Yet, by comparison with other major terrestrial animal groups (e.g., insects, frogs, birds, and mammals), in lizards, it is very limited. Only among the nocturnal geckos do we find extensive use of sound for communication, and even there the sounds produced for signaling are relatively simple in form.

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In most lizards, sound stimuli do not elicit strong behavioral responses, and it has proven very difficult to condition lizards to respond to sound. For example, Rothblum et al. (1979) were able to condition Anolis grahami to respond to sound stimuli only after eliminating any accompanying visual stimuli. Only one behavioral audiogram (response threshold amplitude vs. frequency) has been published, and it was based on a single individual (Manley 2000). Fortunately, a variety of physiological methods that correlate reasonably well with behavioral responses have been used to measure lizard hearing, so there is a good body of information about auditory sensitivity (Wever 1970; Wever and Werner 1970; Sams-Dodd and Capranica 1994; Brittan-Powell et al. 2010; Manley and Kraus 2010). In addition, the anatomy of the lizard ear is well studied (e.g., Peterson 1966; Wever 1968, 1970, 1974; Wever and Werner 1970; reviewed by Manley 2000). Anatomy and Mechanism of Lizard Ears All lizard ears have the same basic design, although there is a great deal of variation among different major clades in many of the details. The external ear of lizards either is nonexistent or consists only of a small skin-covered channel through a typically oval-shaped opening, which leads to the tympanic membrane, to which the skin is attached. Internally, several processes of a cartilage-based organ known as the extracolumella are embedded in the tympanic membrane. This is connected directly to a thin pistonlike bone, the columella, which ends in a footplate that is attached to the oval window of the bone-encased cochlear duct. Vibrations in the air cause the tympanic membrane to vibrate, and these vibrations are efficiently transmitted to the oval window by the columella. This results in vibration of the fluid that fills the cochlear duct, within which lies the basilar papilla where vibrations are converted into neural signals. The base of the basilar papilla consists of the basilar membrane, which supports many rows of hair cells from which emerge bundles of small hairlike stereovilli. The vibrating fluid within the cochlear duct causes the basilar papilla to vibrate, which induces motion in the hair cells. This causes bending of the stereovilli, which produces the receptor potentials in the hair cells that are converted to action potentials sent via the vestibulocochlear nerve to the brain. The hair cells form two (or three) distinct sets. One set, found in all lizard ears, responds primarily to frequencies lower than 1 kHz. The tops of the stereovilli of these cells are embedded in a structure known as the tectorial membrane. The motion of the basilar membrane relative to the stationary tectorial membrane causes bending of the stereovilli, causing neural response. The basilar membrane also supports one (or two depending on the lizard group) additional hair cell populations that respond primarily to frequencies above 1 kHz. In some groups, these are also embedded in the tectorial membrane. In others, the tips of the stereovilli are instead embedded in a series of small, bead-like structures united by threadlike connections, called “sallets.” Finally, in some groups, there are hair cells that are free standing. Some species (geckos, for example) have a second region of high-frequencysensitive cells and have, in addition, a group of hair cells that have no afferent or efferent neural innervation. These hair cells are thought to contribute to the hearing mechanism by resonating in response to vibration and through a micromechanical connection, amplifying the response of the innervated cells (Manley and Kraus 2010). In mammalian hearing, the basilar membrane varies in thickness and different regions resonate to a greater or lesser degree based on stimulus vibration, and thereby plays a role in frequency tuning the response of the ear. However, in lizards, the basilar membrane shows no position-based frequency response (Manley 2000), and plays no role in frequency tuning. Instead, it is the micromechanical resonance response of the individual hair cell bundles that produce frequency tuning. The precise mechanisms are unknown, but it is believed that the length and stiffness of hair cell bundles, electrical tuning properties of the cell membranes, and the nature of mechanical connection between hair cells result in different hair cell groups resonating and moving to different extents in response to different stimulus frequencies.

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Different lizard groups exhibit variations on this plan. Geckos have the largest and most c­ omplex basilar papillae and the greatest number of hair cells and auditory afferents. On average, geckos have the greatest auditory sensitivity, but some other species with a much smaller and less complex basilar papilla have response profiles that are as broad in frequency and nearly as sensitive (Brittan-Powell et al. 2010). Chameleons have the most reduced ear, with a small basilar papilla and no tympanic membrane (Wever 1968), but nonetheless they respond well to air-borne sound, although their sensitivity is less than that of other lizard groups (Wever 1968). Frequency Response Tuning curves have been produced for a number of different species and groups using a variety of physiological criteria. The results are broadly similar for most lizard species. Most exhibit a region of high sensitivity from approximately 0.4 to 1 kHz and a second broad region of high sensitivity from 1 to 4 kHz. In some species, the high-frequency region extends as high as 7–8 kHz (Brittan-Powell et al. 2010; Manley 2014). Recently, a group of snakelike pygopodid geckos (genus Delma) has been shown to be able to detect frequencies as high as 14 kHz (Manley and Kraus 2010). Brittan-Powell et al. 2010 used auditory brainstem potentials to compare frequency tuning in Gekko gecko (the Tokay Gecko) and Anolis carolinensis, and also compared the results to those from similar methods applied to two bird species (budgerigars and screech owls). Gekko gecko exhibited the greatest sensitivity of all of these below 1 kHz, but its sensitivity rapidly decreased above 4 kHz. A. carolinensis is more sensitive than the budgerigar to low frequencies (1 kHz). However, A. carolinensis maintained high sensitivity to nearly 10 kHz, showing a greater frequency range than any of the other animals tested. These results are consistent with others that have shown that (1) lizards are, in some cases, as sensitive and as broad in frequency response to sound as some birds; (2) among lizards, geckos are generally the most sensitive to low frequencies (4 kHz, some groups of species have a broader sensitivity (Manley and Kraus 2010). Another interesting feature is the ability of lizards to localize sound. Mammals localize sound based on differences in arrival time and intensity of signals at the two ears. However, the heads of lizards are too small to rely on this mechanism and instead probably rely on a pressure-differential mechanism for sound localization. The middle ears on each side of the lizard’s head are directly exposed to the oropharynx, resulting in a wide air-filled connection between the two tympanic membranes. Any sound therefore reaches each tympanic membrane through two pathways: from outside the head and traveling through the contra-lateral tympanum to the inside of the tympanic membrane. The difference in phase and intensity of the pressure changes at the tympanum depends strongly on the direction from which the sound emanates relative to head position (ChristensenDalsgaard 2011). Christensen-Dalsgaard and Manley (2005) have measured tympanum motion as a function of signal direction and shown that the response of the tympanum is highly directional, and that the vibration pattern of one tympanum can provide a very precise directional cue. Their measurements and models suggest that the lizard ear may be the most directionally sensitive hearing mechanism found in any vertebrate (Christensen-Dalsgaard 2011), although this has not been confirmed with behavioral experiments. What Do Lizards Use Hearing For? Lizards possess sophisticated ears, but information on what they use hearing for is sparse. Presumably, hearing is used for the location of prey and/or potential threats. Only one study has demonstrated the use of sound for prey localization: Sakaluk and Belwood (1984) showed that the Mediterranean House Gecko (Hemidactylus turcicus) locates crickets based on their calls. Some

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species have been shown to respond to sounds of other species, including alarm calls (Vitousek et al. 2007) or sounds produced by potential predators (Huang et al. 2011). Sound Production and Communication A wide variety of species create simple sounds by rapid expulsion of air from the mouth producing “hissing,” “squealing,” “squeaking,” or “huffing” sounds (Gans and Maderson 1973; Labra et al. 2007, 2013; Hoare et al. 2013; Reyes-Olivares and Labra 2017). These sounds are most often heard when the animals are captured (often referred to as “distress” or “release” calls) or threatened by a predator. Anolis grahami produce such sounds when captured, but they also produce these sounds during aggressive interactions, usually while lunging at an opponent (Milton and Jenssen 1979). All of these sounds are characterized by their simple structure and seem to be produced in the absence of any specialized anatomical structures. Auditory communication is particularly useful at night, and communication using complex vocalizations produced by sound-producing organs occurs only in the nocturnal geckos, where it is widespread. Geckos have evolved specialized modifications of the larynx and glottis that function as vocal cords (Young et al. 2013). Marcellini (1977) noted that geckos can produce sounds ranging from quiet “squeaks” and “chirps” to more intense “growls” or “barking” sounds. He described two basic call forms: “single-chirp” calls consisting of a short emission with a broad frequency range and “multiple chirp” (MC) calls consisting of repeated vocalizations in some regular pattern. Frankenberg and Werner (1992) refer to the single chirp calls as “distress” calls—noting that they are produced when an animal is captured or threatened by a predator. The MC calls are observed in many species during male–male territorial aggressive interactions, as well as in other kinds of social interactions. Hibbitts et al. (2007) showed that the dominant call frequency of the loud territorial calls of Common Barking Geckos (Ptenopus garrulus) correlates with body size and influences the probability of another male attacking. Tang et al. (2001) showed that Gekko gecko utilizes a variety of different call types, including simple “distress” calls and complex advertisement calls made up of combinations of distinctly different types of clicks. In general, the individual elements of gecko calls are not complex, consisting of brief duration broad-frequency emissions. However, some species produce different sounding variations. The individual elements are sometimes combined into a diversity of different call types that may have considerable structure. A critical question for this chapter is whether there is an evolutionary relationship between call structure and auditory response. While lizard hearing across groups is broadly similar in terms of frequency response, there are some differences and there is some evidence that calls and auditory response have coevolved. In most gecko calls, the energy peak falls within the region of highest frequency sensitivity (2–4 kHz). In G. gecko, there are two sensitivity peaks in the audiogram: one at 500 Hz that corresponds to the peak energy of two of their single chirp calls and another at 1.6 kHz that corresponds roughly to the second energy peak at 1.3 kHz in these calls (Brittan-Powell et al. 2010). Chen et al. (2016) studied a set of very soft calls (repeated chirps) produced by Gekko subpalmatus and found that their dominant frequency ranged from 2.47 to 4.17 kHz and generally overlapped with the region of highest auditory sensitivity (2–4 kHz). An unusual case is found in pygopodids of the genus Delma. They possess a remarkable level of high-frequency auditory sensitivity. Auditory stimuli of up to 14 kHz produced a detectable neural response with peak sensitivity at 10–12 kHz. These gekkotans have not been observed to use sound in social contexts, but they do produce “distress” calls when captured. While the calls have a broad frequency distribution, their energy peak is 8–12 kHz (depending on species and call type). These calls would be largely undetectable to predators such as birds, but should be easily detected by conspecifics (Manley and Kraus 2010).

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Communication by Substrate Vibration Not all sound travels through the air, and detection of vibration through solid substrates represents another potential avenue of communication. Substrate vibration has been shown to be used for prey localization by the semifossorial Sandfish Skink, Scincus scincus (Hetherington 1989). By inserting their head into the sand, they can detect the presence of prey up to 15 cm away. The mechanism of detection is unknown, but it is quite possible that direct vibration via the auditory system is used. Wever (1968) noted the great simplification of the chameleon ear (no tympanic membrane). He also noted that the ear could be efficiently stimulated by direct vibration of the head and speculated that their auditory system might have evolved for direct detection of substrate-borne vibration. This prediction was later shown to be true for at least one species of chameleon. Barnett et al. (1999) discovered that male Veiled Chameleons (Chamaeleo calyptratus) produce a series of short low-frequency vibratory signals when a receptive female is placed on the same branch, while the same male produces no vibratory signals when the female is absent. It makes sense that a slow-moving, cryptically colored, strictly arboreal animal like a chameleon would evolve the use of substrate vibration for signaling, as it is almost undetectable to any animal not standing on the same branch. There has been no systematic attempt to look for other examples of vibratory signaling by chameleons, but Barnett et al. (1999) report several anecdotal accounts of other chameleon species producing buzzing or “low purring sounds” that probably serve as substrate vibration signals in the wild. SUMMARY The physical properties of animal signals (and signal components) are the result of a complex set of interacting evolutionary forces. First, they have been strongly influenced by the evolutionary origins of the anatomical structures, physiology, and behaviors that comprise them. Second, the function(s) of each signal places strong selection pressures on physical form. Third, for signals that provide receivers with information (such as signaler quality or status), the properties are strongly influenced by the mechanistic links that constrain them to some degree of honesty. Finally, in addition to these selective forces, there is evolutionary pressure to effectively stimulate the sensory system of the signal receiver. Most sensory systems have evolved in order to sample and extract many different kinds of relevant information from the environment (e.g., the detection of food, shelter, threats, and the behavior of conspecifics). Because of these generalized requirements, sensory response properties are rather similar across broad taxonomic groups and generally appear to be fairly, evolutionarily conservative. Communication signals are much more diverse and, in most cases, appear to have evolved more recently than the sensory systems. Thus, sensory response properties act as a constraining and/or directing force in signal evolution. In visual signaling, we find that attention is elicited most effectively by chromatic and luminance (or brightness) stimuli that are distant in color space from typical backgrounds. We find that some, but by no means all, species evolve colors that are predicted to be the most highly visible. For transfer of information about the signaling individual, chromatic signals are more effective than luminance signals. Information about species or group identity is effectively signaled by stimuli that are distinct in visual space from distractors, and that change little in appearance with small variations in physical makeup. Information about individual quality, or other individual variation, is best signaled by color patterns for which small variations can be readily detected. Such patterns often involve spectra that change shape sharply in regions of high sensitivity to spectral change.

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Visual motion stimuli that involve abrupt steplike patterns, or long duration repeated patterns, are effective at eliciting attention. Species identity is most effectively signaled by motion patterns that use a consistent stereotyped pattern of up and down movement, because visual motion sensitive neurons respond strongly to stops and starts and/or changes in motion direction. Temporal patterns of shifting motion direction do not change with distance viewing angle or partial blockage of view. Changeable elements, including postural alterations or temporally variable movements, can signal motivation or other variable conditions. In lizard chemical communication systems, there is some evidence for environmental tuning. However, we are unable to find any systematic links between signal design and receiver chemosensory capabilities. Thus, it seems that, in contrast to signals associated with other sensory modalities, chemical signals have been little modified during their ritualization from cues to communicative signals. As many chemical signals evolve from sender precursors that are already detectable by receivers, there probably has not been a strong selection pressure for the evolving signals to match the sensitivity of the receivers’ receptors. This, together with the diversity of compounds used as chemical signals and the broad scope and narrow selectivity of vertebrate olfactory systems generally, has produced a scenario with few clear patterns. Auditory (or vibratory) communication in lizards is much more limited in phylogenetic breadth, diversity, and complexity than in the other major terrestrial vertebrate groups. The reason for this is not immediately obvious. While it is clear that other sensory modalities (vision and chemical senses) play a more important role for most lizards, it is not obvious why communication by sound is not more important in this group.

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Chapter  8

Phylogeny and Ontogeny of Display Behavior Michele A. Johnson Trinity University

Ellee G. Cook University of Missouri

Bonnie K. Kircher University of Florida

CONTENTS Introduction..................................................................................................................................... 259 Evolutionary Analysis of Lizard Display Behaviors....................................................................... 262 Diversity of Displays across Lizard Families................................................................................. 265 The Ecological Contexts of Lizard Display: A Closer Look at Four Taxa..................................... 268 Anolis......................................................................................................................................... 268 Sceloporus.................................................................................................................................. 272 Podarcis...................................................................................................................................... 273 Geckos........................................................................................................................................ 275 The Development of Lizard Displays............................................................................................. 275 Development of Motion Displays.............................................................................................. 276 Development of Color Displays................................................................................................. 277 Current Status of Display Development..................................................................................... 278 Conclusions and Future Directions................................................................................................. 278 Acknowledgments........................................................................................................................... 279 Appendix 1: Descriptions of Lizard Display..................................................................................280 References.......................................................................................................................................280 INTRODUCTION The displays that lizards use to interact with one another communicate a diverse range of messages and incorporate a striking variety of behaviors (reviewed in Fox et al. 2003). These behavioral displays may advertise, for example, the intrinsic quality of an individual and/or its immediate motivation, and they often differ between males and females, and between juveniles and adults (Bradbury and Vehrencamp 1998). Many male displays occur in the context of courting females, and females may respond with displays that indicate either receptivity to or rejection of a potential mate. Lizards of both sexes also use displays in aggressive contexts—to defend a territory from an 259

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intruder, to advertise its presence on a territory to any unseen observers (such displays are often called assertion displays), or to indicate dominance or submission during a conflict (Stamps 1977). In addition, many of the same types of displays that are directed to conspecifics in social contexts may be directed toward potential predators to deflect, deter, or confuse the predator’s attack (reviewed in Cooper and Blumstein 2015). Lizard displays often include movements of one or more body parts, frequently revealing brightly colored structures that, in some taxa, can change colors within moments during an interaction, or across seasons to indicate reproductive or dominance status. These visual displays may occur in conjunction with, or independently of, chemical or a­ uditory displays as well. In this chapter, we examine patterns of lizard display at multiple phylogenetic scales to explore their evolution and development. We consider “displays” to include any behaviors (or their static modifiers), of any duration, that serve to communicate a message to conspecific or heterospecific individuals. In this chapter, we focus primarily on the evolution and development of visual displays. Across lizard taxa, species have evolved visual display behaviors that involve moving nearly every part of the body (Figure 8.1). Many of these displays consist of postural changes that may function to make the displaying lizard appear to have a larger body size or indicate the lizard’s motivational state, and include dorsoventral flattening, arching the back or neck, inflating the body, or raising a nuchal or dorsal crest. Movements of the head occur in many displays as well, i­ nvolving up and down headbobs or lifts, or side-to-side head sways or circles (e.g., Martins et al. 2004). Many lizards also gape, holding their mouths open and sometimes also sticking out the tongue, during aggressive displays (e.g., Lappin et al. 2006). Some species extend a throat fan or dewlap during displays, while others inflate or engorge their throat (Ord et al. 2015). Other displays involve movements of the limbs, via push-ups, holding the body off the substrate with full limb extensions, ­lifting or waving the forelimbs or hind limbs, rocking or swaying the body, or walking using stiff or jerky movements (e.g., Martins 1993). Finally, movements of the tail are commonly used in display, as the tail can be raised, wagged, curled, or vibrated (e.g., Marcellini 1977). Many of these movement displays also serve to advertise colorful regions or structures. Although the dorsum of many lizards is fairly inconspicuous, often providing camouflage to the lizards in their habitat, the underside of the throat, belly, vent, or tail is often brightly colored and may be exposed during push-ups or dorsoventral flattening displays (e.g., Wiens 2000; Pérez i de Lanuza and Font 2010). Similarly, the dramatic colors of the tongue or the lining of the mouth may be exposed during gapes. In addition, the head, dorsum, lateral sides, limbs, feet, or tail of the lizard may exhibit vibrantly colored spots or areas. A number of species have also evolved the ability to change the color of their whole body, or of one or more areas of the body, during social interactions. Within seconds to minutes, many lizards can darken or lighten the body, develop colorful spots on the dorsum, or even change their dorsal coloration patterns altogether (e.g., Stuart-Fox et al. 2007). Other species develop seasonal coloration patterns to advertise mating preparedness, receptivity, gravidity, or social dominance (e.g., Weiss 2006). Visual displays may be accompanied by or used independently of chemical displays. Most lizards communicate via chemical cues that are generally produced by the skin or in a series of ­specialized glands, and often deposited through dragging their body along a substrate, or in their feces (reviewed in Simon 1983; Martín and López 2014). Chemical communication is often difficult for researchers to observe, as humans cannot detect these cues directly, but lizards that frequently produce chemical cues often detect such cues via frequent tongue flicks that bring the molecules from the air or substrate into contact with their vomeronasal organ, a behavior that may be easily quantified. Finally, lizards may also produce vocalizations, either as calls or croaks, or via hissing (reviewed in Marcellini 1978). Other species vibrate their tails or other structures to produce a buzzing sound. While visual and chemical displays are common across lizards, auditory communication is r­ elatively rare in this group (with the exception of geckos, which frequently use auditory displays).

Phylogeny and Ontogeny of Display Behavior

(a)

(b)

(c)

(d)

261

(e)

(f)

(h)

(g)

 he diversity of lizards and their Figure 8.1  T displays. (a) Northern curly tailed lizard (Leiocephalus carinatus) performing curled tail displays, Crooked Island, Bahamas. (b) Hispaniolan ground iguana (Cyclura ricordi) performing gaping display, Lago Enriquillo, Dominican Republic. (c) Texas banded gecko (Coleonyx brevis) performing a tail wagging display, Texas. (d) Barred anole (Anolis stratulus) extending its  dewlap, Rio Grande, Puerto Rico. (e) Texas spotted whiptail (Aspidoscelis gularis), Texas. (f) Texas spiny lizard (Sceloporus olivaceus) showing blue belly patch during push-up display, Texas. (g) Brown basilisk (Basilicus ­vittatus) with head crest, Florida. (h) Broad-headed skink (Plestiodon laticeps) with orange breeding colors, Louisiana. (All ­photographs by M.A. Johnson or B.K. Kircher.)

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In this chapter, we first examine the distribution of display behaviors across lizard families, measuring phylogenetic signal in visual displays (posture, motion, and color) and vocal displays, and testing for correlated evolution among these traits. We also review the major components of common displays in each major lizard clade. We next consider the diversity of displays among several well-studied groups of lizards (Anolis, Sceloporus, Podarcis, and geckos) in more detail, with a focus on the selective pressures associated with particular components of display. We then describe the development of lizard display behavior, focusing on two aspects of display on which ontogenetic studies have been conducted—the development of the anole dewlap display, and the transition between juvenile and adult tail color and use in skinks and lacertids. We conclude with a discussion of the major themes identified in the chapter, with an emphasis on the future directions suggested by this work. EVOLUTIONARY ANALYSIS OF LIZARD DISPLAY BEHAVIORS To categorize the remarkable diversity of lizard display behaviors, we performed a survey of the scientific literature using Scopus and Google Scholar, searching for descriptions of behavioral displays in each of the 453 lizard genera in 43 families (Pyron et al. 2013). We recorded whether the displays of any species within each genus included postural changes (e.g., dorsoventral flattening, arching of the back, raising a crest, or inflating the body), head movements (bobs, shakes, circles, or lifts), gaping, extension of the gular region (dewlap extensions or throat ­inflations), limb movements (including push-ups, full limb extensions, swaying or rocking the body, walking with stiff or jerky motions, or lifting or waving the limbs), or tail movements (wags, lifts, curls, or vibrations). From these data, we determined the proportion of genera in each family (among those for whom we found descriptions of displays) that exhibited each of these six classes of postural change or movement in their displays, and the total number of distinct display components performed within each family (e.g., if lizards in a family arched their back, raised a crest, and performed push-ups, this was recorded as three motion/posture components; Figure 8.2). We also recorded how color was used in displays across a genus, noting display-associated ­colors on the belly or vent, throat, dorsum or sides, tail, head, limbs or feet, or inside the mouth. We recorded color using verbal descriptions of color in the literature (e.g., red, yellow, green), although if these descriptions listed multiple descriptions of a similar color (e.g., pink, rose, and light red), we recorded that as one color. Further, because humans also do not see ultraviolet (but lizards do; Fleishman et al. 1993), our summary of color is likely to underestimate the diversity of color in these groups. From these data, we estimated the number of colors used in display for each family, and the number of locations on the body in which colorful patches were used in display. We also noted whether members of each family were known to change their body color during social interactions, or if body colors changed seasonally (Figure 8.2). Finally, we determined the proportion of genera in each family that vocalize during social ­displays. We then mapped all of these display traits onto the family-level phylogeny from Pyron et al. (2013) (Figure 8.2). In our literature survey, we found information on displays of 199 genera in 31 f­ amilies (Appendix 1). The families for which information was most limited were those that are ­primarily ­fossorial and/or nocturnal, often with reduced eyes (Dibamidae, Rhineuridae, Bipedidae, Blanidae, Cadeidae, Trogonophilidae, Amphisbaenidae, Xenosauridae, Anniellidae, Lanthanotidae, and Hoplocercidae). We conducted subsequent family-level analyses using only the 29 families for which we found descriptions of more than 20% of the genera in the family. Although our survey was not an ­exhaustive search of the literature, our compilation of ­descriptions of lizard displays allowed us to identify several broad-scale patterns in the ­evolution of display behaviors.

colo r inter change actio in ns seas onal bree ding colo rs voca lize

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Scincoidea

1

2

3

4

5

6

7

8

9

10

11

12

Sphenodontidae Dibamidae Carphodactylidae Pygopodidae Diplodactylidae Eublepharidae Sphaerodactylidae Phyllodactylidae Gekkonidae Xantusiidae Gerrhosauridae Cordylidae Scincidea Teiidae Gymnophthalmidae Rhineuridae Bipedidae Blanidae Cadeidae Trogonophiidae Amphisbaenidae Lacertidae Xenosauridae Helodermatidae Anniellidae Anguidae Shinisauridae Lanthanotidae Varanidae Chamaeleonidae Agamidae Dactyloidae Tropiduridae Leiocephalidae Corytophanidae Crotaphytidae Phrynosomatidae Polychrotidae Hoplocercidae Iguanidae Opluridae Leiosauridae Liolaemidae

1

1

1

0

1

0

6

1

1

Y

N

0

Blomberg's K P value for K

1

0

0

0

1

1

4

0

0

N

N

1

0.43 0.33 0.60 0.25 0.39

0.29 0.30 0.60 0 0.11

0.43 0 0 0 0.17

0.14 0 0.60 0 0.17

0.71 0.67 0.80 0 0.56

0.57 1 1 1 0.67

9 5 12 4 10

3 0 2 0 6

5 0 3 0 6

N N N N N

N N N N Y

1 1 1 1 1

0.50 0.32 0.67 0

0.25 0.29 0.33 0

0 0.18 0.33 0

0 0.14 0.17 0

0.50 0.14 0.67 0

0.25 0.32 0.33 0.29

5 11 8 2

5 5 3 5

4 5 3 6

N N N Y

Y Y N Y

0 0.04 0 0

0.18

0.05

0

0.09

0.09

0.14

8

5

5

N

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0

0

0

0

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0

1

1

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3

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0

0.13 0

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1 0.78 0.45 1 0.50 1 0 1 0.56 1

1 0.56 0.61 1 0.50 1 1 1 1 1

1 0.56 0.24 0 0.17 1 0 0.50 0 1

1 0.44 0.52 1 0.50 1 0.50 1 0.67 1

0 0.44 0.52 1 0.33 1 0 1 1 1

1 0.33 0.33 0 0.50 1 0 0 0.56 0

5 11 14 5 9 10 2 6 8 5

0 7 7 2 3 0 0 2 3 0

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N Y Y Y Y Y N N N Y

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1 0.33 0.09 0 0 0 0 0 0 0

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0.63 0 0 1

9 6 3 5

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0.13 0 0.33 0

0.60 0.356

0.85 0.011

0.81 0.144

1.18 0.002

0.52 0.600

0.64 0.246

0.47 0.571

0.67 0.163

0.71 0.095

0.68 0.126

0.50 0.716

1.42 0.004

263

Figure 8.2  Phylogeny of lizard families (adapted from Pyron et al. 2013) and the components of their social displays. (Families for which we compiled information for fewer than 20% of the genera in the family are left blank.) The first six columns indicate types of posture- and motion-based displays and report the proportion of genera in a given family that use each type of display. In the cells of these columns, values for families in which more than half of the genera use a particular display type are highlighted in a darker color, and those for families in which more than 30% of genera use that display type are highlighted in a lighter color. The following three columns indicate measures of display complexity—the number of distinct postures or motions in a family’s display repertoire, the number of body areas on which color is displayed, and the number of colors used in that family’s displays. Cells in these columns are highlighted if the family exhibits greater than the median number of posture or motions, or color measures. The following two columns indicate whether members of a family exhibit rapid color changes during interactions, or seasonal color changes to signal reproductive or social status, and cells are highlighted if any members of the family have been reported to do so. The final column indicates the proportion of genera in a family that vocalize during displays, and cells are highlighted as in the first six columns. Measures of phylogenetic signal (Blomberg’s K) and their corresponding p-values for each trait are provided below the phylogeny.

Phylogeny and Ontogeny of Display Behavior

Gekkota

Column Number:

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To measure phylogenetic signal in display traits, we used the phylosig function in the “­phytools” package (Revell 2012) of R (R Core Development Team 2014) to measure Blomberg’s K for each trait. We found significant signal in the proportion of families that exhibit head movements, ­extension of the gular region, and vocalization (Figure 8.2). The presence of strong phylogenetic signal indicates that closely related families are likely to resemble one another in these components of display more than a random assemblage of families would, hinting that these traits may evolve more slowly than the other components of lizard displays. We also explored evolutionary correlations among display traits, using the Maximum Likelihood method of calculating Brownian correlations using the gls function in the nlme package (Pinheiro et al. 2017) in R. We found two main clusters of correlated traits in this analysis. First, five of the six classes of posture and movement displays (postural changes, head movements, gape, gular ­extension, and limb movements) were correlated with one another (all p < 0.056), although tail movements were not correlated with any of these other posture/movement displays (all p > 0.2). This suggests that the complex of posture and movement displays (excluding tail motions) evolved in association (i.e., were gained or lost together) across lizard families. The second cluster of ­correlated traits relate to the complexity of displays: the number of posture/motion displays in a family, the number of colors used in displays, and the number of body parts in which colors are displayed are strongly associated (all p < 0.01). This finding indicates that families evolved complexity in motion and color components of display together. To determine whether families that display color changes differ in display types from those whose colors remain stable, we performed phylogenetic ANOVA using the aov.phylo function in the geiger package (Harmon et al. 2008) in R. We found that families with the ability to change colors quickly (e.g., during social interactions; n = 10) did not differ in any display traits from families that did not change colors quickly (n = 19; all p > 0.13). In contrast, families that evolved seasonal (breeding) color changes (n = 13) had more complex displays than families that did not change color seasonally (n = 16), with more motions in their social displays (F1,27 = 5.04, p = 0.030), more colors in their displays (F1,27 = 25.7, p = 0.001), and more body areas involved in colorful displays (F1,27 = 39.6, p = 0.001). In addition, tail displays were less common in the families with seasonal color change than those without seasonal color changes (F1,27 = 4.51, p = 0.043). Overall, this analysis reveals that some components of display are more common among ­l izards than others, and that the components of social display have not evolved independently of one another across lizard families. This consideration also points to numerous avenues for future work. First, basic natural history research on understudied taxa is a critical need, and addressing these gaps should be a long-term goal of our field. But even among well-studied taxa, many questions remain. For example, ancestral state reconstruction analyses could reveal whether colorful displays evolved repeatedly, or if this is an ancestral display trait that has been maintained in many lizard taxa. These types of analyses could also address whether distantly related nocturnal species have evolved ­similar behavioral displays in parallel, or if the displays of nocturnal species result from repeated evolutionary loss of display complexity. Models of the evolution of multidimensional trait space could suggest whether there are constraints on the pathways through which display components coevolve; perhaps there are limited ways in which an animal can move its various body parts or constraints on the ways movements can be performed together or colors may be produced. Further, tail displays seem to evolve in a very different pattern than other types of movement displays, and more attention to the evolution of these displays is warranted. In addition, this work illustrates that there are lizard taxa with substantial variation in display traits (Figure 8.2). Examination of closely related groups that differ in display behaviors, or of ­families in which some but not all taxa exhibit a certain display component, could reveal the factors that lead to such variation and the physiological or evolutionary mechanisms that underlie it.

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DIVERSITY OF DISPLAYS ACROSS LIZARD FAMILIES In addition to these large-scale patterns in the evolution of lizard displays, a consideration of display diversity within the major clades also reveals notable trends. First, Sphenodontidae, a group whose only extant species (Tuatara) is the closest relative of all other squamates, exhibits a relatively complex display (Gillingham et al. 1995). The tuatara display includes a range of posture and motion displays (push-ups, headbobs and circles, arched back, nuchal crest, and gapes), and a darkening of the shoulder and eye regions during courtship. Tuatara also utilize chemical cues, but do not vocalize. Together, this suggests that the ancestral squamate communication behaviors likely included fairly elaborate movements (although tail movements are not part of tuatara displays), but relatively simple color components of visual display. Because tuatara are primarily nocturnal, yet the common ancestor of lizards was likely diurnal (Fleishman et al. 2011), it is possible that color displays were more elaborate in the ancestral lizard lineage but lost in tuatara as their nocturnal ecology evolved. The Gekkota are a group of seven families, composed of 110 genera (Pyron et al. 2013). Geckos include both nocturnal and diurnal species, and some species are limbless and fossorial (e.g., family Pygopodidae). Gecko communication includes a diversity of posture- and motion-based displays, chemical cues, and notably, frequent vocalizations, but compared to many other taxa, colorful displays are relatively rare in the group. Gecko-typical displays often involve archedback postures, full limb extensions, tail wagging or curling, and in some groups, head movements (reviewed in Marcellini 1977). Among Gekkota, genera in family Gekkonidae are the most colorful, with orange, yellow, black, or white tails; red tongues or mouths; and throat patches or dorsal markings of various colors (Marcellini 1977; Appendix 1). Several Diplodactylidae genera exhibit colorful tails or lining of the mouth (e.g., Melville et al. 2004), and a few Sphaerodactylidae have colorful heads using in display (e.g., Martínez-Cotrina et al. 2014). Few geckos exhibit color changes. Because the diurnal geckos are secondarily diurnal, evolving from nocturnal lineages, they offer a particularly ­interesting group in which to further consider the evolutionary patterns of display behaviors. Scincidea is composed of four families, with a total of 131 genera (113 of which are in family Scincidae; Pyron et al. 2013). Across the infraorder Scincoidea, the prevalence of display behaviors is highly variable, as many species in this group are fossorial and/or limbless, while others are ­conspicuous and social, and all rely heavily on chemical communication. Little information on display behaviors was available for family Xantusiidae, the night lizards, which live in crevices and under rocks or logs, and family Gerrhosauridae, the African plated lizards. Genera in family Cordylidae use a combination of motion and color displays. Posture and motion displays in this group include push-ups, dorsoventral flattening, and occasional tail movements, while many cordylid species exhibit colorful throat and belly patches (and in Platysaurus, forelimbs) that are yellow, orange, or even turquoise (e.g., Wirminghaus 1990; Mouton and Van Wyk 1993; Whiting 1999; Stanley et al. 2011). In the speciose Scincidae group, common displays include back arches, headbobs, gaping, and tail wags, while some taxa wave the forelimbs or enlarge the throat (e.g., Torr and Shine 1994; Murphy and Myers 1996; Head et al. 2005; Sánchez-Hernández et al. 2012). Common skink color displays include yellow or orange head, throat, belly, and vent patches, which often become intensified during the breeding season and may indicate dominance (e.g., Smyth and Smith 1974; Stapley 2008). Infraorder Lacertoidea (Pyron et al. 2013) consists of nine families, with 94 genera, all of whom rely heavily on chemical communication (Baeckens et al. 2015). This group includes the teiids and microteiids (families Teiiade and Gymnophthalmidae, respectively), the lacertids (family Lacertidae), and a monophyletic clade of six families of worm lizards (amphisbaenians) for which little information on social displays is available. While they are sister taxa, teiids and microteiids have very different components of social display. Teiids exhibit complex displays that frequently

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include dorsoventral flattening, full limb extensions, headbobs, gapes, and limb waves (Lindzey and Crews 1986; Herrel et al. 2009). Teiid color displays are less common, but include the blue belly and throat patches and orange venters of the whiptail lizards Cnemidophorus and Aspidoscelis (Bostic 1966). Males of these genera also perform “swiggle walks” to spread pheromones (Lindzey and Crews 1986). Microteiids, on the other hand, perform some tail movements (Teixeira et al. 2013) but no other motion displays. Yet, they exhibit a diverse array of color displays, including red/orange or green/blue belly patches; red and orange throat patches, jaws, and tails; and y­ ellow or orange ­forelimbs (e.g., Vitt 1982; Chávez and Vásquez 2012; Recoder et al. 2014). Some microteiids also exhibit seasonal changes in belly and throat colors (Recoder et al. 2014), and belly color may indicate dominance in aggressive interactions (Fouquette 1968). Lacertids also perform posture changes or movement displays relatively rarely; most genera of lacertids use some movement in their displays, but few include more than one (Appendix 1). Commonly used posture and motion displays include dorsoventral flattening, head or tail movements, and throat inflation (e.g., ­Molina-Borja et al. 1998; Lailvaux et al. 2012). Yet, like microteiids, lacertids exhibit a wide range of color displays, including blue, yellow, orange, and green patches on the belly, throat, and dorsum, and in many taxa, these colors are enhanced during the breeding season (e.g., Galán 2008; Hawlena 2009; Pérez i de Lanuza and Font 2010). Infraorder Anguimorpha includes seven families with 18 genera (Pyron et al. 2013). As a group, anguimorphs use posture and motion displays and chemical communication more often than color displays. The largest family of anguimorphs is Anguidae (glass and alligator lizards), a group in which behavioral displays are relatively rare, although some genera perform dorsoventral flattening, head movements, gaping, or tail wags (e.g., Bowker 1988; Campbell 1994). Anguids may use green, yellow, or red belly patches, blue spots on the dorsum, or yellow feet in their displays (McConkey 1954; Campbell 1994; Capula et al. 1998), and some alligator lizards vocalize (Greene et al. 2006). Anguimorphs also includes three single-genus families that use a diversity of postures and ­movements in their communication displays: Helodermatidae (gila monsters) exhibits dorsoventral flattening, back arches, and neck arches (Beck and Ramírez-Bautista 1991); Shinsauridae (Chinese crocodile lizards) performs push-ups, headbobs, tail wags, limb waves, and gapes (Ray and Walley 2003); and Varanidae (monitor lizards) displays include dorsoventral flattening, headbobs, gapes, tail wags, dewlap extensions, and vocalizations (Murphy and Mitchell 1974; Bels et al. 1995). Those anguimorphs with little available behavioral information include family Xenosauridae, which rarely emerge from rock crevices; family Anniellidae, which are limbless, fossorial lizards (Germano and Morafka 1996); and family Lanthanotidae, which are nocturnal lizards with reduced eyes (Mendyk et al. 2015). Finally, Iguania includes 14 families, composed of 97 genera (Pyron et al. 2013). Most Iguania taxa perform elaborate displays using color, posture, and motion, and these displays have been described in detail for many Iguanian species. Only family Hoplocercidae (clubtails and wood ­lizards) is too little studied to include in this analysis. In contrast, displays of the clade of ­chameleons and agamids have been characterized in detail. Chameleons (family Chameleonidae) are best known for their dramatic ability to rapidly change their body color, and their nuanced use of color in social displays is a focus of much research (e.g., Gehring and Witte 2007; Stuart-Fox et al. 2007). Yet, chameleons also use extensive posture and motion displays, including ­dorsoventral ­flattening, rocking the body, headbobs, gapes, and enlarging the throat, and lizards in several chameleon ­genera also vocalize (e.g., Bustard 1965; Karsten et al. 2009; Chiu 2013) or perform ­substrate vibrations (Barnett et al. 1999). Lizards in family Agamidae also exhibit complex behavioral displays. Agamids frequently perform dewlap or neck frill extensions, push-ups, headbobs, dorsoventral ­flattening, and tail wags, while some also raise a dorsal crest, wave forelimbs, or gape (e.g., Shine 1990; Mori and Hikida 1994; Peters and Ord 2003; Pandav et al. 2007; Patankar et al. 2013). In addition, agamids are strikingly colorful lizards, with patches of color used in displays on the throat, belly, vent, sides, tail, and inside the mouth (e.g., Madsen and Loman 1987;

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LeBas and Marshall 2000; Qi et al. 2011; Baird et al. 2013). Colors used in agamid display range across red, orange, yellow, blue, and black, and can change during social interactions and across seasons (e.g., Norfolk et al. 2010; Quah et al. 2012). Family Dactyloidae (anoles) are among the most diverse and well-studied iguanian lizards, and their displays primarily include push-ups, headbobs, dewlap extensions, and dorsoventral flattening, with nuchal crests and dark eyespots forming in particularly aggressive encounters (Jenssen 1977). Anoles are sometimes called “American chameleons” for their ability to rapidly change color (usually between their base dorsal color and dark brown), and their highly varied, brightly colored dewlaps have been a focus of much work on the evolution of visual display (reviewed in Losos 2009). Similarly, lizards in family Tropiduridae exhibit the same general types of visual display as anoles (e.g., Debusk and Glidewell 1972; Carpenter 1977; Watkins 1998), with species in some genera also displaying yellow and black belly and throat patches, and seasonal orange head patches (e.g., Clark et al. 2015). The displays of family Leiocephalidae (curly tail lizards) most prominently feature curled tails, but also include push-ups and headbobs, and flattening and inflating the body and throat (Cooper 2001). While some species darken during social interactions (Phillips and Howes 1988), color is not a major component of the displays in this group. Lizards in family Corytophanidae perform headbob and dewlap displays (e.g., Davis 1953), and Crotaphytidae use dewlaps, headbobs, push-ups, and gapes in their displays (Yedlin and Ferguson 1973; Tollestrup 1983; Lappin et al. 2006), along with pink, red, or orange spots that indicate reproductive status (Germano and Williams 2007). Family Phrynosomatidae also exhibits Iguania-typical movement displays (headbobs, push-ups, dorsoventral flattening, tail movements, and dewlap extensions), and many phrynosomatids have blue or black belly and throat patches, some of which are enhanced during the breeding season (reviewed in Wiens 2000). The remaining five iguanian families also exhibit variations on the iguanian movement displays. Lizards in the Polychrotidae perform headbobs, gapes, dewlap extensions, and body-rocking, and their colors change during social interactions (Vitt and Lacher 1981). Iguanas (family Iguanidae) perform headbobs and circles, push-ups, dorsoventral flattening and body inflation, gaping, tail movements, and dewlap extensions (e.g., Evans 1951; Carpenter 1961; Dugan 1982; Martins and Lamont 1998). Iguanian color displays consist primarily of darkening the body during dominance interactions, although some species have brightly colored sides. Lizards in the family Opluridae perform push-ups, headbobs, dewlap extensions, and dorsoventral flattening, and exhibit yellow to red throat patches and dorsal coloration during the mating season (e.g., Blanc and Carpenter 1969). Leiosaurs (family Leiosauridae) perform back arches, headbobs, and gapes (e.g., Barreto Lima and de Sousa 2006), and Urostrophus have a dewlap (Etheridge and Williams 1991), while Pristadactylus can communicate by hissing (Labra et al. 2007). Colors are a minor component of leiosaur display. Lizards in family Liolaemidae perform limb waves, headbobs, body flattening, dewlap extensions, and tail wags, but also do not appear to use color in their displays (Martins et al. 2004; Halloy et al. 2013). Together, these descriptions reveal that there are many successful combinations of lizard ­display behaviors. Some taxa rely more on posture or motion than color, others use predominantly color displays, and many use color, posture, and motion. Yet, some taxa appear to use few, if any, visual display behaviors in intraspecific communication. In addition, several lizard taxa use ­auditory communication, and many use chemical cues. These large-scale evolutionary trends in display evolution reflect the pressures imposed by the complex environments in which ­communication occurs. Further, within many lizards, distinctive patterns of display can also be observed among genera, species, and populations, and, in some cases, among individuals within populations. Next, we consider the causes and consequences of display variation at these finer taxonomic scales, and highlight the importance of biotic and abiotic factors in driving the diversification of lizard displays.

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THE ECOLOGICAL CONTEXTS OF LIZARD DISPLAY: A CLOSER LOOK AT FOUR TAXA Lizards occur in a vast array of environments, each of which presents a particular suite of conditions that influence communication. Habitat features, such as light availability or vegetation complexity, may make some signals highly transmissible and render others ineffective. In addition, the composition of the community in which species occur, such as the prevalence of predators or the number of closely related species living in sympatry, may influence the amount of time individuals invest in conspicuous displays. Such constraints exist in every environment, and effective displays must function within them. By considering the contexts in which lizards display, we can begin to understand how evolution has shaped the diversity of displays observed across lizards, and why some elements of display are common across taxa while others are rare. We explored the display behavior of four relatively well-studied groups of lizards—Anolis, Sceloporus, Podarcis, and geckos—in order to highlight both diversity and similarity in display behavior, and communication in general, across the lizard phylogeny. In our discussion of Anolis lizards, we have also included a new phylogenetic analysis of display behaviors to assess evolutionary correlations among display traits in this group. Anolis Among lizards, species in genus Anolis (anoles; family Dactyloidae) have been one of the most prominent systems for investigating the evolution of visual displays (e.g., Jenssen 1977; Ord and Martins 2006). These lizards are diurnal, territorial, insectivorous, and often arboreal. With nearly 400 species distributed throughout the tropical and subtropical regions of the Americas and the Caribbean, and an invasive range that also includes several Pacific islands, Anolis is one of the largest vertebrate genera (Losos and Thorpe 2004; Losos 2009). Species on the Greater and Lesser Antilles have been the most widely studied in this group. Anoles on these islands underwent an adaptive radiation that resulted in the repeated, independent evolution of six types of habitat specialists, called ecomorphs, which differ in behavior, ecology, and morphology (Williams 1972; Losos 1994). The ecomorphs are named for the microhabitat in which they specialize, and include trunk-ground, trunk-crown, trunk, grass-bush, twig, and crown-giant anoles. Anolis lizards that are classified into the same ecomorph frequently r­ esemble one another more closely than do sympatric species in other ecomorphs, although the latter are often more closely related (Losos et al. 1998). This pattern has made Anolis, and particularly the  Caribbean ecomorphs, an interesting group in which to test hypotheses of evolutionary ­convergence in behavior. Anoles rely almost exclusively on visual displays for communication, and they exhibit d­ istinctive display behaviors that consist of headbobs and push-ups accompanied by extensions of a ­colorful throat fan, or dewlap (Jenssen 1977; Fleishman 1992). In most species, dewlaps are present in both sexes, although female dewlaps are often smaller and can differ in color relative to male ­dewlaps. Anole displays are used in a variety of contexts, including territorial defense, courtship, and ­predator deterrence (Trivers 1976; Tokarz 1995; Leal and Rodríguez-Robles 1997). During escalated interactions such as territory disputes, visual displays can be enhanced with several modifiers, including the development of darkened eyespots, dorsal color change, and various postural changes such as dorsoventral flattening and raised nuchal crests. While most anole species exhibit a common repertoire of visual display behaviors, a quick survey of the genus reveals extraordinary diversity in their display characteristics. Among species, there is considerable variation in the temporal patterning of display behaviors—different species perform push-ups, headbobs, and dewlap extensions in a variety of combinations, frequencies, and amplitudes in species-specific patterns (Echelle et al. 1971; Jenssen 1977; Ord and Martins 2006).

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Physical characteristics of the dewlap, including size, color, and pattern, also differ substantially both across the genus and within species (e.g., Nicholson et al. 2007; Ng and Glor 2011). Both display behavior and dewlap morphology likely function in species recognition, which may have contributed to the evolution of variation in displays among sympatric anoles, as evidenced by the observation that display characteristics often differ more between species that co-occur with several congeners than species that occur alone or with one other Anolis species (Williams and Rand 1977; Losos 1985; Ord and Martins 2006). Habitat conditions that influence signal detection also likely played a role in the diversification of anole displays. In particular, differences across habitats in available light conditions may have influenced dewlap design, as allopatric populations of anoles residing in different habitats vary in the dewlap characteristics that contribute to the visibility of the dewlap against the background, such as reflectance (Leal and Fleishman 2004). Additionally, variation in vegetation, the movement of which can interfere with the detectability of motion displays, may make some displays easier to see than others, and therefore may have influenced the diversification of headbob and push-up displays observed across anoles (Fleishman 1986). Interestingly, the same characteristics that make displays highly detectable to anoles may also make them more conspicuous to predators. Furthermore, by utilizing motions that match the background and are thus more difficult to detect by the visual system of Anolis lizards, predators may be effectively concealed from the view of potential prey (Fleishman 1985). Thus, a tradeoff exists in the evolution of displays, balancing the efficacy of signals and the sensory systems attuned to perceive them with constraints present in the environment, such as signaling conditions and predation risk. Although a rich body of research has investigated the behavior, morphology, and ecology ­associated with visual communication in Anolis lizards, many questions remain about the evolution of visual displays in this genus. Here, we present data investigating evolutionary correlations among the components of anole display, and correlations between male and female display. Because interspecific variation in many aspects of ecomorphology has been associated with the repeated radiation of anole species into ecomorph classes (Losos 2009), we also tested the hypothesis that variation in display behavior might also be correlated with ecomorph classification. We examined these relationships using field behavioral data collected from 27 species of anoles from five of the six ecomorphs in the summer breeding season (primarily in May–June 2004–2015 by M. Johnson; data for some species originally published in Johnson 2007; Johnson et al. 2010; Cook et al. 2013). We conducted 10–180 min focal behavioral observations of an average of 31 males per species, and in species where females were observed, an average of 25 females per species (range = 21–152 ­lizards per species). In this dataset, we combined push-up and headbob displays into a single v­ ariable, called push-ups. We performed phylogenetic comparative analyses using the squamate phylogeny in Pyron et al. (2013), pruned to include only the taxa in this study (Figure 8.3). We conducted regressions using PGLS (phylogenetic generalized least squares) with the pgls function in the caper package (Freckleton et al. 2002) in R (R Development Core Team 2014), and phylogenetic ANOVA with the aov.phylo function in the geiger package (Harmon et al. 2008) in R. Among males, the duration of dewlap extension (i.e., the average length of time the dewlap was extended during a single pulse of the dewlap) was not linearly related to the frequency of dewlap extension (i.e., the average rate of dewlap extension per min; PGLS: F1,25 = 1.46, p = 0.24, Adj. R2 = 0.02), yet these traits show a curvilinear relationship where species that extend the dewlap most frequently have a short duration of each display, and those that extend the dewlap for the longest durations do so rarely (Figure 8.4). Most species, however, perform relatively few, relatively rapid dewlap extensions (Figure 8.4). While the frequency of dewlap extension was marginally associated with the frequency of push-ups (PGLS: F1,25 = 3.94, p = 0.058, Adj. R2 = 0.10), this putative relationship disappeared when Anolis carolinensis (a species that performs dewlap and push-up displays far more frequently than the other species in the dataset; Table 8.1) was removed from the analysis (PGLS: F1,24 = 0.24, p = 0.63, Adj. R2 = −0.03). These results show that the components of anole

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Figure 8.3  Phylogeny of Anolis lizards for behavioral data analysis. (Pruned from Pyron et al. 2013.)

Figure 8.4  A  verage male dewlap display measures in 27 species of Anolis lizards.

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Table 8.1  Species Averages for Rate and Duration of Dewlap Display, and Rate of Push-Ups, for Males and Females

Species Anolis angusticeps Anolis bahorucoensis Anolis brevirostris Anolis brunneus Anolis carolinensis Anolis chlorocyanus Anolis christophei Anolis coelestinus Anolis cristatellus Anolis cybotes Anolis distichus Anolis etheridgei Anolis evermanni Anolis grahami Anolis gundlachi Anolis krugi Anolis lineatopus Anolis longitibialis Anolis marcanoi Anolis occultus Anolis olssoni Anolis poncensis Anolis pulchellus Anolis sagrei Anolis smaragdinus Anolis stratulus Anolis valencienni

Ecomorph

Male Dewlaps per Minute

Male Dewlap Duration (s)

Male Pushups per Minute

Female Dewlaps per Minute

Female Pushups per Minute

TW

0.18

2.00

0.58

0.00

0.06

GB

0.00

1.00

0.05

0.00

0.01

T

0.51

2.16

1.12

0.00

0.02

TC

0.19

2.00

1.59

0.00

0.18

TC

1.38

1.91

8.00

0.01

0.47

TC

0.05

27.55

1.07

none

0.12

9.27

1.16

TC

0.13

9.32

1.58

0.02

0.13

TG

0.24

3.51

0.71

0.03

0.07

TG T none

0.23 1.02 0.02

7.79 1.59 7.80

2.03 0.33 0.07

0.02

0.20

TC

0.75

2.13

0.74

TC TG

0.62 0.18

2.50 10.43

0.22 0.69

0.02 0.01

0.11 0.15

GB TG

0.17 0.19

3.56 2.00

0.12 0.33

0.00 0.00

0.01 0.09

TG

0.04

21.70

0.33

TG TW GB GB

0.03 0.15 0.67 0.02

10.18 7.00 1.43 6.25

0.59 0.50 0.39 0.46

0.08 0.12

0.32 0.05

GB

0.39

1.32

0.48

TG TC

0.33 0.32

1.10 1.50

1.19 0.93

0.04 0.00

0.62 0.28

TC TW

2.64 0.61

1.11 1.25

1.13 0.18

0.02

0.03

GB, grass-bush; T, trunk; TC, trunk-crown; TG, trunk-ground; TW, Twig. Blank cells indicate species for which female behavior was not collected.

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display evolve independently of one another—the number and duration of dewlap extensions was not associated with an increase or decrease in the number of push-ups in anoline displays. The displays of males and females were also not related to one another, as male dewlap rate was not associated with female dewlap rate (PGLS: F1,15 = 0.078, p = 0.39, Adj. R2 = −0.01) and male pushup rate was associated with female push-up rate when Anolis carolinensis was included in the a­ nalysis (PGLS: F1,15 = 7.96, p = 0.0129, Adj. R2 = 0.30), but not when it was excluded (PGLS: F1,14 = 3.11, p = 0.10, Adj. R2 = 0.12). Thus, with the exception of A. carolinensis (in which both sexes use pushups at high rates), the frequency of male displays surprisingly does not evolve with the ­frequency of female displays. Our finding that display rates differ between males and females is likely due, in part, to the fact that male anoles generally display much more frequently than females, and particularly perform more territorial assertion displays than females. However, species such as A. carolinensis and A. occultus, in which females display frequently, demonstrate that this is not universally true of anoles. Yet for many species, we lack detailed data on female displays (and female behavior in general). Therefore, this analysis also suggests that not only are we missing basic natural history data on roughly half of the populations that we study, but we may also be missing opportunities to detect how the evolution of displays, communication, and behavior in general may differ in males and females. Further, while there is extensive interspecies variation in dewlap and push-up displays, this variation did not differ by ecomorph for either males (phylogenetic ANOVA: all F5,21 < 1.4, all p > 0.4) or females (phylogenetic ANOVA: all F4,12  0.4). Although the ecomorph concept has been used to explain interspecific variation in a variety of traits among anoles, it is not entirely surprising that variation in display behavior was not predicted by ecomorph. Anolis ecomorph classes are determined by the height and diameter of the perches used most frequently by individuals, factors that have important implications for many aspects of behavior, ecology, and morphology. However, as previously discussed, other habitat features that influence signaling environments, such as light availability (e.g., Leal and Fleishman 2004) or visibility (Johnson et al. 2010), are likely more important than ecomorph class in shaping display diversity among anoles. Thus, many exciting questions on the evolution of social display remain to be investigated, even within a group as well studied as Anolis. In addition to the variation in display traits featured across the genus, another promising avenue for future research lies in investigating potential causes and consequences of intraspecific variation in anoline displays. For example, recent work by Ng et al. (2013) and Driessens et al. (2017) suggest that male and female dewlap morphology differ substantially across the geographic ranges of Anolis distichus and A. sagrei, respectively, likely in response to variation in habitat structure. Yet, how this type of morphological variation is associated with behavioral variation remains unknown, but it is a critical component of understanding the evolution of signaling behaviors in the genus. Sceloporus Lizards in the genus Sceloporus (family Phrynosomatidae) have also been the subject of e­ xtensive study on visual displays. There are more than 90 described species of Sceloporus ­lizards, often referred to as fence or spiny lizards, ranging from southern Canada to as far south as Western Panama (Smith 1946; Bell et al. 2003; Leaché 2010). Sceloporus lizards can occupy ­terrestrial, arboreal, or rocky habitats—some species frequently utilize a particular habitat, while others exhibit variation in habitat use (e.g., Marcellini and Mackey 1970; Davis and Verbeek 1972). Like anoles, Sceloporus are diurnal and insectivorous (Smith 1946), but unlike anoles, which rely exclusively on visual signals, Sceloporus lizards use both visual and olfactory communication. Visual displays are used during competitive and courtship interactions, and are comprised of body movements including push-ups and headbobs that are often accompanied by behavioral ­display of colorful patches located on the ventral surface of the body. Males of most species have a pair of abdominal patches, which are made visible during push-ups or by dorsolateral flattening

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of the body. Some species have lost abdominal patches altogether, while in others, patches have evolved in both sexes (Sites et al. 1992; Wiens et al. 1999). Many species also exhibit colorful throat patches—similar to abdominal patches, they may be present in both sexes, absent in one sex, or sexually dimorphic in color or pattern, and they are also displayed as part of visual communication. Unlike Anolis, in which females often exhibit smaller and less flashy ornamentation, females of some Sceloporus species can exhibit even more striking ventral coloration than males (e.g., Sceloporus pyrocephalus; Weiss 2006; Calisi et al. 2008). While all Sceloporus species exhibit push-ups and headbobs, display patterns can vary considerably across the genus; displays may differ in characteristics such as number of headbobs, number of legs extended during push-ups, and degree of “jaggedness,” a term used to characterize jerky headbob displays (Carpenter 1978; Martins 1993). While prominent differences in display behavior occur between Sceloporus species, there is also evidence of intraspecific, and even intraindividual, variation in display behavior (Martins 1991). Interspecific variation may be influenced by habitat use—for example, headbob and push-up displays differ between some Sceloporus species that use terrestrial or arboreal habitats, but this relationship is not supported when phylogeny is taken into consideration (Martins 1993). In the same study, Martins (1993) hypothesized that species may simply have developed variations in headbob and push-up displays that are suitable to the particular signaling environments in which they occur, contingent upon general trade-offs between effective communication and predation risk, as well as species specific constraints associated with physiology or development. The ventral coloration advertised as part of visual communication also varies within and among Sceloporus species. Ventral patches arise at sexual maturity, and their expression has been ­associated with hormones such as corticosterone, estrogen, and testosterone (e.g., Cox et al. 2005; Calisi and Hews 2007). In many species, abdominal and throat patches are blue and black, but a variety of other colors are observed in various combinations across the genus. Color can change seasonally within individuals and may reflect reproductive status (e.g., Vinegar 1972). Apart from seasonal changes associated with reproduction, ventral coloration can also vary among geographic populations and even members of the same population, an observation that stimulated a large body of research investigating potential mechanisms to explain such variation. In some studies, color variation has been correlated with traits that are associated with fitness, such as body size or parasite load, suggesting that individual variation in color could potentially communicate information about individual quality (e.g., Ressel and Schall 1989; Weiss 2006). However, other studies have failed to find similar associations (e.g., Langkilde and Boronow 2010), and it remains unclear whether color varies in accordance with metrics of individual quality, or whether it is assessed as such in any sort of competitive or courtship context. Aspects of dorsal coloration, including overall body, head, and chin or lip coloration, also vary within and across Sceloporus species, and may function in species recognition and agonistic interactions (Rand 1990; Wiens et al. 1999). Sceloporus lizards also use chemical communication. Different species have been proposed to use chemical cues deposited in feces, as well as compounds found in cloacal or femoral ­secretions (e.g., Duvall et al. 1987; Hews et al. 2011). These lizards may be frequently observed to perform tongueflicking behavior, an indication of attempts to detect such chemical signals deposited ­throughout the environment. Further, simply the visual detection of feces has been ­proposed to elicit tongueflicking behaviors, suggesting that the observation of feces or other secretions may interact with the chemical composition of such substances to communicate information (e.g., Duvall et al. 1987). Thus, strategic deposition of feces and chemical secretions may serve as ­composite signals that function in both visual and olfactory communicative contexts. Podarcis The communication of Podarcis lizards (family Lacertidae), or wall lizards, has also been widely studied. There are 17–18 recognized species of Podarcis, and they are distributed throughout

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Southern Europe and Northern Africa (Harris and Arnold 1999). These lizards are diurnal and largely insectivorous, but some species also exhibit herbivory (Pérez-Mellado and Corti 1993). In their intraspecific communication, Podarcis lizards use chemical cues and visual displays, including both color signals and movements associated with characteristic “foot-shake” displays. Dorsal coloration in Podarcis species is typically cryptic brown or black in adults, but green is also observed on the tails and bodies of adults and juveniles of some species. This coloration can vary throughout development, and dorsal coloration is often sexually dimorphic among adults (Bauwens and Castilla 1998). Dorsal colors can also change during adulthood, potentially reflecting female reproductive status (Galán and Price 2000). Several Podarcis species exhibit color polymorphisms, wherein multiple distinct color morphs exist within the same population. One of the primary differences in Podarcis morphs is the color of their ventral patches, which are commonly red, orange, yellow, or white. The color morphs may be observed in different combinations or frequencies in different species, and in some cases, intermediate morphs are also observed (Pérez i de Lanuza et al. 2013). Sexually mature males typically exhibit colorful throat and belly patches; females also fall into the different morphs, but usually only exhibit throat patches. Researchers have long been interested in the evolution of these polymorphisms, as well as the potential role that color variation among conspecifics might play in ­communication. One hypothesis is that the polymorphism is maintained due to assortative mating, and that individuals may discriminate between mates based on color morph. Some evidence suggests that individuals may select mates of the same morph—in a field study of Podarcis muralis lizards, for example, Pérez i de Lanuza et al. (2013) observed more homomorphic mating pairs than heteromorphic ones, suggesting that individuals may assortatively mate with the same morph. On the other hand, morphs can differ in traits that contribute to fitness, such as reproductive strategy or morphology, prompting the hypothesis that disassortative mating between morphs could also potentially be advantageous. For example, body size and bite force, both of which may confer increased fighting ability, differ among morphs in P. melisellensis (Huyghe et al. 2007, 2009). Further, in P. muralis, females of the different morphs exhibit different reproductive strategies, and female reproductive output also ­varies among mating pairs of different morph combinations (Galeotti et al. 2013). If such traits confer fitness advantages to individuals, individuals may benefit from mating with other morphs. However, whether individuals rely on the color cues alone (or at all) in discriminating between morphs is unclear, given the importance of chemical cues in Podarcis communication. In particular, chemical cues may be more significant than visual cues in Podarcis in the ­context of discriminating between potential mates and competitors (López et al. 2002; but see Font et al. 2012). Chemical cues differ among species, and within species, they differ among age classes and sexes. Within at least one polymorphic species (P. muralis), chemical cues can also differ among some of the color morphs, suggesting that scent marks could also influence discrimination between color morphs, either in combination or separately from color cues (Pellitteri-Rosa et al. 2014). Interestingly, male and female Podarcis react differently to scent marks, suggesting that the sexes may differ in their reliance on chemical cues for sex and species recognition (reviewed in Font et al. 2012). Males behave aggressively when exposed to chemical cues of conspecific males, and perform more tongue flick behaviors toward the scent marks of conspecific females relative to heterospecifics. On the contrary, females do not seem to perform different rates of tongue flicks toward conspecific and heterospecific scents—whether they are unable to discriminate between the chemical cues or rely on different cues for species recognition remains unclear. Several Podarcis species are also known to use “foot-shake” displays, in which the individual raises and rotates one of its legs, for communication in several behavioral contexts. One type of these foot-shake displays is observed when individuals are approached by a predator, suggesting that this display may be used in predator deterrence, either signaling to a potential predator that it has been seen, or possibly with the intent to startle the predator with an unusual stimulus (Van Damme and Quick 2001; Font et al. 2012). Foot shakes are also used by males during intrasexual

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competition, and females have been observed to perform foot-shake displays toward aggressive males, perhaps to signal submission in order to avoid confrontation (López and Martín 2001a, b). Geckos Visual and chemical cues are prevalent in the display behavior of many lizards, but another communication modality is also used by some groups—vocal communication. Geckos (infraorder Gekkota) are the primary group of lizards that make use of all three of these modes of communication, although species vary in their reliance on each of the three modes (Gans and Maderson 1973; Marcellini 1977). Geckos are one of the most speciose groups of lizards, as they compose nearly a quarter of all lizard species, and are distributed across six continents (Pough et al. 2016). Geckos also vary in their active periods—some are diurnal and others nocturnal—making them an ­interesting system in which to investigate the influence of adaptation to these different activity periods on display behavior and multimodal communication. The sensory world of geckos is complex, and they have come to use a variety of different modalities to communicate. Chemical cues present in the skin, feces, and cloacal or femoral secretions function in species and sex recognition in many geckos, and may be assessed during aggressive interactions for information about the quality of a competitor (Briggs 2012; Martín and López 2014). Vocal cues also play an important role in gecko communication. These calls can vary among species, differing in both acoustic structure and behavioral use, and individuals of many species can produce a suite of different calls used in different behavioral contexts. Within species, calls can be sexually dimorphic in structure and behavioral use, and can differ between juveniles and adults (Frankenberg 1982; Frankenberg and Werner 1992). These calls can be used independently of other signals during communication, such as when individuals emit sounds when disturbed or captured, or in combination with other cues during multimodal communication, such as when ­individuals perform postural changes and vocalize during advertisement calls toward mates or conspecific ­competitors (Marcellini 1977; Tang et al. 2001). Unlike many visual cues, chemical and vocal cues are easily transmitted and detected in the dark, and nocturnal species may rely more heavily on these communication modalities as a result. Yet, some geckos—primarily diurnal species—also frequently use visual cues to communicate (Marcellini 1977). Visual cues may include coloration, as some species exhibit vibrant dorsal and coloration and patterning, which are often sexually dimorphic. Color can also vary among conspecifics of the same sex, and such intraspecific variation in color cues may also ­communicate ­information about individual quality during competitive interactions such as territory defense (Ellingson et al. 1995). The most prominent display behaviors in geckos include postural changes, such as repeated arching of the back and lifting of the tail, or raising the body in a full limb e­ xtension posture similar to the push-up displays observed in Anolis and Sceloporus species. Such behaviors are frequently observed during agonistic interactions and courtship displays (Marcellini 1977). Use of visual displays including color, movements, and postures likely differs among diurnal and nocturnal species due to the efficacy of transmitting and detecting such signals in different light conditions. Although some nocturnal species are known to exhibit color variation and utilize some of the previously described visual display behaviors (e.g., use of postural displays by males in very close proximity), both seem to be more elaborate and prevalent within the diurnal species (Marcellini 1977). THE DEVELOPMENT OF LIZARD DISPLAYS The development of behavior has been scarcely studied in lizards, and the few studies that have focused on display development raise several intriguing questions. For example, observations

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of juvenile lizard behavioral displays suggest that juveniles generally behave similarly to adults, using the morphological structures involved in displays in the same general ways. However, this conservation in behavior between juveniles and adults poses an interesting dilemma: display behavior in many adult animals is often used in mating interactions, interactions in which juveniles do not engage because they are not sexually mature. Thus, the meaning of a display may change over ontogeny, even if the display itself is conserved between juveniles and adults. Further, many lizards (e.g., families Scincidae, Teiidae, Lacertidae, and Gymnophthalmidae) also demonstrate developmental changes in coloration, usually of the belly, throat, or tail (Vitt and Cooper 1986). While some of these changes involve the development of conspicuous breeding coloration, others involve the loss of a brightly colored structure as the lizards mature. Why do some organisms invest in the development of a phenotype only to replace it with something different in adulthood? Understanding ­juvenile display behaviors and how they develop into adult displays thus provides a valuable opportunity to study the relationships between juvenile and adult ecology. Below, we discuss the ­development of display behavior and morphologies in several taxa in which juvenile displays have been directly studied: Anolis, Sceloporus, lacertids, and skinks. Development of Motion Displays Because the stereotyped adult display behavior of Anolis lizards is so well understood, they are also an ideal group in which to study the development of displays, and they are one of the taxa in which behavioral development has been most studied. At hatching, the juvenile anole dewlap is barely detectable, but as anoles develop, the structure becomes more pronounced, and more sexually dimorphic, in both size and color. In A. sagrei (the brown anole), dewlap area is non-dimorphic at hatching and becomes dimorphic around 6 months post-hatching (Cox et al. 2015). In contrast, headbobbing, a ritualized and ubiquitous behavior in adult anoles, occurs almost immediately upon hatching; green anole (Anolis carolinensis) hatchlings display headbobbing behavior as early as 30 min after hatching. Juvenile anoles use a simple display repertoire early in life, which d­ evelops into a more complex behavioral display as early as the age of 22 days (Greenberg and Hake 1990). After the initial, simple display behaviors, juvenile A. carolinensis perform a suite of ritualized ­display behaviors, which includes headbobbing and dewlap extension and closely mirrors the ­repertoire seen in adult lizards. Juvenile A. carolinensis direct these displays both at other j­uveniles and at adults. They generally occupy stable territories within the territories of adults (Lovern 2000), and juveniles raised in isolation display at intruders introduced to their habitat (Greenberg and Hake 1990). There are two major differences between adult and juvenile display patterns in Anolis ­carolinensis. First, though the display rates of adult males and females differ dramatically, the display rates for juvenile male and female A. carolinensis are similar. Both male and female juveniles display at the same rate, which is lower than the display rate in both male and female adult lizards, until around 90 days post-hatching (Lovern and Jenssen 2001). Second, as juveniles develop, the amount of time between headbobs tends to decrease (Lovern and Jenssen 2003). Thus, as juveniles grow into adults, there is a fine-tuning of the temporal structure of the display. Though the development of behavioral display has not been studied extensively across Anolis species, detailed field studies of A. aeneus (the bronze anole) suggests that these patterns described for A. carolinensis might generally hold across other anole species. In A. aeneus, male and female juveniles also display at the same rate, and this rate is different than those used by adult males and adult females. Hatchlings also display the same repertoire of behavior as adults, though their frequencies of aggressive and courtship displays is quite different; juveniles display aggressively more often than male or female adult lizards (Stamps 1978). Juveniles in this species are highly territorial, and territorial “residents” who defend a valuable area from intruders are less vulnerable to ­predation (Stamps 1983a). Further, display rate increases when certain predators are added to

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a juvenile enclosure, though this may be a response to the predator itself instead of an increase in ­territory defense behavior (Stamps 1983b). The development of headbob displays in Sceloporus undulatus (the eastern fence lizard) ­follows a similar pattern to the development of anole displays (Rocgenbuck 1986). In brief, while many ­hatchlings display on the day of birth, all hatchlings display after the first 2 days of life. The ­repertoire of display behaviors is identical to that seen in adults, though the amplitude and number of head bobs is lower in juveniles. As in anoles, there is no sexual dimorphism in headbob number or duration in juvenile S. undulatus. As lizards mature, the number of headbobs during a display increases and the display duration and pattern change to the most stereotyped adult display ­behavior patterns. Study of juvenile behavioral mechanism has suggested that behavioral variation is regulated by exposure to differential levels of testosterone during development. Testosterone is detectable in Anolis carolinensis egg yolks and, across juvenile development, concentrations of circulating testosterone in males become significantly higher than those in females between 30 and 90 days post-hatching (Lovern et al. 2001), the same period during which sex-specific patterns of display begin to emerge (Lovern et al. 2001). Juveniles with supplemented testosterone demonstrate higher display rates in both sexes (Lovern et al. 2001), concurrent with the multitude of studies demonstrating behavioral changes in adult anoles after testosterone supplementation. These data suggest that testosterone likely mediates differences in both inter-age and intersex display rates. Development of Color Displays A striking, and relatively well understood, example of the development of color-based displays can be found in the vibrant blue coloration of tails in juveniles of some skink and lacertid species. In three species of Eumeces skinks and the lacertid Acanthodactylus beershebensis (the fringefingered lizard), hatchlings have a patterned body coloration paired with a strikingly bright blue tail. However, as post-hatching development progresses, these colors fade, leaving adults with a dramatically different and much duller tail color and body pattern. In Eumeces, coloration begins to fade after about 10 days after hatching (Hawlena et al. 2006). In A. beershebensis, color is ­maintained until about 21 months of age, the time at which most juveniles have lost this coloration (Vitt and Cooper 1986). Despite the differences in developmental timing, both groups demonstrate a striking morphology that is replaced as the lizards mature. This dramatic developmental change has been hypothesized to decrease predation risk as juveniles occupy niches left open by adults. Juveniles forage in more open, exposed habitats than adults, presumably to avoid competition with adults (Hawlena et al. 2006). This exposes the juveniles to greater predation risk and it has been hypothesized that the colorful tails, when autotomized, are particularly effective at deflecting predatory attacks. Vitt and Cooper (1986) have demonstrated that there is no cost associated with tail loss in juvenile Eumeces under 1 year old (and that tail loss may even encourage growth). Color changes across development are not unique to lizard tails. In Urosaurus ornatus (the ornate tree lizard), yellow chins in juveniles become orange in adults. In addition, throat and belly color appears in males and females within 15 days of hatching (Carpenter 1995). Though belly color begins and persists as blue, throat color always starts as pale orange and changes over time, though this development is variable by sex. Female U. ornatus typically maintain orange throat coloration into adulthood, but some female throats turn yellow. Males who ultimately have a blue throat (i.e., most wild lizards; color can be variable in captivity) transition from orange to (yellow) green, blue-green, and blue. It can take up to 6 months for throat color to change (Carpenter 1995). Further, throat color affects social relationships, as it is important for sex recognition, courtship rejection, and territorial interactions. Males are typically attracted to orange-throated females and will ­tolerate juveniles with orange in their territories (Carpenter 1995).

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In contrast, in Sceloporus and anoles, the ontogeny of display colors follows simpler patterns. In Sceloporus, male subadults (i.e., those in their second breeding, or activity, season) always have the same display colors as adults, and this color, once developed, stays constant throughout ontogeny. In Sceloporus, throat color appears on most males by late June of their second activity season. They then begin breeding in their third year of activity (at approximately 21 months of age; Rand 1990). In Anolis sagrei, brightness of the dewlap is sexually dimorphic, showing a decrease across male dewlap development until, after 9 months of post-hatching growth, male dewlaps are less bright than females (Cox et al. 2015). In A. cuvieri, the Puerto Rican giant anole, hatchling dewlaps are tan with dark streaks, and as development progresses, dewlap color changes gradually to a clear yellow, reaching its terminal color around the time of sexual maturity (Rand and Andrews 1975). These changes in dewlap color do not match ontogenetic changes in body color also observed in this species: the adult body coloration in A. cuvieri develops well before adult dewlap coloration (Rand and Andrews 1975). Current Status of Display Development Together, these data suggest that juvenile display behavior differs from that of adults in three important ways: (1) Juvenile displays generally represent the full repertoire of adult behaviors; ­however, ritualization of the behavioral complex is fine-tuned as juveniles become sexually mature. (2) Juveniles generally display less than adults, though the sexes display at the same rate until sexual maturity. (3) Some juvenile displays may serve an adaptive function in juveniles that becomes less relevant as they mature. Despite a few well-studied cases, display development from hatching to adult is understudied. We still know very little about the mechanisms underlying the phenotypic changes discussed above, while we know even less about the functional roles juvenile phenotypes play as the lizards develop. The patterns described here suggest that there are many interesting ecological, physiological, and evolutionary dynamics interacting across ontogeny, and continued study of the development of displays will yield a more comprehensive understanding of these systems. CONCLUSIONS AND FUTURE DIRECTIONS In this chapter, we review studies of the evolution and ontogeny of lizard displays that reveal dramatic variation in the behaviors and morphological structures with which lizards communicate, and demonstrate the importance of the phylogenetic patterns and ecological opportunities that influence this diversity. Yet despite the abundance of information available on lizard displays (in this chapter, we report descriptions of the displays of 199 genera; Appendix 1), there remain many taxa for which the behaviors involved in communication are not well understood. Although our literature search was not exhaustive, it was comprehensive, and we were unable to find descriptions of displays for 254 lizard genera, many of which primarily occur in Africa and Asia. There is also little known about how fossorial species interact, undoubtedly because their behaviors are difficult to observe, but there may be interesting patterns of behavior in these groups as well. More broadly, studies of natural history, including basic behavior studies, remain critical. Without these data for more groups across lizards, deeper phylogenetic studies and/or interpretations will remain limited. Further, in our search of the literature, we discovered that many of the available descriptions of lizard display are relatively difficult to access. Many of the relevant descriptions of behavior were published only in masters theses, or doctoral dissertations, or in the anecdotal natural history notes of taxonomic descriptions of new species. Further, for some groups, display behaviors have been observed and published in the primary literature, but described only in broad categories

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(i.e., “courtship displays” or “aggressive behaviors”) that render specific comparisons among groups difficult, and so we were unable to include some of those taxa in this study. Thus, we strongly encourage all herpetologists who study behavior to provide detailed descriptions of these behaviors in easily accessible publications. One observation that has emerged from our analysis of lizard communication is that despite the importance of considering what lizards themselves can perceive, and the extent to which the components of display are effective in differing environments, these issues are directly addressed by relatively few behavioral research teams. This information could contribute new perspectives on how and why particular displays have evolved in different lineages, and is important for three reasons. First, the traits that human biologists identify for study may be quite different than those detected by the lizard sensory systems. For example, Anolis dewlaps vary widely in color, which is commonly reported, but many dewlaps also reflect UV, which humans cannot see but lizards can (Fleishman et al. 1993; Kawamura and Yokoyama 1998). In fact, UV reflectance may be the dewlap trait that communicates information of primary importance to anoles. What other traits might we miss, due to the limits of our own perception? Next, traits that appear striking to biologists may not be directly involved in lizard communication. For example, while Podarcis lizards are remarkably colorful, it is not clear whether those colors play an important role in communication in these ­species or whether chemical cues are more significant (López and Martín 2001b; López et al. 2002). Finally, traits that biologists can readily measure may not be detected by lizards. While we can m ­ easure small differences in the size or color of a structure used in display, a lizard observing another lizard’s display may not be able to detect those differences (Fleishman et al. 2017). In g­ eneral, are the signals that we believe to function in a particular context actually interpreted in those contexts by other lizards? These questions offer many opportunities for further empirical study, even among well-studied taxa. In addition, the focus of most biological studies on adult males extends to the field of lizard communication as well, and most of the published reports of lizard displays describe adult male behaviors. Although male displays are often more frequent and flashier than those of females and juveniles, there are likely interesting patterns in these groups that are missed due to the relative lack of study, especially in comparative analyses examining the evolution of female or ­juvenile behavior. For example, the data on Anolis lizards presented here demonstrate that female displays may not be just less frequent versions of male displays, as the rates of display between the sexes were not correlated. Females may be displaying for different reasons than males, or may communicate different information in their displays. Further, female displays may not be solely the result of between-sex genetic correlation with males, as has been hypothesized, but there may be unique selective pressures that produce or maintain displays in females. In parallel, juvenile displays may be the result of selection during development, and not just a simpler version of adult displays. In sum, there remains much to investigate in the evolution of lizard displays. Variation in the color, motion, sound, timing, and complexity of displays, across ontogeny and among social contexts, provides a rich sensory world for lizards and a fascinating system for the study of behavioral evolution. ACKNOWLEDGMENTS The authors thank Daisy Horr for her work to review the scientific literature on lizard d­ isplay. They also thank Manuel Leal, Rebecca Hazen, and Brittney Ivanov for critical discussions of the ideas in this chapter. Michele A. Johnson was supported by NSF IOS 1257021, and Bonnie K. Kircher was supported by an NSF Graduate Research Fellowship.

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APPENDIX 1:   DESCRIPTIONS OF LIZARD DISPLAY This appendix provides the descriptions of display data for each lizard genus, compiled from a search of the primary scientific literature. Motion displays components were categorized as types of postural changes, head movements, mouth displays, gular displays, limb movements, and tail movements. An “x” in a cell indicates that at least one species in that genus has been reported to use a given posture or motion in its display. Color displays were categorized by the body location of the color involved in display, with each color reported to be involved in at least one species in that genus listed. Next, we indicated (with an “x”) if any species in a genus was reported to use ­vocalization displays. References include all sources consulted for these display descriptions (EOL indicates Encyclopedia of Life, eol.org, and ADW indicates Animal Diversity Web, animaldiversity. org, both accessed in February 2017). If we found no information on visual or vocal displays in a genus, the cells associated with that genus were left blank. This appendix is available online at: http://digitalcommons.trinity.edu/bio_faculty/63/.

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Revell, L.J. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223. Rocgenbuck, E. 1986. The ontogeny of display behaviour in Sceloporus undulatus. Ethology 71:153–165. Sánchez-Hernández, P., M.P. Ramírez-Pinilla, and M. Molina-Borja. 2012. Agonistic and courtship behaviour patterns in the skink Chalcides viridanus (Fam. Scincidae) from Tenerife. Acta Ethologica 15:65–71. Shine, R. 1990. Function and evolution of the frill of the frillneck lizard, Chlamydosaurus kingii (Sauria: Agamidae). Biological Journal of the Linnean Society 40:11–20. Simon, C.A. 1983. A review of lizard chemoreception. In Lizard Ecology: Studies of a Model Organism, ed. R.B. Huey, E.R. Pianka, and T.W. Schoener, 119–133. Cambridge: Harvard University Press. Sites, J.W., J.W. Archie, C.J. Cole, and O. Flores Villela. 1992. A review of the phylogenetic hypotheses for ­lizards of the genus Sceloporus (Phrynosomatidae): Implications for ecological and evolutionary ­studies. Bulletin of the American Museum of Natural History 213:1–110. Smith, H.M. 1946. Handbook of Lizards: Lizards of the United States and Canada. Ithaca, NY: Comstock Publishing. Smyth, M. and M.J. Smith. 1974. Aspects of the natural history of three Australian skinks, Morethia ­boulengeri, Menetia greyii and Lerista bougainvillii. Journal of Herpetology 8:329–335. Stamps, J.A. 1977. Social behavior and spacing patterns in lizards. In Biology of the Reptilia, Volume 7. Ecology and Behaviour A, ed. C. Gans and D.W. Tinkle, 265–334. Cambridge: Academic Press. Stamps, J.A. 1978. A field study of the ontogeny of social behavior in the lizard Anolis aeneus. Behaviour 66:1–31. Stamps, J.A. 1983a. The relationship between ontogenetic habitat shifts, competition and predator avoidance in a juvenile lizard (Anolis aeneus). Behavioral Ecology and Sociobiology 12:19–33. Stamps, J. 1983b. Territoriality and the defense of predator refuges in juvenile lizards. Animal Behaviour 31:857–870. Stanley, E.L., A.M. Bauer, T.R. Jackman, W.R. Branch, and P. le FN Mouton. 2011. Between a rock and a hard polytomy: Rapid radiation in the rupicolous girdled lizards (Squamata: Cordylidae). Molecular Phylogenetics and Evolution 58:53–70. Stapley, J. 2008. Female mountain log skinks are more likely to mate with males that court more, not males that are dominant. Animal Behaviour 75:529–538. Stuart-Fox, D., A. Moussalli, and M.J. Whiting. 2007. Natural selection on social signals: Signal efficacy and the evolution of chameleon display coloration. The American Naturalist 170:916–930. Tang, Y.Z., L.Z. Zhuang, Z.W. Wang, and J.D. McEachran. 2001. Advertisement calls and their relation to reproductive cycles in Gekko gecko (Reptilia, Lacertilia). Copeia 2001:248–253. Teixeira, M., R.S. Recoder, A. Camacho, M.A. de Sena, C.A. Navas, and M.T. Rodrigues. 2013. A new species of Bachia Gray, 1845 (Squamata: Gymnophthalmidae) from the Eastern Brazilian Cerrado, and data on its ecology, physiology and behavior. Zootaxa 3616:173–189. Tokarz, R.R. 1995. Importance of androgens in male territorial acquisition in the lizard Anolis sagrei: An experimental test. Animal Behaviour 49:661–669. Tollestrup, K. 1983. The social behavior of two species of closely related leopard lizards, Gambelia silus and Gambelia wislizenii. Zeitschrift für Tierpsycholgie 62:307–320. Torr, G.A. and R. Shine. 1994. An ethogram for the small scincid lizard Lampropholis guichenoti. AmphibiaReptilia 15:21–34. Trivers, R.L. 1976. Sexual selection and resource-accruing abilities in Anolis garmani. Evolution 30:253–269. Van Damme, R. and K. Quick. 2001. Use of predator chemical cues by three species of lacertid lizards (Lacerta bedriagae, Podarcis tiliguerta, and Podarcis sicula). Journal of Herpetology 35:27–36. Vinegar, M.B. 1972. The function of breeding coloration in the lizard, Sceloporus virgatus. Copeia 1972:660–664. Vitt, L.J. 1982. Sexual dimorphism and reproduction in the microteiid lizard, Gymnophthalmus multiscutatus. Journal of Herpetology 16:325–329. Vitt, L.J. and W.E. Cooper, Jr. 1986. Tail loss, tail color, and predator escape in Eumeces (Lacertilia: Scincidae): Age-specific differences in costs and benefits. Canadian Journal of Zoology 64:583–592. Vitt, L.J. and T.E. Lacher, Jr. 1981. Behavior, habitat, diet, and reproduction of the iguanid lizard Polychrus acutirostris in the Caatinga of northeastern Brazil. Herpetologica 37:53–63. Watkins, G.G. 1998. Function of a secondary sexual ornament: The crest in the South American iguanian lizard Microlophus occipitalis (Peters, Tropiduridae). Herpetologica 54:161–169.

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Chapter  9

Behavioral Ecology of Aggressive Behavior in Lizards Martin J. Whiting Macquarie University

Donald B. Miles Ohio University

CONTENTS Introduction.....................................................................................................................................290 Part I: Aggression and Behavior.....................................................................................................290 Descriptions of Aggressive Behavior and Signaling....................................................................... 291 Patterns of Aggressive Behavior..................................................................................................... 292 Consistent Individual Variation in Aggression........................................................................... 292 Lateralization and Aggression.................................................................................................... 293 Aggression and Social Learning................................................................................................ 293 Part II: Development and Mechanisms Underlying Aggressive Behavior...................................... 294 Age-Specific Aggression and the Development of Aggression through Life............................ 294 Physiological Costs of Aggression: The Role of Testosterone.................................................. 295 Part III: The Evolutionary Function of Aggression........................................................................ 295 Natural Selection........................................................................................................................ 295 Female Aggression in Association with Access to Food and Resources............................... 295 Nonadaptive Reasons for Female Aggression....................................................................... 296 Aggression and Competition over Ecological Resources in Males...................................... 296 Sexual Selection......................................................................................................................... 297 Male Aggression and Territorial Behavior............................................................................ 297 Does Female Aggression Play a Role in Sexual Selection?.................................................. 298 Aggression and Alternative Mating Strategies......................................................................300 Aggression within Genetic and Developmentally Determined AMSs.................................. 301 Condition-Dependent AMSs.................................................................................................302 Aggression without Territoriality—Mate Guarding..............................................................304 Aggression and Fitness..........................................................................................................304 Social Selection.......................................................................................................................... 305 Maternal Aggression and the Potential Benefits to Offspring............................................... 305 Patterns of Social Organization in Lizards—Dominance Hierarchies, Hotshots, and Despots..................................................................................................................................306

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Dominance Hierarchies.........................................................................................................306 Leks and Hotshots.................................................................................................................307 Despotic Social Systems.......................................................................................................307 Part IV: Consequences of Aggression for the Evolutionary and Ecological Trajectory of Populations......................................................................................................................................308 Aggression, Color Morphs, and Trophic Polymorphisms..........................................................308 Alternative Mating Strategies and Demographic Stochasticity.................................................309 Alteration of Intrasexual and Intersexual Aggression by Anthropogenic Effects...................... 310 Intersexual Aggression May Affect Reproductive Success and Lead to Population Collapse................................................................................................................................ 310 Future Directions and Lizards as a Model System for Studies of Aggression................................ 311 References....................................................................................................................................... 311

INTRODUCTION Aggression in lizards has been a central focus of a wide range of studies because so many s­ pecies experience intense sexual selection and/or competition over limited resources. Furthermore, many lizards are brightly colored, defend territories in open spaces where they are easy to observe, and allow close approach, making them particularly amenable to study (Fox et al. 2003). Aggressive behavior has been studied in the context of endocrine and physiological control (Chapter 6), signaling (Chapters 3 and 7), rival recognition, access to resources and mates by both sexes, and with respect to social systems (Chapter 10). This chapter reviews the behavioral ecology of aggression at the individual, population, and species levels, and identifies areas where lizards could be a suitable model system for addressing the influence of aggression on fitness more broadly. Our chapter has four key goals. First, we describe aggression, patterns of aggressive behavior in lizards, and how studies of lizards have contributed to animal behavior theory more broadly. Second, we briefly explain the mechanisms that underlie aggression and the emergence of aggression during development. Third, we review the evolutionary function of aggression in different contexts, including natural selection (e.g., survival, acquisition of resources), sexual selection (e.g., competition for mates) and social selection (e.g., kin effects). Finally, we discuss the potential implications of aggression for the ecological and evolutionary trajectory of populations. PART I: AGGRESSION AND BEHAVIOR Aggression hardly needs a definition because it is so ubiquitous and pervades so much of animal and human social behavior. For the purposes of this chapter, aggression is any negative behavior that is directed at one or more individuals that imposes a cost to that individual, either in the short-term (e.g., increased stress) or the long-term (e.g., reduced fitness). Aggressive behavior is a double-edged sword, because while the outcome may be favorable if it results in an animal securing a territory, or keeping a rival from a mate (mate guarding) or a resource, there is a physiological cost to being aggressive (Chapter 10). From a behavioral standpoint, aggression is particularly interesting because it may be exaggerated to bluff a rival or deter a predator and may not be an honest signal (Chapters 3 and 7). In the case of aggressive behavior directed at a predator, species with deimatic displays may use aggression to amplify the effect of a startle display (Umbers et al. 2017). For example, Bluetongue lizards (Tiliqua spp.) use aggressive defensive behavior when they expose their UV-blue tongues at predators (Badiane et al. 2018). The interaction of a startle display and aggression, whereby the display is amplified by an aggressive behavioral response, is particularly

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important in these species. Empirical evidence for deimatic displays is starting to accumulate in light of recent theoretical developments (Umbers et al. 2017) and lizards show great promise as a model system.

DESCRIPTIONS OF AGGRESSIVE BEHAVIOR AND SIGNALING In lizards, aggression is indicated either directly using static and/or dynamic visual signals (Whiting et al. 2003) or indirectly through chemical signals (López and Martín 2002; Carazo et al. 2007, 2008) (Chapter 7). In many species, both visual and chemical signals are used together (Lopez et al. 2003; Whiting et al. 2009) and in the context of aggression, it is likely that visual and chemical signals reinforce the same message (Martin and Lopez 2010; Whiting et al. 2009). For example, chemical scent may be deposited on a substrate and signal territory ownership (Carazo et al. 2007, 2008), or it may be used in close encounters with rivals (Whiting et al. 2009). Conversely, whereas visual signals are also used in close encounters, they are typically effective at a greater distance than chemical scents (Whiting et al. 2009). Many species that experience strong sexual selection signal aggression through colorful displays while also conveying information about fighting ability through femoral gland secretions. Consequently, lizards are a particularly useful model system for studying multimodal signaling. Aggressive displays have been described for a wide range of species, beginning with Charles Carpenter’s seminal work on North American lizards (Carpenter 1977). Many species typically use a graded aggressive response when confronted by a conspecific rival. In this scenario, the level of aggressive response increases in direct proportion to the level of threat, assuming that both rivals are signaling honestly to one another (Whiting et al. 2003). Under particular circumstances, lizards will respond with an aggressive chase without any signal. This is the case in the Augrabies Flat Lizard (Platysaurus broadleyi) when males see rivals at the last moment, when they are at relatively short distances from one another and/or on or close to a resident’s territory. In these scenarios, a threat is immediately of high intensity. However, if they make visual contact at a distance and a rival is away from the boundary of its territory, they will first signal to a rival. Because aggression is costly in terms of energy expended and potential for injury, males typically signal their status to avoid fights with a predictable outcome, such as when two males have a pronounced asymmetry in status. When males are closer in size or dominance, or if they are contesting a high value resource, they are more likely to respond aggressively and fight. For most lizards, visual displays are followed by physical chases and biting if rival males fail to cede to their opponents in a contest. Lizards may have multiple armaments, such as throat color and belly patches, and these may convey different information (e.g., fighting ability and male quality)( Møller and Pomiankowski 1993) or they may serve to reinforce the same message (i.e., redundancy) (Rand and Williams 1970). The type of display used by males also may vary according to social context (Whiting et al. 2003). Classic signals of aggressive behavior include inflating the body; exposing color patches (e.g. on ventrum); inflation of the throat; tail-flicking, waving, or curling; hand-waving; head-bobbing; standing upright and presenting the body laterally/back arching; gaping; and changing color (illustrated by Carpenter (1977). The Marine Iguana (Amblyrhynchus cristatus) engages in an unusual contest behavior involving male head-butting or shoving (Carpenter 1966a) reminiscent of ungulate contests. Males may also convey information on dominance or fighting ability using static traits such as body size (Tokarz 1985; Rodda 1992; Alberts et al. 2002), tail length (Carpenter 1967; Cooper 2001), elongated dorsal spines (Baird et al. 2012), frills (Shine 1990), extensible dewlaps (Nicholson et al. 2007), variation in head shape (Lappin et al. 2006), and color of dewlaps, throat fans, and frills. For many species, variation in color among males in a population indicates fighting ability or aggressive behavior (Molnár et al. 2016). Agonistic displays may also involve a simple

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display such as a male taking a conspicuous position on an exposed or elevated perch (such as in the South Indian Rock Agama [Psammophilus dorsalis]) (Radder et al. 2006a, b). PATTERNS OF AGGRESSIVE BEHAVIOR Consistent Individual Variation in Aggression A key question in behavioral ecology is how stable aggressive behavior is, and whether it represents a personality trait or if it is plastic or condition dependent. Studies of consistent individual variation in animals address whether a trait is consistent within individuals and across contexts while being variable among individuals (i.e., personality or behavioral type) (Bergmüller 2010). Of additional interest is whether the rank order of among-individual variation is consistent across contexts and when the environment changes. While there is great interest in, and evidence for, consistent individual variation in behavioral traits (Sih et al. 2004), behavior is also influenced by state, sex, and life history stage. In the case of aggression, reproductive state clearly influences aggression in both males and females. Nevertheless, some individuals are consistently more aggressive than others, even if there is temporal variation in their level of aggressiveness. Therefore, plasticity in behavior may in fact be constrained (Bergmüller 2010; Dingemanse et al. 2010). In the case of lizards, it is useful to ask whether aggression is a personality trait and if there are ramifications for any associated constraints. Aggression is rarely measured as a personality trait in lizards—it is more common to measure boldness. Indeed, aggression and boldness are often correlated. Nevertheless, aggression has been assayed as a measure of consistent individual variation in a handful of lizard species. In the case of the family-living White’s Rock Skink (Liopholis whitii), aggression was the most repeatable of five behavioral traits (aggression, boldness, exploration, sociability, activity) across two assays, and for both males and females (McEvoy et al. 2015). Aggression was measured by touching the lizard’s snout up to ten times with a plasticine lizard model attached to a stick. Lizards responded with a range of behaviors from taking refuge to back arching, open-mouthed displays, and biting the model. While aggression was repeatable across the two assays, it did not correlate with any of the other behavioral traits measured (either within or between individual covariance) (McEvoy et al. 2015). Interestingly, in a related study in the same species, the authors assayed aggression in the field and during staged contests in the laboratory. Aggression was once again repeatable in the field study, but in the laboratory study, only winners showed consistency in aggressive behavior, whereas losers did not (McEvoy et al. 2012). Aggression was also assayed in another family-living lizard, the Tree-crevice Skink (Egernia striolata). Captive-born offspring were raised either alone or in a pair, and their behavior was assayed four times over a year. Within pairs, a dominant–subordinate relationship formed and subordinates became more aggressive over time, whereas dominant and solitary individuals were consistent in their aggressive responses (Riley et al. 2017). In the monogamous Sleepy Lizard (Tiliqua rugosa), more aggressive males spent less time with their female partners, whereas less aggressive males were more strongly connected to their female partners in a social network, and more often in contact with them. This consistency in behavioral traits across contexts has been suggested to represent a behavioral syndrome in which “lovers” have stronger bonds with female partners than “fighters,” which are more aggressive and have weaker bonds with their female partners (Godfrey et al. 2012). Lizards are an excellent system for answering questions about consistent individual variation because they are easily assayed for aggressive responses either in the field or in the laboratory. Preliminary results, such as those described above, suggest that individuals may have only

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limited flexibility in their levels of aggression. Data on more species will help establish whether this is a general finding. Finally, lizard species that show marked variation in personality offer an ­opportunity for studying the long-term effects of aggression and how it influences survival and reproductive success. Lateralization and Aggression Lateralization of the brain is well known in vertebrates and may be adaptive if it allows complementary behavior simultaneously, such as foraging while remaining vigilant for predators (Rogers 2000). The posterolateral placement of a lizard’s eyes means that if a stimulus is presented directly anteriorly, they respond by turning the head to one side. This allows for field testing of lateralization in different contexts, such as aggression (Hews et al. 2004). Animals can also be tested for lateralization by covering individual eyes and testing responses in a similar way (Deckel 1995). Aggression has been demonstrated to have a left-eye bias in a wide array of vertebrates, including fishes, frogs, lizards, and mammals (Bisazza et al. 1998; Vallortigara 2000). In such cases, conspecific aggression elicits a stronger response when viewed from the left-visual field. Based on a study of seven individuals of the Green Anole (Anolis carolinensis) and three of the Brown Anole (Anolis sagrei) left eye preference was demonstrated for aggressive interactions in eight males and two females (Deckel 1995). In a follow-up study, 10 male A. carolinensis had either their left or right eyes covered, while 15 males did not. Both groups were involved in staged encounters and aggressive responses were more intense for the left side, although left eye aggression steadily increased with time in the case of the unmanipulated (15) lizards. Furthermore, assertion behavior was more heavily influenced by the left eye/right hemisphere (Deckel and Jevitts 1997). The Tree Lizard (Urosaurus ornatus) also uses a range of agonistic displays and has lateralized aggression, favoring the left visual field/right hemisphere (Hews and Worthington 2001). Not only males exhibit a ­left-eye bias during ­aggressive encounters: females of the Striped Plateau Lizard (Sceloporus ­virgatus) favor their left visual field when aggressively rejecting courting males once no longer receptive (Hews et al. 2004). The influence of lateralization on aggression in lizards is, however, greatly understudied, and has the potential to contribute to our general understanding of lateralization more broadly. Aggression and Social Learning Animals use social information to solve problems more quickly or to acquire key information about mates or resources in their environment, such as the location of a food source or suitable habitat patch (Cote et al. 2008; Cote and Clobert 2007; Clobert et al. 2009). Three species of lizard have thus far been tested for their social learning ability in an association task. The family-living Tree-crevice Skink (Egernia striolata) uses social information to short-cut individual learning (Whiting et al. 2018), whereas adults of the Eastern Bearded Dragon (Pogona barbata) use imitation of conspecifics (Kis et al. 2014). In the Eastern Water Skink (Eulamprus quoyii), young, but not old, males use social information to solve tasks (Noble et al. 2014). Given that adult male E. quoyii did not use social information, this raised the possibility that lizards may differentially use social information according to the relative dominance status of any two individuals. To test this hypothesis, contests were first staged between males in order to establish dominant–subordinate relationships between known individuals. Then, social learning tests were conducted in which one male in a pair was a demonstrator and either dominant or subordinate to the naïve learner. Surprisingly, control lizards learnt to solve the task as quickly as social learners, indicating that relative dominance had no influence on learning ability (Kar et al. 2017). The potential role of aggression and relative dominance in lizards is still an open question and deserving of attention.

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PART II: DEVELOPMENT AND MECHANISMS UNDERLYING AGGRESSIVE BEHAVIOR Age-Specific Aggression and the Development of Aggression through Life It is well known that aggression is risky because it also serves to promote confrontation in which a “superior” rival will make the signaler pay the price if their fighting ability is lower than that of the receiver (Johnstone 1997). In birds, for example, there is social enforcement of dominance whereby aggressive behavior is constantly challenged and honest signaling is behaviorally enforced (Rohwer 1982). We are not aware of any example of social control of status signaling in lizards (reviewed by Whiting et al. 2003), but it is certainly plausible. If aggressive behavior is risky in part because it may attract attention from rivals, then the development or ontogeny of aggression, and the timing of its expression, is crucial. To this end, juveniles of many species begin to express some aggressive behavior toward other juveniles at an early age, although, with some exceptions, this dimension of behavioral development is particularly unstudied (Ruby and Baird 1993; Ballen et al. 2014; Stamps 1977b, Stamps 1978, Stamps and Krishnan 1994a, b, 1995, 1998; Fox et al. 1981). Much of what we know about juvenile lizard behavior and aggression is derived from a single study system, Anolis aeneus (the Bronze Anole). Judy Stamps conducted field studies and a series of important experiments (along with V.V. Krishnan) on this species to establish the ontogeny of territorial and aggressive behavior and the factors that determine social dominance during early life experiences. Because anoles use head-bobs to display, it is a straightforward task to measure display rates as an indicator of aggression, and it is also abundantly clear which individual in a dyad initiated an aggressive interaction. In an early study of ontogeny, Stamps (1978) found surprisingly high levels of aggression among juvenile A. aeneus, the intensity of which was dependent upon the size ratio between the juvenile resident and a tethered intruder. For A. aeneus, there is a clear ontogeny of display behavior and aggression. Juveniles, adult females, and adult males all have a similar repertoire of displays but use specific display types at different frequencies. What is perhaps most interesting about the results of Stamps’ (1978) continuous study of juvenile behavior (i.e., ontogeny) in the field, is that juveniles begin with a large repertoire of displays and use particular displays less frequently as they develop. This is in contrast to the hypothesis that juvenile animals begin with limited display and social behavior repertoires, with these becoming more complex during the course of development. (This is more likely to be the case in animals that exhibit parental care.) In other words, adults of A. aeneus can be viewed as animals that have lost several of the displays they employed as juveniles. Stamps (1978) reported that “juvenile social systems are at least as complex and variable as are those of adults.” In terms of ontogeny, juvenile males use fewer “fearful” displays as they mature, and females use fewer aggressive displays. The displays that juveniles use remain stereotyped in adults, with some exceptions—signature bobs are slightly shorter in juveniles. Also, some displays are more variable among juveniles, and the displays of juveniles morph into two forms: a courtship bob and a multibob. Importantly, aggression appears to be as critical for juveniles as it is for adults. Ontogeny of aggressive display has also been reported for A. carolinensis (Lovern and Jenssen 2001), in which juveniles give aggressive displays only during social interactions (i.e., they do not use broadcast signals). Juvenile males and females exhibit similar displays until they become “large,” at which point males display at a higher rate, although these displays remain qualitatively most similar to those of adult females (Lovern and Jenssen 2001). Anolis aeneus is notable for the importance of aggression during the juvenile stage and the stereotypy of many of its displays, and this may be so for other lizard species. In the Algerian Sand Lizard (Psammodromus algirus), more aggressive juvenile males secure larger home ranges, with more vegetative cover, and have higher short-term survival than do less aggressive ones (Civantos 2000). Early experience is potentially important for later social development, and aggression is a key component that drives social interactions (Ballen et al. 2014). For example, juveniles of the

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Veiled Chameleon (Chamaeleo calyptratus) raised in isolation as opposed to being part of a group exhibited more subordinate behaviors than those raised in a group, although their overall levels of aggression were similar (Ballen et al. 2014). It is thought that defense of food is not, in fact, the primary reason for juvenile aggression (Stamps 1978). A more likely explanation is that aggressive interactions are important for future success and the acquisition of territories once juveniles reach adulthood. This could be the case if juveniles repeatedly challenge and dominate subordinates, making it less likely that the latter will attempt to secure space or resources in a particular area in the future (Stamps 1978). Physiological Costs of Aggression: The Role of Testosterone Lizards constitute a model system for understanding the influence of testosterone on aggression and social behavior and many studies have experimentally manipulated testosterone in free-living and captive lizards (Hews et al. 1994; Moore 1988b; Moore and Thompson 1990; Thompson et al. 1993; Weiss et al. 2002; Woodley and Moore 1999b; Stamps 1994; Sinervo et al. 2000; Fox 1983b). With higher levels of testosterone, males become more aggressive (Marler and Moore 1989; Fox 1983a; Moore 1988a; Moore 1986) and, in many species, more conspicuous (Marler and Moore 1988). They may also benefit from enhanced physiological performance (Sinervo et al. 2000) and acquire larger and/or superior home ranges (Fox 1983b; Sinervo et al. 2000). If aggression is accompanied by increased levels of testosterone, however, this may elevate metabolic rate and even compromise the immune system (Folstad and Karter 1992), although this is not always clear-cut (Roberts et al. 2004). Other costs associated with increased levels of testosterone and greater levels of aggression include reduced survival (Marler and Moore 1988), injury and a loss of social status in species for which tails signal status (Fox and Rostker 1982). Testosterone impacts a suite of traits that are all thought to bear on survival and fitness (Cox et al. 2009). Aggression can therefore be thought of as representing a physiological trade-off that may impact on life history and ultimately, fitness attributes (Sinervo and Svensson 1998). PART III: THE EVOLUTIONARY FUNCTION OF AGGRESSION Natural Selection Female Aggression in Association with Access to Food and Resources Compared to males, females of many lizard species frequently have similar, albeit reduced, traits, such as color patches. The function of such traits includes sex recognition, the stimulation of male courtship, the deterring of courting males when females are no longer receptive, and impacting intra-sexual competition for resources or mates (Baird 2004). Female aggression and territoriality, although typically less pronounced than in males, is still relatively common (Stamps 1977b). Aggression may manifest itself in territory defense or as a component of the structuring of a social hierarchy. To this end, female aggression has most commonly been documented in iguanids, but is encountered in many lizard families (Stamps 1977b). Whereas coloration or some phenotypic trait may be the attribute that signals female aggression or dominance, aggressive display behavior can serve the same function. Females of the Collared Lizard (Crotaphytus collaris) may be more aggressive and more likely to defend a territory in habitats that have fewer vantage points that are important for foraging (Baird and Sloan 2003). Competition for food also drives aggressive defense of territories by females of Anolis aeneus, which defend territories throughout the year (Stamps 1977a, 1978). Access to limited portions of habitat and, potentially, limited numbers of nesting sites, is likely to result in higher levels of female aggression. For example, females of the Common Green

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Iguana (Iguana iguana) and the Marine Iguana (Amblyrhynchus cristatus) will aggressively compete for limited burrows and nest sites (reviewed by Stamps 1977b). For five species of Australian skinks it was found that males and females aggressively exclude other species from shelters when suitable habitat is limited (Langkilde and Shine 2004). Nonadaptive Reasons for Female Aggression Females may also be aggressive for nonadaptive reasons, such as a genetic correlation between the sexes (Rosvall 2011). In this scenario, aggression is a by-product of a shared genome with males, and may be heritable. For example, there is evidence in Drosophila melanogaster that male and female aggression is linked, because selection for male aggression concomitantly resulted in more aggressive females (Edwards et al. 2006). Given that females of many species have reduced color patches, similar to those of males, there is a possibility that aggressive behavior is likewise the product of a genetic correlation with males. Aggression and Competition over Ecological Resources in Males Ecological consequences of male aggressive behavior and agonistic interactions among individuals are context dependent. Variation in aggressive behavior in males is typically associated with dominance status, the ability to defend territories, and the concomitant exclusive access to resources. Yet, the outcome and function of aggression in males depends on prevailing population density, abundance and spatial dispersion of resources, variance in the operational sex ratio, and dispersal capacity (Zamudio and Sinervo 2003). Moreover, the levels of aggression among males may fluctuate with age (ontogeny) (Aragon et al. 2004). Inferences regarding the behavioral ecology of aggression in lizards require integration of intrinsic attributes of individuals, the social/demographic milieu, and the environmental context of social interactions. Aggressive encounters between males are expected whenever there is intraspecific competition for limited resources. Ecological resources relevant to lizards include access to basking sites, food, retreat sites or refugia from predators, and acquisition of mates (Magnuson et al. 1979; Brattstrom 1974; Carpenter 1967). In some circumstances, as in moderately to relatively high densities, acquisition of resources (in this case females) enhances the dominance status of the individual. However, at low population densities or extremely high population densities, aggressive defense of a territory is not predicted to be favored by selection (Knell 2009). Basking sites are a critical resource for lizards because body temperature affects physiological performance (Huey 1982). Variation in physiological performance is known to have fitness consequences (Miles 2004; Robson and Miles 2000; Huey 1991). For example, sprint speed is known to vary with temperature (Huey 1982), and faster lizards exhibit greater survival (Miles 2004). In addition, aggressive behavior is temperature sensitive (Mautz et al. 1992). For example, individuals of the Tussock Skink (Pseudemoia entrecasteauxii) with higher preferred body temperatures are also more aggressive (Stapley 2006). One outcome of male aggression is the acquisition of territories that incorporate preferred basking sites, resulting in lizards that attain high body temperatures and thereby maximize physiological performance (Calsbeek and Sinervo 2002b; Kondo and Downes 2007; Olsson and Shine 2000; Stamps 1977a). Indeed, many studies that estimate aggressive behavior in lizards focus on a basking site that serves as a resource to be competed for between males (Perry et al. 2004; Robson and Miles 2000). Thus, defense of territories with greater microhabitat complexity and more favorable basking sites is likely to affect a male’s reproductive success via its ability to thermoregulate at a body temperature that maximizes its physiological performance. An observational study of the Eastern Fence Lizard (Sceloporus undulatus) found that aggressive displays were associated with basking sites (Haenel et al. 2003). Aggressive defense of space is also likely to result in males acquiring territories with higher perch sites which, in addition to enhancing

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the detection of rivals (e.g., Andrews 1971) or promoting the effectiveness of signals (Tokarz 1985), may also provide enhanced opportunities for thermoregulation. Aggressive behavior in males also has the key benefit of promoting the acquisition and defense of territories containing food resources, thereby enhancing their fitness (Stamps and Tollestrup 1984). Several studies have shown that territory size covaries with food availability (Adams 2001; Krekorian 1976; Simon 1975). Moreover, multiple studies have shown that dominant males settle in high quality territories (Calsbeek and Sinervo 2002b; Kohlsdorf et al. 2006). However, whether males are sequestering resource-rich space for their own energetic demands or to attract females (resource defense polygyny) requires experimental manipulation of food resources. For example, male Galápagos Land Iguanas (Conolophus subcristatus) appear, at least in part, to defend territories for access to food (Werner 1982), but an experimental manipulation of food availability (Christian and Tracy 1985) suggested that variation in territory size represented an interaction between the thermal quality of the habitat and its resource abundance. Aggressive interactions may increase predation risk as a consequence of increased exposure during periods of activity. An additional benefit of aggressive behavior, however, is access to retreat sites. This benefits the animal by limiting its exposure to predators or by providing thermally beneficial shelter sites with warmer temperatures during periods of inactivity (Langkilde et al. 2005; Osterwalder et al. 2004). Experimental manipulations and field observations revealed that interspecific competition for preferred “warmer” refugia was intense among five species of skinks in the genera Egernia and Eulamprus (Langkilde and Shine 2004). The limited availability of preferred retreat sites, that is, warmer shelter sites or sites providing protection from predators, may result in dominant individuals that defend these from subordinates. Kohlsdorf et al. (2006) noted that dominant males of the Amazon Lava Lizard (Tropidurus torquatus) defended territories with more refuge sites than were present in lower quality territories. Additionally, dominant males had territories that overlapped with more females when compared to low quality territories. Additional results from experimental manipulations showed that dominant males of Leseuer’s Velvet Gecko (Amalosa [=Oedura] lesueurii) excluded smaller, subordinate males from rocky retreat sites that were warmer and less likely to have been used by a snake predator (Downes and Shine 1998). Sexual Selection Male Aggression and Territorial Behavior Aggression and territorial behavior are thought to influence mating opportunities and, more generally, reproductive success. A common pattern is that the mating success of males is linked with territory size and quality. Territory size serves to influence the number of female home ranges that a male’s territory overlaps, whereas territory quality may be effective in inducing females to establish a home range adjacent to that of a dominant male. An observational and experimental approach by Hews (1990, 1993) demonstrated that males with a higher quality territory, as measured by food availability, led to greater mating success. Such studies support the hypothesis that food abundance in a male’s territory determines, in part, mating opportunities and thus reproductive success (Kwiatkowski and Sullivan 2002). Removal experiments provide evidence that male defense of territories also entails the defense of potential mates. For Urosaurus ornatus, the removal of females from a male’s territory resulted in the latter moving to a new location (M’Closkey et al. 1987b). In contrast, females did not alter their home ranges when the dominant male was removed. Multiple examples are available that demonstrate that male aggression and territorial behavior are linked with mate acquisition— Iguanidae: Sauromalus obesus (=ater) (Kwiatkowski and Sullivan 2002); Ctenosaura hemilopha (Carothers 1981); Phrynosomatidae: U. ornatus (M’Closkey et al. 1987a, b); Sceloporus undulatus (Haenel et al. 2003); Liolaemidae: Liolaemus quilmes (Robles and  Halloy 2009); Crotaphytidae: Crotaphytus collaris (Husak et al. 2009); Lacertidae: Iberolacerta cyreni (Salvador et al. 2008).

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Does Female Aggression Play a Role in Sexual Selection? In order to understand the role of female aggression in sexual selection, it is useful to first clarify what we mean by sexual selection. We follow a broad definition, which is simply stated as “competition for mates” (Shuker 2010), as advocated by Rosvall (2011) for studies of intra-sexual selection. It therefore applies equally to both males and females. Unfortunately, male lizards are far more likely to be the focus of studies of aggression and its role in sexual selection and social behavior than are females. This may, in part, be because males typically exhibit greater levels of aggressive intra-sexual competition and, as a consequence, agonistic display behavior, that they are more overtly territorial, and that they frequently have elaborate ornaments and armaments (Whiting et al. 2003; Kabelik et al. 2006; Stamps 1977b). These factors play into variance in reproductive success, which is typically greater in males, and explains why males are more likely to be ornamented (and aggressive) than are females (Rosvall 2011; Andersson 1994). There is also some debate, about animals more broadly, as to whether female aggression plays a significant role in sexual selection, as opposed to natural selection (Rosvall 2011; Clutton-Brock 2007). Furthermore, in addition to sexual selection, female traits may be the result of a genetic correlation, fecundity selection, or survival selection (the latter two cases being examples of natural selection). The importance of female–female aggression more generally in animals has received increased attention in the past decade (Gill et al. 2007; Clutton-Brock and Huchard 2013; Clutton-Brock 2009; Rosvall 2013; Rosvall 2011), even if the study of lizards has lagged behind that of other taxa, such as mammals and birds, which exhibit more elaborate parental care. Nevertheless, females offer a rich avenue for research because there are numerous contexts in which we would expect females to be aggressive, and multiple hypotheses have been advanced to explain female–female competitive/aggressive behavior (Table 9.1). These are in dire need of testing. In some species, such as the Qinghai Toad-headed Agama (Phrynocephalus vlangalli), females appear to be as aggressive as males, and potentially even more so, because they are aggressive toward both males and females. Likewise, chameleons are renowned for their intolerance of conspecifics, and females of the Cape Dwarf Chameleon (Bradypodion pumilum) are highly aggressive toward courting males, commonly attacking and biting them. Larger female chameleons pose greater danger to courting males and, consequently, smaller females are more likely to be approached and courted by males (Stuart-Fox and Whiting 2005). The females of many lizard species, such as Yarrow’s Spiny Lizard (Sceloporus jarrovi), are highly aggressive and territorial (Ruby 1978; Woodley and Moore 1999a; Sloan and Baird 1999; Stamps 1977b, a). Females are also aggressive for reasons similar to those of males, including social and sexual selection. For example, if mate availability or male encounter rates are low, females are predicted to become more aggressive as they compete for males (in accordance with the mate limitation hypothesis). Furthermore, female aggression and competition are believed to be strongly influenced by male quality, as opposed to simply the number of available males (Rosvall 2011). For females, high quality males that provide direct or indirect (genetic) benefits may be a limiting resource, a factor that is often ignored in studies of both sexes (Rosvall 2011). To the best of our knowledge, the mate limitation hypothesis has only been tested for one species of lizard, the Qinghai Toad-headed Agama (Phrynocephalus vlangalli). This species exhibits male-biased dispersal, which potentially results in lower male availability. This could explain why females are particularly aggressive. In order to test the mate limitation hypothesis, sex ratios were manipulated in large outdoor enclosures under seminatural conditions. Levels of female–female aggression were not, however, greater in enclosures with fewer males, refuting the hypothesis that female aggression is explained by lower male availability. Female aggression has also been demonstrated to influence the mode of paternity acquisition (While et al. 2009a, b). In White’s Rock Skink (Liopholis [=Egernia] whitii), females are consistently, but temporally, aggressive. Whereas female aggression was not influenced by density, body size, or territory size, more aggressive females were more likely to seek extra-pair copulations

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Table 9.1  Hypotheses for Explaining Female Competition/Aggression Hypothesis

Prediction

Plausible in Lizards?

Reference

Sexual Selection Competition for access to mates

Competition for access to highquality mates

Competition for male parental care

Competition for indirect (genetic) benefits

Competition for mating opportunities

Sexual conflict

Females more aggressive/competitive in female-biased OSR; potentially high numbers of receptive females and low numbers of available males Females more aggressive/ competitive when male quality variable or males offer direct benefits. In case of territories, difficult to separate female preference for male or resources (territory) Females compete if shared males result in reduced parental effort, reduced fitness; they compete to exclude rival females from males Females compete for males based on genetic quality, e.g., leks

Females competition/aggression increases with reduced access to mates and resources; e.g., females that control access to key resources may influence rival female RS Females aggressively attack courting males they wish to avoid mating with

Yes, but has not been demonstrated

Yes, but has not been demonstrated

Possibly in kin-based systems (e.g., Egernia group) if shared paternity reduces fitness of female’s offspring More aggressive female Liopholis whitii have more extra-pair offspring; may be better at securing high quality males Unlikely, relies on females mostly or completely excluding rivals from access to males Yes, dwarf chameleons (Bradypodion pumilum) are highly aggressive toward courting males

While et al. (2009a,b)

Stuart-Fox and Whiting (2005)

Natural Selection Density Food

Refugia Nests/eggs/offspring

Female aggression will increase with density; stress levels will increase Female aggression and food availability are inversely related

Yes, may be confounded by competition over resources Yes, evidence in Phrynocephalus vlangalii

Female aggression will increase as refuge availability decreases Female aggression toward conspecifics increases in presence of eggs/offspring

Yes, but has not been demonstrated Parental care in many Egernia group spp. through parent– offspring association reducing infanticide risk Female Eutropis longicaudata will attack snakes to protect nests

Female aggression toward predators to protect eggs/offspring

Genetic correlation

Parent–offspring correlations in aggression, heritability

Wu, Whiting, Fu, Qi unpubl. data

Reviewed in Whiting and While (2017) Huang et al. (2013) and Pike et al. (2016)

Yes, but has not been demonstrated

Source: Modified from Rosvall (2011) and applied to lizards.

(Figure 9.1). It is not clear why females that are more aggressive are also more promiscuous. It may simply be a carryover from other traits (While et al. 2009a, b). For example, offspring of more aggressive females also exhibit higher first year survival (Sinn et al. 2008). Such outcomes are suggestive of the potential importance for female aggression on fitness and highlight the need to look beyond male aggression in studies of sociality and reproductive fitness.

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Figure 9.1  T  he relationship between female aggression and the likelihood of extra-pair paternity in the familyliving White’s Rock Skink (Liopholis whitii). More aggressive females sired a higher proportion of extra-pair offspring. Circle size sample size where the smallest dot 1 and the largest 4. (Figure reprinted from While et al. 2009a, b.)

Aggression and Alternative Mating Strategies Competition for mates among males is often intense and involves a diverse array of behaviors for ensuring reproductive success. Differences in competitive abilities or aggression, such that asymmetries in reproductive opportunity among males become established and favor the evolution of alternative mating strategies (AMSs) (Maynard Smith 1974). Thus, males adopt divergent behavioral strategies, which enhance mating opportunities. Factors promoting variance among males in reproductive success include size hierarchies or dominance hierarchies, where only large or dominant males can acquire territories and mates to the exclusion of smaller, less aggressive males. Alternative mating strategies may be fixed throughout life, or they may be labile (Noble et al. 2013). The former often have a genetic or developmental basis for a polymorphism in male mating tactics. In contrast, the labile polymorphisms in mating tactics may be condition dependent, facultative or plastic (Zamudio and Sinervo 2003). In some species, there may be a morph that switches from one tactic to another during ontogeny and changes in social context (Sinervo et al. 2000). Examples of the genetic basis of alternative reproductive tactics include the fixed color ­polymorphisms of males (e.g., Uta stansburiana, Urosaurus ornatus, Sceloporus grammicus). Condition-dependent alternative reproductive strategies include those relating to body size (Amblyrhynchus cristatus, Iguana iguana), variation in head size and dewlap size (Anolis carolinensis), and variation in ­coloration, for example, Chlamydosaurus kingii (Merkling et al. 2016), Lacerta agilis (Molnár et al. 2016), and Iberolacerta (=Lacerta) monticola (Aragon et al. 2004). Although fixed and labile AMSs result in asymmetries of resource-holding potential and reproductive opportunities, the conditions for the evolution of each type differ (Sinervo and Calsbeek 2006; Miles et al. 2007). In the former, fitness advantages of one morph will ultimately lead to the elimination of other morphs through natural selection (Zamudio and Sinervo 2003). However, if the fitness of one strategy varies according to the frequency of alternative strategies, then multiple morphs may be maintained by negative frequency-dependent selection (Sinervo and Zamudio 2001; Sinervo and Calsbeek 2006; Miles et al. 2007). That is, a specific reproductive tactic will have a fitness advantage when rare. Labile alternative strategies should be maintained when the benefit of pursuing a dominant strategy exceeds its cost (Zamudio and Sinervo 2003). Alternative mating strategies may involve two or more patterns of morphological and behavioral traits among males that are linked with differences in resource holding potential (RHP). A notable feature of AMSs is the variation in energy apportioned into reproductive behavior and competition among the male morphs (Taborsky and Brockmann 2010; Zamudio and Sinervo 2000). In a typical AMS system, a dominant male (also known as a bourgeois male) exhibits high levels of aggression and defends

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a large territory that overlaps with those of multiple females, leading to higher reproductive success and greater resource-holding potential. Variation in the density of dominant males dictates the magnitude of individual interactions and the strength of competition for mates. Monopolization of space by dominant males generates copulation opportunities for subordinate males (Taborsky and Brockmann 2010) (also sometimes called satellite, floater, or sneaker males), which are either not capable of defending territories or unable to usurp space from a resident in an existing territory (Baird et al. 1996). As a consequence, these subordinates exhibit subdued coloration to avoid agonistic interactions with dominant males and rarely engage in aggressive interactions. Reproductive opportunities are obtained by satellite males through parasitizing copulations with females defended by the dominant male or by sneaker males having phenotypic traits that mimic those of females (Sinervo and Lively 1996; Sinervo et al. 2000; Zamudio and Sinervo 2000, 2003; Wikelski et al. 2005). Aggression within Genetic and Developmentally Determined AMSs The alternative mating strategies displayed by a population of Uta stansburiana in the Coast Range of California at Los Baños has been the focus of an intensive long-term study. Males in this population occur at high densities on isolated rocky outcrops. Sinervo and Lively (1996) documented a complex mating system involving three male color morphs. Two of these defend territories using different behavioral strategies (Calsbeek et al. 2002). Ultra-dominant, aggressive orangethroated males (hereafter referred to as orange males) have high resource usurping potential that is based on their extreme fighting ability. Usurpation is a risky strategy that may not result in any mating opportunities (Calsbeek et al. 2002). The aggressive behaviors shown by orange males are associated with high levels of testosterone (Zamudio and Sinervo 2000) and result in the defense of large territories situated in high-quality thermal environments that overlap with those of multiple females (Calsbeek and Sinervo 2002a). However, orange males, owing to their larger territories, are unable to repel the sneaker yellow-throated males (hereafter referred to as yellow males). Bluethroated males (hereafter referred to as blue males) defend smaller territories that overlap with fewer females. Blue males exhibit a mate-guarding strategy and engage in cooperative behavior with other blue males to repel sneaker males (Sinervo et al. 2006). As a result, blue males prevent other males from copulating with their females, but this also reduces opportunities for additional copulations. Among the territorial males, territory size is significantly and positively correlated with the number of overlapping female home ranges. Yellow males adopt a non-territorial, sneaker strategy and remain on the periphery of the ranges of territorial males, using female mimicry to avoid agonistic interactions with dominant males (Zamudio and Sinervo 2003). Mimicking females also allows yellow morph males to sneak copulations without detection by orange males. Another species, Urosaurus ornatus, exhibits a similar pattern of throat color polymorphism in males, yet differs in the behavioral strategies associated with each morph. In many populations of U. ornatus, males are characterized by a discrete throat color polymorphism consisting of three hues: orange, yellow, and blue (Figure 9.2; Thompson and Moore 1991; Lattanzio and Miles 2016; Miles unpublished). A few populations have at least six morphs that co-occur in a population, characterized by the three colors and their combinations, for example, orange-blue, yellow-blue, and orange-yellow (Thompson and Moore 1991). The morphs differ in resource-holding potential and levels of aggression. Blue males, including orange-blue and yellow-blue morphs, defend territories (Lattanzio and Miles 2014; Miles unpublished). Yellow males behave as satellites and are affiliated with dominant males, but do not defend territories (Miles unpublished). Orange males are nomadic (Hews et al. 1994). However, whether a male engages in satellite or nomadic behavior depends on the environmental conditions prevailing during ontogeny (Knapp et al. 2003). One intriguing aspect of the mating system of U. ornatus is the prevalence of geographic variation in the number of morphs within a population and in morph frequency (see Figure 9.2; Hews et al. 1997). Despite

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Figure 9.2  G  eographic variation in morph frequencies among populations and subspecies of Urosaurus ­ornatus. We provide morph data for seven additional species, including two species on islands (U.  clarionensis and U. auriculatus). Trimorphic color patterns have evolved independently in U.  nigricaudus (=microscutatus) and U. ornatus based on ancestor reconstructions (Feldman et al. 2011). Substantial variation in morph frequencies within U. ornatus is evident. Circles portray the number of morphs found in each population. Circles with a single color are monomorphic, with two colors dimorphic and three colors trimorphic. Colors in each circle indicate the morphs found at each population. (Data from Miles (unpublished).)

the pronounced among population variation in the number of morphs, data on aggressive behavior is available for only a few populations. The Tawny Crevice-dragon (Ctenophorus decresii), in some parts of its range, is also characterized by discrete polymorphism consisting of four morphs: orange, orange-yellow, yellow, and gray (Yewers et al. 2016). Orange morphs are the most aggressive, yellow or yellow-orange morphs exhibit intermediate levels of aggression, whereas gray morphs exhibit the least aggression. Variation among the morphs has a genetic basis and can be described by a model with two autosomal loci (Rankin et al. 2016). Orange and yellow morphs also have high heritabilities. The behavioral strategy of yellow morphs (either orange-yellow or yellow) is contingent on the morph of the intruder. Yellow males display more aggressively toward yellow and orange intruders, but show lower levels of aggression to a gray morph intruder. In addition, experimental studies have shown that males recognize intruders based on throat color (Osborne et al. 2012). Thus, C. decresii exhibits a male morph-specific reproductive strategy that comprises ultra-dominant males (orange), satellite males (gray), and a morph (yellow or yellow-orange) with plastic strategy depending on the social context. Condition-Dependent AMSs In mating systems characterized by condition-dependent AMSs, males may exhibit labile or plastic aggressive responses to conspecifics. Thus, males may switch from a territorial, satellite, or sneaker strategy to another contingent on the social and environmental context. Two key attributes

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that determine whether males will transition to a new mating strategy are population structure and availability of territories. Transitioning from a satellite to territorial male depends on the relative density of dominant, territorial males. If few large males are present in the population and sufficient resources/space is available for defending a territory, a male may shift to a new mating strategy. Whether a male adopts a territorial strategy also depends on the age and size of the individual. Larger, older males are more likely to have high resource-holding potential compared to younger, smaller males. The mating behavior of the Marine Iguana (Amblyrhynchus cristatus) provides an example of a labile AMS. Marine iguanas engage in reproductive activities along the coastline that consists of sandy beaches and rocky outcrops. In these habitats, numbers of marine iguanas in local aggregations can be high (e.g., >2,000 individuals on one beach on Isla Genovesa; Wikelski et al. 2005). Three male reproductive phenotypes are present in such a population: territorials, satellites, and sneakers (female mimics). Young males that are smaller tend to adopt the sneaker reproductive phenotype. They resemble females in both size and behavior, yet are reproductively mature (Wikelski et al. 1996). Territorial males cannot discriminate between sneaker males and females, resulting in sneaker males not being harassed when they intrude into a territory. Sneakers attempt copulations when a male is away from his territory. Larger, older territorial males aggressively defend small territories, signaling their status using head-bobbing (Partecke et al. 2002). Satellite males are intermediate in size, have larger heads than sneaker males, elongated dorsal spines, and assume the male breeding coloration. Territorial males engage in agonistic interactions in an attempt to exclude satellite males from their territory. Satellite males, however, move through territorial interstices and will pursue females (Partecke et al. 2002). The territorial status of males is dynamic. Some will expel a holder, thereby usurping adjacent territories. Satellite males can transition to the territorial phenotype depending on their age and the availability of suitable territories. Transitions in territorial status are modulated by testosterone (T) (Wikelski et al. 2005). Males implanted with T exhibited higher rates of head-bobbing, but males implanted with a testosterone antagonist exhibited lower rates of head-bobbing and a concomitant reduction in territory size. The aggressive behaviors of males are mediated by the demographic milieu (that is, the density of older and larger males), and appropriate conditions trigger a surge in T production and leads to a shift in dominance status and, therefore, reproductive phenotype, of satellite males. Size- and age-related variation in aggression is a characteristic of the Eastern Water Dragon (Intellagama [=Physignathus] lesueurii). Males exhibit two reproductive tactics. Dominant, territorial males are larger than members of a second group, non-territorial satellite males, and frequently patrol territories (Baird et al. 2012). Experimental removal of large, dominant males resulted in the transition in mating tactics of large satellite males from non-territorial to territorial (Baird et al. 2012), this being accompanied by a transition in aggressive behaviors on the part of the winning male. In general, most labile AMSs entail transitions in mating tactics as a consequence of size and age (Baird et al. 1996; Baird and Sloan 2003; Baird 2013). A shift in aggressive status may also be accompanied by a transition in coloration. Males of the Iberian rock lizard (Lacerta monticola = Iberolacerta cyreni) have two reproductive phenotypes. Younger, smaller males are dull brown in color and resemble females, whereas older, larger males are green. Green males display more frequently and become engaged in more conspicuous agonistic interactions than brown males (Aragon et al. 2004). An unresolved question in the study of AMSs is whether a male adopting an aggressive strategy always enhances its mating opportunities. Variation in male behavioral morphs in the monogamous Sleepy Lizards (Tiliqua rugosa) can be used to address this question. Males of this species exhibit variation in their level of aggressiveness, but can be placed into one of two behavioral types (Godfrey et al. 2012). “Fighters” exhibit high levels of aggressive behavior (based on behavioral assays) as well as sporting wounds acquired during fights with other males. “Lovers,” in contrast, display

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lower levels of aggressiveness. A social network analysis revealed that less aggressive ­“lovers” had more frequent associations with females. In contrast, highly aggressive “fighters” showed limited associations with females and often remained unpaired (Godfrey et al. 2012). In this species at least, aggressiveness results in lower opportunities for mating. Aggression without Territoriality—Mate Guarding Rather than using aggression to enhance fitness indirectly by defending territories, males may defend females. Species in the family Teiidae are active foragers whose home ranges are correlated with body size and energy requirements (Pianka and Vitt 2003). Although both male and female teiids exhibit aggressive behaviors, they do not defend territories (Winck et al. 2011). For example, the home ranges of male Anguilla Bank Ameivas (Pholidoscelis [=Ameiva] plei) exhibit substantial overlap (Censky 1995). The number of females overlapping with a male’s home range was positively correlated with home range area. Most agonistic encounters between males appear to be directed at access to females, and larger males won the majority of intra-sexual contests. In addition, most copulations were co-opted by a small number of males. After mating, males remain with females during the first days of receptivity. The role of aggression in the absence of territorial behavior in P. plei appears to be related to the acquisition of females and subsequent mate guarding after copulation. The large home ranges of teiids prevent males from defending females from other males. Hence, higher reproductive success in non-territorial males, at least in teiids, is accomplished initially through aggressive behavior by larger males allowing them to gain access to females, followed by mate guarding. Mate guarding has also been documented in European Sand Lizards (Lacerta agilis) where larger males defend females for longer periods of time. Males are also more likely to mate-guard females of similar age to themselves. However, the amount of time a male guarded a female was unrelated to the female’s body size (Olsson et al. 1996). Aggression and Fitness The link between aggression and fitness is largely unexplored because few studies focus explicitly on long-term aggressive behavior and how this may influence fitness. Aggression, however, is linked to many factors, such as AMS, that may covary over a season or lifetime, allowing us to draw some inferences about this relationship. For example, male Collared Lizards (Crotaphytus collaris) with high scores for aggression spent more time courting females (Baird et al. 2007). Paternity analyses have shown a significant link between aggression, social status, and reproductive success (Lebas 2001; Baird et al. 2007; Stapley and Keogh 2006; Husak et al. 2009). In many of the species that have been examined, larger, dominant males of high social status also attained high reproductive success. Larger, dominant males of the Common Puerto Rican Ameiva (Pholidoscelis [=Ameiva] exsul) sired more offspring than did smaller or lower status males (Lewis et al. 2000). Male Iberolacerta cyreni that exhibit higher activity levels, which is associated with dominance, sired the most offspring (Salvador et al. 2008). Interestingly, the same males also have higher survivorship to the next year. As mentioned previously, more aggressive females of Liopholis whitii were more likely to seek extra-pair matings and this may well have positively impacted their fitness. To determine whether this is the case, however, long-term monitoring of their offspring would be needed. For this species, males that were assayed for aggression and followed in the field for a season did not sire more offspring, and their body size and its relationship to aggression was found to be unrelated to reproductive success. Finally, the territories of the more aggressive individuals did not overlap with those of more females, nor did they maintain larger home ranges (McEvoy et al. 2012). In the case of the Side-blotched Lizard (Uta stansburiana), the fitness of the most aggressive morph (orange) is frequency dependent, and therefore, its behavioral type is less important. That is, the fitness payoff

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for orange males is contingent upon the frequencies of the alternative morphs. In particular, yellow males parasitize copulations from females overlapping an orange male’s territory. A complicating factor is that yellow males sire more offspring posthumously. As a consequence, sperm storage by females may have a major effect on the fitness of each morph (Zamudio and Sinervo 2000). A similar pattern was found for the Painted Dragon (Ctenophorus pictus). Red males are aggressive and dominate yellow males (Healey et al. 2007), and emerge earlier. However, yellow males are sneakers and have larger testes (Olsson et al. 2009). Although red males are the dominant, aggressive morph and copulate with females for longer, yellow males sire more offspring (Olsson et al. 2009). Social Selection Maternal Aggression and the Potential Benefits to Offspring Female aggression in lizards, particularly in the context of reproduction, is often linked to season and reproductive state. For example, females may become more aggressive during pregnancy or during the postpartum period (Sinn et al. 2008). If females are most aggressive during pregnancy, this may be a by-product of changing hormonal profiles or may be a strategy for maintaining an exclusive area for the benefit of their offspring. Likewise, female postpartum aggression could be adaptive if offspring gain from reduced competition with nonkin. In the case of egg-laying species, aggression in postpartum females may be a consequence of nest site defense. Although aggression per se was not the focus of research on the Long-tailed Sun Skink (Eutropis longicaudata), it was found that females aggressively protect their nests from egg-eating snakes (Huang 2006; Pike et al. 2016) on Orchid Island (Taiwan). Adults are too big to be preyed upon by sympatric snakes and are able to protect their nests by directly attacking foraging snakes. In the Collared Lizard (Crotaphytus collaris), nest defense was excluded as accounting for postpartum female aggression, with the most likely explanation being that aggression helps females reestablish residency after leaving their territories for several days to lay their eggs (Sloan and Baird 1999). Nest defense and egg brooding has been documented for a variety of lizards (approximately 60 species, 12 families) and is most common among scincid lizards (Somma 2003; While et al. 2009a, b; Noble and Mason 1933). In the case of the Five-lined Skink (Pleistodon [=Eumeces] fasciatus), females aggressively defend their eggs against attack by predators (Noble and Mason 1933). In one instance, a Northern Prairie Skink (Plestiodon [=Eumeces] septentrionalis) attacked and killed a ringneck snake (Diadophis punctatus) introduced into its enclosure where it was brooding a clutch of eggs (Somma 1985). In the Egernia group of lizards, parental presence, and by extension aggression, may well have influenced the evolution of parental care (Chapter 10). Females are viviparous and the offspring of many species exhibit delayed dispersal and live in family groups. If they disperse too soon, they risk infanticide by unrelated adults. By associating with their parents at a time when they are most vulnerable, the risk of attack by an unrelated adult is almost eliminated (While et al. 2014; Whiting and While 2017). This has been experimentally demonstrated for the Black Crevice Skink (Egernia saxatilis) (O’Connor and Shine 2004). Furthermore, both E. saxatilis and Liopholis whitii display heightened female postpartum aggression (O’Connor and Shine 2004; Sinn et al. 2008), and in the case of L. whitii, females are twice as aggressive during and after pregnancy than they are during nonreproductive periods. Furthermore, female aggression toward conspecifics is a predictor of offspring survival in this species (Sinn et al. 2008). There is also the possibility that female and/or male parental aggression may impact offspring survival directly. An adult King’s Skink (Egernia kingii), in the presence of its offspring, attacked and chased an approaching predatory Tiger Snake (Notechis scutatus) (Masters and Shine 2003). Although this is only a single observation, it certainly warrants more experimental follow-up in family-living species. In many Egernia group species, lizards are confined to discrete habitat patches, such as rock outcrops, where they seek refuge

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in crevices. This results in increased competition and greater potential for aggressive encounters with unrelated conspecifics. By delaying dispersal to avoid the costs of aggressive encounters, the stage is set for the evolution of kin-based sociality (Chapter 10) (While et al. 2014; Whiting and While 2017; While et al. 2009a, b). Patterns of Social Organization in Lizards—Dominance Hierarchies, Hotshots, and Despots A major outcome of aggressive behavior is the establishment of social structure in lizards (Carpenter 1967). The type of social structure depends on how individual males differ in their range of assertion displays or intensity of agonistic interactions. Research has demonstrated a positive association between elaborate aggressive displays and complex social structure (Carpenter 1967; Radder et al. 2006a, b). Furthermore, species with greater degrees of expression of sexual dimorphism, as a consequence of high population density and intense contest competition, exhibit more elaborate displays (Ord et al. 2001). Differences in social structure may vary among populations depending on a variety of factors. A primary factor is the role that population density and intensity of intraspecific competition plays. A second factor is the dispersal capacity of individuals, that is, the potential of an individual to change neighborhoods and exploit different social contexts. A third factor involves elements of the habitat, such as habitat type, habitat complexity, resource availability, and dispersion. These latter attributes dictate the heterogeneity of the environment. A habitat with high heterogeneity provides the opportunity for males to defend and monopolize resources. In contrast, homogeneous environments and even distribution of resources may prove to be difficult circumstances for males to defend territories. In most lizard species, social organization may be rigid and not vary within a season. In contrast, social organization may be transient and become modified as conditions change, such as during drought versus wet conditions, or if a dominant individual or a territorial resident dies. Moreover, social structure varies according to the mating system of the species (Brattstrom 1974). Aggressive and agonistic behaviors in males are often linked with territorial defense that excludes intruders from access to resources. Males of Iberolacerta cyreni have a large home range, but a smaller core area is defended from other males (Aragon et al. 2004). Depending on the prevailing circumstances, social structure in lizards may depart from a territorial organization to a dominance hierarchy, leks, or despotic structure. Dominance Hierarchies Dominance hierarchies are expected to emerge in three circumstances. First, high population densities result in increased frequencies of aggressive interactions (Alberts 1994; Brattstrom 1974). This may elevate the cost of defending territories and exceed the realized benefits for either food resources or mating opportunities (Kwiatkowski and Sullivan 2002). In addition, constraints on dispersal favor the development of a dominance hierarchy. Second, if the operational sex ratio is skewed toward females, males are expected to compete for females and, as a consequence, a dominance hierarchy often emerges to enhance harem defense (Carothers 1981). Third, spatially dispersed resources will also facilitate the development of a social hierarchy (Stamps 1977a). At extremely high densities, males are predicted to form leks (Kwiatkowski and Sullivan 2002). Most dominance hierarchies are based on body size, as in the Six-lined Racerunner (Aspidoscelis [=Cnemidophorus] sexlineatus), where captive males form a linear dominance hierarchy structured by an interaction between body size and aggressive behavior (Brackin 1978). The Cuban Iguana (Cyclura nubila) forms dominance hierarchies based on body size, head width, femoral pore size, and display rates. High-ranking, aggressive males are larger; have relatively larger jaw musculature; possess enlarged femoral glands; and have larger home ranges (Alberts et al. 2002). Low- and

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non-ranking males are smaller in size, exhibit lower display rates, and have smaller home ranges. The largest proportion of dominance displays and courtship attempts occur among the largest, highest ranked males. A removal experiment revealed that low ranking males could occupy an abandoned dominant male’s home range. Thus, the larger, dominant males preclude low ranking males from occupying territories. Although a hierarchical structure characterizes the social system of C. nubila, Alberts et al. (2002) classified males into dominant, territorial individuals; non-territorial satellite individuals; and pseudofemale/sneaker individuals based on morphological and behavioral variables (see also Wikelski et al. 1996). In the absence of paternity data, the mating success of these social classes may be hypothesized to represent alternative strategies for mating opportunities. Competition for spatially dispersed and limiting resources (coarse-grained environment) is the likely mechanism that explains the emergence of dominance hierarchies in the dune-inhabiting Desert Plated Lizard (Gerrhosaurus [=Angolosaurus] skoogi) in the northern Namib Desert. Males defend territories centered on the sparsely distributed plant species nara (Acanthosicyos horrida) (Pietruszka 1988). The dominance hierarchy of G. skoogi results from the defense of nara plants. Larger and darker colored males aggressively exclude smaller males from the vicinity of the plants. Dominance hierarchies may also characterize non-territorial species. Species in the family Teiidae typically do not defend territories (Stamps 1977b), but agonistic interactions among individuals are structured by body size. Larger individuals of Pholidoscelis exsul display a size-based dominance hierarchy. Male–male aggressive interactions are likely to center on access to optimal basking and foraging sites (Lewis et al. 2000). An alternative hypothesis is that the size hierarchy among male P. exsul enhances mating opportunities for larger males, which patrol larger home ranges (Lewis and Saliva 1987). Dominance hierarchies also emerge in species when held in captivity. Leks and Hotshots Marine Iguanas (Amblyrhynchus cristatus) form large aggregations on the rocky coastline of the Galápagos Islands and males defend small territories for attracting females within the aggregation during the reproductive season. This pattern of defending a territory for mating opportunities (non-resource based) among a cluster of males meets the definition of a lek. Wikelski and colleagues described the mating system and dominance behaviors in a series of papers (Partecke et al. 2002; Vitousek et al. 2008; Wikelski et al. 1996; Wikelski et al. 2005). Larger males occur within the core area of the lek (Wikelski et al. 1996), but the locations of the leks do not depend on female density (Partecke et al. 2002). Observational data show that males coalesce around large males with established territories. Two explanations for the lekking behavior, that is, clustering of territories, of marine iguanas have been proposed. First, males aggregate around areas that support high densities of females (hotspot model). Second, males selectively settle near males that are attractive to females (hotshot model). These core males exclude subordinate males and are also more frequently visited by females, supporting the hotshot hypothesis (Partecke et al. 2002). Despotic Social Systems In contrast to hierarchies, in which dominance status is arrayed in a linear order, there are social systems in which a few dominant individuals defend territories and the remaining, coexisting males hold subordinate, non-territorial status. These latter individuals may be satellite, nomadic, or floater males. The domination of other males by a few aggressive individuals is characterized as a despotic social system (Carpenter 1967). Despotic behavior is usually observed in territorial lizards for which there is extreme competition for space. Despotic social behavior has been observed in a variety of species: Urosaurus ornatus (Deslippe et al. 1990), Microlophus (=Tropidurus) (Carpenter 1966b), Plica plica (Debusk and Glidewell 1972), Crotaphytus collaris, Uta stansburiana (Calsbeek and

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Sinervo 2002b), Sauromalus ater (=obesus) (Prieto and Ryan 1978), and Lampropholis guichenoti (Torr and Shine 1996). In each instance, despotic behavior is also observed in lizards maintained in captivity. PART IV: CONSEQUENCES OF AGGRESSION FOR THE EVOLUTIONARY AND ECOLOGICAL TRAJECTORY OF POPULATIONS An underappreciated aspect of aggressive behavior is the population consequences that result from agonistic interactions. When resources are limiting, individuals may acquire exclusive access to these resources by aggressively defending space to exclude other individuals. Because the number of territories that may be supported in an environment may be less than the number of mature males, the opportunities for reproduction may be limited. Hence, territoriality is often regarded as a mechanism of density-dependent regulation (López-Sepulcre and Hanna 2005; Philibosian 1975; Stamps and Tollestrup 1984). Two facets are, however, ignored in this conclusion. First, individual variation in resource-holding potential is ignored. Second, species that exhibit alternative mating strategies are composed of individuals with divergent behavioral repertoires. High variation in reproductive success may enhance demographic stochasticity (especially in small populations) that may increase temporal variation in population size (López-Sepulcre and Hanna 2005; Calsbeek et al. 2002). Complex dynamic behaviors are likely to arise depending on fecundity levels (low vs. high), territory size, and the cost of territorial defense (López-Sepulcre and Hanna 2005). In contrast, other studies have suggested that alternative mating systems stabilize social systems (Bastiaans et al. 2013; Aragon et al. 2004). Here, we consider four population consequences of aggressive behavior. First, we consider how individual variation in aggression associated with throat color polymorphisms results in trophic polymorphism. Second, we consider how AMSs generate demographic stochasticity, but potentially moderate the risk of population extinction in species with low density. Third, we show how intrasexual and intersexual aggression may be altered by anthropogenic environmental change. Finally, we discuss an example of how intersexual aggression may affect reproductive success and reduce population growth rates, leading to population collapse. Aggression, Color Morphs, and Trophic Polymorphisms In nearly all studies of AMSs, it is assumed that each morph, despite showing differences in behavior, morphology, physiology and life history characteristics, have few if any differences in other ecological characteristics. For example, no differences in the use of microhabitat among morphs could be detected in the Tawny Crevice-dragon (Ctenophorus decresii) (Teasdale et al. 2013) or diet in the Dalmatian Wall Lizard (Podarcis melisellensis) (Huyghe et al. 2007). In contrast, males of Urosaurus ornatus differ in microhabitat use and diet (Lattanzio and Miles 2016). Agonistic behavior by dominant blue males resulted in microhabitat segregation. Dominant males settled in high-quality territories (live oak trees) with abundant prey, whereas satellite yellow males and nomadic orange males often settled on lower quality habitats (snags) that had lower resource abundance (Lattanzio and Miles 2014). An analysis of dietary patterns using stable isotopes revealed segregation among morphs in the trophic level of their prey base. Blue males fed on prey higher in the trophic web than yellow or orange males (Lattanzio and Miles 2016). Patterns of dietary divergence among morphs also exhibited variation due to habitat disturbance. At high disturbance sites, yellow males converged on the diet of blue males. Orange males in both habitat types consumed a high proportion of either C3 or C4 herbivores (Figure 9.3). The pattern of diet niche segregation among the morphs was taken as evidence that an interaction between socially mediated sexual selection and natural selection exists.

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Figure 9.3  T  rophic niche differences among male U. ornatus color morphs. Trophic relationships at (a) lowfrequency burn and (b) high-frequency burn sites. Points are mean δ13C and δ15N values. Symbols designate different male color morphs: yellow (light gray), orange (gray), or blue (dark gray). Bars represent ±1 standard error (n ≥ 3 for each group). (From Lattanzio and Miles 2014.)

Alternative Mating Strategies and Demographic Stochasticity A characteristic of alternative mating strategies is the unequal fitness among the different behavioral phenotypes. The persistence of morphs within a population is accomplished through the intransitive nature of the fitness differences. One aspect of the AMS in Uta stansburiana is the cyclic behavior of the morph frequencies (Sinervo and Lively 1996). During any phase of a cycle, one of the three morphs will be rare. As a consequence, the rare morph is anticipated to exhibit higher reproductive success due to uncertainty in mating opportunities. Consequently, the long-term geometric mean fitness is equal among the morphs (Calsbeek et al. 2002). However, a key question is how do morphs with unequal fitness persist within a population? The two territorial morphs of U. stansburiana (orange and blue, see above) use alternative methods for acquiring and defending resources (Calsbeek et al. 2002). Ultra-dominant orange males usurp space whereas blue males are resource defenders. The former mating strategy has associated costs acting through the risk of low reproductive payoff. Paternity analyses have revealed that the usurper strategy has a mean fitness greater than the defender strategy, but with a higher variance in reproductive success. That is, usurpers experience extreme variability in the number of progeny sired; some males sire many offspring whereas many males sire none. The variation in fitness promotes the coexistence

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of the two morphs through demographic stochasticity, that is, random variation in either survival or reproduction. This scenario arises because the higher variance in the usurper strategy results in lower geometric mean fitness among generations and approaches the fitness of the defender strategy. Potential fluctuations in population size arising from differences in the reproductive success of each strategy are minimized by the influence of demographic stochasticity. Alteration of Intrasexual and Intersexual Aggression by Anthropogenic Effects Human-induced changes in global environments are resulting in rapid loss of habitat, increased fragmentation of remaining habitat, and a warmer planet. These anthropogenic threats have the potential to drive alterations in aggressive interactions and the structure of lizard social systems. At one extreme, alteration of available thermal niches through global warming and habitat modification (e.g., drought) is predicted to result in local extinction of populations by diminishing hours of activity (Sinervo et al. 2010). Many populations may occupy habitats that are shared with humans. The loss of available habitat to support populations along with increasing interactions with human activity is likely to result in higher local densities and increased agonistic interactions among individuals. A comparison of the Cuban Rock Iguana (Cyclura nubila) inhabiting sites with high anthropogenic activity and those from a site with low activity revealed differences in aggressive behavior and social interactions (Lacy and Martins 2003). Iguanas that occupy sites with high human activity exhibit higher densities (perhaps due to human trophic subsidies (Jessop et al. 2012)) and altered behavioral interactions. Male–male social interactions increased in frequency and included more intense aggressive behaviors. Furthermore, male–female interactions diminished. Overall, human activity resulted in a significant shift in the social organization of rock iguanas. Alterations of intraand intersexual interactions may have demographic consequences that include lower reproductive output and diminished survival of juveniles and adults. Intersexual Aggression May Affect Reproductive Success and Lead to Population Collapse The population ramifications of intersexual aggression have received scant attention in the literature (see Rankin and Kokko 2006). Sexual conflict is likely to perturb population dynamics because of the divergent behavioral roles of males and females during mating and reproduction (Arnqvist and Rowe 2005). In some species, mating behavior of males involves aggression and intimidation of females. For example, aggressive mating behavior in the European Common Lizard (Zootoca [=Lacerta] vivipara) involves coercion (prolonged courtship), multiple mating attempts and copulation (biting of females by males, D.B. Miles pers obs.) (Le Galliard et al. 2008). Thus, mating can result in injury or harm to females as a result of the aggressive behavior of courting males. Potential fitness costs of male aggressive behavior could include a reduction of female survival or lower reproductive output. Le Galliard et al. (2005) manipulated the sex ratio in a series of seminatural population enclosures. The adult sex ratio was skewed toward either females or males. Their results revealed that females in male-biased treatments carried more mating scars, suggestive of multiple male copulations and lower reproductive success (Fitze et al. 2005). In addition, survival probabilities of females decreased, as did fecundity (Le Galliard et al. 2005). Long-term monitoring of the experimental populations has revealed a rapid decline in abundance of lizards in the male-biased treatments (Le Galliard et al. 2005). Local extinction of a population was a consequence of lower lifetime reproductive success of females (Le Galliard et al. 2008), illustrating the population consequences that occur when highly aggressive male behavior incurs a major fitness cost for females.

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FUTURE DIRECTIONS AND LIZARDS AS A MODEL SYSTEM FOR STUDIES OF AGGRESSION Our chapter demonstrates the versatility of lizards as a model system for the study of a­ ggressive behavior and its consequences for our understanding of social systems, population structure, and ultimately, fitness. Lizards, by virtue of the ease with which they can be studied, constitute an ­excellent system for behavioral and evolutionary ecological studies. They are mostly easily observed and habituate to the presence of an observer. They also have an extensive repertoire of dynamic and static signals and the outcome of a contest is normally unambiguous. Furthermore, endocrine and genetic studies have helped uncover the expression of alternate phenotypes linked to reproductive tactics that express differing levels of aggression. Indeed, studies of individual variation in behavior demonstrate consistent differences in behavioral types (i.e., personality) in many species. What is less clear is whether these behavioral types are fixed over an individual’s lifetime and whether there is a trade-off between reproductive success and survival. For example, do more aggressive individuals attain more copulations in a single season, but have lower survival because of the physiological costs of aggressive behavior? We need to know more about both the long-term costs and fitness consequences of aggression. A particularly interesting phenomenon to emerge as a result of recent research on lizards is the existence of sibling rivalry in family-living lizards of the Egernia group (While et al. 2014; Riley et al. 2017). This is well known in birds and mammals, but has not previously been considered in lizard social systems. Subordinate (smaller) individuals are the recipients of sometimes sustained aggression that can result in tail loss (Riley et al. 2017) and presumably, additional physiological costs such as stress, physical injury and reduced access to food, basking areas and/or refuges. We need to investigate the possibility that early social environment and sibling rivalry may be more common than previously believed. Furthermore, as Stamps (see Stamps 1978; Stamps and Krishnan 1994a, b, 1995) has shown, juvenile aggression among non-kin-based lizard social systems is common and may impact fitness to a greater extent than previously considered. Lizards also demonstrate tremendous diversity in social systems and behavioral repertoires that are used to assert resource-holding potential and social status. Finally, many examples of variation in social systems are associated with polymorphisms in coloration or morphology. Lizards, by virtue of their unique biology, offer a valuable opportunity for enhancing our understanding of the proximate and ultimate function of aggression and its role in social behavior. REFERENCES Adams, E. S. 2001. Approaches to the study of territory size and shape. Annual Review of Ecology and Systematics 32:277–303. Alberts, A. C. 1994. Dominance hierarchies in male lizards: Implications for zoo management programs. Zoo Biology 13:479–490. Alberts, A. C., J. M. Lemm, A. M. Perry, L. A. Morici, and J. A. Phillips. 2002. Temporary alteration of local social structure in a threatened population of Cuban iguanas (Cyclura nubila). Behavioral Ecology and Sociobiology 51:324–335. Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press. Andrews, R. M. 1971. Structural habitat and time budget of a tropical Anolis lizard. Ecology 52:262–270. Arnqvist, G. and L. Rowe. 2005. Sexual Conflict. Princeton, NJ: Princeton University Press. Aragon, P., P. Lopez, and J. Martín. 2004. The ontogeny of spatio‐temporal tactics and social relationships of adult male Iberian Rock Lizards, Lacerta monticola. Ethology 110:1001–1019. Badiane, A., P. Carazo, S. J. Price-Rees, M. Ferrando-Bernal, and M. J. Whiting. 2018. Why blue-tongue? A potential UV-based deimatic display in a lizard. Behavioral Ecology and Sociobiology 72:104. Baird, T. A. 2004. Reproductive coloration in female collared lizards, Crotaphytus collaris, stimulates courtship by males. Herpetologica 60:337–348. doi: 10.1655/03-17.

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Tokarz, R. R. 1985. Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Animal Behaviour 33:746–753. Torr, G. and R. Shine. 1996. Patterns of dominance in the small scincid lizard Lamprophilis guichenoti. Journal of Herpetology 30:230–237. Umbers, K. D. L., S. De Bona, T. E. White, J. Lehtonen, J. Mappes, and J. A. Endler. 2017. Deimatism: A neglected component of antipredator defence. Biology Letters 13:20160936. doi: 10.1098/rsbl.2016.0936. Vallortigara, G. 2000. Comparative neuropsychology of the dual brain: A stroll through animals’ left and right perceptual worlds. Brain and Language 73:189–219. Vitousek, M. N., D. R. Rubenstein, K. N. Nelson, and M. Wikelski. 2008. Are hotshots always hot? A longitudinal study of hormones, behavior, and reproductive success in male marine iguanas. General and Comparative Endocrinology 157:227–232. Weiss, S. L., D. H. Jennings, and M. C. Moore. 2002. Effect of captivity in semi-natural enclosures on the reproductive endocrinology of female lizards. General and Comparative Endocrinology 128:238–246. Werner, D. I. 1982. Social organization and ecology of land iguanas, Conolophus subcristatus, on Isla Fernandina, Galapagos. In Iguanas of the World: Their Behavior, Ecology and Conservation. ed. G. M. Burghardt and A. S. Rand, 342–365. Park Ridge, NJ: Noyes Publications. While, G. M., D. L. Sinn, and E. Wapstra. 2009a. Female aggression predicts mode of paternity acquisition in a social lizard. Proceedings of the Royal Society B: Biological Sciences 276:2021–2029. While, G. M., T. Uller, and E. Wapstra. 2009b. Family conflict and the evolution of sociality in reptiles. Behavioral Ecology 20:245–250. While, G. M., B. Halliwell, and T. Uller. 2014. The evolutionary ecology of parental care in lizards. In Reproductive Biology and Phylogeny of Reptiles, ed. J. L. Rheubert, D. S. Siegel, and S. E. Trauth. New Hampshire: Science Publishers. Whiting, M. J. and G. M. While. 2017. Sociality in lizards. In Comparative Social Evolution, ed. D. R. Rubenstein and P. Abbott, 390–426. New York: Cambridge University Press. Whiting, M. J., K. A. Nagy, and P.W. Bateman. 2003. Evolution and maintenance of social status signalling badges: experimental manipulations in lizards. In Lizard Social Behavior, ed. S. F. Fox, J. K. McCoy, and T. A. Baird. Baltimore, MD: Johns Hopkins University Press. Whiting, M. J., J. K. Webb, and J. S. Keogh. 2009. Flat lizard female mimics use sexual deception in visual but not chemical signals. Proceedings of the Royal Society B 276:1585–1591. Whiting, M. J., F. Xu, F. Kar, J. L. Riley, R. W. Byrne, and D. W. A. Noble. 2018. Evidence for social learning in a family living lizard. Frontiers in Ecology and Evolution 6:70. doi: 10.3389/fevo.2018.00070. Wikelski, M., C. Carbone, and F. Trillmich. 1996. Lekking in marine iguanas: Female grouping and male reproductive strategies. Animal Behaviour 52:581–596. Wikelski, M., S. S. Steiger, B. Gall, and K. N. Nelson. 2005. Sex, drugs and mating role: Testosterone-induced phenotype-switching in Galapagos marine iguanas. Behavioral Ecology 16:260–268. Winck, G. R., C. C. Blanco, and S. Z. Cechin. 2011. Population ecology of Tupinambis merianae (Squamata, Teiidae): Home-range, activity and space use. Animal Biology 61:493–510. Woodley, S. K. and M. C. Moore. 1999a. Female territorial aggression and steroid hormones in mountain spiny lizards. Animal Behaviour 57:1083–1089. Woodley, S. K. and M. C. Moore. 1999b. Ovarian hormones influence territorial aggression in free-living female mountain spiny lizards. Hormones and Behavior 35:205–214. Yewers, M. S., S. Pryke, and D. Stuart-Fox. 2016. Behavioural differences across contexts may indicate morph-specific strategies in the lizard Ctenophorus decresii. Animal Behaviour 111:329–339. Zamudio, K. R. and B. Sinervo. 2000. Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proceedings of the National Academy of Sciences USA 97:14427–14432. Zamudio, K. R. and B. Sinervo. 2003. Ecological and social contexts for the evolution of alternative mating strategies. In Lizard Social Behavior, ed. S. F. Fox, J. K. McCoy, and T. A. Baird, 83–106. Baltimore, MD: Johns Hopkins University Press.

Chapter  10

Stable Social Grouping in Lizards Geoffrey M. While University of Tasmania

Michael G. Gardner Flinders University South Australian Museum

David G. Chapple Monash University

Martin J. Whiting Macquarie University

CONTENTS Introduction..................................................................................................................................... 322 Social Behavior in Lizards.............................................................................................................. 322 Social Groupings in Lizards............................................................................................................ 323 What Characterizes Social Groupings in Lizards?......................................................................... 323 Egalitarian Social Groupings..................................................................................................... 323 Fraternal Social Groupings........................................................................................................ 324 Stable Adult Pair Bonds........................................................................................................ 325 Delayed Juvenile Dispersal and Prolonged Parent–Offspring Associations......................... 326 The Evolution of Lizard Social Grouping...................................................................................... 327 Factors That Influence the Emergence of Lizard Social Grouping............................................ 327 Life History Traits................................................................................................................. 327 Ecology.................................................................................................................................. 328 Factors That Influence the Maintenance of Lizard Social Grouping......................................... 329 Relatedness............................................................................................................................ 329 The Costs and Benefits of Social Behavior........................................................................... 330 The Role of Communication................................................................................................. 331 Factors That Influence the Diversification of Lizard Social Grouping...................................... 331 Lizards as Model Organisms for Understanding the Evolutionary Ecology of Complex Sociality.......................................................................................................................................... 332 Conclusions..................................................................................................................................... 333 Acknowledgments........................................................................................................................... 333 References....................................................................................................................................... 334 321

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INTRODUCTION Social behavior is extremely diverse. It ranges from simple and brief interactions between two individuals for the purposes of mating to complex interactions between individuals that occur within large cooperative societies (Szekely et al. 2010; Rubenstein and Abbot 2017). Because of the near ubiquity of social behavior across sexually reproducing animal species, and the fact that our own species is one of the most social of all organisms, there has been a fundamental interest in understanding its ecological and evolutionary causes and consequences. In a very broad sense, social behavior can be compartmentalized into a number of key components. Social structure describes patterns of social interactions and relationships between individuals, while the mating system describes the resulting reproductive consequences of such interactions. Social organization, on the other hand, describes the structure of associations between individuals within a population (e.g., groups), the size of these associations, and their spatial and temporal cohesion. Such social organization can result in the emergence of stable social groups which form the basis from which more elaborate forms of social behavior (including cooperation) can evolve. Stable social groups can emerge either as a result of non-related individuals aggregating together (egalitarian social groups) or as a result of individuals delaying dispersal and remaining within their natal home range, creating strong kin structure (fraternal social groups) (sensu Strassmann and Queller 2010). As we discuss below, whereas lizards have contributed substantially to our understanding of social structure and mating systems (e.g., Stamps 1983; Fox et al. 2003; Uller and Olsson 2008; Whiting and While 2017), it is only in the past few decades that biologists have begun to appreciate their potential to also contribute to our understanding of the evolution of stable social groups (Bull 2000; Gardner et al. 2016; Whiting and While 2017). In this chapter, we provide an overview of research on stable social grouping in lizards, focusing on recent contributions and future directions. In doing so, our aim is not to provide a comprehensive review of all aspects of lizard social behavior itself, as this is clearly beyond the scope of a single chapter. For readers interested in lizard social behavior per se, we point them toward the other chapters in this book that explicitly focus on this topic (e.g., Chapters 9, 10, and 12–14). Instead, we provide a detailed overview of patterns of stable social grouping in lizards and outline the factors which may have led to their emergence, maintenance, and diversification within this structural grade of squamates. We then discuss the role that lizards may play in our continued quest to understand when, where, and why animals live together. SOCIAL BEHAVIOR IN LIZARDS Social behavior per se has been relatively well studied in lizards, beginning with Noble and Bradley’s (1933) monograph of lizard mating behavior and sexual selection. Since then much of the research focus has been on lizard social structure and the resultant mating systems (Brattstrom 1974; Fox et al. 2003). Indeed, lizards have served as excellent model systems for this task as they are frequently diurnal, are easy to catch and follow, and exhibit strong site fidelity (Fox et al. 2003). As a result, lizards have contributed substantially to our understanding of territorial behavior (Stamps 1983; Wikelski et al. 1996), contest competition (Stamps 1977; Fox and Baird 1992; Whiting 1999; Whiting et al. 2003, 2006; Carazo et al. 2008), alternate reproductive tactics (Wikelski et al. 1996; Sinervo and Lively 1996; Whiting et al. 2009; Noble et al. 2013), and communication (e.g., static and dynamic visual signals, chemical signals/cues, vocal signals; Martins 1993; Ord et al. 2002; Ord and Martins 2006; Hibbitts et al. 2007). Lizards have also been the focus of a wide range of sexual selection studies. Stemming from this work, we now have detailed knowledge of the mating systems of many lizard species and an understanding of the consequences of this for variation in male and female reproductive success. For

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almost all species for which there has been genetic paternity testing of offspring, females have been shown to exhibit high levels of polyandry (e.g., multiple mating; Uller and Olsson 2008; Wapstra and Olsson 2014). Thus, while the majority of territorial species have traditionally been classified as being polygynous (Bull 2000), in reality, most are polygynandrous (see Kamath and Losos 2017 for discussion of this in anoles). The high incidence of female polyandry in lizards appears largely to be the outcome of mate encounter rates (Uller and Olsson 2008). Indeed, where the costs of mating to females are low, as they are in most species, patterns of paternity are driven largely by a male’s opportunity to acquire multiple copulations. There are a few exceptions to this, however. For example, in sand lizards (Lacerta agilis), where the population structure elicits strong costs associated with mating with the wrong individual, female multiple mating increases hatching success and lowers the incidence of deformities (Olsson et al. 1994). In general, however, it appears that female multiple mating evolved in lizards in the absence of indirect female benefits via strong selection on males, and that benefits arise only secondarily due to population-specific characters, such as low genetic variation and a high degree of inbreeding depression (Uller and Olsson 2008). SOCIAL GROUPINGS IN LIZARDS While reptiles have been used extensively to study social structure and mating systems, the extent to which they have been used to study social organization and specifically the evolution of stable social groups, has been limited. This is, in part, because it has been assumed that lizard social organization is restricted to territorial overlap and/or nonrandom associations related to mating (see above). However, work over the past three decades has begun to refute this idea. Indeed, following on from Michael Bull’s seminal work in the 1980s (Bull 1988), social groupings have now been documented for 66 lizard species across 18 families, and stable social aggregations have been documented for 16 species across 5 families (Gardner et al. 2016). Importantly, the taxonomic and functional diversity of stable lizard social grouping is similar to that found in many other taxa (e.g., fish and amphibians); taxa which have been used extensively to study the evolution of social complexity (Mank et al. 2005; Summers et al. 2006; Brown et al. 2010). Thus, lizards have the potential to be excellent model organisms for understanding the factors responsible for the emergence, maintenance, and diversification of social groups. WHAT CHARACTERIZES SOCIAL GROUPINGS IN LIZARDS? Social groups in lizards take several forms, in terms of both their genetic makeup and the extent to which they represent stable entities. At a very broad level, lizard social organization assumes two main forms: (1) egalitarian social groups, which emerge as a result of nonrandom associations between unrelated individuals, and (2) fraternal social groups, which form as a result of closely related individuals remaining together. With regard to the latter, social groups can take a range of forms spanning from those that are characterized simply by prolonged parent (usually maternal)– offspring associations, to those comprising large communal family groups in which there are stable adult pair bonds and multiple cohorts of young. Egalitarian Social Groupings Egalitarian social groups, in which unrelated individuals aggregate together, are relatively common among lizards, having been identified across 13 families within four major lizard suborders (the Gekkota, Iguania, Lacertoidea, and Scincoidea; Gardner et al. 2016). Group size can range from a few individuals to several thousand. Group composition may be relatively transient, both in

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terms of its stability (e.g., the extent to which such groups dissolve) and its makeup (e.g., the specific individuals within the group). However, this is not necessarily the case. For example, in the Eastern Water Dragon (Intellagama lesueurii), individuals form relatively stable associations (independent of relatedness) (Strickland et al. 2014). With the relatively recent emergence of social network analysis of animals, there is great potential for the exploration of lizard sociality, more generally, in nonkin-based systems. Many species of lizard also aggregate in greater numbers, although such aggregations may manifest only at daily/nightly sleeping refuges. As a result, the social bonds between individuals within these social aggregations are presumably weak or absent. While the function of these social associations is unknown in most instances, there are a number of ecological reasons that have been suggested as to why lizards may group in this way. For example, individuals from a range of taxa, including thick-tailed geckos (Underwoodisaurus milli), bearded dragons (Pogona vitticeps), and marine iguanas (Amblyrhynchus cristatus), have been shown to aggregate for thermoregulatory benefits (e.g., Wikelski 1999; Shah et al. 2003, 2004; Khan et al. 2010). Similarly, individual banded geckos that aggregate have been shown to exhibit a third less water loss than do solitary geckos suggesting substantial hydrostatic benefits are associated with grouping (Lancaster et al. 2006). Additional benefits suggested to promote the occurrence of egalitarian grouping behavior in lizards include a reduction of predation risk (Mouton 2011), increased foraging efficiency (Barry et al. 2014), and increased access to mates (Lemos-Espinal et al. 1997; Mouton 2011). Alternatively, it has been suggested that such social aggregations form as a result of limited availability of key habitat, for example, the availability of suitable hibernacula (Gregory 1984; Graves and Duvall 1995) or oviposition/rookery sites (Graves and Duvall 1995; Doody et al. 2009), which result in the coming together of individuals at certain times of year. Importantly, while the primary reasons for these aggregations may be ecological (e.g., refugia) or physiological (e.g., temperature/water loss), social benefits could still accrue from the resultant grouping. Furthermore, such grouping behavior, driven by abiotic factors, could act as an initial trigger for the emergence of more stable social aggregations (Graves and Duval 1995; Shah et al. 2003; Lancaster et al. 2006; Davis Rabosky et al. 2012). Fraternal Social Groupings In contrast to the taxonomic diversity of egalitarian social groups, fraternal (kin-based) social groupings (with the exception of those that exhibit only parent–offspring associations) have been identified in only one higher level group of lizards, the Scincoidea. Within the Scincoidea, kin-based sociality has been documented in two families: the Xantusiidae and Scincidae. Members of both the Gerrhosauridae and Cordylidae have been suggested to live in social aggregations, but kin structure is yet to be confirmed (Gardner et al. 2016). The vast majority of the kin-based social aggregations within the Scincidae occur within a single Australasian lineage, the subfamily Egerniinae (hereafter referred to as the Egernia group), a monophyletic assemblage of skinks consisting of the genera Egernia, Liopholis, Lissolepis, Bellatorias, Cyclodomorphus, Tiliqua, and Corucia (Gardner et al. 2008). In total, 11 species of the Egernia group, representing four genera, have been confirmed to live in stable social groups, with anecdotal evidence of social grouping in a further 17 species (Gardner et al. 2016). In contrast to this, a single species of the family Xantusiidae, Xantusia vigilis, has been shown to exhibit kin-based sociality (Davis et al. 2011). Field observations of lizards found in burrows, rock crevices, tree cavities, and underneath cover items that specifically consist of a single adult pair and associated juveniles, however, have been reported for a large number of additional lizard species (reviewed by Chapple 2003; Davis et al. 2011; Gardner et al. 2016), suggesting that kin-based sociality may be more widespread than is currently appreciated (see below). As with other social species, fraternal social groupings in lizards are characterized by long-term stable adult pair bonds and delayed juvenile dispersal, resulting in the formation of family groups

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consisting of adults and their offspring (Chapple 2003; While et al. 2015; Gardner et al. 2016; Whiting and While 2017). Although such traits are relatively consistent across species, there is considerable variation in group size and composition, both within and among species. For example, within the Egernia group, social organization includes species that are largely solitary (e.g., Tiliqua adelaidensis, Schofield et al. 2014; Liopholis inornata, Daniel 1998; Lissolepis coventryi, Taylor 1995), those in which adults pair bond during the breeding season (e.g., Tiliqua rugosa, Bull 2000), those which live in small family groups (e.g., Liopholis whitii, Egernia saxatilis, O’Connor and Shine 2003; Chapple and Keogh 2005; While et al. 2009a), and those species which live in large stable extended family groups (e.g., E. cunninghami, Stow and Sunnucks 2004; E. stokesii, Gardner et al. 2001). Stable Adult Pair Bonds One of the key characteristics of lizard fraternal social groups is the presence of long-term, stable, usually monogamous, pair bond between a male and a female. Perhaps the best example of this comes from the sleepy lizard (Tiliqua rugosa) (Bull 2000). A long-term study documented 31 partnerships that lasted for more than 15 years, 110 pairs that exceeded 10 years, and 1 pair that has been together for at least 27 years (ongoing) (Leu et al. 2015; Bull et al. 2017). Such extended long-term monogamy within and between seasons has since been shown to form the basis for social organization across most species in the Egernia group (Chapple 2003), as well as for Xantusia vigilis (Davis et al. 2011). Although the majority of species in the Egernia group exhibit social monogamy, polygynous social groups, in which some males form pair bonds with multiple females, are also known. Such social groups often exist at a lower frequency than monogamous pair bonds. For example, 30% of social groups in Liopholis whitii are characterized by a single male sharing his crevice site with up to three females (Chapple and Keogh 2006; While et al. 2009a, 2011). This variation in social organization is closely tied to crevice site availability. Indeed, experimental work has shown that the structure of available habitat, along with high levels of female–female aggression, plays a crucial role in mediating social organization in this species (Halliwell et al. 2017a). Similar arguments have been suggested to explain variation in social organization in other Egernia group species (Duffield and Bull 2002; Chapple 2003). Variation in social organization within the Egernia group can also include aggregations of multiple adults of both sexes. For example, in E. stokesii, stable social groups can consist of up to 11 adults (both males and females) sharing the same crevice site (Gardner et al. 2001, 2002; Duffield and Bull 2002). Other species, such as E. cunninghami, E. mcpheei, and E. striolata, have also been reported to live in large communal groups containing multiple adults (Stow et al. 2001; Chapple 2003; Stow and Sunnucks 2004). Similarly, in Xantusia vigilis, group size varies from 2 to 18 individuals, with social organization being represented by both nuclear families and extended family groups (Davis et al. 2011). Monogamous, polygynous, and polygynandrous pair bonds all exhibit surprising stability within and between seasons. Besides the likely lifelong pair bonding of Sleepy Lizards (T. rugosa), in Liopholis whitii pairs also exhibit considerable stability across years, with some pairs having been together for the majority of their reproductive lifespan (e.g., 10 years; G. While, unpublished data). While long-term data for the majority of other systems is relatively sparse, studies over several breeding seasons have confirmed strong pair stability between years for Egernia cunninghami (Stow and Sunnucks 2004), E. saxatilis (O’Connor and Shine 2003), and Egernia stokesii (Duffield and Bull 2002; Gardner et al. 2002). Thus, pair stability appears to be prevalent among social Egernia species. Unsurprisingly, pair separation is extremely rare in these systems. In L. whitii, only 15% of pairs exhibit separation by choice (i.e., not via the mortality of one individual; G. While, unpublished data). Social groups of Xantusia vigilis also show moderate levels of stability, with 29% of groups stable across consecutive years (Davis et al. 2011).

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Although lizards in general tend to exhibit relatively high levels of female polyandry (Uller and Olsson 2008), high levels of genetic monogamy appears to be the rule for lizards that exhibit strong social organization (Gardner et al. 2016; Whiting and While 2017). This is not to say that genetic monogamy is ubiquitous, as all species exhibit some level of extra-pair mating. Interestingly, levels of extra-pair paternity differ considerably both within and among populations/species. In Egernia cunninghami, only 2.6% of litters include extra-pair offspring (Stow and Sunnucks 2004). Levels of extra-pair paternity are also relatively low for other species including 12%–26% for Liopholis whitii (Chapple and Keogh 2005; While et al. 2009b, 2014a), 20% for E. saxatilis (O’Connor and Shine, 2003), 25% for E. stokesii (Gardner et al. 2001), and 19% for Tiliqua rugosa (Bull et al. 1998). Although the data are currently limited, species exhibiting less social, nonfamily behavior appear to exhibit considerably higher levels of genetic polyandry. For example, for Tiliqua adelaidensis, 75% of offspring within litters result from multiple mating (Schofield et al. 2014). Delayed Juvenile Dispersal and Prolonged Parent–Offspring Associations The second defining feature of fraternal lizard social groups is that of delayed offspring dispersal, which results in prolonged associations between parents and their progeny. As with pair bonding, the extent of such prolonged associations varies considerably, both within and among species. For example, in the Egernia group, such association ranges from species in which parents do not associate at all with their offspring (e.g., Liopholis inornata, Daniel 1998; Tiliqua rugosa, Bull and Baghurst 1998), through those in which parents associate predominantly with a single offspring or cohort of offspring (e.g., L. whitii, Chapple and Keogh 2006; While et al. 2009a; L. slateri, Fenner et al. 2012), to those in which parents associate with multiple cohorts of offspring (e.g., Egernia cunninghami, Stow et al. 2001; E. saxatilis, O’Connor and Shine 2003; E. stokesii, Gardner et al. 2001). In the most extreme cases, this results in large communal groups of up to 30 related individuals, including nonbreeding adults who stay within their parents’ social group. For example, in large social groups of E. stokesii, within-group relatedness between adult females is extremely high (between r = 0.25 and r = 0.55), suggesting that these groups comprise mothers and their adult daughters (Gardner et al. 2001). The prolonged parent–offspring association exhibited by fraternal lizard societies raises questions about the extent to which such associations represent a form of parental care. There are several potential functions of parent–offspring associations that may constitute simple forms of parental care. For example, offspring may gain increased access to basking locations, foraging opportunities, and retreat sites (Bull and Baghurst 1998; O’Connor and Shine 2004; but see Langkilde et al. 2007), which may result in an increase in early growth and survival (Botterill-James et al. 2016). Alternatively, offspring may benefit from extended parent–offspring associations via a reduction in the risk of infanticide and conspecific aggression (O’Connor and Shine 2004; Sinn et al. 2008). Members of the Egernia group frequently live in highly saturated environments whereby aggression toward conspecifics is common, and infanticide is a potentially significant source of offspring mortality (Post 2000; Lanham and Bull 2000; O’Connor and Shine 2004). As the parents of most such species aggressively defend their home range from conspecifics (Chapple 2003; O’Connor and Shine 2004), offspring that reside within those territories may gain significant (albeit indirect) benefits. Experimental evidence concerning E. saxatilis has shown that the presence of a parent almost eliminates aggression displayed toward offspring by unrelated adults (O’Connor and Shine 2004), and females of both Liopholis whitii and E. saxatilis have been shown to exhibit heightened aggression during periods of postpartum parent–offspring association, presumably when offspring are most at risk (O’Connor and Shine 2004; Sinn et al. 2008). Finally, offspring may gain from prolonged parent–offspring associations through the inheritance of territories, as suggested by the presence of high levels of genetic relatedness within social groups of Egernia stokesii (see above). Therefore, although levels of parent–offspring interaction are lower than those exhibited by other vertebrate

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species (e.g., full parental provisioning; Clutton-Brock 1991), they nevertheless show a greater level of interaction than previously appreciated and, importantly, may provide a key social context from which more elaborate forms of parental care could evolve (While et al. 2014b; Halliwell et al. 2017c). Parental care and prolonged parent–offspring associations are also evident in a number of lizard species that do not exhibit long-term monogamous pair bonds (e.g., fraternal social groups characterized only by extended parent–offspring associations). Such species may be oviparous or viviparous. The function of such parental care is diverse. In oviparous species it includes selection of nest sites (based on drought, desiccation, temperature extremes, hypoxia, predation, and parasitism), the brooding of eggs, and the defense of nests and eggs against potential predators (Somma 2003; Huang 2006; While et al. 2014b). For example, in Eutropis longicauda, females defend their nests as an extension of territorial behavior (Huang and Pike 2011). In viviparous species (and some oviparous species), this association between parents and offspring can occur post-birth/hatching and may persist from days to a few years. Such prolonged parent–offspring associations have now been documented for 95 species across 23 families and vary in their form, duration, and whether juveniles associate with females only or with adults of both sexes (Halliwell et al. 2017c). The function of such associations between group members ranges from passive tolerance of juveniles within adult home ranges to defense of offspring from conspecifics and predators (e.g., Halloy et al. 2007; Masters and Shine 2003). THE EVOLUTION OF LIZARD SOCIAL GROUPING Social groups form, first and foremost, when individuals regularly encounter and interact with one another. Once these interactions stabilize, a new social context emerges, from which more complex forms of social behavior and social organization can evolve. Thus, when trying to understand the evolutionary processes that have led to the diversity in social behavior evident among lizards (or  indeed any taxa) we must ask (1) what are the factors that facilitate the initial emergence of social interactions that form the foundation of social groups, (2) what are the factors that maintain social interactions and groups once they emerge, and (3) what influences the further refinement and diversification of social behavior and grouping. Factors That Influence the Emergence of Lizard Social Grouping Life History Traits Life history traits have long been suggested to provide a fundamentally important precursory context for the emergence of social organization across a wide range of organisms. Long lifespans, delayed maturity, and high relative investment in offspring have been suggested as phenomena underlying transitions to social life in birds, mammals, and insects (Arnold and Owens 1998; Covas and Griesser 2007). Such traits are likely to have also been important for such transitions in lizards. Indeed, social grouping in lizards, particularly that associated with fraternal social groups, appears to be accompanied by several of these life history traits. First, most lizard species that display stable social groupings are relatively long lived. For example, almost all the Egernia group for which there are data are thought to live for more than 10 years (Chapple 2003) and in some cases for more than 50 years (e.g., Tiliqua rugosa, Bull 1995; Bull et al. 2017; E. cunninghami, P.Harlow, unpublished data). Xantusia vigilis is also relatively long lived (at least 8–10 years) based on an absence of growth in older individuals (Zweifel and Lowe 1966; Davis et al. 2011). However, longevity per se may not be the actual causal mechanism linking life history to social groupings. Instead, several life history traits that are correlated with longevity, such as delayed maturity and high reproductive investment in relatively few offspring may be of significance

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in driving the change (Covas and Griesser 2007; Blumstein and Moller 2008). Members of the Egernia group are not only long lived, but are also often slow to mature (typically 2–3 years, but up to 5 years), skip opportunities to reproduce (i.e., do not reproduce every year), and invest more than related taxa in individual offspring (Chapple 2003). X. vigilis shows the same patterns of small litter size (1–2 years, very rarely 3), of proportionately large offspring, late maturity (2–3 years), and intermittent reproduction especially in years of low rainfall (Miller 1951; Zweifel and Lowe 1966). Combined, these traits fit the prediction that post-hatching parent–offspring associations are linked to high-quality offspring in family-living species (Covas and Griesser 2007). However, the strong phylogenetic bias of the occurrence of fraternal social groups among lizards currently mitigates against formal tests of this hypothesis. Longevity and delayed maturity are also likely to promote the evolution of long-term pair bonds. For example, in the Egernia system, limited availability of suitable habitat (e.g., high habitat saturation; see below), strong territoriality, and relatively long lifespans create low breeder turnover and intense competition over access to limited permanent crevice sites (O’Connor and Shine 2004; Langkilde et al. 2005; While et al. 2009a). These factors heighten the risk of being left without a mate or territory when switching mates between breeding seasons (see also Choudhury 1995) and perhaps favors the evolution of stable social monogamy between seasons (see arguments presented by Botterill-James et al. 2017a). A final trait that is likely to be particularly important in the emergence of fraternal social groups is viviparity. Giving birth to live young increases opportunities for interaction between parents and their offspring and, therefore, should promote transitions from solitary to group living. In support of this, postpartum parent–offspring associations are almost completely restricted to viviparous species (While et al. 2014b). Furthermore, phylogenetically controlled comparative analyses have shown that the evolution of viviparity has repeatedly preceded the emergence of parent–offspring associations in lizards (Halliwell et al. 2017c). Importantly, this has the potential to set the stage for the evolution of more complex forms of stable social aggregations (e.g., transitions from parent–­ offspring associations to family groups). Indeed, phylogenetic reconstructions suggest that live birth also preceded the evolution of more stable social groupings, in which individuals remain in groups across multiple seasons or years (Halliwell et al. 2017c). Interestingly, the evolution of viviparity is associated with cold climates because of the thermal control it affords the mother during embryonic development (Shine 2004, 2014). By extension, if kin-based sociality is dependent on viviparity, the distribution of kin-based sociality could be strongly tied to the geographic, as well as the phylogenetic, distribution of viviparity. Ecology Whereas particular life history traits increase the probability that individuals will come into contact with one another, ultimately it is ecology that dictates whether this probability is realized. Extensive work founded on a broad range of social organisms suggests that resource availability (e.g., ecological constraints) plays a fundamental role in enhancing the probability of contact (Emlen 1982; Stacey and Ligon 1987; Komdeur 1992; Heg et al. 2004; Bach et al. 2006). This is also the case for lizards. Resource availability and ecological constraints are the primary factors that have been suggested to influence the emergence of both long-term pair bonding and delayed juvenile dispersal in Egernia group species (Duffield and Bull 2002; Chapple 2003; Halliwell et al. 2017b; Whiting and While 2017). For example, these species rely on permanent shelter sites that are either naturally occurring structures, such as rock outcrops or tree hollows (Chapple 2003; Michael et al. 2010), or the result of construction via the excavation of deep and complex burrow systems, sometimes by multiple generations of the same family (McAlpin, et al. 2011). Crucially, these structures tend to be patchily distributed across the landscape and separated from one another by unsuitable habitat (Duffield and Bull 2002; O’Connor and Shine 2003). The extent of heterogeneity in habitat availability differs markedly between species. For burrowing species, suitable habitat can be

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relatively homogeneous, separated only by a matter of meters. In contrast, for species that live on rocky outcrops (e.g., Egernia striolata and E. stokesii), patches of suitable habitat can be separated by distances of 50 m or much more (Gardner et al. 2001). Such distances constitute considerable barriers to dispersal. These circumstances have the potential to impact both the availability of potential mates (see above), thus influencing the evolution of long-term pair bonding, and juvenile dispersal, thus influencing the extent of parent–offspring association (see Halliwell et al. 2017a, b for experimental evidence of this in Liopholis whitii). Importantly, a number of other lizard taxa which have been suggested to occur in stable family groups, such as certain cordylid lizards, and Liolaemus and Oligosoma skinks, occur in similar ecological circumstances with regard to their reliance on permanent shelter sites (Halloy and Halloy 1997; Mouton et al. 1999; Mouton 2011; Visagie et al. 2005; Berry 2006). This suggests that lizard social groupings may actually be more common than we currently appreciate, as long as the right ecological and life history conditions occur. However, targeted field and molecular work is required to confirm this. Factors That Influence the Maintenance of Lizard Social Grouping Once social interactions emerge, the extent to which they are stabilized and form the foundation from which more complex forms of social behavior can evolve are dependent on (1) the recurrence of the ecological conditions which promoted their initial emergence and (2) the strength of selection favoring social interactions once they arise. Kin selection is fundamentally important in this context. Indeed, the maintenance of the social interactions that underpin social groups will be promoted when the benefits of those social interactions outweigh their costs, mediated by the level of relatedness between group members (Hamilton 1964). Where groups are made up of largely unrelated individuals (e.g., egalitarian societies), social groups are maintained by a straight cost/benefit scenario, mediated, in some instances, by mutualistic benefits between group members. Fraternal societies, in contrast, have the added advantage of kin structure. This means that individuals have the potential to gain both direct and indirect fitness benefits from social interactions. Therefore, the stability of social groupings in lizards, as for other taxa, depends primarily on factors that influence the components of Hamilton’s rule (rB − C > 0, where r is the level of relatedness between the actor and recipient of a behavior r, B is the benefit of the behavior conferred to the recipient, and C is the cost of the behavior to the actor; Hamilton 1964), and the extent to which these mediate the level of conflict versus cooperation between group members. These social interactions are all mediated through communication, where recognition of kin or siblings is required (see Section “The Role of Communication” for details) and which helps maintain long-term stable associations. Relatedness Central to Hamilton’s rule is relatedness. In instances where relatedness between group members is high, kin selection can promote and maintain cooperative social behavior. This has largely been studied in the context of the elaborate social behaviors exhibited by cooperatively breeding birds, mammals, and eusocial insects (Hughes et al. 2008; Cornwallis et al. 2010; Lukas and Clutton-Brock 2012). However, relatedness is also important for maintenance of relatively simple social behavior. In such systems, the basal level of cooperation is represented by simple interactions between family members, specifically between parents and their offspring and between siblings (Queller 1994). Lessening of relatedness within groups should therefore result in reduced cooperation and increased conflict, leading to decreased social structure and complexity at the population level. Conversely, high levels of relatedness should increase the benefits of investing in parental care and for cooperation among brood mates. Such interactions ultimately promote transitions to more advanced social behavior, such as long-term stable pair bonds and greater interaction within and between cohorts of offspring (While et al. 2009a). Importantly, these traits are the precursors

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for the evolution of more highly derived forms of sociality, such as cooperative breeding and eusociality, present in species showing more advanced socialized interactions (Queller 1994; Field and Brace 2004). Relatedness between group members is influenced primarily by the extent of natal ­philopatry, which means that related individuals remain within the vicinity of one another (see above). However, for a given level of natal philopatry, female mating behavior will have fundamental implications for the structure of relatedness of social groups. Specifically, low levels of female polyandry (high l­evels of monogamy) increase the relatedness between group members, favoring cooperation between individuals. Empirical support for this derives from observations that the distribution of complex sociality across the animal kingdom is closely correlated with low levels of polyandry (e.g., Hughes et al. 2008; Cornwallis et al. 2010; Lukas and Clutton-Brock 2012). Similar arguments are likely to explain the maintenance of social grouping across lizards. For example, there are considerable (albeit low) levels of polyandry across the Egernia group and in some species this has been shown to influence the composition of the family group by promoting enhanced dispersal of extra-pair offspring (While et al. 2009b). Although the behavioral mechanisms mediating these responses have not been directly studied, recent research has suggested that they are most likely influenced by the extent to which conflicts of interest between family members are introduced (Botterill-James et al. 2017a, b). Such conflict is then likely to mediate the extent to which offspring remain versus disperse out of the natal range. Over evolutionary time, this may influence the stability of social living. The Costs and Benefits of Social Behavior For a given level of relatedness, the level of conflict versus cooperation between group members is dictated by the costs and benefits of expressing a particular social behavior. The main factor that influences these costs and benefits is resource availability. When resources are low, the tolerance of offspring by parents, and of siblings, may have significant costs, reducing access to resources and therefore growth and survival. We may, therefore, predict that under resource poor conditions greater conflict between group members will occur, resulting in increased dispersal with resultant smaller group sizes. Conversely, when resource availability is high, competition will be decreased, and group members may even gain kin selected benefits by tolerating other individuals, leading to reduced dispersal and the emergence of larger group sizes. While resource availability, in terms of crevice sites, has been shown to be important in mediating social grouping in lizards at a broad scale (e.g., Halliwell et al. 2017a), the extent to which more fine scale variation in resource availability (e.g., food availability) influences levels of conflict and cooperation and ultimately family dynamics is still relatively unexplored. The one exception is for Liopholis whitii, wherein yearly variation in resource availability (dictated by rainfall patterns) has been shown to be a strong predictor of the level of parent–offspring association (Botterill-James 2014). Future experimental, work in which fine-scale resource availability is manipulated in large-scale experimental setups, will provide opportunities to examine these ideas further. Several other ecological factors may also be important in mediating group dynamics within social lizards. Reduction of predation risk has been suggested to be an important benefit of group living for some Egernia group species. For example, groups of both E. stokesii and E. cunninghami are able to detect predators sooner than solitary individuals (Eifler 2001; Lanham and Bull 2004). Social groupings may also provide thermoregulatory benefits. For example, individuals of Xantusia vigilis that aggregate experience significant thermal benefits that translate into higher fitness (Davis Rabosky et al. 2012). For Egernia stokesii, group size has a positive effect on heat retention, with larger groups maintaining higher nighttime body temperatures than smaller groups (Lanham 2001). Lastly, increased risk of parasite transmission has been suggested to exert significant selective pressure on the maintenance of stable social grouping (Altizer et al. 2003). For both Tiliqua rugosa and Egernia stokesii (Godfrey et al. 2006, 2009; Leu et al. 2010), group structure and social behavior

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increase the rate at which parasites spread between individuals. For E. stokesii, an individual’s position within a transmission network (based upon shared shelter sites) along with the level of within-group relatedness are strongly related to the risk of infection from parasites (Godfrey et al. 2006, 2009). Conversely, group living may also decrease parasite transmission in lizards through either dilution effects (Mooring and Hart 1992), cooperation with regard to ectoparasite removal (Wikelski 1999), or the minimization of contact with individuals outside the social group that may carry novel parasites (Bull and Burzacott 2006; Godfrey et al. 2009). The Role of Communication The final factor central to the maintenance of group living is communication. Indeed, some form of recognition, either mate recognition, parent–offspring recognition, or sibling–sibling recognition, must, to some degree, mediate all levels of social interaction that facilitate the maintenance or dissolution of social grouping. Social lizards tend to lack the overtly visual displays exhibited by their nonsocial counterparts. For example, territorial lizards are often (but not always) conspicuously colored (males) and use dynamic visual signals to communicate at a distance (Ord and Martins 2006). The lack of such overt social behavior has been suggested to be one of the primary reasons for the current lack of appreciation of lizards as model systems for social behavior research (Doody et al. 2013). Instead, social species appear to rely heavily on chemical communication. Members of the Egernia group, and many species of lizards generally, tongue-flick to acquire social information. In some instances, this information is acquired directly from individuals during interactions. However, a number of Egernia group species have also been shown to mark their territories with scat piles (Duffield and Bull 2002; Chapple 2003; Fenner and Bull 2011). Importantly, many of these species have been suggested to exhibit quite sophisticated kin recognition mechanisms (Bull et al. 1994, 1999, 2000, 2001; Main and Bull 1996; O’Connor and Shine 2006), although the principal mechanisms underlying this are still the subject of much debate. Early experimental data suggested that kin recognition may be the outcome of genetic matching (e.g., Bull et al. 2002), providing a means by which the fine-scale ability to recognize individuals of close genetic relatedness could occur, as suggested by patterns of mate choice and offspring dispersal in the wild (e.g., While et al. 2009b, 2014a; Bordogna et al. 2016). However, experimental evidence is equivocal and few studies have convincingly been able to fully eliminate other potential explanatory causes, such as familiarity, in mediating these interactions (but see Bull et al. 2001). Clearly, experimental and comparative work exploring the coevolutionary dynamics between mechanisms of communication and social complexity in lizards provides an exciting avenue for future research. Factors That Influence the Diversification of Lizard Social Grouping Once lizard social groups have emerged, the diversification of social organization will depend upon the extent to which environmental conditions mediate the emergence of additional social interactions between individuals. For example, the communal family groups exhibited by some Egernia group species (e.g., E. cunninhami and E. stokesii; Stow and Sunnucks 2004; Gardner et al. 2001), which incorporate multiple cohorts of young, presumably emerged from nuclear family groups via the extended tolerance of young-of-the-year under particular environmental conditions. Thus, the same conditions that promoted the initial emergence and maintenance of social organization continue to play a role in its diversification. Furthermore, where such social groups are stabilized by selection they provide a novel social context within which additional traits can be co-opted to function in various ways, resulting in the refinement and elaboration of social behavior. For example, once simple parent–offspring associations emerge and are stabilized, any parental trait (such as aggression or forms of feeding) that provides (indirect) benefits to the offspring can be the subject of selection. Indeed, theoretical models suggest that once these relatively simple forms of social

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behavior evolve the elaboration of social behavior and complexity can proceed relatively rapidly (Gardner and Smiseth 2011). Although we do not yet have data for testing these ideas in the majority of systems, lizards offer an exciting opportunity to explore the relatively simple steps that may have contributed to social diversification (see below). LIZARDS AS MODEL ORGANISMS FOR UNDERSTANDING THE EVOLUTIONARY ECOLOGY OF COMPLEX SOCIALITY We hope that we have provided substantive evidence that there is broad taxonomic and functional diversity in stable lizard social organization, equivalent to that seen in other social taxa. With this in mind, we believe that lizards provide an outstanding opportunity for addressing fundamental questions relating to the early evolution of complex sociality. In particular, the fact that social groupings are (1) relatively simple and easily quantifiable, (2) not obligate (e.g., most species exhibit facultative or temporary forms of group living), and (3) exhibit sufficient variation in social organization (both within and among species) to allow for meaningful tests, make lizards a promising assemblage for uncovering the mechanisms that trigger the initial origins, and ongoing maintenance, of stable social grouping in animals (Chapple 2003; Doody et al. 2013; While et al. 2015; Whiting and While 2017). Indeed, much of the work on mammal and bird sociality is focused on the far end of social complexity trajectory, such as complex social tactics (e.g., punishment in primates), alliance formation, and cooperative breeding. In contrast, there has been little attention given to the early evolution and emergence of family living and kin-based sociality in vertebrates more generally. Lizards have the added advantage of being amenable to large-scale experimental studies, allowing us to design targeted experiments to tease apart causal relationships between key biotic and abiotic factors that have been suggested to influence the emergence and maintenance of social organization (e.g., Botterill-James et al. 2016; Halliwell et al. 2017a, b; Botterill-James et al. 2017b). This is not possible for the majority of bird and mammal systems. Despite this, data on reptile sociality remain scarce. The primary impediment to future studies is, therefore, a lack of information regarding the extent of social behavior for most species. One potential reason for this is that reptiles generally lack overt social displays (as detailed above), whereupon social behavior tends to remain relatively cryptic (Doody et al. 2013). Even for lizard species exhibiting the most overt social organization (such as Egernia), key social traits, such as parent–offspring associations, are often only identifiable using molecular techniques and detailed field studies (Gardner et al. 2001; Stow et al. 2001; Chapple and Keogh 2005; While et al. 2009a, b). Future research should therefore target systems in which analogous conditions to those outlined above may have facilitated the convergent emergence of family living. There are several candidate groups for such studies: the Cordylidae of sub-Saharan Africa, the liolaemid iguanids of South America, the oligosomid skinks, and Duvaucel’s Gecko (Hoplodactylus duvaucelii) of New Zealand. All of these display complex social behavior, including postpartum parental care and social aggregations of adults and juveniles (Halloy and Halloy 1997; Mouton et al. 1999; Mouton 2011; Visagie et al. 2005; Berry 2006; Barry et al. 2014). We hope that a growing appreciation that lizards can play a fundamental role in understanding the early evolution of complex sociality, coupled with the advent of more sophisticated molecular and field techniques (e.g., pit tagging and data loggers), will lead behavioral and evolutionary ecologists to pay greater attention to documenting the diversity of social behavior exhibited by lizards. Ultimately, to infer broad evolutionary patterns, the field and experimental studies outlined above need to be combined with comparative analyses of social traits across species. Such an approach will allow us not only to identify the causes and consequences of variation in social behavior in ecological settings but also to translate this understanding into a set of general principles that adequately describe the variation we see across species (Halliwell 2016). This can be achieved in

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several ways using lizards. First, comparisons between species within lineages will reveal how closely related species can take widely divergent social paths. Importantly, the most comprehensive and informative insights will be gained by focusing research efforts on taxonomic groups that allow us both to form clear predictions of phylogenetic patterns in trait distribution and to explicitly test hypotheses of functional links between traits. There are a number of lizard lineages, such as the Egernia group, that have the potential to be particularly important in this regard. Second, studies across broadly disparate lizard groups will allow us to incorporate information on ecology and life history to evaluate common factors that have been important in driving the emergence, maintenance, and diversification of social traits among groups. This approach has been an extremely fruitful avenue of research into social evolution in other taxa (Mank et al. 2005; Summers et al. 2006; Hughes et al. 2008; Cornwallis et al. 2010, 2017; Lukas and Clutton-Brock 2012). Recent research using similar approaches in lizards promises to provide equally informative insights (e.g., Gardner et al. 2016; Halliwell et al. 2017c). CONCLUSIONS In summary, lizards exhibit a wide range of social behavior and organization, ranging from short-term associations for the purpose of mating to large communal family groups which in some instances contain nonbreeding adults. We argue here that a suite of traits and abiotic factors correlate with kin-based sociality in lizards. These include a range of life history traits and the reliance on key habitat requirements. These, in combination, appear to be an important precursor for kin-based sociality, but additional work targeting species that exhibit similar traits is required to reduce the phylogenetic bias currently present in the data. The maintenance of social organization and social dynamics, more generally, is dictated primarily by subtle changes in environmental conditions that mediate the key components of Hamilton’s rule, namely, relatedness and the costs and benefits of cooperating versus competing. If these conditions seem familiar, it is because many of the arguments that we advance for the evolution of kin-based sociality in lizards are analogous to those proposed to explain the evolution of advanced forms of social behavior (e.g., cooperative breeding, eusociality) in other systems (Hughes et al. 2008; Cornwallis et al. 2010; Lukas and Clutton-Brock 2012). Indeed, evolution often results in convergent outcomes, and complex social organization tends to emerge when ecological and life history conditions impose constraints that cause closely related kin to interact. Lizards are no different, but what sets them apart is their ability to provide for an enhanced understanding of the very early stages of social evolution. Recent research has suggested that to ultimately understand why social groups evolved, we need to move away from traditional model systems in which sociality is highly derived, and in which individuals exhibit obligate or permanent forms of group living (Smiseth et al. 2003; Falk et al. 2014). By focusing on identifying the nature of social behavior and organization in species that exhibit facultative and/or temporary forms of social grouping (Whiting and While 2017), we can understand more about the early evolution of social grouping. Lizards offer an outstanding model system for this purpose, and we anticipate that they will feature more prominently in the social behavior literature in the future. ACKNOWLEDGMENTS This chapter is dedicated to the memory of Mike Bull, whose decades of research and insights into lizard social behavior paved the way for so much of what we know about lizard social evolution and will continue to do so into the future. We thank Vincent Bels and Anthony Russell for the opportunity to contribute to this book and two anonymous reviewers for their feedback on an earlier version of the manuscript. This work was

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supported by an Australian Research Council Discovery Grant (DP150102900) awarded to GMW, DGC, and MGG, and an Australian Research Council Discovery Early Career Research Fellowship (DE150100336) awarded to GMW.

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Part  III

Environmental Impact, Global Change, and Behavior

Chapter  11

Hydroregulation A Neglected Behavioral Response of Lizards to Climate Change? Elia I. Pirtle The University of Melbourne

Christopher R. Tracy California State University Fullerton

Michael Ray Kearney The University of Melbourne

CONTENTS Introduction.....................................................................................................................................344 Behavioral and Physiological Buffering of Climate Change.....................................................344 Trade-Offs between Hydroregulatory and Thermoregulatory Behaviors..................................346 Empirical Studies of Behavioral Hydroregulation..................................................................... 347 Modeling Behavioral Hydroregulation........................................................................................... 347 Behavioral Hydroregulatory Parameters of a Biophysical Model............................................. 349 Oxygen Extraction Efficiency............................................................................................... 349 Skin Resistance..................................................................................................................... 350 Microhabitat Selection.......................................................................................................... 350 Activity and Retreat............................................................................................................... 351 Diel Activity Patterns............................................................................................................ 351 Ocular Behavior.................................................................................................................... 351 Introduction to Modeling Approach........................................................................................... 351 Microclimate Scenario Development in Relation to Projected Climate Change....................... 352 Ectotherm Model Settings and Inputs........................................................................................ 353 Modeling Scenarios.................................................................................................................... 353 Results............................................................................................................................................. 355 Current Climates........................................................................................................................ 355 Summertime Water and Activity Budgets............................................................................. 355 Diel Activity Patterns ........................................................................................................... 356 Ocular Behavior ................................................................................................................... 357 Annual Water and Activity Budgets...................................................................................... 357 Climate Change Scenarios......................................................................................................... 363 Summertime Water and Activity Budgets............................................................................. 363 343

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Annual Water and Activity Budgets...................................................................................... 363 Discussion.............................................................................................................................364 Appendix......................................................................................................................................... 367 References....................................................................................................................................... 368 INTRODUCTION The dynamics of heat and water flux through the biosphere are fundamentally interconnected and together determine environmental and biological processes across vast scales (Arora, 2002; Chou et al., 2004; Mitchell et al., 2008; Shukla et al., 1982). There are intimate physical ties between heat and water dynamics for individual organisms (Figure 11.1) (Kearney et al., 2013) and for their microclimates (Rodriguez-Iturbe et al., 1999). The biological implications of climate change for “dry skinned” ectotherms such as lizards, however, have been strongly biased toward temperature effects (Deutsch et al., 2008; Sinervo et al., 2010; Vickers et al., 2011), and the effects of climate change on water budgets have only rarely been addressed (Chown et al., 2011; Pintor et al., 2016). Increases in air temperature as a result of global warming may affect lizards directly through elevated body temperature, which in turn may speed biological rates (Dillon et al., 2010) or increase risk of overheating (Sunday et al., 2014). The correlated response of higher metabolic rates will, however, lead to higher respiratory water loss rates (Welch et al., 1977). In addition, higher air temperatures may create stronger water vapor pressure gradients and thus increase rates of cutaneous water loss (Bentley et al., 1966; Dawson et al., 1966; Dmi’el, 2001; Waldschmidt et al., 1987; Warburg, 1965, 1966) (Figure 11.1). Similarly, water availability in the environment may decline because of higher evaporation rates from the soil, and the effects of this will be exacerbated if precipitation declines (Dai, 2013). The consequent reductions in plant growth and associated responses of prey species may then indirectly reduce water intake through feeding and drinking. Enhanced water stress may also feedback indirectly to thermal responses, such as through reduced thermal preferences, thermoregulatory precision, or performance as a result of dehydration (Ballinger et al., 1970; Bradshaw et al., 2007; Dupre et al., 1985; Ladyman et al., 2003; Mcginnis, 1970; Parmenter et al., 1975; Scarpellini et al., 2015). In absolute terms, reptilian water loss rates are slow, and thus, dehydration may be less of an immediate daily concern than the exceeding of thermal limits or optima. Yet cumulative water stress can still influence a reptile’s survival over relatively short intervals. Most reptiles cannot tolerate desiccation by water loss beyond a 25% reduction from the fully hydrated body weight (Heatwole, 1977; Hertz et al., 1979; Munsey, 1972). Under harshly desiccating conditions, such levels of dehydration may be exceeded in fewer than 30 days, even for desert-adapted species (Munsey, 1972). Dehydration also has sublethal effects on reptiles, and these have important implications for temperature regulation. Dehydration has been shown to reduce thermal preferences, thermoregulatory precision, and performance (Ballinger et al., 1970; Bradshaw et al., 2007; Dupre et al., 1985; Ladyman et al., 2003; Mcginnis, 1970; Parmenter et al., 1975; Scarpellini et al., 2015). Behavioral and Physiological Buffering of Climate Change The direct and indirect effects of global climate change on the temperature and water regimes of some lizards are potentially dire, and there is concern that they will lead to widespread extinctions (Araújo et al., 2006; Sinervo et al., 2010; Thomas et al., 2004). Such concerns have n­ aturally led to the question of how ectotherms such as lizards might buffer the effects of climate change through physiological and behavioral regulatory mechanisms, including the behavioral exploitation of microclimates (Kearney et al., 2009; Sears et al., 2016; Sunday et al., 2011). Herein we focus primarily on responses to climate change that involve manipulations of behavioral p­ atterns (which we refer to

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345

HEAT AND WATER BUDGETS AIR DENSITY AIR SPECIFIC HEAT BOUNDARY LAYER HEAT TRANSFER COEFF

RADIATIVE HEATING AND COOLING

INFRARED LONGWAVE RADIATION

RADIATIVE HEATING

AIR TEMPERATURE

CUTANEOUS EVAPORATION

METABOLIC RATE METABOLIC WATER PRODUCTION

O2 EXTRACT

SOLAR RADIATION

RESPIRATORY EVAPORATION EVAPORATIVE COOLING

% WET

VENT RATE

OCULAR EVAPORATION

BOUNDARY LAYER

RAIN/MOISTURE HARVESTING/ DRINKING

CLOACAL EVAPORATION

CONTACT AREA CONDUCTIVE HEATING AND COOLING SUBSTRATE TEMP

URINARY WATER % WATER IN FAECES

% WATER IN FOOD

Figure 11.1 Temperature and water dynamics of ectothermic species. Heat fluxes are shown with red wording and arrows, water fluxes with blue wording and arrows, and parameters needed to calculate fluxes are written in black. The total water budget of an animal can be modeled through the interaction of thermal and hydric physiology with the environment. The water budget intersects with the thermal budget through the evaporative processes of heat and water loss, and the metabolic processes of heat and water production. A major component of the water budget is evaporative water loss, which occurs in three major ways: respiratory, cutaneous, and ocular. These cumulatively equal total evaporative water loss. Respiratory water loss refers to the water lost to evaporation from the wet surfaces of the lungs, mouth and nares as the animal breathes. Ocular water loss refers to the water that is lost across the wet surface of the eye, if the eye is not covered by a permanent spectacle, as is the case for some scincids, teiids, lacertids, gekkonids, pygopodids, xantusiids, amphisbaenians, and snakes (Greer, 1983), or closed. Cutaneous water loss refers to the water lost across the skin and is controlled by the skin’s structural resistance to evaporation. To solve the equations for heat and mass flux, including these three avenues of evaporative water loss, several environmental conditions must be known, as well as several traits of the species in question. These traits include physiological ones, such as skin emissivity, solar absorptivity, density, thermal conductivity, specific heat capacity, surface area, silhouette area, fraction of surface contacting substrate, and the resistance of the skin to water loss (Kearney et al., 2013; Porter et al., 1969; Tracy, 1976, 1982) Species traits also include behavioral ones, such as minimum temperature to leave retreats, minimum and maximum foraging temperatures, preferred temperature, and minimum and maximum critical temperatures (Porter et al., 1973; Walker et al., 2014).

as behavioral mechanisms of thermo- and hydroregulation). Lizards may also respond to climate change through manipulations in their physiology (physiological mechanisms of thermo- and hydroregulation). The greater our understanding of these regulatory options, the better will be our ability to predict vulnerability and to decide upon appropriate management (Williams et al., 2008). The water budgets of ectotherms are controlled by many environmental factors as well as ­species-specific physiological traits. Moreover, behavioral manipulations may have substantial influence on water budgets, as they do for heat budgets. Cowles and Bogert (1944) first drew attention to the effectiveness of reptilian thermoregulation, demonstrating that many reptiles are able to maintain a remarkably high and constant body temperature in the face of large environmental fluctuations. Extensive research has since uncovered a substantial suite of physiological and behavioral

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mechanisms by which ectotherms regulate their heat budgets (reviewed by Avery, 1982; Hertz et al., 1993; Huey & Slatkin, 1976), including precise microhabitat selection, such as shade seeking and climbing into cooler, more convective conditions above the ground (Adolph, 1990; Beck et al., 2003; Melville et al., 2001; Porter et al., 1973; Vickers et al., 2011), postural adjustments that alter solar load (Bartholomew, 1966; Buttemer et al., 1993) and conductive exchange (Muth, 1977), evaporative cooling (DeNardo et al., 2004; Tracy et al., 2013), and color change (Christian, Bedford, et al., 1996; Norris, 1967; Smith et al., 2016). There is also substantial potential for lizards to alter their water budgets via similar means. Just as dynamic changes of skin color may facilitate temperature regulation (Christian, Bedford, et al., 1996), dynamic skin resistance may facilitate water regulation (Dmi’el, 2001). Moreover, behavioral responses that are typically thought to be temperature driven, such as inactivity patterns (Beck et al., 2003; Bulova, 2002; Christian, Weavers, et al., 1996; Green, 1972; Green et al., 1978) and microhabitat selection (Guillon et al., 2014; Labra et al., 2001), might also serve hydroregulatory purposes. For instance, populations of the Sand Monitor (Varanus gouldii) that occupy semiarid habitats appear to considerably reduce water loss by retreating into burrows during periods when evaporative water loss would be high (Green, 1972), this potentially coming at the expense of lost foraging opportunities. In addition, water supplementation has been shown to increase activity levels of the Gila Monster (Heloderma suspectum) during seasonal droughts, suggesting that inactivity may be driven by water constraints (Davis et al., 2009). Other hydroregulatory behaviors may include preference for water-rich foods (Clarke and Nicolson, 1994; Nagy et al., 1991) and even minimization of time spent with the eyes open (Lanham & Bull, 2004). For example, some reptiles have been observed to close one or both eyes while basking (Lanham et al., 2004; Mathews et al., 2000), or while inactive within burrows (Bulova, 2002). Such eye-closing behavior could save substantial water, considering that the wet surface of the eyes can account for more than 40% of total evaporative water loss in some reptiles (Green, 1969; Waldschmidt et al., 1987). For some species, hydroregulatory behaviors may be even more important than physiological adaptations aimed at reducing water loss (Nagy et al., 1991). Such evidence points to the significance of behavioral hydroregulation, but this question has rarely been investigated quantitatively for reptiles. Trade-Offs between Hydroregulatory and Thermoregulatory Behaviors Huey and Slatkin (1976) were among the first to note that thermoregulatory behaviors often incur costs, and that the precision of thermoregulation will therefore reflect its relative costs and benefits; the same should be true of hydroregulatory behavior. Moreover, the physical coupling between evaporation rates and body temperature can often mean that thermoregulatory and ­hydroregulatory goals are at odds. For example, regulating at a high body temperature would also engender a high evaporative water loss rate (Bentley et al., 1966; Dawson et al., 1966; Dmi’el, 2001; Waldschmidt et al., 1987; Warburg, 1965, 1966). Excessively high water loss rates in turn have the potential to force ectotherms to select cooler, more humid microhabitats where growth and performance are suboptimal or where food may be inaccessible. Trade-offs between hydroregulation and thermoregulation can also extend to activity patterns. For example, the Common Chuckwalla (Sauromalus ater) ceases activity even when thermally suitable surface conditions are available, remaining inside rocky crevice retreats, presumably to conserve water (Nagy, 1972). Unexplained retreat behaviors have also been observed during the dry season in populations of Sand Monitors (Varanus gouldii) in arid Australian habitats, which are known to exploit 96% of available activity time during the wet summer season (Christian & Weavers, 1996; Green, 1972; Green et al., 1978). It is possible that these retreat patterns could ­primarily be serving hydroregulatory purposes at the expense of thermoregulatory goals (Beck et al., 2003; Bulova, 2002; Christian, Weavers, et al., 1996; Green, 1972; Green et al., 1978). It is, ­however, generally very difficult to distinguish thermoregulatory from hydroegulatory goals in the

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field. Behavioral experiments in the laboratory, where microhabitat options can be greatly simplified and controlled, are an alternative approach that facilitate the separation of temperature and water constraints. For example, Corkery et al. (2014) manipulated microhabitats within thermal gradients to demonstrate that juvenile Tuatara (Sphenodon punctatus) will spend more time outside of retreats when humidity is high. We know of only one study that has attempted to experimentally to quantify the trade-off between thermoregulation and hydroregulation in a reptile species: Pintor et al. (2016) used controlled laboratory microhabitats to demonstrate that the Red-throated Rainbow-skink (Carlia rubrigularis) will select more humid retreat sites as temperatures increase, even though these retreat sites are thermally suboptimal. Empirical Studies of Behavioral Hydroregulation The water budgets of ectotherms, and the influence of these on behavior, can be difficult to c­ haracterize through empirical approaches. Much of our understanding to date of water budgets comes from measurements of water loss rates that have been made under carefully controlled laboratory settings, usually employing only a few temperatures or humidity levels (Mautz, 1982b). Interspecific differences in laboratory-measured evaporative water loss rates have been used to explain field observations of habitat selection (Guillon et al., 2014; Neilson, 2002; Sexton et al., 1968) as well as activity patterns (Dawson et al., 1966). Such extrapolations, however, fail to take into account the many factors besides temperature and/or humidity that can influence water loss rates in the field, behavior being the foremost. For example, Green (1972) showed how evaporative water loss rates that appear identical between two populations of the Sand Monitor (Varanus gouldii) in the laboratory resulted in substantially different daily water loss rates in the field because of the behavioral and habitat differences between the two populations. Field measurements of water budgets are attained by subjecting free-ranging animals to injections of doubly labeled water: consisting of water molecules in which both the hydrogen and oxygen atoms have been replaced with isotopes that are easily distinguishable via mass spectrometry from more common isotopes (Lifson et al., 1955; Lighton, 2008; Nagy, 1972). If regular blood samples are taken upon recapture of the animal throughout its active season, subsequent declines in the activity of the hydrogen isotopes can be used to indicate water turnover rates (Nagy, 1972). Field water loss rates can also be evaluated using injections of stable isotopes if an assessment of total body water is made upon each recapture (Green, 1972). Moreover, declines in oxygen isotope activity can be used to calculate carbon dioxide production, and thereby field metabolic rates (Lifson et al., 1955). Even if field water loss and metabolic rates are known, however, it is often difficult to be confident about attributing differences between laboratory and field water loss rates to particular physiological traits, behavioral responses, or environmental conditions (Green, 1972). Again, behavior in particular has the potential to influence field water budgets greatly, and can be better understood through laboratory experiments which provide animals with controlled microhabitats (Pintor et al., 2016). Such empirical approaches provide valuable information regarding water budgets, but it is d­ ifficult to relate them to the consequences of climate variability and change for whole organisms. To achieve this goal, however, it is possible to develop models of both the heat and water budget of a lizard that incorporate physiological and behavioral responses, using the methods of biophysical ecology. MODELING BEHAVIORAL HYDROREGULATION Biophysical approaches use physical principles to derive heat and mass fluxes through an organism as a result of the processes of radiation, conduction, convection, and evaporation (Gates, 1980; Porter et al., 1969, 1973, Tracy, 1976, 1982; Welsch and Tracy, 1977). To solve for these heat and mass fluxes, a key set of environmental conditions must be known, as well as a set of physiological

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and behavioral traits for the species in question, all of which are precisely defined by the underlying biophysical equations (Figure 11.1) (Kearney et al., 2013; Porter et al., 1969; Tracy, 1976, 1982). Solving the heat and mass flux equations allows for predictions to be made of an ectotherm’s body temperature, energy requirements, and water loss rates under the given environmental conditions and behavioral assumptions. One tool available for solving these equations is the NicheMapR R package (Kearney, 2012; Kearney & Porter, 2009, 2016; Kearney et al., 2004, 2013), which includes a biophysical model of an ectotherm that incorporates its thermal and hydric physiological traits, such as ocular surface area and skin resistance, as well as behavioral traits, such as diel activity patterns (e.g., nocturnal or diurnal), burrowing behavior, and thermal preference ranges (Table 11.1). In the field, environmental conditions are far from constant and change dramatically, even across small temporal and spatial scales. This microhabitat variation must be accounted for to make realistic predictions of water budgets in the field. One solution is to combine the heat and water budget model of an ectotherm with a microclimate model that converts macroclimatic data, such as data collected by weather stations, into microclimatic data (Figure 11.2). The NicheMapR package includes such a microclimate model, which can place the ectothermic heat and water budget predictions in the context of different available microclimates (Kearney and Porter, 2016). The result is a mechanistic Table 11.1 Ectotherm Model Parameters for Egernia cunninghami and Liopholis striata E. cunninghami Mass (g) Voluntary thermal maximum (°C) Voluntary thermal minimum (°C) Basking temperature (°C) Emergence temperature (°C) Critical thermal maximum (°C) Critical thermal minimum (°C) Preferred temperature (°C) Diurnal?

L. striata

Source

m VTmax

229.2 ± 47.7 (n = 8) 28.9 ± 0.151 (n = 6) Measured by authors 37.9 ± 1.97 (n = 15) 33.7 ± 2.50 (n = 15) Measured by authors

VTmin

25.7 ± 1.97 (n = 15) 24.9 ± 3.64 (n = 15) Measured by authors

Tbask

22

22

Temerge

15

15

CTmax

42.8 ± 0.8 (n = 6)

43.5 ± 0.8 (n = 6)

Assumed, based on author observations of captive L. striata Assumed, based on author observations of captive L. striata Measured by authors

CTmin

3.9 ± 1.1 (n = 17)

7.5 ± 0.8 (n = 12)

Measured by authors

Tpref

33.3 ± 1.7 (n = 15)

30.2 ± 2.1 (n = 15)

Measured by authors

Yes

No

Nocturnal?

No

Yes

Crepuscular?

No

Yes

Burrowing/crevice dwelling? Skinwet (proportion)

Yes

Yes

pwet

0.00237 ± 0.00092 (n = 8)

0.00309 ± 0.0012 (n = 6)

Skin resistance (s/cm)

Rskin

944.1 ± 281.8 (n = 8)

836.0 ± 324.3 (n = 6)

Ocular surface area (as percent of total surface area) Oxygen extraction efficiency (%)

Peyes

0.081 (n = 1)

0.205 (n = 1)

Author observations of captive individuals; (Barwick, 1965; Pianka et al., 1982) Author observations of captive individuals Author observations of captive individuals Author observations of captive individuals Calculated from total body water loss and oxygen consumption rate measurements made by authors Calculated from total body water loss and oxygen consumption rate measurements made by authors Measured by authors

EO2

16

16

Assumed based on Bennett (1973)

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species-specific data:

ex. Preferred temperature, burrowing behaviour (Table 1)

microclimate data:

multiple microhabitat options ex. temperature on the surface in full sun; temperature 100cm below ground

macroclimate data:

ex. temperature at weather station height

Microclimate model:

Ectotherm model:

NicheMapR

NicheMapR

define parameters with specific microhabitat conditions (i.e. soil type, maximum retreat site depth)

define parameters with species specific behavioural and physiological data

The result :

heat and water budget predictions for an animal behaving realistically within its microhabitat (Figures 3 and 4)

Figure 11.2 Visualization of biophysical modeling approach. First, macroclimate data (such as data obtained from weather stations) are converted into microclimate data that describe conditions within several microhabitats, including different levels of sun and shade and distances above and below ground. The microclimate data are based on parameters which specify microhabitat type (this includes substrate type—i.e., sandy or clay-rich, retreat site depth, and shade availability). The microclimate data are entered into the ectotherm model, along with species-specific behavioral and physiological traits (including preferred temperatures, voluntary thermal minima and maxima, skin resistance to water loss, and so forth). The ectotherm model simulates the animal within its microhabitat and yields predictions about heat and water budgets.

model of an ectotherm interacting with a realistic microhabitat, which gains power from the inclusion of thermo- and hydroregulatory behaviors (Kearney et al., 2013; Walker et al., 2014). Behavioral Hydroregulatory Parameters of a Biophysical Model Here, we use the NicheMapR package to apply a biophysical model of an ectotherm’s heat and water budgets to the simulation of the water budgets of a lizard as it behaves within a realistic microclimate. We conduct virtual explorations of the consequences of interactions between different types of behaviors and physiological traits on an ectotherm’s water budget. Specifically, we quantify the effect on water budgets of six hydroregulatory mechanisms that emerge from the biophysical equations: (1) the adjustment of oxygen extraction efficiency, (2) the adjustment of skin resistance, (3) microhabitat selection, (4) activity and retreat patterns, (5) diel activity patterns, and (6) ocular behavior. Oxygen Extraction Efficiency The amount of water lost via breathing is determined in part by the efficiency with which the animal can extract oxygen from the air (EO2). The more efficient an animal is at extracting oxygen from the air, the less the volume of air that must be pulled into the lungs to obtain the required amount of oxygen (Bennett, 1973). Oxygen extraction coefficients (or the percentage of oxygen extracted from ventilated oxygen) can vary widely across reptile species, and even within species. Oxygen extraction coefficients have been measured across temperature for a few mesic and arid snake species and range

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from 7.4% to 15.6% (Bennett, 1973; Dmi’el, 1972, 2001). It has been recorded to be as high as 68.6% for the arid-dwelling Pygmy Mulga Monitor (Varanus gilleni) of Australia (Bickler et al., 1986). Moreover, it has been shown that for some reptile species, such as the Desert Night Lizard (Xantusia vigilis), the Desert Horned Viper (Cerastes cerastes), and some species of Varanus, oxygen extraction efficiency within an individual can increase by almost 6% with a 12°C increase in temperature (Dmi’el, 1972; Mautz, 1982a; Owerkowicz, 1999; Snyder, 1971). The Ornate Box Turtle (Terrapene ornata) at temperatures between 5°C and 25°C is able to extract anywhere between 10% and 60% of available oxygen (Glass et al., 1979). This flexibility in oxygen extraction efficiency can render respiratory water loss decoupled from, or even independent of, temperature (Dmi’el, 1972) and as such could be a highly useful hydroregulatory mechanism. However, because the mechanisms that control oxygen extraction efficiency are poorly understood, the costs of maintaining a high extraction efficiency are also poorly understood. As such, it is difficult to say how likely it is that a reptile will be able to harness increased oxygen extraction efficiency to conserve water. For example, one suggested mechanism for improving oxygen extraction efficiency is a decrement or abolition of cardiac shunts, allowing more venous blood into the pulmonary circulation, thereby increasing oxygen uptake (Bennett et al., 2001). Experimental data obtained from crocodilians have suggested that such cardiac shunts may improve digestive ability (Farmer et al., 2008). If this is the case, then improving oxygen extraction efficiency to conserve water through decrements to cardiac shunts might come at a digestive cost. Moreover, even for species which, in laboratory experiments appear capable of decoupling respiratory water loss from temperature through flexibility in oxygen extraction efficiency, it is difficult to say for how long such improvements can be maintained. Some experimental evidence suggests that increased oxygen extraction efficiency is associated with short-term physiological states, such as periods of hypoventilation and elevated metabolic rates experienced during postprandial exercise (Bennett et al., 2001). Skin Resistance The skin of a reptile has some intrinsic level of resistance to water loss. Skin resistance (Rskin) is inversely related to water loss and reflects physical properties of the skin, with epidermal lipids constituting the main barrier to water loss in lizards and snakes (Dmi’el, 2001; Lillywhite, 2006). As such, interspecific differences in cutaneous water loss rates can likely be explained to some degree by differences in the structure and lipid content of the skin of the animal. Skin resistance is often correlated with habitat aridity (Dmi’el, 2001), and these correlations may reflect physiological plasticity or genetic adaptation (Dmi’el, 2001). Furthermore, the relationship between Rskin  and temperature is not always constant. Some reptile species, including the Persian Horned Viper (Pseudocerastes persicus, cited as Pseudocerastes persicus fieldii) and the Sinai Agama (Pseudotrapelus siaiatus, cited as Agama sinaita), appear to have dynamic control over their skin’s resistance (Dmi’el, 2001; Eynan et al., 1993). These studies measured cutaneous water loss rates for 14 different snake and lizard species in Israel, at three temperatures between 18°C and 35°C, and found evidence that some individuals were able to alter their skin resistance as temperatures changed. Those individuals were able to achieve nearly constant cutaneous water loss rates across the 17°C increase in temperature, suggesting that dynamic control of skin resistance may be an effective means of regulating water loss rates. The measured changes in skin resistance were found to be reversible, occurring within a short time frame, and were theorized to be achieved through vasodilation and vasoconstriction of the cutaneous blood vessels (Dmi’el, 2001; Eynan et al., 1993; Lahav et al., 1996). Microhabitat Selection Whereas evaporative water loss rates can constrain species to hydrically suitable environments, selective microhabitat use may allow species to maximize the environments they can successfully

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inhabit. Recently, water loss dynamics have been correlated to microhabitat selection for several reptiles. For example, microhabitat partitioning has been observed in the overlap zones between the ranges of parapatric species of vipers, where individuals of species with greater evaporative water loss rates consistently select more humid microhabitats within the shared habitat (Guillon et al., 2014). The different water constraints of the vipers appear to be driving this microhabitat partitioning, potentially maximizing possible activity in the more sensitive species and reducing competition for habitats between the species. Microhabitat selection may also occur on a seasonal scale, as has been observed in the Gila Monster (Heloderma suspectum), which selects more humid microhabitats during the dry, compared with the wet, season (Beck et al., 2003). Activity and Retreat Water loss rates may also determine daily activity patterns (Neilson, 2002). Many species retreat into underground burrows during the hottest periods of the day to avoid exceeding lethal temperature limits (Beck et al., 2003; Bulova, 2002; Christian, Weavers, et al., 1996; Green, 1972; Green et al., 1978); however, this behavior may be aimed, to some extent, at avoiding desiccation. Burrows tend to provide not only a cooler, but also a moister, environment than the surface. Several species, including Agassiz’s Desert Tortoise (Gopherus agassizii), and many desert lizards, have been shown to retreat into burrows at periods during the day when water loss at the surface would be highest (Beck et al., 2003; Bulova, 2002; Green, 1972; Nagy et al., 1991; Roberts, 1968). For instance, behavioral regulation of water loss through retreat patterns has been shown to be very effective for arid populations of the Sand Monitor (Varanus gouldii), which were able to achieve substantial reduction in their water loss rates by remaining within humid burrows during hot periods of the day (Green, 1972). Diel Activity Patterns Some reptile species show flexibility in diel activity patterns (Gordon et al., 2010; Mautz and Case, 1974). These variations may be seasonal, as is the case for the Granite Night Lizard (Xantusia henshawi), which is primarily nocturnal during the summer, but exhibits some diurnal behavior during the winter (Mautz and Case, 1974). Others show flexibility throughout their active season. For example, the arid-zone Leopard Ctenotus (Ctenotus pantherinus) is unique among its diurnal congeners in that it exhibits opportunistic nocturnal activity, in addition to diurnal behavior (Gordon et al., 2010). Our personal observations of the Night Skink (Liopholis striata) and its close relative the Desert Skink (Liopholis inornata), both of which are Australian arid-zone, burrowers, suggest preference for nocturnal and diurnal activity is specific to the individual. For these species, shifting to more nocturnal activity may be a useful hydroregulatory mechanism. Ocular Behavior Significant amounts of water can be lost across the surface of the eyes (Waldschmidt et al., 1987). Consequently, reducing the amount of time spent with the surface of the eye exposed to the air may provide significant water savings. Some species have been observed to close their eyes while inactive within burrows (Bulova, 2002) and others even while basking, when predator risk would presumably be quite high (Lanham et al., 2004). Introduction to Modeling Approach To explore and quantify the significance of these six mechanisms, we simulate their effects on the water budgets of two closely related but ecologically distinct Australian scincid lizards, the Desert

352

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Skink (Liopholis striata) and the Cunningham’s Spiny-tailed Skink (Egernia cunninghami) at one site within the respective habitat of each species. These species are closely related phylogenetically (Gardner et al., 2008; Greer, 1979; Honda et al., 1999), but very distinct ecologically (Chapple, 2003; Koenig et al., 2001). Egernia cunninghami is diurnal, crevice-dwelling, and occupies a mesic to semiarid habitat. Liopholis striata is nocturnal and burrowing, and occupies arid environments. We explore how the significance of each physiological and behavioral hydroregulatory mechanism varies across habitats and lifestyles of these species, and consider the potential for each to improve the ability of each species to cope with changing climatic conditions. It is important to note that herein we focus only on the direct effects of environmental changes on water budgets, by predicting changes in evaporative water loss rates. The conclusions we draw do not account for the indirect effects of environmental change on water budgets, such as potential changes to thermal preferences as a result of dehydration, or the thermoregulatory difficulties that may arise as a result of habitat modification. Some of these indirect effects could be explored using the model we present. For example, habitat modification could be simulated via a manipulation of the microclimate model parameter of maximum shade availability (which is set to 90% for all simulations herein). Other indirect effects related to changes in hydration state could be accounted for by using a full mass-budget model that is explicit about chemical elements, such as the models derived from Dynamic Energy Budget theory (Kearney et al., 2013). However, these indirect effects are beyond the scope of our current study. Microclimate Scenario Development in Relation to Projected Climate Change We used the microclimate model included within the NicheMapR R package (Kearney and Porter, 2016) to create realistic microclimatic scenarios. The microclimate model was implemented as described by Kearney et al. (2014). Specifically, it was driven by historical 0.05° grid (~5 km) daily weather input layers (air temperature, vapor pressure, wind speed, and cloud cover (Jones et al., 2009; McVicar et al., 2008; Raupach et al., 2009)). We simulated future climate by imposing projected monthly changes in temperature, humidity, solar radiation, and wind speed for 2070 onto interpolated daily weather data following the approach described by Briscoe et al. (2016). Projections were obtained from six global circulation models (GCMs), ACCESS 1.3, ACCESS 1.0, CanESM2, GDFL-CM3, HadGem2-CC, and HadGem2-ES, which perform well in capturing past climate in Australia (Watterson et al., 2013). We ran microclimate simulations at one site within the range of each species (Egernia cunninghami: 36°S, 145°E; Liopholis striata: 21°S, 130°E), under two levels of shade (0% and 90%), based on climate data from the year 1990. Humidity experienced when below ground was simulated to be that predicted by the soil water budget model of the microclimate model (Kearney and Porter, 2016) and was typically 99%. This is consistent with both physical expectations (Campbell et al., 1998) and empirical (Schmidt-Nielsen et al., 1950). We note that Walsberg (2000) calculated much lower levels of humidity in the soil, but these are erroneous.1 The outputs of the microclimate model included infrared radiation intensities, aboveground profiles of air temperature, wind velocity, relative humidity, and soil temperature profiles, all under the two user-provided extremes of shading by vegetation. 1

If Campbell et al.’s (1998) equation 4.13 is used to recreate the derivations of soil humidity from Walsberg (2000; his Fig 7a) using the same soil water potential data from Szarek and Woodhouse (1977), the relative humidity levels in soil air space are calculated to be greater than 90% throughout the year.  ψ  Rh = exp   135000 



Where: Rh = relative humidity in the soil (as a fraction) ψ = water potential (J/kg)

(Campbell et al.’s (1998 )’s equation 4.13)

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Ectotherm Model Settings and Inputs The NicheMapR ectotherm model calculations include hourly body temperature, activity state, and water loss as a function of the chosen behavioral constraints. The model assumes that an ­ectotherm will be active at all times at which activity is possible. Parameter values for the ectotherm model inputs, and their sources, for both species are listed in Table 11.1. The physiological input data were determined experimentally for each species (Pirtle et al. in prep). The “skinwet” term ( pwet ) determines the proportion of the total surface area used in the calculation of mass transfer of water from the surface (see Appendix for a more detailed description including derivations). Modeling Scenarios We used the NicheMapR ectotherm model to test the water savings associated with six ­different hydroregulatory mechanisms for these two skink species under each climate scenario: (1) adjustment of oxygen extraction efficiency, (2) adjustment of skin resistance, (3) microhabitat selection, (4) activity and retreat patterns, (5) diel activity patterns, and (6) ocular behavior. We modeled the water budget of each species within its respective microhabitat, based on the animal characteristics given in Table 11.1. Next, we altered those animal characteristics one at a time, to simulate the presence and absence of a hydroregulatory mechanism (Table 11.2). For example, to test for the effect of closing the eyes while basking, we altered the variable Popen , which represents the proportion of time spent with the eyes open while active. We first ran the model with Popen equal to 100%, and then ran the model again with Popen equal to 10%. The water savings of each hydroregulatory mechanism (S) is reported as the percentage difference in water loss rates between the less water conservative state (ex. Popen = 100%) and the more water conservative state (ex. Popen = 10%). S=



Et _ 0 − Et _ 1 100 (11.1) Et _ 0

where: S is the water savings associated with hydroregulatory mechanism expressed as percentage reduction in total evaporative water loss rates (%) Et _ 0 is the average daily cumulative total water loss (g/s) per average daily possible active hours across the year, without the hydroregulatory mechanism in question Et _1 is the average daily cumulative total water loss (g/s) per average daily possible active hours across the year, with the hydroregulatory mechanism in question Table 11.2 Varying Model Parameters for Testing Hydroregulatory Mechanisms for Egernia cunninghami and Liopholis striata Hydroregulatory Mechanism

Term That Is Varied

Oxygen extraction efficiency

EO2 (%)

Skin resistance

Rskin (s/cm)

Microhabitat selection Activity and retreat

Retreat site relative humidity (%) Can the animal retreat underground? Is animal diurnal Popen (%)

Diel activity patterns Ocular behavior

Low Water Conservation State

High Water Conservation State

9 8 300 1,500 150 Ambient No

16 68 700 1,900 1,900 Soil (~99) Yes

Yes 100

No 10

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BEHAVIOR OF LIZARDS

The oxygen extraction efficiency ranges were chosen to match (1) the increase in E O2 achieved by the Desert Horned Viper (Cerastes cerastes) over a 13°C increase in temperature and therefore represents a realistic hydroregulatory mechanism (Dmi’el, 1972), that is, a 7% increase in oxygen extraction efficiency, from 9% to 16%; and (2) the differences between values at the lowest and highest ends of oxygen extraction efficiencies reported for a reptile species (8% and 68%) as a potential adaptive benefit of a high EO2. The highest value comes from juvenile Pygmy Mulga Monitors (Varanus gilleni) at 68% (Bickler et al., 1986) and the lowest from the Palestine Viper (Daboia palaestinae, cited as Vipera palaestinae) at 7.5% (Dmi’el, 1972). For skin resistance, the first scenario aimed to capture the water savings associated with ­increasing a relatively high Rskin of 1500 s/cm, characteristic of arid-adapted species (Dmi’el, 2001), to 1900 s/cm. This particular increase is similar to what has been observed as a result of a 13°C increase in temperature for the Persian Horned Viper (Pseudocerastes persicus) and as such represents a realistic hydroregulatory mechanism (Dmi’el, 2001). The second scenario tested the effect of increasing a low Rskin, characteristic of more mesic adapted species (Eynan et al., 1993), by the same magnitude, from 300 to 700 s/cm. This increase is similar to that reported for two species of agamids in Israel across a 17°C increase in temperature (Eynan et al., 1993). Finally, we tested the water budget differences between two values near the lowest and highest levels of skin resistance reported for any squamate reptile (150 and 1900 s/cm) as evidence of the adaptive significance of a high Rskin. The highest reported value of Rskin is for Cerastes cerastes at 1922 s/cm (Dmi’el, 2001) and the lowest for the Crested Anole (Anolis crisatellus) at 29 s/cm (Dmi’el et al., 1997). For microhabitat selection, we tested the water budget differences between a very humid retreat near 99% relative humidity, as would occur in a backfilled burrow, and a drier retreat site with air at the same vapor pressure as that at the surface. The relative humidity within a burrow will vary with several factors, including surface temperature and humidity, time of day, burrow shape, and days since rain (Bulova, 2002). For the activity and retreat simulations, we tested the benefit of retreating into burrows versus remaining on the surface (in the shade) when temperatures in the sun exceed the voluntary maxima. For the diel activity pattern simulations, we tested the benefits to water budgets associated with switching from diurnal to nocturnal behavior. We assumed thermal preferences do not change from day to night. This is supported by the observation that thermal preferences do not vary from nocturnal to diurnal activity periods for Ctenotus pantherinus (Gordon et al., 2010). Finally, for ocular behavior, we predicted the water budget of each species with its eyes fully open throughout 100% of the activity period and compared this to the outcome of the water budget when the eyes are kept closed for 90% of the activity period (alternatively, this can be thought of as a 90% reduction in the surface area of the eye throughout the activity period). This value was chosen to represent the theoretical maximum water budget savings that could be achieved via this ocular behavior. While an ectotherm may be unlikely to fully close its eyes for 90% of its active interval, the water savings resulting from a 90% reduction of ocular surface area would comparable to the water savings associated with the evolution of a transparent eyelid or a permanent spectacle. Moreover, personal observations of Liopholis inornata and L. striata in captivity and the Military Dragon (Ctenophorus isolepis) in the field suggest that these lizards spend upwards of 50% of their active periods with their eyes fully or partially closed. We also simulated L. striata as basking during the daytime (rather than restricting all activity to nocturnal intervals), based on our own observations that individuals of this species within our captive colony spend considerable time basking in the daytime. It is during such intervals that ocular behavior is most likely to be manipulated. We plotted the average evaporative water loss rates every hour throughout an average January (mid-summer) day under current and future climates, with and without each of the six hydroregulatory mechanisms, and calculated the activity time and water savings associated with each ­hydroregulatory mechanism over the entire year.

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RESULTS Mean hourly water loss rates under the different scenarios in January, during the austral summer, are illustrated in Figures 11.3 and 11.4, with cumulative differences in water loss and activity across the whole year illustrated in Figures 11.5 and 11.6. We only report the 2070 simulation for one of the climate change scenarios because the results were virtually identical for all six climate change scenarios. We now summarize key results for each hydroregulatory strategy, first discussing the summertime results, then the annual budgets, and finally the climate change responses. Current Climates Summertime Water and Activity Budgets Oxygen Extraction Efficiency For the nocturnal Liopholis striata, increasing oxygen extraction efficiency by 7% (changing from 9% to 16%) only reduced the total evaporative water loss during January activity by a maximum of 1.3%. (Figure 11.3a), whereas the diurnal Egernia cunninghami was able to reduce total evaporative water loss by up to 27.2% (Figure 11.3b). When we tested the effect of a 62% change in EO2, from one of the lowest recorded values of oxygen extraction efficiency (8% for Duboia palaestinae [Dmi’el, 1972]) to one of the highest (68% for Varanus gilleni [Bickler et al., 1986]), we found that L. striata only increased its savings by 3.2%, whereas E. cunninghami halved its costs, reducing its total evaporative water loss by up to 50.4% (Figure 11.3c and d). Skin Resistance Increasing an already high level of skin resistance by a realistic 400 s/cm reduced the total evaporative water loss during January by 12.5% and 15.5% for Liopholis striata and Egernia cunninghami, respectively (Figure 11.3g and h). Increasing a low R skin by 400 s/cm yielded greater benefits: 49.7% and 48.5% for the nocturnal L. striata and diurnal E. cunninghami, respectively (Figure 11.3 and f). When we tested the effect of an increase in R skin equivalent from going from the lowest reported values to the highest (150 to 1900 s/cm), we found that total evaporative water could be reduced by 85.7% and 83.3% for the nocturnal and diurnal species respectively (Figure 11.3i and j). Microhabitat Selection Selecting a retreat site with high humidity (~99%) as opposed to a drier retreat site (reflecting ambient vapor pressure) reduced the total evaporative water loss during January by 27.7% for the nocturnal burrowing Liopholis striata and by 19.0% for the diurnal crevice-dwelling Egernia cunninghami (Figure 11.4a and b). Activity and Retreat For the nocturnal burrowing Liopholis striata, daytime burrow retreats reduced the total evaporative water loss during January by 68.1% (Figure 11.4c). For the diurnal crevice-dwelling Egernia cunninghami, water savings achieved by retreating were smaller but still substantial. Total evaporative water loss was reduced by 20.9% when E. cunninghami was allowed to retreat into crevices rather than being restricted to shaded surface sites (Figure 11.4d).

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Diel Activity Patterns Total evaporative water loss during January was 49.8% lower when the nocturnal Liopholis striata was simulated as a nocturnal lizard compared to when simulated as a diurnal lizard (Figure 11.4e). For the diurnal Egernia cunninghami, water loss rates were 87.8% lower when simulated as a nocturnal lizard rather than as a diurnal lizard (Figure 11.4f).

Figure 11.3 Evaporative water loss rates averaged across the month of January at one site in the range of each species (Egernia cunninghami and Liopholis striata), with and without the employment of each physiological hydroregulatory mechanism. The solid lines indicate predictions made under current climate conditions. The dashed lines indicate predictions made under projected future climatic conditions (ACCESS 1.3 model for 2070). The orange lines indicate total evaporative water loss predictions based on the less water-conservative state, for example, a lower value of skin resistance. The blue lines indicate total evaporative water loss predictions based on the more water-conservative state, for example, a higher value of skin resistance. The two percentage values given at the top of each graph represent the percentage difference in total water loss between the solid orange and blue lines (current climate) and between the dashed orange and blue lines (projected future climate). (Continued)

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Figure 11.3 (CONTINUED) Evaporative water loss rates averaged across the month of January at one site in the range of each species (Egernia cunninghami and Liopholis striata), with and without the employment of each physiological hydroregulatory mechanism. The solid lines indicate predictions made under current climate conditions. The dashed lines indicate predictions made under projected future climatic conditions (ACCESS 1.3 model for 2070). The orange lines indicate total evaporative water loss predictions based on the less water-conservative state, for example, a lower value of skin resistance. The blue lines indicate total evaporative water loss predictions based on the more water-conservative state, for example, a higher value of skin resistance. The two percentage values given at the top of each graph represent the percentage difference in total water loss between the solid orange and blue lines (current climate) and between the dashed orange and blue lines (projected future climate).

Ocular Behavior For Liopholis striata, the total evaporative water loss during January was reduced by up to 37.1% when the eyes were kept closed throughout 90% of its active p­ eriods (and diurnal basking was allowed in addition to nocturnal activity) (Figure 11.4g). The same behavior reduced the total evaporative water loss rates of Egernia cunninghami by up to 22.1% (Figure 11.4h). Annual Water and Activity Budgets The effects of the different hydroregulatory mechanisms on the total annual water budget for both lizards reflected the pattern seen during the summer for both species. Each hydroregulatory mechanism achieved reductions in the annual water budgets of both the diurnal Egernia

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Figure 11.4 Evaporative water loss rates averaged across the month of January at one site in the range of each species Egernia cunninghami and Liopholis striata), with and without the employment of each behavioral hydroregulatory mechanism. The solid lines indicate predictions made under current climatic conditions. The dashed lines indicate predictions made under projected future climatic conditions (ACCESS 1.3 model for 2070). The orange lines indicate total evaporative water loss predictions based on the less water-conservative state, for example, a lower value of skin resistance. The blue lines indicate total evaporative water loss predictions based on the more water-conservative state, for example, a higher value of skin resistance. The two percentage values given at the top of each graph represent the percentage difference in total water loss between the solid orange and blue lines (current climate) and between the dashed orange and blue lines (projected future climate). For ocular behavior, we allowed the nocturnal L. striata to bask during the daytime, since daytime basking is when ocular behavior is most likely to be manipulated, and these skinks are known to bask outside their burrows during the day (personal observations).

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Figure 11.5 Cumulative annual evaporative water loss rates (g H2O per g body mass) and cumulative possible annual activity time (hours) at one site in the range of each species (Liopholis striata and Egernia cunninghami), with and without the use of each physiological hydroregulatory mechanism. Predictions are shown for current climatic and future climatic conditions (ACCESS 1.3 model for 2070). The light blue and light orange bars indicate evaporative water loss and activity predictions based on the less water-conservative state, for example, a lower value of skin resistance. The dark blue and dark orange bars indicate evaporative water loss and activity predictions based on the more water-conservative state, for example, a higher value of skin resistance. (Continued)

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Figure 11.5 (CONTINUED) Cumulative annual evaporative water loss rates (g H2O per g body mass) and cumulative possible annual activity time (hours) at one site in the range of each species (Liopholis striata and Egernia cunninghami), with and without the use of each physiological hydroregulatory mechanism. Predictions are shown for current climatic and future climatic conditions (ACCESS 1.3 model for 2070). The light blue and light orange bars indicate evaporative water loss and activity predictions based on the less water-conservative state, for example, a lower value of skin resistance. The dark blue and dark orange bars indicate evaporative water loss and activity predictions based on the more water-conservative state, for example, a higher value of skin resistance.

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Figure 11.6 Evaporative water loss rates averaged across the month of January at one site in the range of each species (Liopholis striata and Egernia cunninghami), with and without the use of each behavioral hydroregulatory mechanism. Predictions are shown for current climatic and future climatic conditions (ACCESS 1.3 model for 2070). The light blue and light orange bars indicate evaporative water loss and activity predictions based on the less water-conservative state, for example, a less humid retreat site. The dark blue and dark orange bars indicate evaporative water loss and activity predictions based on the more water-conservative state, for example, a more humid retreat site. For ocular behavior, we allowed the nocturnal L. striata to bask during the daytime, since daytime basking is when ocular behavior is most likely to be manipulated and these skinks are known to bask outside their burrows during the day (personal observations). (Continued)

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Figure 11.6 (CONTINUED) Evaporative water loss rates averaged across the month of January at one site in the range of each species (Liopholis striata and Egernia cunninghami), with and without the use of each behavioral hydroregulatory mechanism. Predictions are shown for current climatic and future climatic conditions (ACCESS 1.3 model for 2070). The light blue and light orange bars indicate evaporative water loss and activity predictions based on the less water-conservative state, for example, a less humid retreat site. The dark blue and dark orange bars indicate evaporative water loss and activity predictions based on the more water-conservative state, for example, a more humid retreat site. For ocular behavior, we allowed the nocturnal L. striata to bask during the daytime, since daytime basking is when ocular behavior is most likely to be manipulated and these skinks are known to bask outside their burrows during the day (personal observations).

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cunninghami and the nocturnal Liopholis striata. Yearly activity budgets were unaffected by hydroregulatory changes in nearly all cases, with two notable exceptions. First, the simulated transition from diurnal to nocturnal behavior drove substantial decreases in possible activity time for both L. striata and E. cunninghami due to colder nighttime conditions at their simulated sites (Figure 11.4j and l). Second, the crevice-dwelling diurnal E. cunninghami is predicted to have more opportunities for activity when selecting surface retreat sites over cooler burrows (Figure 11.4h). Climate Change Scenarios Summertime Water and Activity Budgets In the January (summer time) simulations, water loss rates were similar or slightly higher than under current climatic conditions for all hydroregulatory scenarios, with two notable exceptions. First, when diurnal activity is simulated for the nocturnal Liopholis striata, water loss rates are reduced under projected future climatic conditions, as a result of temperature-driven activity restriction (Figure 11.4e), in line with the hypothesis of Sinervo et al. (2010). However, when L. striata is simulated as being nocturnal, which is more ecologically accurate, possible activity actually increases under projected future climatic conditions. Second, during the tests of ocular behavior, when we allowed the nocturnal L. striata to bask during the daytime, water loss rates are again reduced under projected future climatic conditions. This is again driven by a reduction in the amount of time L. striata is able to bask during the daytime without overheating. (Figure 11.4g). In general, the degree of water saving associated with each hydroregulatory mechanism was of a similar magnitude under current and projected future climatic conditions, with the exception of activity phase, for which nocturnality reduced the water loss rates of Liopholis striata by nearly 50% under the current climatic scenario, but by only 22% under the projected 2070 climatic scenario (Figure 11.4e). As such, the benefits of transitioning to nocturnality are predicted to diminish as climates become warmer and drier. This is a result of total possible activity for a diurnal and nocturnal lizard converging under the projected future climatic conditions (as possible activity for nocturnal species increases while for diurnal species possible activity decreases). It should be noted that the model can only predict possible activity time; increases in possible activity time will not necessarily translate into actual increases in activity. There were slightly stronger effects of projected climate change on the efficacy of the hydroregulatory mechanisms for the diurnal Egernia cunninghami compared to the nocturnal Liopholis striata, with the projected future climatic conditions reducing the effectiveness of each mechanism by moderate amounts for E. cunninghami (