LIZARD ECOLOGY The foraging mode of lizards has been a central theme in guiding research in lizard biology for three decades. Foraging mode has been shown to be a persuasive evolutionary force molding the diet, ecology, behavior, anatomy, biomechanics, life history, and physiology of lizards. This volume reviews the state of our knowledge on the effects of foraging mode on these and other organismal systems to show how they have evolved with foraging mode over a wide taxonomic survey of lizard groups. The reviews presented here reveal the continuous nature of foraging strategies in lizards and snakes, providing the general reader with an up-to-date review of the field, and will equip researchers with new insights and future directions for the sit-and-wait vs. wide foraging paradigm. This volume will serve as a reference book for herpetologists, evolutionary biologists, ecologists, and animal behaviorists. S TEPHEN M. REILLY is Professor in the Department of Biological Sciences and Director of the Ohio Center for Ecology and Evolutionary studies at Ohio University. L ANCE D. MC B RAYER is an Assistant Professor in the Department of Biology and Curator of Herpetology for the Savannah Science Museum Collections at Georgia Southern University. D ONALD B. MILES is Professor in the Department of Biological Sciences at Ohio University.
LIZARD ECOLOGY The Evolutionary Consequences of Foraging Mode Edited by STEPHEN M. REILLY Department of Biological Sciences, Ohio University LANCE D. MCBRAYER Georgia Southern University DONALD B. MILES Department of Biological Sciences, Ohio University
cambridge university press Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo, Delhi, Mexico City Cambridge University Press The Edinburgh Building, Cambridge CB2 8RU, UK Published in the United States of America by Cambridge University Press, New York Information on this title: /9781107407480 Cambridge University Press 2007 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2007 First paperback edition 2012 A catalogue record for this publication is available from the British Library isbn 978-0-521-83358-5 Hardback isbn 978-1-107-40748-0 Paperback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Information regarding prices, travel timetables, and other factual information given in this work is correct at the time of first printing but Cambridge University Press does not guarantee the accuracy of such information thereafter.
Contents List of contributors page vii Preface Stephen M. Reilly, Lance D. McBrayer, and Donald B. Miles xi Historical introduction: on widely foraging for Kalahari lizards Raymond B. Huey and Eric R. Pianka 1 I Organismal patterns of variation with foraging mode 11 1 Movement patterns in lizards: measurement, modality, and behavioral correlates Gad Perry 13 2 Morphology, performance, and foraging mode Donald B. Miles, Jonathan B. Losos, and Duncan J. Irschick 49 3 Physiological correlates of lizard foraging mode Kevin E. Bonine 94 4 Lizard energetics and the sit-and-wait vs. wide-foraging paradigm Tracey K. Brown and Kenneth A. Nagy 120 5 Feeding ecology in the natural world Laurie J. Vitt and Eric R. Pianka 141 6 Why is intraspecific niche partitioning more common in snakes than in lizards? Richard Shine and Michael Wall 173 7 Herbivory and foraging mode in lizards Anthony Herrel 209 8 Lizard chemical senses, chemosensory behavior, and foraging mode William E. Cooper, Jr. 237 9 Patterns of head shape variation in lizards: morphological correlates of foraging mode Lance D. McBrayer and Clay E. Corbin 271 v
vi Contents 10 Prey capture and prey processing behavior and the evolution of lingual and sensory characteristics: divergences and convergences in lizard feeding biology Stephen M. Reilly and Lance D. McBrayer 302 11 The meaning and consequences of foraging mode in snakes Steven J. Beaupre and Chad E. Montgomery 334 II Environmental influences on foraging mode 369 12 The foraging biology of the Gekkota: life in the middle Aaron M. Bauer 371 13 Foraging mode in the African cordylids and plasticity of foraging behavior in Platysaurus broadleyi Martin J. Whiting 405 14 Interactions between habitat use, behavior, and the trophic niche of lacertid lizards Bieke Vanhooydonck, Anthony Herrel, and Raoul Van Damme 427 15 Food acquisition modes and habitat use in lizards: questions from an integrative perspective Roger A. Anderson 450 16 The evolution of foraging behavior in the Gala pagos marine iguana: natural and sexual selection on body size drives ecological, morphological, and behavioral specialization Maren N. Vitousek, Dustin R. Rubenstein, and Martin Wikelski 491 17 The evolution of the foraging mode paradigm in lizard ecology Lance D. McBrayer, Donald B. Miles, and Stephen M. Reilly 508 Index 522
Contributors ROGER A. ANDERSON, Western Washington University, Bellingham, WA 98225-9160, USA AARON M. BAUER, Villanova University, Villanova, PA 19085, USA STEVEN J. BEAUPRE, Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA KEVIN E. BONINE, Department of Ecology and Evolutionary Biology, University of Arizona, PO Box 210088, Tucson, AZ 85721, USA TRACEY K. BROWN, Biological Sciences Department, California State University, San Marcos, CA 92096-0001, USA WILLIAM E. COOPER, JR., Indiana University Purdue University at Ft. Wayne, Ft. Wayne, IN 46805-1499, USA CLAY E. CORBIN, Department of Biological and Allied Health Sciences, Bloomsburg University, Bloomsburg, PA 17815, USA ANTHONY HERREL, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium RAYMOND B. HUEY, Department of Zoology, University of Washington, Seattle, WA 98195-1800, USA vii
viii List of contributors DUNCAN J. IRSCHICK, 221 Morrill South, University of Massachusetts at Amherst, Amherst, MA 01003, USA JONATHAN B. LOSOS, Washington University, St Louis, MO 63130-4899, USA LANCE D. MCBRAYER, Georgia Southern University, Box 8042, Statesboro, GA 30460, USA DONALD B. MILES, Program in Ecology and Evolutionary Biology, Department of Biological Sciences, Ohio University, Athens, OH 45701, USA CHAD E. MONTGOMERY, Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701, USA KENNETH A. NAGY, Department of Organismic Biology, University of California, 621 S. Young Dr., Los Angeles, CA 90095-1606, USA GAD PERRY, Department of Range, Wildlife, and Fisheries Management, Box 42125, Texas Tech University, Lubbock, TX 79409-2125, USA ERIC R. PIANKA, Department of Zoology, University of Texas, Austin, TX 78712, USA STEPHEN M. REILLY, Program in Ecology and Evolutionary Biology, Department of Biological Sciences, Ohio University, Athens, OH 45701, USA DUSTIN R. RUBENSTEIN, Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14850, USA RICHARD SHINE, School of Biological Sciences, University of Sydney, Sydney, Australia, New South Wales 2006, Australia BIEKE VANHOOYDONCK, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium RAOUL VAN DAMME, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium MAREN N. VITOUSEK, Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
List of contributors ix LAURIE J. VITT, Sam Noble Oklahoma Museum of Natural History, 2401 Chautaugua, Norman, OK 73072, USA MICHAEL WALL, School of Biological Sciences, University of Sydney, Sydney, Australia, New South Wales 2006, Australia MARTIN J. WHITING, Communication & Behaviour Research Group, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits 2050, South Africa MARTIN WIKELSKI, Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
Preface Investigations into the natural history of lizards have been a major source of discovery in many disciplines of biology, including, but not limited to, morphology, physiology, ecology, and evolution. Although lizards serve as model organisms for a variety of research topics, the group has figured prominently in ecological studies. In particular, the 1960s witnessed a proliferation of theoretical and quantitative studies in population and community ecology that were based on data collected from lizards. As a survey of papers from the past 40 years will attest, squamate reptiles continue to serve as key organisms in ecological research. The evolution and ecology of feeding behavior is one area of ecology in which conclusions emerging from studies based on lizards were most influential. Two early papers are especially relevant to the study of feeding ecology in lizards. The study of community structure and habitat use of North American desert lizards by Pianka (1966) was one of the first to suggest a classification of species into either sit-and-wait or constantly moving in an attempt to link resource exploitation, habitat structure and species diversity. A few years later, Schoener (1969a,b, 1971) presented models of optimal predator size based in part on idealized lizard predators that corresponded to sit-and-wait and widely foraging species. Subsequently, Huey and Pianka (1981) considered the question of which ecological traits were potentially affected by differences in foraging mode. Although several papers on foraging modes came out at about the same time (Andrews, 1979; Anderson and Karasov, 1981; Regal, 1978; Toft, 1981), the Huey and Pianka paper was the first to synthesize known patterns into a coherent set of predictions. As these authors acknowledged, the ecological correlates were varied and complex. In short, the paper by Huey and Pianka (1981) crystallized the foraging mode paradigm in lizards. Their paper was important because the conditions for plasticity in foraging mode were also described; this has often been ignored by later studies. In addition, they stated xi
xii Preface that the numerous morphological and physiological adaptations associated with foraging mode may preclude shifts in behavior, or that the shifts may be asymmetric. Finally, they highlighted how foraging mode may be a fundamental trait that influences the evolution of morphology, physiology, and behavior. From the onset many researchers have questioned whether the paradigm was truly a dichotomy of two foraging states or whether it was a continuum of states with wide foraging evolving multiple times (see, for example, Pianka, 1973; Regal, 1978; Pietruszka, 1986; McLaughlin, 1989; Schwenk, 1994; Perry, 1999; Butler, 2005). We note the similarity between the sit-and-wait vs. widely foraging dichotomy in foraging ecology and the r K dichotomy in life history theory; both were instrumental in stimulating research in their respective fields. Advances in lizard ecology have been periodically reviewed in a series of contributory volumes published over the past 40 years: Lizard Ecology: A Symposium (Milstead, 1967); Lizard Ecology: Studies of a Model Organism (Huey et al., 1983); and Lizard Ecology: Historical and Experimental Perspectives (Vitt and Pianka, 1994). As evidenced by these volumes, lizards emerged as a model system for understanding the complex trade-offs among traits in relation to foraging mode. By focusing on sit-and-wait vs. wide-foraging species, students in the fields of ecology, evolutionary biology, and animal behavior could select species with extremely diverse natural histories to test a variety of hypotheses. The breadth of investigation spurred by a dichotomous view of foraging modes is staggering, and ripe for review and evaluation. As shown by chapters in this volume, the foraging mode paradigm has guided and molded numerous studies in morphology (head shape, biomechanics, prey processing), physiology (metabolic rate, locomotor performance, muscle physiology), ecology (predator avoidance, diet choice, niche relations, habitat effects), and behavior (e.g. movement patterns, chemoreception, feeding behavior). Because so many traits appear to be correlated with foraging mode, the sit-and-wait vs. wide-foraging paradigm has emerged as a major explanatory tool for evolutionary patterns in lizard biology. After 40 years of research on how foraging mode permeates practically all aspects of a lizard s biology, it is time to step back and examine how pervasive foraging mode is in structuring trait correlations and trait tradeoffs in squamate reptiles. Accordingly, the goal of this book is to review the current understanding of the influence of foraging mode on the biology of lizards and snakes (squamates). The book as a whole is guided by three central questions. 1. What are the specific patterns in morphology, ecology and behavior that are associated with foraging mode? 2. How do these patterns relate to phylogeny? (Is it simply shared history or are things really evolving in concert?)
Preface xiii 3. How do emergent patterns of organismal traits and behavior integrate or change with the evolution of foraging mode? To review foraging biology of squamates, leaders across biological disciplines studying squamate biology were asked to address these questions with new and existing data. The result, we believe, is both a synthetic review of the foraging mode literature and a novel look at the evolutionary patterns seen at organismal levels across a very diverse vertebrate group. The book is divided into two parts. Part I, Organismal patterns of variation with foraging mode, presents eleven chapters describing the relationships between foraging mode and many aspects of squamate biology ranging from physiology and anatomy to performance and behavior, to diet, to life history. Part II, Environmental influences on foraging mode, covers the influences of nocturnality (geckos), plasticity related to environmental heterogeneity, feeding in the ocean, and the myriad of relationships between food acquisition mode and habitat use. The book concludes with a short synthesis of the general patterns identified by contributors. One of the more interesting, and controversial, findings is that wide foraging has evolved several times rather than once as a deep split in the phylogeny of lizards. Not all contributors agree with this interpretation, however. Many emergent research questions are identified throughout the book that further probe how interconnected traits have evolved, converged, and diverged with foraging mode. Like the r K continuum so important in our understanding of life history evolution, the sit-and-wait vs. wide-foraging paradigm is shifting to a continuum that better represents the emerging patterns of foraging mode biology in squamates. Producing this volume has taken longer than we had hoped but we are confident that it will help bring new students of squamate biology up to speed on the influence of foraging mode and it will help direct the questions addressed by established researchers in the future. If nothing else, all authors agree that although much progress has been made in the past 40 years, much more information is needed in most aspects of squamate foraging biology. We hope this volume will help catalyze some of this effort. As with all such volumes it would not have been possible without the assistance of many other people. We graciously thank the contributors for their submissions and their insights; these have certainly opened our eyes about the pervasive effects of foraging mode in squamates. The production staff at Cambridge University Press has continually been wonderful in their long-term help, guidance, and patience during all stages of the preparation of this book. We offer special thanks to many of our contributing authors and
xiv Preface the following referees for their time, patience, and expertise in providing peer reviews of chapters: Keller Autumn, Vincent Bels, Margaurite Butler, Sharon Downes, Patrick Gregory, Craig Guyer, Bill Mautz, Eric McElroy, Shannon O Grady, Chuck Peterson, Geoff Smith, Howard Snell, Jeff Thomason, Fritz Trillmich, Raoul Van Damme, and Mike Walton. Finally, we thank our institutions for some of the intangible support necessary in order to squeeze such a project into our day jobs. References Anderson, R. A. and Karasov, W. H. (1981). Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards. Oecologia 49, 67 72. Andrews, R. M. (1979). The lizard Corythophanes cristatus: an extreme sit-and-wait predator. Biotropica 11, 136 9. Butler, M. A. (2005). Foraging mode of the chameleon, Bradypodion pumilum: a challenge to the sit-and-wait versus active forager paradigm? Biol. J. Linn. Soc. 84, 797 808. Huey, R. B. and Pianka, E. R. (1981). Ecological consequences of foraging mode. Ecology 62, 991 9. Huey, R. B., Pianka, E. R. and Schoener, T. W. (1983). Lizard Ecology: Studies of a Model Organism. Cambridge, MA: Harvard University Press. McLaughlin, R. L. (1989). Search modes of birds and lizards evidence for alternative movement patterns. Am. Nat. 133, 654 70. Milstead, W. W. (1967). Lizard Ecology: A Symposium. Columbia, MO: University of Missouri Press. Perry, G. (1999). The evolution of search modes: ecological versus phylogenetic perspectives. Am. Nat. 153, 98 109. Pietruszka, R. D. (1986). Search tactics of desert lizards: how polarized are they? Anim. Behav. 34, 1742 58. Pianka, E. R. (1966). Convexity, desert lizards, and spatial heterogeneity. Ecology 47, 1055 9. Pianka, E. R. (1973). The structure of lizard communities. Ann. Rev. Ecol. Syst. 4, 53 74. Regal, P. J. (1978). Behavioral differences between reptiles and mammals: an analysis of activity and mental capabilities. In Behavior and Neurology of Lizards, ed. N. Greenberg and P. D. MacLean, pp. 183 202. Publication (ADM) 77 491. Washington, D.C.: Department of Health, Education, and Welfare. Schoener, T. W. (1969a). Models of optimal size for solitary predators. Am. Nat. 103, 277 313. Schoener, T. W. (1969b). Optimal size and specialization in constant and fluctuating environments: an energy-time approach. Brookhaven Symp. Biol. 22, 103 14. Schoener, T. W. (1971). Theory of feeding strategies. Ann. Rev. Ecol. Syst. 2, 369 404. Schwenk, K. (1994). Why snakes have forked tongues. Science 263, 1573 7. Toft, C. A. (1981). Feeding ecology of Panamanian litter anurans: patterns in diet and foraging mode. J. Herpetol. 15, 139 44. Vitt, L. J. and Pianka, E. R. (1994). Lizard Ecology: Historical and Experimental Perspectives. Princeton, NJ: Princeton University Press.