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I

BIOLOGY OF THE REPTILIA Edited by

CAALGANS The University of Michigan Ann Arbor. Michigan

VOLUME 16, ECOLOGY 8

DEFENSE AND LIFE HISTORY Coeditor for this volume

RAYMOND B. HUEY The University of Washington Seattle, Washington

Branta Books Box 3457

Ann Arbor, Ml 481 06

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Address all Inquiries to the Publisher Branta Books, Box 3457, Ann Arbor, MI 48106

Copyright © 1994 Branta Books Second Printing Under the conditions stated below the owner of copyright for this book hereby grants permission to users to make photocopy reproductions of any part or all of its contents for personal or internal organizational use, or for personal or internal use of specific clients. This consent is given on the condition that the copier pay the stated per-copy fee through the Copyright Clearance Center,lncorporated, 27 Congress Street, Salem, MA 01970, as listed in the most current issue of "Permissions to Photocopy" (Publisher's Fee List, distributed by CCC, Inc.), for copying beyond that permitted by sections 107 or 108 of the US Copyright Law. This consent does not extend to other kinds of copying, such as copying for general distribution, for advertising or promotional purposes, for creating new collective works, or for. resale.

Printed in the United States of America

Contents

CONTRIBUTORS

vii

PREFACE

ix DEFENSE

1. ANTIPREDATOR MECHANISMS IN REPTILES

1

Harry W. Greene

2. MIMICRY AND RELATED PHENOMENA Library of Congress Cataloging-in-Publication Data (Revised for vol. 16) Gans, Carl, 1923Bio1ogy of the reptilia. Vol. 14-15 published by: New York: Wiley; vol. 16published by: New York : Alan R. Liss. Coeditor for v. 16: R.B. Huey. Includes biobliographies and indexes. 869-06748 (v. 1) I. Reptiles-Collected works. I. Title.

QL641.G3

597.9

ISBN 0-84514402-2

153

F. Harvey Pough 3. CAUDAL AUTOTOMY AS A DEFENSE

235

E. N. Arnold

4. PARENTAL CARE IN REPTILES

275

Richard Shine

LIFE HISTORY

68-9113

5. METHODS FOR THE STUDY OF REPTILE POPULATIONS

331

Arthur E. Dunham, Peter J. Morin, and Henry M. Wilbur

6. UFE HISTORY EVOLUTION IN TURTLES Henry

M. Wilbur and Peter J. Morin v

387

I CONTENTS

vi

7. LIFE HISTORY PAnERNS IN SQUAMATE REPTILES

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441

Arthur E. Dunham, Donald B. Miles, and David N. Reznick

8. THE PHYSIOLOGICAL ECOLOGY OF REPTILIAN EGGS AND EMBRYOS

523

Gary C. Packard and Mary J. Packard

AUTHOR INDEX

607

SUBJECT INDEX

635

Contributors

E. N. ARNOLD, Department of Zoology, British Museum (Natural History), London SW7 5BD, England ARTHUR E. DUNHAM, Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104 HARRY W. GREENE, Museum of Vertebrate Zoology and Department of Zoology, University of California, Berkeley, California 94720 DoNALD B. MILES, Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania; present address: Department of Zoological and Biological Sciences, Ohio University, Athens, Ohio 45701 PETER J. MoRIN, Department of Zoology, Duke University, Durham, North Carolina 27706; present address: Department of Biological Sciences, Rutgers, The State University, Piscataway, New Jersey 08854 GARY C. PACKARD, Department of Zoology, Colorado State University, Fort Collins, Colorado 80523 MARY J. PACKARD, Department of Zoology, Colorado State University, Fort Collins, Colorado 80523 F. HARVEY PouGH, Laboratory of Functional Ecology, Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853 DAVID N. REZNICK, Department of Biology, University of California, Riverside, California 92521 RICHARD SHINE, Department of Zoology, University of Sydney, Sydney, New South Wales 2006, Australia HENRY M. WILBUR, Department of Zoology, Duke University, Durham, North Carolina 27706 vii

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Preface

The present volume of the Biology of the Reptilia is the second dedicated primarily to topics of ecology and behavior, although volumes 12 and 13 on physiological ecology obviously fit this area. Furthermore, volume 8 included chapters on venoms and envenomation and volumes 14 and 15 provided accounts of reproduction in crocodilians and turtles and in lepidosaurians, respectively. Also, the latter volume included accounts on parthenogenesis, viviparity, and autotomy mechanisms. The hiatus since the last volume dedicated to Ecology, which appeared in 1976, reflects mainly the untimely demise first of William W. Milstead and then of Donald W. Tinkle. The former had participated in the planning of the ecological components of the series and the latter had coedited the first volume and handled much of the initial contact with prospective authors of future ones. Consequently, I am delighted to have obtained the assistance of Dr. Raymond B. Huey as a colleague who had the knowledge, skill, and commitment to assume the associate editorship of the next volume on ecology. This second volume on Ecology contains chapters dealing with two major areas, namely the defensive behavior of reptiles and the parameters of reptilian life histories. Ancillary to these, but clearly associated, are accounts of reptilian parental care and the physiology and ecology of reptilian eggs. The first section begins with a widely ranging account of reptilian defensive behavior and is followed by chapters on mimicry and caudal autotomy, topics separated only because the extensive work permits their authors a much more detailed and informed discussion. The second section starts with a general account of methods for the study of ill

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PREFACE

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populations. Then follow specific accounts on turtles and squamates, as well as of their eggs. (We regret that logistic and scheduling problems forced omission of the account of crocodilians.) A technique section is included here for two reasons: First, because the series is intended to stimulate much-needed future work rather than merely reporting upon the past. The second is that over the last quarter century, the study of life history phenomena has encountered both a conceptual and a methodological revolution. The methods of the pioneers in the field have been tested repeatedly and sometimes have had to be superceded. The substantial work required to obtain meaningful data on aspects of life history had best benefit from the results of these tests rather than proceed with the use of classical, but now inadequate approaches. More than anything else, this volume documents the theme of diversity within the Reptilia. Such diversity might be expected in comparisons among turtles and sphenodontids, lizards and crocodilians; however, the degree of interspecific and intraspecific variability within each major reptilian group is important and significant. Analysis within such a framework requires knowledge of the full range of diversity, as well as an unusual breadth of viewpoint. Moreover, it requires parallel information about evolutionary and other biological principles, that lets the information be placed into perspective and thus generates a document that facilitates further study. This volume describes the multiple patterns utilized by these ectothermal amniotes and indicates some of the reasons why this group provides us with an unexcelled indicator of environmental diversity. Also it indicates that this diversity is as yet poorly characterized, so that many major phenomena remain to be discovered. From this viewpoint, we do not yet know enough about reptilian biology to make effective use of Krogh's principle, namely that there is an "optimum" species for the study of any biological phenomenon. I am very grateful to our contributors for their responsiveness to the comments of multiple reviewers and for their patience while awaiting the completion of the last-arrived manuscripts of the volume. I am again appreciative for George Zug's careful check of Latin names that permits us to refer to species by the currently appropriate terminology. It is my pleasure to acknowledge the assistance of R.B. Huey and of the large numbers of reviewers. Their efforts represent the key to the generation of volumes intended to remain useful to the herpetological, indeed the zoological community. At the risk of omitting some names we would like to mention R. A. Ackerman, A. Ananjeva, S. J. Arnold, A. d' A. Bellairs, J. F. Berry, D. G. Broadley, C. Carey, J. H. Carothers, B. Dial, R. Dmi'el, J. Endler, J. G. Frazier, J. W. Gibbons, A. E. Greer, L. Houck,

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F. Jaksic, A. R. Kiester, A. Muth, G. Pasteur, T. Pilorge, T. W. Schoener, R. A. Seigel, I. R. Swingland, J. R. G. Turner, L. Vitt, B. Wilson, as well as the authors of the several chapters. Several colleagues, identified in the captions, furnished pertinent photographs to illustrate the major topics. Ms. Katherine Vernon aided substantially with the correspondence. Finally, we appreciate the support of our institutions toward the ever increasing cost of postage and copying. CARLGANS

Ann Arbor, Michigan February 1987 '~

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CHAPTER

1 Antipredator Mechanisms in Reptiles

HARRY W. GREENE Museum of Vertebrate Zoology and Department of Zoology, University of California, Berkeley, California

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J INTRODUCTION

VII. PROBLEMS AND PROSPECTS

CONTENTS I. INTRODUCTION

II. PREDATION ON REPTILES

3

65

3

ADDENDUM

69

4

ACKNOWLEDGMENTS

69

REFERENCES

70

APPENDICES

112

A. Introduction, 4 B. Analysis by Region, 5 C. Analysis by Predator Taxa, 7

A. Some Records of Predation on Reptiles, 112

D. Injury Frequencies, 11

B. Defensive Behavior in Neonate Reptiles, 122

E. Natural and Manipulative Experiments, 12

C. Phenotypic Survey of Antipredator Mechanisms, 124

F. Some Generalizations, 12

D. Taxonomic Survey of Antipredator Mechanisms, 134

Ill. INTRASPECIFIC VARIATION IN ANTIPREDATOR MECHANISMS

14

A. Introduction, 14 B. Stimulus Control and Context, 15 C. Genetics and Ontogeny, 16 D. Intra- and lnterindividual Variation, 20

I. INTRODUCTION

E. Geographic Variation. 22

IV. SYSTEMATIC VARIATION IN ANTIPRI=DATOR MECHANISMS

24

A. Introduction, 24 B. Testudines, 25 C. Crocodilia, 27 D. Rhynchocephalia, 28 E. lguanian Lizards, 28

F. Gekkotan Lizards, 31 G. Autarchoglossan Lizards, 34 H. Amphisbaenia, 37

I. Serpentes, 37 J. Rattlesnakes, 45 V. EVOLUTION OF ANTIPREDATOR MECHANISMS

48

A. Function and Biological Roles, 48 B. Patterns and Processes, 57 C. Fossils, Anachronisms, and Recent Changes, 60

VI. REPTILES AND ANTIPREDATOR THEORY A. Reptiles as Study Organisms, 61 B. Optimality and Limits to Theory, 62 C. Some Generalizations, 63

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61

A great German herpetologist, Robert Mertens, published the first comprehensive review of reptilian antipredator mechanisms in 1946, and discussed them in terms of acoustic signals, chemical discharges, and other modes of expression. Although numerous brief descriptions of defensive behavior have appeared subsequently, only a few experimental studies and summaries of a more restricted nature have been published since Mertens' monograph. The present chapter surveys the nature and extent of predation on reptiles, and provides an updated review of their defensive mechanisms. With that perspective and the benefit of some recent advances in evolutionary biology, I then search for generalizations and address certain broader issues. The study of antipredator mechanisms was a prominent aspect of the post-Darwinian era in evolutionary biology (e.g., Cott, 1940), but, with the notable exception of mimicry (Pough, this volume), defense against predators remains a topic largely without conceptual foundation (Dingle, 1975; Janzen, 1981; Endler, 1986a). A truly comprehensive theory of antipredator mechanisms would enable us to predict structures and responses of an unstudied animal on the basis of other, known aspects of its biology. The extent to which such a general theory is possible and factors that might limit it are addressed in Section VI. The following remarks will orient the reader and provide an interim conceptual framework.

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ANTIPREDATOR MECHANISMS IN REPTILES

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5

PREDATION ON REPTILES

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This chapter is restricted to predation in a strict sense, i.e., the killing and consumption of another animal. Parasitism, scavenging, and predation on the eggs of reptiles (see Packard and Packard, this volume; Wilbur and Morin, this volume) are excluded on the grounds that they are not likely to influence the evolution of behavioral and external morphological aspects of organisms. With predation thus defined, defensive mechanisms can be considered in terms of the costs and benefits associated with searching for, pursuing, handling, and processing food. These components incorporate the probabilities of locating and capturing prey, the risk of injury or death to the predator, and the delay or nonperformance of other essential activities while feeding (Schoener, 1971; Griffiths, 1980; Greene, 1982). An antipredator tactic could work by raising any cost component to unacceptably high levels, or by deceptively indicating higher costs and/or lower benefits than a predator would "willingly" accept. Section II reviews predation on reptiles, as background for understanding antipredator mechanisms. Ethology has traditionally recognized four major issues regarding behavior, viz., development within an individual, sensory and motivational control, evolutionary history, and ecological consequences (Tinbergen, 1963). Parallel questions also are posed with respect to morphological and physiological features of organisms (Gans,"1974; Liem and Wake, 1985), and they highlight important areas that have been largely overlooked in the study of antipredator mechanisms. Factors affecting the individual expression of defensive attributes and intraspecific variation are discussed in Section III. There follows a systematic analysis of variation among species and higher taxa in Section IV and a discussion of the evolution of anti predator mechanisms in Section V. Records of predation on specific taxa in nature, a sur-vey of defensive behavior in neonate reptiles, a descriptive catalogue of antipredator mechanisms, and a taxonomic review are provided in the Appendices. Case studies are emphasized throughout this chapter and, whenever possible, conceptual discussions are biased toward reptiles as examples. Occasional mention is made of unpublished observations, because they influenced my perspective and in hopes that they will inspire more detailed research. Autotomy (Arnold), mimicry (Pough), and parental care (Shine) are dealt with elsewhere in this volume. II. PREDATION ON REPTILES A. Introduction

The kinds and numbers of potential predators involved, the ways in which they interact with prey, and the energetic and reproductive

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consequences of those interactions are necessary parameters for understanding the ecological and evolutionary significance of antipredator mechanisms. The interaction itself is a "behavioral couple" that can vary irrespective of morphological features of predator and prey (Greene, 1982, 1986a). Energetic consequences of the interaction might reflect the roles of morphological and physiological constraints on predators and/or prey (Pough, 1983; Huey and Bennett, 1986), and might figure heavily in the future fitness of both organisms. Reproductive consequences of an encounter are the ultimate measures of fitness for both predator and prey. An evaluation of antipredator mechanisms requires knowledge of actual predation on the prey species of interest, as well as of predator taxa that are not eating it because the encounter would be too "expensive." The latter information can suggest profitable experiments and appropriate interpretations of the behavior. For example, coatis (Nasua narica) and peccaries (Tayassu tajacu) were used as experimental predators of coral snake models (Gehlbach, 1972). Although those sympatric mammals are not known to prey upon venomous coral snakes, they do eat small, cryptic vertebrates, and Gehlbach's data demonstrated that coatis and peccaries actually avoid coral snakes (Greene and McDiarmid, 1981: Note 76). Several sources of information on predation are potentially available, although relatively few data can be applied conclusively to questions about the evolution of antipredator mechanisms. These sources are discussed below, and include autecological studies of hunting techniques and diets, dietary analyses of entire communities of predators, comparative surveys of injury frequencies, and natural and manipulative experiments. Specific records of predation on reptiles in nature are given in Appendix A, and brief summaries for higher taxa are in Section IV. B. Analysis by Region

Animals and their defensive mechanisms evolve in a community context. Work on marine invertebrates (Vermeij, 1978, 1982), poeciliid fishes (Endler, 1978, 1983), and other organisms (e.g., Moynihan, 1971; Maiorana, 1976) underscores the importance of studying simultaneously predation and antipredator responses in geographic and temporal terms. An especially pertinent example is the suggestion that the large biomass of herbivores and carnivores depresses species richness and overall abundance of reptiles in Africa relative to the neotropics Oanzen, 1976). That complex proposal was based on indirect evidence and crude measures of reptilian densities at African and neotropical sites (see

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ANTIPREDATOR MECHANISMS IN REPTILES

criticisms by Kreulen, 1979, and response by Janzen, 1979). Nevertheless, the hypothesis might explain a major pattern in vertebrate geographical ecology, and thereby illustrates the potential value of comparative studies of predation. A few surveys examine the diets of several sympatric predators, usually within a narrow taxonomic focus. Among 29 species of raptors in Surinam, at least six feed frequently on reptiles and at least eight feed occasionally on lizards and snakes. Of those, the laughing falcon (Herpetotheres cachinnans) specializes on snakes and the gray hawk (Buteo nitidus) takes many lizards (Haverschmidt, 1962; Voous, 1969). In Africa, at least 20 of 89 species of diurnal raptors and 2 of 30 species of owls feed only or in part on reptiles, and their collective diets encompass an impressively large number of species (Brown, 1971; Broadley, 1974). For example, 8 secretary birds (Sagittarius serpentarius) contained 61 reptilian prey, including a tortoise, 57 lizards of 6 genera and 11 species, and 1 each of 3 species of snakes. Forty-four reptiles eaten by brown snake eagles (Circaetus cinerus) included a Chamaeleo dilepis, a Varanus niloticus, an Agama sp., and 41 snakes, among which were numerous large, venomous species (Bitis arietans, Dendroaspis polylepis, Naja mossambica; Broadley, 1974). Reptiles are uncommon in the diets of most of 15 species of medium and large carnivores in southern Africa, but several of those predators might have important impact on them (Pienaar, 1969; Broadley, in litt.). Land tortoises (Geochelone pardalis, Kinixys belliana) and water turtles (Pelusios sinuatus, P. subrufa) are eaten by lions (Panthera leo) and two species of hyaenas (Crocuta crocuta, Hyaena brunnea), and the aquatic turtles are eaten commonly by Crocodylus niloticus as well. Python sebae is eaten by lions and leopards (Panthera pardus). In contrast, the smaller African carnivores are regular predators on reptiles. These include a small cat, Felis libyca; all of the canids except wild dogs; all mustelids other than otters; and all viverrids except two insectivorous mongooses (Broadley, in !itt.). Most predation is evidently opportunistic (e.g., an amphisbaenian, ten species of lizards, and four species of snakes in the diet of F. libyca; a tortoise, an amphisbaenian, eight species of lizards, and nine species of snakes eaten by Canis mesomelas), but sometimes predators gorge on particular species or the inhabitants of particular microhabitats. A badger, Mellivora capensis, had eaten 22 geckos, Ptenopus garrulus, as well as an amphisbaenian, rodents, and scorpions. One mongoose, Paracynictis selousi, contained 18 burrowing skinks, Panaspis wahlbergii; 3 lacertids, Nucras taeniolata; 3 snakes, including 2 Lycophidion capense and an Atractaspis bibroni; plus a frog, rodents, and crickets.

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PREDATION ON REPTILES

Comprehensive dietary surveys of entire assemblages of sympatric predators (rather than taxonomic subsets) are available for only four localities, three of them in Mediterranean-type habitats of Spain (Valverde, 1967), Chile (Jaksic et al., 1982), and California (a series of papers by Fitch and colleagues, cited in Jaksic et al., 1982). Among those sites, the overall importance of reptiles as prey is lowest in Chile, intermediate in California, and highest in Spain. The incidence of predation on a species is correlated with its relative abundance in Spain and California, but not in Chile. Behavioral and morphological attributes apparently make some prey species more vulnerable to capture (e.g., a large colubrid snake, Philodryas chamissonis, in Chile) and others less so (e.g., a very fast teiid lizard, Callopistes maculatus, in Chile; a venomous rattlesnake, Crotalus viridis, in California) than their abundances would predict. In an assemblage of more than 100 sympatric vertebrate predators at Finca La Selva, Costa Rica, a katydid, 2 frogs, 2 lizards, at least 17 snakes, 10 raptors, and 2 mammalian carnivores feed on reptiles. Preliminary data from that locality indicate that most lizards and snakes, particularly smaller species, face the threat of a wide variety of avian, mammalian, and snake predators (van Berkum et a!., 1986; Greene, 1987; Greene, Donnelly, Guyer, and Santana, unpubl.). C. Analysis by Predator Taxa 1. INVERTEBRATES

Although reptiles frequently prey on invertebrates, the reverse is rarely true. Most cases of arthropod predation on terrestrial and aquatic reptiles represent occasional attacks on small individuals by predator species that usually eat other invertebrates, but exceptions exist (see McCormick and Polis, 1982, for a review). Some large centipedes, spiders, and scorpions eat vertebrates, and reptiles are apparently an important part of the diet of a few species. Scorpions are abundant in parts of arid western North America, and blind snakes, Leptotyphlops humilis, sometimes form as much as 10% of their diets (McCormick and Polis, 1982). Spiders prey on small snakes (Groves and Groves, 1978; McCormick and Polis, 1982), a mantid ate a gecko (Wright, 1982), a crab caught a hatchling king cobra (Wall, 1926a), a water bug ate a garter snake (Drummond and Wolfe, 1981), and centipedes often eat Galapagos lava lizards (Snell, in !itt.). The prevalence of large, predatory invertebrates in the leaf litter of lowland tropical forests might account for the paucity of small reptiles in those habitats (Myers

8

ANTIPREDATDR MECHANISMS IN REPTILES

and Rand, 1969), but more information on the geographic incidence of arthropod predation on small litter vertebrates is needed to evaluate that hypothesis. Marine reptiles are also preyed upon by invertebrates. A large octopus was found eating a medium sized sea turtle, Eretmochelys imbricata, and flipper damage to other sea turtles might have been caused by octopi (Buxton and Branch, 1983). Crabs probably are prominent predators on hatchling sea turtles throughout the world (e.g., Stancyk, 1981; Frazier, 1984; Cornelius, 1986). 2. FISHES

Relatively few reptiles are aquatic or marine, and predatory fish are probably rarely important in the evolution of reptiles (see Section V.A). The diet of a chub includes terrestrial iguanid lizards, Sceloporus spp. (Neve, 1976); a large catfish had an African viper, Bitis arietans, in its stomach (Thorne and Hamman, 1981); a 3-kg African fish contained a 2-m long black mamba (Dendroaspis polylepis, Broadley, 1983); and a large Amazonian fish had eaten two blind snakes, Leptotyphlops macrolepis (Goulding, 1980). Four Thamnophis sirtalis and one Storeria occipitomaculata were found in 1724 bass (Micropterus salmoides) stomachs in Michigan (Knapik and Hodgson, 1986). An eel (Anquilla rostrata) regurgitated two hatchling musk turtles, Sternotherus odoratus, that survived the encounter (Pough, in litt.). · Six species of sharks take considerable numbers of sea snakes in the waters off Australia, and also perhaps catch them elsewhere (Heatwole, 1975). On rare occasions marine bony fishes eat Pelamis platurus, a surface-feeding sea snake (Pickwell et al., 1983), as well as other marine elapids (Heatwole, 1975). Sharks might pose a significant threat to sea turtles (Stancyk, 1981; Cornelius, 1986) and Galapagos marine iguanas (Amblyrhynchus cristatus, Carpenter, 1966). A single dolphin contained nine young sea turtles of two species (Whitham, 1974). 3. AMPHIBIANS

Most amphibians are not predators on reptiles. The few caecilians that have been studied feed mainly on invertebrates (Wall, 1922; Bemis et al., 1983); an Ameiva undulata and an Anolis dollfusianus in the stomach of a Dermophis mexicanus are the only records of predation on vertebrates by those limbless, tropical amphibians (Moll and Smith, 1967). The only records of predation on wild reptiles by salamanders are of Siren intermedia on a snake, Regina alieni (Godley, 1982); of Dicamptodon ensatus

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PREDATION ON REPTILES

on an iguanid lizard, Sceloporus occidentalis (Bury, 1972); and of Ambystoma tigrinum on a teiid lizard, Cnemidophorus sexlineatus (Camper, 1986). Dicamptodon ensatus is probably the only salamander in the world that regularly eats terrestrial vertebrates in the field. Most frogs are insectivorous and too small to prey on vertebrates, but there are some interesting exceptions. Rana catesbeiana in North America (Minton, 1949; Clarkson and de Vos, 1986), Leptodactylus pentadactylus (Hoogmoed, 1980) in the neotropics, and Pyxicephalus adspersus in Africa (Branch, 1976) eat snakes, including highly venomous species in the first and last cases. A Bufo terrestris ate a brightly colored colubrid snake, Cemophora coccinea (Brown, 1979); a Rana warschewitchii regurgitated a small iguanid lizard, Anolis humilis (Greene, Donnelly, Guyer, and Santana, unpubl.); and a R. grylio ate an Eumeces laticeps (Lamb, 1984). Asiatic B. melanostictus commonly eats blind snakes (Hahn, 1976). Aquatic turtles occasionally fall prey to frogs (Graham, 1984), as do baby Alligator mississippiensis (Neill, 1971). 4. REPTILES

The sole living sphenodontid, Sphenodon punctatus, feeds on a variety of prey, including lizards (Cans, 1983a), but the few sympatric geckos and skinks are not a major part of its diet. Apparently few turtles consume other reptiles in the field, but Macroclemys temminckii is an important predator on other turtles (Pritchard and Trebbau, 1984). Captive observations suggest that a few other species also might eat reptiles in nature (e.g., Terrapene ornata, Legler, 1960). Crocodilians feed on a variety of invertebrates and vertebrates, including turtles, lizards, and snakes. Crocodylus niloticus even eats highly venomous puff adders, Bitis arietans (Cott, 1961). Alligator mississippiensis (Neill, 1971) and C. niloticus (Pienaar, 1969) frequently eat turtles, and several neotropical species occasionally feed on turtles, lizards, and snakes (Alvarez el Toro, 1974; Medem, 1981). Crocodylus palustris sometimes eats sea snakes and marine turtles (Allen, 1974). No crocodilian specializes on reptiles as prey. Most lizards feed mainly or entirely on arthropods, but some occasionally eat other vertebrates and a few are reptile specialists (for general discussion, see Greene, 1982). Species that feed frequently on other lizards include two large teiids of the genus Callopistes (pers. obs.), the iguanid Gambelia wislizeni (Tanner and Krogh, 1975; Parker and Pianka, 1976), the pygopodid Lialis burtonis (Patchell and Shine, 1986), and several species of Australian varanids (e.g., Pianka, 1986; Losos and Greene, unpubl.).

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ANTIPREDATOR MECHANISMS IN REPTILES

Snakes are probably important predators on lizards in many regions (e.g., Shine, 1977, for Australia; McKinney and Ballinger, 1966, for Texas; Fitch, 1949, for California; Duellman, 1978, for Ecuador; Henderson, 1984a, for the West Indies). Some species specialize o~ other snakes (e.g., Ophiophagus hannah, M. A. Smith, 1943; Cylindrophis rufus, Greene, 1983a; Micrurus fulvius, Greene, 1984) or amphisbaenians (Broadley, 1963; Papenfuss, 1982). A few species of snakes occasionally feed on turtles (e.g., Drymarchon corais, Ruthven, 1912; Agkistrodon piscivorus, Burkett, 1966) and/or crocodilians (e.g., A. piscivorus, Allen and Swindell, 1948; Eunectes murinus, Wehekind, 1955; an unidentified Eocene henophidian, Greene, 1983a).

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PREDATION DN REPTILES

rous bats eat nocturnal geckos and diurnal agamid and iguanid lizards (Goodwin and Greenhall, 1961; Douglas, 1967; Tuttle, 1967; Valdez and LaVal, 1971; Vaughn, 1976; Advani, 1981). Sea turtles, especially small individuals, are prey to a variety of terrestrial and marine mammals (Stancyk, 1981). Numerous other mammals in several orders prey occasionally on lizards, amphisbaenians, and snakes (e.g., wild pigs, Sus scrofa, Valverde, 1967) and even adult crocodilians are sometimes taken by lions (Panthera leo, Cott, 1961; Pienaar, 1969) and jaguars (P. onca, Alvarez del Toro, 1974). Nesting females of large arboreal lizards, Iguana iguana, are seasonally important prey for jaguars in northeastern Costa Rica (Greene, Santana, and Braker, unpubl.). A bear (presumably Ursus arctos) perhaps tried to eat a Testudo graeca (Reed and Marx, 1959).

5. BIRDS D. Injury Frequencies

Birds are often enemies of reptiles throughout the world, and at many sites there exists an array of emphasis ranging from occasional to very frequent predation. SpeCies that eat reptiles regularly, at least at times, include the secretary bird (Sagittarius serpentarius) and several other African raptors (Brown, 1971; Sweeney, 1971; Broadley, 1974), roadrunner (Geococcyx californicus, Bryant, 1916; Meinzer, 1983), and numerous tropical hawks (Haverschmidt, 1962; Voous, 1969; Greene, Donnelly, Guyer, and Santana, unpubl. ). Herons eat many young crocodilians (Alvarez del Toro, 1974; Gorzula, 1985), and pelicans can eat moderately large land turtles (Land, 1931). Several species of marine raptors eat sea snakes (Heatwole, 1975), and a variety of birds eat young sea turtles (Stancyk, 1981). Although many diurnal reptiles are probably safe from nocturnal raptors, by virtue of the use of retreats,. some owls regularly take nocturnal gekkonid lizards (Demeter, 1982). In addition to specialists on reptiles, many other birds occasionally or frequently eat them, including shrikes, jays, toucans, puffbirds, cuckoos, and others (for old but still useful reviews of bird predation on snakes, see Wall, 1906a; Guthrie, 1932). 6. MAMMALS

Few mammals regularly take reptiles as prey; examples include some viverrids (Broadley, in litt.), neotropical mustelids (Galictis sp., Jackson, 1979; Rodda and Burghardt, 1985), some foxes (e.g., Vulpes macrotus, pers. obs.), badgers (Klauber, 1956; Messick and Hornocker, 1981; Kruuk and Mills, 1983; Broadley, in litt.), and some primates (Gans, 1964, 1965; Lorenz, 1971). Hyaenas in South Africa frequently eat tortoises, "easily cracking their shells" (Pienaar, 1969). Several carnivo-

Scars and missing body parts do not necessarily index the intensity of successful predation (Schoener, 1979; Jaksic and Greene, 1984; Arnold, this volume), but they can provide a minimum estimate of successful escape from predators (Greene, 1973a), assuming no injuries due to social encounters, mishaps, or illness (Vitt et al., 1974; Khan and Tasnim, 1986a). Injuries are thus potential indicators of predator-prey interactions, both in terms of the frequency and nature of the wounds. Predation is widely assumed to be an ali-or-none phenomenon for prey, although unsuccessful predation is clearly essential for the evolution of antipredator mechanisms (Vermeij, 1982). Observations of encounters and scars indicate that reptiles often confront formidable enemies, incur injuries, and escape. I have found adult iguanid lizards (Callisaurus draconoides, Iguana iguana) with large, healed body scars. A small colubrid snake (Diadophis punctatus) that survived more than 5 minutes of mouthing by a captive kit fox (Vulpes macrotus) was seemingly healthy 2 weeks later (pers. obs.). Recovery from serious wounds has also been reported for Sternotherus odoratus (Ernst, 1986), Terrapene coahuila (Brown, 1974), T. ornata (Legler, 1960), Phrynops zuliae (Pritchard and Trebbau, 1984), Crocodylus niloticus (Cott, 1961), Sauromalus obesus (Camp, 1916; Berry, 1974), Eumeces obsoletus (Fitch, 1955), Coluber constrictor (Brunson, 1986), Pituophis melanoleucus (Brunson, 1986), Xenochrophis piscator (Auffenberg, 1980), and several species of sea snakes (Heatwole, 1975). The abilities of reptiles to survive serious injuries from a predator has relevance for the efficacy and mechanisms of defense. The responses to danger work because the prey push the costs of predation above an acceptable level, or because they deceive a predator about the magni-

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ANTIPREDATOR MECHANISMS IN REPTILES

tude of the costs. Because escape from predators can be accomplished despite actual physical contact, the dynamics of an encounter might influence the behavior of a reptile and a predator in subsequent interactions, but the extent to which this occurs in nature is unknown (see Section III.C). E. Natural and Manipulative Experiments

Reptiles have existed on some small, isolated islands in the near or total absence of predation for long periods, and numerous cases demonstrate unusual tameness in those animals (e.g., Anolis agassizi, Rand et al., 1975). The mechanisms producing such behavior (e.g., selection, habituation) remain unstudied (see Sections III.C, V.C). Modern introductions provide valuable information on the negative impact of predators on populations of prey that are not capable of defense against them. The arrival of armadillos (Dasypus novemcinctus) in peninsular Florida during recent decades occurred contemporaneously with the disappearance of appropriate predators on those generalist hunters, and the result has been a marked reduction in the abundance of leaf litter organisms, including small n;ptiles (Carr, 1982; see also Redford, 1985; Greene, 1987). Introductions of mongoose and feral cats have had severe effects on the reptilian faunas of several Caribbean islands. In a particularly well documented case, the introduction of dogs and cats on a small island devastated a population of large iguanid lizards, Cyclura carinata, in 3 years {Iverson, 1978). Although widely assumed to be a major source of mortality for many reptiles, the impact of predation on population parameters is poorly known (see Dunham et al., this volume). Experimental exclusion of predators significantly increases the survivorship of particular phenotypes of Uta stansburiana (Ferguson and Fox, 1984). F. Some Generalizations

Reptiles are subject to a wide range of predators, although the risks vary geographically as well as among predator taxa at a locality. Even species that might be expected to be relatively free of enemies are eaten, such as those that are predominantly nocturnal (many geckos), aquatic (crocodilians, many turtles), fossorial (amphisbaenians, scolecophidian snakes), heavily armored (cordylid lizards, tortoises), or highly venomous (Bitis, Naja). Studies of experimental populations, of reptiles subject to introduced predators, and of island reptiles underscore the widespread potential importance of predation as a factor in the lives of these

PREDATION ON REPTILES

13

animals. Brief speculation regarding the kinds of problems with which reptiles must contend-the sensory and prey-handling characteristics of their predators-is possible from the information presented above, but generalizations are necessarily broad and tentative. Birds and mammals probably often are the most significant potential factors in the evolution of antipredator mechanisms in reptiles, for several reasons. They are by and large visually hunting predators, although some, especially mammals, are also guided by auditory and chemical cues. Many birds possess particularly acute vision, and thus are particularly likely to circumvent crypsis (Section V.A). Parent birds and mammals often transport immobile, intact prey as food for their offspring, making lack of movement subsequent to capture (i.e., failure to elicit additional prey immobilization tactics) a potentially viable defense option (see Sections V.A, VI. B). Birds and mammals have high metabolic rates and high daily energy needs, such that their consumption rates and impact on a prey population can be high even if the latter constitutes a small part of the overall diet. Snakes frequently prey on lizards and, to a lesser extent, on other snakes. Although some species appear to have good vision, many rely heavily on chemical cues to locate prey (Burghardt, 1970) and usually begin consuming prey while it is immobilized (e.g., Klauber, 1956; Greene, 1984). At equivalent densities, the impact of snakes and other ectotherms on prey populations will be far less than that of endothermic predators. Probably most terrestrial vertebrate predators are capable of solving at least moderately complex learning problems (see Burghardt, 1977a, for a review of learning in reptiles). The available evidence suggests that many birds and mammals take species within a broad prey type (e.g., size, higher taxon) and roughly in proportion to their abundances Oaksic, 1986), although some might avoid preferentially certain dangerous (e.g., Crotalus viridis, Fitch 1949) or particularly fleet (e.g., Callopistes maculatus, Jaksic et al., 1982) species. Some snakes also might feed indiscriminantly on abundant reptiles, but most species probably specialize on a few prey taxa (e.g., certain African burrowing snakes that eat exclusively amphisbaenians, Broadley, 1963; see also Arnold, 1972; Savitzky, 1983). Some predators are "hunting habitat specialists" that feed frequently on reptiles as well as on any other appropriately sized, palatable organisms that they encounter. The neotropical crane-hawk (Geranospiza caerulescens) systematically searches bromeliads and holes in trees for large insects, frogs, lizards, snakes, and nestling birds (Sutton, 1954; Alvarez del Taro, 1971; Bokermann, 1978). Jamaican cuckoos (Saurothera vetula), crows (Corvus jamaicensis), and becards (Platypsaris niger) hunt for

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ANTIPREDATOR MECHANISMS IN REPTILES

anoles and other prey in bromeliads (Cruz, 1972, 1973, 1975). Nocturnal lyre snakes (Trimorphodon spp.) hunt in crevices for resting diurnal iguanid lizards (pers. obs.), and coral snakes (Micrurus spp.) search for small reptilian prey in leaf litter (Greene, 1973b, 1984). African honey badgers (Mellivora capensis) locate a variety of prey, including many lizards and snakes, by digging at the bases of bushes (Kruuk and Mills, 1983; Broadley, in litt.). Such predators present a constant threat to otherwise hidden, inactive animals (e.g., sleeping iguanids at night, quiescent geckos during the day), implying that selection of retreat site might be an important antipredator mechanism. In summary, many reptiles, perhaps especially diurnal forms that are active above ground, potentially face a large number of predators with diverse prey detection and handling capabilities. Diurnal species may be vulnerable in the daytime to one set of enemies that perceive them visually and precipitate a chase,· and to another set that use chemical cues to locate their retreats at night and simply seize the immobile prey. For example, a diurnal desert lizard, Cnemidophorus tigris, may be eaten by kestrels (Falco sparverius), roadrunners, and coachwhip snakes (Masticophis flagellum) during the day, and dug from its burrows by badgers (Taxidea taxus) and long-nosed snal