Feeding: Form, Function and Evolution in Tetrapod Vertebrates

Feeding Form,. Function, and Evolution in Tetrapod Vertebrates

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Feeding Form, Function, and Evolution in Tetrapod Vertebrates Edited by

Kurt Schwenk Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut

:#) San Diego

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ACADEMIC PRESS A Harcourt Science and Technology Company

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Cover photographs: (Inset) Harry W. Greene, © 1999. (Background) Nirvana Filoramo, © 2000. This book is printed on acid-free paper.

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Copyright © 2000 by ACADEMIC PRESS All lights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher. Requests for permission to make copies of any part of the work should be mailed to: Permissions Department, Harcourt Inc., 6277 Sea Harbor Drive, Orlando, Florida 32887-6777

Academic Press A Harcourt Science and Technology Company 525 B Street, Suite 1900, San Diego, California 92101-4495, USA http: / / www.academicpress.com

Academic Press Harcourt Place, 32 Jamestown Road, London NWl 7BY, UK http: / /www.academicpress.com Library of Congress Catalog Card Number: 99-63490 International Standard Book Number: 0-12-632590-1 PRINTED IN THE UNITED STATES OF AMERICA 00 01 02 03 04 05 EB 9 8 7 6 5

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To my teachers: Warren F. Walker, Jr., James R. Stewart, and Marvalee H. Wake

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Contents

Contributors Preface xiii

IV. Kinematics of Feeding: Feeding Stages V. Concluding Remarks 55 References 55

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S E C T I O N S E C T I O N

I

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INTRODUCTION

AMPHIBIA

C H A P T E R C H A P T E R

Tetrapod Feeding in the Context of Vertebrate Morphology

Aquatic Feeding in Salamanders STEVEN M. DEBAN AND DAVID B. WAKE

KURT SCHWENK

I. II. III. IV. V.

I. Introduction 3 11. Approaches to the Study of Tetrapod Feeding 5 III. Concluding Comments 16 References 16

C H A P T E R

Introduction 65 Morphology 68 Function 82 Diversity and Evolution 88 Opportunities for Future Research References 92

92

C H A P T E R

An Introduction to Tetrapod Feeding

Terrestrial Feeding in Salamanders

KURT SCHWENK

DAVID B. WAKE AND STEPHEN M. DEBAN

I. Introduction 21 II. Morphology of the Feeding Apparatus III. Kinematics of Feeding:The Gape Cycle

I. Introduction 95 II. Morphology 97 III. Function 101

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IV. Diversity and Evolution 111 V. Opportunities for Further Research References 114

S E C T I O N

114

IV REPTILIA: LEPIDOSAURIA

C H A P T E R

C H A P T E R

Feeding in Frogs

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KIISA C. NISHIKAWA

I. II. III. IV. V. VI. VII.

Introduction 117 Morphology of the Feeding Apparatus 119 Function of the Feeding Apparatus 124 Neural Control of Prey Capture 135 Evolution of the Feeding Apparatus 139 Conclusions 143 Current and Future Directions 144 References 144

C H A P T E R

Feeding in Lepidosaurs KURT SCHWENK

I. Introduction 175 II. Lepidosaurian Phylogeny and Classification 176 III. Natural History 178 IV. Morphology of the Feeding Apparatus 189 V. Feeding Function 220 VI. Specialized Feeding Systems 257 VII. Evolution of Feeding in Lepidosaurs 264 VIII. Future Directions 277 References 278

C H A P T E R

Feeding in Caecilians JAMES C. O'REILLY

I. 11. III. IV. V

Feeding in Snakes

Introduction 149 Morphology 150 Function 155 Evolution 161 The Future 163 References 164

DAVID CUNDALL AND HARRY W. GREENE

I. II. III. IV. V.

Introduction 293 Form and Function 301 Performance and Size 322 Evolution 322 Concluding Remarks 326 References 327

S E C T I O N

III REPTILIA: TESTUDINES

S E C T I O N

V REPTILIA: ARCHOSAURIA

C H A P T E R C H A P T E R

A Bibliography of Turtle Feeding KURT SCHWENK

I. Introduction II. Bibliography

169 169

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Feeding in Crocodilians

JOHAN CLEUREN AND FRITS DE VREE

I. Introduction II. Morphology

337 340

Contents III. Function 347 IV. Evolution 354 References 357

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V. The Feeding Apparatus 421 VI. Feeding Function 439 VII. Control of Feeding Behaviors 444 References 444

C H A P T E R C H A P T E R

11 Feeding in Paleognathous Birds CAROLE A. BONGA TOMLINSON

14 The Ontogeny of Feeding in Mammals R. Z. GERMAN AND A. W. CROMPTON

I. 11. III. IV. V

Introduction 359 Materials and Methods 360 Morphology of the Hyolingual Apparatus 361 Function of the Hyolingual Apparatus 373 Evolution of the Feeding System 384 References 390

C H A P T E R

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I. II. III. IV. V.

Introduction 449 Morphology 449 Function and Mechanics of Suckling 450 Rhythmicity and Control of Suckling 453 Coordination of Swallowing and Respiration 455 VI. Transition from Suckling to Drinking at Weaning 455 VII. Evolutionary Considerations 456 References 456

Feeding in Birds: Approaches and Opportunities

C H A P T E R

MARGARET RUBEGA

I. Introduction 395 II. Patterns of Analysis III. Conclusion 406 References 406

396

S E C T I O N

VI MAMMALIA

15 Feeding in Myrmecophagous Mammals KAREN ZICHREISS

I. II. III. IV. V.

Introduction 459 Foraging Ecology 462 Morphology of the Feeding Apparatus 464 Functional Morphology 475 Evolution of Myrmecophagous Specializations 478 VI. Directions for Future Research 480 References 481

C H A P T E R

C H A P T E R

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Feeding in Mammals

Feeding in Marine Mammals

KAREN M.HIIEMAE

ALEXANDER WERTH

I. Introduction 411 II. Mammalian Feeding System 414 III. The "Process Model" for Mammalian Feeding 416 IV. Mechanical Properties and Textures of Foods 419

I. Introduction 487 II. Feeding Strategies 492 III. Conclusions 521 References 521 Index

527

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Contributors

Kiisa C. Nishikawa (117) Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona 86011. James C. O'Reilly (149) Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts 01003. Karen Zich Reiss (459) Department of Biological Sciences, Humbolt State University, Areata, California 95521. Margaret Rubega (395) Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269. Kurt Schwenk (3, 21,169,175) Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269. Carole A. Bonga Tomlinson (359) Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138. David B. Wake (65,95) Museum of Vertebrate Zoology, University of California, Berkeley, California 94720. Alexander Werth (487) Department of Biology, Hampden-Sydney College, Farmville, Virginia 23901.

Numbers in parentheses indicate the pages on which the authors' contributions begin.

Johan Cleuren (337) Department of Biology, University of Antwerp, B-2610 Antwerp, Belgium. A. W. Crompton (449) Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138. David Cundall (293) Department of Biological Sciences, Lehigh University, Bethlehem, Pennsylvania 18015. Frits De Vree (337) Department of Biology, University of Antwerp, B-2610 Antwerp, Belgium. Stephen M. Deban (65, 95) Museum of Vertebrate Zoology, University of California, Berkeley, California 94720. Rebecca Z. German (449) Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221. Harry W. Greene (293) Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853. Karen M. Hiiemae (411) Department of Bioengineering and Neuroscience, Institute for Sensory Research, Syracuse University, Syracuse, New York 13244.

XI

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Preface

This book addresses the first of these challenges. It examines in depth and breadth the myriad solutions to the essential problem of feeding in one clade of animals. It summarizes and synthesizes for the first time in 15 years our burgeoning knowledge of tetrapod feeding systems and how they have evolved. It explores the "variations on a theme" in this system and in so doing provides grist for evolutionary theorists. However, its proximate goals are more modest. The book is intended to instruct novice morphologists and others interested in animal form and function. It is both an introduction to the field and a presentation of the "state of the art." It is aimed at advanced undergraduate and gradutate students, as well as experts in the field who wish to delve outside their taxonomic bounds. It provides an accessible entree into an exploding literature and showcases our impressive knowledge—but it highlights also our great ignorance. As Rubega points out in Chapter 12, there are many dissertations on tetrapod feeding left to be written. The greatest possible outcome I can imagine for this book is that it will stimulate and provoke the next generation of morphologists to fill in the gaps and shoot down the dogma. In an effort to promote its utility to students, the book begins with two introductory chapters that establish the conceptual, historical, and factual contexts within which the empirical chapters can be interpreted. The empirical chapters provide a more-or-less phylogenetic survey of tetrapod vertebrate feeding systems. Although a phylogenetic approach is emphasized throughout, there are some cases in which I judged other criteria to be more useful in organizing current knowledge. Hence, some chapters are not limited to a monophyletic taxon, but are based on functional types (e.g., "marine mammals," Chapter 16), dietary types (e.g., "myrmecophagous mammals," Chapter 15), or the medium in which feeding occurs (e.g., "aquatic

Vertebrate morphology stands accused of failing to contribute meaningfully to the neo-Darwinian evolutionary synthesis. Although I strongly doubt this (see Chapter 1), I nonetheless take it as a challenge for the future. Our evolutionary theory is at a cusp—the power and efficacy of reductionism are undeniable, but equally so is its failure to deal effectively with intrinsic, organismal attributes. Despite leaps and bounds in our understanding of genetic- and population-level evolutionary phenomena, we remain almost embarrassingly ignorant about the fundaments of phenotypic evolution. Answers to the most basic questions are beyond our grasp: Why do some lineages evolve rapidly while others remain static? How do complex systems full of interacting characters evolve? And once evolved, how can they change? Our approaches to these questions are often simplistic and too facile. We point to "phylogenetic constraint," for example, as if it explains the failure of a lineage to evolve in some expected way when, in fact, it does little more than describe our ignorance. What is the mechanistic basis of phylogenetic constraint? Is it all just genetic background, or are there phenotypic processes that interfere with diversification and adaptive evolution or that facilitate it? Organisms are multihierarchical, complex systems, and as in other such systems, each level expresses emergent properties that are unpredictable, even unknowable, from the vantage point of other levels. If we want to understand the principles governing the evolution of phenotypes, it is logical, indeed, necessary to study the phenotype directly. Who better to do this than morphologists? The challenge to vertebrate morphology in the next century is therefore twofold: to develop the empirical database and conceptual tools needed to create a phenotypebased evolutionary theory, and to forge a new evolutionary synthesis by integrating this theory with the gene-based, neo-Darwinian paradigm.

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Preface

feeding in salamanders/' Chapter 3). Each chapter is authored by an expert or experts on the group, including both veteran and younger workers. I am very pleased to be able to include chapters on little-known groups, such as caecilian amphibians (Chapter 6), crocodilians (Chapter 10), paleognathous birds (Chapter 11), myrmecophagous mammals (Chapter 15), and marine mammals (Chapter 16). However, my goal of complete taxonomic coverage of all tetrapods was not quite achieved. Owing to many factors, a chapter on turtle feeding could not be completed. To mitigate this taxonomic breach, I have prepared a brief bibliography of turtle feeding to serve as an entree into the literature (Chapter 7). This book has a long and tortured history—even longer and more tortured than most edited works! It was inspired by a symposium on the ecology and evolution of feeding systems in lower vertebrates presented at the annual meeting of the American Society of Ichthyologists and Herpetologists in Austin, Texas, in 1993, to which I was a contributor. The symposium was organized by Drs. Peter Wainwright and Kiisa Nishikawa. Dr. Charles Crumly, a systematic herpetologist and editor at Academic Press, was in attendance. I had been toying with the idea of editing a book in the area of feeding, so when Chuck approached me with the idea I was thrilled to take it on. By the end of the meeting several authors were already lined up. That was the easy part! The project ebbed and flowed over the years as the author roster grew and shifted. Consequently, there is a large span of time over which chapters were completed and submitted. Although I have tried to update the literature where necessary, some chapters are inevitably not as current as others. Thus, authors who worked most dilligently to complete their manuscripts in time for early deadlines should not be held to blame for editorial shortcomings. There are many people to thank for their contributions, direct and indirect, to this project. I must begin by expressing my deep gratitude for the inspiration of my teachers, Warren R Walker, Jr., James R. Stewart, and Marvalee H. Wake, to whom this book is dedicated. Warren Walker first taught me vertebrate biology and comparative anatomy as a junior at Oberlin College and it was his deep knowledge and masterful teaching that led me to embark on a career in vertebrate morphology. I remain in awe of his knowledge of comparative anatomy; his course serves as the benchmark from which I measure my own feeble attempts. Warren had the poor taste to take a sabbatical leave my senior year at Oberlin, but this sad event (for me) had a positive side—James Stewart was hired to replace him that year. Jim came to Oberlin fresh out of Berkeley with a

new set of experiences and ideas. I watched firsthand as he put together his own terrific course on comparative anatomy and I was given the opportunity to assist teaching in the lab. Jim supervised my senior thesis research (on lizard feeding!) and became a friend as well as a mentor. His calm, philosophical, and scholarly approach to both life and science deeply impressed me and continues to inspire me now. At Oberlin, Jim regaled me with stories of Berkeley, the Museum of Vertebrate Zoology, and the "Herp Lab,'' so after a short hiatus as a zookeeper at the Bronx Zoo, I was thrilled to be accepted into Marvalee Wake's lab at Berkeley for graduate study. Marvalee, to me, is the quintessential vertebrate morphologist—painstaking, detailed, thorough, and a scholar of the highest order. She was also the perfect advisor. She knew unerringly when to leave me on my own and when to push me. She supported my work and my psyche. Most important, she set a high standard in the lab and maintained it by example. The depth and breadth of her work on caecilian amphibians are a model of achievement and a personal source of inspiration. I have depended on Marvalee's wisdom for the last 20 years and still turn to her when I am in need of counsel. I am profoundly grateful to each of these people who have contributed so critically to my professional, intellectual, and personal development—often in ways they cannot imagine. Whatever strengths my work has shown since are owed to their mentor ship. I thank my friend and editor at Academic Press, Chuck Crumly, for seeing this project through from the beginnning and for alternately holding my hand and kicking my butt, as required. Donna James and Joanna Dinsmore at AP provided much-needed help in the final stages of manuscript preparation, for which I am very grateful. Mary Jane Spring not only prepared some wonderful original artwork for my chapters, but also slaved over a hot scanner to produce many composite plates and other figures for reproduction. My father, George Schwenk, generously produced the penand-ink illustrations that introduce each section of the book. A number of people critically read chapters in whole or in part, offered comments, checked facts, and/or helped with bibliographic sources: William E. Bemis, A. W. Crompton, Nirvana I. Filoramo, Leo J. Fleishman, Harry W. Greene, Susan W. Herring, Dominique G. Homberger, Parish A. Jenkins, Jr., Kenneth V. Kardong, Nate Kley, John H. Larsen, Matthias Ott, Margaret Rubega, Carl D. Schlichting, Adam Summers, Carole Tomlinson, Giinter P. Wagner, Marvalee H. Wake, and Kentwood D. Wells. David Cundall, Harry Greene, Carl Schlichting, and Giinter Wagner supported this effort with their friend-

Preface ship, beer, and a high tolerance for whining. I thank my graduate students. Nirvana Filoramo and Charles Smith, for their forbearance in dealing with a busy and distracted advisor. My family—George Schwenk, Elizabeth Schwenk, Deborah Schwenk, John Schwenk, and Natalia Schwenk—have always been there for me and don't even seem to mind when I lapse into soliloquies about tongues and lizards. Finally, I thank my wife, Sandford von Eicken, and my son, Colton Schwenk, for their love and incredible patience.

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Work in my lab and preparation of the manuscript were made possible by grants from the University of Connecticut Research Foundation and the National Science Foundation (IBN-9601173) whose financial support is gratefully acknowledged. Kurt Schwenk Storrs, Connecticut April 2000

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S E C T I O N

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C H A P T E R

1 Tetrapod Feeding in the Context of Vertebrate Morphology KURT SCHWENK Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut 06269

I. INTRODUCTION A. Why Study Feeding? B. Delimiting the Topic II. APPROACHES TO THE STUDY OF TETRAPOD FEEDING A. Themes in Vertebrate Morphology B. Schools of Vertebrate Morphology C Techniques of Vertebrate Morphology III. CONCLUDING COMMENTS References

L INTRODUCTION A. Why Study Feeding? Despite huge strides in our understanding of gene structure and function, we remain largely ignorant about how phenotypes evolve. This apparent paradox arises from the fact that phenotypes embody emergent properties not directly codified in the genes. Fience, these properties are unknowable even with an exact and complete knowledge of the genetic system. It is possible to deduce them only from direct study of the phenotype itself. Knowledge of such properties is essential because it is the phenotype, after all, and not the genotype, that performs in an environmental context and it is this phenotype-environment interaction which determines lifetime reproductive success (fitness). A comprehensive view of organismal evolu-

FEEDING (K.SchwenKed.)

tion and diversity must, therefore, integrate genebased (bottom-up) and phenotype-based (top-down) approaches. Because morphology and function are the direct objects of selection, their study can contribute uniquely to the formulation of such a comprehensive view. Indeed, morphological studies have, historically, spawned many of the fundamental concepts of comparative biology: homology, analogy, adaptation, constraint, and Bauplan, for example. Furthermore, morphological principles might be critical to our understanding of how lineages navigate "phenotype space" through evolutionary time. Why do some systems remain static while others diversify? Do certain phenotypes confer intrinsically stable configurations that resist modification? How are segmental or modular body plans functionally integrated and how does the degree of their integration affect their ability to evolve? Such questions are best addressed through phenotypic analysis and it is in this context that a deep and detailed knowledge of form and function gains its greatest value. General principles of form-function evolution can be approached through a process of induction from specific systems. Tetrapod feeding is attractive in this regard because it offers several attributes that enhance its utility as a model system. First, tetrapod feeding systems are hugely variable, ranging from the edentulous jaws and extraordinarily protrusible tongues of ant- and termite-feeding mammals that feed frequently on many minute prey, to the syringe-like fangs and

Copyright © 2000 by Academic Press. All rights of reproductiori in any form reserved.

Kurt Schwenk venom glands of some caenophidian snakes that feed infrequently on few, very large prey. Within this array of systems, however, there has been the repeated acquisition of certain types. Lingual prehension of food, for example, is found in frogs, salamanders, turtles, lizards, birds, and mammals, and truly projectile tongues have evolved independently within salamanders, frogs, and lizards. Such phenotypic diversity allows us to address basic Darwinian questions regarding pattern and process of evolution and biodiversity; why are there so many types of feeding system? Conversely, the repeated acquisition of functionally analogous systems permits us to examine the evolutionary dynamic between extrinsic factors (e.g., environmental selection, adaptation) and intrinsic factors (e.g., developmental and functional constraint) in determining form. Despite extreme variation in form and function, tetrapod feeding systems are amenable to comparative analysis because they represent modifications of the same basic apparatus, comprising, for the most part, a set of unequivocally homologous parts. Many of the relevant skeletal components, for example, derive from the ancestral splanchnocranium (visceral skeleton), a defining set of vertebrate characters significant in the origin of the group and present in the tetrapod head under every variety of form and function (Hanken and Hall, 1993). Indeed, splanchnocranial elements of the feeding apparatus in one clade are modified to function as part of the auditory system in another, or the chemosensory system in a third. Such phenotypic recycling well illustrates the evolutionary truism that novelties are most often realized through the modification of preexisting forms. Finally, the relative functionality of the feeding system has, without a doubt, a large impact on individual survival and hence lifetime reproductive success. It is reasonable, therefore, to presume that feeding systems are under strong selection and that variations in feeding performance will have significant fitness consequences. Such a presumption allows us to apply optimality criteria and engineering principles in analyses of feeding system design and to identify trade-offs and constraints on design modification because very little about the feeding system is likely to be a result of random processes (e.g., fixation through drift). As such, the feeding system is well suited to analyses that address the relative contributions of adaptation and historical contingency to the phenotype. The importance of the feeding system to survival and fitness is underscored by its large impact on the tetrapod body plan, primarily through its influence on cranial form. The concentration of both feeding and

sensory components onto one portion of the body reflects a general, historical trend of increasing cephalization in vertebrate evolution. This, in turn, has set the stage for a complex integration and coevolution of feeding and sensory systems in a number of tetrapod clades through competition of these systems for limited cranial space and their shared use of certain anatomical parts. The characteristics of tetrapod feeding systems outlined earlier—ample variation, homology of parts, reasonable presumption of fitness consequences for variation, large impact on body form, and integration with other systems—promote the utility of feeding systems for comparative, evolutionary studies. Specific insights will emerge from detailed analyses of cladespecific patterns and cross-clade comparisons, as considered in individual chapters of this book. B. D e l i m i t i n g the Topic The decision to limit the coverage of this book to tetrapod vertebrates (as opposed to all vertebrates, including fish) was driven both pragmatically and conceptually. Pragmatically, issues of length and the tradeoff of depth versus breadth had to be considered. As editor, I felt strongly that tetrapod feeding systems were in need of a more in-depth treatment than they had been accorded heretofore. Although various aspects of feeding in fishes have been treated to several overviews (e.g., Lauder, 1982b, 1985; Bemis, 1986; Schaefer and Lauder, 1986; Motta, 1988; Westneat, 1990,1995a; Sanderson et al, 1991; Aerts and De Vree, 1993; Lauder and Shaffer, 1993; Wainwright and Lauder, 1992; Sanderson and Wassersug, 1993; Gerking, 1994; Frazzetta, 1994; Stouder et al, 1994; Vandewalle et al, 1994; Wu, 1994; Gosline, 1996; Drost et al, 1998), the rapidly growing literature in tetrapod feeding has barely been harnessed since the seminal papers of Bramble and Wake (1985) and Hiiemae and Crompton (1985). Only two major overviews of tetrapod feeding have appeared (Smith, 1993; Bels et al, 1994), but their coverage is too broad to achieve the depth for tetrapods aimed for here. One book provides in-depth coverage of "eating" in the context of human biology (Linden, 1998). Perhaps the most important reason to exclude fish from consideration, however, is because tetrapod feeding represents a real and significant departure from fish feeding—so much so that research in each area largely operates within a different paradigm. This departure arises from the simple fact that tetrapods, by definition, evolved to feed on land from ancestors that fed exclusively within water. The radically different

1. Tetrapod Feeding in Vertebrate Morphology physical properties of air versus water required an equally radical remodeling of the feeding system. The impact of the medium (air vs water) is so great that feeding system phenotype, overall, is widely viewed as "medium dependent" (Lauder, 1985; Bramble and Wake, 1985; Liem, 1990; Denny, 1990). Fish (presumably including those ancestral to tetrapods) rely almost universally on either suspension or suction mechanisms for feeding (e.g., Sanderson and Wassersug, 1993; Lauder and Shaffer, 1993), which exploit the high density of food particles in water, their buoyancy, and the frictional forces generated by the high viscosity of water. Faced with a low viscosity medium capable of producing only nominal frictional forces, a relatively much lower density of prey, and the need to lift and support the weight of any food item actually obtained, tetrapod ancestors could rely neither on suction nor on suspension feeding and thus required an entirely new approach to food acquisition and manipulation. They achieved this through invention of a true evolutionary novelty: a mobile, muscular tongue. A second area largely neglected in the present volume is the postcranial contribution to feeding function. Obviously, once captured, processed, and transported to the esophagus, food is further digested, assimilated, and reduced to excreta in the remainder of the gut, and these latter processes can have profound effects on body form. The reason for this neglect is largely historical; postcranial digestion and processing are mostly considered within the province of comparative physiology, whereas this book is rooted in the traditions of functional and evolutionary morphology (see later) (DuUemeijer, 1994). From this perspective, most feeding function occurs within the mouth and pharynx, hence the chapters herein tend to be limited to this region. Nonetheless, it is worth remembering that postcranial feeding adaptations can be significant and must be tightly integrated with cranial specializations for particular diets or feeding modes. An obvious example of such integration is mammalian herbivory, which evinces striking adaptations of the gut, including complex stomachs and enlarged caecae associated with the presence of a symbiotic microfauna capable of digesting cellulose (no vertebrate produces its own cellulase enzyme). A less well-known example is the relationship between feeding mode and digestive physiology in snakes. Most "advanced" (macrostomatan) snakes eat only rarely, but when they do they are likely to eat extremely large prey relative to their body size (Chapter 9). Due to a previous evolutionary commitment to an elongate, narrow-diameter body and small head [probably driven by a period of fossoriality and locomotory adaptation (e.g., Greene, 1997)], there was a

considerable mechanical challenge to be met before large prey could be engulfed. The cranial and mandibular apparatus of such snakes was radically modified for production of a wide gape, thus permitting passage of 'large prey through a small-diameter head into an extensible gut. The gut in such snakes is capable of very rapid and large-scale physiological upregulation when the occasional food item presents itself—for example, the intestine actually doubles in mass, mostly through mucosal growth (Secor and Diamond, 1998). Return to an atrophied, or quiescent, condition during long intervals between meals is energetically advantageous to these ectothermic animals. Thus in snakes, body form and the cranial apparatus are tightly integrated, and these aspects of the phenotype are correlated with less obvious, but equally dramatic adaptations of the intestine and its physiology. This example serves to remind us that feeding form and function are more than head deep, a fact the reader is urged to bear in mind.

II. APPROACHES TO THE STUDY OF TETRAPOD FEEDING As for any aspect of the phenotype, the feeding system can be studied in several complementary ways. Although the authors of the various chapters in this book were asked to cover certain general areas, differences in their contributions reflect not only peculiarities of the taxa they treat, but also differences in philosophy, technique, and approach. There is no agreed upon schema for these different approaches and most studies and investigators defy characterization by simple, typological labels. However, it is worth considering, in a broad sense, the different philosophical bases and "schools of thought" characterizing vertebrate morphology as an intellectual realm. It is this realm that has provided the context for this book and its individual contributions (see also Liem and Wake, 1985).

A. T h e m e s in Vertebrate Morphology Animal anatomy is certainly one of the oldest, if not the oldest, biological science, tracing its origins to preAristotelian times (Cole, 1944; Singer, 1957); however, the term "morphology" was only coined in 1800 (Nyhart, 1995). It was during the 19th century that morphology, as a discipline, achieved its heyday, becoming a dominant area of biological research intellectually, if not institutionally (Nyhart, 1995). Certainly, Darwin's

Kurt Schwenk (1859) formulation of the theory of natural selection grew out of an intellectual milieu in which the extensive and painstaking documentation of morphological variation within and among species figured prominently. It is therefore ironic that morphology is seen as having contributed little to the 20th century evolutionary synthesis, commonly referred to as neo-Darwinism (Ghiselin, 1980; Mayr, 1980; but see Waisbren, 1988). While this may be true, it is equally true that neoDarwinism has failed to incorporate many of the lessons of morphology and there is growing dissatisfaction among some morphologists with the ability of neo-Darwinian theory to deal adequately with the totality of phenotypic evolution (see later). In any case, since Darwin, few fields have embraced evolutionary theory as enthusiastically as morphology {contra Ghiselin, 1980), for it is in evolution that the morphological concepts of homology, analogy, Bauplan, and "unity of type," for example, become sensible and elevated in significance. Indeed, the entire field of systematics as currently practiced is based on the character concept, a pre-Darwinian morphological construct melded with neo-Darwinian evolutionary theory. One cannot overstate the centrality of morphology to the development of modern biological thought. What follows is a subjective and largely overlapping list of dichotomies that attempt to clarify and situate the discipline and subdisciplines of vertebrate morphology. The dynamic and protean nature of the field precludes even the pretense of total agreement in this formalization, but one hopes it might be of some heuristic value to new students of vertebrate form and function. 1. Morphology vs

Anatomy

Unlike botanists, who make a clear and formal distinction between plant morphology and plant anatomy (the former referring to whole-plant form and the organization of parts, the latter to the fine structure, or histology, of parts), zoologists are uncharacteristically vague in their usage of these terms. Morphology "deals with the form of living organisms, and with relationships between their structures" (from the Greek stem morpho), whereas anatomy is "the science of the structure of the bodies of humans, animals, and plants" (derived from the Greek stems ana- and -tomy, meaning "repeated cutting") (Oxford English Dictionary; Brown, 1993). Although these definitions would appear to be more-or-less synonymous, in current zoological usage they connote somewhat different things, the sense of which is hinted at in the etymology. Morphology is the study of "form," which can be generalized to all hierarchical levels, from organelle to whole

organism. It is also concerned with the relationships among structures, hence it includes emergent features of form such as relative size, allometry, and even function and physiology for some (see later). Thus, morphology is a more expansive term, subsuming anatomy (as toad is to frog, so anatomy is to morphology). Anatomy is largely limited to the hierarchical level of organs, or body parts, i.e., those elements of form revealed by dissection, and historically has been associated with human beings (Owen, 1866; Singer, 1957). For example, Gegenbauer (1878), epitomizing the late 19th century view, divided anatomy ("the doctrine of structure") into anthropotomy and zootomy, the dissection of humans and nonhuman species, respectively. According to Gegenbauer, anatomy is not a science because it is restricted to the empirical generation of descriptive data. However, these data achieve the status of science when they lead to synthesis and abstraction, only possible by comparing anatomical data among species, i.e., "comparative anatomy," or what Owen (1866) called "homological" and "zoological anatomy." Gegenbauer (1878) included anatomy within the larger field of morphology such that all of biology could be divided into physiology and morphology (see later) and morphology, in turn, into anatomy and embryology. Thus, while some treat the terms anatomy and morphology equivalently, most modern usage continues to reflect the 19th century view in which anatomy is restrictive, descriptive, based on dissection of body parts, and primarily (but not exclusively) anthropocentric, whereas morphology is holistic, multihierarchical, often synthetic and concerned not only with the structure of the parts, themselves, but relationships among the parts, and of parts to function. Although Owen (1866: vii) did not use the word morphology, his notion of "zoological anatomy" captures nicely the essence of modern animal morphology as "that which investigates the structure of an animal in its totality, with the view of learning how the form or state of one part or organ is necessitated by its functional connections with another, and how the co-ordination of organs is adapted to the habits and sphere of life of the species." The history of these ideas and disciplines is reviewed admirably by Russell (1916), Cole (1944), Singer (1957), and Nyhart (1995), among others. Perhaps the most important distinction between anatomy and morphology as formal disciplines is that anatomy is mostly unconcerned with the origin of structure, whereas the origin and generation of form are at the philosophical core of morphology (e.g., Gegenbauer, 1878; His, 1888; Russell, 1916; Thompson, 1942; Davis, 1960; Nyhart, 1995; Webster and Goodwin, 1996). Indeed, since the early 19th century mor-

1. Tetrapod Feeding in Vertebrate Morphology phologists have endeavored to discern "rules of form" that might underlie ontogenetic and phylogenetic morphological transformations. Interest in rules of transformation predates an evolutionary world view (e.g., Driesch, 1908; Nyhart, 1995). Elucidation of such rules was the goal of Geoffroy Saint-Hilaire (1818; in Russell, 1916) and the "transcendental" morphologists, and explored by Owen (e.g., 1848,1849) in the context of "archetypes." However, this fundamental interest in morphological rules of transformation is clearly evident in the modern structuralist movement (see Piaget, 1970; Rieppel, 1990), which, although it takes many forms, has at its core the notion that phenotypic hierarchies manifest emergent properties that certainly influence, if not dictate, directions of further phenotypic evolution (e.g., Russell, 1916; Whyte, 1965; DuUemeijer, 1974, 1980; Riedl, 1978; Lauder, 1982a; Ho and Saunders, 1979, 1984; Roth and Wake, 1985; Rieppel, 1986; Wagner, 1986; Wake and Larson, 1987; Wake and Roth, 1989; D. Wake, 1991; Smith, 1992; van der Weele, 1993; Schwenk, 1995, 2000; Amundson, 1996; Hall, 1996, 1998; Raff, 1996; Webster and Goodwin, 1996; Arthur, 1997; Wagner and Schwenk, 1999; Schwenk and Wagner, in preparation). Indeed, radical "process structuralists" (see Smith, 1992) go so far as to suggest that random variation, natural selection, and phylogenetic history (the tenets of Darwinism) are secondary players in the generation of hierarchically organized phenotypic diversity. They seek instead a "rational," predictive science of form based on rules of selforganization and organismal development (e.g.. Ho and Saunders, 1979,1984; Goodwin, 1989; Webster and Goodwin, 1996). Whether radical or moderate, inherent in the structuralist, morphological view is the sense that the atomistic, neo-Darwinian, gene-based paradigm of phenotypic evolution is incomplete and that the organism creates the context for its own further evolution, thus setting the stage for a top-down chain of evolutionary causality in phenotypic evolution (Whyte, 1965; Wagner and Schwenk, 1999). 2. Form vs Function The conceptual dichotomy of form and function is ancient, at least as old as Aristotle (Russell, 1916; Lauder, 1982a; Padian, 1995). It was identified by Russell (1916) as a major theme in the history of morphology, as evident in the title of his classic book {Form and Function), and it has continued to be a central theme in the study of phenotype throughout this century (e.g., Woodger, 1929; Bock and von Wahlert, 1965; Lauder, 1981,1982a; Gans, 1969,1988; Wake, 1992; Lauder et a/., 1995; Padian, 1995; Weibel, 2000). Historically, this dichotomy was discussed in terms of primacy (e.g., Rus-

sell, 1916; Woodger, 1929; Lauder, 1982a, 1995, 1996; Appel, 1987; Amundson, 1996): is it form that determines function or function that determines form? In the early 19th century, George Cuvier, for example, believed in the primacy of function, positing that form was imposed by the functional demands of the environment and that similar forms reflected similar functional "adaptation." He believed that form and function were so tightly bound in this causal sense that one could, through the "principle of correlation," predict the whole form of an animal from a single part. In contrast, his contemporary, Etienne Geoffroy St. Hilaire, sought a "pure morphology of organic forms" wherein function emerged as a mere by-product of structure. Indeed, Geoffroy eschewed any consideration of function in comparative anatomy and believed that changes in function followed secondarily upon primary changes in structure (Russell, 1916). Although the debate between Cuvier and Geoffroy epitomizes the contention in the field regarding form and function early in the 19th century, the dichotomy was formalized on a grander scale later in the century when the whole of biology was cleaved into physiology and morphology (e.g., Owen, 1866; Gegenbauer, 1878; see Russell, 1916; Nyhart, 1995). Physiology comprised all aspects of organismal function, whereas "the investigation of the material substratum of those functions, and accordingly of the phaenomena of form of the body and its parts, as well as the explanation of the phaenomena of form by reference to function, is the business of Morphology" (Gegenbauer, 1878:1). Physiology already had a long history separate from morphology and the two fields continued through the 19th century and into the 20th to develop in isolation (Russell, 1916; Woodger, 1929). They have remained distinct traditions until quite recently and even now a complete rapprochement remains elusive (e.g., Weibel et al, 1998; Weibel, 2000). Although there is obvious overlap in domain, comparative physiologists, for the most part, continue to study function of a different sort and in a different context than functional morphologists. Woodger (1929) regarded the splitting of form and function as an abstraction not manifest in nature. The "antithesis" results from employing "different modes of apprehension" and from artificially separating space and time (anatomy focusing on the former, physiology the latter) which are simultaneous attributes of living structures. Certainly, most modern evolutionary morphologists would consider the question of formfunction primacy moot, recognizing the chicken-andegg nature of the dichotomy in a historical context. Indeed, evolutionists do not acknowledge a distinction at all, capturing the seamlessness of form and function in

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the inclusive term "phenotype." Nonetheless, vestiges of the dichotomy persist within morphology. This is most apparent in the question of how one studies function: must one study function directly or is it possible to infer function from structure? Certainly pure, descriptive, anatomical studies are not much interested in function and are therefore not relevant here, but there is, at the same time, a long tradition in vertebrate morphology of inferring animal function from static form. This is most apparent in the 20th century paleontological literature where functional speculation is commonplace (e.g., Rainger, 1989; Hopson and Radinsky, 1980; Thomason, 1995), but it is also rife in studies of living species. Indeed, the ability to predict function from form is at the conceptual core of "ecomorphology" (see later). The presumption that function can be inferred from form stems more or less directly from Cuvier's principle of correlation (see earlier discussion). It depends absolutely on the degree to which form and function are integrated so that each can stand as a proxy for the other. However, Lauder (1995, 1996) has shown that structure and function are not always tightly matched in a predictive sense, thus falsifying the assumption upon which the principle of correlation is based. He advocates a direct, experimental approach to function based on analysis of living specimens and emphasizes the need for quantification of functional data. Experimental, quantitative approaches to functional morphology are relatively recent. Przibram (1931:14), for example, noted, "Whereas in Physics, Chemistry or even Physiology nobody would nowadays try to state laws without experimental evidence, the general statements in animal Morphology have been mostly based on speculations. Only of late has the experimental method been gaining ground in Biology and research is being carried on in a large scale at institutions adapted to the p u r p o s e . . . Again I would refer to Physics and Chemistry as brilliant examples of what may be achieved in the way of unraveling the laws of nature by quantitative experiment and mathematical formulation based thereon." Thompson (1942:2) was, likewise, intent on a more quantitative approach to form: "But the zoologist or morphologist has been slow, where the physiologist has long been eager, to invoke the aid of the physical or mathematical sciences." Thus, while the inseparability of form and function may be intellectually acknowledged by most practicing morphologists, the ancient dichotomy remains manifest in investigators' approach to function: inferential and qualitative or experimental and quantitative. These different approaches are elaborated further. Although the dangers of inferring function from static form seem clear, seldom, if ever, is concern ex-

pressed for the converse: can the detailed study of function in the absence of equally detailed structural data be misinformed? Unquestionably (see also Cans, 1986). I am frequently impressed by the near total lack of morphology evident in some studies of putative "functional morphology" in which quantitative aspects of function are analyzed in a structural vacuum, almost wholly uninformed by knowledge of the relevant anatomy. At the very least, morphological data can, in such cases, eliminate from consideration alternative mechanistic hypotheses. Further, functional conclusions can be revealed as false, or even absurd, when held in the light of form. The dichotomy of form and function is an undeniably useful, heuristic tool. However, we must acknowledge that this dichotomous view is a philosophical construct, simplifying for us the complex notion oiphenotype in which form and function are interwoven dynamically and infrangibly (Woodger, 1929). As Ruffini (1925) noted, "form is the plastic image of function" (in DiDio, 1986:197). There can be no argument for primacy, only relationship. Therefore, all approaches to the study of phenotype are valid, if not complete, so long as conclusions follow from data and speculation is labeled as such. If only for pragmatic reasons, most individual studies will continue to emphasize either form or function, with syntheses relatively rare. Nonetheless, form and function, experiment and description, qualitative and quantitative data must be held as equally important, complementary, and ideally, "reciprocally illuminating" elements in the study of morphology [Lombard (1991) and Lauder (1995) offer related perspectives on these issues]. 3. Idiographic vs

Nomothetic

Idiographic studies are those that characterize a specific case without regard to its typicality or generality. Studies which treat the morphology or function of a single species are of this type. An organism, or part thereof, can be treated purely as mechanism and one can ask, simply, what does it look like? what are its component parts? and how does it function? without regard to whether the results are applicable to a larger group or peculiar to the case at hand. Such studies can have high intrinsic interest and are valuable in proportion to the quality of their data, but they do not inform us about the next system we might study, nor how one form evolves into another. Pattern, causality, and prediction derive, instead, from nomothetic studies, which strive to elucidate higher principles, rules, or, in the strict sense, scientific laws. Comparative morphology, like Owen's (1866) zoological anatomy (see earlier discussion), falls within

1. Tetrapod Feeding in Vertebrate Morphology this realm because it seeks generalities beyond the specific (Gegenbauer, 1878). However, nomothetic, comparative, vertebrate morphology does not require an evolutionary world view. As noted earlier, early 19th century morphologists, such as Cuvier and Geoffroy, were very much interested in general rules of form without reference to historical descent. Indeed, some modern structuralists (see earlier discussion) are also interested in an organism-based theory of form independent of evolution, arguing that * 'evolution provides only limited insight into the problem of form as regards both the causal explanation of form and the relations between forms . . . what is required is the development of a specific causal-explanatory theory of form, a theory of morphogenesis in the most comprehensive sense . . . such a theory will be as fundamental to biology, if not more so, at least as the theory of evolution" (Webster and Goodwin, 1996 :ix; see also His, 1888). Nonetheless, most modern, comparative studies in vertebrate morphology are rooted in the neo-Darwinian tradition, but framed in an explicit cladistic, phylogenetic context (e.g., Lauder, 1981, 1990; Greene, 1986a), whereas still others seek some middle ground (e.g.. Wake and Larson, 1987; Wagner and Schwenk, 1999). Whether organism centered or phylogenetic, such studies are part of a long, nomothetic tradition in vertebrate morphology that has contributed fundamentally to the principles of modern biology. 4. Laboratory vs Field Most vertebrate morphology must, of necessity, be undertaken within the laboratory. However, any consideration of function, whether it is inferential or experimental, is at risk if it fails to consider the actual behavior of organisms in the field (Greene, 1986b, 1994). For the inference of function from form, natural history data can circumscribe the universe of possibilities. For example, one need not waste time speculating about the role of certain skull attributes in processing flesh if it is known from observation and stomach content analyses that the organism in question is an insect specialist. Likewise, a treadmill study of locomotion in gibbons would be largely uninformative about the evolution of its form, whereas initial field observations of its natural locomotory mode (brachiation) would suggest a different experimental approach. These examples are obvious and might appear silly, but there is no doubt that functional and evolutionary morphology can be led astray in failing to consider the natural behavior of animals. A classic case is that of monitor lizard (Varanus) morphology and diet. A persistent theme in functional-morphological (and other) studies is that varanid lizards are adaptively special-

ized for carnivory and the ingestion of large prey (e.g., Rieppel, 1979; Smith, 1982). As such, experimental studies of feeding function have analyzed monitors during feeding on rodents (e.g.. Smith, 1982; Condon, 1987). However, a comparative study of diet in monitor lizards revealed that nearly all species are insectivorous, eating many small prey items rather than a few large ones (Losos and Greene, 1988). Varanus exanthematicus, the most commonly used species in liveanimal studies (e.g.. Smith, 1982), is one of the most extreme insect specialists within the family. Indeed, it is in many other respects unusual and derived— neither a typical lizard nor even a typical varanid. Thus, the experimental conditions of these studies were unnatural, or at least, atypical, and therefore the generality of their results is suspect. Certainly the interpretation of derived varanid cranial attributes as adaptations for eating large, vertebrate prey is without foundation. Rather, the typical monitor lizard cranial apparatus seems to represent a specialized pincer system for effectively nabbing elusive prey with the tips of the jaws (Frazzetta, 1983; see Chapter 8). B. Schools of Vertebrate Morphology The simple 19th century division of biology into physiology and morphology is no longer tenable. Experimentalism, technological advancement, new techniques, new theory, and increasing specialization have driven fragmentation of biology, generally, and vertebrate morphology, specifically. Because no investigator can master all possible approaches to morphology, individual studies tend to emphasize one approach, technique, or school of thought. The following list of approaches to vertebrate morphology is hardly exhaustive, but it represents a cross section of the field as currently practiced. Elements of these different approaches are evident in the chapters of this book. 1. Descriptive

Morphology

Description remains the foundation upon which morphological studies must ultimately rest. Good descriptive morphology is as rare as it is beautiful, virtually an art. Unfortunately, it may be a dying art because it is little valued within the context of modern science. This is tragically short-sighted because one thing is clear about high-quality, well-documented descriptive anatomy: it may represent the only truly hard, objective data in morphological research, as free of fashion and interpretation as possible. It is, therefore, timeless. This timelessness is critical because it means that descriptive data can be used in the service of other studies and new theories, including those not conceived at

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the time the data were generated. As such, descriptive data are of value to future generations of biologists— it is common, for example, for 19th century and even older literature to be cited in modern morphological studies, often in contexts, such as cladistic, systematic analysis, never imagined by the original authors. For how many other fields, or even other approaches to morphology, can this be said? Of what value now, for example, are systematic analyses based on the once widespread and "cutting edge" method of phenetics? How many molecular studies more than 10 years old remain in currency? In contrast, a morphological treatise, such as D. Dwight Davis' (1964) classic study of the giant panda, is unceasingly relevant. Indeed, its value only increases with time as the availability of rare species declines. It is a telling fact that Davis' (1964) conceptual, evolutionary analysis of his descriptive work is dated and of dubious value in today's milieu of cladism and molecular genetics, but the 300 pages of painstaking, descriptive anatomy that precedes it remain—untainted, unfiltered, uninterpreted, and fully available for reanalysis in another context, now or in the future. Descriptive morphology can apply to any hierarchical level, but it is done most commonly at the anatomical level (see earlier discussion). Anatomies can be regional, such as Oelrich's (1954) Anatomy of the Head of Ctenosaura pectinata, or they can be systemic, as in Romer's (1956) Osteology of the Reptiles. Tissue-level morphology is usually referred to as histology, loosely limited to those aspects of morphology resolvable by light microscopy. Cellular and subcellular morphology studied by means of scanning and transmission electron microscopy is referred to as ultrastructure. In the parlance of vertebrate morphology, structure usually refers to organs and organ systems, although it can be in reference to any hierarchical level. However, in the biomedical community, "structural biology" is purely molecular. 2. Evolutionary

Morphology

Evolutionary morphology defies precise characterization because it is the most inclusive school of vertebrate morphology (D. Wake, 1982; M. Wake, 1991, 1992). It can be experimental, functional, or purely descriptive, but it has at its core an evolutionary intent. By definition, therefore, it is comparative. As such, it most clearly manifests the tradition of 19th century comparative anatomy in that it continues to seek higher level understanding of the generation and transformation of form (see earlier discussion; Davis, 1960). Evolutionary morphology is distinct from morpho-

logical systematics in that the latter uses morphology in the service of phylogeny, whereas the former uses phylogeny in the service of morphology. As such, the historical relationships of organisms are of secondary interest to the evolutionary morphologist whose main concern is the history of the characters themselves, i.e. character analysis in the purest sense. Whereas the systematist uses morphological characters as a matter of routine, in evolutionary morphology the character concept is, itself, a subject of study (Wagner, 2000). Furthermore, studies in evolutionary morphology may attempt not only to generate patterns of character evolution, but to address ultimate issues of causality, as such, the processes of phenotypic evolution (e.g., Galis, 1996; Wagner and Schwenk, 1999). 3. Functional

Morphology

The focus of functional morphology, transparently, is function. As discussed earlier, there is contention about whether studies that are limited to the inference of function from structure can be considered "functional." Nonetheless, purely inferential papers continue to appear with "functional morphology," or sometimes "functional anatomy" in their titles. Although the latter term may be an attempt at truth in advertising (i.e., it flags the paper as inferential), "functional anatomy" is to be discouraged because it is, in some sense, an oxymoron (see discussion earlier). Thus, in most recent and I would say preferred usage, functional morphology refers specifically to analyses based on the direct measurement of function in live, behaving animals. Functional morphology may be evolutionary; it is often purely mechanistic and idiographic (D. Wake, 1982; M. Wake, 1992). Like good descriptive morphology, good functional studies of single species can be of great intrinsic interest, and to the extent that data are objective, they are available to other investigators for meta-analyses. It is worth noting here that while most modern functional morphology is "experimental," there are two quite different usages of this word in the field. The first is appropriate and consistent with its use in traditional, reductionist scientific method in referring to hypothesis testing. Such a hypothetico-deductive approach to function usually requires manipulations of experimental subjects and careful controls, thus in functional morphology such studies often require invasive techniques and the use of complex technology. Nonetheless, it is important to note that hypothesis testing, and therefore experimentation sensu stricto, is not restricted to functional studies. It is possible to test certain types of hypotheses, even functional hypotheses, by reference to morphology alone. However, such descriptive

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1. Tetrapod Feeding in Vertebrate Morphology analyses are never labeled "experimental." Thus, in current usage, the application of hypothetico-deductive analysis is insufficient to qualify a study as experimental. Nor would the use of control and manipulated subjects seem sufficient. Rather, the principal criterion appears to be the application of technology itself. This has led to a second, diluted, and much more common (if inappropriate) use of the term to mean any analysis employing technologically based methods. For example, many studies characterize muscle activity patterns during normal behavior using electromyography (EMG) and are labeled "experimental" even though they are purely descriptive—they show X muscle to be active during Y behavior. There need be no control, manipulation of the conditions, nor testing of functional hypotheses. However, not all use of technology seems to merit an experimental epithet. For example, use of binoculars to describe the same behavior, Y, in the field would not be considered experimental, although it may serve to test a functional hypothesis and scientifically it may be the more valuable of the two studies! Therefore, the currency of the technology employed, or perhaps its degree of invasiveness, seems to be a deciding factor. I see no obvious solution to these terminological paradoxes, but highlight them here as a reminder to students of form that scientific merit is a quality independent of technique or titular fashion. 4.

Biomechanics

Biomechanics might be regarded as a subdiscipline of functional morphology—certainly many functional morphological studies contain elements of biomechanical analysis (e.g., Gans, 1976; Rayner and Wootton, 1991). However, biomechanics is, in the strict sense, directly inspired by various fields of engineering and is far more mathematical and less anatomical than is typical of functional morphology (e.g., Fung, 1993). Indeed, biomechanics quickly blends into theory and modeling (see later). In addition, its more-or-less pure design approach to form (see Lauder, 1996) means that biomechanical studies generally eschew comparative or evolutionary issues. In fact, most of the biomechanics literature is biomedical and sports oriented. This can be contrasted with transformation morphology (see later) which, though often highly biomechanical, is concerned with understanding ontogenetic and phylogenetic transformations in form and function. Biomechanics in (nonbiomedical) morphology is especially concerned with the physics of biological materials and surrounding media, and their consequences for organismal form, function, and, occasionally, evolution (e.g., Wainwright et al, 1976; Alexander, 1985; Wainwright, 1988; Vogel, 1988, 1994; Vincent, 1990;

Denny, 1993). For example, it was noted at the outset of this chapter that the tetrapod feeding apparatus is, to a large extent, medium dependent in the sense that, depending on whether the organism lives in air or in water, the physical properties of the medium will impose a limited realm of phenotypic solutions to the problem of ingesting, processing, and swallowing food. Thus the convergence of feeding mechanisms in fish and secondarily aquatic tetrapods could be predicted from biomechanical first principles, i.e., the viscosity and fluid dynamics of water. Indeed, it is often found that certain aspects of the phenotype conform to the expectations of mechanical optimization in some parameter or other in a way that clarifies their functional and evolutionary significance. For example, although the tongue of squamate reptiles was well known to be a chemical sampling device, the functional significance of its forked form in snakes and some other species was not understood. An engineering approach in a comparative context, however, suggested that the fork provides a two-point sampling device for the detection of chemical gradients useful for following pheromonal trails (Schwenk, 1994). Fluiddynamic theory further suggested that the rapid oscillation of the tongue in the air characteristic of these species is an adaptation to enhance the molecular diffusion of environmental chemicals into the fluid on the tongue's surface, thereby amplifying the chemical signal carried into the mouth (Schwenk, 1996). Thus, while biomechanics can be pursued idiographically without reference to evolution, it can powerfully inform questions about the evolution of form and function (Lauder, 1991; M. Wake, 1992). 5. Developmental

Morphology

Like evolutionary morphology, developmental morphology is a broad field that grew out of the 19th century tradition of embryology (see earlier discussion). It implies no particular technique or approach, but is concerned with the ontogenetic transformation of form. Most often such studies are limited to the embryonic period, but they may treat any life stage so long as their concern is ontogenetic transformation. Because the focus of developmental morphology is on intrinsic attributes of individual organisms, it is the part of vertebrate morphology most clearly identified with biological structuralism (e.g., Wagner, 1988; Hall, 1994; D. Wake, 1991; Webster and Goodwin, 1996). Developmental studies have revealed principals of selforganization and pattern formation at the organismic level that are likely to be relevant to the directions and dynamics of phenotypic change in lineages through evolutionary time. Yet neo-Darwinian theory springs

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from population-level phenomena, hence it has neglected the role of the organism in directing patterns of phenotypic change. To a large extent, the modern notion of "evolutionary constraint" has emerged from the field of developmental morphology (e.g., Maynard Smith et al, 1985; Wagner, 1986, 1988; D. Wake, 1991; Schwenk, 1995; Schwenk and Wagner, in preparation). 6. Ecological

Morphology

Ecological morphology (or ecomorphology) is a rather amorphous hybrid of several morphological schools (as suggested in the title of one review; Wainwright, 1991). Nominally it owes its origin to van der Klaauw (1948), but conceptually it is rooted in the ancient observation of the "fit" between organisms and their environments. As such, the prevailing definition of ecomorphology is "the study of the relationship between the morphology of the organism and its environment" (Wainwright and Reilly, 1994a: 3). Indeed, it is difficult to say how the basic premise of ecomorphology differs from Cuvier's "principle of correlation"—both assume that organismal form is tightly correlated to environmental conditions. Like Cuvier, ecomorphology aspires to predict form from ecology and ecology from form (e.g., Emerson, 1991; Motta and Kotrschal, 1992; Norton and Brainerd, 1993; Wainwright and Richard, 1995; Losos et al, 1998). However, unlike Cuvier, modern ecomorphologists invoke natural selection and adaptation to account for the formenvironment fit. Thus, they espouse the need for integrating historical approaches into ecomorphological studies (e.g., Motta and Kotrschal, 1992; Wainwright and Reilly, 1994a; Losos and Miles, 1994; Westneat, 1995b). Wainwright and Reilly (1994b) provide an entree into the ecomorphological literature. As they noted, ecomorphological studies usually are either mostly ecological or mostly morphological (Wainwright and Reilly, 1994a). However, at its best, ecomorphology attempts a true synthesis by addressing questions that are fundamentally ecological through the phenotypic analysis of organisms. The key point is that the study of phenotype is pursued at the population level. I think it is only here that ecomorphology clearly distinguishes itself. Otherwise it tends to suffer one of three fates: it is simply ecology with a few superficial measurements (e.g., limb length) thrown in; it is simply good functional or evolutionary morphology, which should, after all, incorporate ecological and natural history data into its analyses (see earlier discussion); or, most commonly and worst of all, it suffers from naive adaptationism {sensu Gould and Lewontin,

1979), which finds that organisms are, indeed, adapted to their environments, e.g., animals with big mouths can, in fact, eat big prey. Although such studies are not without merit, they evince little conceptual advancement over "natural theology" (e.g., Amundson, 1996)—things are as they must be (see also Liem, 1993). Rather than using the form-environment fit as a point of departure, ecomorphology can and should probe the limits of this assumption by incorporating notions of constraint and other potentially limiting factors into its paradigm (e.g., Barel et ah, 1989; Liem, 1993; Losos and Miles, 1994). Certainly the relationship between the organismal phenotype and the environment is far more complex than usually assumed (e.g., Simpson, 1953; Whyte, 1965; Greene, 1982; Wagner and Schwenk, 1999). 7. Transformation

Morphology

Transformation morphology is related to evolutionary and developmental morphology, but it is concerned specifically with the process of ontogenetic and phylogenetic phenotypic transformation (Barel, 1993; Galis, 1996). Its focus is less on the pattern of transformation (e.g., documentation of form-function complexes in comparative, or ontogenetic series) than on the rules of transformation underlying observed patterns. According to Galis (1996:128), these rules can be elucidated "by constructing biomechanically feasible transformation schemes, by studying key structural changes that break important constraints enabling a cascade of changes, and by studying the mechanisms that preserve the match between form and function during ontogenetic and evolutionary change." Transformation morphology has grown out of the Leiden school of morphology (e.g., van der Klaauw, 1945; DuUemeijer, 1959, 1974, 1980, 1989) and, as such, its emphasis is functional. Furthermore, as suggested by Galis' (1996) quote, modeling and engineering approaches to evolutionary transformation (e.g., Zweers, 1991; Zweers and Vanden Berge, 1997; van Leeuwen and Spoor, 1992; Galis, 1992,1993; Galis and Drucker, 1996; see later) are preferred to the comparative, phylogenetic methods typical of North American workers (e.g., Lauder, 1981,1990; Lauder et al, 1995; Larson and Losos, 1996). 8, Constructional

Morphology

Like transformation morphology, with which it overlaps, constructional morphology is largely a European tradition. It was formalized by Seilacher in the 1970s (e.g., 1970, 1973, 1979), but has earlier roots in Leiden (see references given earlier) (Reif et al., 1985).

1. Tetrapod Feeding in Vertebrate Morphology Constructional morphology deals explicitly with constraints on adaptive evolution arising from the physical properties of materials and the mechanisms of their deposition and growth, although it is occasionally more broadly construed as pertaining to any sort of structural constraint (e.g., Reif et ah, 1985; Barel et at, 1989; see also papers in Schmidt-Kittler and Vogel, 1991). Whereas ecomorphology takes as its starting point the adaptive nature of organismal form, constructional morphology focuses on nonadaptive aspects of form; it therejfore disputes the notion that all morphological variation reflects adaptive responses to different environments. Roth (1989), for example, showed that differences in dental form among nominal species of fossil elephant are attributable to "fabricational noise," reflecting individual differences in masticatory stresses during postnatal development of the teeth. As such, quite large differences in the form of the elephantid dental battery are a consequence of the uniquely retarded growth of elephant teeth as compared to other mammals. While the phenotypic plasticity that permits such individual responses to juvenile stresses might, itself, be an adaptation (e.g., Schlichting and Pigliucci, 1998), the particular morphcJiogical variants that arise are the result of nonadaptive processes stemming from mechanistic aspects of tooth development and growth. It is these processes, and their effects on the evolution of phenotype, that are the focus of constructional morphology. 9.

Morphometries

Morphometries is a catch-all term for a variety of methods that seek to capture and quantify complex shapes based on external measurements. It grew out of the emerging field of biometry in the late 19th century (Bookstein, 1994) and later, the pioneering work of D'Arcy Thompson (1917, revised and expanded in 1942) who sought a mathematization of zoology and morphology. Although best known for his application of Cartesian coordinates to the study of shape transformation, Thompson (1917) actually dealt more extensively with other quantitative aspects of form, especially patterns of growth. This work strongly influenced the subsequent, formal study of allometry, as evident in the dedication of Huxley's (1932) classic book to Thompson. Allometry, therefore, might be considered a part of the morphometric tradition (Huxley, 1932; Gould, 1966). In light of his stated goal, it is ironic that Thompson's (1942) use of deformed Cartesian coordinate planes to describe shape change was largely intuitive and not particularly quantitative. However, a num-

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ber of methods have been described that accomplish Thompson's (1942) intent with greater rigor (e.g., Rohlf and Bookstein, 1990; Bookstein, 1991; Marcus et al, 1996; McLellan and Endler, 1998). However, these are limited in application to two-dimensional shapes, or two-dimensional projections of three-dimensional forms, which diminishes their utility to morphologists interested in complex anatomy (however, some threedimensional morphometric methods are being developed, e.g.. Roth, 1993). Perhaps of greater concern is the question of using coordinate-based, landmark data in evolutionary character analysis. As noted previously, the issue of atomizing organisms and delimiting characters is an area of active empirical and conceptual work (e.g., Wagner and Schwenk, 1999; Wagner, 2000; Schwenk, 2000). It is by no means clear that landmark data fulfill the criteria of homology necessary to establish them as "characters" in the sense of semiautonomous units of phenotypic evolution. Bookstein (1994), for example, has argued that biometrical shape characters are not commensurate with traditional, phenotypic characters as used in systematic analyses, whereas others suggest that, in the proper context, morphometric characters can be used this way (e.g., Zelditchefa/.,1992,1993). 10, Theory and Modeling Although most morphological theory is conceptual (e.g., DuUemeijer, 1974; Gould and Lewontin, 1979; Wake et al, 1983; Wagner and Schwenk, 1999), it can also be highly mathematical (e.g.. Burger, 1986; Van Leeuwen, 1991, 1997). As for other biological disciplines (e.g., ecology and evolution), theory in morphology is most effective in reciprocity with empiricism. The case of chameleon tongue projection offers an excellent example of this synergism. The mechanistic basis of the explosive, ballistic projection of the chameleon tongue defied understanding for centuries (see Chapter 8). However, an incisive, experimental study by Wainwright and Bennett (1992) implicated the use of hydrostatic elongation of the lingual accelerator muscle in this function. The Wainwright-Bennett model, based on an in vitro study, was beautifully supported by a theoretical model of the biomechanics of the accelerator muscle, which accurately predicted details of hyolingual form and function (Van Leeuwen, 1997). The combined results of these studies have, in turn, been corroborated and extended by an in vivo study using high-speed X-ray movies (cineradiography) of chameleon tongue projection (Schwenk et al, in preparation). As a result of this interplay among descriptive anatomy, functional inference, in vitro and

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Kurt Schwenk

in vivo experimentation, and mathematical modeling, the mechanism of chameleon tongue projection is now reasonably well understood. Because many functional-morphological studies focus on musculoskeletal systems, it is no surprise that most of the inspiration for functional models comes fron\ mechanical engineering and materials science (e.g., Gans, 1974; Wainwright et ah, 1976; Alexander, 1983) (see also Section II, B, 4). Frazzetta's (1962) application of a "quadric-crank" model to the amphikinetic lizard skull is an early example of this approach, but mechanical modeling approaches are varied (see references given earlier; other examples include de Jongh et a/., 1989; Otten, 1989; Galis, 1992, 1993; Russell and Thomason, 1993; Weishampel, 1993, 1995; Greaves, 1995; Herrel et al, 1998). Models are especially powerful when they make predictions that can be tested empirically or with natural history data. For example, Galis' (1992) model of bite forces in a cichlid fish showed that ontogenetic changes in the pharyngeal jaws accounted for the inability of small fish to pierce the integument of certain prey types and the absence of such prey in the natural diets of the fish until they achieved a certain size (GaUs, 1993). The model accurately predicted the size at which fish started to include the harder prey type in their diets. Galis (1993) suggested that such patterns establish causality, as opposed to mere correlation, although this assertion is open to debate. C. Techniques of Vertebrate Morphology One of the great beauties of vertebrate morphology is that meaningful results can be obtained with minimal expense and laboratory sophistication. Many studies begin with dissection and, as argued earlier, highquality descriptive anatomy remains at the core of any morphological analysis. Beyond dissection and description, a variety of techniques are used to reveal increasingly reductionist hierarchical levels of anatomy and to record, measure, and quantify components of function. Many of these techniques are revealed in the individual chapters of this book and it is worth reviewing some of them here. I. Anatomical

Techniques

The art of dissection is little changed since the time of Aristotle, with the exception that tissues and whole organisms can now be fixed and preserved indefinitely for later examination. While vivisection is rarely necessary in morphological studies, occasionally fresh, unfixed tissue is required, as in some histochemical

procedures. Otherwise it is desirable to "stiffen" the tissue through fixation, most often in 10% formalin (formaldehyde solution), which not only allows ample time for one's study, but also facilitates the manipulation of the organs to be dissected, as in the separation of muscles along facial planes. The latter process can be made easier through differential staining of muscle and connective tissue with a topically applied stain (Bock and Shear, 1972). Very fine-scale dissection {microdissection) is possible with finely machined tools and a dissecting scope. Skeletal anatomy is often a central element in morphological studies. It is most often examined from dried skeletons, usually held in the collections of major research museums. Although they can be prepared manually, skeletons, especially those of small, delicate species, are best prepared with colonies of dermestid beetles, which conveniently consume any remaining, dried flesh. If the skeleton is retrieved from the beetles at the appropriate time, a clean, but articulated skeleton results. Study of skeletal anatomy can be enhanced through preparation of dried hone-ligament or honemuscle preparations (Hildebrand, 1968). The skeleton in situ can be studied indirectly with radiography (X-ray pictures). This is most useful for simple measurements such as long bone length and width. Stereo radiographs can be made to study more complex structures, such as the skull. Another very powerful technique for studying skeletons in situ is clearing and staining (Wassersug, 1976; Hanken and Wassersug, 1981). In this technique the surrounding flesh is enzymatically macerated and rendered transparent while the bone and cartilage of the skeleton are differentially stained red and blue, respectively. This method can be extended to include simultaneous staining and visualization of the nervous system (Filipski and Wilson, 1984,1985; Bloot et al., 1985) and the circulatory system (Russell et al., 1988). Minute elements of anatomy are revealed through light and electron microscopy. These techniques are used so widely that they fall into the realm of "standard technique" (e.g., Presnell and Schreibman, 1997), although to do them well usually requires skill learned through long experience. Most light microscope histology is carried out with tissues embedded in paraffin or paraffin-plastic polymers and sectioned on the order of 5 to 20 ^tm. Embedding in harder n\edia, such as epoxy resin, allows for thinner sections: 0.5 to 2 /xm for light microscopy and 0.01 to 0.05 yam for transmission electron microscopy (TEM). Scanning electron microscopy (SEM) reveals only surface features of cells and organs and therefore involves coating and examining whole, three-dimensional forms rather than sections.

1. Tetrapod Feeding in Vertebrate Morphology Both Ught microscopy and TEM require differential staining of cells and organelles in order to visualize the structure of interest. Both techniques dissolve, denature, or otherwise destroy some chemical constituents of the cells or tissues that one might like to reveal. Thus, instead of fixing the tissue chemically, it can be hardened and stabilized through freezing and sectioned on a microtome encased in a freezing compartment (a cryostat). In this way the chemical inclusions of the tissue are more or less preserved for visualization by treating frozen sections with stains that react with the desired compounds (histochemistry). It should be noted that all histological staining is histochemical in this sense, but usually histochemistry refers to frozen tissue techniques, which offer a greater variety and, more important, specificity of staining. 2. Functional

Techniques

Perhaps the most basic, and underrated, functional technique is observation. As His (1888) noted, "observation, though generally well marked in children, is more and more neglected, or even suppressed, by the usual school education." Careful observation of unrestricted animals performing natural behaviors is the first step of any functional analysis. Ideally, such observations are made in the field as well as in the laboratory, although this is remarkably rare in functional studies. Many functional techniques represent little more than enhancements of our powers of observation. First among these is standard photography, which captures and freezes for observation a rapid behavior, particularly if short shutter speeds and stroboscopic illumination are used; 35-mm and larger format film provides high-resolution images. Of course, photography has the disadvantage of being unable to record an entire behavioral sequence (the most rapid 35-mm motor drives are usually capable of no more than three to five frames per second). High-speed cinematography (cine film), in contrast, can capture a complete, rapid behavior (frame rates of 500 per second and higher are possible, although 50 to 250 fps is typical), but the rapid speed of the film through the camera and the small, 8- or 16-mm format reduces the resolution possible for individual frame analysis (few biologists have access to commercial 35-mm cine equipment). Furthermore, short shutter speeds and the chemistry of film emulsions require high light levels for proper exposure. Synchronized, stroboscopic illumination again can greatly enhance the resolution of individual cine frames and reduce the heat generated by photo floods. Cine is only infrequently used now that high-speed videography systems are available. Video has many ad-

15

vantages over film, including very high frame rates (up to 1000 fields per second), long recording times, high photosensitivity (only moderate light levels are necessary), and, in some cases, digital image capture and storage, but it still lacks the single-frame resolution of cine and so is not appropriate for some applications. It also has the virtue of being inexpensive to operate, although initial equipment cost is very high, whereas cine equipment is relatively less expensive, but has a high operational cost. Images generated by photography can be subjected to computer-based image analysis. Many commercial and publicly available (e.g., NIH Image) software packages permit numerous types of measurement (e.g., distance, area, image density) directly from imported images. Similarly, motion or kinematic analysis can be performed on sequential images obtained through cinematography or videography. Most often, the X-Y coordinates of relevant points on sequential images are obtained by digitizing them and these data are used for kinematic analysis. Many examples of kinematic plots are found in the chapters of this book. They show relative motion of desired points (e.g., the tips of the jaws) relative to time so that movements of various parts can be shown in synchrony and quantified throughout an entire behavioral sequence. Kinematic analyses can be coupled to simultaneous electromyography (Loeb and Cans, 1986; Cans, 1992) for information about muscle activity. Most often bipolar electrodes are used and these are inserted through a needle into the muscle of interest. The electrode measures the electrical potential across the dipole and when the muscle is active this voltage spikes. Simultaneous recording of activity in many muscles is possible; in some cases a reference muscle that exhibits rhythmic or otherwise predictable behavior is used to synchronize muscle activity patterns in separate groups of muscles measured in different experiments. Muscle activity patterns (motor patterns) are often illustrated in a summary bar diagram that shows relative onset and offset, and relative activity level in all muscles measured in conjunction with relevant kinematic plots. A variety of electronic transducers are now used to measure various functional parameters. Strain gages convert deformations along their axes into microvoltages, which can be resolved into compression and tension. Other transducers measure force, pressure, flow, etc. A unique, analogue method of goniometry for measuring minute flexion across limited-motion joints was employed by Condon (1987). In this technique a pointer and a protractor were glued to two bones

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Kurt Schwenk

across a putative kinetic joint in a lizard skull. The technique was able to measure deflections as small as T, far better resolution than that provided by cineradiographic and strain gage techniques used in previous studies. This technique deserves to be exploited more widely. Lauder has introduced the use of Digital Particle Image Velocimetry in the analysis of fish locomotion (Lauder et al, 1996; Drucker and Lauder, 1997). This method is a great advancement over traditional flow visualization techniques, exploiting the use of laser light to illuminate a precise plane of particles in a flow tank, which are recorded on high-speed video. Software permits a three-dimensional reconstruction of fluid direction and velocity over time. This review has touched on only some of the anatomical and functional techniques employed by modern morphologists. There are many others, particularly if one includes specialized forms of light and electron microscopy and neurological techniques; however, this brief overview should provide an adequate introduction to the field and subsequent chapters of this book. III. C O N C L U D I N G C O M M E N T S If nothing else, the preceding overview should reveal that modern vertebrate morphology is a diverse and intellectually vibrant field. It is unique among the biological sciences in its combination of ancient knowledge with cutting-edge technological and conceptual advances. At its best it is the most integrative of sciences, moving fluidly among hierarchical levels and drawing insight from the interplay of disciplines as divergent as molecular genetics and community ecology. It is hard to imagine a more synthetic field, nor one more fundamentally relevant to the the cornerstones of comparative biology: systematics, evolutionary biology, and ecology. Nonetheless, as a discipline it has suffered its share of indignities, periods of professional and institutional stagnation, and even the sneering disregard of its neophytic, reductionist cousins. We have seen the early, impudent promises of molecular genetics to obviate morphology by "answering" the ultimate questions of phenotypic evolution fade as the emergent complexity of genetic, developmental, and functional systems becomes ever more apparent. I therefore conclude this chapter as I began it—by proclaiming that phenotypic approaches to comparative biology are not only deeply interesting, they are essential. If nothing else, the property of emergence requires that this is so. It is fruitless and petty to argue for primacy of one hierarchical level over another. Morphology shows us clearly that organisms are webs of interaction

and integration, not linear chains of cause and effect. Our task is to connect hierarchies, to hlur their boundaries, not to separate them. Morphologists are uniquely poised to contribute in this regard. Dramatic advances will emerge from explicit attempts to integrate topdown and bottom-up approaches in the study of form and function. Acknowledgments I am grateful to Nirvana Filoramo, Ken Kardong, Carl Schlichting, and Giinter Wagner for commenting on the manuscript. Willy Bemis pointed out some useful references. Preparation of the manuscript was supported by grants from the University of Connecticut Research Foundation and the National Science Foundation (NSF IBN-9601173) to the author.

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C H A P T E R

2 An Introduction to Tetrapod Feeding KURT SCHWENK

Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut 06269

11.

III. IV. V.

A phylogeny of the Tetrapoda and its relatives is given in Fig. 2.1. All taxon names used in this chapter are in reference to this phylogeny. More detailed phylogenies for particular clades are given in subsequent chapters.

INTRODUCTION A. Feeding Form and Function: Background B. Anatomical Terminology C. Phylogenetic Terminology MORPHOLOGY OF THE FEEDING APPARATUS A. Skull and Mandible B. Teeth C. Keratinous Structures D. Hyobranchial Apparatus E. Jaw Musculature F. Hyobranchial Musculature G. Tongue H. Pharynx I. Cheeks, Lips, and Probosces KINEMATICS OF FEEDING: THE GAPE CYCLE KINEMATICS OF FEEDING: FEEDING STAGES A. Overview B. Stages of the Feeding Cycle CONCLUDING REMARKS References

A. Feeding Form and Function: Background Feeding and excreting are common to all animal life. Feeding is required by virtue of the fact that animals, unlike plants (and other autotrophic organisms), cannot harness directly the radiant energy of the sun—the ultimate source of all energy on Earth. Excretion occurs because in every mouthful of material ingested there is some portion of it that an animal cannot assimilate. Solid matter is excreted via the gut, and following intracellular energy extraction, other molecular detritus is eliminated via the urinary system. Apart from the obvious waste implied by excretion, there is a more subtle inefficiency built into every digestive process—the conversion of energy from one form to another. Food that is processed and digested is ultimately reduced to its molecular components and these are circulated throughout the body via the blood-vascular system. Different food molecules have different fates and even the same molecule can be treated differently depending on the physiological state of the individual, but most food is eventually broken down into glucose molecules. These are transported across membranes into the cytoplasm of every living cell and are then systematically dismantled and oxidized in a process known as cellular respiration.

I. INTRODUCTION This chapter serves as a primer for the study of tetrapod feeding systems. It provides a brief overview of feeding form and function, introducing general concepts and a basic vocabulary. Its goal is to prepare the reader for the more detailed, taxon-based chapters that follow, and for the primary literature in functional and evolutionary morphology of tetrapod feeding.

FEEDING (K.SchwenKed.)

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Copyright © 2000 by Academic Press. All rights of reproductioi\ in any form reserved.

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Kurt Schwenk

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FIGURE 2.1. (a) Generally accepted phylogenetic relationships among chordates, including vertebrates. The tetrapod sister taxon, Osteolepiformes, is an extinct group of sarcopterygian fish (e.g., Ahlberg et ah, 1996). Urochordata includes the tunicates, or sea squirts, and Cephalochordata contains the amphioxus, Branchiostoma. Myxini and Petromyzontia are the hagfishes and lampreys, respectively, representing the only extant jawless fishes. Chondrichthians are the cartilaginous fishes and actinopterygians are the bony, ray-finned fishes. Dipnoi are lungfish. (b) Relationships among tetrapod vertebrates. There is some contention about relationships in each of the major clades. Amphibia, Reptilia, and Mammalia (turtles are discussed in the text); however, the phylogeny shown represents a traditional, conservative view.

Cellular respiration releases the energy held in molecular bonds so that it can be used to create new molecules and to drive various chemical reactions constituting the work of the cell. However, not all energy released can be converted into a usable form. Some of it is relinquished as heat. For most ectothermic vertebrates (fish, amphibians, and nonavian reptiles) this small amount of heat is of little consequence—they must depend on extrinsic sources of warmth to elevate their body temperatures above ambient, if at all. Although they might regulate their body temperatures behaviorally during periods of activity, terrestrial ectotherms nevertheless tolerate significant diurnal and

seasonal fluxes. For endotherms (birds and mammals), in contrast, cellular work proceeds fast enough that "waste" heat can be exploited to warm the body core so that a nearly constant high body temperature is maintained. As a consequence, the cellular biochemistry of endotherms has been evolutionarily optimized for these conditions. Indeed, large fluxes in body temperature can be fatal. Primarily physiological, but also morphological and behavioral, mechanisms serve to maintain core temperature within very narrow limits, even when ambient temperature is much lower or higher. These processes are relevant in the context of tetrapod feeding systems in two ways: first, each time energy is converted—initially from solar energy to the chemical bonds within plant cells, then from plant tissue to animal tissue when herbivores feed on plants, and finally, from one type of animal flesh to another type when carnivores feed on other animals—significant amounts of energy are lost in the process. The inherent inefficiency of energy conversion has far-reaching ramifications for the organization of life on earth. At the most basic level it explains, for example, why herbivorous species are far more numerous than carnivorous species. As one ascends trophic (energy conversion) levels, less and less of the solar energy originally harnessed by plants is available to convert into individual animal bodies. In any given food web, therefore, there is far more biomass represented in herbivorous individuals than in carnivorous. This translates into the fact that there are more herbivorous than carnivorous individuals in a given ecosystem, and ultimately there are more herbivorous than carnivorous species of animal. Thus, in considering the functional morphology and evolution of feeding systems among tetrapods, we might expect a greater diversity of herbivorous forms than carnivorous. However, such patterns reflect ecological, not phylogenetic generalities, hence a particular clade may not conform to this expectation, particularly if it derived from a diet-specialized ancestor. Herbivory, for example, is quite unusual among lepidosaurian reptiles, possibly because they descended from an insectivorous ancestor (Chapter 8), whereas in turtles, herbivory is the rule. Certainly many mammalian orders are committed to one particular food type, but if one considers the mammalian or synapsid clade in toto, the predominance of herbivores becomes apparent (Chapter 13). Second, thermal physiology has had significant consequences for the evolution of tetrapod feeding systems. While endotherms might seem to benefit dramatically from a metabolic life in the fast lane, there is a cost—the constant need to fuel high rates of intracellular chemical work. After only hours without

2. An Introduction to Tetrapod Feeding food, the blood glucose levels of an endotherm are exhausted and it begins to metabolize fatty reserves— and eventually, its own flesh—to meet the unceasing demand of its cells for energy. The perpetual need to provision its metabolic machinery requires an endotherm to feed regularly and frequently. Except for a few species that hibernate or aestivate, few endotherms can tolerate lengthy fasting. This problem is exacerbated in some herbivorous species whose high-fiber, low-nutrition forage requires them to spend practically all waking hours procuring and processing food. In contrast, ectotherms need not squander calories solely to maintain a constant, high-body temperature. Thus, ectotherms decrease their daily caloric demand by permitting body temperature to fall during periods of inactivity. Many species can go for days, weeks, or even months without food, virtually shutting down metabolically and entering into a sort of suspended animation until conditions are once again favorable for activity and feeding. This allows them to survive and even to reproduce in places, and through periods of time, no bird or mammal could. Hence, ectothermy is a distinct and cost-effective evolutionary strategy, not merely an inefficient step on the way to endothermy (e.g., Pough, 1983). A consequence of these patterns is that an endotherm must eat far more than a like-sized ectotherm and it must digest its food as efficiently as possible in order to liberate its caloric content quickly and completely. The key to meeting this need is not an increase in digestive efficiency (i.e., the amount of energy liberated per unit mass of food), which is similar in ectotherms and endotherms, but an increase in the rate at which the food is passed through the gut and processed (Karasov and Diamond, 1985, 1988). A critical component of rapid digestion in endotherms is that they initiate significant mechanical and chemical reduction of the food before it enters the stomach. In mammals these adaptations are primarily associated with the teeth and jaws of the masticatory apparatus, and in birds the crop and gizzard serve analogous functions. Ectothermic tetrapods, in contrast, reduce their food comparatively little before it enters the stomach. Indeed, most amphibians and reptiles engulf and swallow food items whole and virtually all digestion occurs chemically within the gut. While some ectotherms (particularly some lizard species) do puncture, slice, or crush their food, they achieve only a paltry level of comminution as compared to mammals whose precise dental occlusion and masticatory orbit allows them to reduce food to a slurry of minute particles and salivary enzymes before it even reaches the esophagus! A profound evolutionary consequence of this fact is that mammalian and, to a lesser extent, avian feeding

23

systems show high dietary specificity in their phenotypes, whereas the feeding systems of amphibians and reptiles generally reflect not what food is eaten, but how it is eaten. In other words, in endotherms there is a relatively tight fit between phenotype and diet, but in ectotherms the fit is loose—a given feeding system accommodates a variety of food types. In sum, the biophysics of energy conversion at the molecular level leads to the basic ecological observation that herbivorous animals are more numerous than carnivorous. The independent evolution of endothermy in birds and mammals was associated in each case with sweeping morphological changes, including adaptations in the feeding apparatus that enhance rapid mechanical and chemical reduction of food before (and after) it enters the stomach. B. Anatomical Terminology Standard anatomical terminology is used freely throughout the book so it is advisable to review it very briefly here (Fig. 2.2). This information is available in any good comparative anatomy text or dissection guide (e.g.. Walker and Homberger, 1992; other citations later). Vertebrate animals are bilaterally symmetrical and most descriptors are defined with reference to the natural planes and axes of the body. Unfortunately (but not surprisingly), most of the earliest anatomical work was concerned with humans (Chapter 1) which are unique in their upright stance and bending of the cranial axis. Thus some human-based anatomical terminology is nonstandard in a comparative context. The standard nomenclature reviewed here is based on quadrupedal animals, and points of disagreement with human-based terms are noted where relevant. "Vertical" and "horizontal" are used with reference to the surface of the earth. Anterior and posterior refer to the head and tail ends of the body, respectively. A limb, for example, might be said to swing anteroposteriorly, meaning from front to back. Sometimes cranial and caudal are used instead. A structure or movement toward the head is craniad, toward the tail, caudad. If one's point of reference is within the head, then rostral (toward the nose) is substituted. A structure on the under or belly side is ventral and one on the upper side, or back, is dorsal. In humans, superior and inferior are used instead of cranial and caudal, and anterior (front) and posterior (back) are substituted for ventral and dorsal. Hence anterior and posterior have completely different meanings in human vs comparative anatomy (Fig. 2.2). Left and right are always with reference to the animal's left and right, not the viewer's (analogous to

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Caudal

Anterior

(Posterior)

Transverse plane

Frontal plane

Inferior

F I G U R E 2.2. Standard anatomical terminology for quadrupedal and bipedal tetrapods. See text for discussion. From ''Functional Anatomy of the Vertebrates: An Evolutionary Perspective/' Second Edition, by W. Walker and K. Liem, © 1994 by Saunders College Publishing, reproduced by permission of the publisher.

"stage left" and "stage right"). Relative to the longitudinal axis, lateral means "to the side" and medial means "toward the axis," or midline. If soniething lies exactly in the midline it is median (e.g., median fins as opposed to paired, lateral fins). Distal and proximal are relative terms that mean farther from or nearer to (respectively) a given reference point (often, but not necessarily, the midline of the body). For example, the hand is distal to the upper arm, the upper arm is a proximal limb segment. The longitudinal axis of symmetry also defines several planes of section. A sagittal section is a vertical, longitudinal plane through the axis, or midline, of the body. As such, it divides the body into left and right halves. Although, by definition, a sagittal section is in the midline, it is usually specified as such by referring to it as midsagittal to distinguish it clearly from sections in the sagittal plane but away from the midline, or parasagittal sections. A vertical section that is perpendicular to the sagittal plane, running across the body from left to right, is transverse. A frontal section lies in a horizontal, longitudinal plane. In humans, a transverse section corresponds to the quadrupedal condition in cutting left to right across the axis, but because of the vertical posture it is now a horizontal plane (Fig. 2.2). Similarly, a frontal section is now vertical (if a human were to assume a position on "all fours" the planes would revert to their standard orientation). A section in the frontal plane in humans is usually referred to as a coronal section because it

aligns with the coronal (frontoparietal) suture of the skull roof. With reference to the head, this usage becomes particularly problematic. This is because the evolution of human bipedality was accompanied by a radical reorientation of the cranial axis such that the ancestral (quadrupedal), longitudinal axis of the skull was bent 90°. The facial skeleton retains, more or less, its original orientation, but the skull base is deformed (relative to quadrupeds) so that the spinal cord emerges from the occiput vertically (ventrally), rather than horizontally (posteriorly), to accommodate the upright spine. Thus, a coronal section in a human head would correspond to a transverse section in a quadruped, whereas a transverse section in a human head would correspond to a frontal section in a quadruped! The term "coronal" is only applicable to humans and other anthropoid primates. Its general use in comparative anatomy is strongly discouraged. Elevation refers to raising a structure relative to a reference point and depression to lowering it. Muscles that elevate are called elevators (or sometimes, levators) and muscles that depress are depressors (similarly for the following terms). Flexion refers to bending something or, specifically, to decreasing the angle between two skeletal elements, such as limb bones, whereas extension extends, or increases, the angle. Adduction is movement toward a point of reference (usually the ventral midline of the body) and abduction is movement away from the reference. Jaw closure, for example, is jaw adduction and the muscles that accomplish this are

2. An Introduction to Tetrapod Feeding usually referred to as jaw adductors (occasionally, jaw levators). Opening the lower jaw (mandible) is called jaw depression and the muscles that accomplish this in nonmammalian tetrapods are the mm. depressor mandibulae (the prefix m. is an abbreviation for the Latin term musculus and is used in formal descriptions of muscles; mm. is the plural form, i.e., the depressor mandibulae muscles). Protraction moves something forward, or out (when the tongue is protruded out of the mouth it is protracted), and retraction is the opposite. Rotation refers to movement around an axis, such as jaw rotation about the jaw joint. Twisting rotation around a central, longitudinal axis is axial rotation. C. Phylogenetic Terminology As for anatomy, a phylogenetic vocabulary is necessary to appreciate fully most current evolutionary morphology. In-depth treatments of these and related topics can be found in the following references, but a very brief review of terms is included here for convenience (see Hennig, 1966; Wiley, 1981; Forey et al, 1992; de Queiroz and Gauthier, 1994; Sanderson and Hufford, 1996). A taxon (pL, taxa) is a formally recognized group of organisms representing any hierarchical or categorical level in a classification. The lizard species Varanus niloticus is a taxon, as is the genus Varanus, the family Varanidae, and the suprafamilial group, Varanoidea. In cladistic usage, a taxon is expected to be natural, or monophyletic, but many traditionally named taxa are not (e.g., Invertebrata, or the traditional use of Reptilia, which excludes birds). A monophyletic group, or taxon, is one which includes an ancestor and all of its descendants (hence, the cladistic use of Reptilia includes birds because birds and "typical" reptiles share a common ancestor). A monophyletic group of organisms is also called a clade. A group that includes an ancestor and some, but not all, of its descendants is paraphyletic. The traditional notion of Reptilia again serves as an example: if we trace all living reptiles to their common ancestor, this same ancestor would also be shared by birds. Hence, to exclude birds from the taxon Reptilia would be to define a group that excludes some of the descendants of a common ancestor, i.e., a paraphyletic group. There is disagreement on how best to define a polyphyletic group. It is perhaps most easily thought of as a taxon in which the ancestor is not included (Hennig, 1966). This usually results when a taxon is defined not on the basis of its evolutionary descent, but on the basis of superficial similarity. For example, if the class Mammalia is defined as a taxon containing only those species with a dentary-squamosal jaw joint (as was traditionally done), then this taxon would be polyphyletic because such a jaw joint

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evolved independently in several synapsid lineages. To make this group monophyletic we would have to trace these separate lineages back to their common ancestor and include it and all intermediate species in Mammalia, but not all mammals thus defined would have a dentary-squamosal jaw joint, the feature regarded as definitive of the taxon. In order to base modern classifications on monophyletic groups, it is preferable that taxa be defined according to their cladistic relationships (i.e., on the basis of a common ancestor and all of its descendants) rather than according to the presence of some "key" character (de Queiroz and Gauthier, 1994). A character is a homologous trait or attribute of a group of organisms (e.g., Wagner, 1996). It is a unit of phenotypic evolution that is developmentally individuated from other characters around it (Wagner, 1999). As such it is assumed that its evolution is largely, or entirely, uncorrelated with the evolution of other characters. This assumption can only be partially true because all characters in an organism are to some extent correlated with all others (e.g., Schwenk, 2000b); however, it is also true that some features of organisms evolve largely independent of change in other features. All phylogenetic analyses begin with a character analysis: identifying characters, documenting their various forms, or states in different taxa, and then determining which state of the character is plesiomorphic {primitive or representative of the ancestral condition) and which states are apomorphic {derived, or newly evolved). The character analysis is done with reference to a particular, monophyletic group of interest, the in-group. "Derived" and "primitive" are relative terms only applicable to character states with reference to a particular in-group. In other words, a character cannot in any absolute sense be considered "primitive"—a form, or state, of the character is only primitive in the context of a comparative analysis applied to a particular ingroup. The nearest clade to the in-group taxon is its sister group, i.e., the in-group and the sister group share a nearest common ancestor. More distantly related taxa are referred to as out-groups. Character states within the in-group are usually determined to be primitive or derived based on comparison to outgroup character states {out-group comparison). The character state inferred to exist at the common ancestor of the in-group and the first out-group defines the plesiomorphic state and other states of the character are, therefore, regarded as derived within the in-group. A derived character state shared by two or more taxa is said to be a synapomorphy. A shared primitive character state in two or more taxa is called a symplesiomorphy. Character similarity that is independently evolved, either convergently or in parallel, is known as homoplasy. Only synapomorphies are taken as evidence

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of evolutionary relationship. Sharing a trait implies that the taxa in question share a common ancestor in which the trait evolved uniquely. In contrast, similar appearance stemming from characters that are symplesiomorphic simply means that the character failed to evolve from the ancestral condition. Such similarity gives no information about relationship. For example, the presence of hair is of little use in reconstructing the relationships of an in-group including only living mammals because this trait is symplesiomorphic for the group. However, if our in-group were expanded to included both reptiles and mammals, then hair would be a synapomorphy uniting the mammal species because it evolved once in their common ancestor. Hence, phylogenetic hypotheses, depicted as branching patterns representing putative genealogical relationships {cladograms), are constructed from patterns of synapomorphy only and monophyletic taxa are likewise diagnosed by lists of synapomorphies. Homoplasies potentially confound our ability to discern evolutionary relationships based on character analysis, but a key assumption in phylogenetic analysis is that the simplest solution is the correct one. This is known as the principle of parsimony. In other words, it is assumed that character evolution is a more-or-less direct process that does not usually reverse itself; nor is detailed similarity expected to evolve independently. Thus, a phylogenetic tree (cladogram) that minimizes the number of homoplasies necessary in character evolution is usually the goal of phylogeny reconstruction.

II. MORPHOLOGY OF THE FEEDING APPARATUS As noted in Chapter 1, the functional-morphological approach to vertebrate feeding is primarily concerned with the acquisition, processing, and swallowing of food (see later). Hence, our treatment of morphology is limited to the structures which participate in these functions, for the most part located in the head and neck. Much greater detail for many of these topics will be found in the following chapters; however, not all structures (and functions) reviewed here are relevant to every taxon or functional type. A. Skull and Mandible 1, Origin and

Development

Perhaps no single structure is more quintessentially vertebrate, nor more evocative of the whole, living organism, than the skull. It concentrates in one place most of the feeding apparatus, the braincase and the sensory

capsules, and it is this combination of attributes that makes the skull so revealing about an animal's habits. This is particularly true for mammal skulls whose jaw configurations and dental batteries are especially revelatory about diet and feeding function. The skull is a diagnostic vertebrate (or craniate) character. Indeed, the vertebrate head, or at least its anterior part, is widely regarded as an entirely novel structure built around the contributions of two, new, embryonic, ectodermal tissues, the neural crest and epidermal placodes (Northcutt and Cans, 1983; Gans, 1989,1993). Evolution of a head (a trend called "cephalization") and other novel aspects of vertebrate complexity seem to have been permitted by duplication of the ancestral Hox gene array, as inferred from the condition in Branchiostoma (the amphioxus), a member of the vertebrate sister group, Cephalochordata (e.g., Garcia-Fernandez and Holland, 1994; P. Holland et al, 1992; P. Holland and Garcia-Fernandez, 1996; L. Holland et al, 1996; L. Holland and Holland, 1998) (Fig. 2.1). Gene duplication is an important, if not the most important, mechanism for the introduction of novelty and complexity in evolving lineages (e.g., Arthur, 1997; Nowak et al, 1997), and the Hox (and related) genes are especially important in this regard because their expression controls patterning along the anteroposterior body axis, including the head (e.g., Hanken and Thorogood, 1993). The fact that the tetrapod skull is usually a unitary, structural entity belies its terrific complexity and composite nature (Fig. 2.3). It is, first of all, composed of many individual bones or cartilages that fuse or become sutured together, and these derive from different embryonic and evolutionary sources. Patterns of loss, fusion, and integration among elements vary considerably among lineages so that skull form is widely divergent among tetrapods. Skull is a nontechnical term that usually refers to the braincase and facial skeleton, including the upper jaw, but it must be kept in mind that the total head skeleton also includes the lower jaw and the hyobranchial apparatus (Fig. 2.4). The latter is touched upon here, but is treated more fully in a separate section later. Minimally, morphologists recognize three basic components of the vertebrate head skeleton (Fig. 2.3): the chondrocranium (or neurocranium), splanchnocranium (or viscerocranium), and dermatocranium (or dermal skull). Elements of each are present in the head skeletons of adults in all craniate (vertebrates excluding hagfish; e.g., Janvier, 1996) groups except the lampreys and Chondrichthyes, which, lacking bone in their skeletons, do not form dermatocranial elements. These separate sources of cranial elements are most clearly evident in early developmental stages. In later

2. A n I n t r o d u c t i o n to T e t r a p o d F e e d i n g

a. Chondrocranium

Otic capsule Opisthotic

Prootic

Vertebrae (

Basi-ExOrbitosphenoid Presphenoid Mesethmoid Supraoccipitals Basisphenoid Sphenethmoid (lower tetrapods)

Hyomandibula (

3d-5th arches

Hyoid arch

27

^ Meckel's cartilage

Palatoquadrate

Mandibular arch

Columella (stapes - ^ ^ of mammals) Quadrate (Incus Articular Epipterygoid of mammals) (malleus of mammals)

The chondrocranium forms first in cartilage. It provides a basin for the brain at the anterior end of the notochord and "capsules," which contain most of the special sensory structures (e.g., nose, eyes, ears). In cartilaginous fishes the basin is roofed with cartilage and the sensory capsules are fused to its sides to form a solid, enclosed structure. This chondrocranial structure remains as the adult skull in Chondrichthyes. In bony vertebrates, however, the cartilaginous model of the chondrocranium eventually ossifies (a process known as endochondral ossification). The brain basin is roofed by dermal bone (see later), which also forms most of the facial skeleton and palate. These dermal bones fuse insensibly with the endochondral bones of the chondrocranium to form the unitary skull. Sometimes even sutural junctions between ossifications centers are lost so that an apparently single bone in the adult skull, such as the mammalian temporal bone, is actually a composite structure. In adults of most species the chondrocranial contribution to the skull is most apparent at the occiput, surrounding the foramen magnum and forming the floor and walls of the braincase. h. Splanchnocranium

Vault series Orbital series Temporal series' Palatal series — Mandibular

FIGURE 2.3. A series of ontogenetic stages in the development of the tetrapod head skeleton showing contributions of the chondrocranium (dark shading), splanchnocranium (no shading), and dermatocranium (medium shading). Bones and cartilages derived from each ontogenetic source join and merge to form the adult skull. Reproduced from Kardong (1998), with permission of The McGrawHill Companies.

stages of growth, individual cranial elements become reduced, lost, ossified, fused, or invested by new bone so that the composite origin of the adult skull is obscured. The information reviewed briefly here is covered in greater depth in most comparative anatomy texts (e.g.. Walker and Liem, 1994; Hildebrand, 1995; Kardong, 1998) and in other, more specialized sources (e.g.. Flower, 1885; Bolk et al, 1936; de Beer, 1937; Romer, 1956; lordansky, 1973; Langston, 1973; Trueb, 1973; Moore, 1981; Hanken and Wake, 1982; Duellman and Trueb, 1986; Kuhn and Zeller, 1987; Hanken and Hall, 1993).

The splanchnocranium also forms initially as cartilage. In the early chordate ancestors of vertebrates the splanchnocranium supported the walls of the pharynx and is presumed to have served as a filter feeding basket, as in living ammocoetes (larval lampreys) and amphioxus. It consisted of a series of U-shaped arches (visceral arches) with openings in between through which water was expelled to create a one-way feeding current through the pharynx. It is believed that the visceral arches eventually developed joints and an intrinsic musculature capable of flexing them, putatively to create a more efficient, muscular pump for filter feeding. Gills also became associated with the arches so that water flow through the pharynx served both to transport food and to oxygenate the blood as it passed out the pharyngeal (now gill) slits. In one group of vertebrates, the gnathostomes ("jaw mouths"), the first arch became modified to open and close the mouth, thus effectively transforming the first arch into jaws (Forey and Janvier, 1993; Janvier, 1996). The jaws, or mandibular arch, became attached to the chondrocranium along its upper portion. Although the origin of jaws is traditionally attributed to feeding function and the evolution of a more active, predaceous lifestyle (e.g., Northcutt and Gans, 1983), the initial impetus may have been respiratory in that jaw closure could seal the pharynx to prevent reflux of water

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Kurt Schwenk

pd

p'a

of

pi pa

frm

FIGURE 2.4. Skull of a gymnophione amphibian {Dermophis mexicanus) shown in dorsal (a), ventral (b), and lateral (c) views. The left mandibular ramus (one-half of the mandible) is shown in lateral (d) and medial (e) views. From Wake and Hanken (1982), Journal of Morphology, copyright © 1982, John Wiley & Sons. Reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.

during its forceful expulsion posteriorly out the gill slits (Mallatt, 1996). In any case, jaws and, shortly thereafter, teeth became associated with the ability to grasp and consume larger, more active prey, and the ancestral mode of filter feeding was lost in gnathostomes (many living fish and some aquatic tetrapods have reevolved filter feeding systems secondarily). The second visceral arch was modified along with the first. Its upper elements connected the jaw joint to the otic (ear) region of the chondrocranium, bracing or suspending the posterior end of the first arch jaw. Its lower elements supported the floor of the mouth and, through rapid depression, could expand the pharynx to produce suction. More posterior arches supported the gills. The second visceral arch is referred to as the hyoid arch, and those posterior as branchial arches. In living fishes, particularly cartilaginous fishes, the splanchnocranium is little changed from the condition just described. However, in bony fishes many of the arch elements either ossify directly or become overlain by dermal bone (see later). The branchial arches are hidden beneath a large, bony operculum and other superficial, dermal bones of the head skeleton. In

tetrapods, some aquatic (mostly larval) forms retain gills and these continue to be supported by branchial arches. However, in terrestrial tetrapods the splanchnocranium is highly modified and often difficult to detect in adults. Some arch elements are entirely lost, as are portions of others; some ossify into separate bones, some fuse, some are covered over, and virtually all are transformed to serve various functions. The upper and lower jaws, for example, continue to form as cartilaginous, visceral arch elements in embryos, but these are soon ensheathed by dermal bones as development proceeds. The upper jaw cartilage, in particular, is covered over and fused to the ossifying chondrocranium and the dermal bones of the facial skeleton. However, various bits of the visceral arches ossify directly to create small bones, which contribute in various ways to the adult skull (Fig. 2.3). The posterior ends of upper and lower jaw cartilages, for example, ossify into the bones of the jaw joint in all nonmammalian tetrapods (a lower articular and an upper quadrate bone). The dorsal component of the hyoid arch (the hyomandibula) is robust in early tetrapods and putatively served to transmit low-frequency vibrations from the lower jaw

2. An Introduction to Tetrapod Feeding to the ear. During tetrapod evolution the hyomandibula is increasingly reduced in size, becoming more sensitive to airborne, high-frequency vibration, particularly in association with the evolution of a tympanum (ear drum), and is thus modified into a middle ear ossicle (now called the stapes). The ventral component of the hyoid arch fuses, or becomes articulated with, elements of the first and second branchial arches to form the hyobranchial apparatus (tongue and throat skeleton; see later). Other branchial arch elements contribute to the cartilages of the larynx and trachea. In mammals, a new jaw joint evolved between two dermal bones of the skull (the dentary of the lower jaw and the squamosal of the upper) and the original, endochondral jaw joint bones (articular and quadrate) were incorporated into the middle ear along with the stapes to form a chain of three middle ear ossicles (malleus, incus, stapes, respectively) (e.g., AUin, 1975, 1986). Other small ossifications of the first arch cartilages are incorporated into the mammalian skull as well. The evolution of the mammalian middle ear system from components of the ancestral jaws is one of the most dramatic and best documented gradual, morphological transformations in vertebrate history. c. Dermatocranium The dermatocranium is represented by a series of bones that ossify directly without a cartilage precursor. Most dermal ossification is relatively superficial, tending to form sheet-like ("intramembranous") bones and struts that either stand alone or invest chondro- or splanchnocranial cartilages (hence dermal bone is often referred to as "membrane" bone). Most of what gives shape to the adult, tetrapod skull is dermal bone. In mammals, the dermatocranium is a particularly dominant feature of the skull and most cranial adaptation is manifested here. In general the skull can be divided topologically into the braincase and the facial skeleton (van der Klaauw, 1945). This is particularly true for mammals. The facial skeleton comprises the snout and jaws, which are almost entirely dermal. The base of the braincase forms from the chondrocranium, but its sides and roof form from dermal bone. The dermatocranium, and skull generally, can be further subdivided according to various parameters. Some anatomical subdivisions of the skull are considered next. 2. Anatomical

Units

We can decompose the tetrapod skull into a number of anatomical units or, more accurately, topological regions because it is unlikely that these regions are individuated in developmental, functional, or evo-

29

lutionary senses (Schwenk, 2000b; see van der Klaauw, 1945). However, it is convenient to consider them separately because, to some extent, clade-specific adaptations and trends are circumscribed within each. a. Braincase The braincase surrounds and protects the brain. It is derived primarily from the chondrocranium. It is surprising that in many tetrapods, such as lizards, the braincase is not enclosed entirely in bone; much of its inner, anterior portion is membranous. However, in fossorial (burrowing) members of the clade, or in those with a fossorial ancestry, such as snakes, the braincase becomes completely osseous, as it is in most tetrapods. The posterior end of the braincase is perforated by a large foramen magnum, the opening for the spinal cord. One or two occipital condyles protrude lateral or ventral to the foramen magnum and these articulate with the first vertebra, the axis. The ability to rotate the head is a tetrapod novelty, as is a neck, both reflecting enhancement of head mobility characteristic of terrestrial vertebrates. In general, the largest portion of the jaw-closing musculature takes it origin on the side, and sometimes the top, of the braincase, passing ventrally to insert along the lower jaw (see later). In some taxa, this musculature and most of the braincase are obscured by lateral expansions of the dermal roofing bones so that a cavity is formed between the braincase and the dermal roof, which is filled in life by the jaw musculature (e.g., many turtles). The braincase incorporates the otic capsules of the chondrocranium into its base, and this dense, bony region contains the semicircular canals and other sensory structures of the inner ear. Air- or ground-borne vibrations are carried to the inner ear by one (most tetrapods) or three (mammals) tiny ear ossicles that bridge an air-filled cavity called the middle ear. In most tetrapods the ear ossicles are connected laterally to a tympanum (ear drum), but in some species a tympanum is absent and low-frequency vibrations are collected by the lower jaw or the skin at the side of the face (a tympanum evolved several times independently among tetrapods). The middle ear cavity forms from the embryonic first pharyngeal pouch (e.g., Kardong, 1998). Continuity of the middle ear cavity and the pharynx is maintained in most tetrapods (in some lizards light held up to one ear can be seen through the other!), but in mammals the middle ear is a separate cavity, which, in most species, is expanded into a bubble-like chamber called the bulla. The mammalian pharynx is highly modified relative to other tetrapods (see later) and its connection to the middle ear cavity is restricted to a narrow, soft tissue slit (the Eustachian tube).

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Kurt Schwenk

b. Jaws While the upper jaw is, in most cases, fused to the facial skeleton by dermal bone, the lower jaw is articulated with it at the jaw joint and is referred to as the mandible (sometimes in the bird literature, upper and lower bills are both referred to as mandibles, but this is an idiosyncratic usage). Although the upper jaw is rarely as movable as the lower, in some species with kinetic skulls, independent movement of the upper jaw is possible, which may have significant functional consequences. In typhlopid snakes, for example, each maxilla of the upper jaw can pivot through a significant arc, sweeping ant and termite larvae into the mouth with large, anteriorly directed teeth (Parker and Grandison, 1977; Kley, 1998, unpublished data), and in snakes, generally, the upper jaws are independently movable within the highly kinetic skull (Chapter 9). Most tetrapod jaws contain teeth of various sorts (see later) that form a margin around the mouth. The premaxilla and maxillae of the upper jaws and dentaries of the mandible are the dentigerous (tooth-bearing) bones of the jaws. The jaw joint lies between two splanchnocranial bones, the (lower) articular and the (upper) quadrate, in all tetrapods except mammals in which it is between two dermal bones, the dentary and squamosal. As noted earlier, the articular and quadrate were incorporated into the middle ear of mammal ancestors. The jaw joint is highly variable in position, form, and function, but in most cases it acts primarily as a hinge, permitting vertical rotation of the mandible (depression and elevation). Species whose feeding mode requires limited rotational movement of this type have a joint morphology restricting lateral and anteroposterior deviation of the mandible so that it is virtually 'Tocked" into position (e.g., many carnivoran mammals). However, in herbivorous mammals, some turtles, and several other tetrapod taxa, considerable movement is possible at the joint so that the mandible is capable of more complex motion, including side-to-side rotation and anteroposterior sliding. In rodents, for instance, the mandible slides forward to engage upper and lower incisor teeth for gnawing and then slides back for molar occlusion during grinding. In general, jaw mechanics are far more complex than the simple scissors action implied by a hinge joint (Greaves, 1995). Three-dimensional considerations, such as the height of the jaw joint relative to the tooth row and the fact that chewing usually occurs on one side at a time, have important consequences for the form of the jaw, the nature of the mandibular symphysis, the placement of the teeth on the jaws, the optimal bite point, and the activity of the jaw muscles (e.g.. Bramble, 1978; see Greaves, 1995, for an overview).

Left and right halves of the mandible are joined anteriorly at a joint of varying firmness. In most species this joint is extremely tight and fibrous and called a symphysis. The mandibular symphysis is particularly well developed in mammals (e.g., Scapino, 1965,1981; Beecher, 1979) and well suited to resisting the tortional stresses associated with asymmetrical chewing (Hylander, 1985). In other groups a true symphysis does not form and some movement is possible. This is particularly true for most snakes and some salamanders in which there is a high degree of bilateral asymmetry in feeding movements (e.g., Bellairs, 1984; Cundall et ah, 1987; Elwood and Cundall, 1994). In advanced snakes, left and right halves of the mandible are virtually unattached, allowing them to expand the oral apparatus in order to engulf prey larger than the head (Gans, 1961; Bellairs, 1984; Young, 1998). c. Facial Skeleton The facial skeleton is a system of dermal bones that protrudes anteriorly off the braincase. It comprises the snout, upper jaws, and palate (the latter two are considered further in separate sections) and, in life, contains the eyes and nose. In mammals, the form of the facial skeleton is largely influenced by the latter two sensory systems: nocturnal species tend to have very large, prominent orbits, whereas those species with very sensitive olfactory systems tend to have long snouts. However, these are rough correlations and the shape of the facial skeleton is affected by many other factors. For example, ant- and termite-feeding mammals nearly always acquire an elongate, tapered snout that accommodates a long, slender prehensile tongue, together used to probe nests (Chapter 15). In birds, bill form is indicative of feeding mode (Chapter 12), and although the bill is a keratinous investment of the upper and lower jaws, the facial skeleton largely mirrors the form of the bill (Bock, 1966). Fossorial species of all kinds, such as gymnophione amphibians (Fig. 2.4) and amphisbaenian squamates, exhibit heavily ossified snouts with adjacent bones tightly sutured to withstand the stresses of burrowing (M. Wake, 1993). In contrast, the facial skeleton of most other amphibians and squamates is quite a delicate affair of struts and vacuities. Facial shortening is a prominent feature of anthropoid primate evolution and is noteworthy in a variety of other taxa, such as feliform (cat-like) carnivoran mammals and algae-scraping marine iguanas {Amblyrhynchus). Shortening of the facial skeleton is often related to feeding mode. As noted earlier, the facial skeleton is not a distinctly separate moiety in the adult skull (van der Klaauw, 1945). Posteriorly it is continuous with the dermal skull roof overlying the braincase, and laterally and ventrally, with the endochondral bones of the

2. An Introduction to Tetrapod Feeding braincase, itself, to create the unitary structure of the skull (Fig. 2.4). d. Palate The palate is represented by a series of dermal bones filling in the area between left and right upper jaws (Fig. 2.4b). Dermal bones of the palate join posteriorly with endochondral bones of the braincase. In most taxa the palate is relatively flat, or planar. In all tetrapods the palate is perforated by the internal nares {choanae), openings that allow the passage of air inspired through the nostrils into the nasopharynx (and from there, through the glottis and into the trachea and lungs). In squamate reptiles and many mammals, anterior palatal openings allow access to the vomeronasal organs from the oral cavity (called the incisive foramina in mammals). Many taxa are characterized by additional palatal vacuities; anuran amphibians, for example have a particularly reduced palate dominated by large vacuities ventral to the orbits. The eyeballs are actually retracted through these vacuities into the oral cavity during swallowing (see later)! Palatal form has been exploited as a taxonomic character in birds (e.g., Pycraft, 1900, in Goodrich, 1930; Witmer and Martin, 1987) and squamates (e.g., Lakjer, 1927; Bellairs and Boyd, 1950); however, Bellairs (1949) cautioned that similarity in the superficial (soft tissue) palate may belie significant differences in the hard (bony) palate. Teeth are found on the palates of some amphibians and reptiles. In some taxa a secondary palate forms ventral to the primary palate. As such, the choanae open into a separate chamber above the mouth that exits posteriorly into the mouth or pharynx. The secondary palate forms from medially projecting shelves of dermal jaw and palatal bones. It is best known in mammals where it is complete and robust. It evolved in synapsid ancestors of mammals and is presumed to be correlated with the evolution of endothermy, suckling, and the masticatory apparatus (e.g.. Walker and Liem, 1994; Hildebrand, 1995). It effectively isolates the respiratory passage from the oral cavity, allowing breathing to continue uninterrupted by bouts of feeding. However, initially the secondary palate was incomplete in the midline and is unlikely to have served this function. Probably the initial advantage to medial flanges on the palate was mechanical, serving to resist bending and torsional stresses during biting (Thomason and Russell, 1986; Russell and Thomason, 1993). Also, it should be noted that in mammals a significant part of the secondary palate posteriorly is composed of soft tissues and it is possible that a more extensive soft palate closed off the nasal passage in mammal ancestors with incomplete secondary palates. The presence of a complete, bony secondary palate

31

in crocodilians supports the notion of a respiratory function. Crocodilians forage with their mouths submerged and their nostrils elevated above the water. Because all nonmammalian tetrapods lack lips, cheeks, and other soft tissues that could seal the mouth cavity (see later), a separate respiratory passage allows crocodilians to breath with water-filled mouths—analogous to mammals that breath while suckling or masticating. Less well known is that some turtles (Gaffney, 1979) and scincid lizards (Goppert, 1903; Greer, 1989) have partial or complete bony, secondary palates. In turtles the secondary palate is best developed in aquatic taxa and is thus likely to serve a respiratory function, but in scincids its functional significance is unknown. 3. Temporal Fenestrae Fenestra is Latin for "window" (architects refer to the pattern of windows in a building as fenestration). Temporal fenestrae are windows, or openings, in the temporal region of the dermal roof of the skull. As such, the fenestrae reveal the underlying braincase. They have a characteristic pattern, position and relationship to particular dermal bones in different amniote taxa. Four basic patterns are recognized: anapsid, diapsid, synapsid, and euryapsid (Fig. 2.5). In anapsids (putatively the most primitive) there are no temporal fenestrae. The dermal skull roof forms a solid vault over the braincase with the jaw adductor musculature filling the cavity between the two. Many turtles exemplify this condition, but most living species are derived in having the dermal roof emarginated posteriorly or ventrally so that the braincase is partially, or wholly, exposed (Romer, 1956). Nonetheless, the earliest amniotes were clearly anapsid (e.g., Carroll, 1988). Diapsids are those amniotes with two temporal fenestrae, one above the other. The ventral border of each opening is called an "arch" (in Latin, apsis, hence the names for fenestration patterns actually refer to the number and position of the arches rather than the fenestrae themselves). The ventral border of the upper arch is formed by the squamosal and postorbital bones, and this arch is used as an anatomical landmark for establishing putative homologies in the fenestration pattern. The ventral border of the lower arch is formed by the quadrate and jugal bones. Although primitively both temporal arches are present in diapsids, some derived diapsids have lost the lower (squamates and euryapsids) or upper (birds) arch and their skulls are sometimes referred to as "modified diapsid." Although once considered a separate type, euryapsid skulls are also now believed to represent a modified diapsid condition with a single fenestra corresponding to the upper fenestra of the diapsid skull (i.e., its lower border is formed from the postorbital and squamosal bones).

32

Kurt Schwenk Sq P Po Emargination Modified Modified anapsid testudines diapsid snake

Modified diapsid lizard

Qj Modified Modified diapsid bird synapsid mammal

F I G U R E 2.5. Types of temporal fenestration in tetrapod skulls and a traditional view of skull evolution. Reproduced from Kardong (1998), with permission of The McGraw-Hill Companies. J, jugal; P, parietal; Po, postorbital; Qj, quadratojugal; Sq, squamosal.

Euryapsid taxa comprise a diverse assemblage of extinct, mostly marine reptiles (e.g., ichthyosaurs, plesiosaurs, and pliosaurs). Synapsids are those amniotes with a single temporal fenestra that corresponds to the lower opening of the diapsid condition. This condition is restricted to the clade comprising the mammals and all their extinct relatives forming the sister group to the Reptilia (Synapsida). In most living mammals the synapsid temporal fenestra is difficult to discern. This is because in the evolution of recent mammals two parallel trends have tended to obscure it: the enlargement of the fenestrae and the expansion of the braincase. As a result, the braincase has, in effect, swollen into the vacuity ancestrally present between it and the dermal skull roof while the dermal cranial vault itself has receded. The temporal fenestra can best be visualized in those taxa with well-developed temporal crests and ridges, which serve as attachment sites for the temporalis adductor muscle. The fenestra is evident as the space occupied by this muscle, bordered dorsally by the sagittal crest, posterodorsally by the lambdoidal, crest and ventrally by the zygomatic arch (cheekbone). The pattern of temporal fenestration in amniotes has long been held as indicative of phylogenetic relationship (reviewed by Goodrich, 1930). However, recent cladistic and molecular analyses have thrown into question this venerable contention. Although retained as a formal taxon, Diapsida is diagnosed as having an upper temporal fenestra (among other things), the presence of a lower fenestra being plesiomorphic for this group (e.g., Gauthier, 1984; Evans, 1988). As such, Diapsida includes Euryapsida within it. Monophyly

of the euryapsid skull condition itself is in question (Rieppel, 1994); however, some studies have allied ichthyosaurs with plesiosaurs and their relatives, thus retaining a monophyletic taxon Euryapsida within the Diapsida. Most surprising, perhaps, is the suggestion that turtles are also derived from within Diapsida (Rieppel, 1993, 1994; Rieppel and deBraga, 1996; deBraga and Rieppel, 1997; Platz and Conlon, 1997; Zardoya and Meyer, 1998; Hedges and Poling, 1999). If true, the traditional notion of a monophyletic Anapsida uniting turtles with fossil forms (e.g., Gaffney and Meylan, 1988) would be shattered. Furthermore, the anapsid condition of the turtle skull, long considered a retention of the primitive amniote condition, would represent a reversal from a diapsid ancestor, i.e., the loss of a fenestrated skull and reevolution of an uninterrupted dermal vault! However, at the time of this writing the character evidence supporting this contention is in dispute and molecular data are being reanalyzed (e.g., Wilkinson et a/., 1997; Lee, 1997; M. Lee, personal communication), hence the phylogenetic position of turtles and, therefore, evolutionary patterns of temporal fenestration remain open questions. The functional basis for the origin of temporal fenestration is unknown, but it is generally thought to be related to the distribution of stress on the dermal skull roof generated by the jaw adductor musculature (Olson, 1961; Frazzetta, 1968). According to Olson (1961 : 214), "the skull tended to become a network of lines of stress which were narrowly confined and precisely delimited." Attachment of muscle to bone is putatively more effective on edges and ridges than on smooth surfaces, particularly at sutures, hence there may have

2. An Introduction to Tetrapod Feeding

been initial selection for the formation of ridges on the underside of the skull roof. As adductor origin became increasingly restricted to marginal ridges, there would have been consequent selection to reduce the deposition of bone in intervening areas to conserve both weight and metabolic cost. Both these putative evolutionary trends are paralleled by plastic responses of bone in living individuals—bone tends to be deposited in areas of stress and resorbed in areas lacking it. Carroll (1988) further suggested that the typically rounded form of temporal fenestrae might serve to dissipate stress energy around the periphery of the cheek region to prevent the development of cracks. 4. Cranial Kinesis Cranial kinesis refers to any type intracranial mobility. As such, at least one component of the cranium is capable of moving relative to another, implying the presence of joints or flexure zones within the skull (Fig. 2.6). Cranial kinesis is widely distributed among vertebrates, but systems of kinesis are diverse and Parietal unit

Snout unit

FIGURE 2.6. Putative system of cranial kinesis in a lizard {Varanus) modeled as a system of joints and linkages. Reproduced from Kardong (1998), with permission of The McGraw-Hill Companies. Based on Frazzetta (1962).

33

should not be regarded as homologous. An intracranial joint was present in the sarcopterygian fishes ancestral to tetrapods (retained in the coelacanth) (reviewed by Jarvik, 1980), but was lost in the transition to tetrapods (Ahlberg et ah, 1996). Early tetrapods remained akinetic, a condition retained in living amphibians (with the possible exception of some caecilians; Wake and Hanken, 1982; J. O'Reilly, personal communication), but many amniote groups evolved some form of kinesis (see Goodrich, 1930). In most groups the inception of cranial kinesis was directly related to the evolution of temporal fenestration, which transformed the ancestral, massively bony, anapsid skull into a system of slender struts and vacuities. The significance of this transformation is most evident in diapsid reptiles, such as the living squamates, that have lost the lower temporal arch. In such modified diapsid skulls the quadrate is no longer fixed in place but is free to swing anteroposteriorly, a condition known as streptostyly (Versluys, 1912; Robinson, 1967). Streptostyly adds, in effect, an additional element to the lower jaw that allows anteroposterior translation of the mandible (Fig. 2.6). In advanced snakes the quadrate becomes very long and slender and can swing laterally, as well as anteroposteriorly, as part of the mechanism that permits an exceptionally wide gape for engulfing very large prey relative to body size (Chapter 9). In squamates, additional types of kinesis have evolved that allow the snout and facial skeleton to move relative to the braincase and the upper jaw to flex dorsoventrally (e.g., Frazzetta, 1962; lordansky, 1966; Arnold, 1998; see Chapter 8). In advanced snakes, kinesis can be extreme, including independent movement of left and right sides of the upper jaws and palate and flexure of the anterior snout (e.g., Albright and Nelson, 1959a,b; Kardong, 1977; Cundall and Shardo, 1995). Similarly, in birds, skull kinesis is variable and often extensive (e.g.. Bock, 1964; Biihler, 1981; Zusi, 1993). Much of the kinesis in birds relates to movement of the upper jaw, including independent movement of the tip. The skulls of mammals and their synapsid antecedents are singularly akinetic due to extensive fusion of the facial skeleton to the braincase and the evolution of a secondary palate. Nonetheless, it has been argued that some therapsid synapsids (ancestral to living mammals) had a connective tissue joint between the braincase and the facial skeleton that acted as a shockabsorbing device. Loss of this kinesis in living mammals is associated with expansion of the braincase (Crompton, 1955). In modern hares a zone of connective tissue divides the braincase into two, potentially kinetic moieties. Bramble (1989) suggested that this joint absorbs impact energy when the front legs hit the ground during saltatory locomotion. Inertial

34

Kurt Schwenk

movement of the large, extended pinnae (external ears) "resets" the mechanism during hind limb push-off. Caution must be exercised in the interpretation of cranial kinesis because its presence in the vast majority of cases is inferred only from anatomical evidence, such as the histology of putative joints or the manipulation of dead specimens. Functional demonstrations of kinetic movements in living animals are rare. Consequently, the functional significance of cranial kinesis in most groups remains unclear. However, with the exception of the hare example given earlier, nearly all scenarios identify kinetic mechanisms with feeding function. In birds, for example, kinesis increases gape for in-flight scooping of insect prey (see Zusi, 1993) and in other cases it may function as part of a mandibular lock important for shock absorption (e.g.. Bock, 1964; van den Heuvel, 1992). In lizards, simultaneous movement of upper and lower jaws may produce a pincer apparatus that enhances the efficacy of prey prehension with the tips of the jaws (Frazzetta, 1983; Condon, 1987; Schwenk, 1987) or it may aide flattening of the skull in crevice-dwelling forms (Arnold, 1998). B. Teeth Teeth, like the skull itself, are a vertebrate innovation associated with the presence of neural crest tissue. They are integumentary derivatives composed of several hard tissues (enamel, dentine, and cementum), but their origin is unclear. Traditionally they were thought to have arisen from hard tissues found in the dermal body armor of ancient, jawless fishes, but the presence of teeth in the even more ancient, soft-bodied conodonts, now believed to be basal vertebrates, throws this hypothesis into question. The discovery of dentine (a neural crest derivative) in conodont teeth supports the contention that conodonts were vertebrates and that their teeth are homologous to those of other groups (Sansom et al, 1994). Typically, vertebrate teeth have an exposed crown of very hard enamel with an inner core of somewhat softer dentine (Fig. 2.7a). The tooth is attached to a skeletal element by a layer of cementum. Tooth form, number, and position are highly variable among tetrapods. In most taxa teeth are restricted to the marginal elements of the jaws, primarily the premaxilla and maxillae of the upper jaw and the dentary of the lower jaw (in bony vertebrates). Many amphibians and lepidosaurian reptiles have palatal teeth as well. In gymnophione (caecilian) amphibians, for example, there are two upper rows of teeth, one marginal and one palatal (Fig. 2.4b). The teeth of the lower jaw fit in between those of the upper (Duellman and Trueb, 1986), probably enhancing the shearing function of a bite. The up-

per teeth of the lepidosaur, Sphenodon, are similarly arranged with two rows between which fit the lower teeth (Edmund, 1969). During chewing the lower teeth are slid longitudinally between the upper tooth rows for effective shearing (Gorniak et al, 1982). In advanced snakes the maxillary teeth are reduced and palatal teeth on the pterygoid bones are used unilaterally to pull the head of the snake over the prey item. In venomous viperids the maxilla is very short and contains a single, elongated fang (plus several replacements) that is erected when the maxilla is rotated during a strike. The fang is hollow and serves as a conduit to inject venom, forcefully expelled from the venom gland, into the prey (Chapter 9). Crocodilians and mammals lack palatal teeth, but many mammals have transverse, cornified ridges on the hard palate called palatal rugae that function analogously to hold food items in place during mastication and tongue movement. Turtles and birds lack teeth entirely and have replaced them with homy (keratinous) bills or beaks (e.g., Homberger, 1999; see later). Some frogs and many mammals also lack teeth. In all cases, the loss of dentition is a secondarily derived condition. In mammals, tooth reduction is typically associated with ant- and termitefeeding as part of a suite of adaptations enhancing lingual prehension of prey (Chapter 15). Filter-feeding baleen whales have also lost their teeth, as have some "toothed" whales (Chapter 16). In nearly all living amphibians the tooth crown is separated from the base, or pedicel, by a constricted zone of uncalcified dentine or connective tissue (Fig. 2.7g). Such teeth are called pedicellate (Parsons and Williams, 1962; Duellman and Trueb, 1986). Most amphibian teeth are conical and unicuspid, although bicuspid and even spatulate teeth occur. All living crocodilians are carnivorous and have conical teeth deeply rooted in the jaw bones {thecodont; Fig. 2.7d) (Edmund, 1969); however, a fossil species has been described with multicuspate, molariform teeth, suggesting a herbivorous diet (Wu et al, 1995). Lepidosaurian reptiles have a variety of tooth types. Most attach to the medial sides of the jaws {pleurodont; Figs. 2.7b and 2.7e), but in Sphenodon, some iguanians (Agamidae), and some amphisbaenians (Trogonophidae) the teeth are cemented to the apex of the jaws {acrodont; Figs. 2.7c and 2.7f) (Edmund, 1969; Cans, 1960). Cusp shape is highly variable. Carnivorous and insectivorous species tend to have conical, unicuspid crowns while in herbivorous species they are usually spatulate and multicuspate (Hotton, 1955; Edmund, 1969). Species whose diets include hard prey (durophagy) typically have teeth with broad, flat, or rounded crowns (e.g., Dalrymple, 1979; Rieppel and Labhardt, 1979). Tooth form and phylogeny are often closely correlated in squamates so not

2. An Introduction to Tetrapod Feeding

35

enamel dentine

bone pulp cavity

. .•;;

dental ligament cement a.

FIGURE 2.7. Tetrapod teeth, (a) Section through mandible and tooth of a mammal illustrating basic tooth anatomy; from Wake (1979), with permission; (b-d) types of tooth attachment in tetrapods: pleurodont, acrodont, and thecodont, respectively; from Wake (1979), with permission; (e) medial view of left mandibular ramus in a lizard (Morunasaurus) with pleurodont dentition; from Estes et ah (1988), with permission; (f) upper right tooth row of a lizard (Uromastix) with acrodont dentition; from Edmund (1969), with permission; (g) pedicellate teeth of a salamander (Amphiuma); from Duellman and Trueb (1986), with permission; and (h) lateral view of dentition in a female chimpanzee (Pan) in full occlusion; note that the teeth vary in form along the tooth row (heterodonty) and that uppers and lowers fit together very precisely (occlusion); from Owen (1868). Parts a - d copyright © 1979, University of Chicago Press. Reprinted from Hyman's Comparative Vertebrate Anatomy, 3rd ed.

all dental differences necessarily reflect adaptation to diet. In most amphibians and reptiles the teeth are polyphyodont, meaning that they are replaced throughout

life as they are worn or broken. Upper and lower teeth do not meet precisely, i.e., they do not occlude as they do in mammals, although in some amphisbaenians

36

Kurt Schwenk

upper and lower teeth do mesh to create a potential "cookie-cutter" shearing mechanism (Gans, 1960, 1974). Mammalian teeth are extremely variable and especially indicative of diet. This is because, unique among tetrapods, mammals masticate their food. Mastication requires a precise alignment of upper and lower tooth rows for the teeth to be mechanically effective in grinding, crushing, or slicing. Consequently their form is very sensitive to the mechanical attributes of the food processed (e.g., Hiiemae and Crompton, 1985; Strait, 1997). So that this alignment, or occlusion (Fig. 2.7h), is maintained, many (eutherians) or most (marsupials) teeth are never replaced. Some are replaced (the deciduous or milk dentition), but only once when suckling is completed and the oral apparatus nears adult size {diphyodonty). In most mammals, teeth have specialized functions along the tooth row, hence the teeth in a single animal vary significantly in form {heterodonty; Fig. 2.7h)—anterior incisors nip, crop, or gnaw, canines puncture and hold, premolars puncture and slice, and molars crush or grind (teeth with similar form or function in nonmammalian taxa are sometimes referred to as "incisiform," "caniniform," or "molariform"). In carnivorous, most insectivorous, and omnivorous mammals, molar tooth crowns are entirely covered with enamel, but in many herbivorous species, apical surfaces of the molars are dentine or dentine traversed by ridges of enamel. The softer dentine wears faster then the enamel so each tooth forms a corrugated grinding surface. Similarly, the gnawing incisors of rodents lack enamel on their posterior side so that they wear unevenly front to back, creating a chisel-like cusp. Mammal teeth are deeply rooted (thecodont). C. Keratinous Structures In the edentulous turtles and birds the jaws are covered by a keratinous or horny investment known as the rhamphotheca. In birds the rhamphotheca is called either the bill or the beak and in turtles it is called a beak. The beak is derived from the outer layer of dead, keratinized cells characteristic of all tetrapod integument (e.g., Homberger and Brush, 1986). In both taxa, beak form largely conforms to the shape of the bony jaws, but in some birds it extends significantly beyond the jaw tips. In others, keratinous ornaments occur seasonally during courtship and reproduction, but are later shed (Bock, 1966; Gaffney, 1979; Welty and Baptista, 1988). In both groups, the horny beak wraps around the jaw margins and extends onto the palate and floor of the mouth, especially anteriorly, to form a triturating surface for processing food (Fig. 2.13b). In turtles the beak is hard with a very sharp apical edge. When ele-

vated, the mandible fits snugly inside the upper jaw so that the lateral surface of the lower beak slides past the inner surface of the upper in a scissors-like shearing action. Some crushing of food may occur inside the mouth between the triturating surfaces. In birds, beak form is extremely variable among species and is closely correlated with diet (Fig. 2.8) (Bock, 1966; Ziswiler and Farner, 1972; Welty and Baptista, 1988; Witmer and Rose, 1991; Gill, 1995). There are beaks designed for probing, spearing, crushing, shearing, prying, and filtering. In spoonbills the cross-sectional shape of the broad, flat bill forms a hydrofoil that sheds a vortex as it sweeps through the water, disturbing the substrate and lifting buried prey items (Weihs and Katzir, 1994). In mallard ducks, flamingos, and some other aquatic birds the lateral margins of upper and lower bills form a series of lamellae that interact with each other and the tongue to form a filtering device (Jenkin, 1957; Zweers et al, 1977). In some shorebirds, the narrow bill is used to pluck minute prey out of the water like forceps and to move it along the beak to the mouth within a droplet of water using a unique mechanism of surface tension transport (Rubega and Obst, 1993). In many birds the beak is horny and hard, as in turtles, but in others, part or all of the beak is only lightly keratinized and remains relatively soft and pliant (Ziswiler and Farner, 1972; Gill, 1995). Furthermore, the beak and palate of many species are well supplied with proprioceptors (100-400 per mm^) and, in some cases, taste buds so that the beak is an extremely sensitive tactile and chemosensory organ used to locate, recognize, and manipulate food items (e.g., Berkhoudt, 1985a,b; Zweers and Berkhoudt, 1991; Dubbeldam, 1992). The so-called bills and beaks of monotreme mammals (platypus and echidnas) are only superficially bird-like. They are covered by naked skin that is not exceptionally keratinized (Griffiths, 1978). However, the tongues of all three living species of monotreme possess heavily keratinized pads and spines that abrade against similar horny structures on the palate (Owen, 1868; Doran and Baggett, 1972; Griffiths, 1978). These keratinous structures function as tooth analogues to process food. In the long-beaked echidna (Zaglossus), the anterior part of the tongue is also endowed with a series of barbed, keratinous spines that lie within a groove at rest (Griffiths, 1978). When the tongue is extended the spines are exposed and used to impale and apprehend slimy earthworm prey. The tongues of many birds and mammals are also covered by keratinous spines and projections, although none as well developed as in monotremes. In felid mammals, for example, heavily keratinized, spinous lingual papillae are used to rasp the flesh off bones, and in many nectar-feeding birds and mammals the tongue tip is elaborated into a

37

2. A n I n t r o d u c t i o n to T e t r a p o d F e e d i n g

MERGANSER Fish grasper

EAGLE

OYSTER

Moot fearer

CATCHER

Mollusc opener

WOODCOCK Earth probe

HUMMINGBIRD Flower probe

WOODPECKER Wood cutter

RAVEN Generolized

bill

CARDINAL

CROSSBILL

Seed cracker

Pine seed extroctor

FIGURE 2.8. Diversity of beak form in birds and its association with feeding types (see Chapter 12). Bony elements of the jaws largely, but not entirely, correspond in shape to their keratinous investment. From ' T h e Life of Birds,'' Second Edition, by J. C. Welty, © 1975 by Saunders College Publishing, reproduced by permission of the publisher.

filamentous brush (Figs. 2.13d and 2.13e) (e.g., Richardson et al, 1986; Homberger, 1988; Gill, 1995; Birt et ah, 1997). In many birds the underside of the tongue tip is heavily keratinized and stiff. This may serve to return the tongue tip to its original shape after deformation during feeding (Homberger and Brush, 1986; Homberger, 1988). Baleen whales derive their name from keratinous structures known as haleen, which they use to filter small prey from within or at the surface of the water (Chapter 16). The baleen grows as transverse plates suspended from the palate on each side of the midline (Pivorunas, 1979). The plates overlap and are frayed along their terminal margins to form a dense, comblike mat of fibers. Although they grow continuously, they are worn away during use. Baleen form corresponds to both phylogeny and feeding mode. Species with very long baleen plates (e.g., right whales) surface skim, whereas species with shorter baleen (e.g., blue whales) typically engulf large schools of prey beneath the surface (Pivorunas, 1979; Lambertsen, 1983). Water is expelled from the mouth, through the baleen, either by compression of an expanded pharynx and hollowed

tongue as in some species or by the piston-like action of a large, muscular tongue in others. In either case, minute prey are trapped in the frayed baleen, which acts as a sieve (Chapter 16). In some artiodactyl mammals (e.g., deer and antelope), there are no upper incisors. Instead, the underlip and anterior palate are covered by a thick, keratinous pad that the lower incisors contact to crop vegetation (e.g., Owen, 1868). Sirenians (manatees and dugongs) have thick keratinous pads at the ends of both upper and lower jaws, which, at least in some cases, are used to crop and process vegetation (e.g., Forsten and Youngman, 1982; see Chapter 16). Rhinoceroses lack both upper and lower incisors and some species have heavily keratinized lips used for cropping (Nowak, 1991). As noted previously, keratinous palatal rugae serve as anchor points for food during processing and tongue movement in most mammals. D . Hyobranchial Apparatus As noted previously, the hyobranchial apparatus (or hyobranchium) is the most obvious remnant of the

38

Kurt Schwenk

visceral skeleton (splanchnocranium) in tetrapods. It is derived from the ventral elements of the second (hyoid) visceral arch and as many as three branchial arches (visceral arches 3, 4, and 5). It lies within the tissues of the throat (pharynx) with its anterior part usually between the mandibular rami where it supports the tongue in the floor of the mouth (Fig. 2.9). The hyobranchial apparatus is often referred to, imprecisely, as the hyoid apparatus, or simply the hyoid. This usage is most appropriate for mammals, in which the branchial arch contribution is reduced. In fishes the

hyobranchial apparatus supports the gills and is an essential part of the suction-generating mechanism by means of pharyngeal expansion. Visceral arches also form an inner set of "pharyngeal jaws" in some fishes (notably cichlids) that bear teeth and process food (e.g., Liem, 1973; Liem and Sanderson, 1986), and in filterfeeding groups the branchial arches form part of the food-trapping system (Northcott and Beveridge, 1988; Sanderson and Wassersug, 1993). In tetrapods, only larval amphibians and some aquatic, paedomorphic adults retain branchial arch

ptat proc

B hyoid plate I—pmed proc

I—hyoid plate pmed proc plat proc

phyd bone

— den -Mc c (mand sym)

^ angsp '—hyog memb '—ant proc hyl Mc c

-angsp -antlai proc -hyale -hyog memb -den -mmc (mand sym)

vocal slit

FIGURE 2.9. Spatial relationships among the mandible, hyobranchial apparatus, and tongue in two species of frog, shown in anterodorsal view. The hyobranchium lies embedded in the throat musculature, its anterior portion between the mandibular rami. In most tetrapod taxa, as here, the hyobranchial skeleton supports and moves the tongue to which it is attached by muscle and connective tissue. However, the degree to which the tongue can move independent of the hyobranchium varies a great deal among tetrapod taxa. On the left is Rhinophrynus dorsalis (A and C); on the right is Bufo marinus (B and D). After Trueb and Gans (1983), with permission of Cambridge University Press.

39

2. An Introduction to Tetrapod Feeding gills. Larval salamanders, in particular, maintain an extensive set of arches. However, in adult amphibians and all other tetrapods the hyobranchial apparatus functions primarily to support and move the tongue and pharynx. In some secondarily aquatic tetrapods the hyobranchium has reverted to its role in pharyngeal expansion to generate suction. In these species the hyobranchial apparatus is typically large and robust (Bramble and Wake, 1985). A respiratory function for the hyobranchial apparatus is maintained in many tetrapods lacking gills, particularly in salamanders that use a "buccal p u m p " to ventilate the lungs (e.g., Brainerd and Monroy, 1998). Some lizards and other reptiles also use a buccal pump for lung ventilation (Owerkowicz ei a\., 1999; E. L. Brainerd, unpublished results) and to move air in and out of the nasal chamber for olfaction (Dial and Schwenk, 1996; Schwenk and Brainerd, in preparation). Gular or buccal movements and pharyngeal expansion are also associated in squamate reptiles with various displays and with evaporative cooling (e.g., Bels, 1992; Deban ei a\., 1994; Bels ei a\., 1995). Extreme examples of hyobranchialmediated display behavior occur in iguanian lizards, notably the erection of the dewlap in anoloid lizards (Font and Rome, 1990; Bels, 1990), the frill in the frilled lizard (Beddard, 1905), and the beard in the bearded dragon (Throckmorton ei a\., 1985). Hyobranchial morphology is diverse (Fiirbringer, 1922) (Fig. 2.10) and the names for individual elements vary among clades and workers. Indeed, homologies among elements in different taxa are not always certain and are sometimes controversial (e.g., Reilly and Lauder, 1988). However, there is always an anterior, median element derived from the hyoid arch, usually referred to as the body or basihyal The basihyal lies at the base of the tongue and is sometimes embedded within it. In some taxa, such as lepidosaurs and birds, the basihyal has an anterior extension that projects into the tongue. In lepidosaurs this lingual process is a slender rod, but in birds the tongue is more or less filled by an additional, apparently neomorphic cartilage called the paraglossal (ossified in some species, notably parrots; Homberger, 1986,1999). A first pair of hyoid arch elements curves laterally from the basihyal. These are usually called ceraiohyals. Subsequent (more posterior) arches are derived from ancestral branchial arches. They are given a variety of names, but their proximal elements are usually called hasibranchials and their apical elements, epibranchials. Arch elements can be fused, articulated with, or separate from the basihyal, depending on the arch and the taxon. Elements of the hyobranchial arches usually extend toward the larynx and the otic region of the skull base. Embryologically the association of the stapes to the second (hyoid) arch

is clearly evident. In many mammals hyobranchial elements form ligamentous or bony chains that attach the hyobranchium to the larynx and the styloid process of the skull (Hiiemae and Crompton, 1985; Homberger, 1994, 1999). A reduction in the branchial arch contribution to the hyobranchium in mammals is correlated with their greater contribution to the cartilages of the larynx. This increase in laryngeal complexity may be associated with more complex sound production, an important part of the sociobiology of mammals (Walker and Liem, 1994). With regard to mammals, it is typical that hyobranchial terminology is distinct and confusing relative to other tetrapods. In most mammalian species there are only two arches represented (Fig. 2.10i). The anterior arch corresponds to the ceratohyals, which are second visceral arch derivatives. These are referred to as the anierior cornua (horns). A second arch represents a basibranchial (third visceral arch) contribution called the posierior cornua (or thyrohyals). In most mammals the anterior cornua are prominent and comprise a chain of bones with a ligamentous connection to the styloid process of the skull base. The posterior cornua are smaller and associated with the larynx. However, in humans and other anthropoid primates it is the posterior cornua that are prominent while the anterior cornua are reduced to nubbins to which the stylohyoid ligament attaches (e.g., Shipman ei al, 1985), thus the anterior cornua are referred to as the "lesser horns" and the posterior cornua as the "greater horns" (Fig.2.10j). In some taxa virtually all tongue movement is a result of hyobranchial movement (e.g., most birds). However, in tetrapods with complexly muscled tongues (lepidosaurs, some turtles, parrots, and mammals), the tongue is also capable of complex, intrinsic movement independent of hyobranchial movement (see later). Many tetrapods capture prey by protruding or projecting the tongue out of the mouth. Tongue protrusion is usually a combination of hyobranchial protraction, intrinsic shape change of the tongue, and, sometimes, sliding of the tongue on the lingual process of the basihyal. During tongue protraction in salamanders, most or all of the hyobranchial apparatus is projected out of the mouth along with the tongue (Chapter 4), whereas in chameleons the lingual process of the basihyal is protruded and stabilized while the tongue is projected off of it (Chapter 8) (see later). E. Jaw Musculature As visceral arch derivatives, the jaws are moved by the muscles of the visceral arches, collectively known as the branchiomeric musculaiure. A deeply entrenched

40

Kurt Schwenk

FIGURE 2.10. Diversity in the form of the hyobranchial apparatus in amphibians (a-c), reptiles (d-h), and mammals (i-j). (a) Caecilian (Gymnophiona, Gymnopis); from Duellman and Trueb (1986), with permission; (b) frog (Anura, Leptodactylus); from Duellman and Trueb (1986), with permission; (c) salamander (Urodela, Amides); from Duellman and Trueb (1986), with permission; (d) hzard (Lepidosauria, Basiliscus); from Romer (1956), with permission; (e) snake (Lepidosauria, Vipera); from Romer (1956), with permission; (f) turtle (Testudines, Clemmys); from Romer (1956), with permission; (g) bird (probably Picaformes); from Proctor and Lynch (1993), with permission; (h) crocodile (Crocodylia, Crocodylus); from Romer (1956), with permission; (i) dog (Camivora, Canis); from Flower (1885); and (j) monkey (Primates, Papio); from Flower (1885). All hyobranchia are shown in ventral view with anterior toward the top, except for (i), which is an anterior view. Parts a—f, h copyright © 1956, University of Chicago Press. Reprinted from Osteology of the Reptiles.

notion in vertebrate morphology is that the branchiomeric musculature is "viscerar' in the sense that it is associated with the gut tube (pharynx) and therefore represents an anterior extension of unsegmented musculature investing the gut (the hypomere) (e.g., Goodrich, 1930; see Kardong, 1998; Walker and Liem, 1994). Recent developmental and neuroanatomical work, however, has cast doubt on this dogma and suggests the possibility that the branchiomeric muscula-

ture has a segmental origin from the paraxial mesoderm of the cranial somitomeres rather than deriving from the unsegmented hypomere (Northcuttt, 1990; D. Wake, 1993; see Jacobson, 1993, for a discussion of somitomeres). In the trunk the hypomere forms involuntary, smooth muscle of the gut and visceral organs, but in the visceral arches the branchiomeric musculature is striated and mostly voluntary. Furthermore, the branchiomeric musculature is innervated by the

41

2. A n I n t r o d u c t i o n to T e t r a p o d F e e d i n g

cranial nerves, which are serially homologous with the more posterior, segmented spinal nerves innervating the striated body musculature derived from somitic mesoderm. Thus, we can recognize serial, presumably segmental homologies in the branchiomeric muscles that move the visceral arches. The jaw musculature includes muscles that open and close the jaws and, in some cases, protract and retract them (Fig. 2.11). This apparent functional simplicity is belied by the remarkable variation and complexity of the jaw musculature among tetrapods. Ancestrally, and as retained in many fishes and amphibians, a large, relatively simple adductor mandibulae muscle elevates

the mandible to close the jaws (all muscles are bilaterally paired unless otherwise noted). It arises from the side of the braincase and upper jaw and inserts on the mandible. In gymnophione amphibians an additional large (and functionally more important), ventral interhyoideus muscle inserts on an exceptionally long retroarticular process behind the jaw joint, pulling it down to elevate the mandible (Bemis et al., 1983). In some plethodontid salamanders the mandible is connected by a stout ligament, over the skull, to the anterior cervical vertebrae. Because the ligament crosses the neck joint it is stretched when the head is sharply ventroflexed, pulling up on the mandible to effect a

iVI. temporalis

aponeurosis covering M temporalis

M. zygomaticomandibularis

M digastricus M masseter pars profunda /

3,^,10-be|,y

posterior belly

pars superficialis aponeurosis covering

M. zygomaticomandibularis

M temporalis M. pterygoideus extern us

d.

postenor belly M digastncus anterior belly

M. pterygoideus internus

FIGURE 2.11. Jaw musculature in a herbivorous mammal (Artiodactyla, Ovis). (a-c) Progressively deeper views in left lateral view; (d) a ventrolateral view with the left mandibular ramus removed except for its condylar process (shown in section next to the insertion of the m. pterygoideus externus). Note the pinnate form of the temporalis muscle and the highly complex and subdivided masseter complex (many workers would also include the m. zygomaticomandibularis as part of the masseter). Also note that the combination of jaw muscles supports the mandible in a "sling/' which can be moved in virtually any direction. The digastric muscle (a and b) inserts on the anteromedial surface of the mandibular ramus and serves to open the jaw. After Turnbull (1970), with permission.

42

Kurt Schwenk

powerful bite (Schwenk and Wake, 1993). In this case it is large, anterior trunk muscles ventroflexing the head that contribute to jaw closing. In arrmiotes, the adductor mandibulae is variously subdivided. In reptiles the adductor mass is internally partitioned into many fascicles or nominal muscles of varying degrees of separation and confluence, achieving its greatest complexity in squamates (e.g., Haas, 1973; Wineski and Gans, 1984). These muscles insert onto a vertical process on the mandible formed by the coronoid bone. In addition, a wholly separate muscle (m. pterygoideus) arises from the base of skull and forms a sling around the posterior end of the mandible, extending onto the retroarticular process. As one might imagine, the adductor musculature is particularly complex in snakes with highly kinetic skulls (e.g., Haas, 1973; Zaher, 1994). In mammals the principal adductor mass is relatively simple and is called the m. temporalis (Fig. 2.11). It lies in the position typically filled by the adductor mandibulae and inserts onto the coronoid process of the dentary bone (mandible). Mammals also have a well-developed pterygoideus muscle and a novel adductor (putatively differentiated from the temporal adductor mass) called the m. masseter, which takes its origin from the zygomatic arch. The masseter muscle is often apportioned into several, largely separate parts, particularly in rodents and other herbivorous mammals that rely on complex masticatory movements to grind plant food (e.g.. Fig. 2.11). Each of the three main adductor muscles in mammals has a different line of action, including anterior, posterior, lateral, and medial components, so that the lower jaw is held completely within a muscular sling capable of producing the finely controlled movements necessary for dental occlusion and mastication (TurnbuU, 1970; Crompton, 1989). The arrangement of the jaw adductors in mammals also helps to control reaction forces at the jaw joint during biting, a condition that may have permitted the reduction and eventual loss of the ancestral jaw joint bones to the middle ear (Crompton and Hylander, 1986; Crompton, 1989,1995). The apparent simplicity of mammalian adductors grossly is often in startling contrast to their high degree of internal, histological complexity. Most adductors are characterized by complex patterns of pinnation and some (particularly the masseter) are subdivided into many, independently controlled motor units, resulting in fine-scaled functional partitioning of the muscle (e.g.. Herring, 1980,1992). In all nonmammalian tetrapods the jaws are opened primarily by the m. depressor mandibulae, which arises from the back of the skull and neck and lifts the retroarticular process behind the jaw joint to depress the mandible. Although it acts on the jaw (first visceral

arch), the depressor mandibulae is derived from the ancestral hyoid (second) arch levator to which it corresponds topologically, if not functionally. In nonmammalian tetrapods, jaw opening is also probably aided by strap-like muscles in the ventral midline. These arise from the hyobranchial apparatus, which is itself connected by serially homologous muscles to the sternum. These muscles are hypohranchial, rather than branchiomeric, developing as anteroventral extensions of more posterior somites (striated, segmented body musculature). In mammals the depressor mandibulae is lost and the lower jaw is depressed primarily by the digastric muscle running ventrally from the back of the braincase to the mandible. Although the brief description just given summarizes significant complexity in the jaw musculature, it remains a gross simplification. For example, taxa with kinetic skulls have additional muscles that affect upper jaw movement independent of the braincase. As noted, in snakes that use unilateral movements of the upper jaw elements and which erect fangs, this musculature is intimidating indeed (e.g., Kochva, 1962; Haas, 1973; Kardong, 1973; Cundall, 1983,1987; Cundall and Rossman, 1993; Zaher, 1994). Cranial elevation at the atlanto-occipital joint contributes to mouth opening in many tetrapods, in addition to jaw depression, hence dorsal axial muscles inserting on the cranium may also function as "jaw muscles" (e.g., Bemis et ah, 1983; Larsen and Beneski, 1988). As noted earlier, head depression affected by ventral axial muscles in some salamanders causes jaw closing by means of a tendinous link between the mandible and the first vertebra (Schwenk and Wake, 1993). F. Hyobranchial Musculature The hyobranchial musculature is sufficiently complex and variable that relevant details are left for subsequent chapters. However, of note here is that, for the most part, the hyobranchial apparatus lacks direct connections to other skeletal components and is therefore free-floating within the musculature of the throat. In addition to its own intrinsic musculature that moves its various elements relative to one another, it has an extrinsic musculature that connects it to the mandible anteriorly, the skull dorsally, and the shoulder and sternum posteriorly (Fig. 2.12). Thus the hyobranchium is held within a three-dimensional array of muscular slings that permit movement in virtually any direction. The kinematic potential of this arrangement is particularly important regarding the hyobranchium's association with the tongue. In nearly all tetrapods the tongue is directly coupled to the basihyal with varying degrees of intimacy and most gross tongue movement

2. A n Introduction to Tetrapod Feeding

43

FIGURE 2.12. Muscles acting on the hyoid body of an opossum (Marsupialia, Didelphis) represented as vectors. The hyobranchium is thus suspended in the throat region by a series of paired, straplike muscles that can move it in any direction with precise control. Due to its connection to the tongue, hyobranchial movements usually translate into lingual movements. In addition, several extrinsic lingual muscles arise from the hyobranchium and insert within the tongue. From Crompton et al. (1977), with permission. A Dig, m. digastricus, anterior belly; GnGl, m. genioglossus; GnHy, m. geniohyoideus; OmHy, m. omohyoideus; P Dig, m. digastricus, posterior belly; StHy, m. sternohyoideus.

is a direct result of hyobranchial movement. Fine control of hyobranchial-mediated tongue position is particularly important during rhythmic feeding cycles in which hyolingual movements are used to transport and position food in the mouth and pharynx (see later). In addition to tongue movement, the hyobranchial musculature is largely responsible for pharyngeal compression associated with swallowing (see later). Movement of hyobranchial elements in display behavior usually involves the action of its intrinsic musculature, whereas gross hyolingual positioning, as during feeding, is the result of extrinsic muscle function. In species with highly protrusible or projectile tongues the hyobranchial musculature is often highly specialized, particularly in salamanders (Lombard and Wake, 1976, 1977; Chapters 3 and 4). G. Tongue Tongue form is enormously variable among tetrapods (Fig. 2.13) and its diversity is largely congruent with phylogeny rather than ecology (e.g., Schwenk, 1988; Homberger, 1989). Hence, superficial tongue morphology has been exploited in taxonomic and phylogenetic treatments of several groups (e.g., salamanders: Regal, 1966; Ozeti and Wake, 1969; Lombard and

Wake, 1977,1986; frogs: Regal and Cans, 1976; Horton, 1982; Grant et al, 1997; squamates: Camp, 1923; McDowell and Bogert, 1954; Schwenk, 1988; birds: Gardner, 1925; Bock, 1978; Homberger, 1980; mammals: Sonntag, 1925; Stadtmiiller, 1938b; Doran, 1975; see also specific chapters). The tongue is an essential part of the feeding apparatus of terrestrial tetrapods. It is used as a prehensile organ during the ingestion of food in most amphibians, most reptiles (including birds), and many mammals. It almost universally functions to manipulate food once it is in the mouth and to transport it posteriorly to the esophagus for passage into the gut. Hence the tongue is important in virtually every stage of feeding (see later). Within some clades, among-taxon differences in tongue morphology can largely be attributed to differences in the functional role played by the tongue during each feeding stage (Schwenk and Throckmorton, 1989). In aquatic tetrapods that have reverted to suction or filter feeding, the tongue is secondarily reduced and simplified, and in suction feeders the hyobranchial apparatus is large and robust due to its role in expanding the pharynx (Bramble and Wake, 1985). In many tetrapods the tongue is relatively simple. In some taxa it is little more than an epithelial elaboration

44

Kurt Schwenk

Tongue anchored to posterior end of stemtnn

FIGURE 2.13. Diversity of tongue form in tetrapods. (a) Salamander {Salamandra), showing mucous pad and pleated mucosa of the floor of the mouth indicative of the ability of the tongue to be protruded far beyond the mandible for lingual prey capture; from Stadtmiiller (1938), with permission; (b) tortoise {Testudo), showing papillose surface of the tongue; also shown is the triturating surface of the lower jaw covered in the hard keratin of the beak, which forms sharp cutting edges along its margins; from Stadtmuller (1938), with permission; (c) lizard (Cordylus), showing scale-like and plicate papillae, and notched tongue tip typical of squamates; from Schwenk (1995), with permission; (d) nectar-feeding bat (Choeronycteris), showing cylindrical form typical of highly extensible tongues, which employ a muscular-hydrostatic mechanism for elongation; also shown is a keratinous ''brush'' tip used to collect nectar; from Stadtmuller (1938), with permission; (e) nectar-feeding bird (Coereba), showing curled margins and bifurcate, brush tip; from Orinthology by Gill, © 1990, 1995 by W. H. Freeman and Company, used with permission; and (f) myrmecophagous mammal (Tamandua), showing an extremely long tongue originating on the sternum and hypertrophied salivary glands; from Feldhamer et al. (1999), with permission of The McGrawHill Companies.

overlying a median element of the hyobranchium. This is most evident in birds in which the tongue is essentially a superficial, largely keratinous adornment of

the paraglossal cartilage. In crocodilians the tongue is more substantial, but it is mostly fatty, lacks intrinsic musculature, and is attached to the floor of the mouth along its entire length (Schumacher, 1973; Ferguson, 1981), hence it provides little more than a pad used to seal the pharynx during submersion. Thus, both living archosaurian clades show lingual simplification, although this is undoubtedly independent and secondarily derived. Most frogs similarly lack intrinsic lingual musculature, although their tongues are highly protrusible (Chapter 5). In caecilian amphibians the tongue is an nonprotrusible muscular pad in the floor of the mouth that, at least in some species, is riddled with vascular sinuses (M. Wake and Schwenk, unpublished results). Salamanders, likewise, have tongues that are primarily mucous pads (Fig. 2.13a), but unlike caecilians, salamanders are characterized by extensive tongue protrusion and even ballistic tongue projection used for prey prehension (Chapter 4). Most of the morphological complexity of this system, however, is associated with the hyobranchial apparatus and its musculature extrinsic to the tongue. In contrast to the taxa just noted, terrestrial turtles, lepidosaurs, parrots, and mammals are characterized by highly complex, muscular tongues. Lepidosaurs and mammals, in particular, have large, intrinsically mobile tongues. In most lepidosaurs the tongue is supported by a median process of the basihyal {lingual, or entoglossal process), but in mammals there is no such support and the basihyal is restricted to the very base of the tongue. Muscles that contribute to the corpus of the tongue are typically divided into two types: extrinsic fibers originate from outside the tongue (usually from the mandible and elements of the hyobranchium) and insert within it and intrinsic fibers arise and insert entirely within the tongue. This simple dichotomy is belied by the complex organization of the fibers within the tongue where both types of fiber sometimes merge into a single, organized system so that identification of a particular lingual "muscle" as either "intrinsic" or "extrinsic" is problematic (Schwenk, 2000a). In any case, such muscular complexity reflects the unusual biomechanical properties of such tongues that function as muscular hydrostats (Kier and Smith, 1985; Smith and Kier, 1989). Tongues are similar in this sense to elephant trunks and squid tentacles, which are also complexly muscled organs lacking skeletal support. Such organs exploit the incompressibility of water (in this case intracellular fluid within muscle cells) in a constant volume structure to effect length and shape changes. Although the term "muscular hydrostat" was only coined recently, this biomechanical attribute of the tongue was recognized long ago by Owen (1868), if not earlier, who described

2. An Introduction to Tetrapod Feeding it in reference to the prehensile giraffe tongue. In all muscular hydrostats there are some muscle fibers oriented longitudinally, and others transversely, obliquely or vertically. The latter type serve to decrease the tongue's diameter which, due to the maintenance of a constant volume, translates into an increase in length. In addition, localized muscle contractions can cause complex shape changes in the tongue. Mammal tongues are especially protean in this regard. Tongue shape is maintained overall by an elastic, connective tissue tunic that may also help restore the tongue to its resting conformation through elastic recoil (Schwenk et al, manuscript). Although virtually all lepidosaur and mammal tongues are capable of some hydrostatic shape change, some groups, such as snakes and myrmecophagous mammals, show a high degree of lingual specialization for hydrostatic elongation (Fig. 2.13f). Parrots are unique among birds in their possession of a large, mobile tongue containing extensive intrinsic musculature (Homberger, 1986). They also contain cavernous vascular sinuses that may function hydraulically. These neomorphic modifications of the tongue are associated with parrots' unique feeding mechanism, specifically their ability to manipulate seeds for processing by the bill. Turtle tongues (Fig. 2.13b) are little studied, but terrestrial turtles are capable of significant tongue movement, including limited tongue protrusion for food prehension. Their tongues are supported by a robust basihyal with a small lingual process and include some intrinsic musculature (Schumacher, 1973). Although frogs generally lack intrinsic lingual musculature and therefore the ability to cause hydrostatic volume changes in the tongue, one exceptional species has been found. An African ranoid, Hemisus marmoratum, was shown to use an unusual form of slow, linear tongue extension during prey capture distinctly different from the typical anuran pattern of "flipping" the tongue over the mandibular symphysis (Ritter and Nishikawa, 1995). A morphological study found that Hemisus is unique among frogs in its possession of an intrinsic, vertical muscle fiber system, which is presumed to decrease the diameter of the tongue to effect hydrostatic elongation (Nishikawa et al, 1999). Hemisus is an ant and termite specialist. A similar system may operate in another, unrelated myrmecophagous frog, Rhinophrynus (Trueb and Gans, 1983), although this is unconfirmed. The association of hydrostatic elongation during lingual feeding in myrmecophagous tetrapods is striking: as noted earlier, ant- and termitefeeding mammals exhibit extreme modifications of the tongue in this regard (Fig. 13f), and even among lizards, which as a rule show little dietary specialization of the tongue (Schwenk, 1988), ant-eaters such as Phry-

45

nosoma and Moloch show adaptations for hydrostatic tongue protrusion (Schwenk and W. Sherbrooke, in preparation). In most species the dorsal surface of the tongue is elaborated into a series of papillary projections. These are highly variable in form and function (Fig. 2.13). In mammals, for example, they are usually quite keratinized (see earlier discussion), whereas in many squamates they are soft, filamentous, and covered with a simple mucous epithelium. In taxa that use the tongue for prehension of food, the tongue surface is usually very papillose and always well endowed with mucous or seromucous secretions. These fluids originate either intrinsically, as noted earlier, or from extrinsic salivary glands. The salivary glands of myrmecophagous species are usually hypertrophied (Fig. 2.13f), which may reflect their role in producing copious mucus for prey prehension, or may be related to the production of secretions that digest, detoxify, or immobilize noxious ant prey (which may bite, sting, and contain both formic acid and venom). In snakes, papillae are lost and the tongue surface is smooth, presumably due to exclusive use of the tongue in chemosensory tongue flicking with concomitant loss of tongue participation in feeding function. In addition to its role in the mechanics of feeding, the tongue also serves as a sensory organ. In particular, the tongue is the site of gustation, or taste, a chemical sense mediated by small organs in the lingual (and oral) epithelium known as "taste buds" (e.g., Gilbertson, 1998). In mammals, taste buds are restricted to specialized fungiform, circumvallate, and foliate papillae (e.g., Murray, 1973), but in other tetrapods they are distributed more generally (e.g., Schwenk, 1985). In frogs they take the form of large disc-like taste organs (Sato, 1976; Barlow, 1998). Lingual taste buds are a plesiomorphic feature of tetrapods, hence their absence in some species, such as snakes and monitor lizards (Schwenk, 1985; Young, 1997), is unusual. However, in these taxa loss of lingual taste buds probably follows secondarily on extreme modification of the tongue to subserve the vomeronasal system, a second chemical sense related to olfaction and mediated by paired vomeronasal organs in the snout above the palate (Halpern, 1992; Schwenk, 1994, 1995). In this case the tongue plays no direct sensory role, but functions to sample environmental chemicals and to delivery them to the vomeronasal organs. In most tetrapods the tongue tip is also probably utilized in tactile exploration of the environment (e.g., Kubota et al, 1962). Sensory use of the tongue is important during foraging in many taxa, especially squamate reptiles, and in the assessment of palatability of food once it is brought into the mouth (e.g.. Chapters 8 and 13).

46

Kurt Schwenk H. Pharynx

The pharynx is an ill-defined portion of the gut tube that lies between the mouth {buccal cavity) and the esophagus. Its anterior margin corresponds roughly to the posterior end of the tongue. In mammals, particularly, it is sometimes subdivided into an anterior oropharynx, a dorsal nasopharynx, and a laryngopharynx dorsal to the larynx. However, in most tetrapods these distinctions are unwarranted. This is because in nonmammalian species the pharynx is often a capacious cavity that blends indistinguishably with the buccal cavity anteriorly and the middle ear (tympanic) cavities laterally. In such species the pharynx is better described by the inclusive term oropharyngeal cavity (e.g.. Smith, 1992). In nonman\malian species the pharynx serves as a collection site for food that is transported there inertially or by the tongue and hyobranchial apparatus. Food does not remain long here before being moved further posterior into the esophagus for peristaltic transport to the stomach. Swallowing in nonmammalian tetrapods is properly called "pharyngeal emptying." In mammals, swallowing takes a special form and is referred to as "deglutition" (see later). Of particular relevance here is the condition of the pharynx in mammals (Smith, 1992). Unlike all other vertebrates, mammals possess a muscular pharynx that is associated with the evolution of facial musculature, a soft palate, modifications of the tongue, and several novel behaviors, notably suckling in infants and an explosive, muscular swallow that is integrated into the feeding cycle. Smith (1992) noted that the mammalian muscular pharynx seems to be entirely neomorphic, without homologues in related tetrapods. The muscular pharynx and its neuromuscular control are part of a sweeping reorganization of the feeding system associated with the evolution of the mammalian masticatory system. In effect, mammals have inserted a muscular sleeve into the ancestral pharynx that is continuous posteriorly with the esophagus and anteriorly with the soft palate and extrinsic muscles of the tongue. Thus in mammals the entrance to the pharynx (the pyriform recess) is marked by a sphincter-like orifice of muscles that run from the tongue base to the soft palate and from the soft palate into the pharyngeal musculature (Smith, 1992). Contraction of these muscles elevates the base of the tongue and creates a seal between the tongue and the soft palate. Creation of this seal may be critical to generating suction during suckling (Chapter 14). Masticated food collected in the pharynx is then swallowed during a reflexive contraction of the pharyngeal musculature coordinated with posterior tongue movement (e.g., Koltai and Gates, 1981; Miller, 1982; Hiiemae and Crompton, 1985; Crompton, 1989; Thexton and Crompton, 1998;

see later). The nature of deglutition in mammals, as well as its coordination with the rest of the feeding cycle, is unique to mammals (Smith, 1992). I. Cheeks, Lips, and Probosces In addition to the novel origin of pharyngeal musculature, mammals also uniquely possess facial muscles that endow them with facial mobility and their characteristic use of facial expression in communication (e.g., Darwin, 1896). Unlike the pharyngeal musculature, facial muscles have clear homologues in their expressionless kin, the reptiles (including birds), which have a set of thin, sheet-like, superficial muscles (mm. constrictor colli, intermandibularis posterior, and depressor mandibulae) innervated by the same cranial nerve (VII, the facial) (e.g.. Ruber, 1930; Smith, 1992). These muscles primarily elevate and constrict the pharynx in reptiles (helping to empty the pharynx, among other things), but in mammal ancestors they migrated onto the front and sides of the face where they function not only in facial expression, but in feeding as well. Of most importance in mammalian feeding are the cheeks and lips (e.g., Stadtmiiller, 1938a). The presence of these structures is a significant departure from other tetrapods because they provide walls and a flexible, anterior seal to the buccal cavity. This is in striking contrast to amphibians and reptiles whose mouths must gape when the jaws are open. The ability to seal the mouth permits therian mammals to generate intraoral suction, which is a fundamental part of the suckling mechanism used by infants (Chapter 14). Although monotremes lack lips and cheeks, Griffiths (1978) maintained that echidnas also suckle, and do not lap, their milk, and was convinced that they can generate intraoral suction for this purpose. It is unknown how platypus infants imbibe their milk, but some observations suggest suckling also. Owen (1868) noted that, as infants, monotremes have fleshy lips "transitorily manifested . . . at the suckling period." Some adult mammals, such as walruses and many cetaceans, also exploit suction during feeding (e.g., Gordon, 1984; Kastelein et al, 1994) (Chapter 16). In addition to helping seal the mouth during suction, the cheek (buccinator) muscles also function during mastication to maintain food between the upper and lower tooth rows for processing. Tongue and cheek movements coordinate to move food from one side to the other (side switching) during mastication (Hiiemae and Crompton, 1985). In some whales an expansive upper "lip" forms a lateral flap covering the baleen, overhanging the mandible when the mouth is closed (Owen, 1868). Finally, as noted previously, a mobile, prehensile upper lip is used by rhinoceroses

2. An Introduction to Tetrapod Feeding and other mammals for prehension of grasses and leaves. Some other structures to which the facial muscles contribute are significant in mammal feeding. Notable among these is the elephant trunk. Elephant trunks are muscular hydrostats that are stiffened and moved without the aid of internal skeletal support (Kier and Smith, 1985; Smith and Kier, 1989; see earlier discussion of the tongue). They are used as prehensile organs to grasp food items and to bring them into the mouth. The trunk terminates in one (Asian elephant) or two (African elephant) finger-like projections that can manipulate even very tiny objects (Shoshani, 1997). The subtlety of movement possible by the trunk is remarkable. Other mammals also use muscular hydrostatic, facial structures in feeding. Manatees use a large, mobile snout to evert stiff, perioral bristles that are used to sweep aquatic vegetation into the mouth (Marshall et ah, 1998a,b; Keep et al, 1998). The mobile snout of walruses may also function as a muscular hydrostat. The snout moves a dense mat of bristles, which are inferred to function, in part, during food identification, excavation, manipulation, and processing (e.g., Kastelein and Mosterd, 1989; Kastelein et al, 1991, 1994). Some mammals, including bovid antelope (Artiodactyla) and tapirs (Perissodactyla), have very mobile probosces that may function during feeding; in one species of dikdik, at least, the mobile snout is implicated in olfaction-mediated food selectivity, if not in feeding itself (e.g., Frey and Hofmann, 1996, 1997). Somewhat mobile anterior snouts {rhinaria) are characteristic of many mammals, particularly pigs and peccaries, which use them to root and to manipulate elements of the substrate during foraging (Herring, 1972). As noted previously, the lips are often used as prehensile organs to grasp plant matter during ingestion. Black rhinoceroses, for example, have a highly mobile, prehensile upper lip that is rather long and pointed, whereas white rhinoceroses have a square, nonprehensile lip (Kingdon, 1979; Nowak, 1991). This difference corresponds to the fact that the former species is a browser that grasps succulent vegetation with the lip, pulling it into the mouth, whereas the latter is a grazer that uses its stiff, keratinized upper lip as a stiff surface for cropping grasses. Extreme lip mobility is presumably effected by a muscular hydrostatic mechanism.

III. KINEMATICS OF FEEDING: THE GAPE CYCLE Having dealt briefly with the various parts potentially involved in tetrapod feeding, we can turn to their movements, or kinematics. Obviously, the ways in which tetrapods procure and process food are varied.

47

but virtually all feeding involves some degree of coordinated movement among jaws, tongue, and hyobranchium. As noted in Chapter 1, the form and function of these oropharyngeal structures are the focus of functional-morphological studies of vertebrate feeding. During feeding, movements of these morphological elements are repeated cyclically throughout food prehension, processing, transporting through the oral cavity, and swallowing. The pattern of movement is often highly regular, or stereotyped. The patterning and rhythmicity of such cyclical movements, which typically occur during feeding and locomotion, are thought to be initiated and controlled by central pattern generators (e.g., Dellow and Lund, 1971; Thexton, 1973; Cohen et al, 1988; Cohen, 1992). Central pattern generators are neural circuits that generate rhythmic patterns of neural output that, in turn, create rhythmic motor patterns, often without benefit of higher brain function. The motor patterns can be initiated and sustained by the central pattern generator without peripheral sensory feedback, but increasingly it is believed that in active, behaving animals there is extensive sensory modulation of cyclical feeding movements (e.g., Jtich et ah, 1985; Schwenk and Throckmorton, 1989; Cohen, 1992; Anderson and Nishikawa, 1993, 1997; Huang et al, 1993; Hiiemae, 1993; Hiiemae et al, 1995, 1996; Maglia and Pyles, 1995; Deban, 1997; Thexton and Hiiemae, 1997). In analyses of feeding the standard kinematic "unit" is the gape cycle (Bramble and Wake, 1985; Hiiemae and Crompton, 1985). The gape cycle represents simply the sequential pattern of velocity changes that occur during a single cycle of jaw opening and closing. This can be represented graphically as a gape profile or plot (Fig. 2.14). A complete feeding sequence usually involves many such cycles repeated one after the other (see later). It is often useful, therefore, to depict several gape cycles in a single plot to capture a larger portion of the feeding cycle. Furthermore, using the gape cycle as the point of reference, motions of the tongue, hyobranchium, head, and other relevant parts can be plotted simultaneously to create a schematic snapshot of a complex kinematic sequence involving many parts. Muscle activity patterns can be added to these for an even more complete picture (Fig. 2.15). Hence, implicit in the use of "gape cycle" is the occurrence of a suite of coordinated movements among oropharyngeal structures within the time frame delimited by a single open-close sequence of the jaws. Although gape profiles vary in their shape and complexity, they often exhibit a characteristic pattern of velocity changes that suggest discrete, intrinsic kinematic phases. The phases are delimited by inflection points in the profile {contra Smith, 1994) and when they occur each phase is given a standard name (Fig. 2.14): slow

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Kurt Schwenk

HEAD & NECK

MANDIBLE

SKULL

Extent. Retract.

Down

Up

Down

Up

HYO-LING. COMPLEX Post.

Ant.

Down

Up

GAPE

Open

Close

F I G U R E 2.14. Kinematic plot of a single "moder' gape cycle as proposed by Bramble and Wake (1985), with permission. FC, fast close; FO, fast open; SC-PS, slow close-power stroke; SO, slow open.

open I (SO I), slow open II (SO ll)Jast open {¥0)Jast close (FC), and slow close-power stroke (SC-PS). The ubiquity of this pattern among tetrapods led to the suggestion that there is a generalized "model/' or ancestral, gape cycle (which exhibits each of these phases along with characteristic patterns of synchrony in movements of the hyolingual complex and head) (Bramble and Wake, 1985). Some tetrapod taxa may not exhibit all phases of the model gape cycle, hence the generality of this model has been questioned (e.g., Bels and Goosse, 1990; Reilly and Lauder, 1990; Smith, 1994). Certainly, the model pattern is phylogenetically widespread and occurs variably even in taxa, such as salamanders, reputed to lack it (Larsen et al, 1989; Miller and Larsen, 1990; contra Reilly and Lauder, 1990). In any case, the model gape cycle is based primarily on intraoral transport cycles (see later). Cycles from other feeding stages tend to deviate from the model cycle in characteristic ways. As noted, the Bramble-Wake model predicts coordinated movements of the jaws, hyolingual complex, head, and neck, and therefore, a particular pattern of activity in associated muscles (Fig. 2.14). In general, the model suggests that as the jaws initially part, the tongue and hyobranchium are protracted, moving forward under the food item. In those species with muscular tongues, the tongue surface is "fitted" to the food item during this stage. At the initiation of FO, the tongue and hyobranchium are rapidly retracted with

the food adherent. During SC-PS the hyolingual complex is once again protracted to its rest position. The rapid increase in gape during FO serves to release the food item from contact with the teeth and palate so that it can be transported posteriorly by the tongue toward the pharynx. Lingual papillae create a "frictional surface" (McDowell, 1972) that interlocks with the food item to move it back. During hyolingual protraction to "reset" the mechanism, the food item is held in place by palatal teeth or rugae while the tongue is slid beneath it. SC-PS applies most appropriately to mammals whose jaw muscles are active during this phase to crush food between the tooth rows. In lizards and other tetrapods, jaw muscle activity does not necessarily occur during the intervening period between cycles (e.g., Throckmorton, 1980; Smith, 1984), hence in most taxa a short power stroke may be followed by a relatively longer stationary phase. In any case, a short slow-close phase is often apparent as the teeth once again contact the food item if still present between the jaws, slowing the rate of jaw closure. As noted earlier, a typical feeding sequence requires multiple gape cycles for completion that span multiple functions from prey capture to swallowing (see next section). A weakness of the Bramble-Wake model is that a single, general cycle (based primarily on transport cycles) cannot capture the variation one might expect in the kinematic relationships necessary to perform these different functions. Furthermore, although

49

2. An Introduction to Tetrapod Feeding

of the food as it is processed. Thus the Bramble-Wake generalized tetrapod gape cycle is a heuristic model that serves as a hypothesis for testing rather than a fixed reality of feeding kinematics in tetrapods (see Smith, 1994). Variation and evolution of the gape cycle are discussed further in Chapter 8. LOWER JAW

IV. KINEMATICS OF FEEDING: FEEDING STAGES A. Overview

R. DEEP TEMPORALIS

L. DEEP TEMPORALIS

L. GENIOHYOID

R. STERNOHYOID

ANTERIOR TONGUE MARKER (cm)

HYLOID MARKER (cm)

CONDYLE POSITION (cm)

FIGURE 2.15. Two successive masticatory cycles in a mammal (Tenrec), showing the synchronous representation of kinematic variables and muscle activity (EMG); from Oron and Crompton (1985), Journal of Morphology, copyright © 1985, John Wiley & Sons. Reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc. Abbreviations as in Fig. 2.14.

a series of feeding cycles might be entrained by a central pattern generator, patterning is modified by sensory feedback. Thus, modifications of this basic cycle are expected depending on where in the sequence of feeding the cycle occurs (i.e., which feeding stage; see next), the type of food, and the changing physical state

A complete feeding sequence involves from one to many gape cycles, which subserve several different behaviors. First, food must be captured or otherwise apprehended and brought to the mouth. Second, the food must be transported through the oral cavity toward the pharynx. During this traverse it may be processed in some way by the oral apparatus. Third, food collected in the pharynx must be emptied into the esophagus where peristalsis eventually takes over, moving the food into the stomach. These feeding stages are known, respectively, as ingestion, intraoral transport, and swallowing (Bramble and Wake, 1985; Hiiemae and Crompton, 1985). Sometimes processing is recognized as a separate stage. Although the nominal feeding stages are described as if discrete kinematic events, they often blend one into another so that transitional cycles are possible. Nonetheless, each stage has different functional outputs and makes different biomechanical demands on oropharyngeal structures, hence they are separable along these lines. As such, kinematic patterns of morphological elements vary more or less among stages. A standard terminology is suggested here and is maintained throughout the book (Table 2.1). Lack of consistency in the primary literature heretofore suggests that it would be worthwhile for workers to adopt such a standard nomenclature. Although the terms proposed here are as consistent as possible with mainstream usage in the primary literature, as a rule I have tended to split rather than to lump terms. This preserves specificity in meaning of certain terms that have tended to be conflated—a practice that greatly reduces their utility in scientific discourse. B. Stages of the Feeding Cycle 1. Ingestion Ingestion is the initial stage of feeding in which food is procured and brought into the mouth. For animals that feed on live prey, this stage is often equivalent to prey capture or prey prehension (in many mammals and a few other tetrapods, however, prey capture is a

50

Kurt Schwenk TABLE 2.1 Stage

Stages of Tetrapod Feeding

Predominant types

Comments

1. Ingestion

Jaw prehension Lingual prehension Suction Forelimb

Usually equivalent to prey capture in nonherbivorous species, but in some taxa a separate capture or subjugation phase precedes ingestion

2. Intraoral transport

Hyolingual Inertial Hydrodynamic

In mammals, stage I and stage II transport are recognized

Chewing (teeth) Puncture- crushing Mastication Nondental reduction (e.g., beaks and other keratinous structures) Shearing Crushing Rasping

Not all tetrapods process their food

4. Pharyngeal packing

Hyolingual

Probably restricted to lizards and turtles with muscular tongues, especially those with pronounced posterior lingual lobes

5. Pharyngeal emptying (swallowing)

Gravity Pharyngeal compression Cervical flexion Internal concertina Deglutition

Deglutition is restricted to mammals

3. Processing (food reduction)

distinct behavior that precedes ingestion). It remains true that ingestion is the least studied and least understood stage of feeding in most tetrapods (Hiiemae and Crompton, 1985; Schwenk and Throckmorton, 1989). Mechanisms for ingestion are variable. Most often it involves prehension of food with the jaws, usually their anterior portions. The actual points of contact, in most cases, are with the teeth or beak (in mammals the lips sometimes participate, as well). Jaw prehension is characteristic of caecilian amphibians, many turtles, many lizards, all snakes, crocodilians, many birds, and many mammals (Fig. 2.16a). Often there are morphological and behavioral specializations that enhance the ability to apprehend food with the jaws, particularly if the prey are fast-moving. Cranial kinesis in lizards may be one such adaptation (see Chapter 8). An elongate neck used for rapid strikes is characteristic of most snakes, some lizards, some turtles, and many birds. Many shorebirds have long, sharp bills used for spearing prey. Carnivoran mammals rip flesh from subdued prey with the teeth and some herbivorous species crop vegetation with the incisor teeth. Many aquatic tetrapods use the jaws for prehension underwater. Some

In mammals, deglutition cycles may be interlaced with transport cycles

The forelimbs participate in some taxa, alone, or with the jaws, to reduce food to smaller pieces before intraoral processing

All other forms of pharyngeal emptying characterize various nonmammalian taxa

crocodilians, for example, have narrow snouts and many sharp, monocuspid teeth that are putative adaptations for catching fish using rapid, sideways strikes of the head. Tongue, or lingual prehension, is the second most common form of ingestion (Fig. 2.16b). It is characteristic of terrestrial feeding in most frogs and salamanders.

FIGURE 2.16. (A) Jaw prehension (ingestion) in a lizard (Elgaria); note that the tongue is retracted and depressed; based on Frazzetta (1983); and (B) lingual prehension in a lizard (Phrynocephalus); based on Schwenk and Throckmorton (1989).

2. An Introduction to Tetrapod Feeding many turtles, many lizards, many birds, and many mammals. In some taxa, tongue prehension of prey is extremely rapid and the tongue is capable of lengthy excursions outside the mouth. This is most extremely developed in those species employing some form of ballistic tongue projection, notably some salamanders, frogs, and chameleons (see later). Many herbivorous mammals strip leaves off branches with the tongue or wrap the tongue around a bunch of grass to pull it out of the ground and draw it into the mouth. In all cases, lingual ingestion requires some form of lingual prehension, i.e., the tongue acts as a prehensile organ that grasps or adheres to a food item and draws it into the mouth. In most taxa there is direct adhesion between the food item and the lingual surface. Lingual adhesion probably results from a combination of frictional interlocking and wet adhesion (Bramble and Wake, 1985; Wagner and Schwenk, 2000; Schwenk, unpublished results), i.e., interdigitation of lingual rugosities with food surface features in combination with sticky mucus. In rare cases, suction may be generated by the tongue to enhance adhesion (Schwenk, 1983; Schwenk and Wake, 1988). There are a variety of ways in which the tongue can be protruded to effect food prehension. In most cases the tongue is anatomically coupled to the hyobranchium; however, the nature of this coupling is highly variable. In some species the coupling is tight so that little tongue protraction independent of the hyobranchium is possible (e.g., in most birds), but in other taxa there is only a loose connection. In most mammals, for example, the tongue is tightly adherent to the basihyal at its base, but it is nonetheless capable of extensive protrusion by means of hydrostatic deformation (see earlier discussion). In some ant- and termite-eating mammals the tongue musculature bypasses the hyobranchium altogether (Chapter 15) so that tongue and hyobranchial movements are virtually uncoupled. In most frogs the tongue has a muscular connection to the hyobranchial apparatus, but it is projected some distance from the mouth by inertial (rather than hydrostatic) elongation (Chapter 5). In salamanders the tongue varies in the extent of its attachment to the hyobranchium, but tongue protrusion is effected primarily by hyobranchial protraction rather than by protrusion of the tongue independent of the hyobranchium (Chapter 4). In extreme cases the entire length of the hyobranchial apparatus is projected from the mouth (Deban et al, 1997). In lingual feeding lizards, most tongue protrusion is also caused by hyobranchial protraction (Schwenk and Throckmorton, 1989), but some anterior tongue movement, both translational and hydrostatic, occurs as well (Chapter 8). In chameleons, the tongue is protruded on the hyobranchium as

51

in other lizards, but it is then projected entirely off the lingual process. The term tongue projection should be restricted to such cases in which there is a true, ballistic (i.e., free-floating) phase in the protrusion sequence. This will be true only for chameleons, some frogs, and some salamanders. In all other cases, extraoral tongue movement during ingestion is more accurately referred to as protrusion. In some aquatic tetrapods, ingestion is accomplished by means of suction generated by rapid expansion of the mouth and pharynx. In some cases the prey is actually drawn into the mouth, but in other cases the suction is "compensatory" in that it prevents the food item from being pushed away by the pressure wave generated by the head of the approaching predator (e.g.. Summers et al, 1998). In a few exceptional salamander species the tongue is used for prehension under water (Schwenk and Wake, 1988; J. Larsen, S. Deban, personal communication). Finally, the limbs occasionally participate in ingestion in some species. Although unusual among tetrapods as a whole, use of the forelimbs is the dominant mode of ingestion in primates in which the hands are typically the organs of food prehension. Food is grasped in the hand and brought to the mouth for processing (I have observed small primates taking bites from a mealworm held in the hand like a banana). Some other mammals commonly use the forelimbs for ingestion, including squirrels and other rodents, and raccoons (Carnivora). Mongooses (Carnivora) have been observed to pick up hard-shelled millipedes in the hand and dash them against a rock to split them open (Eisner and Davis, 1967; Eisner, 1968), however, the jaws are used for ingestion. Other carnivoran mammals, such as felids, use the forelimbs for apprehension and killing, but the jaws for ingestion. Some frogs use the forelimbs to hold or manipulate prey and occasionally to deliver it into the mouth. Occasional grasping and ingestion with the forelimbs are restricted to arboreal species, suggesting that climbing adaptations preadapted the forelimb for use in ingestion (Gray et al., 1997). Terrestrial turtles sometimes use the forelimbs to hold or manipulate food during ingestion, but they are never used to deliver food into the mouth (personal observation). Parrots often use a hind limb to grasp seeds and carry them to the mouth for husking by the beak and tongue (Homberger, 1986). Kinematics of the gape cycle during ingestion often depart somewhat from the Bramble-Wake model gape cycle. In some jaw-feeding lizards the gape profile is bell shaped, without discrete phases (e.g., Bels and Goosse, 1990), and in lingual-feeding species, slow open often occurs at wider gape angles relative to transport cycles, presumable to accommodate the

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Kurt Schwenk

thickness of the tongue during its extraoral excursion (e.g., Schwenk and Throckmorton, 1989). 2. Intraoral

Transport

Intraoral transport is the movement of food through the mouth following ingestion. Sometimes food is transported directly to the pharynx for swallowing, but often it is first moved to a position between upper and lower tooth rows for processing. In mammals that masticate, two stages of intraoral transport are recognized (e.g., Hiiemae et al., 1978; Hiiemae and Crompton, 1985). In stage I transport, food is moved posteriorly from the prehension point to a position between the postcanine teeth for processing. This movement usually involves lateral manipulation and positioning of the food item with the tongue, as well as propalineal transport. In stage 11 transport, food particles are transported further posteriorly to the pharynx during and after chewing. They are collected in the spaces behind the tongue, in front of, and to the sides of the larynx, called the vallecular and pyriform recesses. When a large enough bolus forms there a swallow cycle is interjected amidst the masticatory (chewing) cycles (see later). In nonmammalian species, stage I and stage II transport are not clearly distinguished, although analogous stages may occur in some species. In general, it should be recognized that food must initially be transported from its point of arrival in the mouth following ingestion to a position appropriate for processing, if it occurs. While this is most often a posterior movement of the food, it need not be. Following lingual ingestion in some salamanders, for example, some prey items initially come to lie posteriorly on the back of the tongue. They are then transported by the tongue anteriorly to a position between the teeth for crushing (e.g., Schwenk and Wake, 1993). In any case, during or following processing, food particles are next transported posteriorly into the pharynx in preparation for swallowing. In species that do not process their food (e.g., many amphibians), all transport cycles serve to move ingested food directly to the pharynx. In frogs, the tongue is uniquely attached at the front and flipped over the mandible during ingestion so that the end of the tongue that is posterior while at rest in the mouth becomes anterior and the point of prey contact while out of the mouth. Consequently, when the adherent food item is returned into the mouth it comes to rest far posterior in the oral cavity, nearly within the pharynx (see Chapter 5). Hence, in some cases, intraoral transport might be bypassed altogether and swallowing initiated immediately after ingestion. Hyolingual transport is the most common form of in-

traoral transport in tetrapods. Food is moved on the surface of the tongue, which, in turn, is moved by the hyobranchial apparatus. Hyolingual transport cycles most often approximate the model gape cycle of Bramble and Wake (1985). Usually discrete SO, FO, FC, and SC-PS phases are evident. During SO the tongue is moved anteriorly under the food item. In species with muscular tongues, the tongue is formed to the food, "cupping" it for more effective transport (e.g.. Smith, 1984; Franks et al, 1984, 1985; Schwenk et al, unpublished). At the initiation of FO the tongue is retracted rapidly, carrying the food item with it. Hyolingual retraction continues through jaw closing and reverses at the onset of the next transport cycle. During protraction the tongue moves ventrally, disengaging from the food item while it is held in place by palatal teeth, palatal rugae, or some other obstruction so that the tongue can be slid beneath it. Thus, caudad progression of the food item during transport is ratchet-like. In some salamanders and possibly other amphibians, protraction is a lengthy process that occurs during prolonged recovery and preparatory phases between gape cycles (Reilly and Lauder, 1990). Hyolingual transport in amniotes involves cyclical movements of the tongue body and hyobranchium, which are often evident as oval or "figure 8" trajectories in lateral view (e.g., Crompton et al, 1977; Hiiemae et al, 1981,1995; Crompton, 1989; Hiiemae and Crompton, 1985). In some species, inertial, rather than hyolingual, transport is utilized. Most often, as in many birds and some lizards, inertial transport involves a posterodorsal jerk of the head accompanied by jaw opening so that the food item is disengaged from the jaws and carried back toward the pharynx by its inertia (Cans, 1969). Following release the head is usually moved anteriorly over the food item to increase the extent of posterior movement. It is noteworthy that inertial transport is most often characteristic of taxa with reduced tongues. Crocodilians and some mammals that bolt large pieces of food also employ inertial transport. A rather different form of inertial transport is used by macrostomatan snakes (Chapter 9). In this case, the inertia of a large prey item is used to hold it in place while the snake uses asymmetrical, kinetic movements of its jaws to pull itself over the stationary prey. This is not inertial transport as typically conceived, but rather represents an unusual form of jaw-mediated intraoral transport. Nonetheless, inertia plays a significant role in its execution. In some constricting snakes, the prey item is pinned or held by the coils while the head is literally pushed over it by the elevated cervical region (Cundall, 1995). The prey is thus transported far posteriorly into the pharynx. Thus in snakes, distinctions among feeding stages are particularly blurred.

2. An Introduction to Tetrapod Feeding Finally, some aquatic tetrapods have secondarily evolved hydrodynamic transport in which water movements are used to transport prey items following suction feeding. Because the food is buoyant in the water, it need not be supported by the tongue. Indeed, the tongue is apparently a hindrance in most aquatic feeders and is usually reduced or lost (Bramble and Wake, 1985; see earlier discussion). As for suction during ingestion, expansion of the pharynx is used to generate negative pressures within the buccal and pharyngeal cavities to draw food items posteriorly. Food position in the mouth is manipulated by modulating intraoral pressure through pharyngeal expansion and contraction so that the food item can be drawn backward and also forward for positioning during processing and then swallowing. 3. Processing Processing is the mechanical breakdown of food within the oral cavity before it is swallowed. As noted earlier, it can be considered a subset of intraoral transport cycles, but because it is kinematically distinct from transport in the strict sense, it is considered separately here. There are different sorts of food processing and it is worth establishing a standard nomenclature to maintain clarity. First, any kind of intraoral food reduction or breakdown can be referred to generically as processing. Most processing involves the use of teeth to puncture, crush, grind, or slice the food. Food reduction with the teeth is referred to as chewing. Chewing usually results in the breakdown of the food into smaller pieces, a process known as comminution; however, in some cases the food item is merely punctured and crushed, softening the food and introducing salivary enzymes without its separation into smaller bits. This type of chewing is common in many lizards, for example, and is called, aptly enough, puncture-crushing. Puncture-crushing is typical of chewing in nonmammalian tetrapods in which upper and lower teeth do not occlude. Most often it involves the use of the marginal teeth of the jaws, but it can employ palatal teeth as well. Chewing in nonmammalian taxa is not limited to puncture-crushing. It was noted earlier, for example, that tuatara (Sphenodon) use double upper tooth rows and propalineal movements of the lower tooth row between them to create a shearing action that effectively slices food. In most mammals the upper and lower teeth fit precisely together so that tightly apposed surfaces slide past one another, cusps are aligned with basins, etc., a condition known as occlusion (Fig. 2.7h). Often, occlusion is so precise that tooth wear is used literally to hone

53

the fit between upper and lower teeth. Occlusion enables mammalian teeth to perform a variety of biomechanical tasks very effectively so that extreme comminution is typical of mammalian chewing (Hiiemae and Crompton, 1985). Chewing in mammals with occlusion is called mastication. The efficacy of occluding teeth is enhanced, in most cases (especially herbivores), by lateral or anteroposterior movements of the lower jaw that create a masticatory orbit (Hiiemae, 1978). Occlusion and masticatory orbits uniquely characterize mammalian chewing (although some mammals have secondarily lost one or both). Mastication is sometimes used indiscriminately in reference to any kind of chewing, but this is inaccurate and undesirable. Mammal species that do not masticate their food (e.g., cetaceans and myrmecophages) typically lack dental occlusion and often exhibit simplified or reduced teeth, or no teeth at all. Finally, processing may involve structures other than the teeth. In many turtles and birds, for example, the tight fit of the lower jaw into the upper jaw creates a shearing action of the beak. Additional crushing can occur anteriorly and laterally in the beak between upper and lower triturating surfaces (see earlier discussion). Some monotreme mammals reduce food by rasping it with keratinous structures on the tongue and palate (see earlier discussion). 4.

Swallowing

Swallowing is the movement of food particles collected in the pharynx into the esophagus. Once in the esophagus, peristalsis transports the bolus to the stomach (once mechanically reduced or swallowed, the food item is referred to as a bolus). In lizards (and possibly other nonmammalian tetrapods), true swallowing is preceded by a separate stage called pharyngeal packing (Smith, 1984, 1986). This is treated later. In mammals, these actions are more or less combined into a single, reflexive contraction of the pharynx that empties it of the food that has collected during mastication and transport. Smith (1992) suggested that the general term "pharyngeal emptying" be applied to nonmammalian tetrapods and that "swallowing" and "deglutition" be restricted to mammals whose mechanism of pharyngeal emptying is highly derived. I use Smith's (1992) terms here with slightly modified meaning: swallowing is the generic, nontechnical term for pharyngeal emptying in all tetrapods; pharyngeal emptying is the generic, but technical term for swallowing in tetrapods; and deglutition is the specialized form of pharyngeal emptying unique to mammals. Although I am reluctant to deviate terminologically from Smith (1992), I believe that retention of "swallowing" as a

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general tetrapod term is more consistent with common usage. Likewise, "pharyngeal emptying" describes a general tetrapod feeding stage of which "deglutition" is a specialized sort. Very little is known about swallowing in amphibians. In terrestrial salamanders and some frogs, intraoral transport is hyolingual, so presumably food is moved into the pharynx by means of the tongue, possibly followed by pharyngeal constriction in a manner similar to lizards (later). However, there are potentially at least two unique features of amphibian swallowing (Duellman and Trueb, 1986). First, the pharynx in many species is ciliated, suggesting that very small food particles might be moved into the esophagus by ciliary transport. Second, in most frogs and salamanders, food is pushed backward into the esophagus by retraction of the large eyeballs into the buccal cavity! This action is mediated by the retractor bulbi muscles, which pull the eyes down through large palatal vacuities, possibly forcing food posteriorly. In caecilians, the lack of tongue (and eye) mobility suggests a different mechanism for swallowing. Tongue inflation and elevation by means of engorgement with blood may help pack food into the pharynx or to empty it (some caecilian tongues contain large vascular sinuses; see earlier discussion). In reptiles, pharyngeal emptying is variable. In lizards and turtles with muscular tongues, food is initially pushed into the capacious pharynx by posterodorsal movements of the tongue and hyobranchial apparatus (Smith, 1984; Bramble and Wake, 1985) during a discrete kinematic stage known as pharyngeal packing. Pharyngeal packing is followed by pharyngeal emptying (swallowing in the strict sense), which is accomplished by contraction of the superficial, sling-like constrictor colli muscles that compress the pharynx to force food posteriorly into the esophagus. In some cases, ventroflexion of the head at the atlanto-occipital joint serves analogously to constrict the pharynx (personal observation). In varanid lizards (and possibly other species that lack posterior, muscular lobes of the hindtongue; see Fig. 2.13c) pharyngeal packing is accomplished by movements of the unusually complex hyobranchial apparatus (Smith, 1986). In snakes, the initial stages of swallowing are no more than a continuation of intraoral transport by means of skull kinesis. Large food items are simply forced into the esophagus by movements of the jaws or palate, or constricted prey are pinned by body coils and the head is forced over the immobilized prey item (see earlier discussion). However, in many, if not most, snakes, swallowing is facilitated in later stages by sinuous, concertina-like movements of the body axis within the body wall (i.e., the "concertina" flexion is internal), which

take over from the kinetic skull in pushing the bolus through the elongated esophagus (Cundall, 1995; Kley and Brainerd, 1996). In archosaurs (birds and crocodilians) the pharynx is emptied by means of gravity (e.g., Busbey, 1989; Zweers, 1982) and hyobranchial compression (Chapter 10). Long-necked birds frequently exhibit cervical flexure during swallowing as well. In nonmammalian tetrapods, swallowing is usually manifest as a discrete kinematic stage subsequent to intraoral transport. During pharyngeal packing in lizards, the posterodorsal movements of the hyolingual apparatus occur during SO, whereas in other feeding stages the tongue always moves anteriorly during SO (Smith, 1984). Thus, packing and swallowing cycles present distinct kinematic profiles that deviate significantly from the model cycle. In mammals, however, the kinematics of pharyngeal emptying are quite different. As noted, mammals employ a unique mechanism of swallowing known as deglutition. Smith (1992) enumerated several derived aspects of mammalian deglutition: (1) it is driven primarily by the action of internal pharyngeal muscles, which are lacking in all other tetrapods; (2) the swallow is a stereotyped reflex involving an explosive, but highly coordinated contraction of the palatal, lingual, pharyngeal, and hyobranchial musculature; (3) cranial nerve X (trigeminal) is primarily involved in deglutition through innervation of the pharyngeal muscles, whereas in other tetrapods, cranial nerve VII (facial) is primarily involved through its innervation of the constrictor colli muscles; and (4) deglutition cycles are integrated into intraoral transport cycles, which in turn are integrated into processing cycles. In reptiles, pharyngeal packing and emptying are discrete stages that follow upon a series of transport cycles. The essential characteristic of mammalian deglutition is the participation of the unique pharyngeal musculature (discussed earlier). The transformation of the mammalian pharynx into a muscular "tube" continuous with a soft, muscular palate, and the muscles of the tongue and hyobranchium, is part of a sweeping reorganization of the mammalian feeding apparatus relative to other tetrapods. A mammalian swallow represents an explosive, sphincter-like contraction of this musculature that restricts the lumen of the pharynx, forcing the food bolus into the esophagus. The reflex is apparently driven by sensory feedback from the pharynx that alerts the central nervous system to the presence of a sufficiently large bolus of processed food in the vallecular and pyriform recesses (Hiiemae and Crompton, 1985; Crompton, 1989; Thexton and Crompton, 1998). The extreme rapidity of this reflex allows it to be interjected into cyclical transport and chewing cycles, as opposed to the relatively slower and more involved pha-

2. An Introduction to Tetrapod Feeding

ryngeal packing and emptying cycles of lizards, which must follow a discrete stage of intraoral transport.

V. C O N C L U D I N G REMARKS If nothing else, this chapter serves to highlight the remarkable diversity of the tetrapod feeding apparatus that is all the more remarkable for its exploitation of a common set of parts (see Chapter 1). Perhaps the most important underlying theme to tetrapod feeding is the evolution of the tongue and its integration with the hyobranchial apparatus in feeding function. Modification and adaptation of the hyolingual apparatus are prominent features of tetrapod feeding evolution. As lengthy as it is, this introduction provides only a very superficial view of tetrapod feeding diversity. Few overarching patterns will be evident to the novice reader. This is partly an artifact of this cursory treatment, but it is also reflects the fundamental fact that many general attributes of the feeding system are clade specific. As such, although diverse overall, particular systems are typically characteristic of large, monophyletic species groups represented taxonomically at the family or suprafamilial level, within which they remain somewhat uniform. While this might also be an artifact resulting from the loss of intermediate forms through extinction, it more likely reflects real processes that limit the ease with which complex, functionally integrated systems can be evolutionarily reorganized (e.g.. Wake et al, 1983; Roth and Wake, 1989; Wagner and Schwenk, 2000; Schwenk, 2000b). Thus, we should expect that the kind of phenotypic remodeling necessary to create a novel feeding system to be a relatively rare evolutionary event associated phylogenetically with the origin of new clades and adaptive radiations. A prediction of this line of reasoning is that local adaptation to transient ecological conditions is not a general feature of tetrapod feeding evolution. Rather, feeding systems seem to reflect more fundamental aspects of phenotypic organization and adaptation. It is a challenge, therefore, to discern commonalties among the related, but divergent types of feeding systems among tetrapods. Individual, taxonspecific chapters address the issues of feeding system form, function, and evolution on a finer and more tractable scale. References Ahlberg, P. E., J. A. Clack, and E. Luksevics (1996) Rapid braincase evolution between Panderichthys and the earliest tetrapods. Nature 381:61-64. Albright, R. G., and E. M. Nelson (1959a) Cranial kinetics of the gen-

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ing mechanics in the shingle-back lizard Trachydosaurus rugosus (Scincidae, Reptilia). ]. Morph. 181:271-295. Witmer, L. M., and L. D. Martin (1987) The primitive features of the avian palate, with special reference to Mesozoic birds. Docum. Lab. Geol. Lyon, No. 99:21-40. Witmer, L. M., and K. D. Rose (1991) Biomechanics of the jaw apparatus of the gigantic Eocene bird Diatryma: implications for diet and mode of life. Paleobiology 17:95-120. Wu, X.-c, H.-D. Sues, and A. Sun (1995) A plant-eating crocodyliform reptile from the Cretaceous of China. Nature 376:678-680. Young, B. A. (1997) On the absence of taste buds in monitor lizards (Varanus) and snakes. ]. Herp. 31:130-137. Young, B. A. (1998) The comparative morphology of the intermandibular connective tissue in snakes (Reptilia: Squamata). Zool. Anz. 237:59-84. Zaher, H. (1994) Comments on the evolution of the jaw adductor musculature of snakes. Zool. ]. Linn. Soc. I l l : 339-384. Zardoya, R., and A. Meyer (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc. Natl. Acad. Sci. USA 95:14226-14231. Ziswiler, V, and D. S. Earner (1972) Digestion and the digestive system. Pp. 343-430. In: Avian Biology, Vol. 2. D. S. Earner and I. R. King (eds.). Academic Press, New York. Zusi, R. L. (1993) Patterns of diversity in the avian skull. Pp. 391-437. In: The Skull, Vol. 2. ]. Hanken and B. K. Hall (eds.). Univ. of Chicago Press, Chicago. Zweers, G. A. (1982) The feeding system of the pigeon (Columba livia L.) Adv. Anat. Embryol. Cell Biol. 73:1-105. Zweers, G. A., and H. Berkhoudt (1991) Recognition of food in pecking, probing, and filter feeding birds. Pp. 897-901. In: Acta XX Congressus Internationalis Ornithologici. New Zealand Ornithological Congress Trust Board, Wellington. Zweers, G. A., A. F. C. Gerritsen, and P. ]. van Kranenburg-Voogd (1977) Mechanics of feeding of the mallard {Anas platyrhynchos L.; Aves, Anseriformes): the lingual apparatus and the suctionpressure pump mechanism of straining. Pp. 1-109. In: Contributions to Vertebrate Evolution, Vol. 3. M. K. Hecht and F. S. Szalay (eds.). Karger, Basel.

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C H A P T E R

3 Aquatic Feeding in Salamanders STEPHEN M. DEBAN AND DAVID B. WAKE Museum of Vertebrate Zoology and Department of Integrative Biology University of California Berkeley, California 94720

canum. Some undergo partial metamorphosis and possess both adult and larval features when reproductive, such as the fully aquatic Cryptobranchus. Others are primarily terrestrial and become secondarily aquatic as metamorphosed adults, notably during the breeding season. The family Salamandridae contains the most representatives of this type, known commonly as newts. Salamanders covered in this chapter may be terrestrial, semiaquatic, or fully aquatic. They may return to the water only periodically and may feed on both land and in water. Discussion here focuses on the aquatic feeding biology of these taxa. Terrestrial feeding of semiaquatic and terrestrial salamanders is discussed in the next chapter. Here we describe the various feeding behaviors: foraging, ingestion (prey capture), prey processing, intraoral prey transport, and swallowing. We review the relevant morphology and function of the sensory and motor systems and analyze the biomechanical function of the feeding apparatus. Finally, we consider the evolution of aquatic feeding systems within and among the major taxa of salamanders.

I. INTRODUCTION A. Systematics B. Natural History C. Feeding Modes and Terminology II. MORPHOLOGY A. Larval Morphology B. Adult Morphology C. Sensory and Motor Systems III. FUNCTION A. Ingestion Behavior and Kinematics B. Prey Processing C. Functional Morphology D. Biomechanics E. Metamorphosis F. Performance G. Variation IV. DIVERSITY AND EVOLUTION A. Features of Salamander Families B. Phylogenetic Patterns of Feeding Form and Function V. OPPORTUNITIES FOR FUTURE RESEARCH References

L INTRODUCTION

A. Systematics In this chapter and the next we use a recent phylogenetic hypothesis (Fig. 3.1) based on combined morphological and molecular data (Larson and Dimmick, 1993). The suborder Sirenoidea (Duellman and Trueb, 1986) is the basal clade in this phytogeny, containing only the Sirenidae, followed by a split between the Cryptobranchoidea (which contains the families Cryptobranchidae and Hynobiidae, both of which are external fertilizers) and the Salamandroidea (which has

Aquatic feeding is w^idespread among salamanders. All 10 families include members that are aquatic during part of their lives and all have members that are aquatic or semiaquatic as adults. Aquatic feeding behavior, morphology, and function in salamanders are accordingly diverse. Most aquatic adult salamanders are perennibranchiate or paedomorphic forms that forego metamorphosis and function as larvae w^hen sexually mature, such as the axolotl, Ambystoma mexi-

FEEDING (K.SchwenKed.)

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Copyright © 2000 by Academic Press. All rights of reproduction in any form reserved.

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S t e p h e n M. D e b a n a n d D a v i d B. W a k e

Sirenidae

_J

Sirenoidea

Cryptobranchidae Cryptobranchoidea Hynobiidae Amphiumidae Plethodontidae Rhyacotritonidae Salamandridae

Salamandroidea

Ambystomatidae Dicamptodontidae Proteidae

F I G U R E 3.1. Phylogenetic hypothesis of the relationships of the salamander families, from Larson and Dimmick (1993). This tree is based on a combined set of morphological and molecular data.

internal fertilization). The interrelationships of the three main clades within the Salamandroidea are uncertain. The first clade contains the Rhyacotritonidae, and the second the Plethodontidae and Amphiumidae as sister taxa. Within the third clade, the Proteidae is the outgroup to the Salamandridae, Dicamptodontidae, and Ambystomatidae, with the last two being sister taxa. B. Natural History Intimately tied to the form and function of the feeding systems of salamanders is their life history. The ancestral life history of salamanders is complex, like that of many frogs and caecilians, and includes an aquatic larval stage and a terrestrial or semiterrestrial adult stage, separated by a period of concentrated postembryonic development known as metamorphosis. Throughout this biphasic life history a salamander must capture and subdue living prey, first in water and then on land, and uses different means in these two environments. Aquatic salamanders typically ingest prey by rapidly expanding the mouth and throat, drawing prey in by suction, whereas terrestrial salamanders project a sticky tongue from the mouth to ensnare prey. These behaviors are performed rapidly, in a fraction of a second, ensuring that even highly evasive prey are captured. Six families of extant salamanders have members with the ancestral life history: Hynobiidae, Salamandridae, Rhyacotritonidae, Dicamptodontidae, Ambystomatidae, and Plethodontidae. The most frequent

departure from the ancestral life history is paedomorphosis, in which sexual maturity occurs while larval morphology is retained. This pattern is present in most families of salamanders in varying degrees of expression. It is most apparent in the Sirenidae and Proteidae, where it is termed perennibranchiation because of the retention of external gills and posterior gill bars, and less apparent in the Amphiumidae and Cryptobranchidae, whose members possess a mixture of larval and adult features. Both perennibranchiate forms and those with the ancestral life history are found in the Hynobiidae, Ambystomatidae, Dicamptodontidae, Plethodontidae, and Salamandridae. A second common departure from the ancestral life history is direct development, in which the terrestrial adult lays eggs on land, the larval stage remains encapsulated or is bypassed altogether, and a terrestrial juvenile emerges from the egg. Direct development is found only in Plethodontidae, but has evolved repeatedly in this family. This life history characterizes most plethodontids (i.e., all members of the tribes Plethodontini and Bolitoglossini) and thus over half of all salamanders. The third departure is viviparity, in which embryonic development occurs inside the oviducts of the mother, and is present only in the genera Salamandm and Mertensiella of the Salamandridae. In taxa with the ancestral life history, the aquatic larva ingests and manipulates prey using suction generated in the mouth, whereas the terrestrial adult uses the tongue. Perennibranchiate forms which retain the larval morphology also retain the larval suction feeding behavior. Direct developers either pass through a nonfeeding larval stage while encapsulated or bypass the larval stage altogether and emerge as tongueflipping terrestrial juveniles. Viviparous salamandrids give birth either to larvae, which suction feed, or to metamorphosed, terrestrial juveniles, which use tongue protrusion. During development in the oviducts of the mother, larvae and metamorphs feed on unfertilized eggs or smaller developing siblings (Alcobendas et al, 1996); the intraoviductal feeding behavior remains undescribed. Aquatic salamanders inhabit diverse freshwater environments, including lakes, ephemeral ponds, bogs, swamps, drainage ditches, springs, rivers, streams, and mountain brooks. Larvae can be divided into three types based on external morphology (Valentine and Dennis, 1964): pond type, stream type, and mountainbrook type. Pond-type larvae have large, bushy gills, deep tail fin that extends onto the body, peculiar paired organs called balancers protruding from the head during early larval development, and are found in standing or slowly flowing water where they float and swim

3. Aquatic Feeding in Salamanders in the water column. Stream-type larvae generally have small external gills and a shallow tail fin that does not extent onto the back, are found in quickly flowing water, and locomote by walking on the substrate and swim in short bursts. Mountain brook types have tiny gills and a shallow tail fin that does not extend onto the body and live in torrents and steep, cold mountain streams. Both stream and mountain brook types may be associated with a stream habitat, making use of different microhabitats. Most larval and perennibranchiate salamanders can be classified into one of these groups, although intermediates do exist. These three types of salamander larvae do not differ markedly in feeding biology. The literature on salamander diet is enormous and cannot be reviewed here in any detail, however, somie generalizations are presented. Salamanders are carnivorous in all stages of life, eating primarily live prey, including arthropods (mostly insects: Diptera, Ephemeroptera, and Trichoptera; as well as crustaceans: Isopoda, Ostracoda, Amphipoda, and Decapoda), mollusks, worms, fish, and amphibians (Martof and Scott, 1957; Peck, 1973; Joly, 1981; Petersen et ah, 1989; Tumlison et al., 1990). Some forms (e.g., cryptobranchids; Nickerson and Mays, 1973) may occasionally scavenge. Cannibalistic morphs oiAmbystoma eat primarily other salamanders, including members of their own species (e.g., Collins and Holomuzki, 1984). Terrestrial and aerial prey are occasionally eaten as they happen to fall or land in the water. The stomach contents of aquatic salamanders are generally representative of the prey available in the microhabitat, suggesting that little dietary specialization occurs (Duellman and Trueb, 1986). Avoidance of distasteful prey is more probable than specialization, although salamanders may select prey based on various parameters such as size, movement pattern, and nutrient value (Avery, 1968; see Roth, 1987, for a review). Larvae of a given species of salamander at different stages of growth may show differences in diet due to prey capture abilities (Bell, 1975; Brophy, 1980) or habitat partitioning (Leff and Bachmann, 1986), and diet may vary with seasonal changes in prey abundance (Burton, 1977). In general, the diet contains prey items of the appropriate size (White, 1977) in the frequency that they are likely to be encountered within the microhabitat. Depending on prey density and prey type, salamanders exhibit either active foraging in which they seek out and pursue prey or sit-and-wait foraging where they remain stationary and let prey come to them (Anthony et al, 1992; Jaeger and Barnard, 1981; Uiblein et ah, 1992); some salamanders have been shown to switch between foraging modes in the course of larval

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development (Leff and Bachmann, 1986). Salamanders, as ectotherms, do not require much food to sustain themselves. A larval or adult salamander can be maintained in captivity on little food, and some remain healthy after months without eating. Simply obtaining enough food to stay alive is probably not a challenge for most salamanders; however, salamanders living in marginal conditions such as caves probably experience a scarcity of prey. The amount eaten influences growth rate and energy stores, and body size and the amount of stored fat are directly related to reproductive output. These relationships make competition for prey and, more generally, the trophic ecology of salamanders potentially important in understanding salamander feeding and may help explain the outstanding prey-capture abilities of some species. C. Feeding M o d e s and Terminology Aquatic salamanders capture or ingest prey by using the tongue, the jaws, or water flow (i.e., suction). The prey is then transported into the mouth and manipulated by water flow or movements of the tongue. Processing of prey is minimal and usually does not involve reduction or chewing, although this may occur to some degree in large taxa (e.g., amphiumids). Swallowing is the final stage of feeding in which the prey enters the esophagus. Salamanders capture prey by rapid movements of the body, jaws, and hyobranchial apparatus. A salamander can cover the initial distance between itself and the prey by (1) bringing the prey toward itself as in suction feeding, (2) extending an appendage to grasp the prey as in lingual prehension, or (3) moving its whole body toward the prey as in jaw prehension. A combination of these methods is often used to get the prey into the mouth. Suction feeding involves expanding the buccal cavity during mouth opening and drawing water and prey into the mouth while the gill slits are held closed. The buccal cavity is expanded by depression of the hyobranchial apparatus. Water is then expelled through the gill slits or mouth by elevation of the hyobranchial apparatus. Suction feeding is also called "gape-and-suck'' feeding. Lingual prehension involves grasping prey with the tongue and also relies on movements of both the jaws and hyobranchial apparatus. The hyobranchial apparatus, with the sticky tongue pad at its rostral tip, is protruded from the mouth toward the prey. The tongue pad adheres to the prey and the hyobranchial apparatus is then retracted, bringing prey either between the jaws or entirely into the buccal cavity. This behavior is also called tongue prehension, tongue flipping, tongue projection.

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or tongue protrusion and is accomplished by forward sHding and folding movements of hyobranchial apparatus. Jaw prehension is simply closing the mouth around the prey item so that it is trapped between the upper and the lower jaws. The salamander brings the jaws near the prey by lunging forward or sweeping the head laterally. The hyobranchial apparatus plays little role in jaw prehension. While jaw and lingual prehension are performed both on land and in water, suction feeding can only be performed aquatically because it relies upon the incompressibility of water to create enough flow to entrain the prey. The additional term ram feeding denotes ingestion behavior in which the salamander lunges forward and engulfs the prey without grasping it between the jaws. Suction feeding is the most conimon mode of ingestion among aquatic salamanders—it is used by all larvae and most species of aquatic adult salamanders. In addition, it is used by most bony fish (MuUer and Osse, 1984). The widespread use of suction feeding among aquatic vertebrates implies that it is an extremely effective way to capture prey in water (see also Chapter 16). Suction feeding is rapid; a large Cryptobranchus completes the behavior in less than one-tenth of a second. Suction feeding is also forceful and can draw even large, elongate, or highly elusive prey entirely into the mouth. Most secondarily aquatic adult salamanders are paedomorphic and perennibranchiate, and suction feed as their larvae do. Many aquatic salamanders, such as aquatic salamandrids and some hynobiids, undergo metamorphosis and lose larval features, but continue to suction feed with their adult morphology. Some salamandrids, for example Pachytriton, do so with great proficiency (Miller and Larsen, 1989) (Fig. 3.2). Others, such as cryptobranchids and amphiumids, appear to undergo partial metamorphosis, developing unusual adult structures while retaining some larval features such as posterior branchial cartilages, labial lobes, gill slits, and external gills; these groups suction feed. Some metamorphosed aquatic and semiaquatic salamanders, including all plethodontids and rhyacotritonids and some hynobiids, do not use suction to capture prey in water. Instead they use ancestral terrestrial ingestion behaviors, lingual and jaw prehension, to capture aquatic prey (Deban and Marks, 1992; Schwenk and Wake, 1993; Larsen, personal communication). Because lingual prehension and jaw prehension are performed more commonly by terrestrial forms and because they are performed in water in the same way they are on land, they will not be stressed here. Instead they will be discussed in the following chapter on terrestrial feeding in salamanders. Suction feeding behav-

F I G U R E 3.2. Suction-feeding behavior of an adult Pachytriton sp., a fully aquatic newt of the family Salamandridae. Note the rapid disappearance of the worm into the salamander's mouth, the extensive upper labial lobes occluding much of the lateral gape, and the pronounced buccal expansion and hyobranchial depression. The video frames are 8.3 msec apart, and the background is a 5-mm grid.

ior, morphology, and function in both larval and adult salamanders will be emphasized in this chapter. II. MORPHOLOGY Morphology is one of the most completely known aspects of the feeding biology of salamanders. Exten-

3. A q u a t i c F e e d i n g in S a l a m a n d e r s

sive anatomical data have been gathered over the last century and descriptions of head morphology exist for many salamander taxa (Parker, 1882; Driiner, 1901, 1904; Francis, 1934; Edgeworth, 1935; Piatt, 1938; Schumacher, 1958; Severtsov, 1964). Still, all morphological data relevant to feeding are not available for every group. Feeding behavior relies on morphological features of the skull, jaws, hyobranchial apparatus, tongue pad, gill slits, and labial lobes. Both larval and adult aquatic salamanders must feed in the same environment, and thus share many of these features. This section describes the general pattern of the feeding morphology of larval and adult salamanders. Most features of the larval feeding system presented here persist in the adults of perennibranchiate forms, i.e., perennibranchiate adults retain an essentially larval morphology. Metamorphic forms lose many larval morphological features, but may retain the larval feeding behavior while supplementing it with terrestrial feeding behavior. Metamorphic forms are discussed in a later section on adult morphology. A. Larval Morphology The head of larval salamanders is tapered anteriorly with an anterior mouth opening and posterior gill slits. Bushy external gills protrude posterolateral^ and have up to four main branches, or rami, each with numerous vascularized fimbriae. The eyes are lidless and do not protrude. Neuromasts of the lateral line system are abundant around the mouth and sides of the head.

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and prominent labial lobes occlude the sides of the mouth. The teeth of larval salamanders are sharply pointed, typically nonpedicellate, and monocuspid and consist of a cylindrical base fused to a conical apex. They lack the suture plane of adult pedicellate teeth (Beneski and Larsen, 1989a,b). Dentition is generally homodont, and teeth are borne on the premaxilla, maxilla, vomer, and palatine or palatopterygoid of the upper jaw and the dentary and coronoid of the lower jaw (Fig. 3.3). Teeth grow in size and number during larval life. New tooth loci are added with the enlargement of jaw bones (Bonebrake and Brandon, 1971). Teeth are added posteriorly along the maxillae and dentaries and posterolaterally to the vomers (Parker and Dunn, 1964; Worthington and Wake, 1971). At metamorphosis, teeth of the coronoid and palatopterygoid usually disappear with the disintegration of these bones, and vomerine teeth extend onto the parasphenoid (Wilder, 1928). The tongue is usually absent or poorly developed in larvae; if present, it possesses few of the glands or papillae of the tongue pad of postmetamorphic individuals. Larvae often possess a fold in the floor of the mouth just rostral and ventral to the anterior elements of the hyobranchial apparatus, called a buccal fold or anterior fold. This region of overlap is just beneath the tongue and it accommodates ventral expansion of the buccal floor during suction feeding. A ventral gular slit is often present at the level of the external gills and accommodates extension of the skin of the throat during buccal expansion. Extensions of skin on the upper and lower jaws

premaxilla maxilla lacrimal pterygoid

1 cm

F I G U R E 3.3. Larval skull of the aquatic hynobiid Batrachuperus mustersi in dorsal, lateral, and ventral views. Note the presence of maxillae, lacrimals, septomaxillae, and prefrontals, as well as separate prootic, opisthotic, and exoccipital ossifications.

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Stephen M. Deban and David B. Wake

called labial lobes block the sides of the mouth and direct the gape anteriorly. Upper and lower lobes are fused posteriorly and interlock or simply overlap anteriorly; in larvae the regions where upper and lower lobes meet are called labial folds. Labial lobes have long been recognized as important for effective suction feeding (Matthes, 1934). These interlocking lobes and their folds allow for expansion during mouth opening and, at the same time, prevent water from entering the mouth from the sides. During suction feeding, the labial lobes narrow the gape and direct it anteriorly, thus restricting, focusing, and accelerating water flow and increasing the likelihood that prey are captured. Two or three gill slits (also called gill apertures or gill clefts) are located on each side of the head below the external gill rami. The gill slits lie between the distal elements (epibranchials) of the hyobranchial apparatus and open into the mouth. Water that enters the mouth during suction feeding is expelled through the gill slits after the prey has been captured. Interlocking fingers of tissue or mineralized tooth-like elements called gill rakers are present on the pharyngeal surfaces of the gill bars of some taxa and help prevent prey from escaping as water is expelled. 1. Larval Skull, Jaws, and Hyobranchial

Apparatus

The larval skull consists of the posterior neurocranium and auditory capsules connected via parachordals and trabeculae to the anterior nasal capsules, invested by dermal bones dorsally and by palatal bones and attached ventrally to the suspensorium (Fig. 3.3). Posterior ossifications include the prootic, opisthotic, and exoccipital, which together comprise the occipitootic (Trueb, 1993). Dorsal bones include the paired frontals and parietals. Marginal tooth-bearing bones are the paired maxillae and the premaxillae, which are paired or fused medially. Bones of the palate include the paired vomers, the single parasphenoid, and the paired palatines or palatopterygolds. Palatines are present as separate elements only in the Sirenidae, positioned caudal to the vomers and bearing many teeth. Palatopterygoids are present caudal to the vomers in the Proteidae (where they articulate with the vomers and quadrates to form robust components of the upper jaw) and in larval plethodontids (where they are freefloating) and bear teeth on their rostrolateral edges. The orbitosphenoids form around the trabecular cartilages. The suspensorium, which connects the lower jaw to the skull, consists of the cartilaginous palatoquadrate and osseous quadrate invested by the bony pterygoid (which is absent in all plethodontids) and squamosal. The quadrate articulates with the articular of the lower jaw.

The skull bones of larval salamanders are loosely articulated and less robust than in the adult. Sutures between bones are lacking or incomplete, or gaps exist between bones. During growth, the bones increase in relative size and their degree of overlap and fusion. Larval skull morphology appears more conservative taxonomically than that of adults, and the phylogenetic diversity of larval skull morphology is not as well documented. The upper jaw consists of the paired or fused premaxilla, vomer, palatopterygoid, and, in some cases, the late-appearing paired maxilla, all of which bear teeth. The maxilla, when present, is loosely attached to the skull. The maxillae are absent in the larva of many taxa and appear during metamorphosis. In some perennibranchiate taxa the maxilla never forms (e.g., Necturus and Pseudobranchus) or appears late and remains a small, free-floating element (e.g.. Siren; Reilly and Altig, 1996). In these, the palatine or palatopterygoid forms a robust, dentate component of the upper jaw. In all taxa the medial parasphenoid forms the palate. The lower jaw consists of Meckel's cartilage invested by the tooth-bearing dentary, the prearticular (also called the gonial), usually the toothed coronoid (also called the splenial), and the angular (in cryptobranchoids). The articular cartilage of the lower jaw forms a joint with the quadrate of the skull, which is positioned between the orbit and the otic capsule. The jaw joint is far anterior in most larvae and perennibranchiate forms, reducing the gape. The hyobranchial apparatus of larval salamanders is composed of interconnected skeletal elements that lie in the floor of the mouth and throat and border the gill slits. An unpaired medial element, the basibranchial (sometimes called the copula), forms the main axis of the larval hyobranchial apparatus (Fig. 3.4) with which the remaining bilaterally paired elements articulate. The basibranchial articulates rostrally with the ceratohyals and caudally with the first and second ceratobranchials. These elements are sometimes called hypobranchials (Reilly and Lauder, 1988b), but likely represent the fusion of the ancestral hypobranchial and ceratobranchial, and here are called ceratobranchials. A third ceratobranchial is present in cryptobranchoids, but does not meet the basibranchial (see Batrachuperus, Fig. 3.4). The ceratobranchials are in turn attached to the more distal epibranchials (sometimes called ceratobranchials; Reilly and Lauder, 1988b), which number three or four on each side of the main axis and which curve dorsally to border the gill slits and support the external gills. An unpaired, medial element, the urohyal (also called the second basibranchial or os thyroideum), lies caudal to the basibranchial and is often continuous with it. Hypohyals lie between the ceratohyals and the

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Dicamptodon ensatus (L)

Pseudobranchus striatus (A)

Gyrinophilus porphyriticus

Proteus anguinus (A)

(L)

Batrachuperus mustersi (L)

Amphiuma means (L)

F I G U R E 3.4. Hyobranchia (in ventral view) of larval and perennibranchiate salamanders of six families. Cartilage is shown in white and ossification or mineralization is shaded. Scale bars equal 3 mm. See Table 3.1 for abbreviations. Proteus drawing is adapted from Marche and Durand (1983), with permission.

basibranchial in some taxa (e.g., Dicamptodon and Amphiuma, Fig. 3.4). The basibranchial and ceratobranchials are fused to form a branchial plate in some taxa (e.g., plethodontids, see Gyrinophilus, Fig. 3.4). The shapes of the hyobranchial elements show variation among taxa (Fig. 3.4), but with some underlying common themes. The basibranchial is usually elongate and circular or triangular in cross section. The ceratohyals are flat and broad, and the ceratobranchials are often cylindrical. The epibranchials are triangular in cross section and taper to points or terminate with knobs at the posterior tips, which are attached by muscles to the skull and dorsolateral neck region. The ceratohyals and first epibranchials are usually the largest elements of the larval hyobranchial apparatus; more posterior elements are progressively smaller. Articulations between elements are generally loose.

and elements are held together by shared membranes rather than by ligaments. The ceratohyals, however, are linked at their midpoints to the mandibles by the hyomandibular ligaments or at their caudal ends to the prearticulars or quadrates by hyoquadrate ligaments. A single branched ligament may be present in some taxa (Elwood and Cundall, 1994) or at some stages of development (Reilly and Altig, 1996). The elements of the hyobranchial apparatus are mostly cartilaginous, although ossification or mineralization occurs in some elements and is usually more extensive in older larvae. The basibranchial and ceratohyals are entirely cartilaginous, whereas the urohyal is usually the first element to ossify. The second and third ceratobranchials may be ossified or calcified in cryptobranchoids, and the epibranchials are ossified in some taxa (e.g., dicamptodontids and plethodontids). Adults

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of perennibranchiate species may show the metamorphic (i.e., adult) pattern of ossification, but a larval number and configuration of hyobranchial elements (e.g., Proteus and Fseudohranchus, Fig. 3.4). 2. Larval Head

Musculature

The muscles of the head can be divided into four broad functional groups: jaw muscles, hyobranchial muscles, skull muscles, and throat muscles. The general pattern of larval muscle morphology is presented in this section. Some taxa may not possess all of the muscles listed. Current names of muscles are used; some synonyms are listed in parentheses and are not mentioned thereafter (for more thorough lists of homo-

logues and synonyms, see Edgeworth, 1935; Francis, 1934). Only muscles likely to function in feeding are presented, and discussion of their functions is restricted to their expected actions when they contract. A later section on feeding function discusses in more detail the roles of various muscles in producing coordinated feeding movements. Mouth opening and closing are performed by antagonistic sets of muscles: the depressors, which open the mouth, and the levators, which close the mouth (Fig. 3.5A). The mouth-opening muscle is the depressor mandibulae (DM), which is sometimes divided into two parts: depressor mandibulae anterior (DMA) and posterior (DMP) (see Table 3.1 for abbreviations). DM muscles originate on the skull in the vicinity of the

F I G U R E 3.5. Larval (A) and adult (B) cranial muscles of the salamandrid Taricha granulosa in ventral and lateral views. In ventral views, deep muscles are depicted on the left side and more superficial muscles are shown on the right side. See Table 3.1 for abbreviations and the text for descriptions of muscles.

3. Aquatic Feeding in Salamanders TABLE 3.1 Abbreviations, Homologs and Synonyms of Skeletal Elements and Muscles Homologs and Synonyms" Skeletal elements A Angular BB Basibranchial BP Branchial plate BH C CB CH CO D EB

Basihyal Comua Ceratobranchial Ceratohyal Coronoid Dentary Epibranchial

HH L M OG PA R UH

Hypohyal Lingual Meckel's cartilage Otoglossal Prearticular Radial Urohyal

Muscles AA

Adductores arcuum

BH

Branchiohyoideus

CDSP

Cephalodorsosubpharyngeus

BM

Branchiomandibularis

DM DMA DMP DT G GG GGL GH GHL GHM HOYP IMA IMP IH IHP

Depressor mandibulae Depressor mandibulae anterior Depressor mandibulae posterior Dorsalis trunci Gularis Genioglossus Genioglossus lateralis Geniohyoideus Geniohyoideus lateralis Geniohyoideus medialis Hebosteoypsiloideus Intermandibularis anterior Intermandibularis posterior Interhyoideus Interhyoideus posterior

lOQ ITCS

Interossaquadrata Intertransversarius capitis superior Intervertebral epaxial Levatores arcuum branchiarum Levator mandibulae externus Levator mandibulae internus Levator mandibulae internus anterior Levator mandibulae internus posterior Lateral subvertebralis Medial subvertebralis Quadratopectoralis Rectus cervicis Rectus cervicis profundus Rectus cervicis superficialis Subarcualis rectus Subhyoideus Transversus ventralis

IVE LAB LME LMI LMIA LMIP LSV MSV QP RC RCP RCS SAR SH TV

^Synonyms are in parentheses.

(Copula) Splits into BB and CBs on metamorphosis (Hypobranchial) (Splenial) (Ceratobranchial); fused larval CB and EB in some taxa

(Gonial) R 1 formed from larval H H (Second Basibranchial, Os thyroideum) (Subarcualis obliquus, Transversus ventralis 1) (Ceratohyoideus, Ceratohyoideus externus) Formed from fusion of larval LAB and TV (Ceratomandibularis, Hyomandibularis)

Formed from larval IHP Formed from larval GG (Coracomandibularis) Formed from larval G H Formed from larval G H Formed from larval RC (Submentalis) (Sphincter colli, Interbranchialis) Formed from larval IH

Formed from larval IHP (Abdominohyoideus) (Sternohyoideus) Formed from larval IH

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squamosal and quadrate (the DMP originates on the ceratohyal in Siren) and insert on the ventrocaudal surface of the articular or prearticular just beneath the jaw joint. The branchiomandibularis (BM, also called ceratomandibularis or hyomandibularis) originates on the distal tip of the first epibranchial and either merges with the DMP to insert on the prearticular or inserts on the hyomandibular ligament. In addition to depressing the lower jaw, the BM is in a position to aid in hyobranchial depression by drawing the epibranchial tips dorsorostrally. All exert dorsal and caudal components of force on the caudal side of the jaw joint. Contraction of these muscles swings the lower jaw downward by rotating it about its articulation with the quadrate. In addition to those jaw depressors which span the jaw joint, elongate ventral muscles may contribute to mouth opening by pulling the tip of the lower jaw posteroventrally. These include the geniohyoideus [GH, also called the coracomandibularis (Lauder and Shaffer, 1985)] and the rectus cervicis superficialis and profundus (RCS and RCP). The GH originates on the mandibular symphysis and inserts on the urohyal. The RCS (also called the sternohyoideus) originates from the sternum and the RCS originates on the rectus abdominus muscles, which in turn originate on the pelvis. The RCP (also called the abdominohyoideus) and RCS may be indistinct from one another at their rostral ends, where they insert on the basibranchial, first ceratobranchials, or the branchial plate. These muscles can affect mouth opening if the GH contracts simultaneously and the skull is prevented from flexing ventrally. The connection between mandibles and ceratohyals by the hyomandibular ligament may also affect mouth opening as the hyobranchial apparatus is depressed (Reilly and Lauder, 1990). Mouth-closing muscles include the levator (or adductor) mandibulae, which is divided into two main parts: the levator mandibulae externus (LME) and the levator mandibular internus (LMI). The internus is sometimes further divided into the internus anterior (LMIA) and internus posterior (LMIP). The LMIA and LME originate on the skull and the LMIP originates on the atlas. All insert primarily on the prearticular, but also on the dentary of the lower jaw. These muscles are positioned to produce primarily dorsal, but also medial components of force on the rostral side of the jaw joint, and swing the lower jaw upward or apply biting force. Suction feeding requires movements of the hyobranchial apparatus in addition to movements of the jaws. Muscles of the hyobranchial apparatus are divided here into (1) hyobranchial depressors and levators, which produce primarily dorsoventral and rostrocaudal movements, (2) branchial adductors and abductors, which produce lateral movements, and

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(3) hyobranchial stabilizers, which anchor or adjust the branchial tips. Hyobranchial depressors swing the hyobranchial apparatus ventrally and caudally and are responsible for enlarging the buccal cavity during suction feeding. The RCS and RCP exert a caudal force on the center of the hyobranchial apparatus. The branchiohyoideus (BH, also called ceratohyoideus or ceratohyoideus externus) originates on the ventral surface of the ceratohyal, inserts on the tip of the first epibranchial, and may share fibers with the adjacent BM (Fig. 3.5A). The BH pulls the epibranchial tip closer to the rostral end of the ceratohyal, buckling the hyobranchial apparatus ventrad and pulling the epibranchial tip ventrad. As mentioned previously, the BM may similarly aid in hyobranchial depression. Hyobranchial levators either cradle the hyobranchial apparatus or attach directly to it and function to compress the buccal cavity and return the hyobranchial apparatus to its resting position. The geniohyoideus (GH) originates on the urohyal, inserts at the mandibular symphysis, and pulls the center of the hyobranchial apparatus rostrad. As mentioned earlier, because of its attachment to the mandibular symphysis, this muscle may also act as a mouth opener if the hyobranchial apparatus is stabilized in its depressed position. The intermandibularis posterior (IMP) originates on the medial aponeurosis of the floor of the mouth and runs laterally to insert on the dentary and prearticular. A small intermandibularis anterior (IMA, also called submentalis) is usually present, spanning the mandibular symphysis. The interhyoideus (IH) originates with the IMP on the medial aponeurosis but runs caudally as well as laterally to insert on the caudal tip of the ceratohyal or on the hyoquadrate ligament. An interhyoideus posterior (IHP, also called the interbranchialis or sphincter colli) is often distinct from the IH, lies just caudal to the IH, and runs from the distal tip of the first epibranchial medially to insert on the medial aponeurosis of the throat. The IMP, IH, and IHP all raise the floor of the mouth, cradling and pushing the hyobranchial apparatus upward to its resting position. The IHP may also function in branchial adduction. Branchial abductors move the epibranchials apart, opening the gill slits. The BH is in a position to abduct the first epibranchial laterally in some species (e.g., Ambystoma tigriunum), whereas in others (e.g., plethodontids) it appears to move the epibranchial medially. The tranversus ventralis (TV) muscles, which vary in number among taxa, originate at the midline on the ventral surface of the pharynx and insert on or near the medial edge of the most medial epibranchial. The TV

muscles are in a position to move the last epibranchial medially. Branchial adductors move the epibranchial tips toward one another. The BH may serve this function in some taxa. The subarcularis rectus 1 (SAR 1), which originates on the ventral surface of the ceratohyal and inserts on the first epibranchial, can adduct the epibranchial medially. Subarcualis rectus muscles 2 through 4 span the epibranchials and can move them toward one another. The single or double adductores arcuum (AA, also called the subarcualis obliquus or transversus ventralis 1) runs from the ceratobranchial or branchial plate to the second and third epibranchials and can adduct the epibranchials medially. This may close or open the gill slits, depending on the relative position of the first epibranchial, or may swing the basibranchial relative to the epibranchial to return the hyobranchial apparatus to its resting position. Hyobranchial stabilizers include the levatores arcuum branchiarum (LAB), which originate broadly on the dorsalis trunci muscles (DT) of the neck or on the otic region of the skull and insert on the epibranchial tips (Fig. 3.5A). They are in a position to move the epibranchial tips dorsally or rostrally or to anchor them and prevent caudal excursion. The head is moved dorsally, ventrally, or laterally to direct the gape during suction feeding and to aid in prey manipulation and swallowing. Four sets of muscles can produce these movements. The dorsalis trunci (DT) originates on the vertebrae and inserts on the occipito-otic of the skull and can flex the head dorsolaterally. The intervertebral epaxial muscle (IVE), sometimes not distinct from the DT, can also raise the cranium. The intertransversarius capitis superior (ITCS) originates on the atlas, inserts on the occipitootic, and can deflect the cranium dorsolaterally. The levator scapulae and cucuUaris muscles originate on the pectoral girdle and insert on the skull and can flex the head laterally. The skull can be flexed ventrolaterally by the medial subvertebralis muscle (MSV), which originates on the ribs of the first few vertebrae and inserts on the parasphenoid. The lateral subvertebralis (LSV) originates from the lateral body wall musculature, inserts in the otic region, and can flex the skull laterally. The IMP, IH, and IHP can raise the floor of the mouth and constrict the pharynx and may function in prey manipulation or swallowing. In addition to branchial adduction, the TV can constrict the pharynx and aid in swallowing. The skull levators (DT, IVE, ITCS) and depressors (MSV, LSV), as well as the levator scapulae and cucullaris muscles, can aid in swallowing by moving the head.

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3. Aquatic Feeding in Salamanders B. Adult Morphology Adult aquatic salamanders represent the full range of metamorphic patterns, from completely larviform, perennibranchiate species, such as the axolotl, to completely metamorphosed forms, such as most newts. We divide this spectrum of developmental patterns into three groups, based on the overall degree of metamorphosis of the feeding system. (1) "Perennibranchiates" possess all or most larval features, including gill slits, external gills, posterior branchial elements, and interlocking labial lobes. They possess few adult features, such as maxillae and a tongue pad. This group includes all of the Sirenidae and Proteidae and some members of other families. (2) "Partial metamorphs'' possess a mixture of larval and adult features. They may lose external gills and gill slits, but may retain labial lobes and posterior branchial elements. They possess maxillae and a rudimentary tongue pad. This group includes all members of the Cryptobranchidae and Amphiumidae, as well as ambystomatids formerly placed in the genus Rhyacosiredon. (3) "Metamorphs'' have lost external gills, gill slits, posterior branchial elements, interlocking labial lobes, and have fully formed maxillae and tongue pads with intrinsic tongue muscles. This group includes the newts and all terrestrial and semiaquatic salamanders. The adult morphology of metamorphs and partial metamorphs is the focus of this section. Perennibranchiate adults are considered here as well, but are emphasized in the previous section on larval morphology. Unlike the heads of larval and perennibranchiate salamanders, which have pointed or tapered rostra, the heads of metamorphosed and partially metamorphosed salamanders are more rounded and blunt. The external gills and tail fin are lost, the eyes protrude, and eyelids form. In addition to these superficial changes, which occur at metamorphosis, deeper alterations are made in most components of the feeding system, including the teeth, tongue, jaws, skull, hyobranchial apparatus, and many muscles of the head. The teeth of metamorphosed salamanders consist of a bony pedicel attached by fibrous connective tissue to an enamel-coated crown. Teeth of metamorphosed animals are either monocuspid or dicuspid, with various crown shapes, including clubs, discs, and spikes. Older perennibranchiate and metamorphosing animals possess biscupid, subpedicellate teeth. The dentition is generally monostichous and homodont (Beneski and Larsen, 1989a,b). Partially metamorphosing species may possess bicuspid teeth (Erdman and Cundall, 1984; Elwood and Cundall, 1994). Perennibranchiate forms generally lack a tongue

pad, whereas partially metamorphosing forms possess a raised glandular field in the floor of the mouth. Metamorphosing species have tongues of various sizes and degrees of complexity. Suction feeding forms tend to have smaller, simpler tongues, whereas those that use tongue prehension in water have larger, more complex tongues such as those of terrestrial species. Adult tongue morphologies of those species that use tongue prehension will be presented in the next chapter. The labial lobes of adult salamanders are of two types: those that are essentially retained larval features and those that form after metamorphosis. Labial lobes of the larval type are found in all larval and perennibranchiate salamanders and in many partially metamorphosing forms. Sirenids have by far the most extensive labial lobes of this type; the lateral gape is entirely occluded and the mouth forms a small, rectangular anterior opening. Cryptobranchus is unusual in that it retains larval labial lobes on the lower jaws, but not on the upper jaws. The fully aquatic, suction feeding ambystomatids formerly placed in the genus Rhyacosiredon (now placed in Ambystoma) retain larval labial lobes and otherwise appear to be partially metamorphosed (Reilly and Brandon, 1994). The labial lobes of aquatic adult salamandrids and hynobiids are of the second type and only form on the upper jaw. These adult labial lobes are simple flaps and are not homologous to the more complex, interlocking larval lobes. All perennibranchiate and many partially metamorphosing forms possess gill apertures. Cryptobranchus and Amphiuma possess one gill aperture, or spiracle on each side of the head. Andrias has no gill openings. Perennibranchiate forms may possess a gular slit, whereas some partially or completely metamorphosing forms possess a fold in this location. Cryptobranchoids and the fully aquatic salamandrid, Pachytriton, are unusual in having longitudinal folds in the buccal floor that accommodate ventral expansion. Cryptobranchids also retain the larval anterior fold beneath the hyoid and are capable of perhaps the greatest increases in buccal volume of any salamander. 1. Adult Skull, Jaws, and Hyobranchial

Apparatus

Metamorphosis from the larval to adult form involves changes in the skull, jaws, and hyobranchial apparatus. These changes are presented here in order to introduce the adult form of these skeletal systems. Elements that do not change substantially during metamorphosis are not mentioned in this section. During metamorphosis, elements of the skull are lost, appear, or are remodeled, and further ossification

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Stephen M. Deban and David B. Wake

and expansion occur. In addition to the bones present in the larva, some of which enlarge and overlap, prefrontals, lacrimals, nasals, and septomaxillae may develop in the rostrum of the skull, paralleling the developmental appearance of rostral elements in the hyobranchial apparatus. Some taxa, particularly hynobiids, already possess many of these elements as larvae (Fig. 3.3). During metamorphosis, the jaws are strengthened. The maxilla appears or broadens its attachments to the skull. The vomer and premaxilla enlarge and reinforce their connections with the skull, and the orientation of vomerine tooth rows changes with the change in shape of the vomer. Dentate extensions of the vomer migrate posteriorly onto the parasphenoid, and the toothbearing, palatine portion of the palatopterygoid is lost. The dentaries become more heavily ossified and abut at the symphysis, and the coronoid is lost (except in Dicamptodon in which only the teeth are lost). Meckel's cartilage is reduced and the dentary and prearticular may fuse to one another. The jaw articulation is repositioned posteriorly so that it comes to lie behind the orbit as the squamosal and quadrate swing posteriorly, increasing the gape. The hyobranchial apparatus of perennibranchiate species is essentially larval in configuration. In some taxa, such as Proteus, extensive ossification occurs, but all larval elements are retained (Marche and Durand, 1983). In metamorphosing taxa, the transformation from the larval to the adult hyobranchial configuration involves loss, remodeling, and often ossification of elements. The posterior branchial arches are lost, typically leaving two pairs of ceratobranchials and one or two pairs of epibranchials in the adult. Some terrestrial members of the Salamandridae lack discrete first ceratobranchials as adults, and the epibranchials appear elongated. These adult elements are probably the product of fusion of the larval first ceratobranchials and first epibranchials and are called the epibranchials. The epibranchial and ceratobranchial persist as a separate element in all aquatic members of the Salamandridae. In the Plethodontidae the larval epibranchials disintegrate completely and a new adult epibranchial develops at metamorphosis from undifferentiated tissue (Alberch and Gale, 1986). In the Hynobiidae, two pairs of epibranchials persist, the first cartilaginous and the second bony. The Cryptobranchidae show variation in the degree of metamorphosis of the hyobranchial system. Cryptobranchus has a larval number of posterior elements, but with more ossification and mineralization than in the larva, whereas Andrias loses the more posterior epibranchials (Cox and Tanner, 1989). The ceratohyal becomes thinner and more blade-like anteriorly and narrowed and elongate posteriorly dur-

ing metamorphosis. Ligamentous and connective tissue attachments to surrounding skeletal elements are variable. A hyoquadrate ligament or hyomandibular ligament persists or develops in adults of some taxa, such as plethodontids. This ligament may be replaced in some of the Salamandridae (e.g., Taricha) by a hyosuspensory ligament between the upper quadrate and the posterior tip of the ceratohyal (Findeis and Bemis, 1990). The hypohyals, when present in the larva, may vanish entirely or give rise to adult elements, such as the radial cartilages found in the Ambystomatidae, Rhyacotritonidae, Dicamptodontidae, and Hynobiidae. The ceratohyal loses its connection to the basibranchial, except in hynobiids, ambystomatids, and dicamptodontids. In these taxa, the ceratohyals and basibranchial are connected by narrow radial cartilages (see Batrachuperus, Fig. 3.6). In some hynobiids, these cartilages form elongate loops, which cross in a figure-eight fashion over the midline and connect the two ceratohyals (Cox and Tanner, 1989; Larsen et al., 1996). The developmental appearance of new elements at the rostral end of the hyobranchial apparatus is common among salamanders, and these new elements may articulate with the basibranchial, for example, the second radii, otoglossal cartilage, or lingual plate of the Ambystomatidae and Dicamptodontidae (Krogh and Tanner, 1972) and Salamandridae (Ozeti and Wake, 1969), or may lie adjacent to it, like the basihyals and hypohyals of the Amphiumidae and Cryptobranchidae. In some taxa, anterior projections of the basibranchial, called cornua, form and support the adult tongue pad (Fig. 3.6). In some plethodontids a separate lingual cartilage forms at the tip of the basibranchial and functions in rotation of the tongue pad (Lombard and Wake, 1977). The articulations between the basibranchial and ceratobranchials are altered at metamorphosis. The branchial plate of the larvae of some taxa gives rise to separate basibranchial and ceratobranchials. The urohyal loses its attachment to the basibranchial and may disappear altogether, as in many salamandrids. Complete metamorphosis of the hyobranchial apparatus makes tongue protrusion possible. The ceratohyals are freed somewhat from the remaining elements, allowing folding and forward movements of the rest of the apparatus to which the tongue pad is attached. The ossification pattern of the hyobranchial apparatus varies taxonomically (Fig. 3.6). Only the urohyal, when present, is universally ossified. Aquatic plethodontids, which do not suction feed, such as Desmognathus marmoratus, possess slender cartilaginous hyobranchia; only portions of the basibranchial are ossified. In other taxa, the basibranchial, epibranchial tips.

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3. A q u a t i c F e e d i n g in S a l a m a n d e r s

Batrachuperus mustersi

Rhyacosiredon rivularis

Cryptobranchus

alleganiensis

Pachytriton sp.

Leurognathus marmoratus

Pleurodeles waltl

FIGURE 3.6. Hyobranchia (in ventral view) of adults of metamorphosing and partially metamorphosing salamanders from five families. Bone or mineralization is shaded and cartilage is unshaded. Some elements are cut away to reveal underlying elements or the outlines of underlying elements are shown as dashed lines. Scale bars equal 1 cm. See Table 3.1 for abbreviations. Cryptobranchus drawing is adapted from Elwood and Cundall (1994). /. Morph. 220, 47-70. Copyright © 1994. Reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.

and posterior portion of the ceratohyal are frequently ossified. Almost the entire apparatus may ossify in suction-feeding members of the Salamandridae, such as Pachytriton, with only the rostral portion of the ceratohyal remaining cartilaginous (Ozeti and Wake, 1969). Rhyacosiredon has a more robust hyobranchial apparatus than other ambystomatids and shows extensive ossification of the epibranchials and ceratohyal, as well as ossification of the first ceratobranchial. Cryptobranchoids show an unusual, but consistent pattern of ossification of the second ceratobranchial and epibranchial, which may be indicative of an unusual method of force transmission during feeding (see Section III,D).

In partially metamorphosing taxa, such as cryptobranchids and amphiumids, the hyobranchial apparatus of the adult retains some larval features. Hypohyals, as well as basihyals, are present in the adult. Articulations between hyobranchial elements are strengthened during development. The anterior hyobranchial elements of cryptobranchids remain cartilaginous, even in large animals, and are extremely broad, filling the space between the mandibles (Cox and Tanner, 1989; Elwood and Cundall, 1994). The hypohyals of Rhyacosiredon have a morphology intermediate between the larval configuration and that of the adults of fully metamorphosing ambystomatids (Reilly and Brandon, 1994).

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Posterior epibranchials persist in amphiumids, as well as in Cryptobranchus in which the third epibranchial calcifies. The first epibranchial and ceratobranchial fuse to one another to form a single element, the epibranchial, in amphiumids, cryptobranchids, and some hynobiids (Fig. 3.6). In amphiumids, the second ceratobranchial is absent, even in larvae. In sirenids and proteids, the anterior ceratohyal, the basibranchial, and ceratobranchials ossify. In sirenids the basibranchial is particularly unusual: the anterior tip is bulbous where it meets the ceratohyals (Cope, 1889). In proteids the epibranchials also ossify (Fig. 3.4). Some taxa show divergent skull and jaw morphologies. Sirenids, amphiumids, and Proteus have elongate, tapered heads and jaws, whereas cryptobranchids have broad, rounded heads and jaws. Amphiumids have enlarged jaws, teeth, and jaw musculature and are capable of a powerful bite; they can bite violently when handled. Members of the Salamandridae have particularly robust skulls; many possess a bony arch joining the frontal and squamosal and some have the maxilla and pterygoid abutting. Cryptobranchoids possess an ossified angular element in the lower jaw (Noble, 1931), and the mandibular symphysis forms a joint consisting of cartilaginous pads and collagen ligaments, allowing the mandibles to flex considerably ventrally and dorsally with respect to one another (Cundall et al, 1987; Elwood and Cundall, 1994). This unilateral jaw depression is possible only because the mandibles are unusually strongly curved. Their curvature allows them to swing independently of one another, producing an anterolateral gape when one side is depressed relative to the other. Desmognathine plethodontids have specializations associated with a strong bite, including stalked occipital condyles, modified anterior vertebrae, and robust skulls (see Schwenk and Wake, 1993, and references therein). 2. Adult Head

Musculature

Muscles change in size, orientation, and function during metamorphosis and may be lost, form, or give rise to new muscles. In general, more muscles are lost than appear, mostly those associated with gill and epibranchial movements, including the SAR muscles (except SAR 1), AA, and LAB (Fig. 3.5B). Those feeding muscles that typically change during metamorphosis are emphasized here. The BM is lost or shifts its posterior attachment from the epibranchial tip to merge with the DMP and fan out posteriorly onto the fascia cephalodorsalis, thereby losing its role in hyobranchial depression. The new combined muscle is called the DMR In some taxa the DMA and DMP become indistinguishable at meta-

morphosis and are known as the DM thereafter. In desmognathine plethodontids, the tendon associated with the LMIP is enlarged at metamorphosis, forming the distinctive atlanto-mandibular ligament (Schwenk and Wake, 1993). The BH is lost at metamorphosis in metamorphosing and partially metamorphosing taxa. The SAR 1 enlarges, often forming a muscular bulb around the first epibranchial (or ceratobranchial in those species that lack a separate epibranchial), and shifts its function to tongue protrusion. In partially metamorphosing forms (i.e., cryptobranchids and amphiumids) and in many newts, the SAR 1 replaces the BH in position and function (Fig. 3.5B). The remaining SAR muscles are lost. In plethodontids, a geniohyoideus lateralis (GHL) arises from the GH, which then becomes known as the geniohyoideus medialis (GHM). The GHL originates on the mandible lateral to the symphysis and inserts on the lateral edge of the ceratohyal. The GHM retains its larval origin and insertion, but the urohyal separates from the basibranchial before metamorphosis is complete. The posterior attachment of the GH shifts to the RCS in those taxa lacking a urohyal. The GHM loses its function in drawing the hyobranchial apparatus anteriorly and becomes a buccal stabilizer in plethodontids. In other taxa, the GH similarly loses its attachment to the basibranchial and acts as a sling that can stabilize or raise the hyobranchial apparatus. The rectus cervicis (RC) muscles become more distinct as profundus (RCP) and superficialis (RCS). A superficialis lateralis (RCSL) slip may form in plethodontids. The entire group of RC muscles functions in tongue retraction or hyobranchial depression. A hebosteoypsiloideus (HOYP) muscle, the function of which is unknown, becomes distinct from the RC group at metamorphosis in plethodontids, originating on the urohyal (or basibranchial) and inserting on the RCP near the sternum (Lombard and Wake, 1977). Among the dorsal muscles of the head and neck, only the IVE changes significantly at metamorphosis, becoming distinct from the DT. This new muscle functions in cranial elevation. The metamorphic fate of the superficial throat muscles varies among taxa and has been the source of much nomenclatural confusion. In plethodontids, the IHP of the larva gives rise to both the quadratopectoralis (QP) and the gularis (G) of the adult. The G is the only remnant of the IHP to persist in most adult plethodontids. The desmognathines and Aneides possess both; the QP becomes a strong head depressor, shifting its dorsal attachment from the epibranchial to the quadrate, and shifting its caudal attachment to the pectoral fascia. The G in these taxa is a small strap muscle that lies against the QP. In adults of all other

3. Aquatic Feeding in Salamanders salamander taxa (i.e., nonplethodontids), the IHP retains its general larval position or shifts its origin to the fascia cephalodorsalis, but is still called the IHP (Piatt, 1940). In the Salamandridae and Hynobiidae, the IH of the larva splits to give rise to the anterior subhyoideus (SH) and the posterior interossaquadrata (lOQ). The SH originates from the posterior end of the ceratohyal and inserts anteriorly on the dorsal fascia of the IMP or on the mandible near the symphysis, and upon contraction draws the ceratohyal rostrally (Fig. 3.5B). The lOQ may shift its insertion from the ceratohyal to the quadrate. In adults of all other families, the Iti retains its larval position (Krogh and Tanner, 1972) and name. The cephalodorsosubpharyngeus (CDSP) forms from the fusion of the posterior larval TV and LAB muscles and is in a position to constrict the pharynx and aid in swallowing. A genioglossus (GG) forms or is elaborated during metamorphosis, originating on the mandibular symphysis and fanning out into the tongue pad. The GG draws the tongue pad toward the mandibular symphysis. In Cryptobranchus, this muscle inserts on the hyopohyals and acts as a hyobranchial levator (Elwood and Cundall, 1994). In ambystomatids, the GG gives rise to the genioglossus lateralis (GGL), which inserts on or in the vicinity of the lateral edge of the ceratohyal (such as the GHL in plethodontids) (Larsen and Guthrie, 1975). Rhyacotritonids may possess both SH and GGL (Krogh and Tanner, 1972). These muscles and the intrinsic tongue muscles, which also form at metamorphosis, function primarily in tongue prehension and will therefore be discussed in the next chapter. Feeding muscles are divided into two series, branchiomeric and hypobranchial, based on developmental origin and innervation. The branchiomeric (branchial) series includes the majority of the feeding muscles, is innervated by visceral motor components of the nervous system, and forms from the embryonic myomeres. Branchiomeric feeding muscles include IM, IMP, IH, SH, IHP, LM, DM, BH, LAB, and SAR. The hypobranchial series forms from rostral growths of myotomes behind the branchial area, is innervated by somatic motor components of the nervous system (i.e., the hypoglossal nerve), and includes the GH, GHL, GG, GGL, RCP, and RCS and the intrinsic muscles of the tongue pad. C. Sensory and Motor Systems Larval and adult salamanders foraging in water are presented with the same array of sensory stimuli and generally use the same set of sensory modalities to detect and localize prey, but differ in the degree to which

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they use a particular modality. Larvae and perennibranchiate forms typically rely on mechanical, electrical, and olfactory senses, but can use vision as well (Luthardt-Laimer, 1983; Besharse and Brandon, 1974). Adults of metamorphosing forms rely to a lesser degree on olfactory and lateral line stimuli; they use primarily vision and have well-developed eyes. The eyes of salamanders have all the components of typical vertebrate eyes, including a cornea, lens, iris and pupil, and multilayered retina of cells and fibers. The retina includes photoreceptors (rods and cones), horizontal cells, bipolar cells, amacrine cells, and ganglion cells. The cornea is flat and the lens is spherical, suited for an aquatic environment in which only the lens and not the cornea is responsible for focusing the image (Roth, 1987). Salamanders are capable of color vision, and larvae and aquatic adults are more sensitive to longer wavelengths of light (which predominate in water) than terrestrial adults (Himstedt, 1973a,b). Focusing on near objects such as prey is accomplished by contraction of the protractor lentis muscle, which moves the lens away from the retina. The eyes are reduced and covered with skin in many cave-dwelling salamanders, many of which are perennibranchiate. These species show a decrease in overall eye size and a degeneration of the retina and optical structures. Eyelids are lacking in larval and perennibranchiate salamanders, cryptobranchids and amphiumids; they are reduced in some fully aquatic salamandrids and hynobiids, and Rhyacosiredon, and are present in fully metamorphosed salamanders. The optic nerve, which consists of the axons of the retinal ganglion cells, crosses the optic nerve of the contralateral eye at the optic chiasm and enters the diencephalon from below. Fibers terminate in, or project to, various parts of the diencephalon (e.g., thalamus and pretectum), the optic tectum in the dorsal portion of the mesencephalon, and the tegmentum in the ventral portion. Most fibers of the optic nerve travel to the contralateral side of the thalamus, pretectum, and tectum; however, some ipsilateral projections exist (Fig. 3.7). The proportion of ipsilateral projections varies among taxa and developmental stages. Proportionally more ipsilateral projections are present after metamorphosis in those taxa with larvae. Ipsilateral projections are most abundant in completely terrestrial forms, especially those with greatly overlapping visual fields and binocular vision, such as bolitoglossine plethodontids (Roth, 1987). Information from the optic tectum is relayed through three descending tecto-bulbar tracts to the brain stem where motor nuclei controlling feeding muscles reside (Dicke and Roth, 1994). Salamanders possess two olfactory systems: the

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Olfactory Bulb Vomeronasal

I I Muscles I I Skeletal elements Lateral line system Olfactory system Vomeronasal system Visual system Motor nerves Brain tracts XI Motor nuclei

Lateral Line System

F I G U R E 3.7. Sensory-motor schematic of the feeding system of a generalized salamander, showing both larval and adult features. Sensory information entering the eyes, nostrils, and lateral line organs is integrated in the telencephalon, diencephalon, and mesencephalon. These centers activate motor nuclei (numbered ovals) in the brain stem, which control the contraction of muscles (striped gray) through cranial nerves (black lines) and consequently produce feeding movements of the jaws and hyobranchial apparatus (solid light gray). Nerves and brain tracts are solid black lines or gray channels and muscle innervations are shown as black dots, and sense organs and parts of the brain are shown in white or dark gray. Motor nuclei are numbered according to the cranial nerves they supply See Table 3.1 for muscle abbreviations.

3. Aquatic Feeding in Salamanders primary olfactory system and the vomeronasal organ or accessory olfactory system. The main olfactory system includes the nasal epithelium with chemosensory olfactory cells, each of which has many filaments exposed to the nasal chamber which are capable of responding to molecules in the environment. Axons of olfactory cells form the first cranial nerve, which projects to the olfactory bulbs of the forebrain (Fig. 3.7). The vomeronasal system opens into the nasal chamber and has receptors in a separate sac, lateral to those of the main olfactory system (Dawley, 1988), and has a separate accessory bulb in the brain (Eisthen ei a\., 1994). Plethodontids possess the additional feature of nasolabial grooves, which form at metamorphosis and which conduct substrate-borne molecules to the vomeronasal sac. This vomeronasal system is important in courtship behavior and may be used in prey tracking. Taste buds on the tongue and pharynx are used to reject distastful or noxious prey. The glossopharyngeal nerve (cranial nerve IX) conducts impulses from the taste buds to the brain. Additional taste buds are present on the skin and may be used to locate prey. The lateral line system is present in all aquatic salamanders and is used to detect water currents and electrical charges. The lateral line system is closely associated with the auditory system and the two are collectively called the acousticolateralis system. Lateral line detectors form series of small depressions or raised "stitches" on the head and along the body, containing ampuUary organs, neuromasts, or pit organs. Ampullary organs are present on the head and function as electroreceptors, which can detect the tiny electrical fields generated by the muscle contractions of prey up to a few centimeters away (Bartels ei al., 1990). Neuromasts and pit organs extend down the head, body, and tail and are mechanoreceptive, containing sensory hair cells that are responsive to water movements and pressure changes. Larval salamanders possess all three types of receptors, as do some aquatic adult salamanders (Fritzsch and Wahnschaffe, 1983). Lateral line organs become covered with epidermis in salamanders that spend time out of water, such as Notophthaltnus and Siren, but become exposed to the skin surface and become functional again when the salamander returns to water (Dawson, 1936; Reno and Middleton, 1973). Axons of sensory cells of the lateral line system enter the brain through five separate nerves in the vicinity of the auditory nerve (VIII) and project to the acousticolateral area of the somatic sensory column of the medulla (Northcutt and Brandle, 1995). Lateral line information is relayed to the tectum of the midbrain, where it is processed and where the lateral line sensors

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are represented as a topographical map (Bartels et al., 1990). Salamanders use lateral line information to detect predators as well as to localize and orient to moving prey and to direct the predatory strike (Himstedt et al, 1982). Salamanders are capable of detecting prey using visual, olfactory, tactile, and lateral line receptors and are most responsive to live, active prey. Aquatic salamanders use olfactory and visual cues for initial orientation to prey and to direct the prey-capture strike (Martin et ah, 1974), but also use mechanoreception and electroreception (Joly, 1981; Himstedt,1967; Griffiths, 1993). Cave salamanders may have slender, elongate legs, which are used during foraging to lift the body above the substrate and enhance mechanoreception by exposing more of the lateral line system to water movements (Peck, 1973). Blind urodeles, such as Proteus, are sensitive to olfactory stimuli and will respond readily to immobile, dead prey, whereas salamanders that use vision are less responsive to dead prey and olfactory cues and rely on prey movement (Durand et al., 1982; Uiblein et al., 1992). In light, vision dominates prey localization and inhibits olfactory detection; darkness (or blindness) appears to release this inhibition (Roth, 1987). Feeding movements are controlled by clusters of motor neurons or motor nuclei of the brain stem (Roth et al., 1990). Motor nuclei of the feeding muscles are arranged in two columns along each side of the brain stem from the medulla oblongata to the second spinal nerve (Fig. 3.7). The motor nuclei supply axons to the cranial and first and second spinal nerves, which innervate the feeding muscles (Piatt, 1938). The trigeminal (cranial nerve V) innervates the IMP and LM. The facial (VII) innervates the IH, SH, BH, and DM. The glossopharyngeal (IX) innervates the SAR 1. The vagus (X) innervates the AA, LAB, SAR 2-SAR 4, TV, CDSP, and the SAR 1 of adults of some taxa (e.g., plethodontids). The accessory (XI) serves the cucuUaris. The hypoglossus (XII, formed from first and second spinal nerves) innervates the GG, GGL, GHM, GHL, RCP, RCS, and muscles of the tongue pad. Salamanders must gather sensory information about their prey and produce the approprialte behavior to make a successful capture. Information Is perceived by the sense organs and is processed in the brain, which then activates motor nuclei in the brain stem, contracting muscles in the proper sequence to generate coordinated movements of the body, head, jaws, and throat. Most if not all of the sensory and motor components of the feeding system are known. Flowever, the specific nuclei and connections of the brain that are involved in integrating the various sensory inputs (olfaction.

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lateral line, vision) and in producing the appropriate activation of motor nuclei are as yet undetermined. Sensory-motor integration in amphibians in general remains a rich area of research. III. FUNCTION A. Ingestion Behavior and Kinematics The feeding behavior of salamanders has been divided into four stages: orientation, approach, fixation, and snapping (Roth, 1987). Orientation involves lifting the head from the substrate and directing it toward the prey item. Approach involves walking or swimming toward the prey item until it is within reach. Fixation is a period during which the salamander assesses the prey, usually while the prey is stationary. Snapping, or striking, is the ingestion behavior: suction feeding or tongue or jaw prehension, sometimes combined with a lunge. Snapping is typically triggered, or "released," by prey movement. Snapping usually occurs so rapidly that it is effectively invisible to the eye and has been difficult to describe or analyze until recent technological advances in high-speed cinematography and videography. The other stages occur at a speed that is observable to the unaided eye. The four stages are often discrete, but some may be absent or blend together. For example, if the prey is already within reach, the approach may be omitted, or if the prey is moving continuously the fixation period may be skipped. Salamanders may also perform an olfactory test, in which the snout is pressed downward onto or near the prey, after the fixation stage but before striking at stationary prey. 1. Suction Feeding Snapping in most aquatic salamanders involves generating intraoral suction to capture prey. During suction feeding, the mouth is opened while the buccal cavity is expanded. This expansion creates a drop in buccal pressure relative to ambient pressure, causing water and prey to flow into the mouth. The gill slits are closed and labial lobes restrict the mouth opening to the front. The head is raised during mouth opening. This allows for ventral excursion of the lower jaw and also serves to aim the gape at the prey. The buccal cavity continues expanding as the mouth is closed and the head is lowered, resulting in continuous water flow throughout the gape cycle. The gill slits open before mouth closure and before maximum buccal expansion. After the mouth closes, water is expelled slowly through the open gill slits by compression of the buccal

cavity. Salamanders that lack or have a reduced number of gill slits expel water slowly out of the mouth, which is held ajar. Gill rakers or teeth prevent the prey from escaping during water expulsion. Suction feeding requires special morphology to be successful, including a robust hyobranchial apparatus and associated musculature to generate rapid and forceful buccal expansion and labial lobes or other means of restricting water flow to the front of the mouth. The coordination of buccal expansion and mouth opening is also important for successful suction feeding, although some variation in these two behaviors exists. Variation in suction feeding behavior across taxa or developmental stages involves changes in the extent, timing, and duration of jaw and hyobranchial movements during the prey-capture strike. Comparative studies of feeding behavior make use of kinematic analysis of the movements of the jaws and throat during prey capture. These movements are confined primarily to the sagittal plane, so are best visualized in lateral view, and are typically rapid and must be captured by high-speed videography or cine. Gape cycle durations for some representative taxa are as follows: 17-30 msec in larval Desmognathus quadramaculatus (Deban, personal observation), 35-47 msec in larval Salamandra salamandra (Reilly, 1995), 40 to over 80 msec in adult Cryptobranchus (Elwood and Cundall, 1994) and Amphiuma tridactylum (Erdmann and Cundall, 1984), and 80-110 msec in larval Ambystoma mexicanum (Lauder and Shaffer, 1985). Quantification of the strike by kinematic analysis involves recording the positions of various anatomical points throughout the course of the behavior (i.e., on each frame of a video sequence). Displacements, distances, angles, and velocities can be calculated from these position data, as can the timing and duration of events. Quantification of behavior in this way facilitates comparisons across taxa or developmental stages. Such data can then be visualized by kinematic profiles, which depict distances or the positions of points through time (Fig. 3.8). Two measures typically made on suction feeding salamanders are gape distance, or the distance between the tips of the jaws, and hyobranchial depression distance, or the distance between the top of the neck and the ventralmost point on the throat. Gape distance and hyobranchial depression distance both increase and then decrease during the suction feeding behavior. The kinematic profile of gape distance (the gape profile) typically appears as a bellshaped curve (Fig. 3.8). The hyobranchial profile appears as a skewed curve, showing a rapid increase and a slower decrease. By plotting both kinematic profiles

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3. A q u a t i c F e e d i n g in S a l a m a n d e r s

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Time (ms) F I G U R E 3.8. Kinematic profiles of jaw, hyobranchial, and head movements through the course of a single suction-feeding event in a larval Desmognathus quadramaculatus (snout-vent length is 30 mm). Hyobranchial depression that continues into mouth closing is typical of suction feeding. The head angle increases as the head is raised during mouth opening, directing the gape at the prey, and later decreases as the head is tucked during and after mouth closing.

against the same time axis, the temporal relationship of the two movements can be seen. Figure 3.8 shows the typical pattern for suction feeding: mouth opening and closing occur much more rapidly than hyobranchial depression and elevation, and maximum gape is reached before maximum hyobranchial depression. Kinematic profiles of this type are used to examine how the relationship between the two movements might vary among taxa or with different prey types. In addition to gape and hyobranchial distance, other kinematic variables differ among suction feeding salamanders, including the angle between head and body (Fig. 3.8) and the distance of forward lunging. For example, Cryptobranchus shows especially large buccal expansion for its size, and both Cryptobranchus and Ampliiuma display pronounced head dipping on mouth closing (Reilly and Lauder, 1992). Cryptobranchids are unique in that they often display asymmetrical kinematics during capture and intraoral transport in which one side of the lower jaw or hyobranchial apparatus is abducted more rapidly or farther than the other side (Elwood and Cundall, 1994).

2. Tongue Prehension Tongue prehension is used to capture prey by all terrestrial salamanders and by several aquatic salamanders (e.g., some plethodontids and rhyacotritonids) (Schwenk and Wake, 1988; personal observation). The behavior involves forward movement of the hyobranchial apparatus which propels the tongue out of the mouth. The SAR and SH muscles protract the tongue, and the RCS and RCP muscles retract it. Several muscles of the tongue tip rotate and shape the tongue pad. The gape profile is usually not bell shaped as in suction feeding, but often has a plateau region of constant gape corresponding with tongue protrusion. Gape increases to its maximum not as the tongue is protruded, but rather as the tongue returns with the prey to the mouth, producing a three- or four-part gape profile. 3. Jaw Prehension Prey capture by jaw prehension is used in both aquatic and terrestrial feeding and involves movements of

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the jaws and Httle movement of the hyobranchial apparatus. A forward lunge of the body or lateral turn of the head is used to bring the jaws to the prey. The gape cycle produces a bell-shaped profile similar to suction feeding, but the hyobranchial apparatus shows extremely small excursions relative to those seen during suction feeding. B. Prey Processing After prey is captured, it must be prepared for swallowing. Salamanders usually swallow their prey whole, without chewing or reducing it, although there are some exceptions, such as cryptobranchids and amphiumids. Processing prey usually involves only positioning it in the oral cavity and lubricating it with mucus. Occasionally, prey that protrudes from the mouth after capture is pushed against the substrate to orient it or to move it into the mouth. The head is sometimes thrashed laterally to orient the prey, to reduce it, or to break it free from the substrate. Prey is sometimes moved into and out of the mouth across the teeth repeatedly by water flow to center it; this may have the effect of macerating the prey. The forelimbs are not used in prey manipulation. Like prey capture, intraoral transport of prey involves coordinated movements of the jaws and hyobranchial apparatus and can be accomplished by suction or tongue movements. Suction-based transport of prey within the mouth to the esophagus is achieved by movements similar to suction-feeding movements (Gillis and Lauder, 1994). Prey is moved toward the esophagus by currents of inflowing water and held with the teeth or pressed to the roof of the mouth until the next cycle of intraoral transport. This process is repeated until the prey is in a position to be swallowed. Lingual-based prey transport (hyolingual transport) is accomplished by rapid cyclical movements of the hyobranchial apparatus and tongue. The prey adheres to the tongue pad and is moved caudally and ventrally in the mouth. As the tongue is moved forward for the next cycle, the teeth and jaws prevent the prey from being pushed forward. This ratchet-like process slowly moves prey toward the esophagus. Movements of the cranium, for example, head tucking in desmognathine plethodontids (Schwenk and Wake, 1993), may assist in forcing prey toward the rear of the throat. The tongue is first moved forward in the mouth, pressed against the prey, and then retracted rapidly, producing a drop in the floor of the buccal cavity similar to that seen in suction feeding. This process is repeated until the prey is swallowed. Swallowing involves forcing prey down the esophagus by contraction of the pharyngeal musculature, re-

traction of the eyeballs, and movements of the head. The tongue may be used as well in salamanders that possess it. Swallowing is similar in both terrestrial and aquatic salamanders, involving contraction of the transverse throat musculature (IM, IH, G, QP, CDSP, TV) and retractor bulbi, which squeeze prey down the esophagus. The dilator and constrictor laryngis muscles open and close the larynx and glottis except in plethodontids, which lack these muscles. Peristaltic contractions of the smooth muscles of the esophagus then move prey to the stomach. C. Functional Morphology Prey capture, intraoral transport, and processing are accomplished by movements of the jaws and hyobranchial apparatus. The type of hyobranchial movements and relative timing of jaw and hyobranchial movements differ among the various feeding behaviors (suction feeding, tongue prehension, and jaw prehension). The hyobranchial apparatus is thrust forward (tongue prehension), swung backward (suction feeding), or held relatively stationary (jaw prehension) by different patterns of muscle activity. The muscles involved in each of these behaviors, as well as their hypothesized roles in producing feeding movements, are discussed in this section. Feeding movements are discussed as though they are symmetrical, although some taxa, such as cryptobranchids, are known to move asymmetrically (e.g., Cundall et ah, 1987). Again, suction feeding is emphasized over tongue and jaw prehension; the latter behaviors are covered in the next chapter. The buccal expansion of suction feeding is produced by the hyobranchial apparatus and its associated musculature (Fig. 3.5). The hyobranchial apparatus at rest is folded and lies in the floor of the mouth and the throat and rather close to the palate. During buccal expansion, it is swung ventrally and caudally about its attachments to the lower jaw, skull, and neck. The attachments of the ceratohyal to the jaw joint and of the epibranchials to the neck and skull form the dorsal points of rotation for this hyobranchial depression. The basibranchial retains its horizontal orientation, but is translated downward and backward. In addition to rotation around joints, elasticity of the cartilaginous elements has been proposed to play a role in some movements of the hyobranchial apparatus, such as opening and closing of the gill slits (Severtsov, 1966). The entire apparatus may move slightly dorsoventrally as well because the points of rotation at the jaw joint and neck are somewhat mobile. Also, the distal tips of the ceratohyals and epibranchials may move laterally during buccal expansion, broadening the pharynx. Both the

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3. Aquatic Feeding in Salamanders dorsoventral shifting of the hyobranchial apparatus and the lateral expansion of the pharynx contribute only slightly to buccal expansion, and will not be discussed further; ventrocaudal rotation of the hyobranchial apparatus is considered the primary movement producing buccal expansion. As the hyobranchial apparatus rotates and drops, it applies a downward force to the buccal lining and the skin of the throat, which unfold and expand ventrally to produce the volume change that draws water, and usually prey, into the mouth. When the buccal cavity has expanded fully, it begins to compress by elevation of the hyobranchial apparatus, which is accomplished like hyobranchial depression, only in reverse and much more slowly. Water is expelled through the gill slits or mouth and prey is retained by the gill rakers or teeth. Mouth opening and closing must be coordinated with hyobranchial depression and elevation to ensure capture and prevent subsequent escape of the prey. The mouth is opened and closed simply by rotation of the mandible about its articulation with the skull. The mouth is opened and begins to close during buccal expansion and is kept closed or ajar during buccal compression. If a prey item is not brought entirely into the mouth during the initial strike, it is gripped by the opposing teeth of the dentary on the lower jaw and the premaxilla and maxilla (when present) on the upper jaw. Some large salamanders, such as amphiumids and cryptobranchids, have robust jaws and teeth that can be used for crushing or tearing prey. Labial lobes are critical for effective suction feeding (Matthes, 1934; Miller and Larsen, 1989). They effectively prevent water from entering the sides of the mouth and restrict water flow to the front. By reducing the area of the aperture through which a given volume of water must flow in a certain period of time, labial lobes increase the velocity of the flow and thus increase the probability that elusive prey will be entrained. Labial lobes are so frequently present in suction feeders that the presence of these structures in the absence of behavioral data is evidence that the salamander suction feeds. Salamanders that lack labial lobes may, however, use suction when feeding in water, for example, breeding Ambystoma (Miller and Larsen, 1986). The importance of labial lobes in suction feeding is reflected in the poor prey-capture success of these salamanders that lack them (Reilly and Lauder, 1988a). Other morphological and functional features may also enhance suction-feeding ability. In amphiumids, the maxillae are attached loosely to the rest of the skull and undergo medial displacement during suction feeding, consequently reducing frontal gape and potentially improving capture success (Erdmann and Cundall, 1984). Cryptobranchids are unique in that they

can depress the mandibles asymmetrically, opening only one-half of the mouth at a time, a behavior observed most often during prey manipulation. This behavior may serve the same function as labial lobes in other taxa, restricting the gape and accelerating water flow. Cryptobranchids can also depress the hyobranchial apparatus asymmetrically during prey capture and manipulation (Cundall et al, 1987). The ability of cryptobranchids to move the jaws and hyobranchial apparatus unilaterally indicates that muscles may not be functioning symmetrically during feeding, as many functional studies tend to assume. The gill slits of many aquatic salamanders have also been proposed to contribute to suction-feeding performance (Lauder and Shaffer, 1986; Reilly and Lauder, 1988a). Gill slits have been shown to open during suction feeding before maximum buccal expansion. This timing of gill slit opening would allow the momentum of the primary flow to carry water posteriorly out the gill slits, preventing turbulence that could disrupt flow into the mouth (MuUer and Osse, 1984). Alternatively, the momentum of the primary water flow can be absorbed by a relatively enormous buccal expansion, in which water is stored for later expulsion during buccal compression. This latter mechanism likely operates in Cryptobranchids, which have no gill slits or only a tiny spiracle, and in metamorphosed newts, which lack gill slits. The exact biomechanical role of gill slits in suction feeding remains to be determined and likely differs in taxa with different morphologies. Gill slits are clearly not always necessary for successful suction feeding in salamanders, given the suction-feeding prowess of some postmetamorphic salamandrids that lack gill slits, many of which suction feed as effectively as larvae (Miller and Larsen, 1989). D . Biomechanics Analyses of feeding kinematics and anatomy of the feeding system can be combined to produce a model of the biomechanical events of suction feeding. This section presents such a model for salamanders, which is intended to be used as a heuristic device to identify developmental and evolutionary transitions in hyobranchial function. It is to be used as a foundation on which to build hypotheses of functional transformation, rather than as a precise representation of all of the events occurring during suction feeding. The skeletal elements of the skull and hyobranchial apparatus of larval salamanders form a system of rigid elements on which the muscles act to produce movments. Suction feeding involves primarily rotational movements of the jaws and hyobranchial apparatus (Fig. 3.9A) and can be modeled as a system of levers.

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IHP RCP F I G U R E 3.9. Mechanics of hyobranchial depression during suction feeding, showing hyobranchial apparatus and jaws in the elevated position on the left and the depressed position on the right. Larval skull, jaws, and hyobranchial elements, shown in lateral view (A), are modeled as systems of levers (B). Muscles (black lines) contract to produce movements of the levers. Muscles shown on figures on the left produce movements that place the elements in the positions shown on the right, and vice versa. Oblique views (C) show displacements of the hyobranchial apparatus in three dimensions, including twisting of vertical elements about their long axes.

The skull and jaw^s form a single lever system. The hyobranchial apparatus, together with the skull and neck, can be represented in simplified form as a fourbar mechanism (Fig. 3.9B) in w^hich rotation of any one element causes equal rotation of the parallel element. The skull and neck, taken together, can be considered a single component, which forms the dorsal element of the mechanism. The basibranchial forms the ventral element. These two horizontal elements are linked by the paired ceratohyals and a pair of epibranchials (either the first or the second pair), which form the rostral and caudal elements, respectively. Each of the four elements of the mechanism articulates with neighboring elements and rotates with respect to them. The buccal cavity is expanded by parallel rotation of the rostral

and caudal elements, anchored by the dorsal element and linked by the ventral element, which undergoes ventrocaudal translation without rotation. The rostral and caudal elements are bilaterally paired, but articulate with the single, medial ventral and dorsal elements. The entire system thus resembles two four-bar linkages functioning in parallel, sharing some components (Fig. 3.9C). The jaw and hyobranchial lever systems act in concert to produce the movements of suction feeding. Movement of the skeletal levers is accomplished by contraction of the associated musculature. In the case of the jaws, the DM and LM act as antagonists to open and close the mouth, respectively. The GH is in a position to open the mouth as well, via its attachment to

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3. Aquatic Feeding in Salamanders the mandible (Fig. 3.9B). The mechanical advantage of the GH in mouth opening is increased when the hyobranchial apparatus is depressed. The muscles of the neck direct the gape dorsally, ventrally, or laterally, and some (the DT and ITCS) are in a position to provide resistance to skull depression when the GFi is used in mouth opening. The hyobranchial apparatus is swung ventrocaudally by the RCP, RCS, and BH and is swung dorsorostrally by the GH, IMP, IFF, and IFFP. The RCP is attached to the basibranchial and pulls that ventral element caudally, forcing it to pivot about its attachments to the rostral and caudal elements, which, in turn, pivot about their attachments to the skull and neck. The BH is attached to the tip of the first epibranchial and to the rostral tip of the ceratohyal and contracts to pull the diagonal corners of the mechanism toward one another, forcing the basibranchial ventrocaudally. The BH and RCP both contribute to the same resultant force vector and produce the same ventrocaudal movement of the basibranchial. These two muscles are likely to be coactive during feeding, together producing a powerful expansion of the buccal cavity. In addition to forcing the hyobranchial apparatus ventrocaudally, the BH has two further roles in buccal expansion. It is in a position to pull the tips of the epibranchials ventrally and to rotate the flat ceratohyals about their long axes so that their medial edges are directed ventrally when the hyobranchial apparatus is fully depressed. This latter action brings the broad surfaces of the ceratohyals into contact with the buccal walls, supporting the buccal lining and aiding in expansion. During the first part of buccal expansion the gill slits are held closed by the SAR muscles, which adduct the epibranchials. Acting in direct opposition to the RCP is the GH, which draws the basibranchial rostrally via its attachment to the urohyal. In adults in which the urohyal loses its attachment to the basibranchial, the GH retains its larval role but functions by cradling the hyobranchial apparatus rather than pulling directly on it. The IMP, IH, and IHP also do not attach directly to the linkage, but all cradle the ventral and caudal elements and exert dorsal components of force, moving the basibranchial rostrodorsally and reducing buccal volume. The LAB muscles are in a position to pull the epibranchial tips dorsally, further compressing the buccal cavity. The lever system of the jaws is common to all salamanders, whereas the four-bar linkage system of the hyobranchial apparatus is present in its purest form in larval salamanders. The first epibranchial is usually the most robust element of the larval hyobranchial apparatus and forms the caudal component of the linkage system. The ceratobranchials may contribute either to

the ventral element, as in the branchial plate of plethodontids, or to the caudal element as in amphiumids, in which they are fused with the epibranchials. Some larval salamanders possess additional skeletal elements, which lie between components of the linkage, but these act as part of one of the elements of the system and do not alter its mechanical function as proposed here. Adult salamanders may lack one or more connections in the linkage, making the system a series of levers. Some aquatic salamandrids, for example, lack a tight connection between the ceratohyals (rostral element) and the basibranchial (ventral element). Adults also lack the BH, which pulls diagonal corners toward one another; however, the SAR enlarges at metamorphosis to replace the BH in both position and function. All adults retain the primary muscle of the system, the RCP, which alone can swing the entire linkage ventrocaudally. In many larvae both the first epibranchial and the ceratohyal are equally robust and probably bear comparable loads during buccal expansion. However, the relative robustness of these elements is variable among taxa and across developmental stages, reflected in the extent of ossification of the elements or the crosssectional shape and area. In some groups, the ceratohyals are more robust than the epibranchials, whereas in others the reverse is true. During development and evolution, the primary axis of the linkage system may shift from one set of skeletal elements to another or from the rostral to the caudal components. Cryptobranchoids, for example, are unusual in having the caudal component of the linkage be the second ceratobranchial and epibranchial, rather than the first as in other taxa. This caudal component is ossified and forms the main load-bearing component; the rostral component, the ceratohyal, is flattened and cartilaginous. In larval salamandrids, the ceratohyal is more robust than the epibranchials and is thus likely to bear more load, whereas in adults that feed aquatically, the epibranchials form the primary load-bearing axis of the system and are more fully ossified than the ceratohyal. In taxa that also feed on land using tongue protraction, the rostral portions of the hyobranchial apparatus are generally more flexible and less capable of bearing compressive loads, whereas the caudal components are more robust, bearing loads during both suction feeding and tongue protraction. E. Metamorphosis Following metamorphosis, many salamanders leave the water to forage on land. Suction feeding, the primary mode of aquatic salamanders, relies on the incompressibility of water to move prey into the mouth

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and therefore must be abandoned and replaced by a mode that can operate in air. Terrestrial salamanders must capture prey by either tongue or jaw prehension, behaviors that make use of many of the same morphological components as suction feeding. The jaws are strengthened at metamorphosis and assume more importance in prey capture. The hyobranchial apparatus is remodeled extensively for propelling the tongue from the mouth, but in many cases can continue to function in buccal expansion. In general, the skull and jaws begin a gradual metamorphosis before the hyobranchial apparatus, which undergoes a more abrupt transformation (Rose, 1996). Suction-feeding performance can thus be maintained at a high level late into larval life in those taxa that make a developmental transition to tongue or jaw prehension. In some taxa, such as plethodontids, suction-feeding function is lost completely as the hyobranchial apparatus transforms and tongue function is emphasized. Even completely aquatic adult plethodontids lack the ability to suction feed and use tongue or jaw prehension to capture prey in water (Deban and Marks, 1992). F. Performance Many of the changes that occur during metamorphosis can potentially affect suction-feeding performance, including the loss of labial lobes, transformation of the hyobranchial apparatus, development of the tongue, reduction in buccal volume, and closure of the gill slits. Larvae and perennibranchiate salamanders, which undergo few of these changes, are the most adept at suction feeding. Larval Notophthalmus viridescens capture worms in up to 99% of their attempts (Reilly and Lauder, 1988a), larval Salamandra salamandra up to 91% of attempts (Reilly, 1995), and larval Amybstoma tigrinum capture worms in 93% of attempts and can catch even highly elusive prey such as fish 33% of the time (Lauder and Shaffer, 1986). Partially metamorphosing taxa such as amphiumids and cryptobranchids perform as well as larvae, even though they may lack some larval features. The suction-feeding performance of aquatic adult salamandrids is variable but comparable to that of larvae and is correlated with the degree of head tapering and hyobranchial ossification, and the size of the labial lobes (Miller and Larsen, 1989). Adult semiaquatic newts with rounded heads and modest labial lobes {Taricha, Cynops, Notophthalmus, Paramesotriton, and Pleurodeles) capture earthworm pieces 90-97% of attempts, fairy shrimp 3 8 58% of attempts, and fish 13-23% of attempts, whereas the fully aquatic Pachytriton, with a strongly tapered snout, fully ossified hyobranchial apparatus, and large labial lobes, captures these same prey 100,90, and 65%

of attempts, respectively. The absence of gill slits in the adult newts does not affect their suction-feeding performance (Miller and Larsen, 1988; Reilly and Lauder, 1988a). G. Variation Larger suction-feeding salamanders show considerable variation in the relative timing of events during prey capture. This variation across prey type and among individuals can be due to the salamander actively modulating its behavior or selecting from a repertoire of stereotyped behaviors based on an assessment of conditions before initiating a predatory strike. The high speed of suction-feeding movements is likely to preclude any adjustments via sensory feedback during the strike. Cryptobranchus and Amphiuma show variation in the timing of movements of the hyobranchial apparatus, jaws, and body. When capturing slowly moving or stationary prey, they show little forward movement and mouth opening occurs before buccal expansion begins. When feeding on elusive prey, these salamanders exhibit forward lunging and synchronous mouth opening and buccal expansion. Mouth opening and buccal expansion are greater when feeding on elusive prey compared to sluggish prey (Erdman and Cundall, 1984; Elwood and Cundall, 1994). Slight individual variation in muscle activity patterns has been recorded in larval Ambystoma feeding on the substrate, but variation due to prey type was not detected (Reilly and Lauder, 1989). Ambystoma larvae have been observed to forage in the water column and strike at prey from a distance (Hoff et ah, 1985), suggesting that additional variation in prey-capture behavior remains to be investigated in some taxa. Explicit studies of variation are few (Erdmann and Cundall, 1984; Shaffer and Lauder, 1985a,b; Elwood and Cundall, 1994), however, leading to the impression that salamander prey-capture is an invariant, stereotyped behavior. This notion is gradually being dispelled as more incidental kinematic evidence of variation is gathered. Nonetheless, studies directly examining the taxonomic and developmental diversity of both preycapture performance and variation are needed.

IV. DIVERSITY A N D EVOLUTION The preceding sections have presented the general pattern of morphology, function, and behavior of the feeding systems of aquatic salamanders. Characters have been emphasized over taxa. The following sections are designed to place these characters in the context of taxa that possess them. Unique features of each

3. Aquatic Feeding in Salamanders family, common patterns of evolution (convergence and homoplasy) within the Caudata, as well as synapomorphies of larger clades (above the family level) are discussed. Features common to most families have already been covered. A. Features of Salamander Families Each of the 10 families of salamanders possesses unusual or unique features of feeding biology. In the following accounts the developmental patterns (i.e., perennibranchiate, paedomorphic, metamorphic) of each family is discussed as well as its bearing on feeding form and function. 1. Sirenidae Sirenids are dwarf {Pseudohranchus, two species) or giant {Siren, two species) paedomorphic, perennibranchiate, fully aquatic salamanders that are elongate and lack hindlimbs entirely. They possess a fundamentally larval skull and hyobranchial configuration, which are unusual in many respects (Reilly and Altig, 1996). They possess premaxillae and robust tooth-bearing palatines in the upper jaw. The frontal processes of the premaxillae border the nasals laterally rather than medially as in most other salamanders. The skull is strongly tapered rostrally, and the lower jaw is nearly triangular and rather small, bearing teeth only on the coronoid (in Siren) and with the unusual ball-andsocket jaw joint far anterior. Maxillae are lacking in Pseudohranchus but are present in Siren as tiny, freefloating elements (Parker, 1882; Larsen, 1963; Duellman and Trueb, 1986). The hyobranchial apparatus is extensively ossified and the anterior tip of the basibranchial is bulbous where it articulates with the ceratohyals. Three epibranchials are present in Pseudohranchus and four in Siren. The labial lobes are the largest of any salamander, larval or adult, with upper lobes overlapping the lower jaw to such a degree that they almost meet ventrally. Sirenids are powerful suction feeders, due to the combination of the robust hyobranchial apparatus and the entirely frontal gape afforded by the immense labial lobes. The Sirenidae is the sister taxon to all other salamanders (Fig. 3.1), but its morphology is unsual and not representative of the ancestral condition. 2.

Hynobiidae

The sister group of the Cryptobranchidae, the Hynobiidae, is a large family with about 39 species in seven genera. Some perennibranchiate populations of Hynohius exist. Most species are metamorphic, how-

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ever, and many are aquatic or semiaquatic. Little is known of their feeding behavior. The semiaquatic Salamandrella keyserlingii and Batrachuperus persicus use jaw prehension in water (Deban, personal observation), whereas the fully aquatic Batrachuperus and Pachyhynohius possess pronounced labial lobes and a pleated buccal lining, morphology that is consistent with suction feeding. Fiynobiids possess complex skulls and hyobranchia, with more elements than the other salamanders (Fig. 3.3), a condition that has led, in part, to the conclusion that they are basal within the Caudata (with the cryptobranchids) after the Sirenidae (Fig. 3.1). Two epibranchials are present in adults, compared to one in all other metamorphosing taxa. The second ceratobranchials and epibranchials are ossified whereas the first are cartilaginous, a feature shared with the Cryptobranchidae. Free radii are completely lacking, but unusual, elongate, radial cartilages connect the ceratohyals to one another or to the basibranchial. 3.

Cryptobranchidae

The Cryptobranchidae is a small family with two genera and three species, all aquatic. Cryptobranchids possess unusual behavioral and morphological features related to aquatic feeding. Not only do they reach enormous size as adults (up to 75 cm in Cryptohranchus and 150 cm in Andrias), but they also have the largest buccal expansion relative to body size of any salamander, due in part to the broad, flat head and pleated buccal lining. As a consequence they are supreme suctionfeeders and are unique in that they can direct their strike to the side using unilateral jaw and hyobranchial depression (Elwood and Cundall, 1994). This behavior is facilitated by the loose mandibular symphysis, strongly curved mandibles, and broad hyobranchial elements. The pattern of hyobranchial ossification is unusual and shared with the Hynobiidae: the first ceratobranchial and epibranchial (which are fused to one another) are cartilaginous and the second are bony. This second set acts as the primary lever in hyobranchial depression, as compared to the first set in most other salamanders. Cryptobranchids are essentially metamorphic in their skull morphology, but retain other larval features, such as lidless eyes, a poorly developed tongue pad, lower labial lobes, posterior branchial elements, and spiracles; the last two features are present in Cryptohranchus and absent in Andrias. Cryptobranchids will scavenge, but can also capture elusive prey such as fish and can handle aggressive prey such as crayfish. They are unusual among suction-feeding salamanders in that they can modulate their feeding behavior (the timing and extent of jaw

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and hyobranchial movements), depending on the elusiveness of the prey. 4. Proteidae The Proteidae includes the genera Necturus (five species) and Proteus (one species), completely aquatic paedomorphic perennibranchiates with an essentially larval morphology including labial lobes and two gill slits. The hyobranchial apparatus is heavily ossified and retains the larval configuration throughout life. Proteids have only three epibranchials, a feature shared only with some plethodontid larvae and Pseudobranchus (Fig. 3.4). The upper jaw lacks maxillae but contains massive, dentate palatopterygoids that replace them in function. Proteids are strong suction feeders. Proteus is elongate, blind, and cavernicolous and is adept at locating prey in complete darkness by olfactory and lateral line senses (Durand et ah, 1982; Uiblein and Parzefall, 1993). 5.

Amphiumidae

The Amphiumidae is a small family with three species, all aquatic, elongate, and with four tiny limbs and a reduced number of toes. Amphiumids resemble cryptobranchids in behavior and in their degree and pattern of paedmorphosis, despite marked differences in morphology and ecology. They retain some larval features (lidless eyes, small tongue pad, interlocking labial lobes, spiracles, and posterior branchial elements) but have solid and robust skulls with some metamorphic features. Amphiumids are strong suction feeders and, like cryptobranchids, can modulate their behavior depending on prey type (Erdmann and Cundall, 1984). They have powerful jaws and teeth and can capture and crush formidable prey, and can bite viciously (Conant and Collins, 1991). The skull is elongate and tapered anteriorly, quite unlike the rounded, flattened skull of cryptobranchids. 6.

Salamandridae

The Salamandridae is a large and diverse family with 14 genera and about 45 species, most of which are aquatic or semiaquatic. The majority of species are fully metamorphic and possess the adult configuration of hyobranchial elements, although some populations are perennibranchiate. Salamandrids possess the full range of hyobranchial morphologies, from almost entirely cartilaginous, slender apparati that are used in long-distance tongue protraction (e.g., Salamandrina and Chioglossa) to the almost fully ossified, robust apparati used for powerful suction feeding (e.g., Pachytriton and Cynops). Salamandrids of the latter type

are perhaps the most proficient suction feeders of all metamorphic salamanders. Taxa that use both suction feeding and tongue protraction (e.g., Taricha and Notophthalmus) possess an intermediate hyobranchial morphology. This morphology must play two disparate feeding roles and represents a functional compromise (Findeis and Bemis, 1990). Salamandrids that feed aquatically after metamorphosis develop labial lobes on the upper jaws that are functionally similar to larval lobes (Ozeti and Wake, 1969) and increase suctionfeeding performance. Those that return to the water to breed develop these lobes temporarily but resorb them rapidly (within 48 hr) on resuming a terrestrial existence (Matthes, 1934). A terrestrial eft stage is present after metamorphosis in many taxa that are aquatic as adults (e.g., Notophthalmus), during which time prey is captured with the tongue. A particularly unsual situation occurs in Pachytriton, in which adults have a tiny tongue pad and completely lack tongue protraction ability as do their larvae. However, a terrestrial eft stage occurs after metamorphosis in which tongue prehension presumably is used (Thiesmeier and Romberg 1997), suggesting that a secondary loss of tongue structures accompanies the return to a permanently aquatic lifestyle. The only viviparous salamanders are in this family. The fetuses of these species feed on unfertilized ova or smaller embryos in utero and are born as larvae or metamorphs; the terrestrial juveniles and adults do not feed in water. Chioglossa is unusual in that it possesses a slender hyobranchial apparatus specialized for tongue protraction, suggesting that it does not suction feed. It is known, however, to spend time in water (Arntzen, 1981) and may capture aquatic prey using tongue or jaw prehension. 7.

Rhyacotritonidae

The Rhyacotritonidae contains four species of one genus, Rhyacotriton, all semiaquatic and metamorphic with reduced lungs. Adults possess a generalized hyobranchial morphology similar to the Ambystomatidae and modest tongue protraction, which they use on land and in water (Larsen, personal communication). They suction feed only as larvae. 8,

Dicamptodontidae

The Dicamptodontidae contains four species of one genus, Dicamptodon, three metamorphic and one perennibranchiate (D. copei). The larvae and perennibranchiate adults suction feed in a typical manner. No information is available on aquatic feeding in adults, which are essentially terrestrial but which return to the water to breed and guard their eggs (Nussbaum, 1969).

3. Aquatic Feeding in Salamanders 9.

Ambystomatidae

The Ambystomatidae, the sister taxon of the Dicamptodontidae, is a large family with one genus, Ambystoma, and 31 species. Most are metamorphic and terrestrial, but some species (e.g., the axolotl A. mexicanum) and populations of other species (e.g., A. tigrinum) are perennibranchiate. Larvae and perennibranchiate adults suction feed. Adults may use suction (although poorly) to capture prey when returning to the water to breed. Species formerly placed in the genus Rhyacosiredon are partially metamorphic; the adults inhabit mountain streams and retain larval features such as labial lobes, lidless eyes, and a small tongue pad. They possess a midmetamorphic hyobranchial configuration, with broader, more heavily ossified elements than other adult ambystomatids and less elaboration of anterior lingual elements (Fig. 3.6) (Reilly and Brandon, 1994). These features strongly suggest they are suction feeders, although behavioral information is lacking. 10,

Plethodontidae

The Plethodontidae is the largest family of salamanders, with over 275 species in 28 genera. Most of these species are members of the tribes Plethodontini and Bolitoglossini of the subfamily Plethodontinae and are completely terrestrial and direct developing. Two basal clades within the family, the subfamily Desmognathinae and the tribe Flemidactyliini (within the subfamily Plethodontinae), have members that retain the ancestral life history of metamorphosis from an aquatic suction-feeding larva. Direct development has also evolved two to three times within the Desmognathinae. Morphologically, plethodontid larvae are typical in most respects, but possess dentate palatopterygoids and lack maxillae and ossified pterygoids. Most hemidactylines possess only three epibranchials as larvae and many are perennibranchiate and suction feed as adults with their larval morphology. Two of these taxa, Haideotriton and Typhlomolge, are blind cave salamanders with one and two species, respectively. Metamorphic plethodontids that feed in the water use tongue or jaw prehension, even the fully aquatic desmognathine Desmognathus marmoratus (Schwenk and Wake, 1988; Deban and Marks, 1992; note that previous studies refer to D. marmoratus as Leurognathus marmoratus; however, we follow the recommendation of Titus and Larson, 1996, based on their recent molecular study of desmognathine relationships). Suction feeding has not been documented in metamorphosing adult plethodontids. They have probably lost the ability to suction feed as a result of the elaboration

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of the tongue protraction system that followed on the loss of robust hyobranchial elements that can function as a mechanism for expanding the buccal cavity. Instead they use terrestrial feeding behaviors in water. The completely terrestrial bolitoglossines have a unique pattern of one embryonic epibranchial. All plethodontids are lungless and possess nasolabial grooves, a feature unique to the family. B. Phylogenetic Patterns of Feeding Form and Function Many features of the feeding morphology and behavior of salamanders have evolved convergently. Paedomorphosis, or the retardation of development relative to the ancestral condition, is a common pattern among salamanders and, when taken to the extreme, results in perennibranchiation. Perennibranchiation appears in 7 of the 10 salamander families and has evolved more than once in some of these (notably the Ambystomatidae and Plethodontidae). Extensive ossification of the hyobranchial apparatus has evolved independently in the Sirenidae, Proteidae, Salamandridae, Amphiumidae, and Cryptobranchidae and contributes to the strong suction-feeding abilities of these taxa. Free hypohyals in larvae and first radii of adults (which we consider homologues) have been lost independently in the Sirenidae, Proteidae, and Plethodontidae, but are present at some stage of development in the other families. Four larval epibranchials appear to be the ancestral condition for salamanders, and the presence of only three has evolved at least three times: in Pseudohranchus, the Proteidae, and in the Hemidactyliini (and in the embryos of the Plethodontini). A composite first epibranchial representing the fusion of the first ceratobranchial to the first epibranchial has evolved convergently in the Amphiumidae and some members of the Cryptobranchoidea and Salamandridae. The presence of a third larval ceratobranchial is unique to the Cryptobranchoidea, as is the functioning of the second set of branchial elements as the primary lever in hyobranchial depression. Free-living larvae, and thus suction feeding, have been lost numerous times, at least twice with the evolution of viviparity among salamandrids that give birth to metamorphosed young and at least three times with the evolution of direct development in plethodontids. Suction feeding has been lost at least three times in adult salanianders that feed in water: among semiaquatic and aquatic rhyacotritonids, plethodontids, and hynobiids, which have exapted the terrestrial ingestion behaviors of tongue or jaw prehension to capture aquatic prey.

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V. OPPORTUNITIES FOR FUTURE RESEARCH The fundamental structure, function, and natural history of feeding in salamanders are well known. Studies of foraging behavior have been conducted on a number of species, and diet is known for many more taxa. Cranial anatomy has been described for many species from most of the major groups, although more detailed morphological studies are needed for a number of taxa, including the Sirenidae (especially Pseudobranchus), Dicamptodontidae, and Rhyacotritonidae. The Rhyacotritonidae, which possesses a generalized and perhaps ancestral morphology, is particularly interesting because of its phylogenetic position. There are some groups for which scant morphological information is available, such as the Hynobiidae. The basic function of the suction-feeding system common to most aquatic salamanders is fairly well understood, but the functional significance, if any, of the great morphological diversity of salamanders remains largely uninvestigated. Feeding function of only a handful of the approximately 400 species of salamanders has been studied in any detail, and even fewer species have been examined at more than one level of biological organization. Studies of prey-capture behavior and kinematics among the aquatic taxa have focused on the families Ambystomatidae and Salamandridae, and little information is available for the other families (Terrestrial taxa are more fully studied; see Chapter 4). Physiological studies of in vivo muscle function (i.e., electromyography) have been undertaken in only seven species of aquatic salamanders representing half of the families. Clearly more diversity remains to be explored, including those taxa that show pronounced modulation or asymmetry of movement, such as Cryptobranchus and Amphiuma. The development of feeding behavior and function has been studied in only two species of salamanders, and early development of larval feeding remains completely unstudied. Little information is available on the feeding behavior and function in larvae of the unusual Cryptobranchoidea, particularly the Hynobiidae. The diversity of life histories among aquatically feeding salamanders has not yet been exploited. Comparisons between 1-year and multiyear larvae, and among larvae, paedomorphic adults, and secondarily aquatic metamorphic forms, may reveal relationships among structure, function, and life history. Our understanding of salamanders as a group is very limited in areas of neural control mechanisms, learning abilities, developmental plasticity in behavior and morphology, and variation and modulation. Most major salamander taxa remain to be examined in these

areas. Taxonomic and developmental diversity among salamanders remain to be exploited by researchers of biomechanics, physiology, development, and neuroethology. As long as representatives of most of the major groups of salamanders can be obtained, technological advances in high-speed imaging, electromyography, muscle physiology, and neurophysiology will continue to provide opportunities to explore the form and function of the feeding systems of salamanders at multiple levels. Acknowledgments We thank members of the Wakelunch group and Marvalee Wake for providing constructive comments on the manuscript. Karen Klitz rendered Figs. 3.4 and 3.6.

References Alberch, P., and E. A. Gale (1986) Pathways of cytodifferentiation during the metamorphosis of the epibranchial cartilage in the salamander Eurycea bislineata. Dev. Biol. 117:233-244. Alcobendas, M., H. Dopazo, and P. Alberch (1996) Geographic variation in allozymes of populations of Salamandra salamandra (Amphibia: Urodela) exhibiting distinct reproductive modes. J. Evol. Biol. 9:83-102. Anthony, C. D., D. R. Formanowicz, Jr., and E. D. Brodie, Jr. (1992) The effect of prey availability on the search behavior of two species of Chinese salamanders. Herpetologica 48:287-292. Amtzen, J. W. (1981) Ecological observations on Chioglossa lusitanica (Caudata, Salamandridae). Amph.-Rept. 1:187-203. Avery, R. A. (1968) Food and feeding relation of three species of Triturus (Amphibia: Urodela) during the aquatic phases. Oikos 19: 408-412. Bartels, M., H. Miinz, and B. Claas (1990) Representation of lateral line and electrosensory systems in the midbrain of the axolotl, Ambystoma mexicanum. J. Comp. Physiol. A. 167:347-356. Bell, G. (1975) The diet and dentition of smooth newt larvae {Triturus vulgaris). J. Zool. Lond. 176:411-424. Beneski, J. T., Jr., and J. H. Larsen, Jr. (1989a) Interspecific, ontogenetic, and life history variation in the tooth morphology of mole salamanders (Amphibia, Urodela, and Ambystomatidae). J. Morph. 199:53-70. Beneski, J. T, Jr., and J. H. Larsen, Jr. (1989b) Ontogenetic alterations in the gross tooth morphology of Dicamptodon and Rhyacotriton (Amphibia, Urodela, and Dicamptodontidae). J. Morph. 199:165-174. Besharse, J. C., and R. A. Brandon (1974) Postembryonic eye degeneration in the troglobitic salamander Typhlotriton spelaeus. J. Morph. 144:381-406. Bonebrake, J. E., and R. A. Brandon (1971) Ontogeny of cranial ossification in the small-mouthed salamander, Ambystoma texanum (Matthes). J. Morph. 133:189-204. Brophy, T. E. (1980) Food habits of sympatric larval Ambystoma tigrinum and Notophthalmus viridescens. J. Herp. 14:1-6. Burton, T. M. (1977) Population estimates, feeding habits and nutrient and energy relationships of Notophthalmus v. viridescens, in Mirror Lake, New Hampshire. Copeia 1977:139-143. Collins, J. P., and J. R. Holomuzki (1984) Intraspecific variation in diet within and between trophic morphs in larval tiger salamanders {Ambystoma tigrinum nebulosum). Can. J. Zool. 62:168-174.

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guides feeding behavior in amphibians. Naturwissenschaften 69: 552-553. Hoff, K. S., M. J. Larmoo, and R. J. Wassersug (1985) Kinematics of midwater prey capture by Ambystoma (Caudata: Ambystomatidae) larvae. Copeia 247-251. Jaeger, R. G., and D. E. Barnard (1981) Foraging tactics of a terrestrial salamander: choice of diet in structurally simple environments. Am. Nat. 117:639-664. Joly, F. (1981) Le comportement predateur du Triton alpestre (Triturus alpestris). I. fitude descriptive. Biol. Behav. 6:339-355. Krogh, J. E., and W. W. Tanner (1972) The hyobranchium and throat myology of the adult Ambystomatidae of the United States and Northern Mexico. Brigham Young Univ. Sci. Bull. 16:1-69. Larsen, J. H., Jr. (1963) The Cranial Osteology of Neotenic and Transformed Salamanders and Its Bearing on Interfamilial Relationships. Fh.D. Dissertation, Univ. of Washington, Seattle. Larson, A., and W. W. Dimmick (1993) Fhylogenetic relationships of the salamander families: an analysis of congruence among morphological and molecular characters. Herp. Monogr. 7:77-93. Larsen, J. H., Jr., and D. J. Guthrie (1975) The feeding system of terrestrial tiger salamanders (Ambystoma tigrinum melanostictum Baird). J. Morph. 147:137-154. Larsen, J. H., Jr., J. T. Beneski, Jr., and B. T. Miller (1996) Structure and function of the hyolingual system in Hynobius and its bearing on the evolution of prey capture in terrestrial salamanders. J. Morph. 227:235-248. Lauder, G. V., and H. B. Shaffer (1985) Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders. J. Morph. 185:297-326. Lauder, G. V., and H. B. Shaffer (1986) Functional design of the feeding mechanism in lower vertebrates: unidirectional and bidirectional flow systems in the tiger salamander. Zool. J. Linn. Soc. 88:277-290. Leff, L. G., and M. D. Bachmann (1986) Ontogenetic changes in predatory behavior of larval tiger salamanders (Ambystoma tigrinum). Can. J. Zool. 64:1337-1344. Lombard, R. E., and D. B. Wake (1977) Tongue evolution in the lungless salamanders, family Flethodontidae. II. Function and evolutionary diversity. J. Morph. 153:39-80. Luthardt-Laimer, G., and G. Roth (1983) Reduction of visual inhibition to stationary prey by early experience in Salamandra salamandra (L.). Z. Tierpsychol. 63:294-302. Marche, C , and J. F. Durand (1983) Recherches comparatives sur Fontogenese et revolution de Fappareil hyobrachial de Proteus anguinus L., proteidae aveugle des eaux souterraines. Amph.Rept. 4:1-16. Martin, J. B., N. B. Witherspoon, and M. H. Keenleyside (1974) Analysis of feeding behavior in the newt Notophthalmus viridescens. Can. J. Zool. 52:277-281. Martof, B. S., and D. C. Scott (1957) The food of the salamander Leurognathus. Ecology 38:494 -501. Matthes, E. (1934) Bau und Funktion der Lippensaume wasserlebender Urodelen. Zeit. Morph. Okol. Tiere 28:155-169. Miller, B. T., and J. H. Larsen, Jr. (1986) Feeding habits of metamorphosed Ambystoma tigrinum melanostictum in ponds of high p H (<9). Great Basin Nat. 46:299-301. Miller, B. T., and J. H. Larsen, Jr. (1989) Feeding performance in aquatic postmetamorphic newts (Urodela: Salamandridae): are bidirectional flow systems necessarily inefficient? Can. J. Zool. 67:2414-2421. MuUer, M., and J. W. M. Osse (1984) Hydrodynamics of suction feeding in fish. Trans. Zool. Soc. Lond. 37:51-135. Nickerson, M. A., and C. E. Mays (1973) The hellbenders: North American ''giant salamanders." Milwaukee Public Mus. Pub. Biol. Geol. 1:1-106.

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Noble, G. K. (1931) The Biology of the Amphibia. McGraw-Hill, New York. Northcutt, R. G., and K. Brandle (1995) Development of branchiomeric and lateral line nerves in the axolotl. J. Comp. Neurol. 355: 427-454. Nussbaum, R. A. (1969) Nest and eggs of the Pacific giant salamander, Dicamptodon ensatus (Eschscholtz). Herpetologica 25: 257-261. Ozeti, N., and D. B. Wake (1969) The morphology and evolution of the tongue and associated structures in salamanders and newts (family Salamandridae). Copeia 91-123. Parker, H. W., and E. R. Dunn (1964) Dentitional metamorphosis in the Amphibia. Copeia 1964:75-86. Parker, W. K. (1882) On the structure and development of the skull of urodeles. Trans. Zool. Soc. Lond. 11:171-214. Peck, S. B. (1973) Feeding efficiency in the cave salamander Haideotriton wallacei. Int. J. Speleol. 5:15-19. Peterson, C. L., J. W. Reed, and R. F. Wilkinson (1989) Seasonal food habits of Cryptobranchus alleganiensis (Caudata: Cryptobranchidae). Southwestern Nat. 34:438-441. Piatt, J. (1938) Morphogenesis of the cranial muscles of Amblysioma punctatum. J. Morph. 63:531-587. Piatt, J. (1940) Correct terminology in salamander myology. II. Transverse throat musculature. Copeia 1940:9-14. Reilly, S. M. (1986) Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens (Caudata: Salamandridae), and its relationship to metamorphosis and neoteny. J. Morph. 188: 315-326. Reilly, S. M. (1995) The ontogeny of aquatic feeding behavior in Salamandra salamandra: stereotypy and isometry in feeding kinematics. J. Exp. Biol. 198:701-708. Reilly, S. M., and R. Altig (1996) Cranial ontogeny in Siren intermedia (Caudata: Sirenidae): paedomorphic, metamorphic, and novel patterns of heterochrony. Copeia 1996:29-41. Reilly, S. M., and S. M. Brandon (1994) Partial paedomorphosis in the Mexican stream Ambystomatids and the taxonomic status of the genus Rhyacosiredon Dunn. Copeia 1994:656-662. Reilly, S. M., and G. V. Lauder (1988a) Ontogeny of aquatic feeding performance in the eastern newt, Notophthalmus viridescens (Salamandridae). Copeia 87-91. Reilly, S. M., and G. V. Lauder (1988b) Atavisms and the homology of hyobranchial elements in lower vertebrates. J. Morph. 195: 237-245. Reilly, S. M., and G. V. Lauder (1989) Physiological bases of feeding behavior in salamanders: do motor patterns vary with prey type? J. Exp. Biol. 141:343-358. Reilly, S. M., and G. V. Lauder (1990) Metamorphosis of cranial design in tiger salamanders (Ambystoma tigrinum): a morphometric analysis of ontogenetic change. J. Morph. 204:121-137. Reilly, S. M., and G. V. Lauder (1992) Morphology, behavior, and evolution: comparative kinematics of aquatic feeding in salamanders. Brain Behav Evol. 40:182-196. Reno, H. W., and H. H. Middleton (1973) Lateral line system of Siren intermedia Le Conte (Amphibia: Sirenidae), during aquatic activity and aestivation. Acta Zool. 54:21-29. Rose, C.S. (1996) An endocrine-based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles. J. Zool. Lond. 239:253-284.

Roth, G. (1976) Experimental analysis of the prey catching behavior of Hydromantes italicus Dunn (Amphibia, Plethodontidae). J. Comp. Physiol. 109:47-58. Roth, G. (1987) Visual Behavior in Salamanders. Springer-Verlag, Heidelberg. Roth, G., K. C. Nishikawa, D. B. Wake, U. Dicke, and T. Matsushima (1990) Mechanics and neuromorphology of feeding in amphibians. Netherlands J. Zool. 40:115-135. Schumacher, G. H. (1958) Zur Morphologie des Mundboden der urodelen: untersuchungen an Cryptobranchus japonicus. Gegenbaur Morph. Jahrbuch 99:344-371. Schwenk, K., and D. B. Wake (1988) Medium-independent feeding in a plethodontid salamander: tongue projection and prey capture underwater. Am. Zool. 28:115A. Schwenk, K., and D. B. Wake (1993) Prey processing in Leurognathus marmoratus and the evolution of form and function in desmognathine salamanders (Plethodontidae). Biol. J. Linn. Soc. 49:141162. Severtsov, A. S. (1964) Formation of the tongue in the Hynobiidae. DokL Biol. Sci. 154:34-37. Severtsov, A. S. (1966) Food-seizing mechanism in urodele larvae. Dokl. Biol. Sci. 168:230-233. Shaffer, H. B., and G. V. Lauder (1985a) Aquatic prey capture in ambystomatid salamanders: patterns of variation in muscle activity. J. Morph. 183:273-284. Shaffer, H. B., and G. V. Lauder (1985b) Patterns of variation in aquatic ambystomatid salamanders: kinematics of the feeding mechanism. Evolution 39:83-92. Thiesmeier, B., and C. Hornberg (1997) Paarung, Fortpflanzung und Larvalentwicklung von Pachytriton sp. {Pachytriton A) nebst Bemerkungen zur Taxonomie der Gattung. Salamandra 33: 97-110. Titus, T. A., and A. Larson (1996) Molecular phylogenetics of desmognathine salamanders (Caudata: Plethodontidae): a reevaluation of evolution in ecology, life history, and morphology. Syst. BioL 45:451-472. Trueb, L. (1993) Patterns of cranial diversity among the Lissamphibia. Pp. 255-343. In: The Skull Vol. 2. J. Hanken and B. K. Hall (eds.). Univ. of Chicago Press, Chicago. TumHson, R., G. R. Cline, and P Zwank (1990) Prey selection in the Oklahoma salamander {Eurycea tynerensis). J. Herp. 24:222-225. Uiblein, F., J. P Durand, C. Juberthie, and J. Parzefall (1992) Predation in caves: the effects of prey immobility and darkness on the foraging behaviour of two salamanders, Euproctus asper and Proteus anguinus. Behav. Process. 28:33-40. Uiblein, F., and J. Parzefall (1993) Does the cave salamander Proteus anguinus detect mobile prey by mechanic cues? Mem. Biospeol. 20:261-264. Valentine, B. D., and D. M. Dennis (1964) A comparison of the gillarch system and fins of three genera of larval salamanders, Rhyacotriton, Gyrinophilus, and Amby stoma. Copeia 1964:196-201. White, R. L., II (1977) Prey selection by the rough skinned newt {Taricha granulosa) in two pond types. Northwest Sci. 51:114-118. Wilder, I. W. (1925) The Morphology of Amphibian Metamorphosis. Smith College Fiftieth Anniversary Publications. Smith College, Northampton, MA. Worthington, R. D., and D. B. Wake (1971) Larval morphology and ontogeny of the ambystomatid salamander, Rhyacotriton olympicus. Am. Midi. Nat. 85:349-364.

C H A P T E R

4 Terrestrial Feeding in Salamanders DAVID B. WAKE AND STEPHEN M. DEB AN Museum of Vertebrate Zoology and Department of Integrative Biology University of California Berkeley, California 94720

A. Systematics

I. INTRODUCTION A. Systematics B. Natural History C. Feeding Modes and Terminology 11. MORPHOLOGY A. Skeleton B. Musculature C. Sensory and Motor Systems III. FUNCTION A. Foraging, Prey Detection, and Localization B. Prey Capture and Ingestion C. Biomechanics and Functional Morphology D. Prey Processing E. Modulation of Feeding Behavior IV. DIVERSITY AND EVOLUTION A. Origins and Outgroups B. Phylogenetic Diversity C. Feeding Biology and Evolution V. OPPORTUNITIES FOR FUTURE RESEARCH References

There are roughly 450 species of salamanders currently placed in 10 families (Fig. 4.1). Evidence exists for the monophyly of the Caudata and for the sistergroup relationship of Caudata to Anura (Clouthier and Trueb, 1992; Larson and Wilson, 1991; Larson, 1991). How^ever, relationships within the Caudata are unstable, and different results are obtained from DNA sequence analysis and from morphological characters (Larson, 1991). We use one of tw^o similar phylogenetic hypotheses resulting from a combined data analysis (Larson and Dimmick, 1993). In this tree (Fig. 4.1), Sirenidae (aquatic, gilled, elongate, lacking hind limbs, and presumed to have external fertilization) is basal, followed by a branch leading to the sister-taxa Hynobiidae and Cryptobranchidae (which have external fertilization). The more derived salamanders form a monophyletic group (all have internal fertilization), but the base is unstable. Whereas earlier workers placed plethodontids as one of the most derived taxa, Larson's (1991) DNA data place it as one of the most basal lineages, and only the combined data pull it up in the tree to the base of the derived taxa. The diverse and much studied ambystomatids and salamandrids are deeply nested and envisioned as highly derived. Most terrestrial salamanders belong to the Plethodontidae, which includes about two-thirds of all species of salamanders. About three-quarters of the plethodontid species have no aquatic larval stage and develop directly from eggs laid on land (Wake and Flanken, 1996). Relationships within the Plethodontidae are discussed in Lombard and Wake (1986). Flynobiidae and Salamandridae are both relatively speciose and display

L INTRODUCTION Chapter 3 presented a general introduction to the feeding biology of salamanders, w^ith a focus on feeding in aquatic habitats. This chapter deals with feeding by metamorphosed individuals, or the free-living stage of direct-developing species. Much basic information concerning morphology and diversity applies to both aquatic and terrestrial salamanders, and we have repeated information in this chapter only v\^here necessary. The previous chapter provides essential background information for the present one.

FEEDING (K. Schwenk, ed.)

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Copyright © 2000 by Academic Press. All rights of reproduction in any form reserved.

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David B. Wake and Stephen M. Deban Sirenidae

_| Sirenoidea

Cryptobranchidae

Cryptobranchoidea

Hynobiidae Amphiumidae Plethodontidae Rhyacotritonidae Salamandridae

| Salamandroidea

Ambystomatidae Dicamptodontidae Proteidae F I G U R E 4.1. Hypothesis of phylogenetic relationships of the salamander families, adapted from one of two most-parsimonious trees from Larson and Dimmick (1993) based on an analysis of combined molecular and morphological data. See text for discussion.

diverse morphology related to feeding. Relationships of hynobiid genera are discussed in Zhao and Hu (1988) and those of salamandrids by Titus and Larson (1995). Only one genus of Ambystomatidae is recognized, but it is relatively speciose and the species display morphological variation with respect to feeding. Species relationships within Ambystoma were studied by Shaffer et ah (1991). Only a single genus is recognized for the Dicamptodontidae and the Rhyacotritonidae, and each contains four species. Relationships of the species of Dicamptodontidae are discussed by Good (1988) and of the Rhyacotritonidae by Good and Wake (1992). B. Natural History The vast majority of salamanders either have a terrestrial phase during which they feed on terrestrial prey or are terrestrial throughout life. The Cryptobranchidae, Sirenidae, Proteidae, and Amphiumidae, which are strictly to essentially aquatic, are emphasized in Chapter 3 and will not be discussed here. Together these four families include only about 16 species. Most members of the families Ambystomatidae, Dicamptodontidae, Hynobiidae, and Salamandridae metamorphose from aquatic larvae to terrestrial adults, but some remain aquatic as adults, either in a perennibranchiate (e.g., Ambystoma mexicanum, Dicamptodon copei) or in a fully metamorphosed state. The four species of the Rhyacotritonidae metamorphose, but they remain closely associated with water throughout life. The situ-

ation is complicated in the Plethodontidae, which is the largest family. The Plethodontidae includes the most terrestrial of salamanders, but adults of some taxa are fully aquatic, either perennibranchiate (e.g., Haideotriton, Typhlomolge, and some species of Eurycea and Gyrinophilus) or metamorphosed (e.g., Desmognathus marmoratus). All members of the plethodontid tribes Plethodontini and Bolitoglossini (together accounting for well over 50% of the living species of salamanders) undergo direct development (in encapsulated eggs) and are strictly terrestrial throughout life. A few salamandrids have a stage with larval-like morphology that develops within the oviduct and these, too, are fully terrestrial. Terrestrial salamanders are strict carnivores, and the main prey are arthropods, especially insects (Lynch 1985; Keen 1979; Sites 1978; Kuzmin, 1991). Annelids are eaten by hynobiids (Kuzmin, 1991), ambystomatids (Bishop, 1941), and salamandrids (Roth, 1987). Some large salamanders eat other salamanders (Bishop, 1941; Hairston, 1987) and even such vertebrates as frogs, shrews, mice, lizards, and snakes (Dicamptodon, Bury, 1972; Gyrinophilus, Bishop, 1941). Snails and isopods are widely eaten. C. Feeding M o d e s and Terminology This chapter deals not only with all terrestrial feeding, but also salamanders that use essentially terrestrial mechanisms when feeding under water, such as the desmognathine plethodontids. Prey capture typically is by the tongue, which is extended from the mouth and returns to the buccal cavity with the prey attached, a behavior known as tongue protraction or tongue protrusion. We reserve the term tongue projection for prey-capture mechanisms in which the tongue is fired from the mouth ballistically and reaches the prey under its own momentum, a mechanism known only in bolitoglossine plethodontids. Many terrestrial salamanders have weak jaws and teeth, particularly those that rely primarily on the tongue to bring prey into the buccal cavity. There are, however, species that have robust jaws: Dicamptodon, Ambystoma tigrinum, and some species of Batrachuperus have very large heads and strong jaws as adults, the desmognathine plethodontids have well-ossified skulls, powerful jaws, and unique jaw mechanics (Schwenk and Wake, 1993), and the plethodontid genus Aneides has strong jaws and very large, saber-like teeth (Wake, 1963; Staub, 1993). These species and others that typically use tongue protraction to capture prey will resort to capturing prey with the jaws, in a behavior known as jaw prehension, when the tongue fails to return prey to the mouth.

4. Terrestrial Feeding in Salamanders II. MORPHOLOGY Salamanders have a generalized morphology with a relatively narrow head, well-developed eyes, and a short and broad neck. The head is flattened and is broader than high. The external nares are well separated at the front of a short face. The eyes are at the dorsolateral margin of the face, and head muscles lie behind them. There are varying degrees of eye frontality, but visual fields of the two eyes typically overlap to some degree (Roth, 1987). The mouth opening is large, characteristically extended to a point ventral to the eye. At the margins of the mouth, generally small, bicuspid, pedicellate teeth are found in opposing semicircular rows, one on the premaxillary and maxillary bones and the other on the dentaries. There are also palatal teeth on the vomer in various arrangments and highly varied in number among species; these teeth typically do not parallel the marginal teeth. The tongue is typically large and fleshy, varying among species in the degree to which the margins are attached to surrounding tissues (from completely attached to entirely free). The surface of the tongue is covered with sense organs and the openings of numerous mucous glands, and it is soft and spongy in texture. Internally the tongue has an extensive musculature, including both extrinsic muscles that originate outside the tongue pad and intrinsic muscles that are associated with tongue retraction as well as molding of the tongue pad. General surface morphology of the tongue in relation to the mouth and teeth is illustrated for a variety of species by Bishop (1941) and Lombard and Wake (1977).

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tals and parietals. Prootic and opisthotic bones form the braincase posterolaterally and enclose the inner ear, and the opisthotics are fused with the exoccipitals and bear the occipital condyles. In most families and species there is a single ossification, termed occipitootic. The jaw suspensorium (largely cartilaginous) is attached to the ventrolateral sides of the occipito-otic and is covered dorsally by the squamosal. The distal part of the suspensorium is the ossified quadrate. The lower jaw includes two or three bones: dentary, prearticular (to which jaw muscles attach), and angular (Hynobiidae and Cryptobranchidae) or coronoid (which does not bear teeth in the only metamorphosed salamanders to have this bone, the Dicamptodontidae). Meckel's cartilage is persistent to some degree in all species, and the proximal portion is expanded to form the articular, which articulates with the quadrate. Teeth are generally small, pedicellate, and bicuspid, with a small medial and a larger labial cusp. The marginal teeth are borne on the premaxillary and maxillary bones of the skull and the dentary of the lower jaw. Vomerine teeth are always present, and in salamandrids and plethodontids they extend posteriorly under the parasphenoid bone. In most plethodontids the posterior vomerine teeth are disconnected from the anterior ones and form a pair of large patches of small teeth, often exceeding 100 in number. Some members of the plethodontid genus Aneides have large, unicuspid teeth that apparently are used more in aggressive interactions than for feeding (Staub, 1993). A few small tropical species of the bolitoglossine plethodontids lack maxillary dentition (Wake 1966). 2. HyoUngual Skeleton

A. Skeleton 1, Skull and Jaws Skulls of salamanders are weakly ossified and contain relatively few, thin bones. Premaxillary bones (single or paired) have rising, posteriorly oriented frontal processes that articulate with surrounding bones and provide support (Carroll and Holmes, 1980; see also Chapter 3, Fig. 3.3). Laterally the bones articulate with the much larger maxillary bones. The maxillaries have a frontal process that rises to articulate with surrounding bones (nasal, lacrimal, prefrontal, and frontal, depending on species). The premaxillaries and maxillaries have small, medially projecting, shelf-like processes that articulate with the expanded vomers to form the roof of the buccal cavity. The eyes lie lateral to the brain case, which is formed by a ventral parasphenoid, lateral orbitosphenoids, and dorsal, paired fron-

A hyolingual apparatus (also referred to as a hyobranchial apparatus, particularly in aquatic species) is associated with the tongue in all terrestrial salamanders and it varies substantially among taxa. The elements of the apparatus are cartilaginous to some degree, and in most taxa there is little or no bone, but the apparatus may ossify extensively in others. The general morphology of the hyolingual apparatus is discussed in detail in Chapter 3 (see Figs. 3.4 and 3.6, as well as Figs. 4.2 through 4.4). In metamorphosed salamanders, an elongate basibranchial and a urohyal lie along the ventral midline. The urohyal is continuous with the basibranchial in embryos but the connection is lost before metamorphosis. Unlike the basibranchial, which is usually cartilaginous, the urohyal ossifies early. Paired arches extend posterolaterally and somewhat dorsally from the basibranchial: a hyoid and two branchial arches. The homologies of the arch

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David B. Wake and Stephen M. Deban

Onychodactylus japonicus

Hynobius leechii

Rhyacotriton olympicus

Dicamptodon ensatus

Amhystoma maculatum

Ambystoma texanum

Taricha granulosa

Salamandra salamandra

Chioglossa lusitanica

F I G U R E 4.2. Hyobranchial apparatus of terrestrial salamanders. Ventral views, showing relation of apparatus to lower jaw. Note the radial loops and two pairs of epibranchials in the two hynobiids shown, Onychodactylus japonicus and Hynobius leechii, the otoglossal cartilage in Rhyacotriton olympicus and Ambystoma maculatum, and the lingual plate in Dicamptodon ensatus and forked second radii in Ambystoma texanum. Compare the ossification of Taricha granulosa and the elongate basibranchial, radii, and epibranchials of Chioglossa lusitanica to the more generalized condition in Salamandra salamandra. Bone is stippled and cartilage is outlined. Scale is 5 mm. Abbreviations are explained in Chapter 3, Table 3.1. In some instances, an element has been interrupted or cut on one side to reveal the element dorsal to it. In other instances, the hidden element is indicated by a dotted line.

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elements are debated and terminology varies among authors. All authors use the same terms for the first arch elements: a small hypohyal (proximal; absent in most taxa, possibly fused to the remaining element) and a much larger ceratohyal (distal). The proximal elements of the next two arches are called hypobranchials by some authors and ceratobranchials by others. A serial homologue of the hypohyal would be expected to be short, but this branchial element is characteristically long; the element may well represent both hypobranchial and ceratobranchial or the hypobranchial may be absent (Fig. 4.2). The more distal elements are termed either ceratobranchials or epibranchials. We use the term ceratobranchial for the more proximal of the paired branchial elements and epibranchial for the more distal element. There are only two branchial arches in terrestrial salamanders. Although the two proximal elements are universally present, there may be one (most taxa) or two (hynobiids) epibranchials (Fig. 4.2). When one epibranchial is present, the two ceratobranchials on each side connect to the single epibranchial, either directly or indirectly (in some taxa the second ceratobranchial connects at its distal end to the first ceratobranchial instead of the epibranchial). The articulated hyolingual skeleton of terrestrial salamanders includes the basibranchial, various skeletal pieces connected near its anterior tip (radii, otoglossal, lingual cartilage), and elements of the first two branchial arches. Ceratohyals lack articulations, other than with the hypohyal (when present); they are attached proximally to the suspensorium by the hyoquadrate ligament, and there are quasi-ligamentous connections of the flattened, distal blade to the lower jaw. When present the urohyal is an ossified triangular or crescentic element well separated posteriorly from the other elements and embedded in musculature. Hynobiids have two epibranchials, but all other terrestrial salamanders have one (compare Onychodactylus and Hynobius in Fig. 4.2 to the others). The ceratohyals in hynobiids are continuous with one another across the midline by a slender, looped cartilage (radial cartilage; radial loop of Larsen et ah, 1996) of uncertain homology (but sometimes termed hypohyal, and considered by other authors to represent the first radials) arranged in the form of a flat spring with the loop extending posteriorly and crossing at the midline. At its most posterior limit it may be attached to the basibranchial. The basibranchial in hynobiids is of moderate length in some species but very short in others, whereas it is relatively long in the other taxa. There are two pair of radii in most salamandrids and in the ambystomatids, dicamptodontids, and rhyacotritonids. The last three families also have an unpaired, medial otoglossal associated with the tongue pad. There

Desmognathus monticola

Ensatina eschscholtzii

Gyrinophilus porphyriticus

Plethodon neomexicanus

FIGURE 4.3. Hyobranchial apparatus of semiaquatic and fully terrestrial plethodontid salamanders. Ventral views, showing relation of apparatus to lower jaw. Note the heavy jaw in Desmognathus monticola and the extended jaw and large urohyal in Gyrinophilus porphyriticus. The epibranchials are lengthened in Ensatina eschscholtzii compared to the more generalized Plethodon neomexicanus. Bone is stippled and cartilage is outlined. Scale is 5 mm. Abbreviations are explained in Chapter 3, Table 3.1. In some instances, an element has been interrupted or cut on one side to reveal the element dorsal to it. In other instances, the hidden element is indicated by a dotted line.

is a small interradial cartilage in most salamandrids that may be a homologue of the otoglossal. The first pair of radii has no muscles attached to it; we consider it to be the ontogenetic homologue of the hypohyals, as have other authors (Driiner, 1901). When only one pair

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David B. Wake and Stephen M. Deban

Batrachosevs attenuatus

Thorius narisovalis

F I G U R E 4.4. Hyobranchial apparatus of bolitoglossine plethodontid salamanders. Ventral views, showing relation of apparatus to lower jaw. Note that apparati are entirely cartilaginous. The epibranchials of Hydromantes platycephalus are the longest of any salamander. The small, tapered first ceratobranchial in Thorius narisovalis disarticulates from the basibranchial during tongue protraction. Bone is stippled and cartilage is outlined. Scale is 5 mm. Abbreviations are explained in Chapter 3, Table 3.1. In some instances, an element has been interrupted or cut on one side to reveal the element dorsal to it. In other instances, the hidden element is indicated by a dotted line.

of radii is present, it is the second. Some plethodontids lack radii and in others they are elongate. The most elongate radii occur in the salamandrid genera Salamandrina and Chioglossa (Fig. 4.2). These genera, as well as Salamandra and Mertensiella, have an epibranchial

that results from the fusion of the epibranchial and first ceratobranchial of other genera. The two epibranchials of hynobiids are attached to the ends of the first and second ceratobranchials. In general, differences among taxa with respect to the hyolingual apparatus are

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4. Terrestrial Feeding in Salamanders mainly due to differences in proportions, which in turn reflect functional diversity, for example, differences in the length of the epibranchials among plethodontids (Figs. 4.3 and 4.4). B. Musculature The musculature associated with feeding is derived from the so-called branchiomeric series (Wake, 1993) and the somitic hypobranchial series. Detailed descriptions of muscles common to all salamanders are presented in Chapter 3 (see Chapter 3, Fig. 3.5). Among the branchiomeric derivatives are the jaw levators and depressors and the tongue protractors; the tongue retractors are somitic in origin. The neck is poorly differentiated, but epaxial somitic muscles are involved in raising the skull, and the levator scapulae (most families) and/or cucuUaris (plethodontids) is associated with postural movements of the head. Details of tongue musculature relevant to feeding movements are discussed later in the context of tongue function (Section III,C,l,b). C. Sensory and Motor Systems 1. Vision, Olfaction, and the Brain Terrestrial salamanders locate prey by olfaction and vision, but vision predominates. The olfactory system is well developed but generalized. There is typically a rather elongate snout that houses the paired and cartilaginous olfactory capsules. Within each capsule is a large medial olfactory sac, lined with olfactory epithelium, and a small ventrolateral sac, lined with a specialized sensory epithelium (Dawley and Bass, 1989). The smaller sac is the vomeronasal organ. Plethodontids have a unique organ, the nasolabial groove, associated with each external nostril. The groove lies in the skin of the snout and extends to the margin of the jaw, where typically it opens broadly. In males, tissues associated with the groove swell and elongate during the courtship season (Eurycea) or throughout life (tropical plethodontids). The groove draws surface water into the nasal/vomeronasal sacs and is thought to be important in courtship behavior (Dawley and Bass, 1989), but it may also play a role in feeding. The lateral eyes are large relative to larvae and to permanently aquatic species, and vision is good. The eyes are laterally oriented in species with more generalized terrestrial feeding, but in those species with highly protrusible tongues the eyes become frontally oriented and the animals are able to determine distance of the prey from the head with great accuracy. Visual behavior has been studied extensively, with spe-

cial emphasis on its role in feeding (reviewed in Roth, 1987). The optic nerve projects to the well-developed midbrain, which has an enlarged optic tectum, the main center for the coordination of feeding in salamanders. Projections are both contralateral and ipsilateral, and ipsilateral projections are especially well developed in bolitoglossine plethodontids. The existence of this dual projection system contributes to visual acuity and the ability to accurately estimate distance. 2. Tectobulbar Pathways, Brain Stem, and Innervation Patterns Descending pathways from the optic tectum and tegmentum to the bulbar portion of the brain stem are generalized in salamanders and less clearly differentiated from one another spatially than those of frogs. In sharp contrast with the situation in frogs, there is involvement by more cranial nerves in feeding, and motor nuclei are less condensed and overlap more extensively. As yet there has been little demonstration of interneurons in the reticular formation of the brain stem, and there is some evidence of direct innervation of motor neurons. There are few neurons in the motor nuclei, and their cell bodies are characteristically large (Roth, 1987). The 4th, 5th, 7th, 9th, 10th, and 11th cranial nerves are all involved in feeding, as are the 1st and 2nd spinal nerves. The 4th nerve (abduscens) has well-differentiated lateral and medial subnuclei. The lateral serves extrinsic eye muscles, whereas the medial serves the retractor bulbi, muscles that function in part in aiding in swallowing. The 5th nerve (trigeminal) innervates the jaw levators and anterior constrictors of the buccal cavity, and the 7th nerve (facial) innervates the jaw depressors as well as throat constrictors. The 9th (glossopharyngeal) and 10th (vagal) nerves serve the tongue protractor muscles. The eleventh (accessory) nerve innervates musculature associated with movements of the head on the neck. The 1st and 2nd spinal nerves (which have trunks that unite to form the ramus hypoglossus) innervate the retractor muscles of the tongue, the muscles of the tongue pad, and the strap-like muscles paralleling the body axis that contribute to throat movements and throat stability.

IIL FUNCTION A. Foraging, Prey Detection, and Localization Foraging has been studied in plethodontids by Jaeger and associates (Jaeger and Barnard, 1981; Jaeger

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David B. Wake and Stephen M. Deban

and Gergits, 1979; Jaeger and Rubin, 1982; Jaeger et al, 1982), but only incidentally for other groups (e.g.. Flower, 1927). Terrestrial salamanders forage actively at night under appropriate conditions of temperature and humidity, under suboptimal conditions the animals adopt a sit and wait strategy, remaining in burrows in the soil or other retreats with only the head exposed. Capture of prey by salamanders involves a sequence of activities (Roth, 1987). Orientation is elicited by visual or mechanical stimuli and involves a turning movement of the head, which permits binocular fixation of the prey. The salamander next approaches the prey by walking to a point within reach of the tongue, which varies substantially in length among taxa. If the prey are not evasive, an olfactory test then may take place in which the salamander places its snout directly on the prey. Once within attack distance, binocular fixation of the prey may occur again. Finally, snapping occurs, and in this phase the mouth opens and the tongue seizes the prey, which is drawn into the mouth. Typically, prey capture is by lingual prehension, although forward lunging of the whole body may accompany tongue protraction. Visual aspects of feeding have been studied in detail by Roth and associates (reviewed by Roth, 1987). Species differ greatly in the size of stimuli they prefer, which is correlated with natural food preferences. Species such as the plethodontid Hydromantes, which feed on insects, prefer smaller stimuli than Salamandra, which feeds mainly on worms. Both maximum and minimum size of response stimuli is much smaller in Hydromantes than in Salamandra. Salamandra feeds on prey moving at velocities from 0.5 to about 2 cm/sec, but bolitoglossine plethodontids have been recorded to feed on prey moving from 6 to 10 cm/sec. Motionless prey normally are ignored by terrestrial salamanders. Salamanders typically forage at night and are able to use visual cues at extraordinarily low levels of light (Roth, 1976, Himstedt, 1982). Laboratory experiments demonstrate that they are able to feed visually at illumination levels equivalent to open areas on clouded or rainy nights. Salamanders also feed from olfactory cues in the absence of visual stimuli, as in complete darkness. When light is present, odoriferous dead prey will be ignored for a long time, but if vision is ineffective the food is eaten quickly. Salamanders that live so deep in caves (e.g., Typhlotriton) that there is no light probably use a combination of smell and touch to obtain food. Salamanders have both binocular and monocular depth perception. They do not use lens accommodation, but rather rely on disparities between direct ipsilateral and contralateral retinotectal projections. They

apparently are able to make immediate calculations of depth and feed with great accuracy (Wiggers and Roth, 1991). B. Prey Capture and Ingestion Feeding involves mouth opening/closing, and tongue protraction/retraction. When prey are small relative to the salamander, jaws are not used in feeding, and marginal dentition does not contact prey. However, larger species feeding on larger prey (e.g., members of Dicamptodon and Ambystoma) do use their jaws. The role of vision in feeding is uncertain once the prey is localized. In general, the feeding act is so rapid that once feeding starts relatively little modulation of the strike itself is possible because of delays in response to sensory information (Thexton et al., 1977). Some species close their eyes during the strike, whereas others do not, and this variation occurs even among confamilial species (Roth, 1976; Larsen and Beneski, 1988; Larsen et al, 1989; Miller and Larsen, 1990). In general, those species with the fastest tongues and the greatest degree of protraction are the most likely to keep the eyes open during the feeding cycle. Correspondingly, those that lunge forward strongly during feeding often close their eyes, presumably to protect them. Because prey are out of sight during tongue protraction and lunging, these movements are thought to be preplanned and executed without modification once begun. C. Biomechanics and Functional Morpliology 1. Lingual Feeding a. Kinematics Lingual feeding has been observed in all families of terrestrial salamanders. The published literature is dominated by information concerning ambystomatids, hynobiids, plethodontids and salamandrids, and little information is available for the small families Rhyacotritonidae and Dicamptodontidae. The prey object is first contacted by a protracted tongue pad that is delivered rapidly through a gaping mouth into the buccal cavity. The mode of protraction has been characterized as a lift and thrust mechanism (Beneski et ah, 1995). Both a tongue cycle and a necessarily associated gape or mouth opening and closing cycle can be recognized. These combine to form the basis of a model of a generalized vertebrate feeding cycle, based on the premise that lingual prehension was ancestral in tetrapod feeding (Bramble and Wake, 1985). The four stages, first formally recognized in mammalian feeding (Hiiemae,

4. Terrestrial Feeding in Salamanders 1978), include slow open (SO), fast open (FO), fast close (FC), and slow close-power stroke (SC-PS). Subsequent research on salamanders has recognized patterns generally similar to these four stages. Subtle distinctions have been drawn, however, with some authors continuing to use these designations, some choosing strictly temporal terminology (e.g.. Phases I IV; Larsen and Beneski, 1988), and others choosing new descriptors (e.g., preparatory, fast open, close, recovery; Reilly and Lauder, 1990a). In part, the distinctions are based on the fact that different taxa were studied by different workers. Gape cycles for ambystomatid salamanders using lingual prehension consist of only three parts (lacking a second phase of mouth opening), whereas those of hynobiids, plethodontids and salamandrids generally have the standard fourpart cycle. Plethodontids may show variation in feeding kinematics which complicates the division of the gape cycle into distinct stages (e.g., see Fig. 4.5). The three-part cycle of ambystomatids involves rapid mouth opening, a period of stable positioning of the head during tongue protraction and retraction, and rapid mouth closing (Reilly and Lauder, 1989). The four-part cycle of other taxa includes an initial brief gape phase that opens the mouth only slightly, a second phase during which the mouth is held open just wide enough for tongue protraction, a third phase when gape is increased rapidly during tongue retraction, followed by mouth closure (Larsen and Beneski, 1988). Ambystomatids have modest abilities for tongue protraction, and the gape cycle has been simplified as a result. Beneski et ah (1995) and Larsen et al (1996) characterize the ambystomatid feeding pattern as "lift and roll" in reference to the modest protraction of the tongue in the family and the extensive involvement of tongue pad ventral rolling over the rostral end of the protracted basibranchial and the extensive movement and "fitting" of the tongue pad onto the prey. Members of the other families have varying degrees of tongue protraction, but prey captured by tongue prehension often do not contact the teeth of the jaws. Some species, including even such highly proficient tongue-protracting forms as the plethodontid Ensatina, may use teeth and jaws with relatively large prey. The power stroke of the fourth phase of the generalized vertebrate feeding cycle is modified or absent in salamanders. The extreme degree of reliance on tongue prehension in terrestrial salamanders may account for the departures noted from the general model. Some studies have been conducted on salamandrids feeding without tongue prehension, using only jaws, and these differ from the generalized model in having a two-phase gape cycle: rapid mouth opening followed immediately by rapid mouth closing (Miller and Larsen, 1990). However,

103

these exceptional cases are typically aquatic species feeding on land. The typical strike in salamanders is accompanied by a forward lunge of the entire body toward the prey. This is the ancestral mode and it is widely retained. Lunging effectively increases the strike distance and may also increase the force of the strike. This may be of significance in forcing the tongue pad to conform to the prey surface, thus increasing the area of contact (Larsen et al, 1996). Furthermore, the lunge may continue as tongue retraction occurs so that teeth are quickly brought into contact with the prey item (Larsen et ah, 1996). The lunge is absent in certain taxa that display high-speed tongue protraction, including bolitoglossine plethodontids (Larsen et al., 1989; Roth and Wake, 1985b) and the salamandrid Salamandrina (Miller et al, 1990), and is rarely present in some hemidactyliine plethodontids with long tongues (e.g., Eurycea). b. Protraction Lombard and Wake (1976) studied biomechanics of tongue protraction in plethodontids and presented a theoretical model of folding of the hyobranchial apparatus. The model was based on assumptions dealing with the nature of materials (that the central main elements, the basibranchial and the ceratobranchials, do not bend during protraction or retraction), the stability of joints (there is no disarticulation during protraction and retraction), and other considerations (e.g., the system folds dor sally rather than ventrally). The model was used to formulate hypotheses concerning biomechanical events and was generated with specific reference to plethodontids. Members of this family are sufficiently different from other salamanders in hyobranchial structure that it is unclear if the biomechanical model has generality, but folding occurs to some degree in other taxa as well [e.g., the salamandrid Taricha; Findeis and Bemis (1990) and the hynobiid, Hynobius; Larsen et al (1996)]. Hypotheses generated from the model were tested in various ways. The fundamental part of the model is that the skeletal parts of the tongue are folded into a kind of bundle, formed together with protractor and retractor muscles, other connective tissue, and nerves. This compact unit is protracted from the mouth, to some degree in a ballistic manner, carrying the attached tongue pad at its tip. The cylindrical epithelial sheath surrounding the bundle is heavily pleated when at rest, and as the bundle is protracted it unpleats. The folding of the apparatus is initiated with the contraction of the protractor muscles, the subarcualis rectus I, which originate on the ventral side of the anterior blade-like portion of the ceratohyals and extend to

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Time (ms) F I G U R E 4.5. Kinematic profiles for the bolitoglossine plethodontid salamander Hydromantes platycephalus. The panels are, from top to bottom, tongue reach and gape distance, gape distance, jaw deflections, and head angle, all presented on the same time axis. Gape distance is presented in both the first and the second panels, on different ordinates, to illustrate the vast differences in excursion between the tongue and jaws. This preycapture event was performed with small prey and lacks a distinct second phase of mouth opening, which often occurs during tongue retraction.

4. Terrestrial Feeding in Salamanders form a complex, pimiate muscle wrapped around the tapered epibranchial. The protractor muscles are differentiated in the plethodontids into an anterior, parallel-fibered portion and a distinct, posterior, bulb-like muscle, which is greatly enlarged in relation to that found in members of other families. The hyolingual apparatus contains two triangular units, formed by the medial basibranchial and the ceratobranchials on either side, so in order to form a compact bundle without bending, it folds in three dimensions as it is protracted, moving along a morphological track having the geometrical form of a tractrix. This form has favorable attributes. It appears to act as an accelerator of movement and contributes to the rapidity of protraction. It also acts as a brake for the returning apparatus. The three-dimensional expansion of a tractrix is known geometrically as a bugle body, and it exists, in a limited degree, in the floor of the mouth. The sides of the bugle body are formed by the medial margins of the ceratohyals. The bottom is formed by intermandibularis muscles and the top by a strap-like, unpaired suprapeduncularis muscle (the last muscle unique to the Plethodontidae). The structural element thus formed, called the cylinder by Lombard and Wake (1977), controls the direction of tongue protraction. In species that are most proficient in tongue protraction, members of the plethodontid tribe Bolitoglossini, the cylinder is well formed and incorporates a number of muscles that serve different functions in other taxa. These muscles include the anterior fibers of the subarcualis rectus I, the geniohyoideus medialis, anterior fibers of the rectus cervicis superficialis, and the hebosteoypsiloideus. According to the biomechanical model of Lombard and Wake (1976, 1977) movement of the cylinder from side to side within the mouth is possible. The cylinder appears to rest in the floor of the mouth attached posterolateral^ to the mandible by a slender and poorly defined mandibulohyoid ligament and anteriorly by the geniohyoidius lateralis. Thus there appears to be a kind of "firing platform," and a relatively large contraction of the left geniohyoideus lateralis is hypothesized to direct the tongue toward the right. The biomechanical model also hypothesizes that a mechanical linkage between parts of the hyolingual apparatus accomplishes at least a partial rotation of the tongue pad during protraction. The very action of folding is biomechanically coupled to rotate the tongue pad around the tip of the basibranchial so that the fleshy, mucous-covered pad contacts the prey. A ligament-like bundle of connective tissue extends from the anterolateral part of the first ceratobranchial into the substance of the tongue pad. This fiber bundle extends anteriorly from each side, coalescing at the ventral midline of the anterior tip of the basibranchial and then

105

variously attaching to a flexible tip of the basibranchial, to a detached anterior part of the basibranchial known as the lingual cartilage, or extending dorsally around the tip of the basibranchial and then fanning out posteriorly into the substance of the tongue pad. When the skeleton folds as it is protracted, the fibers become taut and the tongue pad is pulled forward to rotate around the tip of the basibranchial in such a fashion that the sticky dorsal surface is presented to the prey. The cylinder of plethodontids is lined along its inner surface by serous glands, which apparently lubricate the bundle within it during protraction. Protraction can result in the bundle being rapidly propelled forward and can be so great as to result in the skeletal elements, totally evacuating the cylinder as well as the bulb formed by the subarcualis rectus muscles. Momentum of the projectile carries the epibranchial cartilages fully out of the mouth in species of the genus Hydromantes and other bolitoglossine species we have observed. In these taxa the tongue is fired ballistically from the mouth as a projectile (Fig. 4.6; Deban et ah, 1997). Auxiliary protraction mechanisms function in other, nonplethodontid taxa. The subhyoideus connects the posterolateral parts of the ceratohyals to the mandible (see Fig. 3.5B). When these paired muscles contract, the ceratohyals are moved forward as a first stage in tongue protraction. The subarcualis rectus are presumably firing at the same time so the two-stage protraction involves (1) the anterior movement of the ceratohyals carrying with them the entire tongue apparatus, and (2) the independent protraction of the articulated hyobranchial apparatus and attached tongue pad relative to the first segment (Findeis and Bemis, 1990; Miller and Larsen, 1990). This has been termed the "mobile ceratohyal system" by Findeis and Bemis (1990), who contrast it with the other main evolutionary trend involving a "stable ceratohyal system" in plethodontids (which we believe is the ancestral condition). Another auxiliary system found in salamandrids (Chioglossa and Salamandrina) involves the rotation of elongated radii (Fig. 4.2) in an arc around the tip of the strengthened, mineralized basibranchial, which is "T" shaped in cross section (Ozeti and Wake, 1969). This action carries the tongue pad forward, effectively flipping the free posterior flap of the pad well out of the mouth. c. Prehension and the Tongue Pad The tongue pad varies considerably in shape among terrestrial salamanders. In general, it is attached firmly to somewhat loosely at the front, has varying degrees of freedom along the sides, and has the greatest

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D a v i d B. W a k e a n d S t e p h e n M. D e b a n

F I G U R E 4.6. Photograph of Hydromantes genei capturing a housefly, showing projection of the hyoHngual apparatus. The projectile includes the retractor muscle and the bundle of cartilages wrapped in a cylindrical membrane of connective tissue and epithelium. The tongue pad has enveloped the fly, but is not extended so maximal reach for the tongue would be considerably longer than is apparent in this photograph. The epibranchial has left the borders of the mouth. The bends near the distal tip of the projectile indicate the positions of the end of the basibranchial and the epibranchial-ceratobranchial joints.

degree of freedom posteriorly. The posterior part of the tongue may be extended into two limbs that are loose and form relatively long strands during full protraction. This is especially true in some salamandrids and some plethodontids. In two plethodontid clades the tongue has lost its anterior attachment (the genioglossus muscles are absent) and the tongue has a mushroom-like shape. In these species the pad typically becomes relatively small and round; these groups show the greatest distance of tongue protraction. Shaping of the tongue pad may be facilitated by the contraction of muscles inside the tongue pad that arise from the tip of the basibranchial and fan out into the posterior part of the tongue (hyoglossus), extend to the tips of the radii (basiradialis), extend between the tips of the radii (interradialis), or extend from the tips of the radii into the tongue pad (radioglossus). For the plethodontid salamanders, Lombard and Wake (1977) proposed three functional classes of tongue pad muscles: rotators (genioglossus, circumglossus, basiradialis, and intraglossus), molders (interradialis and hyoglossus), and restorers (rectus cervicis profundus). Families differ substantially with respect to relative numbers, sizes, and proportions of skeletal elements and muscles pres-

ent, and the tongue pad varies significantly among taxa; however, this diversity has not been the subject of detailed comparative analysis. The surface of the tongue is rotated by a combination of skeletal and muscular movements so that the glandular dorsal surface covered with relatively sticky mucous contacts the prey. The tongue pad shape is transformed and expanded during protraction so that it is relatively large and expansive when it contacts the prey. In those taxa having an otoglossal cartilage, movement of this element during protraction is postulated to carry the glandular field of the tongue pad dorsoanteriorly so that it contacts the prey (Larsen et ah, 1996). In ambystomatids, the tongue pad is rotated forward as protraction occurs via the connection between the first radii and the hypohyals. The mechanism of tongue protraction in plethodontids is somewhat simplified in relation to the other group that has been studied in detail, the ambystomatids (Reilly and Lauder, 1989, 1990b). In the ambystomatids the ventral throat constrictors (intermandibularis and interhyoideus) and two longitudinal muscles (geniohyoideus and genioglossus) are active during protraction. The constrictors and the geniohyoids are

4. Terrestrial Feeding in Salamanders implicated in provision of a lift vector to the hyolingual apparatus. The subarcualis rectus I provides a separate forward and upward vector, and when well protracted the geniohyoids and genioglossus provide a third forward and ventral vector to the protraction. The combined effect of these three vectors is a resultant horizontal vector that advances the entire hyolingual system, and flipping of the tongue pad is attributed in part to the action of the genioglossus. d. Retraction The articulated hyolingual skeleton has one retractor muscle attached to it at the posterior border of the anterior end of the first ceratobrancial. This is a muscle with several names, but is usually termed the sternohyoideus or the rectus cervicis lateralis (in some taxa the muscle is not well differentiated from the rectus cervicis superficialis). It arises from the sternum and is an anterior continuation of the rectus abdominis series. However, this muscle appears to be a secondary retractor, and the main retractor is a muscle that extends forward under the ventral surface of the hyolingual skeleton and passes through the triangular gap between the first and the second ceratobranchials and the basibranchial. From this position the paired muscles extend forward and then bend abruptly dorsally to enter the tongue pad, where they typically attach to a mass of connective tissue long known by the German term Sehnenplatte ("tendon plate"). This muscle is also known by various names, including the abdominohyoideus and the rectus cervicis profundus. This muscle arises from the lateral margin of the sternum, from a tendinous inscription lateral to the sternum that separates it from the rectus abdominis profundus, or as a direct and continuous anterior extension of the last named muscle, which in extreme cases (Plethodontidae) represents an undivided muscle that arises from the posterior border of the ischium and proceeds uninterrupted into the tongue pad. Retraction of the tongue appears to be exclusively the result of the action of the two different segments of the rectus cervicis series. In the most proficient tongue protractors, the bolitoglossine plethodontids, the rectus cervicis lateralis muscle is absent in two of the three major lineages, and retraction is exclusively by the rectus cervicis profundus. The omohyoideus is also missing in these taxa, and the hebosteoypsiloideus, which is part of the general retractor system in most taxa, is incorporated into a muscular cylinder through which the tongue is folded as it is protracted. e. Speed and Distance of Lingual Feeding The effectiveness of lingual feeding has not been studied in most taxa. As a generalization, species dem-

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onstrating true tongue projectility are the fastest, the most accurate, and have the greatest range. The fastest tongue recorded to date is that of Bolitoglossa occidentalis, which takes less than 10 msec from the start of electrical activity in the subarcualis rectus I muscles to the time the tongue strikes the target. Maximum tongue extension (from tip of snout) has been measured in a number of species. In six species of Ambystoma the largest average distance was 2.4 ± 0.3 mm {A. californiense) and the smallest was 0.3 ± 0.4 mm {A. niabeei){Beneski et al., 1995). Hynobiids can extend their tongues only a few millimeters beyond the tip of the snout, but as much as 7% of snout-vent length (Larsen et al, 1989, 1996). However, Hynobius kimurae was found to protract its tongue 4 - 6 mm beyond the symphisis (J. Larsen, personal communication), and in our laboratory a large (6 to 7 cm snoutvent length) Salamandrella keyserlingii has protracted its tongue 6.6 mm, thus some hynobiids are apparently far more proficient than those reported to date. Salamandrids are apparently the most variable with respect to maximal tongue extension. Pachytriton brevipes, an aquatic species that lacks a defined tongue pad (Ozeti and Wake, 1969), retracts rather than protracts the hyolingual apparatus during terrestrial feeding (Miller and Larsen, 1990), thus in essence performing an aquatic, suction-feeding behavior on land (see Chapter 3 for details of this behavior, including Fig. 3.2). In most species of salamandrids, tongue protraction is relatively short, from 1.1 to 2.7 mm (average extension beyond snout), the latter distance in Tylototriton verrucosus (Miller and Larsen, 1990). Salamandrina terdigitata has a complex tongue protraction involving an initial protraction of the hyolingual apparatus from the mouth and then flipping of the pad (Ozeti and Wake, 1969; Miller and Larsen, 1990). The average maximal tongue extension recorded by Miller and Larsen (1990) for this species is 7.4 mm, or 20% of snout-vent length (4.7 mm is reported in the paper, but a printer's error reversed the digits; J. Larsen, personal communication). Chioglossa lusitanica probably has the longest tongue extension of the salamandrids, based on its morphology (Ozeti and Wake, 1969), but it remains largely unstudied. Maximum tongue extension is variable in plethodontids; distances are about 7% of snoutvent length in species with attached tongues {Desmognathus quadramaculatus and Plethodon glutinosus), about 15% in a species with an attached protrusible tongue {Ensatina eschscholtzii), and 30-44% in Bolitoglossa occidentalis (Thexton et ah, 1977; Larsen et ah, 1989). This species is capable of firing the tongue effectively for at least 17 mm from the head, or as much as 44% of the snout-vent length of the salamander (Thexton et ah, 1977). Hydromantes italicus, a larger species, is reported

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to be capable of capturing prey 40 mm from the head, and the intermediate-sized Bolitoglossa subpalmata can project its tongue 30 mm (Roth, 1987). Adult Hydromantes supramontis can project the tongue accurately to a distance of about 80% of snout-vent length (over 60 mm from the head)(Fig. 4.6; Deban et al, 1997). The prey-capture success rate has been measured in only a few species, but is higher in the proficient tongue protractors than in more generalized species. Salamandra salamandra was successful in only 39% of attempts (Luthardt-Laimer, 1983) compared with above 50% in the generalized plethodontid genera Plethodon, Eurycea, and Batrachoseps. The very long tongued bolitoglossine genera Bolitoglossa and Hydromantes "rarely miss," although no exact figures are available (Roth, 1987). These last two genera may engage in "stalking" in the laboratory to move slowly into range (Roth, 1987; personal observation). The total length of the kinematic cycle is variable among the different taxa studied. The mean gape cycle (in species with tongue protrusion) ranges from 92.8 to 115.7 msec in hynobiids (Larsen et al, 1996), 78 to 214 msec in ambystomatids (Beneski et al, 1995), 100 to 238 in salamandrids (Miller and Larsen, 1990), and 87 to 110 in plethodontids (Larsen et al, 1989; Beneski and Larsen, 1988). Gape cycle time is apparently rather similar across a wide array of morphologies. Speed of the tongue strike (tongue protraction, equivalent to phase II of Beneski and Larsen, 1988) varies greatly among taxa. The fastest tongues are found in Bolitoglossa, which has a mean duration of phase II of 5.0-7.7 msec, with Ensatina at 11.6 msec being only a little slower (although we have measured one individual Ensatina at ca. 7 msec from the time the tongue left the mouth until it touched the prey). Pseudotriton ruber, a hemidactyliine with a free tongue, has a protraction time of as little as 11 msec (Deban, 1997). The plethodontids with attached tongues are slower still: Plethodon glutinosus takes 19.3 msec and Desmognathus quadramaculatus takes 37.3 msec to protract the tongue (Larsen et al, 1989). Roughly comparable times are reported for other taxa (different papers use slightly different methods of reporting). Ambystomatids range from 16 msec for Ambystoma mabeei to 87 msec for Ambystoma cingulatum (Beneski et al, 1995). Maximum tongue protraction in Ambystoma tigrinum is reported by Reilly and Lauder (1989) to take 45 msec, and by Dockx and De Vree (1986) to take 39.6 ± 1 1 . 0 msec. Hynobiids are reported to range from 25.1 msec for Hynobius kimurae to 36.0 msec for H. nebulosus by Larsen et al (1996) [27.4 msec and 36.0 msec for the same species by Larsen et al (1989)]. Among salamandrids, tongue protraction times are reported by Miller and

Larsen (1990) to range from 22.0 msec in Salamandra salamandra to 111.9 msec in Paramesotriton hongkongensis. Dockx and De Vree (1986) report 84 ± 21.7 msec for tongue protraction in Salamandra salamandra, and Findeis and Bemis (1990) report a range of durations from 80 to 140 msec for Taricha torosa. f. Physiology Electromyographic (EMG) investigations of tongue movement (Thexton et al, 1977; Reilly and Lauder, 1990b) in two very different taxa (a bolitoglossine plethodontid with a highly protractible, free tongue and an ambystomatid with a weakly protrusible, attached tongue) show that the protractor (subarcularis rectus I) and the retractor (rectus cervicis) have essentially synchronous onset and similar motor patterns. Because electrical signals are delivered to the protractors and retractors simultaneously, the activity of the system is thought to be controlled by the peripheral organization of the system. The length-tension properties of the protractors favor immediate force generation, whereas those of the much longer (and in terrestrial plethodontids, somewhat lax and even looped) retractors have delayed biomechanical activity. Differences in contractile properties of the two muscles, such as time to peak tension, remain a possibility that is yet unstudied. The similarity in EMG patterns of the two species studied may suggest that motor patterns are phylogenetically conserved. While the electromyographic patterns of larval and metamorphosed ambystomatids suction feeding in water are remarkably similar, they are radically different from those of adults feeding on land (Shaffer and Lauder, 1988; Lauder and Shaffer, 1988). In general, there is little variability detected in experiments, and the motor patterns appear to be highly stereotyped. These facts suggest that changes in the peripheral arrangement of the muscles, skeletal elements, and other connective tissues are critical in determining biomechanical function during feeding. Most of the physiological work has involved ambystomatids (Reilly and Lauder, 1990b). The epaxial muscles connecting the neck to the head and the mandibular depressors are active prior to mouth opening (which involves raising the head slightly to greatly in all species studied) and they remain active until mouth closing. There is a second peak of activity in the epaxial muscles during tongue retraction. The jaw adductors are also active prior to mouth opening, but they have a large burst of activity again as the jaws close. The muscles responsible for tongue protraction (subarcualis rectus) and pad flipping (genioglossus) have peaks of activity during the tongue protraction phase, but unexpectedly the subarcualis rectus muscles have

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4. Terrestrial Feeding in Salamanders a second peak during the retraction phase. Buccal muscles in the floor of the mouth are active throughout the cycle, but tend to peak early and then taper off. The main retractor muscle (rectus cervicis profundus) peaks at the time retraction begins and activity continues until after mouth closing. We take the coactivity of antagonistic muscles as a sign of fine control over tongue and jaw movements and the prolonged activity of the buccal floor muscles as an indication that they are performing a stabilizing function. In Bolitoglossa strain gauges were used to measure force of tongue impact with the prey (Thexton et ah, 1977). At relatively short distances, force varies considerably, probably indicating differences in motivation and concomitant muscle activity level. However, at distances exceeding 10 mm from the snout (animals have a maximal head-body size of about 44 mm), force fell off dramatically as a function of distance from the snout, finally failing to register at the greatest distance (19 mm). This supports the idea that there is a ballistic phase (at the end of muscular protraction) to long-distance tongue projection in the species most proficient in tongue protraction. 2. Jaw Feeding Use of the jaws to capture prey is unusual in terrestrial salamanders, but it does occur, at least in members of the families Ambystomatidae and Salamandridae (Larsen and Guthrie, 1975; Miller and Larsen, 1990). We have also observed it infrequently in various terrestrial species of the Plethodontidae in circumstances when the tongue fails to apprehend the prey. In addition, we have observed the semiaquatic plethodontid Desmognathus quadramaculatus and the hynobiids Salamandrella keyserlingi and Batrachuperus persicus using jaw prehension in water and the fully aquatic plethodontid Desmognathus marmoratus using either tongue or jaw prehension in water (see also Schwenk and Wake, 1993). Kinematics of the gape profile of salamanders using jaw prehension differs from either the generalized four-part or the specialized three-part pattern of other taxa and consists of a bell-shaped, two-part gape profile. The action is relatively rapid (on the order of 60 msec) and resembles that of fully metamorphosed ambystomatids that feed underwater without using tongue protraction (Reilly and Lauder, 1989). While the standard pattern of feeding in salamanders involves participation of the tongue in apprehending the prey, species such as Pachytriton hrevipes, which effectively lacks a tongue pad (Ozeti and Wake, 1969), and other mainly aquatic salamanders feeding on land (Miller and Larsen, 1989) can use jaw prehension, al-

though not very effectively. Jaws are used in aggressive encounters in salamanders (Staub, 1993), and it is evident that biting without tongue protraction is possible. Nonetheless, we expect that salamanders feeding in terrestrial situations typically will display a pattern of feeding that involves tongue prehension (Bramble and Wake, 1985). D . Prey Processing Prey immobilization is significant when the prey are too large to be fully engulfed at the time of capture. Large-bodied salamanders are capable of eating long and slippery (e.g., earthworms in ambystomatids) and even very large prey (e.g., mice in dicamptodontids) relative to body size. In these species, strength of the jaw-closing muscles is important, as well as size and strength of the marginal tooth-bearing bones. The mouth is closed at the end of the strike and if the prey protrudes from the mouth there may be a delay of a few milliseconds to several seconds before processing and/or swallowing proceeds. This process has been most thoroughly studied in ambystomatids and is described later. Dicamptodontids have heads that are the largest of terrestrial salamanders both absolutely and relatively, and they seize (it is not recorded if this is by lingual prehension or jaw prehension) prey such as mice and hold them in the buccal cavity until the prey suffocates before further processing proceeds. Two groups of plethodontids have special prey-processing features. Aneides includes species (e.g., A. lugubris) that have greatly enlarged adductor muscles, jaws and marginal teeth (Wake, 1963). These may well be associated mainly with aggressive behavior (e.g., Staub, 1993), but they also enable these species to eat larger food than co-occurring species of similar size (Lynch, 1985). Desmognathine plethodontids engage in a unique behavior, cranial ventroflexion or head tucking (Dalrymple et al, 1985; Larsen and Beneski, 1988; Schwenk and Wake, 1993), that is enabled by the presence of a number of morphological modifications of the head and neck regions, including a ligamentized tendon extending over either side of the skull from a specialized ridge on the atlas to the lower jaw. This behavior is characteristically performed after lingual capture of the prey and involves a sharp ventroflexion of the head relative to the neck with the prey caught in the jaws. Head tucking may occur as a final component of mouth closing following capture, or without mouth opening, and it represents an extreme form of a static pressure feeding system (Olson, 1961) in salamanders. The result is the penetration of the prey by the teeth and the effective immobilization of the prey. Both Aneides and the

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desmognathines have enlarged quadrapectoralis and an additional muscle (often termed gularis) that contribute to their ability to deliver a strong bite. Prey transport has been studied most extensively in Ambystoma tigrinum (Reilly and Lauder, 1990a, 1991b; Gillis and Lauder, 1994), and only fragmentary information is available for other taxa (Dockx and De Vree, 1986; Thexton et al, 1977). Four phases of intraoral prey transport are recognized in metamorphosed ambystomatids feeding on worms on land (as well as in the water as larvae): preparatory, fast operung, closing, and recovery. Transport per se is accomplished during fast opening and closing. Electromyographic recordings reveal that the preparatory phase involves electrical activity in muscles of the buccal floor (both the longitudinal genioglossus and geniohyoideus, and the transverse intermandibularis and interhyoideus) and then there is a short period of electrical silence before a fast opening of the mouth that is accompanied by simultaneous activity of all muscles studied, even antagonists such as the mandibular depressors and adductors (Reilly and Lauder, 1991b). Reilly and Lauder (1990b) divided the preparatory phase into two parts. In the first part the prey item is pressed against the roof of the mouth by the elevated hyoid apparatus. Gape increases slowly but is never great during phase one. During the second phase, which is shorter in duration, the gape is held constant. Then the fast opening phase occurs, followed quickly by a closing phase, and in each cycle of opening and closing between 4 and 8 mm of prey is transported. Intraoral transport of the prey occurs at the beginning of mouth opening, as the rectus cervicis contract, thus retracting the hyobranchial apparatus and moving the tongue pad (to which the prey is sticking) posteriorly into the pharynx. The muscle that protracts the tongue during prey capture, the subarcualis rectus I, is also active during this time, and Reilly and Lauder (1991a) postulate that it may act antagonistically to the retractors so as to stabilize the interaction of the articulated hyobranchial apparatus and the ceratohyal and to enable the system to function as a whole in aiding the rapid posterior movement of the tongue. There is no inertial component to prey transport. The mouth closes as the prey moves backward. During recovery, hyobranchial protraction carries the tongue forward under the prey, for now the prey is held by the combination of palatal and marginal teeth. The intraoral prey transport system in Ambystoma is very similar during aquatic and terrestrial feeding. However, electromyographic patterns differ between prey capture and transport (reviewed by Lauder and Gillis, 1997). Variation in feeding kinematics is event specific rather than reflecting the environment in

which it occurs (Gillis and Lauder, 1994). Reilly and Lauder (1991) hypothesize that prey transport in terrestrial feeding retains an ancient (extending to fishes) motor pattern associated with suction feeding by larvae. The facts that prey transport behaviors are similar in fishes and salamanders and that they are faster and involve less excursion than prey capture have been used to hypothesize that the prey transport system of terrestrial salamanders may have been directly inherited from the aquatic transport behavior based on suction in aquatic ancestors (Gillis and Lauder, 1994; Lauder and Gillis, 1997). Many salamanders, especially plethodontids but also members of other families, eat small prey that are ingested fully on capture. In these species the marginal dentition does not contact the prey, and transport within the buccal cavity differs from the pattern seen in ambystomatids. Frequently the mouth is not opened again, but evidence shows that the tongue is repositioned and then retracted further, moving the prey into the pharynx. Thexton et al. (1977) recorded two to three bursts of activity in the rectus cervicis muscles following prey capture in the diminutive plethodontid Bolitoglossa occidentalis. This implies that the tongue is being protracted and retracted repeatedly with the mouth closed, and that swallowing follows. E. Modulation of Feeding Behavior Little attention has been given to modulation of feeding behavior under different conditions. Substantial modulation is possible under different circumstances, especially with respect to differences in prey (Deban, 1997; unpublished observations). The species that have been most intensively studied to date are Salamandra salamandra (earlier work reviewed by Roth, 1987; see also Reilly, 1995) and Ensatina eschscholtzii (Deban, 1997); other species studied less intensively include various salamandrids (e.g.. Miller and Larsen, 1990) and plethodontids {Hydromantes italicus, Roth, 1987; Plethodon cinereus, Maglia and Pyles, 1995). The greatest modulation occurs in newts that feed both on land (using tongue protraction) and in the water (using suction feeding) (Miller and Larsen, 1990). Bolitoglossa occidentalis showed little evidence of modulation in early studies (Thexton et al, 1977; Larsen et al, 1989), but our observations show a high degree of modulation of the timing and extent of tongue movements in several species of bolitoglossines. Among ambystomatids, some species (e.g., Ambystoma tigrinum) are apparently highly stereotyped in tongue protraction, whereas others {Ambystoma macrodactylum) show evidence of sonie modulation (Larsen and Guthrie, 1975).

4. Terrestrial Feeding in Salamanders When tested with two distinctly different kinds of prey (waxworms and termites), Ensatina eschscholtzii modulated both the timing and the magnitude of tongue and jaw movements with respect to different prey. When feeding on waxworms, the larger prey, feeding took less time and tongue and jaw movements attained a higher velocity than when feeding on termites (Deban, 1997). In Plethodon cinereus, maximal tongue extension was as great as 17% of snout-vent length when feeding on adult Drosophila (mean 10.4%), but as little as 1% (mean 4.5%) when feeding on larval Drosophila (Maglia and Pyles, 1995). In Ensatina, distance of protraction correlated with distance of the prey from the head, not prey type. In both species, prey capture is completed more quickly on large than on small prey.

IV. DIVERSITY A N D EVOLUTION A. Origins and Outgroups Extant out-group taxa for the order Caudata include the orders Anura and Gymnophiona, both of which differ profoundly with respect to feeding mechanisms from all salamanders. There has been a general consensus that the three orders of living amphibians (Lissamphibia) were derived from a temnospondyl labyrinthodont stock; one widely accepted hypothesis is that lissamphibians might be a sister taxon of the temnospondyl group Dissorophoidea (Bolt, 1977). Another alternative is that lissamphibians are derived from a lepospondylous ancestral stock, perhaps somewhere in the microsaur radiation (Laurin and Reisz, 1996). A further alternative is that lissamphibians do not form a monophyletic group with respect to fossils (Carroll and Holmes 1980). Regardless of phylogenetic considerations, living salamanders have a hyobranchial apparatus that is more generalized in morphology and more similar to known fossils (whether temnospondyls or lepospondyls) than either frogs or caecilians, and we (in accord with Lauder and Reilly, 1994) consider salamanders to be an appropriate model for the first terrestrial feeding system. B. Phylogenetic Diversity Six families of salamanders have species that metamorphose and feed on land: Hynobiidae, Rhyacotritonidae, Dicamptodontidae, Ambystomatidae, Salamandridae, and Plethodontidae. The last three families have been studied in greatest detail with respect to feeding mechanisms and the last two display great diversity.

1.

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Hynobiidae

There is a general consensus that hynobiids are the most basal of the terrestrial taxa of the Caudata (Larson and Dimmick, 1993), and certain features of their feeding mechanism retain apparent ancestral states. The most evident of these is the retention of two branchial arches, with two epibranchials. All other terrestrial salamanders have a single epibranchial, supported by two ceratobranchials. There are, however, indications that hynobiids do not retain the ancestral structure, because they have a unique feature, the radial loop. The ceratohyals are connected to the basibranchial by means of elongated, attenuate hypohyal derivatives arranged in the form of a flat spring (Fig. 4.2). This arrangement is associated with a modest degree of tongue protraction, which occurs with great speed (Larsen et al, 1989,1996; unpublished data). The tongue pad itself has been described as "sac-like" (Larsen et al., 1996) and lacks differentiated musculature, and the basibranchial is extended forward in the radial loop, pulling it along as the hyobranchium is protracted. The extent of protraction is apparently limited by the structural connection of the the hyoid arch to the basibranchial, a connection that exists to a more limited extent in other terrestrial salamanders that do not protract their tongues so far. Tongue protraction is accompanied by a strong forward lunge of the entire body of the salamander, so the effective strike distance is relatively great. Apart from the radial loop, which represents the first radii of other families, the structural arrangement of the tongue in hynobiids is generalized. The second basibranchials are ossified, whereas the first remain cartilaginous, suggesting that the second basibranchials are the main force-transmitting elements from the protractile musculature to the tongue pad. There is a well-developed subhyoideus muscle in hynobiids, and the subarcualis rectus I muscle is wrapped around both first and second epibranchials. These two muscles, working together, serve to protract the hyobranchial apparatus, but functional morphology of the musculature has not been well studied (Severtsov, 1971). A pair of "cornua" are found at the anterior end of the basibranchial in many hynobiids (Cox and Tanner, 1989); these are paired anteriolaterally directed projections continuous with the anterior end of the basibranchial, and they are drawn out into long processes in Onychodactylus (Fig. 4.2). Cornua resemble the radii of plethodontids, but phylogenetic analysis suggests that the resemblance is homoplastic. The hynobiid condition has been proposed to be the most basal salamander feeding mechanism, based on the combination of its morphology and the fact that it

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displays a generalized four-part feeding cycle (Larsen et al, 1996; Beneski et al, 1995). However, the specialized nature of the radial loop precludes the possibility that it retains the ancestral morphology or function entirely. 2.

Rhyacotritonidae

The Rhyacotritonidae has only recently been recognized as a distinct taxon that is relatively basal phylogenetically within the Caudata. Rhyacotritonids have a generalized hyobranchial morphology (Fig. 4.2). The first radii are present but not elongate as in the hynobiids. There is an otoglossal cartilage, an unpaired, dorsal, medial element that either joins the tips of the two second radii or lies freely between them. The articulated elements of the hyolingual skeleton remain cartilaginous, and there is only a single pair of very short epibranchials. The musculature is also generalized. The family resembles the Hynobiidae and the Salamandridae in having a subhyoideus muscle, which may function in a two-phase tongue protraction system. 3.

Dicamptodontidae

The four species comprising this family are large, robust animals, three of which have a terrestrial stage. The tongue is unique and largely unstudied. It combines elements of the tongues of hynobiids, rhyacotritonids, and ambystomatids. The first radii are drawn into an attenuated loop that recalls the situation in hynobiids but is less extreme. The second radii are joined by a thin cartilaginous plate (Fig. 4.2) that appears to be the homologue of the otoglossal cartilage of rhyacotritonids and ambystomatids and supports the relatively enormous tongue pad that is used to capture prey of a wide range of sizes. There is no subhyoideus muscle. The single pair of epibranchials are short and ossified near their proximal ends. 4.

Ambystomatidae

This is a large family of North American salamanders that has been relatively well studied. Both otoglossal cartilages and two pairs of radii are present. However, in contrast to the situation in hynobiids, rhyacotritontids, and dicamptodontids, the first radii are neither attenuate nor drawn into a radial loop that is continuous with the hyoid arch, but their distal tips are loosely connected to the free anterior ends of the ceratohyals. The second radii may be forked and elongate in the subgenus Linguaelapsis (Fig. 4.2). Ambystomatids lack a subhyoideus muscle. They have a muscle termed the genioglossus lateralis that lies in the same general area as the subhyoideus but that has an entirely different origin and innervation

(Piatt, 1940). This muscle may be used to move the ceratohyals medially, thus orienting the tongue. 5.

Salantandridae

Basal salamandrids have two pairs of radii. The first radii are typically rather short and tapered, with free distal ends. The first radii are apparently lacking in Salamandrina and Chioglossa, in which the second radii have moved to the distal tip of the basibranchial and rotate around it as the tongue pad is flipped. The radii are moderately long and robust in Salamandrina, but very long and attenuate in Chioglossa (Fig. 4.2). In both genera the basibranchial is stout and is the only part of the articulated hyobranchial apparatus that is mineralized. In Salamandrina it is T shaped in cross section. In other salamandrid genera the second radii are located behind the first radii, and an interradial cartilage (possibly a homologue of the otoglossal of other taxa) extends between them. Tongue pad musculature is relatively complicated in the Salamandridae, and several muscles occur that are not found in other families (e.g., radioglossus) whereas others are larger than in other families (e.g., basiradialis). The most complicated tongue pad is found in Salamandrina, in which tongue pad flipping is thought to be accomplished by rapid rotation of the radii by the basiradialis muscles (Ozeti and Wake, 1969). Salamandrid genera were divided into two functional groups based on tongue structure and use of the tongue in feeding by Ozeti and Wake (1969). Most genera have a "water tongue" and they have been known as "Wassermolchen" in the German literature (Wolterstorff and Herre, 1935). In these genera the hyolingual apparatus is used for suction feeding in the water and for tongue prehension on land. Characteristically the skeleton of the hyolingual apparatus is relatively heavy and well ossified. At least one genus, Pachytriton, is permanently aquatic, has no tongue prehension ability, and has a very reduced tongue pad. Paradoxically, Pachytriton has a terrestrial eft stage (common in other newts) in which tongue prehension likely occurs (Thiesmeier and Hornberg, 1997), prior to the return as an adult to a permanently aquatic existence in which tongue prehension is impossible. The most terrestrial salamandrids, Salamandra, Mertensiella, Chioglossa, and Salamandrina, have "land tongues." They either do not enter water or feed in water using terrestrial behaviors and they have specialized tongues used for prehension of prey. Typically the hyolingual apparatus is either entirely cartilaginous or only the basibranchial is ossified. A significant part of tongue protraction in Chioglossa and Salamandrina is accomplished by flipping and extension of the large tongue pad (Miller and Larsen, 1990).

4. Terrestrial Feeding in Salamanders Salamandrids have a subhyoideus muscle (see Fig. 3.5 in Chapter 3) that is used to protract the ceratohyals and the tongue in general (Findeis and Bemis, 1990). Some salamandrids have some lateral muscle fibers arising near the genioglossus (e.g., Ozeti and Wake, 1969), and these may be homologues either of the genioglossus lateralis of ambystomatids or possibly the geniohyoideus lateralis of plethodontids. 6.

Plethodontidae

Otoglossals are absent in the Plethodontidae, and some taxa have a medial unpaired "lingual cartilage'' (Fig. 4.4). Rose (1996) has shown that the lingual cartilage may have some connection with the hypohyals of experimental animals treated with thyroxin. Wake (1966) argued that the ,cartilage is derived from the anterior extension of the basibranchial that lies in front of the attachment of the radii. Out-group taxa that have an anterior extension also have either a pair of first radii attached to it or bear a pair of cornua. It is possible that the anterior extension represents the fusion of the lingual cartilage to the basibranchial; perhaps the lingual cartilage should be considered a homologue of a long missing basihyal. The first radii of out-group taxa that have two pairs of radii lack muscular attachments, and because the single radii of plethodontids have muscular attachments they are best considered to be homologues of the second radii of other taxa. An alternative interpretation is that the radii of plethodontids may be homologues of the cornua of hynobiids, because in many plethodontids the radii are homocontinuous with the cartilage of the basibranchial, although in others they are articulated with the basibranchial, as are the second radii in members of other families. If, as argued earlier, the first radii represent hypohyals of out-group taxa, the lingual cartilage represents the basihyal, the distal (with respect to distance from the midline) element found in rhyacotritonids represents the epihyal, and portions of the middle ear complex are derived from the arch as well, all components of the entire hyoid arch are present in the Caudata, but not in any single taxon. There is no subhyoideus muscle in plethodontids. A well-developed geniohyoideus lateralis may play an important role in controlling lateral to medial movements of the ceratohyal and thus direct the firing of the tongue, but this has not been demonstrated behaviorally (Lombard and Wake, 1977). Feeding mechanisms in plethodontids have been studied extensively, and summary discussions of feeding in a phylogenetic context accompanied by evolutionary scenarios are presented by Roth and Wake (1985b), Lombard and Wake (1986), and Wake and Larson (1987). Phylogenetic analyses (Jackman et ah, 1997)

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support the hypothesis (Wake, 1966; Lombard and Wake, 1986) that the freely projectile tongues of the supergenera Hydrotnantes and Bolitoglossa are derived independently. Both are derived independently of the even more phylogenetically remote members of the tribe Hemidactyliini, which also have evolved freely projectile tongues. Thus, within the Plethodontidae there are three lineages that have evolved highly specialized tongue projection mechanisms. The hemidactyliine tongue is folded according to one of two hypothetical possibilities (Lombard and Wake, 1976, 1977), called option 1. This folding pattern involves holding the first ceratobranchial and epibranchial coplanar during folding. It results in a relatively bulky projectile that is postulated to have more limited projectability than is involved in option 2 (Wake, 1982). This option has been hypothesized as a necessary consequence of the retention of an aquatic larval stage and associated larval suction feeding in hemidactyliines (Wake, 1982). In contrast, bolitoglossines, which all have direct terrestrial development and no aquatic larval stage, all use option 2 folding, in which the second ceratobranchial and the epibranchial are held coplanar. This option results in a slenderer projectile that is less limited in length than in hemidactyliines. There are two modifications of the option, that of Hydrotnantes, which has apparently optimized for distance by having evolved extremely long epibranchials, and that of the supergenus Bolitoglossa, which also has elongated epibranchials but substantially shorter than in Hydromantes, and is apparently optimized for speed (Larsen et ah, 1989). C. Feeding Biology and Evolution 1. Ecology and Selective Regime The evolution of terrestrial feeding in salamanders has proceeded in a great diversity of habitats and microhabitats, and in the absence of information about close sister taxa of Caudata it is impossible to reconstruct the habitat occupied by the first terrestrial feeders. However, it seems likely that early salamanders had a biphasic life cycle, involving feeding in water and on land, and that courtship and mating probably occurred in the water. Accordingly, feeding most likely entailed suction feeding both as larvae and as adults, and tongue protraction, apprehension, and capture on land. The most specialized terrestrial feeding mechanisms tend to be associated with species that do not spend much time in the water, or that are entirely terrestrial. The exception to this generalization is the family Hynobiidae, in which species with aquatic larvae and semiaquatic habits as adults have a hyolingual system that is fast and biomechanically specialized (e.g..

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Larsen et al, 1996). In the hemidactyhine plethodontids and in salamandrids such as Chioglossa and Salamandrina, tongues are also highly specialized for speed and distance of protraction, and these forms all have aquatic larvae. However, all are lungless or have reduced lungs, and this appears to be a necessary, but not sufficient, precondition for the high specialization of the tongue (Roth and Wake, 1985b). Rhyacotritonids, whose tongue and feeding are relatively unstudied but which have a generalized morphology, also have reduced lungs. The greatest specialization in tongue speed and protrusion is foimd in the bolitoglossine plethodontids, all of which lack an aquatic larval stage. These species have diverged far beyond the ancestral home of not only salamanders as a group but of plethodontids, and occur in a great diversity of terrestrial habitats and microhabitats, including waterless caves, cavities in trees, epiphytes, scrublands, and other settings in which foraging is restricted by environmental considerations. Whatever the environment in which tongue specialization evolved, it is a highly effective feeding strategy. 2.

Homoplasy

Homoplasy is common in the evolution of terrestrial feeding mechanisms of urodeles and has been discussed extensively (e.g.. Wake, 1966, 1982; Lombard and Wake, 1986). What has attracted the greatest attention is tongue protrusion. While some degree of tongue protrusion occurs in all salamanders that metamorphose and have a terrestrial feeding stage, longdistance tongue protrusion has evolved independently along very different biomechanical pathways within at least three families (Hynobiidae, Salamandridae, and Plethodontidae). In hynobiids, tongue protrusion is associated with modest increases in length of the two pairs of epibranchials and with the flat spring arrangement of the hyoid loop, which is attached to the articulated lingual skeleton in some way. However, the basibranchial remains short. Paired, relatively elongate cornua appear in Onychodactylus (Fig. 4.2), and while these may represent retained ancestral elements homologous to the second radii of other taxa, phylogenetic analysis suggests homoplasy. Tongue protrusion is never as great as in the other two families, but the tongue is fast and maneuverable. Larsen et al (1996) argue that the radial loops and the attachment of the ceratohyals to the suspensorium constitute a functional constraint that mechanically limits the extent of tongue protrusion. Wntiether there has been homoplasy within the Hynobiidae awaits a modem phylogenetic analysis of the family and further morphological studies.

V. OPPORTUNITIES FOR FUTURE RESEARCH Research effort has been unevenly distributed with respect to salamander clades. Biomechanical models of tongue protraction have been produced and tested for plethodontids and ambystomatids, but are largely lacking for other taxa. Detailed morphological studies date to the early part of this century and do not include several families, including Dicamptodontidae, Hynobiidae, and Rhyacotritonidae. However, comparative anatomical studies of some of the larger families, including Ambystomatidae, Plethodontidae, and Salamandridae, are relatively complete. What is needed is a broad and integrated comparative anatomical analysis of the musculoskeletal system of all the families, with special attention given to the establishment of homologies. Quantitative studies of kinematics are limited to only a few species and in general have been conducted in artificially controlled conditions and with limited, sometimes unnatural, prey. The modulation of behavior has been investigated in only a handful of species, even though most species feed on a diversity of prey and under a variety of conditions. Diet and foraging are in need of further study in most taxa. Two families, the Dicamptodontidae and the Rhyacotritonidae, have been especially understudied with respect to kinematics. References Beneski, J. T., Jr., and J. H. Larsen, Jr. (1989) Interspecific, ontogenetic, and life history variation in the tooth morphology of mole salamanders (Amphibia, Urodela, and Ambystomatidae). J. Morph. 199(1): 53-70. Beneski, J. T., Jr., J. H. Larsen, Jr. and B. T. Miller (1989) Ontogenetic alterations in the gross tooth morphology of Dicamptodon and Rhyacotriton (Amphibia, Urodela, and Dicamptodontidae). J. Morph. 199(2): 165-174. Beneski, J. T, Jr., and J. H. Larsen, Jr. (1995) Variation in the feeding kinematics of mole salamanders (Ambystomatidae: Ambystoma). Can. J. Zool. 73:353-366. Bishop, S. C. (1941) The salamanders of New York. New York State Mus. Bull. No. 324:1-365. Bolt, J.R. (1977) Dissorophoid relationships and ontogeny, and the origin of the Lissamphibia. J. Paleo. 51:235-239. Bramble, D. M., and D. B. Wake (1985) Feeding mechanisms in lower tetrapods. Pp. 230-261. In: Functional Vertebrate Morphology. M. Hildebrand, D. M. Bramble, K. E Liem, and D. B. Wake (eds.). Harvard Univ. Press, Cambridge, MA. Bury, R. B. (1972) Small mammals and other prey in the diet of the Pacific Giant Salamander (Dicamptodon ensatus). Am. Midi. Nat. 87:524-525. Carroll, R. L. and R. Holmes (1980) The skull and jaw musculature as guides to the ancestry of salamanders. Zool. J. Linn. Soc. 68:1-40. Dalrymple, G. H., J. E. Juterbock, and A. L. La Valley (1985) Function

4. Terrestrial F e e d i n g in S a l a m a n d e r s of the atlanto-mandibular ligaments of desmognathine salamanders. Copeia 1985:254-257. Dawley, E. M., and A. H. Bass (1989) Chemical access to the vomeronasal organs of a plethodontid salamander. J. Morph. 200: 163-174. Deban, S. M. (1997) Modulation of prey-capture behavior in the plethodontid salamander Ensatina eschscholtzii. J. Exp. Biol. 200: 1951-1964. Deban, S. M., D. B. Wake, and G. Roth 1997. Salamander with a ballistic tongue. Nature 389:27-28. Dockx, P., and F. De Vree (1986) Prey capture and intra-oral food transport in terrestrial salamanders. Stud. Herpetol. 521-524. Driiner, L. (1901) Studien zur Anatomie des Zungebein-, Kiemenbogen- und Kehlkopfmuskeln der Urodelen. I. Theil. Zool. Jahrb. Abteil. Anat. 15:435-622. Findeis, E. K., and W. E. Bemis (1990) Functional morphology of tongue projection in Taricha torosa (Urodela: Salamandridae). Zool. J. Linn. Soc. 99:129-157. Flower, S. S. (1927) Loss of memory accompanying metamorphosis in amphibians. Proc. Zool. Soc. Lond. 1:155-156. Francis, E. B. T. (1934) The Anatomy of the Salamander. Clarendon Press, Oxford. Good, D. A. (1988) Hybridization and cryptic species in Dicamptodon (Caudata: Dicamptodontidae). Evolution 43:728-744. Good, D. A., and D. B. Wake (1992) Geographic variation and speciation in the torrent salamanders of the genus Rhyacotriton (Caudata, Rhyacotritonidae). Univ. Calif. Publ. Zool. 126:1-91. Hairston, N. G., Sr. (1987) Community Ecology and Salamander Guilds. Cambridge Univ. Press, Cambridge. Hiiemae, K. M. (1978) Mammalian mastication: a review of the activity of the jaw muscles and the movements they produce in chewing. Pp. 359-398. In: Develoment, Function and Evolution of Teeth. P. M. Butler and K. A. Joysey (eds.). Academic Press, New York. Himstedt, W. (1982) Prey selection in salamanders. Pp. 47-66. In: Analysis of Visual Behavior. D. Ingle, M. A. Goodale, and R. J. W. Mansfield (eds.). MIT Press, Cambridge, MA. Jaeger, R. G., and D. E. Barnard (1981) Foraging tactics of a terrestrial salamander: choice of diet in structurally simple environments. Am. Nat. 117:639-664. Jaeger, R. G., D. E. Barnard, and R. G. Joseph (1982) Foraging tactics of a terrestrial salamander: assessing prey density. Am. Nat. 119: 885-890. Jaeger, R. G., and A. M. Rubin (1982) Foraging tactics of a terrestrial salamander: judging prey profitability. J. Anim. Ecol. 51:167-176. Keen, W. H. (1979) Feeding and activity patterns in the salamander Desmognathus ochrophaeus (Amphibia, Urodela, Plethodontidae). J. Herp. 13:461-467. Kuzmin, S. L. (1991) Feeding of the salamander Ranodon sibiricus. Alytes 9:135-143. Larsen, J. H., Jr., and J. T. Beneski, Jr. (1988) Quantitative analysis of feeding kinematics in dusky salamanders (Desmognathus). Can. J. Zool. 66:1309-1317. Larsen, J. H., Jr., J. T. Beneski, Jr., and B. T Miller (1996) Structure and function of the hyolingual system in Hynobius and its bearing on the evolution of prey capture in terrestrial salamanders. J. Morph. 227:235-248. Larsen, J. H., Jr., J. T Beneski, Jr., and D. B. Wake (1989) Hyolingual feeding systems of the plethodontidae: comparative kinematics of prey capture by salamanders with free and attached tongues. J. Exp. Zool. 252:25-33. Larsen, J. H., Jr., and D. J. Guthrie (1975) The feeding system of terrestrial tiger salamanders (Amhystoma tigrinum melanostictum Baird). J. Morph. 147:137-154.

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Larson, A. (1991) A molecular perspective on the evolutionary relationships of the salamander families. Evol. Biol. 25:211-277. Larson, A., and A. C. Wilson (1989) Patterns of ribosomal RNA evolution in salamanders. Mol. Biol. Evol. 6:131-154. Larson, A., and W. W. Dimmick (1993) Phylogenetic relationships of the salamander families: an analysis of congruence among morphological and molecular characters. Herp. Monogr. 7:77-93. Lauder, G. V., and S. M. Reilly (1994) Amphibian feeding behavior: comparative biomechanics and evolution. Adv. Comp. Environ. Physiol. 18:163-195. Lauder, G. V., and H. B. Shaffer (1985) Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders. J. Morph. 185:297-326. Lauder, G. V., and H. B. Shaffer (1988) Ontogeny of functional design in tiger salamanders {Amhystoma tigrinum): are motor patterns conserved during major morphological transformations? J. Morph. 197:249-268. Laurin, M., and R. R. Reisz (1997) A new perspective on tetrapod phylogeny. Pp. 9-59. In: Amniote Origins: Completing the Transition to Land. S. S. Sumida and K. L. M. Martin (eds.). Academic Press, San Diego. Lombard, R. E., and D. B. Wake (1976) Tongue evolution in the lungless salamanders, family Plethodontidae. I. Introduction, theory and a general model of dynamics. J. Morph. 148:265-286. Lombard, R. E., and D. B. Wake (1977) Tongue evolution in the lungless salamanders, family Plethodontidae. II. Function and evolutionary diversity. J. Morph. 153:39-80. Lombard, R. E., and D. B. Wake (1986) Tongue evolution in the lungless salamanders, family Plethodontidae. IV. Phylogeny of plethodontid salamanders and the evolution of feeding dynamics. Syst.Zool.35(4):532-551. Luthardt-Laimer, G. (1983) Distance estimation in binocular and monocular salamanders. Zeit. Tierpsychol. 63:233-240. Luthardt-Laimer, G., and G. Roth (1983) Reduction of visual ir\hibition to stationary prey by early experience in Salamandra salamandra (L.). Z. Tierpsychol. 63:294-302. Lynch, J. F. (1985) The feeding ecology of Aneides flavipunctatus and sympatric plethodontid salamanders in northwestern California. J. Herp. 19:328-352. Maglia, A. M., and R. A. Pyles (1995) Modulation of prey-capture behavior in Plethodon cinereus (Green) (Amphibia: Caudata). J. Exp. Zool. 272:167-183. Maiorana, V. (1978) Behavior of an unobservable species: diet selection by salamander. Copeia 1978(4): 664-672. Miller, B. T, and J. H. Larsen, Jr. (1990) Comparative kinematics of terrestrial prey capture in salamanders and newts (Amphibia: Urodela: Salamandridae). J. Exp. Zool. 256:135-153. Olson, E. C. (1961) Jaw mechanisms: rhipidistians, amphibians, reptiles. Am. Zool. 1:205-215. Ozeti, N., and D. B. Wake (1969) The morphology and evolution of the tongue and associated structures in salamanders and newts (family Salamandridae). Copeia 1969:91-123. Reilly, S. M. (1995) The ontogeny of aquatic feeding behavior in Salamandra salamandra: stereotypy and isometry in feeding kinematics. J. Exp. Biol. 198:701-708. Reilly, S. M., and G. V. Lauder (1988) Atavisms and the homology of hyobranchial elements in lower vertebrates. J. Morph. 195:237245. Reilly, S. M., and G. V. Lauder (1989) Physiological bases of feeding behavior in salamanders: do motor patterns vary with prey type? J. Exp. Biol. 141:343-358. Reilly, S. M., and G. V. Lauder (1990a) The evolution of tetrapod feeding behavior: kinematic homologies in prey transport. Evolution 44:1542-1557.

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Reilly, S. M., and G. V. Lauder (1990b) The strike of the tiger salamander: quantitative electromyography and muscle function during prey capture. J. Comp. Physiol. A 167:827-839. Reilly, S. M., and G. V. Lauder (1991a) Experimental morphology of the feeding mechanism in salamanders. J. Morph. 210:33-44. Reilly, S. M., and G. V. Lauder (1991b) Prey transport in the tiger salamander: quantitative electromyography and muscle function in tetrapods. J. Exp. Zool. 260:1-17. Rose, C. S. (1996) An endocrine-based model for developmental and morphogenetic diversification in metamorphic and paedomorphic urodeles. J. Zool. Lond. 239:253-284. Roth, G. (1976) Experimental analysis of the prey catching behavior of Hydromantes italicus Dunn (Amphibia, Plethodontidae). J. Comp. Physiol. 109:47-58. Roth, G. (1987) Visual Behavior in Salamanders. Springer-Verlag, Heidelberg. Roth, G., K. Nishikawa, U. Dicke, and D. B. Wake (1988) Topography and cytoarchitecture of the motor nuclei in the brainstem of salamanders. J. Comp. Neurol. 278:181-194. Roth, G., K. C. Nishikawa, D. B. Wake, U. Dicke, and T. Matsushima (1990) Mechanics and neuromorphology of feeding in amphibians. Neth. J. Zool. 40:115-135. Roth, G., and D. B. Wake (1985a) The structure of the brainstem and cervical spinal cord in relation to feeding of lungless salamanders, family Plethodontidae. J. Comp. Neurol. 241:99-110. Roth, G., and D. B. Wake (1985b) Trends in the functional morphology and sensorimotor control of feeding behavior in salamanders: an example of the role of internal dynamics in evolution. Acta Biotheor. 34:175-192. Roth, G., and D. B. Wake (1989) Conservatism and innovation in the evolution of feeding in vertebrates. Pp. 7-21. In: Complex Organismal Functions: Integration and Evolution in Vertebrates. D. B. Wake and G. Roth (eds.). Wiley, Chichester. Schwenk, K., and D. B. Wake (1993) Prey processing in Leurognathus marmoratus and the evolution of form and function in desmognathine salamanders (Plethodontidae). Biol. J. Linn. Soc. 49:141162. Severtsov, A. S. (1971) The mechanism of food capture in tailed amphibians. Doklady Akademii Nauk SSSR 197:728-731. Sites, J. W. (1978) The foraging strategy of the dusky salamander, Desmognathus fuscus (Amphibia, Urodela, Plethodontidae): an empirical approach to predatiion theory. J. Herp. 12:373-383. Shaffer, H. B. and G. V. Lauder (1988) The ontogeny of functional design: metamorphosis of feeding behaviour in the tiger salamander (Amhystoma tigrinum). J. Zool. London 216:437-454. Shaffer, H. B., J. M. Clark, and R Kraus (1991) When molecules and morphology clash: a phylogenetic analysis of the North American

ambystomatid (Caudata: Ambystomatidae) salamanders. Syst. Zool. 40:284-303. Thexton, A. J., D. B. Wake, and M. H. Wake (1977) Tongue function in the salamander Bolitoglossa occidentalis. Arch. Oral Biol. 22: 361-366. Thiesmeier, B., and C. Romberg (1997) Paarung, Fortpflanzung und Larvalentwicklung von Pachytriton sp. {Pachytriton A) nebst Bemerkungen zur Taxonomie der Gattung. Salamandra 33:97-110. Titus, T. A., and A. Larson (1995) A molecular phylogenetic perspective on the evolutionary radiation of the salamander family Salamandridae. Syst. Biol. 44:125-151. Trueb, L., and R. Cloutier (1991) A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). Pp. 223-313. In: Origins of the Higher Groups of Tetrapods: Controversy and Consensus. H.-P. Schultze and L. Trueb (eds.). Comstock Publ. Assoc, Ithaca. Wake, D. B. (1963) Comparative osteology of the plethodontid salamander genus Aneides. J. Morph. 113:77-118. Wake, D. B. (1966) Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Mem. Southern Calif. Acad. Sci. 4:1-111. Wake, D. B. (1982) Functional and developmental constraints and opportunities in the evolution of feeding systems in urodeles. Pp. 51-66. In: Environmental Adaptation and Evolution. D. Mossakowski and G. Roth (eds.). Gustav Fischer, Stuttgart. Wake, D. B. (1991) Homoplasy: the result of natural selection, or evidence of design limitations? Am. Nat. 138(3): 543-567. Wake, D.B. (1993) Brainstem organization and branchiomeric nerves. Acta Anat. 148:124-131. Wake, D. B., and A. Larson (1987) Multidimensional analysis of an evolving lineage. Science 238:42-48. Wake, D. B., and J. Hanken (1996) Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40:859-869. Wake, D. B., K. C. Nishikawa, U. Dicke, and G. Roth (1988) Organization of the motor nuclei in the cervical spinal cord of salamanders. J. Comp. Neurol. 278:195-208. Wiggers, W., and G. Roth (1991) Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae. J. Comp. Physiol. A 169:165-176. Wolterstorff, W., and W. Herre (1935) Die Gattungen der Wassermolche der Familie Salamandridae. Arch. Naturgesch. N.F. 4: 217-229. Zhao, E., and Q. Hu (1988) Studies on Chinese tailed amphibians. English translation. Pp. 1-44. In: Studies on Chinese Salamanders. E. Shao, Q. Hu, Y. Jiang, and Y. Yang (eds.). Society for the Study of Amphibians and Reptiles, Miami, OH.

C H A P T E R

5 Feeding in Frogs KIISA C NISHIKAWA Department of Biological Sciences Northern Arizona University Flagstaff, Arizona 86011

animals. One aspect of this goal is to compare the function of the feeding apparatus across the major clades of tetrapod vertebrates. For each clade, the function of the feeding apparatus can be addressed by asking the following questions: (1) Which muscles are involved in producing feeding movements and v^hat is the specific contribution of each? (2) What are the spatial and temporal patterns of muscle activation and how do they relate to movement? and (3) What are the neural mechanisms that are responsible for producing observed patterns of muscle activity? Since the early 1990s, my research has focused on understanding the evolutionary relationships among morphology, biomechanics, and neural control of movement using prey capture of anurans as a model system. This chapter provides a summary of this work and a historical perspective on hypotheses concerning the mechanisms of anuran prey capture. The chapter begins by briefly reviewing the phylogeny and natural history of anurans (Section I). Subsequent sections describe the morphology (Section II) and function (Section III) of the anuran feeding apparatus, the neural control of prey capture movements (Section IV), and the evolution of mechanisms of tongue protraction and neural control of prey capture (Section V). The chapter ends with a summary of conclusions and a description of current and future directions. It is hoped that by describing the pitfalls that have been encountered in attempting to understand the mechanisms of prey capture in frogs, this chapter will help future workers avoid similar problems in the future. It is also hoped that our attempts to understand the biomechanics and neural control of prey capture in frogs will stimulate functional morphologists to undertake similar studies

I. INTRODUCTION A. Phylogeny of Anurans B. Natural History of Anurans II MORPHOLOGY OF THE FEEDING APPARATUS A. Craniun\ and Jaw Muscles B. Mandible and Buccal Floor Muscles C. Hyoid and Associated Muscles D.Tongue and Associated Muscles III. FUNCTION OF THE FEEDING APPARATUS A. Methods for Studying the Function of the Feeding Apparatus B. Hypotheses for the Mechanism of Tongue Protraction C. Functional Diversification among Anuran Taxa IV. NEURAL CONTROL OF PREY CAPTURE A. Visual Analysis of Prey Features B. Role of Tongue Afferents C. Interactions between Tongue Afferents and Visual Input V. EVOLUTION OF THE FEEDING APPARATUS A. Evolutionary Transitions in Mechanisms of Tongue Protraction B. Morphological Correlates of Tongue Protraction Mechanisms C. Evolution of Tongue Afferents D. Evolutionary Transitions in Mechanisms of Neural Control VI. CONCLUSIONS VII. CURRENT AND FUTURE DIRECTIONS References

I. INTRODUCTION A major goal of functional morphology is to understand the evolution of functional differences among

FEEDING (K.SchwenKed.)

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in other groups of animals so that the generality of our results can be tested in other groups.

Ascaphidae Leiopelmatidae Bombinatoridae

A. Phylogeny of Anurans On superficial examination, frogs appear to be a morphologically homogeneous group. They are easily distinguished from other amphibians by their welldeveloped hind legs and the absence of a tail in adults. Frogs are, however, quite diverse morphologically, particularly in terms of their feeding apparatus, which has played an important role in anuran classification schemes for more than a century (Giinther, 1859; Griffiths, 1963). Recent workers recognize 21-27 families of frogs (Duellman and Trueb, 1986; Ford and Cannatella, 1993). A number of phylogenetic hypotheses have been published for the anuran families, based on morphological (e.g.. Ford and Cannatella, 1993) or genetic characters (e.g., Hillis et al, 1993; Hay et al, 1995). In these studies, the relationships of some anuran families are agreed upon generally, but relationships of the majority of families remain to be resolved definitively (Hillis efflZ., 1993). This chapter uses a recent phylogenetic hypothesis of anuran familial relationships (Fig. 5.1) that was developed using morphological characters by Ford and Cannatella (1993). In this hypothesis, the "archaeobatrachian" families (Ascaphidae, Leiopelmatidae, Bombinatoridae, and Discoglossidae) represent the most basal lineages of frogs. These families share many ancestral morphological characteristics, but are not closely related to each other and do not constitute a monophyletic group (Ford and Cannatella, 1993). On the basis of genetic characters, however. Hay et ah (1995) concluded that the Archaeobatrachia may, in fact, be monophyletic. In Ford and Cannatella's (1993) phylogeny, the Mesobatrachia (Fig. 5.1) is a monophyletic group that includes two lineages: the pelobatoids (families Pelobatidae, Pelodytidae, and Megophryidae) and pipoids (families Pipidae and Rhinophrynidae). The remaining families are placed in the clade Neobatrachia. Within the Neobatrachia, the families Hylidae, Centrolenidae, and Pseudidae appear to form a clade, as do the ranoids (families Ranidae, Arthroleptidae, Hyperoliidae, Rhacophoridae, Dendrobatidae, Hemisotidae, and Microhylidae), although the relationships among ranoid families are unresolved. The placement of the dendrobatids remains controversial and some authors believe that they are more closely related to bufonids than to ranoids (Hass, 1995; Hay et ah, 1995; Ruvinsky and Maxson, 1996). The relationships among the other neobatrachian families are also unresolved (Fig. 5.1). Most of the currently recognized anuran families

Pelobatidae Pelodytidae Megophryidae Rhinophrynidae Pipidae

_

Limnodynastinae Myobatrachlnae Sooglossidae Heleophrynidae "Leptodactylidae" Brachycephalidae Bufonidae Rhinodermatidae Centrolenidae Hylidae Pseudidae "Ranidae" Arthroleptidae Hyperoliidae Rhacophoridae Dendrobatidae Hemisotidae Microhylidae

F I G U R E 5.1. A phylogeny of the living anurans modified from Ford and Cannatella (1993). The archaeobatrachians are a grade group that share many ancestral characteristics but are not closely related to each other. The families Leptodactylidae and Ranidae are indicated in quotes because there is no evidence for their monophyly.

appear to be monophyletic, with the possible exception of Myobatrachidae, Leptodactylidae, and Ranidae (Ford and Cannatella, 1993). The family Myobatrachidae may not be monophyletic because its subfamily Myobatrachlnae shares several characteristics with the family Sooglossidae that are absent in the subfamily Limnodynastinae. For the families Ranidae and Leptodactylidae, monophyly has been rejected, but the relationships of the subfamilies to other taxa remain to be resolved (Ford and Cannatella, 1993). At present, the unresolved relationships among neobatrachian frogs are a serious impediment to understanding anuran evolution. B. Natural History of Anurans Nearly all frogs are carnivorous after metamorphosis, and invertebrates are the most common prey, although there are reports of frogs that eat fruits (Silva et ah, 1989) and leaves (Das and Coe, 1994; Das, 1995, 1996). Most anurans are also feeding generalists, eating any prey that will fit into their mouths in proportions that match the relative abundance of prey in

119

5. Feeding in Frogs nature (Toft, 1981). Dietary generalists tend to be widemouthed, sit-and-wait predators. A few species of anurans are known to specialize on a narrower range of prey types (Toft, 1981). Some forest floor species, including the genus Bufo (Smith and Bragg, 1949; Inger and Marx, 1961; Berry and Bullock, 1962; Clarke, 1974; Zug and Zug, 1979; Toft, 1981), and many burrowing anurans, such as Hemisus (Emerson, 1976a), specialize on small prey such as ants, coUembolans, termites, or mites (Simon and Toft, 1991; Toft, 1995; Caldwell, 1996), consuming them in greater proportions than their relative abundance in nature. Small prey specialists tend to lack teeth, have relatively narrow mouths, and search actively for prey (Toft, 1981). They also tend to have higher aerobic capacities and lower anaerobic capacities than dietary generalists (Taigen and Pough, 1983). Several anurans are known to consume rather peculiar types of prey, such as snails (Drewes and Roth, 1981), crabs (Premo and Atmowidjojo, 1987), fish (Knoepffler, 1976), or even other frogs (Emerson, 1985). However, these species also take a wide range of other prey types and so are not strict dietary specialists. There have been relatively few attempts to correlate the morphology of the feeding apparatus with natural diets in anurans. Emerson (1985) and colleagues (Emerson and Voris, 1992, Emerson and Bramble, 1993; Emerson et ah, 1994) have studied the relationships among skull morphology, feeding behavior, and diet among diverse species. She found that frogs that eat relatively large prey have relatively longer jaws and wider skulls than those that eat small prey. In addition, the feeding cycle is longer and more asymmetrical (i.e., mouth closing takes longer than mouth opening) in species that eat large prey than in species that eat small prey. Gray (1997) compared the diets of sympatric hylid frogs with short vs long tongues. She found that there was overlap in the types of prey taken by the two species, but long-tongued species consumed a greater proportion of rapidly moving prey than shorttongued species. The ecological significance of differences among frogs in the morphology of the feeding apparatus is a topic that deserves further study.

II. MORPHOLOGY OF THE FEEDING APPARATUS Feeding mechanisms of amphibians (frogs, salamanders, and caecilians) are extremely diverse. The tongues of caecilians are small and cannot be protruded from the mouth so jaw prehension is used to capture prey and some species possess a highly specialized jawclosing mechanism (Bemis et ah, 1983; Nussbaum,

1983). In contrast to caecilians, terrestrial salamanders and frogs use lingual protraction to catch prey. They depend heavily on lingual adhesion for prey capture. In salamanders, the articulated hyobranchial skeleton forms an internal support for the tongue, which leaves the mouth with the tongue during protraction (Lombard and Wake, 1976; Thexton et ah, 1977). Salamanders vary widely in their tongue morphology, especially with regard to projection distance, muscle attachment, and hyobranchial folding (Ozeti and Wake, 1969; Regal, 1966; Wake, 1982; Lombard and Wake, 1977, 1987). In contrast to salamanders, the anuran tongue consists only of muscles and connective tissue, with no intrinsic cartilaginous or bony skeleton. The hyobranchial apparatus is an unarticulated plate formed from the ontogenetic fusion of the cartilaginous larval elements. It cannot be folded and does not leave the mouth with the tongue during feeding (Gans, 1961, 1962; Gans and Gorniak, 1982a,b; Roth et ah, 1990). Frogs also vary in their tongue morphology, especially with regard to the anatomy of the protractor muscle (Regal and Gans, 1976; Horton, 1982) and projection distance (Deban and Nishikawa, 1992; Nishikawa et ah, 1992). Variation in the morphology of the feeding apparatus has been studied extensively in frogs (MagimelPelonnier, 1924; Regal and Gans, 1976; Emerson, 1976b, 1985; Horton, 1982; Cannatella, 1985). Until recently, there have been few attempts to map morphological characteristics of the feeding apparatus onto a cladogram of anuran taxa, particularly in a functional context. In general, although the size and shape of elements of the feeding apparatus may differ dramatically among species, there is a great deal of overall similarity in the bones and muscles of the feeding apparatus among frogs (Figs. 5.2A-5.2C). The functional significance of anatomical variation remains unknown in most cases. The feeding apparatus of frogs consists of the cranium, mandibles, hyoid, and tongue, each of which is associated with a series of muscles. The morphology of each of these elements is described next, along with brief descriptions of hypothesized functions of the musculoskeletal elements and a brief review of diversity among taxa, where known. A more detailed examination of the function of the feeding apparatus is given in Section III. A. Cranium and Jaw Muscles The morphology of the anuran cranium was studied extensively by Trueb (1973), and a fairly detailed summary can be found in Duellman and Trueb (1986). Cranial morphology is highly variable among species.

120

Kiisa C. N i s h i k a w a Hyla cinerea

Hemisus marmoratum

Bufo marinus M. submentalis

M. intermandibularis

geniohyoideus

M. intermandibularis

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hyoid M. interhyoideus

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l\^. submentalis M. geniohyoideus

^ interhyoideus

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M. hyoglossus M. stemohyoideus

M. genioglossus

M. genioglossus

M. geniohyoideus medialis M. geniohyoideus lateralis

M. hyoglossus

M. hyoglossus M. hyoglossus

M. omohyoideusM. stemohyoideus

M. stemohyoideus

tongue tip " I ^ M. hyoglossus \ lingual sinus

,„„„«oo mucosa I

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^- hyoglossus

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u inte,h„«iHai,c / // M. intertiyoideus / (/ . ^ ._, M. submentalis ^ M. geniohyoideus

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hyoid plate

F I G U R E 5.2. Musculature of the feeding apparatus in Hyla cinerea (A), Bufo marinus (B), and Hemisus marmoratum (C). Superficial muscles of the feeding apparatus include M. intermandibularis, M. interhyoideus, and M. submentalis. Deep muscles include the extrinsic tongue muscles M. hyoglossus and M. genioglossus, and the hyoid protractor M. geniohyoideus and retractor M. stemohyoideus. A sagittal section of the tongue of Hemisus (D) shows the dorsoventral and longitudinal compartments of the M. genioglossus.

which exhibit a continuum from reduced ossification (e.g., Ascaphus) to hyperossification (e.g., pipid frogs). Reduction or loss of bones has occurred in numerous taxa, and a few taxa possess neomorphic cranial elements (Trueb, 1973). Bones of the neurocranium include the sphenethmoid and the paired prootics and exoccipitals. The dermal roofing bones usually include only the nasals and the frontoparietals. The frontoparietals and prootics provide attachment sites for the M. levator mandibulae anterior longus and M. levator mandibulae posterior longus (= M. temporalis). The bones of the palate include the paired vomers, which are often absent, and the parasphenoid, which is always present and covers the neurocranium ventrally. The prevomers, palatines, and pterygoids are absent in many taxa. Although quite variable in shape, the squamosal is always present. It acts as an important attachment site for the jaw levators. Maxillary arch bones always include the premaxilla and maxilla, and sometimes the quadratojugal. The premaxilla is highly

variable and is important in determining the shape of the snout (Trueb, 1973). The teeth of frogs are reduced compared to most other vertebrates (Duellman and Trueb, 1986). Maxillary and premaxillary teeth are usually, but not always, present. Vomerine teeth are usually present if the vomers are present. No other bones of the upper jaw bear teeth in frogs. Small prey specialists, such as toads (family Bufonidae), lack teeth entirely (Duellman and Trueb, 1986). The jaw muscles consist of one main depressor for opening the mouth and a complex of six levators (= adductors) for closing it. The M. depressor mandibulae originates from the dorsal fascia and/or otic capsule and inserts on the proximal tip of the mandible (Emerson, 1977), close to the jaw joint and therefore in a position of relatively low mechanical advantage. The muscles of the M. levator mandibulae complex extend from the otic capsules and squamosal to the mandible as follows: (1) the M. levator mandibulae anterior longus (= M. pterygoideus) originates on the frontoparietal

121

5. Feeding in Frogs and prootic and inserts via a tendon on the medial side of the angulosplenial; (2) the massive M. levator mandibulae posterior longus (= M. temporalis) originates from the median raphe on the skull roof, the lateral surface of the frontoparietal, and the dorsal surface of the prootic and it inserts via a tendon on the medial side of the angulosplenial; (3) the M. 1. m. posterior lateralis originates on the ventral arm of the squamosal and inserts on Meckel's cartilage and the lateral surface of the angulosplenial; (4) the M. 1. m. posterior articularis originates on the quadrate and inserts on the mandible; (5) the M. 1. m. externus originates on the zygomatic process of the squamosal and inserts laterally on the mandible; and (6) the M. 1. m. posterior subexternus also originates on the zygomatic process of the squamosal and inserts on the posterior end of the mandible (Duellman and Trueb, 1986). All of the Mm. levator mandibulae insert farther from the jaw joint, in a position of relatively greater mechanical advantage, than the M. depressor mandibulae. The Mm. levator

Hyla cinerea

mandibulae are innervated by the trigeminal nerve, whereas the M. depressor mandibulae is innervated by the facial nerve (Figs. 5.3D-5.3F). Although there is much variation in the morphology of the skull and jaws of frogs (Trueb, 1973) and considerable variation among species in the jaw musculature (Starrett, 1968), the functional significance of interspecific differences remains largely unknown (Duellman and Trueb, 1986). James Birch (personal communication) is using morphometric methods to analyze the functional consequences of changes in anuran skull shape during development as well as differences among species. B. Mandible and Buccal Floor Muscles The mandibles of frogs generally consist of three paired bony elements associated with Meckel's cartilage: the angulosplenial, dentary, and mentomeckelian bones (which are absent in pipoids and a few other

Bufo marinus

Hemisus marmoratum

F I G U R E 5.3. Camera lucida drawings of the peripheral nerves of adult Hyla cinerea (A,D), Bufo marinus (B,E), and Hemisus marmoratum (C,F) stained with Sudan black B. (Top row) The glossopharyngeal nerve is shown on the left and the hypoglossal nerve is shown on the right. (Bottom row) The trigeminal nerve is shown on the left and the facial nerve is shown on the right. The stippled area indicates the tongue pad. The glossopharyngeal nerve provides only sensory innervation of the tongue. The hypoglossal nerve innervates the Mm. genioglossus basalis and medialis (if present), the M. hyoglossus, and the M.m. geniohyoideus, sternohyoideus, and omohyoideus. The M. genioglossus basalis is innervated by the most proximal branches of the hypoglossal nerve at the base of the tongue, whereas the M. genioglossus medialis is innervated by the more distal branches. The trigeminal nerve crosses over the mandible and innervates the M. intermandibularis and M. submentalis. At the base of the mandible, the facial nerve innervates the M. interhyoideus.

122

Kiisa C. Nishikawa

species). The presence of a movable joint between the mentomeckelian and dentary is an unusual feature of the mandibles of most anurans (Regal and Gans, 1976; Nishikawa and Roth, 1991). In most species, depression of the mandibular tips results not only from downward movement of the mandibles relative to the cranium (mandibular depression), but also from downward movement of the mentomeckelian bones relative to the rest of the mandible (mandibular bending). Most frogs lack teeth on the mandible. Only one species (Amphignathodon guentheri) is known to possess mandibular teeth (Duellman and Trueb, 1986), although some species (e.g., Ceratophrys) possess tooth-like processes on the dentary. A series of three transversely oriented muscles form the floor of the buccal cavity: the M. submentalis, M. intermandibularis, and M. interhyoideus (Figs. 5.2A5.2C). The M. submentalis connects the anterior ends of the mandibles. During feeding, it bends the mandibles downward by depressing their tips. During breathing, the M. submentalis closes the nares by lifting the mentomeckelian bones upward. This upward movement deforms the alary cartilages, which closes the nares (Gans and Pyles, 1983; Nishikawa and Gans, 1996). The M. intermandibularis extends between the posterior ends of the mandibles (Figs. 5.2A-5.2C). In some species, the M. intermandibularis has supplementary elements of unknown function (Tyler, 1974; Emerson, 1976b). The M. interhyoideus lies posterior to the M. intermandibularis and supports the vocal sacs (Figs. 5.2A-5.2C). The Mm. submentalis and intermandibularis are innervated by the trigeminal nerve, whereas the M. interhyoideus is innervated by the facial nerve (Figs. 5.3D-5.3F). Contraction of the M. intermandibularis and M. interhyoideus raises the buccal floor (Gans and Gorniak, 1982b). C. H y o i d and Associated Muscles The hyobranchial apparatus of adult anurans is a broad plate that forms from the fusion of larval branchial elements (De Jongh, 1968). The slender hyalia extend from the anterior end of the plate and usually attach to the prootic bones, although the hyalia are disjunct in most mesobatrachians and are missing altogether in pelodytids (Cannatella, 1985). Alary processes and posterolateral processes are usually present on the lateral margins of the hyoid plate, and posteromedial processes flank the larynx. In most anurans, only the posteromedial processes are ossified. A pair of muscles, the M. geniohyoideus and M. sternohyoideus, serve to protract and retract the hyoid, respectively (Emerson, 1977; Gans and Gorniak, 1982b). The M. geniohyoideus originates on the pos-

terolateral processes of the hyoid and inserts near the mandibular symphysis (Figs. 5.2A-5.2C). In most species, it consists of separate medial and lateral compartments. The M. sternohyoideus originates on the sternum and inserts on the posterolateral edge of the hyoid plate (Figs. 5.2D-5.2F). The Mm. petrohyoidei anterior et posteriores and the M. omohyoideus elevate and depress the hyoid, respectively (de Jongh and Gans, 1969; Emerson, 1977). The glossopharyngeal nerve innervates the M. petrohyoideus anterior and the vagus nerve innervates the Mm. petrohyoidei posteriores, whereas the hypoglossal nerve innervates the Mm. omohyoideus, sternohyoideus and geniohyoideus (Figs. 5.3A-5.3C; Gaupp, 1896). A great deal of variation in hyoid morphology is found among anurans (Duellman and Trueb, 1986). Aquatic suction feeders (e.g., Hymenochirus, family Pipidae) possess large, articulated, ossified hyoids, whereas terrestrial lingual feeders possess small, fused, cartilaginous hyoids. A similar pattern is found among aquatic and terrestrial turtles, in which suction feeders possess large, ossified, articulated hyoids whereas terrestrial feeders possess small, cartilaginous ones (Bramble and Wake, 1985). An ossified and articulated hyoid appears to be associated with the ability to generate large forces, such as those necessary for moving large volumes of water during aquatic suction feeding. The role of the hyoid in lingual feeding varies widely among tetrapods. In salamanders, it forms a skeletal support for the tongue, and both tongue and hyoid are projected from the mouth as a unit (Lombard and Wake, 1977). In chameleons, the hyoid is a tapered rod around which an accelerator muscle contracts to project the tongue from the mouth (Gans, 1967; Wainwright et ah, 1991). In frogs, the hyoid forms a base on which the tongue rests. The hyoid does not leave the mouth with the tongue. The only connection between hyoid and tongue is the M. hyoglossus, which originates on the posterolateral process of the hyoid and inserts broadly in the tongue. Movements of the hyoid plate appear to play an important role in buccal expansion and contraction during breathing and calling in anurans (de Jongh and Gans, 1969; Martin and Gans, 1972; Emerson, 1977). The role of the hyoid in anuran feeding is less clear (see Section III,B). Cineradiographic recordings of hyoid movement during feeding in Bufo marinus show that the hyoid is stabilized in a retracted position during the initial phase of tongue protraction and that it moves anteriorly during tongue protraction (Emerson, 1977). Based on these observations, Emerson (1977) hypothesized that the hyoid acts as a stable platform for the tongue during the initial stages of protraction, that it stores potential energy during intermediate stages.

5. Feeding in Frogs and that the stored energy is imparted to the tongue during the final stages of protraction. However, this mechanism appears to be unlikely (see Section III,B). In contrast to the neobatrachians that have been studied, the hyoid appears to play a more important role in feeding in mesobatrachians. Based on anatomical observations and muscle stimulation experiments, Trueb and Gans (1983) suggested that the hyoid plays an important role in tongue protraction during feeding in the termite-eating frog, Rhinophrynus dorsalis. This hypothesis remains to be tested experimentally in feeding animals. In the spadefoot toad {Spea multiplicata), another mesobatrachian, tongue movements were impaired after bilateral denervation of the M. geniohyoideus, suggesting that hyoid protraction is necessary for normal tongue protraction in this species (O'Reilly and Nishikawa, 1995). The disjunct hyoid of mesobatrachians may be responsible for the greater role of hyoid protraction during feeding in this group. In most frogs, the cornua of the hyoid are fused to the prootic bones, which may limit forward excursion of the hyoid (Cannatella, 1985). In mesobatrachians, the cornua are continuous until metamorphosis, at which time a gap develops in the cornua, which frees the hyoid plate from its attachment to the skull (Ridewood, 1897), perhaps allowing the hyoid to move farther anteriorly during feeding than it can in other frogs. D . Tongue and Associated Muscles There are several problems that terrestrial frogs must overcome to capture prey successfully. These include contacting the prey with the tongue, ingesting prey, transporting it through the oral cavity, and finally swallowing it. In terrestrial anurans, the sticky tongue plays an important role in ingesting, transporting, and swallowing prey. There are no known instances of inertial feeding or transport among anurans, probably because they consume mostly small prey. Frogs do not masticate their food, and there is relatively little manipulation of the food by the tongue once it is in the oral cavity. Little is known about differences among anuran species in modes of oral transport and swallowing. All anurans possess a relatively simple tongue that consists only of two pairs of extrinsic muscles: the M. genioglossus and M. hyoglossus (Gaupp, 1901; Regal and Gans, 1976). In contrast to most other terrestrial vertebrates, intrinsic muscles are absent in most species. The M. genioglossus originates near the mandibular symphysis and inserts posteriorly into the tongue pad (Figs. 5.2A-5.2C). In many anurans, the M. genioglossus is subdivided by connective tissue

123

into a number of different compartments, which vary widely among species (Horton, 1982). The M. hyoglossus originates on the posteromedial process of the hyoid and inserts along the lateral margin of the tongue pad, often interdigitating with the fibers of the M. genioglossus (Figs. 5.2A-5.2C). The Mm. genioglossus and hyoglossus are innervated by the hypoglossal nerve (Figs. 5.3A-5.3C). In most frogs, the M. genioglossus is used to place the tongue on the prey (discussed in detail in Section III) and prey are returned to the mouth by the M. hyoglossus. In Bombina, Bufo, Phrynomerus, and Hemisus, denervation experiments demonstrate that the M. hyoglossus plays an important role in prey capture, oral transport, and swallowing (Ritter and Nishikawa, 1995; Tso et ah, 1995). Small prey are returned to the mouth and delivered to the esophagus by the tongue in a single movement, sometimes with the help of the forelimbs, whereas large prey are nearly always transported with the help of the forelimbs, presumably because lingual transport would be ineffective by itself (Gray et ah, 1997). Because most anurans retract the eyes into the orbit during swallowing, it has been suggested that the M. retractor bulbi also plays a role in anuran swallowing (Regal and Gans, 1976). However, this hypothesis has yet to be tested experimentally (Duellman and Trueb, 1986). There have been three broadly comparative morphological studies of the tongue musculature of anurans. Magimel-Pelonnier (1924) studied 45 species. Regal and Gans (1976) studied 12 species, and Horton (1982) studied 63 species, predominantly from Australia. In all, 61 genera are represented. From these studies, three different patterns of tongue morphology have been described. The first pattern consists of a round tongue that is broadly attached to the floor of the mouth, both anteriorly and posteriorly, so that there is no free flap posteriorly. In these tongues, the fibers of the M. hyoglossus radiate from the hyoid into the tongue pad and the ventralmost fascicles insert near the base of the tongue (Horton, 1982). The fibers of the M. genioglossus arise near the niandibular symphysis and radiate into the tongue, where they interdigitate with those of the M. hyoglossus (Regal and Gans, 1976; Horton, 1982). This morphology is found in all archaeobatrachians (i.e., Ascaphus, Leiopelma, Bombina, Alytes, and Discoglossus), some mesobatrachians {Pelobates, Pelodytes, and Rhinophrynus), and some neobatrachians, including Telmatobius, Litoria, Hyla, Gastrotheca, Rheobatrachus, and several genera of limnodynastines (Magimel-Pelonnier, 1924; Regal and Gans, 1976; Horton, 1982; Trueb and Gans, 1983). Based on their origins and insertions. Regal and

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Kiisa C. Nishikawa

Gans (1976) hypothesized that, upon contraction, the M. genioglossus pulls the tongue toward the symphysis in these species, whereas the M. hyoglossus pulls the tongue toward the esophagus. These hypotheses have been confirmed by denervation of the M. genioglossus in Bombina (Nishikawa et ah, 1992), Discoglossus (Nishikawa and Roth, 1991), and Hyla (Deban and Nishikawa, 1992) and by denervation of the M. hyoglossus in Bombina (Tso et ah, 1995). The second pattern is found only among aquatic pipid frogs (e.g., Xenopus, Pipa, and Hymenochirus), which possess large articulated, ossified hyoids (Cannatella, 1985) and are secondarily tongueless (Cannatella and Trueb, 1988) although they possess vestiges of tongue musculature (Horton, 1982). These species use suction or ram feeding to ingest and transport prey (Sokol, 1969; Avila and Frye, 1977; O'Reilly et al, 1999). A third pattern consists of a muscular tongue that is attached anteriorly to the buccal floor, with a free posterior flap that varies in length among species (Regal and Gans, 1976) and varies to some extent among fixed specimens within a species (Magimel-Pelonnier, 1924). This type of tongue is found in some pelobatoids {Scaphiopus, Spea, and Megophrys) and some neobatrachians, such as Hyla and Limnodynastes (Magimel-Pelonnier, 1924; Regal and Gans, 1976; Horton, 1982). In these tongues, the fibers of the M. hyoglossus recurve to insert in the more distal parts of the tongue, rather than its anterior base. In contrast to the M. hyoglossus, which is relatively homogeneous among species, the arrangement of the M. genioglossus varies widely (Magimel-Pelonnier, 1924; Regal and Gans, 1976; Horton, 1982). All species retain the interdigitating element that is found in species with round, broadly attached tongues, but several additional elements also may be present (Regal and Gans, 1976; Horton, 1982). These elements fall into two groups: those with fibers that run parallel to the long axis of the tongue [i.e., the ventral, dorsomedial and superficial elements of Horton (1982)] and those with transverse fibers [i.e., the genioglossus basalis of Gaupp (1901)]. At present, there is no information concerning the functional significance of this variation in the arrangement of the M. genioglossus (but see Section III,C). As in species with round, broadly attached tongues, retraction of the tongue is accomplished by contraction of the M. hyoglossus (Gans and Gomiak, 1982a,b; Ritter and Nishikawa, 1995; Tso et al, 1995). On the basis of their anatomy, the tongues of species with free posterior flaps are presumed to rotate over the mandibular symphysis so that the dorsal surface of the tongue at rest becomes the ventral surface of the fully protracted tongue, as has been shown to occur in Rana (Gans, 1961, 1962) and Bufo (Gans and Gorniak,

1982a,b). It has been hypothesized that these "flipping tongues" have evolved convergently several times among frogs (Regal and Gans, 1976), and this idea is supported by phylogenetic analysis (Section V,A). Despite the variation in tongue morphology, most frogs (with the exception of pipids) share several important features of the tongue: (1) it is attached anteriorly near the mandibular symphysis; (2) most of the fibers in both the protractor and the retractor muscles are oriented nearly parallel to the long axis of the tongue so that their shortening would pull the tongue pad either toward the symphysis or toward the esophagus (Horton, 1982); (3) those fibers that are transverse (i.e., genioglossus basalis) are relatively short and are associated with large amounts of connective tissue (Horton, 1982); (4) the resting length of the tongue approximates the length of the mandibles; and (5) the mass of the tongue is approximately 0.5-1.0% of body mass, which is about as large in relative terms as the human heart.

III. FUNCTION OF THE FEEDING APPARATUS This section first gives an overview of methods that can be used to study the function of any morphological system, in this case the feeding apparatus. It next discusses previously published hypotheses for the mechanism of tongue protraction in anurans, including an analysis of which methods were informative, which were uninformative, and which were positively misleading. The section ends with a discussion of functional diversification of the mechanism of tongue protraction among anuran species. A. Methods for Studying the Function of the Feeding Apparatus Before undertaking a comparative and functional analysis of feeding, it is important to ask what types of experiments and observations can best be used to understand the function of the feeding apparatus. Obviously, the necessary data include a description of anatomy as well as a description of movement patterns, which usually involves some type of kinematic analysis. These often are supplemented with information about muscular and neural activity. Traditional methods include recordings of electrical activity from relevant muscles and nerves as well as electrical stimulation experiments. Kinematic studies are of three types: (1) description of films or still photos; (2) analysis of kinematic profiles in which values of kinematic variables, such as gape angle, are plotted over time (Fig. 5.4); and (3) trajectory

90 80

Hyla cinerea

Hemisus marmoratum

Bufo marinus

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Time (ms) F I G U R E 5.4. Kinematic profiles for Hyla cinerea, Bufo marinus, and Hemisus marmoratum showing gape angle (°), gape velocity (°/msec), mandible angle (°), head rotation (°), tongue length (cm), lunge length (cm), and jaw position (cm) as a function of time. Mandible angle is the angle subtended by the jaw joint and the tip of the mandibles, with the midpoint of the mandible at the vertex. It is approximately 180° at rest and bends downward to approximately 140° under the contraction of the M. submentalis. Head rotation is the angle formed between a line connecting the jaw joint and upper jaw tips and the horizon line and measures the change in head position relative to the horizon. In this sequence, H cinerea uses jaw prehension to capture the prey, and the head is rotated downward to an angle of 45° below the horizon. Lunge length is the horizontal position of the upper jaw tip in each field. Jaw position shows the vertical position of the upper and lower jaw tips in each field.

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Kiisa C. N i s h i k a w a

analysis, in which the positions of elements of the feeding apparatus are plotted in space relative to each other as well as relative to an external reference (Figs. 5.557). Trajectory analysis has the advantage that the displacements, velocities, and accelerations of elements relative to each other can be calculated over time and, if the masses of the elements are known, then the relative accelerations can be used to estimate the forces produced at each joint by muscular contraction. Traditionally, kinematic profiles have been used in studies of functional morphology (see, e.g.. Bramble and Wake, 1985; Reilly and Lauder, 1989), whereas trajectory analysis has been more commonly used in studies of motor control (e.g.. Bout and Ziegler, 1994). Whereas the anatomy of the feeding apparatus has been studied in 61 genera of frogs (Magimel-Pelonnier, 1924; Regal and Gans, 1976; Horton, 1982), kinematic studies have been performed for only a handful of genera. Among anurans, still photos are available for Discoglossus pictus, Pelobates fuscus and Rana temporaria (Vences, 1988). Descriptions of films are available for Ascaphus truei (Larsen and Guthrie, 1975), Bombina orientalis (Regal and Gans, 1976), Xenopus laevis (Avila and Frye, 1977), Hymenochirus boettgeri (Sokol,

F I G U R E 5.5. Movement trajectories of Hyla cinerea, a frog that uses mechanical pulling to protract the tongue. Anterior is toward the right. Trajectories A - C begin at the same point, but are offset for clarity. Arrows show the direction of movement in each segment of the trajectories, and open circles indicate the position of each element in each video field. In this sequence, the frog uses tongue prehension to capture the prey so there is little craniovertebral flexion. Trajectories of (A) the upper jaw tip, (B) lower jaw tip, and (C) tongue tip relative to an external reference point. Relative to an external reference point, the upper jaw tip moves forward during the lunge and backward during body recovery and the lower jaw tip moves forward during the lunge, then downward as the mouth opens and upward and back as the mouth closes during body recovery. (D) Relative to the upper jaw tip, the lower jaw tip moves downward and backward during mouth opening, then upward and forward during mouth closing. (E) Relative to the lower jaw tip, the tongue tip moves upward then forward relative to the lower jaw tip, then down and back. The tongue shortens during protraction and never protrudes more than a few millimeters beyond the tips of the mandibles.

F I G U R E 5.6. Movement trajectories of Bufo marinus, a frog that uses inertial elongation to protract the tongue. Anterior is toward the right. Trajectories A - C begin at the same point, but are offset for clarity. Arrows indicate the direction of movement in each segment of the trajectories, and open circles indicate the position of each element in each video field. Trajectories of (A) the upper jaw tip, (B) the mandibular tip, and (C) the lingual tip relative to an external reference. The lingual tip follows a nearly straight trajectory from mouth to prey during protraction as it elongates by up to 180% of its resting length. Relative to an external reference point, the upper jaw tip moves downward and forward during the lunge, then upward and back during body recovery. (D) Relative to the upper jaw tip, the movement of the lower jaw tip moves is mostly limited to the vertical plane. (E) The trajectory of the lingual tip relative to the mandibular tip is first upward and forward as the tongue shortens, but then changes abruptly to downward and forward as the tongue elongates and the lingual tip passes beyond the mandibles.

1969), B. marinus (Gans and Gorniak, 1982a,b), and Rana catesbeiana (Gans, 1961, 1962). Kinematic profiles have been published for a handful of genera, including Bufo (Lauder and Reilly, 1994), Rana, Bufo, Kaloula, Pyxicephalus, and Dyscophus (Emerson, 1985), Ascaphus truei (Nishikawa and Cannatella, 1991), Discoglossus pictus (Nishikawa and Roth, 1991), Hyla cinerea (Deban and Nishikawa, 1992), phyllomedusine hylids (Gray and Nishikawa, 1995), S. multiplicata (O'Reilly and Nishikawa, 1995), Rana pipiens (Anderson, 1993), and Hemisus marmoratum (Ritter and Nishikawa, 1995). The marine toad B. marinus is the only amphibian for which a trajectory analysis of feeding movements has been published (Nishikawa and Gans, 1996). Kinematic profiles (Fig. 5.4) are useful for analyzing the timing of movements of different elements of the feeding apparatus relative to each other. However, as a method for quantifying movement, kinematic profiles are limited by the fact that displacements are plotted in time rather than space. Important information about

127

5. Feeding in Frogs

5 mm

F I G U R E 5.7. Movement trajectories of Hemisus marmomtum, a frog that uses hydrostatic elongation to protract its tongue. Anterior is toward the right. Trajectories A - C begin at the same point, but are offset for clarity. Arrows indicate the direction of movement in each segment of the trajectories, and open circles indicate the position of each element in each video field. Trajectories of (A) the upper jaw tip, (B) the mandibular tip, and (C) the lingual tip relative to an external reference. There is relatively little head movement during feeding, although the head moves slightly upward and forward, then down and back during feeding. (D) The lower jaw tip is both depressed and retracted during mouth opening, and retraction of the lower jaw counteracts the upward rotation of the tongue tip relative to the mandibles so that the initial trajectory of the tongue (C) is straight out of the mouth. (E) Unlike inertial elongators, the tongue does not follow a straight line from mouth to prey during protraction.

head, jaw, and tongue movements and their coordination can often be obtained by performing a trajectory analysis. For example, from kinematic profiles, we can observe that the skull typically begins to rotate upward as the mouth opens during feeding in Hyla and Bufo (Fig. 5.4). By plotting the trajectory of the mandibular tip relative to the tip of the upper jaw, we also see that mouth opening involves nearly pure depression of the mandibles in Bufo (Fig. 5.6), whereas the mandibles are both depressed and retracted to some extent in Hyla (Fig. 55) and Hemisus (Fig. 5.7). From the trajectory analysis, we can see that in Bufo the upward rotation of the head during mouth opening balances the retraction of the mandibles, which is an inevitable consequence of downward rotation of the mandibles, whereas the retraction of the mandibles is not entirely balanced by upward head rotation in Hyla and Hemisus. As a second example, we can examine tongue movements during prey capture. Kinematic profiles (Fig. 5.4) show that anuran species protract their tongues to different degrees and at different rates of speed. In addition, trajectory analyses show that the tongue tip of Bufo (Fig. 5.6) follows a straight line from mouth to

prey, whereas the tongues of Hyla (Fig. 5.5) and Hemisus (Fig. 5.7) do not. This straight trajectory can be seen to emerge from the precise coordination of head, jaw, and tongue movements (Fig. 5.6). Electromyographic (EMG) recordings coupled with kinematic analyses may help generate hypotheses about the roles that individual muscles play during feeding (Gans and Gorniak, 1982a,b). For anurans, EMG studies of feeding behavior have been performed only in the toads B. marinus (Gans and Gorniak, 1982a,b) and B. japonicus (Matsushima et al., 1985) and the frog R. pipiens (Anderson and Nishikawa, 1993). Gans and Gorniak (1982a,b) obtained records of EMG activity from several muscles in freely behaving toads feeding on natural prey. Matsushima et al. (1985) stimulated the optic tectum with implanted electrodes to elicit tongue flipping in freely behaving animals. In addition to EMG recordings, muscle stimulation has often been used to study the function of muscles believed to be involved in feeding behavior. It is often possible to perform muscle stimulation on uncooperative species that refuse to eat in captivity (Bemis et ah, 1983; Trueb and Gans, 1983). Among anurans, muscle stimulation experiments have been performed only in B. marinus (Emerson, 1977; Gans and Gorniak, 1982a,b) and R. dorsalis (Trueb and Gans, 1983). In addition to these traditional techniques, a variety of other techniques may provide additional information that may be used to understand the roles of particular elements of the feeding apparatus. One method is to denervate individual muscles by surgically transecting the nerves that innervate them in order to study how movements change after a muscle or set of muscles has been inactivated. This technique can be used to demonstrate that a particular muscle is either necessary or sufficient for performing a given movement (Nishikawa and Roth, 1991). However, because most peripheral nerves contain both sensory and motor fibers, it is important to consider the possibility that some observed effects of nerve transection may be due to deafferentation rather than to muscle denervation (Nishikawa and Gans, 1992). B. Hypotheses for the Mechanism of Tongue Protraction Historically, numerous mechanisms have been proposed to explain tongue flipping in anurans (for a review, see Gans and Gorniak, 1982b). Two relatively recent hypotheses include the hyoid model of Emerson (1977) and the ballista model of Gans and Gorniak (1982a,b). Both of these studies used a variety of techniques to study feeding in the marine toad, B. marinus. Both studies proposed relatively complex mechanisms

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Kiisa C. Nishikawa

for tongue protraction and, although based on accurate and repeatable observations, both have been shown to have problems with some aspects of data interpretation (Nishikawa and Gans, 1992, 1996). It is useful to describe these hypotheses and the evidence on which they were based in order to determine which techniques were helpful, which were relatively uninformative, and which were misleading in terms of understanding the mechanism of tongue protraction in anurans. Emerson (1977) used dissection, cineradiography, and electrical stimulation to develop a biomechanical model of tongue protrusion in toads. Cineradiographic observations revealed that the hyoid is held in the retracted position during mouth opening, moves downward and forward during tongue protraction, and upward and backward during retraction. When stimulated electrically, the tongue protractor muscle M. genioglossus "positioned the tongue in the preflip condition but did not cause the tongue to leave the mouth." Stimulation of the M. depressor mandibulae did not cause the jaws to open, although stimulation of the Mm. geniohyoideus and sternohyoideus resulted in mouth opening. From these and other observations, Emerson (1977) hypothesized that the hyoid plays a static role during mouth opening and a dynamic role during protraction and retraction of the tongue. Specifically, she proposed that the hyoid retractor M. sternohyoideus stabilizes the hyoid in a retracted position in the floor of the mouth and stores potential energy during the early stages of mouth opening, which she presumed to be caused by contraction of the hyoid muscles Mm. geniohyoideus and sternohyoideus. As the mouth opens more fully under the contraction of the M. depressor mandibulae and the M. sternohyoideus stops contracting, potential energy is released as the hyoid moves anteriorly, and this released energy is imparted to the tongue as kinetic energy. Posterior movement of the hyoid, perhaps due to elastic recoil, would initiate retraction of the tongue, which would then be fully retracted by contraction of the M. hyoglossus. When the hyoid is fully retracted, it is once again held in place by the action of the M. sternohyoideus. Emerson's (1977) model was refuted by Gans and Gorniak (1982a,b) who showed that (1) the pattern of EMG activity in the muscles of the hyoid and tongue is inconsistent with the model; (2) the tongue is stiff rather than flaccid when protracted; and (3) when the hyoid is wired to the sternum, and thus can impart no kinetic energy to the tongue, toads were observed to feed normally. As an alternative to Emerson's hyoid model, Gans and Gorniak (1982a,b) offered their ballista model of

tongue protraction in anurans, which is now widely accepted. This model was derived initially from kinematic analyses and muscle stimulation experiments in R. catesheiana (Gans, 1952,1961; Severtzov, 1961). Later, additional species were studied anatomically (Regal and Gans, 1976) and the model was eventually tested using dissection, electromyography, and muscle stimulation experiments in the toad B. marinus (Gans and Gorniak, 1982a,b). In the ballista model, the M. genioglossus medialis forms a stiffened rod and the M. genioglossus basalis forms a wedge at the anterior end of the rod near the mandibular symphysis. The main force-generating element is the M. submentalis, which depresses the mandibular symphysis, lifts the middle of the lingual rod, and rotates it about the symphysis (Gans and Gorniak, 1982a,b). The observations on which the model was based include: (1) electromyographic data showing that the M. submentalis and Mm. genioglossus basalis and medialis are active during tongue protraction and (2) the observation that stimulation of the M. genioglossus basalis resulted in rotation of the base of the tongue toward the mandibular symphysis, whereas stimulation of the M. genioglossus medialis resulted in stiffening of the tongue with no anterior movement. Results of muscle denervation experiments and detailed kinematic analyses have shown that the ballista hypothesis for tongue protraction also requires substantial revision (Nishikawa and Gans, 1996). Specifically, denervation of the M. submentalis, which is the major force-producing element in the ballista hypothesis, had no effect on tongue protraction in B. marinus, whereas denervation of the Mm. genioglossus basalis and medialis reduced tongue protraction significantly. From these experiments, Nishikawa and Gans (1996) concluded that the M. genioglossus medialis not only stiffens the tongue during protraction, but also is the main force-generating element that pulls the tongue forward out of the mouth. We can now examine why the models of Emerson (1977) and Gans and Gorniak (1982a,b), although based on accurate and repeatable observations, failed to identify the muscles that are responsible for tongue protraction in toads. First, neither study described the kinematics of tongue protraction in toads with either kinematic profiles or trajectory analyses, so both studies overlooked the fact that the tongue normally elongates by approximately 180% of its resting length during protraction (Nishikawa and Gans, 1996). Second, EMG studies were relatively uninformative because numerous muscles are activated simultaneously during feeding (Gans and Gorniak, 1982b), which makes it difficult to understand how each contributes to feeding movements. Furthermore, electromyographic data

129

5. Feeding in Frogs were positively misleading because some muscles that are active during tongue protraction (i.e., the M. submentalis) appear to have little or no effect on tongue movements as demonstrated by surgical denervation experiments (Nishikawa and Gans, 1996). Finally, the results of muscle stimulation experiments were also positively misleading. At least three repeatable results were misinterpreted by Emerson (1977), Gans and Gorniak (1982a,b), or both. First, Emerson (1977) reported accurately that stimulation of the M. depressor mandibulae is insufficient to open the mouth of a spinal pithed toad. The explanation for this result, however, is not that the force produced by the muscle is insufficient to open the mouth, but rather that, even in spinal pithed toads, tonic contractions of the Mm. levator mandibulae resist mouth opening (Nishikawa and Gans, 1992). During normal feeding, this tonic activity is inhibited during mouth opening so that the M. depressor mandibulae does not have to overcome the additional force produced by tonic activity. When the M. levator mandibulae is denervated, stimulation of the M. depressor mandibulae results in rapid opening of the mouth (Nishikawa and Gans, 1992). Second, Emerson (1977) accurately reported that stimulation of the M. geniohyoideus causes the mouth to open. Once again, however, the explanation is rather complex. In this case, the hypoglossal nerve runs through the body of the M. geniohyoideus and it contains sensory fibers from the tongue that, when stimulated, inhibit tonic contractions of the M. levator mandibulae (Nishikawa and Gans, 1992). When the M. geniohyoideus is stimulated, the hypoglossal nerve is also stimulated, and tonic contractions of the M. levator mandibulae are inhibited. In this case, stimulation of the M. geniohyoideus causes the mouth to open, but it takes less force to open the mouth because the tonic contractions of the M. levator mandibulae are inhibited by electrical stimulation of the hypoglossal nerve that runs through the belly of the M. geniohyoideus. When the hypoglossal nerve is transected before it enters the M. geniohyoideus, stimulation of the M. geniohyoideus no longer produces mouth opening because the tonic contractions of the M. levator mandibulae are no longer inhibited (Nishikawa and Gans, 1992). Both of these examples illustrate the fact that muscle stimulation experiments can be positively misleading because the neural pathways, both sensory and motor, may remain intact even after spinal pithing and affect the force necessary to achieve a given movement. In muscle stimulation experiments, tonic muscle activity may be present that is not present during normal behavior in the intact animal. Furthermore, electrical stimuli may activate not only muscle fibers but also

nearby nerve fibers. In turn, stimulation of sensory nerve fibers may activate central neural circuits that modulate tonic activity of other muscles, thereby changing the amount of force that is necessary to achieve a given movement. For these reasons, the results of muscle stimulation experiments should always be interpreted with caution. Finally, both Emerson (1977) and Gans and Gorniak (1982b) noted that stimulation of the Mm. genioglossus in a spinal pithed toad does not result in protraction of the tongue. Based on this and other observations, Emerson (1977) hypothesized that the hyoid played an important role in tongue protraction, whereas Gans and Gorniak (1982a,b) hypothesized that the M. submentalis was the major force-generating element for tongue protraction. In contrast, denervation experiments suggest that the Mm. genioglossus are the major forcegenerating elements for tongue protraction during feeding (Nishikawa and Gans, 1996). The resolution of these conflicting observations seems to be that the dynamics of tongue protraction, which in toads involves large, simultaneous displacements of the jaws and tongue in as little as 35 msec (Nishikawa and Gans, 1996), cannot be duplicated under the static conditions in which muscle stimulation experiments necessarily are conducted. In my opinion, our current understanding of the feeding mechanisms of anurans has come mostly from detailed anatomical descriptions, kinematic analyses of movement, including both kinematic profiles and trajectory analyses, and experimental denervation of feeding muscles. In the case of anuran feeding behavior, both electromyographic studies and muscle stimulation experiments have been mostly uninformative and sometimes even misleading. An understanding of the biomechanics of complex anatomical systems can only be achieved by using as many techniques as possible to develop and test hypotheses about function. C. Functional Diversification among Anuran Taxa Over the past several years, my students and I, along with several collaborators, have used many different techniques to study the function of the anuran feeding apparatus. Detailed studies have been published for several anuran species, including D. pictus (Nishikawa and Roth, 1991); S. multiplicata (O'Reilly and Nishikawa, 1995); Hyla cinerea (Deban and Nishikawa, 1992); Pachymedusa dacnicolor (Gray and Nishikawa, 1995); B. marinus (Nishikawa and Gans, 1996); Dendrohates, Phyllobates, and Epipedobates (Wiltenmuth and Nishikawa, 1994); R. pipiens (Anderson, 1993); H. marmoratum (Ritter and Nishikawa, 1995); and

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Phrynomerus bifasciatus (Jaeger and Nishikawa, 1993; Meyers et al, 1996). From these comparative studies, we have identified three different mechanisms that anurans use to protract their tongues during feeding in terrestrial environments. These mechanisms are mechanical pulling, inertial elongation, and hydrostatic elongation, and each is described in detail in the following sections. All of the nearly 150 species that have been examined so far fall into one of these categories, although additional mechanisms, such as hyoid pushing in mesobatrachians (see Section II,C; O'Reilly and Nishikawa, 1995), may also be present. 1, Mechanical

Pulling

The first mechanism of tongue protraction is mechanical pulling, here exemplified by H. cinerea (Fig. 5.8). It is found in all archaeobatrachian lineages, including Ascaphus (Ascaphidae) (Nishikawa and Cannatella, 1991), Leiopeltna (Leiopelmatidae), Bombina (Bombinatoridae), and Discoglossus (Discoglossidae) (Nishikawa and Roth, 1991), as well as in some mesobatrachians (e.g., Pelobates and Spea) and some neobatrachians (e.g., Hyla). Anatomically, the tongues of mechanical pullers tend to be round in shape, broadly attached to the floor of the mouth, and there is much interdigitation of the M. hyoglossus and M. genioglossus medialis throughout the tongue pad (MagimelPelonnier, 1924; Regal and Gans, 1976; Horton, 1982). The ventralmost fibers of the M. hyoglossus insert near the anterior tip of the tongue (Horton, 1982). In mechanical pullers, the function of the tongue protractor muscle M. genioglossus is most like that of typical vertebrate skeletal muscle. Both the M. genioglossus and the tongue as a whole shorten during protraction as the fibers of the M. genioglossus contract and pull the tongue tip toward the mandibular symphysis (Fig. 5.8). This mechanism is essentially similar to that proposed by Regal and Gans (1976). In mechanical pullers, the resting length of the tongue is approximately equal to the length of the mandibles (Figs. 5.3A-5.3C). The tongue shortens as the M.

F I G U R E 5.8. Selected frames from a normal prey-capture sequence for Hyla cinerea, showing mechanical pulling. The number in the right-hand corner of each picture indicates the time (msec) from the onset of mouth opening. The squares in the background are 1 X 1 cm. The short tongue can be seen at full protraction ait = 17 msec. In this sequence, the frog uses jaw prehension to capture the waxworm. The craniovertebral joint is flexed downward between t = 42 and t = 92 msec, and at f = 92 msec, the jaws close on the prey.

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5. Feeding in Frogs TABLE 5.1 Characteristics of the Different Mechanisms of Tongue Protraction Characteristics

Hydrostatic elongation

Inertial elongation

Mechanical pulling

Example

Hyla cinerea

Bufo marinus

Hemisus marmoratum

Tongue movement

Tongue shortens

Tongue elongates 180%

Tongue elongates 200%

Velocity (cm/sec)

79

286

24

Acceleration (m/sec^)

66

310

3.5

Tongue/jaw synchrony

No

Yes

No

Aiming

Distance

None

Distance, azimuth, elevation

Accuracy

95%

33%

>99%

On-line correction

Yes

No

Yes

Feedforward control

Yes

Yes

Yes

Feedback control

Yes

No

Yes

Hypoglossal afferents

No

Yes

No

genioglossus contracts, pulling the tongue pad upward and forward toward the symphysis (Figs. 5.4, 5.5E, and 5.8). Thus, in mechanical pullers, the tongue is shorter at full protraction than it is at rest in the floor of the mouth. In H. cinerea, for example, the length of the tongue at maximum protraction is approximately 60% of its resting length (Fig. 5.4). Movements of the head, jaws, and tongue are small and rather asynchronous (Fig. 5.11) in mechanical pullers. Because the tongue shortens during protraction, the frogs must lunge forward with their entire bodies in order to place the tongue on the prey (Figs. 5.4,5.5A, and 5.8). When capturing relatively large prey, the frogs also exhibit head flexion in order to bring the tongue down onto the prey, and the prey are apprehended with the jaws (Figs. 5.4 and 5.8). For small prey, tongue prehension is used for prey capture and there is less flexion of the head (Fig. 5.5A). During feeding, the lower jaw tip is depressed and retracted slightly relative to the upper jaw tip (Fig. 5.5D). The short tongue can hardly be moved independently of the lower jaw (Fig. 5.5D) and the maximum reach of the tongue beyond the jaws typically is not more than a few millimeters (Fig. 5.4; Deban and Nishikawa, 1992). Relative to the lower jaw tip, to which the tongue is attached, the tongue reaches moderate velocities (79 cm/sec) and accelerations (66 m/sec^) during protraction (Table 5.1). Tongue movements can be corrected in progress within a single gape cycle and there is little, if any, ability to aim the tongue relative to the head (Deban and Nishikawa, 1992). In the two species of mechanical pullers that have been studied (Gray, 1997), prey capture success ranges from 95% in H. cinerea to 68% in H. arenicolor when feeding on relatively small, slow-moving prey such as waxworms.

2. Inertial Elongation In contrast to mechanical pullers whose tongues shorten during protraction, the tongues of many frogs elongate during protraction (Figs. 5.9 and 5.10). Given the fact that muscles can only contract to do work, and given that all frogs exhibit rather similar morphologies of the extrinsic tongue muscles in which most fibers run parallel to the long axis of the tongue, it is rather surprising that the tongues of these frogs can elongate beyond resting length during protraction. What mechanisms are responsible for tongue elongation and which muscles are responsible? Many anurans use inertia to elongate the tongue during protraction. Inertial elongation is found among several anuran lineages, including some leptodactyline leptodactylids {Physalaemus and Pleurodema), some eleutherodactyline leptodactylids {Eleutherodactylus), all bufonids, all phyllomedusine hylids, and all ranoids except hemisotids and microhylids (Nishikawa et ah, 1992). This chapter uses the marine toad, B. marinus, as an example of a typical inertial elongator (Fig. 5.9). The tongues of inertial elongators are similar morphologically to those of mechanical pullers, except that the fibers of the protractor and retractor muscles are relatively longer, which produces a posterior flap that is free from the floor of the mouth (Magimel-Pelonnier, 1924; Regal and Gans, 1976; Horton, 1982). In addition, there is less interdigitation between the M. hyoglossus and the M. genioglossus in the tongue pad, and the ventralmost fibers of the M. hyoglossus recurve to insert in the posterior, rather than the anterior, part of the tongue (Horton, 1982). The relative mass of the tongue is typically smaller in inertial elongators (0.5%) than in mechanical pullers (1.0%).

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The initial stages of tongue protraction are similar in mechanical pullers and inertial elongators. Inertially elongated tongues shorten at first as the M. genioglossus medialis contracts and accelerates the tongue pad upward and forward. In inertial elongators, however, the tongue elongates by as much as 180% of its resting length under its own inertia after the initial shortening phase (Nishikawa and Gans, 1996). Inertial elongation appears to be the fastest and least accurate mechanism of tongue protraction in anurans. In toads (B. marinus), the tongue tip reaches velocities of up to 270 cm/sec and accelerations of 310 m/sec^ (more than 30 times gravity) relative to the tips of the mandibles during protraction (Nishikawa and Gans, 1996). These velocities and accelerations are several times greater than those of mechanical pullers (Table 5.1). Toads are also much less accurate (30%) at capturing prey than mechanical pullers (Table 5.1; Gray, 1997). Because tongue protraction is rapid and ballistic, tongue movements cannot be corrected within the gape cycle (Nishikawa and Gans, 1996). Like mechanical pullers, toads possess little, if any, ability to aim the tongue relative to the head. The complexity of tongue and jaw movements during feeding in inertial elongators is demonstrated by the trajectories of the upper jaw tip, mandibular tip, and lingual tip (Fig. 5.6), which show how the individual movements of these elements contribute to tongue protraction (Nishikawa and Gans, 1996). A remarkable feature that emerges from this analysis is that the lingual tip follows an almost straight line from mouth to prey, despite rotation of the tongue over the mandibular symphysis during protraction, from top to bottom as well as rear to front, and despite substantial changes in the shape of the tongue during protraction (Fig. 5.9). The straight-line trajectory of the lingual tip relative to an external reference is the sum of the relative trajectories of all the elements to which the tongue is attached: (1) the trajectory of the upper jaw tip relative to an external reference, which is first downward and forward, then upward and back (Fig. 5.6A); (2) the trajectory of the mandibular tip relative to that of the upper jaw tip, which is mostly restricted to the vertical plane

F I G U R E 5.9. Selected frames from a normal prey-capture sequence for Bufo marinus, showing inertial elongation. The number in the right-hand corner of each picture indicates the time (msec) from the onset of mouth opening. The squares in the background are 1 X 1 cm. The tongue shortens at first (f = 8 msec) but then elongates by up to 180% of its resting length under its own momentum (f = 2 5 42 msec).

5. F e e d i n g in Frogs

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(Fig. 5.6D); and (3) the trajectory of the lingual tip relative to the mandibular tip, which first rises as the tongue shortens and moves forward, but then changes direction abruptly as the lingual tip passes beyond the oral cavity and moves downward and forward as the tongue elongates (Fig. 5.6E). Trajectory analysis demonstrates that precise coordination among head, jaw, and tongue movements is responsible for the straight trajectory of the tongue tip from mouth to prey. First, the downward and forward and then the upward and back movement of the head counteracts the tendency for mouth opening to produce retraction of the lower jaw, which would occur without compensatory head movements because the jaw tip must transcribe a circular path about the jaw joint. Furthermore, a large upward acceleration of the lingual tip occurs simultaneously with a large downward acceleration of the mandibular tips (Fig. 5.11). The acceleration of the tip of the mandibles relative to that of the upper jaw is oriented downward, whereas the acceleration of the lingual tip relative to that of the mandibles is oriented upward and forward. These large, synchronous, partially opposed jaw and tongue movements add together precisely to generate the straight lingual trajectory (Nishikawa and Gans, 1996). Nishikawa and Gans (1996) used a simple matrix model to demonstrate that the linear trajectory of the tongue depends on the simultaneous accelerations of tongue and jaws. In this model, the relative timing of displacements of the jaws and tongue was varied systematically and the change in tongue trajectory was measured. This analysis showed that changes in the relative timing of the displacements had only a small effect on the horizontal position of the tongue tip. However, the vertical position of the lingual tip strongly depends on the simultaneous displacement of the mandibular and lingual tips. If the vertical displacements of the lingual tip are added to the vertical displacements of the upper jaw and mandibular tips 8 msec (i.e., one video field) earlier than they actually occur, then the trajectory of the lingual tip would intersect that of the upper jaw (i.e., the tongue would contact the palate). If the lingual displacements occur 8 msec too late, then the lingual tip would drop with the mandible before accelerating upward, which would

FIGURE 5.10. Selected frames from a normal prey-capture sequence for Hemisus marmoratum, showing hydrostatic elongation. The number in the right-hand corner of each picture indicates the time (msec) from the onset of mouth opening. The squares in the background are 1 X 1 cm. The tongue elongates slowly during protraction {t = 25-125 msec).

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Hemisus

>

-0.75 -200

-100

Time (ms) F I G U R E 5.11. Horizontal (above) and vertical (below) displacements between successive frames for Hyla, Bufo, and Hemisus (upper jaw tip, closed circles; mandibular tip, open circles; lingual tip, open squares). For Hyla, horizontal displacements of the upper jaw tips are greater than those of the mandibular and lingual tips, whereas for Bufo and Hemisus, horizontal displacements of the lingual tip are greater than those of the upper jaw and mandibular tips and are positive during protraction and negative during retraction. In Bufo, the downward displacement of the mandible during mouth opening occurs simultaneously with a large upward displacement of the lingual tip, whereas movements of the jaws and tongue are asynchronous in Hyla and Hemisus.

produce a nonlinear trajectory that deviates from the observed trajectory by more than 1 cm (approximately 20% of tongue length). Thus, the synchrony of the large displacements of the tongue and mandibles is necessary for successful prey capture in inertial elongators, but not in mechanical pullers (Table 5.1). 3. Hydrostatic

Elongation

The third mechanism of tongue protraction, hydrostatic elongation, is possessed only by members of the families Hemisotidae and Microhylidae. This chapter uses Hemisus marmoratum as a representative hydrostatic elongator (Fig. 5.10). Hemisus may elongate its tongue up to 200% of resting length (Ritter and Nishikawa, 1995). However, it protracts its tongue too slowly to use an inertial mechanism. The tongue tip reaches maximum velocities of 15 cm/sec (nearly 20 times slower than inertial elongators) and accelerations of 0.5 m/sec^ (more than 600 times slower than inertial elongators. Table 5.1). Instead of inertia, a hydrostatic mechanism is used to protract the tongue (Nishikawa et al, 1995). In hydrostatic elongators, the tongue protractor muscle (M. genioglossus) consists of two compartments, one in which the muscle fibers are oriented par-

allel to the long axis of the tongue as in other frogs and one in which the fibers are oriented vertically (Nishikawa et al, 1995; Fig. 5.2D). During protraction, the volume and the width of the tongue remain constant. When the vertical fibers contract, they decrease the thickness of the tongue and, because the volume of the tongue is constant, this change in shape is translated directly into tongue elongation (Nishikawa et ah, 1995). A decrease in tongue thickness of 50% (from 2 to 1 mm) is translated into a 100% increase in tongue length (from 5 to 10 mm). Ritter and Nishikawa (1995) favored a hydraulic mechanism of tongue elongation in Hemisus because they overlooked the presence of the dorsoventral compartment of the M. genioglossus in H. marmoratum. The presence is apparent only in sections, and not in gross dissection. In contrast to inertial elongators, which must protract their tongues rapidly in order to achieve elongation, hydrostatic elongators may protract their tongues either slowly or rapidly. In terms of prey capture, H. marmoratum is the slowest and most accurate of the anuran species that have been studied to date (Ritter and Nishikawa, 1995). Other hydrostatic elongators, such as Dyscophus insularis, protract their tongues more rapidly than Hemisus. Hydrostatic elongators exhibit high accuracy of prey capture (99%; Gray, 1997) and on-line

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5. Feeding in Frogs correction of tongue movements within a gape cycle (Table 5.1). In contrast to both mechanical pullers and inertial elongators, there is very little head movement during feeding in hydrostatic elongators, although the head moves slightly upward and forward and then down and back during feeding (Fig. 5.7A). The lower jaw tip is both depressed and retracted during mouth opening (Fig. 5.7D), and retraction of the lower jaw counteracts the upward rotation of the tongue tip relative to the mandibles so that the initial trajectory of the tongue is straight out of the mouth, rather than upward and forward as in inertial elongators (Fig. 5.7C). In contrast to inertial elongators, the tongue does not follow a straight line from mouth to prey during protraction (Fig. 5.7E). As in mechanical pullers, movements of the head, jaws, and tongue are asynchronous (Fig. 5.11). All anurans studied to date can aim their heads relative to their bodies and do so readily during feeding. In addition, some mechanical pullers can modulate tongue protraction distance in response to prey distance (Deban and Nishikawa, 1992; O'Reilly and Nishikawa, 1995). All hydrostatic elongators can modulate tongue protraction distance in response to prey distance, and in addition are the only anurans that can aim their tongues relative to their heads in dimensions other than distance (Ritter and Nishikawa, 1995; Jaeger and Nishikawa, 1993; Meyers et al, 1996). Phrynomerus bifasciatus (family Microhylidae) aims its tongue relative to the head in distance and azimuth (Jaeger and Nishikawa, 1993; Meyers et al, 1996), whereas H. marmoratum aims its tongue relative to its head in distance, azimuth, and elevation (Ritter and Nishikawa, 1995). Insight into the mechanism of tongue aiming comes from denervation experiments in Hemisus (Ritter and Nishikawa, 1995) and Phrynomerus (Meyers et ah, 1996). In both species, when unilateral denervation of the M. genioglossus is performed, the tongue bends toward the inactivated side. In Phrynomerus, the tongue deviates by up to 90° from the target, whereas in Hemisus it deviates by more than 180°. These experiments are consistent with the proposed hydrostatic mechanism of tongue protraction, in which the tongue bends toward the inactivated side to equalize tensile stresses in the tongue. They also suggest that microhylids and hemisotids may regulate the azimuth of the tongue by differential recruitment of the right and left sides of the M. genioglossus (Ritter and Nishikawa, 1995). In contrast, the amplitude of tongue movement is reduced after unilateral denervation of the M. genioglossus in B. marinus, but the direction of tongue protraction is unaffected (personal observation). Finally, H. marmoratum is the only frog that is known to possess a truly prehensile tongue. In other frogs, the

tongue sticks to prey by wet adhesion. In Hemisus, the tongue not only sticks to prey but actually grasps it (Ritter and Nishikawa, 1995). If a termite is held with forceps, the tongue of H. marmoratum can generate enough tensile force to tear it in half. Muscle denervation experiments demonstrate that activation of the M. hyoglossus is necessary for this prehensile function. The M. hyoglossus sends a fascicle into each lobe of the bilobed tongue and, when inactivated, prehension is eliminated, although the frogs can still capture prey using lingual adhesion (Ritter and Nishikawa, 1995; Tso et al, 1995). These experiments also demonstrate that the M. hyoglossus plays an important role in swallowing. Intact Hemisus always ingests, transports, and swallows termites in a single movement, whereas the tongue is often protracted with a previously captured termite still adhering to it after M. hyoglossus denervation.

IV. NEURAL CONTROL OF PREY CAPTURE Until the 1970s, when in vitro intracellular recording techniques became feasible in the intact vertebrate central nervous system, patterns of motor output were widely believed to result from a chain of reflex-like interactions between sensory and motor neurons (Delcomyn, 1980). Since then, however, in vitro and deafferentation studies in a large number of animals, ranging from leeches to primates, have shown that intrinsic patterns of motor output are produced in the absence of sensory input (Delcomyn, 1980; Grillner, 1985). The neurons responsible for producing this output have been termed central pattern generators (CPGs). These CPGs are implicated in the production of numerous behavior patterns, including breathing, swimming, walking, and feeding. In frogs, a variety of evidence points to the medial reticular formation as a possible site of the CPG for prey capture (Matsushima et al, 1989; Weerasuriya, 1989). Unlike a spinal cord in a dish, however, all behaving animals must produce varied patterns of motor output that are exquisitely appropriate to the animal's changing conditions. Adaptive behavior involves the production of a motor response that is appropriate in the context of incoming sensory stimuli. In order to understand the neural basis of adaptive behavior, we need to know how central pattern generators and motor neurons interact with sensory receptors to produce motor output that tracks changes in an animal's external environment as well as its internal state. Current theories suggest that sensory input acts directly on CPGs to change the frequency, amplitude, and phase of

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motor patterns (Rossignol et al, 1988). In theory, such changes result from the effects of neurotransmitters and neuromodulators on the membrane properties of CPG neurons (Harris-Warrick, 1988). Empirically, however, the mechanisms by which sensory input influences CPGs are not yet well understood, even in relatively well-studied systems such as lamprey swimming (Grillner et al, 1988). Comparative studies of the neural control of movement should be conducted in the context of the adaptive modification of CPG activity by incoming sensory input. Within this conceptual framework, we can investigate which sensory modalities are involved in modulating prey capture movements, how sensory information influences the pattern of motor activity produced by central pattern generators, and how sensory modalities interact to modulate movement. We can then proceed to ask whether species differ in these aspects of motor control. There are several problems that frogs must overcome to capture prey successfully. These include detecting the prey, locating it in space, and analyzing its relative size, shape, and speed of movement. Once prey are detected and located, a frog must respond to it before it escapes, place its tongue accurately on the prey, apprehend it, and bring it back to the mouth. Apprehension requires planning and execution of precisely coordinated movements of the head, jaws and tongue (Nishikawa and Gans, 1996). Some of these problems will be discussed later. Other problems, such as locating prey in space (Ingle, 1983), are beyond the scope of this chapter. In terms of neural control, prey capture in frogs is a goal-oriented movement that is similar to reaching in humans (Gottlieb et al, 1989; Flanders et al, 1992) or pecking in pigeons (Bermejo and Ziegler, 1989). Performance of these goal-oriented tasks requires sensory information about the target and sensory information about the animal's internal state, both of which are used to modulate the output of CPGs. Relevant information about the target is often obtained visually and includes target position in three dimensions (distance, azimuth, and elevation), size, shape, and velocity. Relevant information about the animal's internal state is obtained through a variety of proprioceptive sense organs distributed throughout the body and includes the length and mass of musculoskeletal elements, the force-velocity relationships and mechanical advantage of the muscles, the position of musculoskeletal elements before and during movement, and the action of forces such as gravity and inertia. Prey recognition has been studied extensively in amphibians (Ewert, 1987; Roth, 1987), and a review of these studies is beyond the scope of this chapter. To date, motor control of prey capture has been studied in

detail in only two anuran species, R. pipiens (family Ranidae) and B. marinus (family Bufonidae). Methods that have been used to study neural control of prey capture include behavioral studies, deafferentation experiments, electrophysiological recording, and neuroanatomical tracing. These studies have focused on the modulatory effects of visual analysis of prey features (Anderson, 1993; Valdez and Nishikawa, 1997), of proprioceptive tongue afferents (Nishikawa and Gans, 1992; Nishikawa et al, 1992; Anderson and Nishikawa, 1993, 1997), and of the interaction between vision and proprioception in controlling feeding movements (Anderson and Nishikawa, 1993,1996). The modulatory effects of visual input on prey capture movements, the modulatory effects of tongue afferents on prey capture movements, and the interaction between vision and proprioception in controlling feeding movements are described in detail next. A. Visual Analysis of Prey Features Some anurans will snap in response to tactile stimulation (Comer and Grobstein, 1981). Some species also can locate prey on the basis of olfactory cues alone (Dole et al, 1981; Shinn and Dole, 1978). Even auditory stimuli can be used to locate prey (Martof, 1962; Jaeger, 1976). However, vision appears to be the dominant sensory modality that most frogs use to detect prey. When vision is intact, frogs seldom lunge or snap at stationary prey (Lettvin et al, 1959; Kaess and Kaess, 1960; Ewert, 1985; Satou and Shiraishi, 1991). There have been numerous studies of the visual cues used in prey recognition by toads (reviewed in Ewert, 1987). These studies measured the rates of orientation and snapping elicited by artificial, two-dimensional, prey-like stimuli that differed in shape, size, and speed of movement. These studies showed that toads (B. hufo) exhibit higher orienting rates for rectangular objects which move in a direction that is parallel to their long axis (i.e., worm orientation) than for similar objects that move perpendicular to their long axis (i.e., antiworm orientation). Not only the tendency to respond, but also patterns of movement change in response to prey characteristics (Anderson, 1993; Anderson and Nishikawa, 1996; Valdez and Nishikawa, 1997). For example, R. pipiens (an inertial elongator, family Ranidae) exhibits different behavior patterns to capture small vs large prey (Anderson, 1993). Small prey are captured with the tongue and are transported to the esophagus without contacting the jaws (here termed "tongue prehension"), whereas large prey are first contacted with the tongue but the head rotates downward, the prey are captured in the closing jaws, and are transported into the oral cavity with the forelimbs (here termed "jaw

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prehension"). During tongue prehension, the head remains more nearly level with respect to the horizon, the lunge distance is shorter, the tongue is protracted to a greater distance, and the mouth remains open for a longer time than during jaw prehension (Anderson, 1993). Because they depend heavily on lingual adhesion to capture prey, it is not surprising that frogs with generalized diets use different strategies to capture prey of different sizes. Tongue prehension is more effective for capturing small prey than jaw prehension because the prey is transported to the esophagus in a single movement, which offers less chance for escape. However, tongue prehension is effective only if the mass of the prey is less than the adhesivity between tongue and prey. Thus, jaw prehension is more effective for capturing large prey (Anderson and Nishikawa, 1996; Valdez and Nishikawa, 1997). It has been shown that the decision to use jaw vs tongue prehension is made on the basis of a visual analysis of prey size (Anderson and Nishikawa, 1996). When offered pieces of earthworm ranging in size from 1.5 to 4.5 cm, adult frogs {R. pipiens) always use tongue prehension to capture 1.5-cm prey and jaw prehension to capture 2.0-cm and larger prey (Figs. 5.13A and 5.13B). Not surprisingly, the distinction between "small" vs "large" prey is relative to the size of the frog. Larger frogs switch behavior patterns at larger prey sizes than smaller frogs. Another study compared prey capture movements across five different types of live prey (earthworms, waxworms, newborn mice, crickets, and termites) in the Australian frog, Cyclorana novaehollandiae (a mechanical puller, family Hylidae) (Valdez and Nishikawa, 1997). This study showed that these frogs modulate their feeding movements in response to features of prey in addition to size, especially shape and speed of movement. It also showed that the ability to use a visual analysis of prey characteristics to modulate feeding movements is widespread among frogs. Distantly related frogs with different tongue morphologies (i.e., R. pipiens, family Ranidae, and C. novaehollandiae, family Hylidae) use tongue prehension to capture small prey and jaw prehension to capture large prey. However, some frogs appear to have lost the ability to switch between tongue prehension and jaw prehension. For example, B. marinus uses tongue prehension to capture large prey as well as small prey, whereas Leptopelis uses jaw prehension to capture both small and large prey. B. Role of Tongue A£f erents In both frogs (R. pipiens) and toads (B. marinus), mechanosensory afferents of the tongue, innervated by

the hypoglossal nerve, serve a variety of functions in feedforward (i.e., open loop, planned in advance) control of jaw and tongue movements during prey capture. One function is to modulate the phase of activity in the mouth opening and closing muscles (Nishikawa and Gans, 1992; Anderson and Nishikawa, 1993). In intact frogs and toads, the mouth opening muscles are active approximately 90 msec before the mouth closing muscles. After bilateral transection of the hypoglossal nerves, the mouth remains closed when Rana or Bufo attempt to feed because the M. levator mandibulae and the M. depressor mandibulae are activated simultaneously (Figs. 5.12E-5.12H and 5.13C). Thus, sensory input from the tongue coordinates jaw muscle activity by sending an afferent signal to the brain that delays activity of the jaw levators. This signal is produced

After

Before

200 ms FIGURE 5.12. The function of hypoglossal afferents in the marine toad, Bufo marinus. (Left) Normal feeding in an intact toad before deafferentation, illustrating inertial elongation. (A) The toad orients toward the prey, (B) the mouth opens and the tongue is protracted, (C) the tongue is retracted, and (D) the mouth closes. (Right) After deafferentation, (E) toads orient normally, but (F-H) the mouth fails to open during the feeding attempt. Electromyographic traces on the left show activity in the jaw muscles depressor mandibulae (DM) and levator mandibulae (LM) in intact toads before deafferentation. DM reaches its peak activity approximately 90 msec before LM. Right traces show that DM and LM reach their peak activity simultaneously after deafferentation. These results demonstrate that hypoglossal afferents modulate the phase of activity in the jaw muscles during feeding.

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Before

After

would be absent, or would have a different function, in mechanical pullers and hydrostatic elongators because these frogs lack synchronous acceleration of tongue and jaws, as well as a straight trajectory of the tongue tip from mouth to prey (Table 5.1). Studies on the evolution of hypoglossal afferents are described in more detail later (Section V,C). C. Interactions b e t w e e n Tongue Afferents and Visual Input

FIGURE 5.13. The function of hypoglossal afferents in the leopard frog, Rana pipiens. Top portion: (A) intact frogs use tongue prehension to capture small prey, (B) intact frogs use jaw prehension to capture large prey, (C) when deafferented frogs attempt to feed on small prey, the mouth fails to open; but (D) when deafferented frogs attempt to feed on large prey, the mouth opens normally. Bottom portion: The four panels on the left show intact frogs feeding on earthworm pieces that vary in size from 1.5 to 4.5 cm (size of prey is indicated by numbers in upper right corner of each picture). The frogs always exhibit tongue prehension for 1.5-cm prey and jaw prehension for 2.0-cm and larger prey. The five panels on the right show deafferented frogs feeding on earthworm pieces. After deafferentation, the mouth always fails to open when the frogs feed on 1.5-cm prey and the mouth always opens when the frogs feed on 2.5-cm and larger prey. However, when the frogs feed on 2.0-cm prey, they alternate randomly between opening and not opening the mouth. This result demonstrates that hypoglossal afferents in the tongue influence motor program choice.

before the onset of mouth opening and may result from stimulation of tongue mechanoreceptors by retraction of the hyoid during the preparatory stage of feeding. In intact frogs and toads, we hypothesize that this afferent signal coordinates the simultaneous acceleration of the tongue and mandibles, which ensures that the lingual trajectory will fall on a straight path from mouth to prey (Nishikawa and Gans, 1996). If this hypothesis is correct, then we would expect that these afferents

It is somewhat surprising that afferent input from the tongue interacts with visual input in controlling prey capture movements. In R. pipiens, the modulatory effect of tongue afferents depends on attributes of the visual stimulus that is presented to elicit feeding (Anderson and Nishikawa, 1993). When presented with small prey, deafferented frogs attempt to use tongue prehension to capture the prey and the mouth remains closed, as noted earlier. However, when the same deafferented frogs are presented with large prey, they use jaw prehension to capture the prey and their mouths open normally (Fig. 5.13; Anderson and Nishikawa, 1993). These results demonstrate that the modulatory effect of hypoglossal afferents on feeding movements is itself modulated by visual input, and they suggest that visual input has a gating effect on the hypoglossal afferents. Hypoglossal afferents also interact with visual input during motor program choice in R. pipiens (Anderson and Nishikawa, 1996). As mentioned previously, intact adult frogs use tongue prehension to capture 1.5-cm pieces of earthworm, but switch to jaw prehension for 2.0-cm and larger prey. Based on the results of the hypoglossal deafferentation experiments described earlier, we would expect that the mouth would never open for 1.5-cm prey and always open for 2.0-cm and larger prey. When the tongue afferents are inactivated, the mouth never opens for 1.5-cm prey and always opens for 2.5-cm and larger prey, as expected. However, the frogs alternate randomly between tongue prehension and jaw prehension when 2.0-cm prey are offered (Fig. 5.13). Thus, the ability to choose between motor programs for tongue prehension and jaw prehension is impaired by hypoglossal transection. In R. pipiens, hypoglossal afferents not only subserve typical motor control functions, such as modulating motor output, but also have become involved in behavioral decision making. Neural network modeling is being used in conjunction with neuroanatomical tracing studies to understand the premotor circuits that underlie interactions between vision and proprioception in the control of feeding movements (Corbacho et al, 1996).

5. Feeding in Frogs V. EVOLUTION OF THE FEEDING APPARATUS A major goal of comparative and functional morphology is to understand the evolution of complex functional systems. This goal can be achieved using cladistic analysis, in which a phylogeny is obtained for the group, data are collected on characters of interest, and the distribution of these characters is mapped onto the phylogeny. A cladistic analysis permits identification of the ancestral condition for the character(s) of interest, which represents the starting point for evolutionary diversification. This type of analysis also locates transitions in character state on the phylogeny that indicate when and how the condition has changed. Studies in my laboratory have used a cladistic approach to study the evolution of mechanisms of tongue protraction and neural control of feeding behavior in anurans, and the results of these studies are described next. A. Evolutionary Transitions in Mechanisms of Tongue Protraction A phylogenetic analysis (Fig. 5.14) of feeding behavior in 148 species of frogs representing 15 of approximately 330 described genera (23%) and 20 of 27 families (74%) was conducted by mapping characters derived from high-speed video motion analysis (Nishikawa ei al., 1992) onto the most recent hypothesis of frog phylogeny (Ford and Cannatella, 1993). The results of this analysis show that all archaeobatrachian frogs that have been studied {Ascaphus, Ascaphidae; Leiopelma, Leiopelmatidae; Bomhina, Bombinatoridae; and Discoglossus, Discoglossidae) possess mechanical pulling tongues that shorten during protraction (Fig. 5.14). Some members of the clades Mesobatrachia (e.g., Pelobates) and Neobatrachia (e.g., hyline hylids) also possess short tongues (Fig. 5.14). The most parsimonious interpretation of the observed character distribution across taxa is that anurans ancestrally possess tongues that shorten during protraction and therefore can be protracted only a few millimeters beyond the tips of the mandibles. Other ancestral characteristics include (1) downward bending of the lower jaw during mouth opening and (2) use of the whole body as a projectile, which brings the short tongue into contact with the prey (Nishikawa et al, 1992). Tongues that elongate during protraction have evolved many times independently from mechanical pulling tongues that shorten during protraction (Fig. 5.14). It is difficult to estimate the exact number of independent evolutionary events due to the lack of resolution of family relationships (Cannatella et al, 1992).

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However, at least seven lineages possess elongating tongues (Fig. 5.14). Among mesobatrachians, the most parsimonious hypothesis is that mechanical pulling is ancestral and inertial elongation has evolved once in the common ancestor of Megophrys montana and Leptobrachium. Megophrys is the only known genus in which the constituent species differ in tongue length, with M. aceras using mechanical pulling and M. montana using inertial elongation to protract the tongue (Fig. 5.14). Among neobatrachians, mechanical pulling also appears to be the ancestral method of tongue protraction based on parsimony analysis. The most parsimonious hypothesis is that mechanical pulling is ancestral for the group and that elongating tongues evolved independently in as many as six different lineages: (1) Ceratophrys and Chacophrys, (2) Physalaemus and Fleurodema, (3) Eleutherodactylus and Syrrhophus, (4) the phyllomedusine hylids, (5) the bufonids, and (6) the ranoids (Nishikawa et al, 1992). The most variable families are the Leptodactylidae (which is probably not monophyletic; Ford and Cannatella, 1993) and Hylidae, both of which possess species with both long and short tongues. Most frogs with elongating tongues share many derived behavior patterns, particularly a reduction in lunge length (Nishikawa et al, 1992). The phyllomedusine hylids are exceptional in retaining a long lunge despite possessing a long tongue (Gray and Nishikawa, 1995). However, there are many differences among long-tongued lineages as well. Long tongues appear to have evolved to enhance crypsis in Bufo (Gray, 1997), for catching rapidly moving prey in the phyllomedusines (Gray and Nishikawa, 1995), for capturing large prey in Megophrys (Emerson, 1985; Gans et al, 1991), and for capturing prey accurately in H. marmoratum (Ritter and Nishikawa, 1995). Among species with elongating tongues, all use inertial elongation to protract the tongue, except members of the families Microhylidae and Hemisotidae, all species of which use hydrostatic elongation. Given the phylogeny of Ford and Cannatella (1993), it appears that mechanical pulling is the ancestral tongue protraction mechanism, that inertial elongation evolved up to seven times independently from mechanical pulling, and that hydrostatic elongation evolved once or maybe twice from inertial elongation within the ranoid clade (Fig. 5.14). This hypothesis is somewhat counterintuitive, however, because hydrostatic elongation is the slowest mechanism of tongue protraction whereas inertial elongation is the fastest (Table 5.1). However, these tongue types appear to represent a morphocline in terms of the amount of connective tissue in the tongue that would restrict elongation (see next section; Webster, 1996).

140

Kiisa C. N i s h i k a w a Ascaphus Leiopelma Bombina Discoglossus Scaphiopus Spea Pelobates Pelodytidae Megophrys aceras Megophrys montana Leptobrachium Rhinophrynidae Pipidae Limnodynastes Myobatrachinae Sooglossidae Heleophrynidae Ceratophrys Chacophiys Lepidobatrachus Leptodactylus Pleurodema Physalaemus Telmatobius Caudiverbera Eleutherodactylus Syrrhophus ] Brachycephalidae Bufonidae Rhinodermatidae Centrolenidae Pseudidae Hylinae

Protraction Mechanism • • •

mechanical pulling unknown none inertial elongation hydrostatic elongation I '

Hemiphractinae Pelodryadinae Phyllomedusinae Ranidae Arthroleptidae Hyperoliidae I Rhacophoridae Dendrobatidae Hemisotidae Microhylidae

F I G U R E 5.14. Cladogram illustrating the evolution of tongue protraction mechanisms among frogs. For mechanisms of tongue protraction, mechanical pulling is the ancestral condition. Inertial and hydrostatic elongation are derived conditions that evolved several times independently among frogs.

B. Morphological Correlates of Tongue Protraction Mechanisms It is interesting to ask what morphological changes are responsible for the profound functional changes in

the biomechanics of the feeding apparatus that have occurred during anuran evolution (Table 5.1). Comparative studies have demonstrated considerable diversity in the feeding behavior of frogs (compare Figs. 5.8, 5.9 and 5.10; Table 5.1). Anuran species vary

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5. Feeding in Frogs considerably in the length of the fully protracted tongue, which ranges from less than 10% of jaw length in semiaquatic species such as Lepidobatrachus llanensis (unpublished observation) to nearly 300% of jaw length in H. marmoratum (Ritter and Nishikawa, 1995). Even among frogs with relatively long tongues, species vary in the speed of tongue protraction from 24 cm/sec in the slowest hydrostatic elongators to 270 cm/sec in the fastest inertial elongators (Table 5.1). In anurans, these functional changes appear to have involved relatively small quantitative and qualitative changes in the anatomy and physiology of the muscles of the feeding apparatus. The transition from mechanical pulling to inertial elongation appears to have involved (1) a decrease in relative tongue mass; (2) an increase in the relative length of muscle fibers in both the M. genioglossus and M. hyoglossus; (3) a change in insertion of the M. hyoglossus from the anterior to the posterior part of the tongue pad (Horton, 1982); (4) a decrease in the amount of connective tissue (as measured subjectively from scanning electron micrography of muscles digested with NaOH), which appears to restrict tongue elongation in mechanical pullers (Webster, 1996); and (5) an increase in contraction velocity compared to mechanical pullers (Peters and Nishikawa, 1999). The transition from inertial to hydrostatic elongation involved only (1) the addition of a new dorsoventral compartment in the M. genioglossus, which elongates the tongue when it contracts; and (2) a further decrease in the amount of connective tissue in the tongue. Peters and Nishikawa (1999) completed a study of the contractile properties of the tongue protractor and retractor muscles of mechanical pullers, inertial elongators, and hydrostatic elongators. The studies show that although there are some differences (e.g., in contraction and half relaxation time of the muscles), the contractile properties of the muscles alone cannot account for differences in function (i.e., differences in length or velocity of tongue protraction). A major difference among frog tongues is in the amount of connective tissue they contain, as well as the orientation of collagen fibers within the tongue (Webster, 1996). Mechanical pullers have the most connective tissue, inertial elongators are intermediate, and hydrostatic elongators have the least. Furthermore, the orientation of collagen fibers also differs among taxa. Mechanical pullers have the largest proportion of fibers with low orientation angles (<55°) relative to the long axis of the tongue, inertial elongators are intermediate, and hydrostatic elongators have the most fibers with high orientation angles (>55°). In mechanical pullers, these parallel connective tissue fibers would

actively resist elongation of the tongue. In H. marmoratum, most of the collagen fibers are oriented nearly perpendicular to the long axis of the tongue (modal angle = 80°), where they do not resist tongue elongation but instead resist increases in tongue diameter (Nishikawa et fl/., 1999). The differences in tongue morphology among mechanical pullers, inertial elongators, and hydrostatic elongators are so small and subtle that it has not proved possible to predict differences in function on the basis of anatomical differences. Ironically, the functions of most of the larger and less subtle anatomical differences that have been described among anuran species remain obscure. Based on the preliminary data described earlier, it seems quite likely that relatively small quantitative differences in the amount and orientation of connective tissue in the tongue, via their effects on passive properties, may have a greater effect on tongue function than anatomical and physiological differences in tongue muscles among anurans. C. Evolution of Tongue Afferents We next conducted a cladistic analysis of the evolution of hypoglossal afferents among anurans (Nishikawa et ah, 1993). For the cladistic analysis, 57 species of anurans representing 39 genera and 15 families were filmed while feeding before and after bilateral transection of the hypoglossal nerves (Fig. 5.15). Results of this analysis show that hypoglossal afferents that modulate the phase of activity in the jaw muscles are absent in all mechanical pullers and all hydrostatic elongators (Fig. 5.15). Some but not all inertial elongators possess hypoglossal afferents that modulate the phase of activity in the jaw muscles, and it appears that these afferents have evolved convergently at least four times independently: (1) in the leptodactyline leptodactylids Pleurodema and Physalaemus; (2) in the phyllomedusine hylids; (3) in the bufonids; and (4) in ranoids except for hemisotids and microhylids, in which hypoglossal afferents appear to have been lost (Fig. 5.15). Although the function of these afferents is very similar across species at the behavioral level, both cladistic analyses and comparative neuroanatomical studies show that the circuits are convergent rather than homologous in the different anuran lineages (Nishikawa et al, 1993; Anderson and Nishikawa, 1997). Frogs ancestrally lack afferents in the hypoglossal nerve, as do most vertebrates (Ariens-Kappers et ah, 1936). In toads of the family Bufonidae, sensory fibers from the glossopharyngeal nerve have invaded the tongue via the hypoglossal nerve and these fibers ascend to higher brain centers in the tractus solitarius (Nishikawa et al., 1993). In frogs of the family Ranidae, large myelinated

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Kiisa C. N i s h i k a w a Ascaphus Leiopelma Bombina Discoglossus Scaphiopus Spea Pelobates Pelodytidae Megophrys aceras Megophrys montana Leptobrachium Rhinophrynidae Pipidae Limnodynastes ] Myobatrachinae ] Sooglossidae ] Heleophrynidae Ceratophrys ] Chacophrys ] Lepidobatrachus Leptodactylus ] Pleurodema ] Physalaemus ] Telmatobius ] Caudiverbera ] Eleutherodactylus ] Syrrhophus ] Brachycephalidae ] Bufonidae ] Rhinodermatidae ] Centrolenidae ] Pseudidae

Hypoglossal Afferents

• • •

absent J present ] unknown

Hylinae Hemiphractinae Pelodryadinae Phyllomedusinae Ranidae Arthroleptidae Hyperoliidae Rhacophoridae Dendrobatidae Hemisotidae Microhylidae

F I G U R E 5.15. Cladogram illustrating the evolution of hypoglossal afferents among frogs. Hypoglossal afferents are ancestrally absent among frogs. These afferents have evolved several times independently, but only in frogs that use inertial elongation to protract the tongue. These afferents appear to have been lost in hydrostatic elongators (families Hemisotidae and Microhylidae).

afferents of the most anterior cervical spinal nerve have invaded the tongue via the hypoglossal nerve (Anderson and Nishikawa, 1997). These fibers ascend and descend in the dorsomedial funiculus and project to the granular layer of the cerebellum and the medial reticu-

lar formation. The source of hypoglossal afferents remains unknown in leptodactylids and hylids. During invasions of new territory in Rana and Bufo, sensory fibers have changed their peripheral pathways as well as their central connections, although the location

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5. Feeding in Frogs of their cell bodies and the basic class of cutaneous mechanoreceptors that they innervate appear to have been conserved. Current studies are exploring how these convergent neural circuits differ physiologically. D . Evolutionary Transitions in Mechanisms of Neural Control An important question that remains largely unanswered concerning the function and evolution of tetrapod feeding systems is whether evolution of the morphology and mechanics of the feeding apparatus affect mechanisms of neural control. A related question simply asks whether there is variation in the neural control of the feeding apparatus among tetrapods and, if so, what is the nature and significance of the variation. Because anuran species exhibit variation in the morphology and mechanics of the feeding apparatus, they offer a unique opportunity to investigate these questions. Motor control differs in several ways among frog species that use different mechanisms to protract their tongues. The first difference is that inertial elongators use only feedforward, open loop control to coordinate jaw and tongue movements. In inertial elongators, there is no opportunity for on-line, feedback correction after the tongue is launched because tongue protraction is ballistic (Nishikawa and Cans, 1996). In contrast, mechanical pullers and hydrostatic elongators can rely on both feedforward and feedback control of tongue movements because there is no inertial stage of tongue elongation (Table 5.1). A second difference in motor control is that, in inertial elongators, accurate placement of the tongue on the prey requires precise coordination of the extremely rapid, simultaneous movements of the tongue and jaws. Precise coordination is not necessary in mechanical pullers because the movement of the short tongue pad relative to the lower jaw is restricted to a few millimeters so that the tongue pad will always end up in nearly the same location as the tips of the mandibles. Precise coordination is unnecessary in hydrostatic elongators because the tongue is moved slowly and can be moved independently in three dimensions relative to the head. In inertial elongators, tongue afferents that are innervated by the hypoglossal nerve have evolved convergently in at least four independent lineages for the precise coordination of tongue and jaw movements. Small changes in the central and peripheral connections of cranial (Bufonidae) or spinal (Ranidae) mechanosensory afferents have led to the emergence of novel functions in coordinating feeding behavior in inertial elongators, including modulating the phase of activity in jaw muscles and influencing motor program choice during feeding.

Finally, the three-dimensional aiming ability of hydrostatic elongators implies several changes in neural control that have yet to be investigated. For both threedimensional aiming and high accuracy, we would expect that motor units should be smaller and more numerous in hydrostatic elongators than in other species. VL C O N C L U S I O N S In summary, the feeding behavior of anurans has proved to be an interesting model system for understanding the process of functional diversification during evolution. Comparative studies have demonstrated that frogs exhibit at least three different mechanisms for protracting their tongues. These are mechanical pulling, inertial elongation, and hydrostatic elongation. These mechanisms differ in the extent of tongue movement relative to the head, in the velocity, acceleration, and trajectories of tongue movements, in aiming ability, and in the accuracy of prey capture (Table 5.1). Morphologically, the feeding apparatus of frogs is rather homogeneous. All species possess similar sets of muscles and bones, although there is variation in the presence of compartments within muscles, for example, the dorsoventral compartment of the M. genioglossus in hydrostatic elongators, which has a major effect on tongue function. There are also differences among species in the contractile properties of tongue muscles as well as in the connective tissue that is responsible for transmitting the forces produced by the tongue muscles during feeding. In general, numerous small qualitative and quantitative morphological differences among species appear to be responsible for the rather large differences in the biomechanics of tongue protraction across anuran species. Species that differ in the biomechanics of tongue protraction also differ in mechanisms of neural control. Species differ in the relative importance of feedforward vs feedback control, in the requirement for precise coordination of multijoint movements, in the afferents that are used to coordinate these movements, and finally in aiming ability and accuracy of prey capture. There has been considerable rewiring of cranial or cervical spinal afferents in inertial elongators to provide a mechanism for precise coordination of tongue and jaw movements. In summary, these studies show that small changes in the anatomy of the feeding apparatus may lead to large changes in biomechanics and that small changes in neuroanatomy may lead to large changes in sensorimotor coordination. Potential precursors for novel sensory pathways appear to be prevalent and may change readily in response to natural selection. In anurans, high levels of neural and behavioral evolution

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are found, even among closely related species and in parts of the brain usually thought to be evolutionarily conservative. A major implication of these studies on the evolution of frog tongues is that, for any given species, the neural networks that subserve sensorimotor coordination are fine-tuned to its particular morphology and environment (Nishikawa, 1997). VII. CURRENT A N D FUTURE DIRECTIONS Numerous questions remain to be studied concerning the biomechanics and neural control of prey capture in anurans. In terms of biomechanics, a few differences in morphology and biomechanics of the feeding apparatus have been quantified in just a few species, and for many anatomical differences, their functional significance remains to be studied. Current research in my laboratory is focused on using biomechanical modeling to investigate the diversification of function in frog tongues (Nishikawa et al, 1997). With Eric Mallett and Gary Yamaguchi at Arizona State University, we have developed a planar, forward dynamic, multijoint, rigid body model of the anuran tongue to study the dynamics of tongue protraction and retraction during prey capture. The model contains four degrees of freedom, including the lower jaw (fixed length) and three segments of variable length in the tongue. In the model, the M. genioglossus and M. hyoglossus are used to actuate the tongue, while impulsive joint torques are applied at the jaw joint to open or close the mouth. Joint torques are obtained from a muscle model that incorporates nonlinear springs and dampers to simulate the forcelength-velocity characteristics of the tongue muscles. The model takes anatomical data on the size and shape of the feeding apparatus, as well as contractile properties of the tongue muscles, as input. Simulations involve varying the pattern of muscle activation to find the optimal pattern for each mechanism of tongue protraction. This model is being used to explore the following questions: (1) how much complexity must be incorporated into the model in order for it to predict movement trajectories accurately? (i.e., is a four degree of freedom model sufficient, or are more segments necessary? is the mentomeckelian joint needed? is a movable hyoid needed?) (2) how will differences in size and shape affect movement kinematics? (3) do changes in musculoskeletal design represent suites that together may enhance a particular aspect of kinematics? (4) can the same pattern of muscle activation be used for all species? and (5) how much can morphology change before a different muscle activation strategy becomes desirable?

In terms of neural control, differences in the neuroanatomy of proprioceptive pathways have been described in only two anuran species, and the neurophysiology of convergent afferent pathways remains to be explored. The anatomy and physiology of hypoglossal mechanosensory receptors also require further study. Finally, hypoglossal afferents are only one of many proprioceptive pathways that coordinate feeding movements, and the modulatory effects of additional afferent systems on feeding behavior, such as the lingual withdrawal reflex (Matsushima et ah, 1986, 1987,1988), remain to be described. Our studies of the neural control of prey capture in anurans have barely scratched the surface of understanding the evolutionary relationships among morphology, biomechanics, and neural control of movement. It is hoped that our attempts to understand the evolution of prey capture in frogs will stimulate functional morphologists to undertake similar studies in other groups of animals. Acknowledgments I thank the many undergraduate and graduate students from my laboratory who have contributed to this work and who made the process of doing it both fun and exciting. This research was supported by the National Science Foundation (IBN-9507497) and the National Instihites of Health (S06-GM08215). I thank James Birch, Lucile Gray, James O'Reilly, Philip Service, Steve Wainwright, Kentwood Wells, and Erika Wiltenmuth for constructive comments on the manuscript. Drawings were made by Tad Theimer (Fig. 5.2) and Virginia Coryell (Fig. 5.3), and Robyn O'Reilly prepared the figures on the computer.

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Nishikawa, K. C , and D. C. Carmatella (1991) Kinematics of prey capture in the tailed frog, Ascaphus truei. Zool. J. Linn. Soc. 103: 289-307. Nishikawa, K. C , and C. Gans (1992) The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus. J. Exp. Zool. 264:245-252. Nishikawa, K. C , and C. Gans (1996) Mechanisms of prey capture and narial closure in the marine toad, Bufo marinus. ]. Exp. Biol. 199:2511-2529. Nishikawa, K. C , and G. Roth (1991) The mechanism of tongue protraction during prey capture in the frog Discoglossus pictus. J. Exp. BioL 159:217-234. Nishikawa, K. C , C. Anderson, S. Deban, and J. O'Reilly (1992) The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav. Evol. 40:125-140. Nishikawa, K. C , J. C. O'Reilly, B. W. P Sasongko, and C. W. Anderson (1993) Convergent evolution of hypoglossal afferents that influence jaw muscle activity in frogs. Soc. Neurosci. Abstr. 19:161. Nishikawa, K. C , W. M. Kier and K. K. Smith (1999) Morphology and mechanics of tongue movement in the African pig-nosed frog (Hemisus marmoratum): A muscular hydrostatic model. J. Exp. BioL 202:771-780. Nishikawa, K. C , E. S. Mallett, and G. T. Yamaguchi (1997) A biomechanical model for the simulation of prey capture in toads. Soc. Neurosci. Abstr. 23:2135. Nussbaum, R. A. (1983) The evolution of a unique dual jaw closing mechanism in caecilians (Amphibia: Gymnophiona) and its bearing on caecilian ancestry. J. Zool. (London) 199:545-554. O'Reilly, J. C , K. C. Nishikawa, and S. M. Deban (2000) Derived life history characteristics constrain the evolution of aquatic feeding behavior in amphibians. Zoology: Analysis of Complex Systems: In press. O'Reilly, S. R., and K. C. Nishikawa (1995) Mechanism of tongue protraction during prey capture in the spadefoot toad Spea multiplicata (Anura: Pelobatidae). J. Exp. Zool. 273:282-296. Ozeti, N., and D. B. Wake (1969) The morphology and evolution of the tongue and associated structures in salamanders and newts (family Salamandridae).Copeia 1969:91-123. Peters, S. E., and K. C. Nishikawa (1999) Comparison of isometric contractile properties of the tongue muscles in threee species of frogs, Litoria caerulea, Dyscophus guinetti and Bufo marinus. J. Morphol. 242:107-124. Premo, D. B., and A. H. Atmowidjojo (1987) Dietary patterns of the "crab-eating frog," Rana cancrivora, in West Java. Herpetologica 43:1-6. Regal, P. J. (1966) Feeding specializations and the classification of terrestrial salamanders. Evolution 20:392-407. Regal, P. J., and C. Gans (1976) Functional aspects of the evolution of frog tongues. Evolution 30:718-734. Reilly, S. M., and G. V Lauder (1989) Kinetics of tongue projection in Ambystoma tigrinum: quantitative kinematics, muscle function, and evolutionary hypotheses. J. Morphol. 199:223-243. Ridewood, W. G. (1897) On the structure and development of the hyobranchial skeleton and larynx in Xenopus and Pipa; with remarks on the affinities of the Aglossa. J. Linn. Soc, Zool. 26: 53-128. Ritter, D. A., and K. C. Nishikawa (1995) The kinematics and mechanism of prey capture in the African pig-nosed frog {Hemisus marmoratum): the description of a radically divergent anuran tongue. J. Exp. Biol. 198:2025-2040. Rossignol, S., J. P. Lund, and T. Drew (1988) The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates: a comparison between locomotion, respiration and mastication. Pp. 201-284. In: Neural Control of Rhythmic Movements in Vertebrates. A. H. Cohen, S. Rossignol, and S. Grillner (eds.), Wiley, New York.

5. F e e d i n g in Frogs Roth, G. (1987) Visual Behavior in Salamanders. Springer Verlag, Berlin. Roth, G., K. C. Nishikawa, D. B. Wake, U. Dicke, and T. Matsushima (1990) Mechanics and neuromorphology of feeding in amphibians. Neth. J. Zool. 40:115-135. Ruvinsky, I., and L. R. Maxson (1996) Phylogenetic relationships among bufonid frogs (Anura: Neobatrachia) inferred from mitochondrial DNA sequences. Mol. Phylogen. Evol. 5:533-547. Satou, M., and A. Shiraishi (1991) Local motion processing in the optic tectum of the Japanese toad, Bufo japonicus. J. Comp. Physiol. A 169:569-589. Severtzov, A. S. (1961) On the mechanism of tongue protrusion in anuran amphibians. Doklad. Akad. Nauk SSSR 140:256-259 (translation). Shinn, E. A., and J. W. Dole (1978) Evidence for a role for olfactory cues in the feeding response of leopard frogs, Rana pipiens. Herpetologica 34:167-172. Simon, M. P., and C. A. Toft (1991) Diet specialization in small vertebrates: mite-eating frogs. Oikos 61:263-278. Smith, C., and A. Bragg (1949) Observations on the ecology and natural history of Anura. VII. Food and feeding habits of the common species of toads in Oklahoma. Ecology 30:333-349. Sokol, O. M. (1969) Feeding in the pipid frog Hymenochirus boettgeri (Tornier). Herpetologica 25:9-24. Starrett, P. H. (1968) The Phylogenetic Significance of the Jaw Musculature in Anuran Amphibians. Ph. D. Dissertation, University of Michigan. Taigen, T. L., and F. H. Rough (1983) Prey preference, foraging behavior, and metabolic characteristics of frogs. Am. Nat. 122: 509-520. Thexton, A. J., D. B. Wake, and M. H. Wake (1977) Tongue function in the salamander Bolitoglossa occidentalis. Arch. Oral Biol. 22:361366. Toft, C. A. (1981) Feeding ecology of Panamanian litter anurans: patterns in diet and foraging mode. J. Herpetol. 15:139-144. Toft, C. A. (1995) Evolution of diet specialization in poison-dart frogs (Dendrobatidae). Herpetologica 51:202-216.

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Trueb, L. (1973) Bones, frogs, and evolution. Pp 65-132. In: Evolutionary Biology of the Anurans. J. Vial (ed.). Univ. of Missouri Press, Columbia. Trueb, L., and C. Gans (1983) Feeding specializations of the Mexican burrowing toad, Rhinophrynus dorsalis (Anura: Rhinophrynidae). J. Zool. London 199:189-208. Tso, T. A., J. C. O'Reilly, and K. C. Nishikawa (1995) Conservation of function of the m. hyoglossus during feeding in frogs. Am. Zool. 35:123A. Tyler, M. J. (1974) Superficial mandibular musculature and vocal sac structure of the Mexican burrowing toad, Rhinophrynus dorsalis. Herpetologica 30:313-316. Valdez, C. M., and K. C. Nishikawa (1997) Sensory modulation and motor program choice during feeding in the Australian frog, Cyclorana novaehollandiae. J. Comp. Physiol. A 180:187-202. Vences, M. (1988) Zum Beutefang Verhalten der europaischen Amphibien. Herpetofauna 10:6-10. Wainwright, P C , D. M. Kraklau, and A. F Bennett (1991) Kinematics of tongue projection in Chamaeleo oustaleti. J. Exp. Biol. 159: 109-133. Wake, D. B. (1982) Functional and developmental constraints and opportunities in the evolution of feeding systems in urodeles. Pp. 51-66. In: Environmental Adaptation and Evolution. D. Mossakowski and G. Roth (eds.) Gustav Fischer, Stuttgart. Webster, S. (1996) The Morphology of the Connective Tissues of Extensible Tongues. Unpublished Honors Thesis, College of Cardiff, University of Wales. Weerasuriya, A. (1989) In search of the pattern generator for snapping in toads. Pp. 589-614. In: Visuomotor Coordination, Amphibians, Comparisons, Models and Robots. J.-P. Ewert and M. A. Arbib (eds.). Plenum, New York. Wiltenmuth, E. B., and K. C. Nishikawa (1994) Scaling of feeding kinematics across four species of dendrobatid frogs. Am. Zool. 34:57A. Zug, G., and P. Zug (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithsonian Contr. Zool. 284-1-58.

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C H A P T E R

6 Feeding in Caecilians JAMES C. O'REILLY Organismic and Evolutionary Biology University of Massachusetts Amherst Amherst, Massachusetts 01003

I. INTRODUCTION 11. MORPHOLOGY A. Sensory Organs B. Musculoskeletal Anatomy III. FUNCTION A. Finding Prey B. Capturing Prey (Ingestion) C. Intraoral Transport IV. EVOLUTION V. THE FUTURE References

son, 1989). In Central and South America, they are known from southern Mexico to northernmost Argentina. In Asia, they range from India and Sri Lanka to Indochina. In southeast Asia they range from the southernmost Philippines and southern China south through the Greater Sunda Islands to Wallace's line. No caecilians are known from the rain forests of New Guinea or Australia. In Africa, they are abundant throughout the humid coastal regions of the west and from several disjunct areas in the east, including parts of Tanzania, Ethiopia, Kenya, Malawi, and Rwanda (Nussbaum and Hinkel, 1994). Only a single specimen is known from all of central Africa (Nussbaum and Pfrender, 1998) and no caecilians have been reported in Madagascar. Six species, which appear to be a monophyletic group, are found in the Seychelles Archipelago (Nussbaum, 1985a; Nussbaum and Ducey, 1988), islands approximately halfway between India and Madagascar. Most caecilians are fossorial but several species are semiaquatic, and at least four South American species are entirely aquatic (Moodie, 1978; Nussbaum and Wilkinson, 1989; Wilkinson, 1989; Wilkinson and Nussbaum, 1997). Fossorial species primarily dwell in highly organic, friable surface layers of the soil where they maintain tunnel systems (Tanner, 1971; Himstedt, 1991,1996; Ducey ei al, 1993; Wake, 1993b). These surface-dwelling burrowers display a high degree of mechanical independence of the vertebral column and skin (Gaymer, 1971; Summers and O'Reilly, 1997) and can generate extraordinary burrowing forces by using their entire bodies as single chambered hydrostatic skeletons (O'Reilly ei al., 1997). However, observations

L INTRODUCTION Caecilians are legless, burrowing amphibians that superficially resemble earthworms and are found only in the tropics. Currently, there are about 150 species and six families recognized (Nussbaum and Wilkinson, 1989). There is a growing consensus concerning the phylogenetic relationships among the basal caecilian families (Hedges et ah, 1993; Wilkinson and Nussbaum, 1996; Fig. 6.1); however, over two-thirds of the species and over three-quarters of the genera are currently placed in the paraphyletic Caeciliidae. There are currently no widely accepted phylogenetic hypotheses that include more than a small fraction of the genera within Caeciliidae, thus relationships among the vast majority of caecilians remain uncertain (Nussbaum and Wilkinson, 1989; Hedges et al, 1993; Wake, 1993a; Wilkinson and Nussbaum, 1996; Wilkinson, 1997). Caecilians have been found throughout most of the humid tropics (Taylor, 1968; Nussbaum and Wilkin-

FEEDING (K. Schwenk, ed.)

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James C. O'Reilly Rhinatrematidae Ichthyophiidae Uraeotyphlidae Scolecomorphidae "Caeciliidae" Typhlonectidae

FIGURE 6.1. Current phylogenetic hypothesis of caecilian relationships modified from Hedges et al. (1993) and Wilkinson and Nussbaum (1996). Caeciliidae is almost certainly paraphyletic with respect to Typhlonectidae.

of captive specimens of some extremely elongate species that lack independence between the vertebral column and skin (e.g., Boulengerula) indicate that they seem to modify preexisting spaces rather than excavating tunnel systems of their own design. As far as is known, all of the members of the basal families (Rhinatrematidae, Ichthyophiidae and Uraeotyphlidae) have a life history that includes a free-living, aquatic larval stage and a terrestrial adult stage (Sarasin and Sarasin, 1887-1890; Parker, 1956; Taylor, 1968; Wake, 1977a; Wilkinson, 1992b). At least three genera of Caeciliidae {Grandisonia, Praslinia, and Sylvacaecilia) have species with a free-living larval stage (Parker, 1958; Largen et al, 1972; Nussbaum, 1992). The larval period of caecilians can last several months and is followed by a gradual metamorphosis to the adult stage (Breckenridge et al, 1987; Himstedt, 1991,1996). Members of the rest of Caeciliidae, Scolecomorphidae, and Typhlonectidae, for which there are data, have either direct development or are viviparous (Parker 1956; Wake, 1977a,b, 1992; Wilkinson and Nussbaum, 1998). After their yolk has been depleted, fetuses of viviparous species are matrotrophic, feeding on secretions of the epithelial cells of the oviduct and, at least inadvertently, the epithelial cells themselves (Parker, 1956; Welsch et al, 1977; Wake, 1977a,b). Unfertilized eggs, expelled from the ovaries well after pregnancy has begun, may also be consumed in some species. Gestation is known to last from 6 months in Typhlonectes (Exbrayat and Delsol, 1985) to as long as a year in Dermophis (Wake, 1980a). At least one viviparous species, Geotrypetes seraphini, guards its young for some time after birth (Sanderson, 1937). Little is known about the diet of caecilians relative to other tetrapods. As far as is known, all caecilians are carnivores. Wake (1980a) found that earthworms dominate the diet of one population of Dertnophis from Guatemala, and Moll and Smith (1967) reported a

specimen of Dertnophis having eaten a lizard. Barbour and Loveridge (1928) and Hebrard et al (1992) concluded that termites are the predominant prey of two different east African species of Boulengerula. Moodie (1978) and Wake (1978) found coleopteran larvae, shrimp, and small arthropods in the digestive tracts of Typhlonectes. Loveridge (1936) and Nussbaum and Pfrender (1998) reported termites, earthworms, and insects in the stomachs of Schistometopum. Remaining data on the caecilian diet are based on captive animals. In captivity, larvae of Epicrionops will eat only small aquatic arthropods when originally captured, but can be trained to eat earthworms (O'Reilly, 1995, 1996). Specimens of Siphonops and Dertnophis will readily eat newborn rodents. Several species that have been kept in captivity (e.g., species of Caecilia) have refused to eat anything but earthworms (O'Reilly, 1996). Boulengerula also appears to have a specialized diet as those kept in captivity will only eat termites and small crickets while ignoring earthworms (O'Reilly, 1996). In contrast, adults of some species (e.g., Hypogeophis rostratus) are apparently opportunists that will eat a wide variety of prey, including salmon eggs and pieces of veal, items that they presumably would never come across in nature (Tanner, 1971). The current dearth of information on caecilian phylogeny and feeding behavior limits the following discussion primarily to functional interpretations of sensory and musculoskeletal anatomy. It is my hope that this will be a starting point from which more complete studies of feeding behavior can be undertaken. I begin by summarizing the relatively abundant literature on caecilian cranial anatomy and reviewing the few functional studies on caecilian feeding. I will then propose some general hypotheses about the forces driving the evolution of caecilian head anatomy and feeding behavior. Finally, I will discuss areas that would be productive for future investigation. 11. MORPHOLOGY This section describes what is known about the sensory and musculoskeletal morphology of caecilians. In the section on sensory organs, the descriptions are organized by the functional system. In the musculoskeletal anatomy section, the anatomy of larvae, fetuses, and adults will be discussed in turn. A. Sensory Organs 1. Eye With the exception of some scolecomorphids that have protrusible eyes, caecilian eyes are small and buried either under skin or dermal bones (Wake, 1985;

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6. Feeding in Caecilians Himstedt, 1995; O'Reilly et ah, 1996). All caecilians that have been examined in detail possess a retina that is linked to the brain with a complete, although sometimes extremely attenuate, optic nerve (Wake, 1985). Among those species for which data are published, the lens is variably developed with the exception of Boulengerula, which is lensless, and the extrinsic eye muscles have been coopted for other functions, reduced in size, or no longer develop (Wake, 1985). The eyes of caecilians are also reduced in terms of neuroanatomical features. The optic nerve of Ichthyophis has far fewer fibers than those of lungfish, frogs, and salamanders (Roth et ah, 1993). In Ichthyophis (both larvae and adults) and Typhlonectes, the visual fields of the optic tectum are virtually absent, but bilateral thalamic projections to the medial optic tracts are well developed (Clairambault et ah, 1980; Fritzsch et ah, 1985; Himstedt and Manteuffel, 1985). 2. Olfactory

System

In contrast to the visual system, the olfactory system of caecilians is well developed relative to frogs and salamanders. Like all anamniote sarcopterygians that possess lungs, caecilians use buccal pumping to breath (Carrier and Wake, 1995). In this method of breathing, air is sucked into the buccal cavity via the nares (and nasal epithelia) before it is pumped into the lungs by muscles of the hyobranchial apparatus. When not filling the lungs, less dramatic movements of the floor of the buccal cavity cause air to be flushed over the nasal epithelia. The main nasal cavity is lined with olfactory epithelium at its anterior end and respiratory epithelium at the caudal end (Schmidt and Wake, 1990). The olfactory epithelium lines the majority of the nasal cavity in most species, but is reduced in the typhlonectids in which the majority of the cavity is lined with respiratory epithelium. Still, both morphological and behavioral evidence indicate that typhlonectids use buccal pumping in order to smell in water (Wilkinson and Nussbaum, 1997). 3. Tentacle Organ Caecilians posses a unique sensory organ called the tentacle that is derived from the tear duct and other parts of the eye (Wiedershiem, 1879; Engelhardt, 1924; Billo and Wake, 1987) and is directly connected to the vomeronasal organ (Badenhorst, 1978; Fiimstedt and Simon, 1985). The tentacle is seen in all metamorphosed caecilians but is not present in larvae. Among rhinatrematids, the tentacle lies immediately in front of the eye and is not protractile. In all other caecilians, the tentacle is in a more anterior position and the degree to which it can be protracted varies. In some species (e.g., Ichthyophis kohtaoensis) the tentacle can be pro-

truded a considerable distance (several millimeters) out of the head. Other species (e.g., Dermophis mexicanus) are capable of only very limited protrusion and members of the genus Typhlonectes do not protrude the tentacle at all (Wilkinson and Nussbaum, 1997). Fox (1985) found evidence of tactile sensory cells on the surface of the tentacle of Ichthyophis but no evidence of chemosensory cells. The paired vomeronasal organs of typhlonectids are proportionally larger and have more extensive projections to the bulbus olfactorius accessorius than those of other caecilians that have been examined (Schmidt and Wake, 1990). 4. Lateral Line Caecilians can possess two types of lateral line organs: neuromasts (mechanoreceptor organs) and ampuUary organs (electroreceptors). Larvae of five genera {Epicrionops, Ichthyophis, Uraeotyphlus, Grandisonia, and Sylvacaecilia) have been described as having a lateral line system (Parker, 1958; Taylor, 1970; Largen et al, 1972; Hetherington and Wake, 1979; Fritzsch et al, 1985; Wahnschaffe et al, 1985; Fritzsch and Wake, 1986; Wake, 1987; Wilkinson, 1992a,b), but only that oi Ichthyophis has been examined in detail. Larvae of Ichthyophis possess a lateral line system with both neuromasts and ampuUary organs. The neuromasts are found both on the head and along the trunk, whereas ampuUary organs are restricted to the head (Fritzsch et al, 1985; Wahnschaffe et al, 1985). Larvae of Epicrionops possess two rows of neuromasts on the trunk, whereas other larvae possess only one row that is homologous to the dorsal row of Epicrionops (Wilkinson, 1992a). As in other anamniotes, the lateral line afferents of Ichthyophis project to the dorsal nucleus of the rhombencephalic alar plate (Fritzsch et al, 1985). Lateral line organs have not been reported in any fetal caecilians, but are presumably present at least late in development in fetal typhlonectids. With the exception of the semiaquatic Hypogeophis rostratus and the semiaquatic and aquatic typhlonectids, which have only ampuUary organs, lateral line organs are absent in adult caecilians (Fritzsch and Wake, 1986). 5. Auditory

System

An excellent comparative study and literature review of the anatomy of the caecilian auditory apparatus and its inervation has been provided by Fritzsch and Wake (1988). The inner ear of amphibians is generally composed of six regions: three semicircular canals (horizontal, anterior, and posterior), the utriculus, the sacculus, and the lagena. Each of these regions has distinct sensory epithelia innervated by branches of the eighth cranial nerve. These epithelia primarily function as vestibular sensors, but both the sacculus and

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the lagena also play a role in the perception of low frequency sounds (Lewis et al, 1985). All of these sensory epithelia are found in all caecilians with the exception of the lagena, which has not been observed in Boulengerula, Oscaecilia, or typhlonectids (Fritzsch and Wake, 1988). In addition to the general inervation of the epithelia of the inner ear chambers, three specialized auditory patches of epithelial cells, termed papillae, are found in the utriculus and sacculus. The basilar papilla is found in Latimeria, most amniotes, frogs, and some salamanders. This papilla is present only in basal caecilians (rhinatrematids, ichthyophiids, and uraeoty phlids) where it located in a side pocket of the sacculus (Fritzsch and Wake, 1988). This region of epithelial cells is sensitive to high-frequency sounds in frogs (Lewis and Lombard, 1988) and presumably serves the same function in those caecilians that possess it. The papilla neglecta is a synapomorphy of living gnathostomes, but has been lost in both salamanders and frogs. It resides in the utriculus just earlier the open ing to the sacculus and is sensitive to low-frequency sounds (Lewis et al., 1985). The amphibian papilla, a synapomorphy of living amphibians, is found in the sacculus just later the utriculus and is sensitive to lowfrequency sounds in anurans (Lewis et al, 1985). Based on ontogenetic data from Dermophis, Fritzsch and Wake (1988) argue that the amphibian papilla is derived directly from part of the papilla neglecta. Despite the relatively reduced size of the papillae

spiracle

lateral line

eye

nares

of the caecilian ear relative to other amphibians, the eighth cranial nerve shows no appreciable degeneration. The auditory projections of Ichthyophis are very similar to those seen in salamanders and have been interpreted as primitive in organization by Fritzsch (1988) because they resemble those of Latimeria and Dipnoi more than those of amniotes and frogs. B. Musculoskeletal Anatomy 1. Larvae Among basal caecilians, young first feed as freeliving aquatic larvae. The only available detailed descriptions of larval cranial anatomy are based on Ichthyophis. It is difficult to assign the descriptions presently available to any particular species of Ichthyophis and it is likely that at least some of the series described include mixtures of more than one species. Fortunately, other than the proportions of the skull and the number of gill slits, there is little variation between the specimens described. Larval caecilians have well-developed labial lobes, which give the head a squared-off appearance relative to adults (O'Reilly, 1995; Fig. 6.2), but the skull is much more fusiform in shape. The skull of larval Ichthyophis has large temporal fenestrae and the large jaw levator muscles originate along the sagital midline before traveling through the fenestra to the lower jaw (Edgeworth, 1935; Visser, 1963). The lower jaw is well ossi-

annulus annular groove

eye nares tentacle

FIGURE 6.2. Illustration of the external cranial morphology of larval and adult Ichthyophis banannicus. Note the large labial folds and resulting blunt head shape of the larvae. Upon metamorphosis, the skull becomes ossified more heavily and the skin becomes connected more tightly to the dermal bones, resulting in the more fusiform head shape of the adult. Illustration by Loree Harvey.

6. Feeding in Caecilians fled, with two rows of recurved teeth and a prominent retroarticular process that curves dorsally posterior to the jaw articulation, and a well-developed interhyoideus posterior (Edgeworth, 1965; Visser, 1963). The upper jaws also have two rows of teeth, including a premaxillary-maxillary row and a vomerine-palatine row. In larval caecilians the maxillary and palatine are separate bones, but these are always fused into a maxillopalatine with a much extended row of maxillary teeth in adults (Reiss, 1996). The quadrate of larvae is relatively independent, becoming more firmly attached to the squamosal and maxillopalatine during metamorphosis (Visser, 1963). The hyobranchial apparatus and associated musculature is well developed in larval Ichthyophis and consists of several pairs of independent elements. A ventromedial basibranchial articulates with a pair of ceratohyals and four pairs of ceratobranchials, with the fourth ceratobranchial articulating with the third (Edgeworth, 1935). In Ichthyophis, the hyobranchial skeleton is cartilaginous, but in larval Epicrionops, it is well ossified (Wake, 1989). 2. Fetuses Many species of caecilians have a fetal developmental stage that is associated with a suite of derived cranial characteristics. In the earliest developmental stages of Dermophis pictured by Wake and Hanken (1982), the hyobranchial apparatus has the same design as that of adults (cartilaginous with left and right elements fused). During the early stages of this fetal period, the head is conspiciously larger and more advanced in development than the rest of the body. In contrast to free-living larvae, which have teeth like those of adult caecilians, fetuses possess up to 12 rows of spatulate teeth that are sometimes combed at the tips (Parker, 1956; Parker and Dunn, 1964; Wake, 1976). The teeth extend well outside the oral cavity and the bases of the teeth are sometimes fused into plates (Parker, 1956). The mouth is almost terminal (Wake and Hanken, 1982; Wilkinson, 1991; Wake, 1993c), with the teeth, quadrate, and jaws ossifying well ahead of the rest of the skull (Wake and Hanken, 1982). 3. Adults In all adult caecilians, the hyobranchial apparatus is cartilaginous and all of the paired elements that are independent in larvae fuse whereas most medial elements degenerate. The tongue is large but is tightly connected to the mandible along its margins and is not protrusible (Bemis et al, 1983). The teeth are recurved.

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pedicellate, and can be either monocuspid or bicuspid (Lawson, 1965a; Wake and Wurst, 1979). Most caecilian teeth are sharply pointed, but at least some typhlonectids possess more blade-like tooth tips (Wake and Wurst, 1979; Wilkinson, 1991). Most caecilians possess a unique diminutive muscle, the levator quadrati, which originates on the os basal and inserts on the quadrate (Edgeworth, 1925, 1935; Wilkinson and Nussbaum, 1997). Caecilians are also unique in that the interhyoideus muscle inserts on the retroarticular process of the lower jaw rather than the tips of the ceratohyals (Fig 6.3) and contributes to jaw closing (Nussbaum, 1977,1983; Bemis et a/., 1983). The mandibles and associated musculature display significant variation among species. Descriptions of the five morphological groups that follow are summaries of data from Nussbaum (1983) and Wilkinson and Nussbaum (1997) unless otherwise noted. a. Group I Members of Rhinatrematidae possess skulls with large temporal fenestrae as adults. The lower jaw has a well-developed, mainly horizontal retroarticular process. The adductor mandibulae complex is larger than in other caecilians, extending through the temporal fenestra to the midline of the cranium. The interhyoideus posterior is smaller than that of other caecilians, in terms of cross section, but the fibers are of similar length to those of other groups. The depressor mandibulae has a broad origin with fibers ranging in orientation from horizontal to vertical with all fibers converging on a narrow insertion on the tip of the retroarticular process. h. Group II Members of Ichthyophiidae and Uraeotyphlidae have skulls that either have no temporal fenestra or a small fissure between the squamosal and the parietal. The retroarticular process is strongly recurved just posterior to the jaw articulation. The adductor complex of all adult members of this group is confined below the squamosal and fibers do not extend onto the surface of the skull. As a result, the fibers of the adductor complex are relatively much shorter than those seen in group I. The interhyoideus posterior of this group has fibers of similar length as those seen in group I, but the muscle extends much farther up the side of the body. This greatly increases the physiological cross section of the interhyoideus posterior relative to group I while maintaining a fusiform body cross section. In contrast to group I, all of the fibers of the depressor mandibulae have assumed a horizontal orientation.

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James C. O'Reilly I me

FIGURE 6.3. (A) Dorsolateral view of the cranial anatomy of an adult Dermophis mexicanus. Note the large size of the interhyoideus and its insertion on the retroarticular process of the mandible, rl, rectus lateralis; seo, obliquus externus superficialis; lab, levator arcus branchiales; dm, depressor mandibulae; ih, interhyoideus; dt, dorsalis trunci; p, parietal; f, frontal; npm, nasopremaxilla; s, squamosal; mp, maxillopalatine; pa, pseudoangular; pd, pseudodentary. (B) Ventrolateral view of Dermophis with superficial muscles removed. Note the diminutive size of the levators mandibulae. Ic, longus capitis; imp, levator posterior; Ime, levator mandibulae externus; Ima, levator mandibulae anteior; im, intermandibularis; gh, geniohyoideus; gg, genioglossus; re, rectus cervicus; pa, pseudoangular; pd, pseudodentary. From Bemis et ah (1983).

c. Group III According to Nussbaum (1985b), members of Scolecomorphidae can have solidly roofed skulls {Crotaphatrema) or skulls with large temporal fenestrae (Scolecomorphus). Regardless of the presence or absence of the fenestrae, the adductor mandibulae complex is diminutive and restricted to the adductor chamber. Like in group II, the retroarticular process of the mandible is strongly recurved. However, unlike the re-

troarticular process of group II, the mandible curves anterior to the jaw articulation (Nussbaum, 1985b). Thus, the mandibular fossa opens caudally in scolecomorphids in contrast to most other caecilians. Like group II, the interhyoideus posterior is massive and many of the fibers extend horizontally along the first several segments of the trunk. In contrast to all other groups, some fibers of the interhyoideus posterior insert on the lower jaw anterior to the jaw joint. The de-

155

6. Feeding in Caecilians pressor mandibulae is diminutive, oriented obliquely, and inserts on the retroarticular process.

we can start to understand how caecilians go about localizing and subduing potential food items.

d. Group IV With the exception of the typhlonectid Atretochoana, all of the members of Caeciliidae and Typhlonectidae can generally be grouped together because they share moderate curvature of the retroarticular process, diminutive adductors, and a well-developed interhyoideus posterior (Fig. 6.3). The skulls of this group range from solidly roofed (e.g., Caecilia and Dermophis) to having large temporal fenestrae {Geotrypetes and typhlonectids) (Taylor, 1969). The adductor mandibulae complex is restricted to the adductor chamber even in those species with large temporal fenestrae. The interhyoideus posterior varies in size, reaching its most extreme form in Microcaecilia and Praslinia where it extends many segments down the body and is pinnate in form. The depressor mandibulae is obliquely oriented and inserts well posterior to the jaw joint. e. Group V The final morphological group contains a single species, Atretochoana eiselti. Although long recognized as distinct species (Taylor, 1968), the morphology oi Atretochoana has only recently been described in detail (Nussbaum and Wilkinson, 1995; Wilkinson and Nussbaum, 1997). This relatively large (only two known specimens are over 70 cm in length and robust in proportions) caecilian is unique among Gymnophiona in that it completely lacks lungs and functional choanae. The jaw apparatus oi Atretochoana has several unique characteristics. The most obvious is the extreme dorsoventral compression relative to other caecilians. The jaw joint is placed well behind the rest of the skull, due to extreme elongation of quadrate. The retroarticular process is very small and recurved sharply directly before the jaw articulation (as in type III). The temporal fenestra is proportionally much larger than in any other known caecilian. The jaw levators are proportionally larger than those seen in type II, III, and IV skulls and are oriented horizontally between the skull and lower jaws, rather than dorsoventrally as in other caecilians. A detailed description of the anatomy of this unique species with comparisons to other caecilians can be found in Wilkinson and Nussbaum (1997). III. F U N C T I O N With the exception of two experimental behavioral studies and several reports that include observations on feeding, we have little direct evidence of how caecilians find and capture their prey. However, by combining these studies with available morphological data.

A. Finding Prey In both larvae and adults, the sense of sight probably plays little or no role in prey identification or localization. There are currently no data to suggest that the eyes of any caecilian are capable of forming images or play any role in localizing prey. Negative phototaxis has been reported in Hypogeophis (Taylor, 1968) and Ichthyophis (Himstedt and Manteuffel, 1985) and has been observed in many other species that have been kept in captivity. However, in larval and adult Ichthyophis, the number of optic nerve fibers and the afferent projections of the optic nerve suggest that the retina functions only as a light receptor (Himstedt and Manteuffel, 1985; Fritzsch et ah, 1985; Himstedt, 1995). The use of the eye as a photoreceptor is probably widespread among caecilians (Wake, 1985) except in those species where the eyes are completely covered by bone and may no longer serve any sensory function. As with the eye, the morphology of the ear of caecilians suggests that it plays little or no role in prey detection. The lack of a tympanum, the reduction of the auditory epithelia of the inner ear, and the poorly developed auditory centers of the alar plate of caecilians indicate that the sense of hearing is not well developed (Fritzsch and Wake, 1988). The basal papilla, which is sensitive to high-frequency sounds, is not present in most caecilians, whereas those epithelia thought to be involved in the detection of low-frequency sounds (sacculus, lagena, papilla neglecta, and the amphibian papilla) are largely retained. Available data (from Ichthyophis, Geotrypetes, and Dermophis) on the sensitivity of caecilian ears to airborne sounds of different frequencies indicate that they are not very effective in air but might function well in water or mud (Wever, 1975; Wever and Gans, 1976). A functional role of lowfrequency sound detection for prey localization has yet to be demonstrated. Both lateral line organs and olfaction apparently play an important role in prey detection in aquatic species. Results of behavioral experiments carried out on larvae of Ichthyophis indicate that the ampuUary organs of the head are fully functional electroreceptors that are used to locate prey (Himstedt and Fritzsch, 1990). The functional role of the neuromasts of the lateral line have not been tested, but they may sense prey movement, detect the approach of predators, or act as proprioreceptors during locomotion. Most adult caecilians primarily feed on land and lack ampullary organs. The presence of ampullary organs in the heads of aquatic foraging typhlonectids and Hypogeophis (Fritzsch and

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Wake, 1986) implies that they may be used to locate aquatic prey in these species (Wilkinson, 1992a). The behavior of typhlonectids indicates that olfaction probably also plays an important role in prey detection (Wilkinson and Nussbaum, 1997) The single behavioral study of how terrestrial caecilians find prey was performed by Himstedt and Simon (1995) on Ichthyophis. They found that Ichthyophis can usually locate pieces of bovine heart at a distance of 12 cm in less than 2 min (significantly faster than the salamander Triturus alpestris). When the nares were blocked, this species was not only incapable of locating prey, but apparently could not identify prey items when they are in direct contact with the snout. These results suggest that olfaction via the nares is the principle sensory modality used by terrestrial caecilians to find food. The tentacle organ appears to play little or no role in the detection of airborne substances given off by prey, but is more likely important for following trails of molecules left in tunnels by passing prey items (Himstedt and Simon, 1995). The lack of chemosensory cells on the tentacle of Ichthyophis (Fox, 1985) suggests that it must aid in chemoreception by gathering molecules from the substrate and delivering them to the chemosensory cells of the vomeronasal organ (Badenhorst, 1978; Himstedt and Simon, 1995). B. Capturing Prey (Ingestion) After locating a prey item it must be captured before it can be eaten. In water, larval and adult salamanders generally use suction feeding to apprehend prey items (Reilly and Lauder, 1992; O'Reilly, 1995). Suction feeding is relatively rare among frogs and caecilians (O'Reilly, 1995). The only larval caecilian for which kinematic data are available (an unidentified species of Epicrionops from Ecuador) suction feeds (Fig. 6.4, left). However, anatomical evidence suggests that suction feeding is the general method of prey capture used by larval caecilians (O'Reilly, 1995). The jaw movements are highly stereotyped in larval Epicrionops (Fig. 6.5A) and display a pattern similar to the jaw movements of suction-feeding salamanders (Reilly and Lauder, 1992). In many viviparous caecilians, the young feed for extended periods in the oviduct before being born (Parker, 1956; Wake, 1977b). The subject of what fetal caecilians feed on and the mechanism by which they feed has been the subject of some inference, but direct observations of feeding have yet to be reported. The extended gestation period and the fact that fetal caecilians increase many times in body mass after they have resorbed their yolk indicate that they are gaining considerable nutrition from the mother during development (Parker, 1956). The gut contents of fetal caecili-

ans suggest that they are feeding orally (histotrophy), rather than absorbing nutrients through their skin or gills (Parker, 1956; Wake, 1977b). Fetuses appear to be eating "uterine milk" from secretory cell beds in the uterine epithelium and some shed epithelial cells (Parker, 1956; Wake, 1977b) and may also eat unfertilized eggs, which are produced by the ovaries of at least some species well into fetal development. Parker and Dunn (1964) concluded that the dentition of fetal caecilians was not functional, but effective arguments to the contrary have been made by Wake (1977b) and Wilkinson (1991). The fact that the epithelial lining of the oviduct is no longer present in the immediate vicinity of advanced fetuses but is intact elsewhere (Wake, 1977b) suggests that fetal caecilians are wearing down the epithilium while feeding and lend support to the conclusion that fetal teeth are an aptation for oviductal feeding. In contrast to salamanders and frogs, which generally use their tongues to capture prey on land (Lauder and Reilly, 1993; Nishikawa et al, 1992), all caecilians observed thus far {Boulengerula, Caecilia, Dermophis, Epicrionops, Grandisonia, Hypogeophis, Ichthyophis, Schistometopum, Scolecomorphus, and Siphonops) use jaw prehension for terrestrial prey capture (Figs. 6.4, right, and 6.6, left). Caecilians generally contact prey before a gape cycle is initiated (although excited individuals have been observed to wave their heads back and forth with the mouth open after smelling food), implying that tactile information is usually needed to trigger a feeding sequence. Data from Ichthyophis with blocked nares suggest that olfactory cues are also needed for prey capture to be initiated (Himstedt and Simon, 1995). Relative to frogs and salamanders, the feeding movements of adult caecilians are extremely slow (Table 6.1) and appear strongly modified by sensory information gathered midstrike (O'Reilly. 1995). Once prey is contacted, the jaws are slowly opened while precisely tracing the outline of the prey item. The process of opening the jaws and placing them on the prey can take well over a second in Ichthyophis (Fig. 6.5B). Jaw closing is often initiated and then interrupted repeatedly in apparent attempts to gain better jaw placement (Fig. 6.5). However, at the slightest sign of attempted escape, the jaws are closed relatively rapidly. Jaw movements are much more rapid when Ichthyophis is presented with a cricket rather than an earthworm, even if the cricket is pinned to the substrate with forceps so that it cannot escape. These observations suggest that the gape cycle is modified both by a priori olfactory information about prey type and by tactile information received during the strike itself. Aquatic feeding in adult caecilians is qualitatively very similar to terrestrial feeding with some minor

6. F e e d i n g in Caecilians

F I G U R E 6.4. (Left) High-speed cinematography of an aquatic prey-capture sequence in larval Epicrionops eating a piece of an earthworm. Note the movement of the prey toward the feeding individual, the occluded lateral margin of the gape, and hyobranchial expansion after mouth closing. (Right) Selected video frames of terrestrial prey capture in an adult Ichthyophis kohtaoensis. Note the forward lunge, lack of tongue protraction, and lack of hyobranchial depression.

157

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F I G U R E 6.5. Selected sample gape cycles from (A) aquatic larval Epicrionops {n = 5), (B) terrestrial adult Ichthyophis {n = 3), (C) terrestrial adult Hypogeophis {n = 3), and (D) aquatic adult Typhlonectes {n = 3). Note the extreme length of some adult gape cycles and how jaw closing can be interupted and the gape cycle restarted multiple times before the mouth is finally closed on the prey item.

differences. The two aquatic foraging caecilians for which data are available {Typhlonectes and Hypogeophis) use jaw prehension to capture aquatic prey and cannot suction feed (O'Reilly, 1995). However, Typhlonectes does depress the hyobranchium in conjunction with mouth closing (Fig. 6.6, Right), which probably keeps the lunging caecilian from pushing prey items away ("compensatory suction" of Van Damme and Aerts 1997). Compared to terrestrial caecilians, Typhlonectes has relatively fast jaw movements for its body size (O'Reilly, 1995). Individuals of Hypogeophis increase the speed of their jaw movements when fed the same prey item in water than on land. However, this facultative increase in speed does not result in movements as quick as those seen in Typhlonectes, suggesting that the timing of feeding behavior has diverged significantly from that of its terrestrial ancestors. The degree to which the retroarticular process is re-

curved and whether it curves antiororly or posteriorly to the jaw articulation is likely to have significant functional consequences (Fig. 6.7). When the retroarticular process is straight, the interhyoideus will be most effective at large gape angles (Fig. 6.7A). As the retroarticular process becomes more recurved, bite force performance at low gape angles will improve, but at the expense of performance at high gape angles (Fig. 6.7B). The decrease in performance with increasing gape is more pronounced if the jaw curves upward anterior to its articulation with quadrate (Fig. 6.7C). Available data on maximum gape angles support this model, as Ichthyophis, which has a strongly recurved retroarticular process, has only been observed to open the jaws during feeding to about 50°, whereas Hypogeophis and Typhlonectes, with less recurved retroarticular processes, open their mouths to over 70° (O'Reilly, 1995).

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6. Feeding in Caecilians TABLE 6.1 Species Gymnophiona Epicrionops sp.—larvae^ Hypogeophis rostratus' Ichthyophis kohtaoensis^ Typhlonectes nutans ^ Anura Ascaphus truei" Bombina orientalist Bufomarinus^ Discoglossus pictus^ Hyla cinerea" Hymenochirus curtipes^ Rana pipiens (waxworm)^ R. pipiens (earthworm)" Caudata Ambystoma dumerilii^ A. mexicanum^ A. mexicanum^ A. ordinarium^ A. tigrinum—larvae^ A. tigrinum^ A. tigrinum^ Amphiuma means ^ Bolitoglossa occidentalism' B. mexicana^ Cryptobranchus allegheniensis ^ Cynops pyrrhogaster^ Desmognathus fuscus ^' D. marmoratus^ D. quadramaculatus^ D. quadramaculatus' Dicamptodon tenebrosus—larvae^ Ensatina eschscholtzii^ Hynobius nebulosus^ H. kimurae^ Necturus maculosus ^ Pachytriton brevipes^ P. brevipes^ Plethodon glutinosus^ Pleurodeles waltl^ P. waltl' Paramesotriton hongkongensis" Salamandra salamandra" Salamandrina terdigitata^ Siren intermedia ^ Taricha torosa'' Tylototriton verrucosus''

Duration of the Gape Cycle in Amphibians^ Source

Range (msec)

Mean (± SE)

42-58 400-1733 367-4734 300-1033

51.8 ± 1.8 1028 ± 73 1819 ± 189 572 ± 41

O'Reilly O'Reilly O'Reilly O'Reilly

80-280 83-158

-140 126.5 ± 7.6 143 ± 22 134 152 ± 8.1 62.7 ± 4.2 100.8 ± 6.4 163.2 ± 9.8

Nishikawa and Cannatella (1991) O'Reilly (1995) Cans and Gorniak (1982) Nishikawa and Roth (1991) Deban and Nishikawa (1992) O'Reilly (1995) Anderson (1993) Anderson (1993)

88 ± 3.5 59 ± 1.8 69.7 ± 1.2 73 ± 2.6 83 75 107 72 ± 1.9 99.6 ± 1 . 4 108 ± 2 53.3 ± 1.1 162 ± 16.3 92.6 ± 19.6 128 136.1 ± 6.1 109.9 ± 1.1 54.4 ± 2.5 87.4 ± 4.9 115.7 ± 7.2 94.4 ± 5.7 51 ± 1 79 ± 10.9 44.4 ± 2.4 96.3 ± 6.3 75.9 ± 3.2 220 ± 21.2 211 ± 30.3 100 ± 7.1 240 ± 23.1 61 ± 2.8 246 160 ± 10.7

Shaffer and Lauder (1985) Reilly and Lauder (1992) Shaffer and Lauder (1985) Shaffer and Lauder (1985) Shaffer and Lauder (1988) Shaffer and Lauder (1988) Shaffer and Lauder (1988) Reilly and Lauder (1992) Larsen et al (1989) Larsen et al (1989) Reilly and Lauder (1992) Miller and Larsen (1990) Larsen and Beneski (1988) Schwenk and Wake (1993) Larsen and Beneski (1988) Larsen et al (1989) Reilly and Lauder (1992) Larsen et al (1989) Larsen et al (1989) Larsen et al (1989) Reilly and Lauder (1992) Miller and Larsen (1990) O'Reilly (1995) Larsen et al (1989) O'Reilly (1995) Miller and Larsen (1990) Miller and Larsen (1990) Miller and Larsen (1990) Miller and Larsen (1990) Reilly and Lauder (1992) Findeis and Bemis (1990) Miller and Larsen (1990)

92-325 42-108

84-288

50-112 25-58 50-125 144-312 64-468 60-136 90-326

72-248

(1995) (1995) (1995) (1995)

^Note how long the gape cycles of adult caecilians are relative to frogs and salamanders. ^Aquatic feeding. '^Terrestrial feeding.

C. Intraoral Transport After prey is seized, caecilians use different methods of prey transport, depending on the medium in which they are feeding (air vs water) and the size and type

of prey being eaten. Larvae of Epicrionops have only been observed using hydraulic transport (O'Reilly, 1995), despite the presence of a well-developed tongue (Wake, 1989). Metamorphosed caecilians employ two or three methods of transport, depending on the

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F I G U R E 6.6. (Left) Selected video frames of terrestrial prey capture in an adult Hypogeophis rostratus. Note the forward lunge, lack of tongue protraction, and lack of hyobranchial depression. (Right) Selected video frames of aquatic prey capture in an adult Typhlonedes nutans. Note the forward lunge, lack of tongue protraction, and substantial hyobranchial depression during mouth closing.

161

6. F e e d i n g in Caecilians

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90°

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20 0,

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Gape Angle (°)

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F I G U R E 6.7. Model of the relationship of mechanical advantage and gape angle in the three major arrangements of the retroarticular process and interhyoideus found in living caecilians. Dashed lines with arrows represent force applied by the interhyoideus. Arrangement A has its best mechanical advantage at high gape angles. Arrangements B and C reach peak performance at low gape angles. Model assumes identical force input and retroarticular process length across all systems.

situation. On land, caecilians use a combination of inertial transport (releasing prey and lunging over it, using the mass of the prey as a counter weight) and lingual transport on larger prey items, while using lingual transport alone on smaller items (Bemis et ah, 1983; O'Reilly, 1995). In water, adults add hydraulic transport sequences to the mix (O'Reilly, 1995). During transport, caecilians often use longitudinal spinning to help subdue prey (Tanner, 1971; Bemis et al, 1983), the function of which is still not well understood. Larger arthropods (such as large crickets) are often rubbed against the substrate to disable or remove their limbs.

IV. EVOLUTION Living caecilians represent an ancient lineage and began to diverge from one another over 100 million

years ago (Hedges et al, 1993). The only fossil material that has been attributed to Gymnophiona that includes cranial material is Eocaecilia micropodia from the early Jurassic. This species is thought to be the closest known outgroup to living caecilians Jenkins and Walsh, 1993). Unlike living caecilians, Eocaecilia had limbs and limb girdles. Its skull was solidly roofed, lending some support to arguments that the ancestor of living caecilians lacked fenestrae in the skull (Carroll and Currie, 1975; Jenkins and Walsh, 1993). However, read Wake and Hanken (1982) and Nussbaum (1983) for counterarguments and reviews of the available evidence. The issue of whether the solidly roofed skull has secondarily evolved in living caecilians as an adaptation for burrowing or is homologous to the condition seen in the first tetrapods will only be settled by a vast improvement in the available fossil record of the ancestors of living amphibians. For the purposes of this

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chapter, I will largely follow the scenario of Nussbaum (1977,1983) while acknowledging that the fenestrated condition of adult rhinatrematids may have evolved within that lineage from a solid skulled ancestor through paedomorphosis. The common ancestor of living caecilians was most likely oviparous, with the female guarding her clutch of eggs until they hatched into free-living, aquatic larvae. These larvae localized prey by the combined use of olfaction and electroreception, after which they used suction feeding for prey capture. The skull had large temporal fenestrae and was strongly kinetic, especially in the case of movement of the quadrate relative to the braincase (streptostyly). The hyobranchial apparatus may have been cartilaginous or ossified, but almost certainly possessed many independent elements that articulated such that posterior-directed force applied to the basibranchial series was translated into ventrally directed force expanding the buccopharynx. The flow of water that carried prey into the mouth was focused by well-developed labial lobes. The teeth where pedicellate and best developed in the front of the mouth, where two rows where present on both the upper and the lower jaws. On the upper jaw, the outer (premaxillary-maxillary) series of teeth did not extend as far caudally as the inner (vomer-palatine) series. In contrast, on the lower jaw, the outer row of teeth was more extensive than the inner row. After capture, hydraulic transport was used to transport prey to the pharynx. After spending many months as a larva, this common ancestor metamorphosed into a terrestrial, semifossorial adult. During metamorphosis, the skull became more solidly constructed and less kinetic due to the fusion of some dermal elements that were independent in larvae. However, the skull still had large temporal fenestrae, components of the levator mandibulae complex originating on the midline of the skull and passing through a large gap between the squamosal and the parietal before inserting on the lower jaw. Although the quadrate was now connected more firmly to an expanded squamosal, it could still move mediolaterally relative to the neurocranium during prey transport. The lateral line system, not being useful on land, was lost at metamorphosis. The lacrimal (tear) ducts were used to transport chemicals directly to the vomeronasal organ from the eye, possibly allowing the animals to smell even when the nostrils were pressed into the soil during burrowing. This adult used jaw prehension to capture prey, with the levator mandibulae complex being aided during mouth closing by an unusually oriented interhyoideus muscle inserting on the ventral edge of the retroaricular process of the lower jaw. The dentition consisted of two rows of numerous

teeth in both the upper and the lower jaws, with all four rows extending caudally to the corner of the gape. The mouth opening was terminal, looking like that of an adult salamander. The first evolutionary changes from the just-described ancestral pattern concerned the terrestrial adult stage, with the characteristics of the larval stage remaining relatively constant. As the adult stage became more specialized for burrowing, some signficant changes took place in head anatomy. The mouth opening became sub terminal, with the lower jaw being recessed into the upper jaw. The tear duct chemosensory system became more elaborate, with extrinsic eye muscles and other parts of the eye being incorporated into the now protusible tentacle apparatus with an independent aperture located well in front of the orbit. Important transitions during the evolution of the caecilian feeding apparatus include changes in the arrangement of the jaw levators and the degree to which the adductor chamber is roofed by dermal bones. The ancestor of living caecilians apparently possessed a skull that was broadly open between the squamosal and the temporal. Prominent jaw levators originated on the top of the skull and traveled down through these fenestrae and inserted on the lower jaw. This primitive condition is still seen in larval caecilians and in adult rhinatrematids. In a common ancestor of all caecilians other than rhinatrematids, the squamosal became much larger, completely covering the temporal fenestra. Concurrently, the jaw levators were reduced in size, being restricted to the now din\inutive adductor chamber under the squamosal. Temporal fenestrae have subsequently reappeared convergently in three groups {Geotrypetes, Scolecotnorphus, and typhlonectids), but in all of these cases the jaw levators have remained restricted to the adductor chamber. Transitions in the arrangement of the retroarticular process and interhyoideus posterior were also important. A common ancestor of caecilians had a small retroarticular process and an interhyoideus muscle, which originated midventrally and inserted on the ceratohyals. The original shift of insertion to the retroarticular process and subsequent enlargement of the process and muscle probably originally occurred as an adaptation for breathing. As the ancestors of caecilians became more elongate in body form, the ratio of the volume of the buccal chamber to that of the lungs became progressively smaller. Moving the insertion of the interhyoideus to the retroarticular process would increase the stroke volume of the buccal pump and at least partially compensate for these changes (Carrier and Wake, 1995). This condition is closely approximated by the condition seen in living rhinatrematids.

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6. Feeding in Caecilians After the initial shift in the insertion of the interhyoideus, ancestral caecilians made major rearrangements in the jaw apparatus as they became progressively more fossorial. First, there was a concurrent increase in the size of both the interhyoideus and the retroarticular process. At least three times (in ichthyophiids and uraeotyphlids, scolecomorphids, and Atretochoana), the relatively straight retroarticular process has been recurved radically upward. In ichthyophiids and uraeotyphlids, the process is curved posterior to the jaw articulation, whereas in scolecomorphids and Atretochoana the curve occurs before the jaw articulation, such that the articular surface lies in the vertical rather than the horizontal plane. The primitive arrangement of the jaw muscles and skull presents at least two problems for active burrowers that use their heads as the only means of penetration. First, large levators necessarily increase the diameter of the head. Because elongate limbless burrowers use compression to create tunnels, the cost of constructing a given length of tunnel is exponentially related to tunnel diameter (Gans, 1974) and they are most likely under strong selection to minimize body diameter. Because the interhyoideus is tucked behind the skull, relying on it as the primary jaw-closing muscle permitted a vast increase in maximum jawclosing forces with no increase in head diameter. Muscle is also more subject to injury when exposed to crushing forces than is bone. Moving the primary jawclosing muscles behind the skull and roofing the levators with bone would allow more violent burrowing movements than were possible in ancestral caecilians. While the unique arrangement of caecilian jaw-closing muscles is a spectacular adaptation for head-first burrowing, it may have also led to a severe constraint on caecilian cranial evolution. The interhyoideus, ancestrally functioning only as a breathing muscle, has at least one new function (jaw closing) and its position suggests that it plays a prominent role in head movements during burrowing as well (Lawson, 1965b). Condensing all of these functions to a single muscle potentially conserves an enormous amount of muscle volume that would otherwise increase body diameter. However, as single components take on multiple functions, their evolution tends to become severely constrained (Lauder and Liem, 1989). In most living caecilians the interhyodius is the dominant muscle in breathing, jaw closing, and side-to-side head movements during burrowing and, despite its great age, we see remarkably little variation in its arrangement. Interestingly, the only great experiment in caecilian head design is seen in Atretochoana, an animal that does not breathe and is apparently not an accomplished bur-

rower (Nussbaum and Wilkinson, 1995; Wilkinson and Nussbaum, 1997). V. THE FUTURE Caecilians are the most poorly known major group of tetrapods. Regardless of why this is the case, it makes them a gold mine of opportunity for any researcher willing to make the extra effort to acquire and work with these animals. The study of caecilian feeding is no exception. Despite a relatively good understanding of variation in caecilian cranial anatomy, there is a dearth of experimental studies on every aspect of caecilian feeding behavior. The neurophysiology and neuroethology of caecilian prey capture remain to be described. There are only two experimental studies on the sensory systems of caecilians (Himstedt and Fritzsch, 1990; Himstedt and Simon, 1995). Thus we still know very little about how any caecilian perceives its surroundings and finds prey, let alone how prey detection abilities vary among different species. The relative importance of different types of stimuli in different environments and the cellular physiology of various receptors are currently unknown. The motor control of feeding movements and how the neural connections of the interhyoideus have changed during its integration into the jaw closing system also await study. There is currently a single published paper (Bemis et ah, 1983) describing prey capture and transport in any detail and this treats only a single species {Dermophis). There are no detailed descriptions of the feeding behavior of larval or fetal caecilians. There are no quantitative studies on the functional significance of the differences among the five major arrangements of the adult caecilian feeding apparatus, including variation in feeding kinematics, bite force generation, or prey transport behavior. The variation in the contractile characteristics of the different jaw adductors and how this is related to the various biomechanical arrangements seen in living caecilians is also unknown. Although cranial kinesis is widespread among caecilians (Nussbaum, 1977; Wilkinson and Nussbaum, 1997), we know little about its potential functional significance. Ultimately, it would be ideal if the just-mentioned studies were placed in ecological, ontogenetic, and evolutionary contexts. Understanding how caecilians interact with their actual environment would be the ultimate test of the relevance of laboratory studies. Understanding how function varies during ontogeny will provide a complete picture of the demands placed on

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the feeding system as well as the opportunities available through heterochrony during evolution. Finally, placing future studies in an explicit phylogenetic context will allow the synthesis of functional, ecological, and developmental data into a robust portrait of caecilian evolution. Acknowledgments First, I must extend my deep appreciation to Kurt Schwenk for his encouragement and patience during the writing of this chapter. Adam Summers and Nate Kley provided many helpful comments on earlier drafts of this manuscript. Ron Nussbaum and Mark Wilkinson introduced me to caecilian biology and have continued to provide mentoring and insight in all things caecilian for the last 12 years. Ron Nussbaum also supplied many of the animals on which the observations herein are based. Edmund Brodie, Jr., Jonathan Campbell, Louis Porras (Zooherp, Inc., Sandy, Utah), Rob Maclnnes (Glades Herp. Inc., Ft. Myers, Florida), and Ed Budziak aided in the acquisition of specimens. Carl Cans provided logistical and financial support during my initial forays into the topic of caecilian prey capture. Steve Deban and Dale Ritter helped in the videotaping of feeding sequences. Kiisa Nishikawa provided extensive advice and support throughout all aspects of this project. This work was supported by NSF Grants IBN-8909937 and IBN-9211310 to Kiisa Nishikawa, a grant-in-aid-of-research from Sigma Xi, and a Darwin Postdoctoral Fellowship from the Organismic and Evolutionary Biology Program at the University of Massachusetts Amherst.

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and Typhlonectes nutans (Amphibia: Gymnophiona). Zool. J. Linn. Soc. 121:65-76. Tanner K. (1971) Notizen zur pflege und zum verhalten einiger blindwiihlen (Amphibia: Gymnophiona). Salamandra 7 : 9 1 100. Taylor, E. H. (1968) The Caecilians of the World: A Taxonomic Review. Univ. of Kansas Press, Lawrence, KS. Taylor, E. H. (1969) Skulls of the Gymnophiona and their significance in the taxonomy group. Univ. Kansas Sci. Bull. 48:585-689. Taylor, E. H. (1970) The lateral-line system in the caecilian family Ichthyophiidae (Amphibia: Gymnophiona). Univ. Kansas Sci. Bull. 48:861-868. Van Damme, J., and P. Aerts (1997) Kinematics and functional morphology of aquatic feeding in Australian snake-necked turtles (Pleurodira: Chelodina). J. Morph. 233:113-125. Visser, M. H. C. (1963) The cranial morphology of Ichthyophis glutinosus (Linne) and Ichthyophis monochrous (Bleeker). Annale Universiteit van Stellenbosch, Ser. A 38:67-102. Wahnschaffe, U., B. Fritzsch, and W. Himstedt (1985) The fine structure of the lateral-line organs of larval Ichthyophis (Amphibia: Gymnophiona). J. Morph. 186:369-377. Wake, M. H. (1976) The development and replacement of teeth in viviparous caecilians. J. Morph. 148:33-63. Wake, M. H. (1977a) The reproductive biology of caecilians: an evolutionary perspective. Pp. 73-101. In: Reproductive Biology of Amphibians. E. H. Taylor and S. I. Guttman (eds.). Plenum, New York. Wake, M. H. (1977b) Fetal maintenance and its evolutionary significance in the amphibia: Gymnophiona. J. Herp. 11:379-386. Wake, M. H. (1978) Comments on the ontogeny of Typhlonectes obesus, particularly its dentition and feeding. Papeis Avulsos de Zoologia32:l-13. Wake, M. H. (1980a) Reproduction, growth and population structure of the Central American caecilian Dermophis mexicanus. Herpetologica 36:244-256. Wake, M. H. (1980b) Fetal tooth development and adult replacement in Dermophis mexicanus (Amphibia: Gymnophiona): fields versus clones. J. Morph. 166:203-216. Wake, M. H. (1985) The comparative morphology and evolution of the eyes of caecilians (Amphibia, Gymnophiona). Zoomorph. 105:277-295. Wake, M. H. (1987) A new genus of African caecilian (Amphibia: Gymnophiona). J. Herp. 21:6-15. Wake, M. H. (1989) Metamorphosis of the hyobranchial apparatus in Epicrionops (Amphibia, Gymnophiona, Rhinatrematidae): replacement of bone by cartilage. Ann. Sci. Nat. Zool. Biol. Anim. 10:171-182. Wake, M. H. (1992) Reproduction in caecilians. Pp. 112-120 In: Re-

productive Biology of South American Vertebrates. W. C. Hamlett (ed.). Springer-Verlag, New York. Wake, M. H. (1993a) Non-traditional characters in the assessment of caecilian phylogenetic relationships. Herp. Monog. 7:42-55. Wake, M. H. (1993b) The skull as a locomotor organ. Pp. 197-240 In: The Skull Vol. 3. J. Hanken and B. K. Hall (eds.). Univ. of Chicago Press, Chicago. Wake, M. H. (1993c) Evolution of oviductal gestation in amphibians. J. Exp. Zool. 266:394-413. Wake, M. H., and J. Hanken (1982) The development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J. Morph. 173:203223. Wake, M. H., and G. Z. Wurst (1979) Tooth crown morphology in caecilians (Amphibia: Gymnophiona). J. Morph. 159:331-340. Welsch, U., M. Miiller, and C. Schubert (1977) Elektronenmikroskopische und histochemische beobachtungen zur fortpflanzungs vivaprer gymnophionen (Chthonerpeton indistinctum). Zoologische Jahrbuch von Anatomie 97:532-549. Wever, E. G. (1975) The caecilian ear. J. Exp. Zool. 191:63-72. Wever, E. G., and C. Gans (1976) The caecilian ear: further observations. Proc. Natl. Acad. Sci. USA 73:3744-3746. Wiedersheim, R. (1879) Die Anatomie der Gymnophionen. Verlag Gustav Fischer, Jena. Wilkinson, M. (1989) On the status of Nectocaecilia fasciata Taylor, with a discussion of the phylogeny of the Typhlonectidae (Amphibia: Gymnophiona). Herpetologica 45:23-36. Wilkinson, M. (1991) Adult tooth crown morphology in the Typhlonectidae (Amphibia: Gymnophiona): a reinterpretation of variation and its significance. Zeitschrift fiir zoologische Systematische un,d Evolutions-forschung 29:304-311. Wilkinson, M. (1992a) The phylogenetic position of the Rhinatrematidae (Amphibia: Gymnophiona): evidence from the larval lateral line system. Amphibia-Reptilia 13:74-79. Wilkinson, M. (1992b) On the life history of the caecilian genus Uraeotyphlus (Amphibia: Gyrrmophiona). Herp. J. 2:121-124. Wilkinson, M. (1997) Characters, congruence and quality: a study of neuroanatomical and traditional data in caecilian phylogeny. Biol. Rev. 72:423-470. Wilkinson, M., and R. A. Nussbaum (1996) On the phylogenetic position of the Uraeotyphlidae (Amphibia: Gymnophiona). Copeia 1996:550-562. Wilkinson, M., and R. A. Nussbaum (1997) Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae). Biol. J. Linn. Soc. 62:39-109. Wilkinson, M., and R. A. Nussbaum (1998) Caecilian viviparity and amniote origins. J. Nat. Hist. 32:1403-1409.

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7 A Bibliography of Turtle Feeding KURT SCHWENK Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut 06269

I. INTRODUCTION 11. BIBLIOGRAPHY

lonian Bauplan suggests some kind of uniformity. Our comparative ignorance of feeding function in turtles hampers our ability to discern general patterns in the history of tetrapod feeding. The fact that they are an ancient group that might retain ancestral amniote features in some aspects of their feeding system makes their further study all the more desirable.

I. INTRODUCTION The bibliography that follows is hardly exhaustive, but it does serve as an introduction to the literature on turtle feeding. General references on natural history and diet are not included, but a number of important papers on digestive physiology are. Also omitted are references on the systematics of turtles. The emphasis here is on the morphology of the feeding apparatus, feeding function, and behavioral observations of feeding in turtles. Historically, the functional morphology of feeding in turtles has been sadly neglected, but several recent contributions suggest that this is changing. In any case, turtle feeding is badly in need of investigation. One of the attractive features of turtles, as a group, is their diversity. Among other things, they span the range from fully terrestrial to fully aquatic, with everything in between. Thus, turtles, like salamanders, offer the opportunity to examine phenotypic changes in the feeding system associated with a change in the feeding medium (see Bramble and Wake, 1985; Lauder, 1985). Terrestrial turtles share with mammals and lepidosaurs a mobile, muscular tongue, but the intrinsic anatomy, biomechanics, and function of the turtle tongue are virtually unstudied. In general, there is a great deal of morphological diversity among turtle feeding systems that is largely unappreciated, perhaps because the che-

FEEDING (K. Schwenk, ed.)

II. BIBLIOGRAPHY Beisser, C J., J. Weisgram, and H. Splechtna (1995) Dorsal lingual epithelium of Platemys pallidipectoris (Pleurodira, Chelidae). J. Morph. 226:267-276. Beisser, C. J., J. Weisgram, H. Hilgers, and H. Splechtna (1998) Fine structure of the dorsal lingual epithelium of Trachemys scripta elegans (Chelonia: Emydidae). Anat. Rec. 250:127-135. Belkin, D. A., and C. Gans (1968) An unusual chelonian feeding niche. Ecology 49:768-769. Dels, V. L., and S. Renous (1991) Kinematics of feeding in two marine turtles {Chelonia mydas and Dermochelys coriacea). Pp. 73-78. In: Proceedings of the 6th Ordinary General Meeting of the Societas Europaea Herpetologica. Z. Korsos and I. Kiss (eds.). Hungarian Natural History Museum, Budapest. Bels, V. L., J. Davenport, and V. Delheusy (1997) Kinematic analysis of the feeding behavior in the box turtle Terrapene Carolina (L.), (Reptilia: Emydidae). J. Exp. Zool. 277:198-212. Bjorndal, K. A. (1980) Nutrition and grazing behavior of the green turtle Chelonia mydas. Mar. Biol. 56:147-154. Bjorndal, K. A. (1985) Nutritional ecology of sea turtles. Copeia 1985: 736-751. Bjorndal, K. A. (1986) Effect of solitary vs group feeding on intake in Pseudemys nelsoni. Copeia 1986:234-235. Bjorndal, K. A. (1987) Digestive efficiency in a temperate herbivorous reptile, Gopherus polyphemus. Copeia 1987:714-720. Bjorndal, K. A. (1989) Flexibility of digestive responses in two gen-

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eralist herbivores, the tortoises Geochelone carbonaria and Geochelone denticulata. Oecologia 78:317-321. Bjomdal, K. A. (1990) Digestive processing in a herbivorous freshwater turtle: consequences of small-intestine fermentation. Physiol. Zool. 63:1232-1247. Bjorndal, K. A. (1990) Digestibility of the sponge Chondrilla nucula in the green turtle, Chelonia mydas. Bull. Mar. Sci. 47:567-570. Bjorndal, K. A. (1991) Digestive fermentation in green turtles, Chelonia mydas, feeding on algae. Bull. Mar. Sci. 48:166-171. Bjorndal, K. A. (1992) Body size and digestive efficiency in a herbivorous freshwater turtle: advantages of small bite size. Physiol. Zool. 65:1028-1039. Bjorndal, K. A. (1993) Digestive efficiencies in herbivorous and omnivorous freshwater turtles on plant diets: do herbivores have a nutritional advantage. Physiol. Zool. 66:384-395. Bjomdal, K. A. (1997) Fermentation in reptiles and amphibians. Pp. 199-230. In: Gastrointestinal Microbiology, Vol. 1. R. I. Mackie and B. A. White (eds.). Chapman and Hall, New York. Bjorndal, K. A. (1997) Foraging ecology and nutrition of sea turtles. Pp. 199-321. In: The Biology of Sea Turtles. P L. Lutz and J. A. Musick (eds.). CRC Press, Boca Raton, LA. Bramble, D. M. (1971) Functional Morphology, Evolution, and Paleoecology of Gopher Tortoises. Unpublished doctoral dissertation, Univ. of California, Berkeley. Bramble, D. M. (1973) Media dependent feeding in turtles. Am. Zool. 13:1342. [abstract] Bramble, D. M. (1974) Occurrence and significance of the Os transiliens in gopher turtles. Copeia 1974:102-109. Bramble, D. M. (1978) Functional analysis of underwater feeding in the snapping turtle. Am. Zool. 18:623. [abstract] Bramble, D. M. (1980) Feeding in tortoises and mammals: why so similar? Am. Zool. 20:931. [abstract] Bramble, D. M., and D. B. Wake (1985) Feeding mechanisms of lower tetrapods. Pp. 230-261. In: Functional Vertebrate Morphology. M. Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake (eds.). Harvard Univ. Press, Cambridge, MA. Carmignani, M. P. A., and G. Zaccone (1975) Histochemical distribution of acid mucopolysaccarides in the tongue of reptiles. I. Chelonia {Pseudemys scripta Clark). Ann. Histochim. 20:77-88. Dalrymple, G. H. (1977) Intraspecific variation in the cranial feeding mechanism of turtles of the genus Trionyx (Reptilia, Testudines, Trionychidae). J. Herp. 11:255-285. Dalrymple, G. H. (1979) Packaging problems of head retraction in trionychid turtles. Copeia 1979:655-660. Davenport, J., M. Spikes, S. M. Thornton, and B. O'Kelly (1992) Crabeating in the diamondback terrapin Malaclemys terrapin: dealing with dangerous prey. J. Mar. Biol. Assoc. U. K. 72:835-848. Davenport, J., T. M. Wong, and J. East (1992) Feeding and digestion in the omnivorous estuarine turtle Batagur baska (Gray). Herp. J. 2:133-139. Drummond, H., and E. R. Gordon (1979) Luring in the neonate alligator snapping turtle {Macroclemys temminckii): description and experimental analysis. Z. Tierpsychol. 50:136-152. Edgeworth, F. H. (1935) The Cranial Muscles of Vertebrates. Cambridge Univ. Press, Cambridge. Fenchel, T. M., C. P McRoy, J. C. Ogden, P Parker, and W. E. Rainey (1979) Symbiotic cellulose degradation in green turtles, Chelonia mydas L. Appl. Environ. Microbiol. 37:348-350. Ferdinand, L. Prinz von Bayern (1884) Anatomic der Zunge. Fine vergleichend-anatomische Studie. Literarisch-Artistische Anstalt (Theodor Riedel), Munich. Fuchs, H. (1907) IJber das Hyobranchialskelett von Fmys lutaria und seine Entwicklung. Anat. Anz. 31:33-39. Fiirbringer, M. (1922) Das Zungenbein der Wirbeltiere insbesondere der Reptilien und Vogel. Abh. der Heidelberger Akad., math.naturw.Kl. 11:1-164.

Gaffney, E. S. (1972) An illustrated glossary of turtle skull nomenclature. Am. Mus. Novit. No. 2486:1-33. Gaffney, E. S. (1979) Comparative cranial morphology of Recent and fossil turtles. Bull. Am. Mus. Nat. Hist. 164(2): 67-376. George, J. C , and R. V. Shah (1954) The myology of the head and neck of the common Indian pond turtle, Lissemys punctata granosa Schoepff. J. Anim. Morphol. Physiol. 1:1-12. George, J. C , and R. V. Shah (1955) The myology of the head and neck of the Indian tortoise, Testudo elegans. J. Anim. Morphol. Physiol. 2:1-13. Gnanamuthu, C. P. (1937) Comparative study of the hyoid and tongue of some typical genera of reptiles. Proc. Zool. Soc. Lond. Ser.B 1937:1-63 Graper, L. (1932) Die das Zungenbein und die Zunge bewegenden Muskeln der Schildkroten I. Jena. Z. Naturwiss. 66:169-198. Graper, L. (1932) Die das Zungenbein und die Zunge bewegenden Muskeln der Schildkroten II. Jena. Z. Naturwiss. 66:274-280. Hailey, A. (1997) Digestive efficiency and gut morphology of omnivorous and herbivorous African tortoises. Can. J. Zool. 75:787794. Iwasaki, S.-I. (1992) Fine structure of the dorsal epithelium of the tongue of the freshwater turtle, Geoclemys reevesii (Chelonia, Emydinae). J. Morph. 211:125-135. Iwasaki, S.-I., T. Asami, Y. Asami, and K. Kobayashi (1992) Fine structure of the dorsal epithelium of the tongue of the of the Japanese terrapin, Clemmys japonica (Cheloia [sic], Emydinae). Arch. Histol.Cytol. 55:295-305. Iwasaki, S.-I., T. Asami, and C. Wanichanon (1996) Ultrastructural study of the dorsal lingual epithelium of the soft-shelled turtle, Trionyx cartilagineus (Cheloia [sic], Trionychidae). Anat. Rec. 246: 305-316. Iwasaki, S.-I., T. Asami, and C. Wanichanon (1996) Fine structure of the dorsal lingual epithelium of the juvenile hawksbill turtle, Eretmochelys imbricata bissa. Anat. Rec. 244:437-443. Iwasaki, S.-I., C. Wanichanon, and T. Asami (1996) Histological and ultrastructural study of the lingual epithelium of the juvenile Pacific ridley turtle, Lepidochelys olivacea (Chelonia, Cheloniidae). Ann. Anat. 178:243-250. Iwasaki, S.-I., C. Wanichanon, and T. Asami (1996) Ultrastructural study of the dorsal lingual epithelium of the Asian snail-eating turtle, Malayemys subtrijuga. Ann. Anat. 178:145-152. Kochva, E. (1978) Oral glands of Reptilia. Pp. 43-161. In: Biology of the Reptilia, Vol. 8. C. Gans and K. A. Cans (eds.). Academic Press, New York. Korte, G. E. (1980) Ultrastructure of the tastebuds of the red-eared turtle, Chrysemys scripta elegans. J. Morph. 163:231-252. Lakjer, T. (1926) Studien Uber die Trigeminus-versorgte Kaumuskulatur der Sauropsiden. C. A. Rietzel, Copenhagen. Lauder, G. V. (1985) Aquatic feeding in lower vertebrates. Pp. 210229. In: Functional Vertebrate Morphology. M. Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake (eds.). Harvard Univ. Press, Cambridge, MA. Lauder, G. V., and T. Prendergast (1992) Kinematics of aquatic prey capture in the snapping turtle Chelydra serpentina. J. Exp. Biol. 164:55-78. Lee, M. S. Y. (1997) The evolution of beaks in reptiles: a proposed evolutionary constraint. Evol. Theor. 11:249-254. Legler, J. M. (1962) The Os transiliens in two species of tortoises, genus Gopher us. Herpetologica 18:68-69. Legler, J. M. (1976) Feeding habits of some Australian short-necked tortoises. Victorian Nat. 93:40-43. Legler, J. M. (1978) Observations on behavior and ecology in an Australian turtle, Chelodina expansa (Testudines: Chelidae). Can. J. Zool. 56:2449-2453. Legler, J. M. (1989) Diet and head size in Australian chelid turtles, genus Emydura. Ann. Soc. Roy. Zool. Belgique 119, Suppl. 1:1-10.

7. A Bibliography of Turtle F e e d i n g Legler, J. M. (1993) Family Chelidae. Pp. 142-152. In: Fauna of Australia, Vol. 2A. C. J. Glasby G. J. B. Ross, and P. L. Beesley (eds.). Australian Government Publ. Service, Canberra. Legler, J. M. (1993) Morphology and physiology of the Chelonia. Pp. 108-119. In: Fauna of Australia, Vol. 2A. C. J. Glasby G. J. B. Ross, and P. L. Beesley (eds.). Australian Government Publ. Service, Canberra. Lemell, P., and J. Weisgram (1997) Feeding patterns of Pelusios castaneus (Chelonia: Pleurodira). Neth. J. Zool. 47:429-441. Lubosch, W. (1933) Untersuchungen iiber die Visceral muskulatur der Sauropsiden. (Der Untersuchungen iiber die Kaumuskulatur der Wirbeltiere 3. Teil.). Gegenbaurs Morph. Jb. 72:584-666. Lubosch, W. (1938) Muskeln des Kopfes: Viscerale Muskulatur. Pp. 1011-1106. In: Handbuch der Vergleichenden Anatomie der Wirbeltiere, Vol. 5. L. Bolk, E. Goppert, E. Kallius, and W. Lubosch (eds.). Urban and Schwarzenberg, Berlin (1967 reprint, A. Asher and Co., Amsterdam). Marlow, R. W., and K. Tollestrup (1982) Mining and exploitation of natural mineral deposits by the desert tortoise, Gopherus agassizii. Anim. Behav. 30:475-478. Meyer, V., and L. Prutkin (1974) An ultrastructural study of the oral mucous membrane of the turtle, Pseudemys scripta elegans. Acta Anat. 89:89-99. Meylan, A. (1988) Spongivory in hawksbill turtles: a diet of glass. Science 239:393-395 Nalavalde, M. N., and A. T. Varute (1976) Histochemical studies on the mucins of the vertebrate tongue. VIII. Histochemical analysis of mucosubstances in the tongue of the turtle. Folia Histochem. Cytochem. 14:123-134. Owen, R. (1866) On the Anatomy of Vertebrates, Vol. 1. Longmans, Green, and Co., London. Parsons, T. S. (1968) Variation in the choanal structure of Recent turtles. Can. J. Zool. 46:1235-1263. Pevzner, R. A., and N. A. Tikhonova (1979) Fine structure of the taste buds of the Reptilia. I. Chelonia. Tsitologiya 21:132-138. Poglayen-Neuwall, I. (1953) Untersuchungen der Kiefermuskulatur und deren Innervation bei Schildkroten. Acta Zool. 34:241-291. Poglayen-Neuwall, I. (1953/54) Die Besonderheiten der Kiefermuskulatur von Dermochelys coriacea. Anat. Anz. 100:22-32. Pritchard, P. C. H. (1971) The leatherback or leathery turtle, Dermochelys coriacea. lUCN Monograph 1:1-39. Ray, C. E. (1959) A sesamoid bone in the jaw musculature of Gopherus polyphemus (Reptilia: Testudinidae). Anat. Anz. 107:85-91. Rhodin, A. G. J., F Medem, and R. A. Mittermeier (1981) The occurrence of neustophagia among podocnemine turtles. Br. J. Herp. 6:175-176. Romer, A. S. (1956) Osteology of the Reptiles. Univ. of Chicago Press, Chicago. Ruckes, H. (1937) The lateral arcades of certain emydids and testudinids. Herpetologica 1:97-103. Schumacher, G.-H. (1953/1954) Beitrage zur Kiefermuskulatur der Schildkroten. I. Mitteilung. Wiss. Z. Univ. Greifswald Math. Nat. 3:457-518. Schumacher, G.-H. (1954/1955) Beitrage zur Kiefermuskulatur der Schildkroten. II. Mitteilung. Wiss. Z. Univ. Greifswald Math. Nat. 4:501-518. Schumacher, G.-H. (1954/1955) Beitrage zur Kiefermuskulatur der Schildkroten. III. Mitteilung. Wiss. Z. Univ. Greifswald Math. Nat. 4:559-601. Schumacher, G.-H. (1956) Morphologische Studie zum Gleitmechanismus des. M. adductor mandibularis externus bei Schildkroten. Anat. Anz. 103:1-12. Schumacher, G.-H. (1956) Uber die Fascien des Kopfes der nebst einigen Bemerkungen zu der Arbeit von Tage Lakjer 1926. Zool. Anz. 156:35-54.

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Schumacher, G.-H. (1973) Die Kopf- und Halsregion der Lederschildkrote. Anatomische Untersuchungen im Vergleich zu anderen rezenten Schildkroten. Abhandl. Akad. Wissensch. DDR, No. 2. Akademie-Verlag, Berlin. Schumacher, G.-H. (1973) The head muscles and hyolaryngeal skeleton of turtles and crocodilians. Pp. 101-199. In: Biology of the Reptilia, Vol. 4. C. Gans and T S. Parsons (eds.). Academic Press, New York. Secor, S. M., and J. Diamond (1999) Maintenance of digestive performance in the turtles Chelydra serpentina, Sternotherus odoratus, and Trachemys scripta. Copeia 1999:75-84. Sewertzoff, S. A. (1929) Zur Entwicklungsgeschichte der Zunge bei den Reptilien. Acta Zool. 10:231-341. Shah, R. V. (1963) The neck musculature of a cryptodire (Deirochelys) and a pleurodire (Ghelodina) compared. Bull. Mus. Comp. Zool. 129:343-368. Siebenrock, F (1898) Uber den Bau und die Entwicklung des Zungenbein-apparates der Schildkroten. Ann. Naturhist. Hofmus. Wien. 13:424-437. Smith, D. T. J. (1989) The Cranial Morphology of Fossil and Living Sea Turtles (Cheloniidae, Dermochelyidae and Desmatochelyidae). Unpublished doctoral dissertation, Kingston Polytechnic University, United Kingdom. Sondhi, K. C. (1958) The hyoid and associated structures in some Indian reptiles. Ann. Zool. Acad. Zool. (Lond.) 2:155-239. Spindel, E. L., J. L. Dobie, and D. F Buxton (1987) Functional mechanisms and histologic composition of the lingual appendage in the alligator snapping turtle, Macroclemys temmincki (Troost) (Testudines: Chelydridae). J. Morph. 194:287-301. Summers, A. P., K. F. Darouian, A. M. Richmond, and E. L. Brainerd (1998) Kinematics of aquatic and terrestrial prey capture in Terrapene Carolina, with implications for the evolution of feeding in cryptodire turtles. J. Exp. Zool. 281:280-287. Thompson, J. S. (1932) The anatomy of the tortoise. Sci. Proc. Roy. Soc. Dublin 20:359-461. Uchida, T (1989) Ultrastructural and histochemical studies on the taste buds in some reptiles. Arch Histol. Jap. 43:459-478. Van Damme, J., and P. Aerts (1997) Kinematics and functional morphology of aquatic feeding in Australian snake-necked turtles (Pleurodira; Chelodina). J. Morph. 233:113-125. Versluys, J. (1936) Kranium und Visceralskelett der Sauropsiden. 1. Reptilien. Pp. 699-808. In: Handbuch der Vergleichenden Anatomie der Wirbeltiere. Vol. 4. L. Bolk, E. Goppert, E. Kallius, and W. Lubosch (eds.). Urban and Schwarzenberg, Berlin (1967 reprint, A. Asher and Co., Amsterdam). Vogt, R. C , D. M. Sever, and G. Moreira (1998) Esophageal papillae in pelomedusid turtles. J. Herp. 32:279-282. Weisgram, J. (1985) Feeding mechanics of Claudius angustatus Cope 1865. Pp. 257-260. In: Functional Morphology in Vertebrates (Fortschr. Zool. Vol. 30). H.-R. Duncker and G. Fleischer (eds.). Gustav Fischer, Stuttgart. Weisgram, J., and H. Splechtna (1990) Intervertebral movability in the neck of two turtle species {Testudo hermanni hermanni, Pelomedusa subrufa). Zool. Jb. Anat. 120:425-431. Weisgram, J., and H. Splechtna (1992) Cervical movement during feeding in Chelodina novaeguinaeae (Chelonia, Pleurodira). Zool. Jb. Anat. 122:331-337. Weisgram, J., H. Ditrich, and H. Splechtna (1989) Comparative functional anatomical study of the oral cavity in two turtle species. Plzen. Lek. Sborn., Suppl. 59:117-122. Winokur, R. M. (1988) The buccopharyngeal mucosa of the turtles (Testudines). J. Morph. 196:33-52. Wocheslander, R., H. Hilgers, and J. Weisgram (1999) Feeding mechanism of Testudo hermanni boettgeri (Chelonia, Cryptodira). Neth. J. Zool. 49:1-13.

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8 Feeding in Lepidosaurs KURT SCHWENK

Department of Ecology and Evolutionary Biology University of Connecticut Storrs, Connecticut 06269

I. INTRODUCTION

I. INTRODUCTION 11. LEPIDOSAURIANPHYLOGENY AND CLASSIFICATION III. NATURAL HISTORY A. Diet B. Foraging Ecology C. Sensory Basis of Food Location and Identification IV. MORPHOLOGY OF THE FEEDING APPARATUS A. Skull and Mandible B. Dentition C. Hyobranchial Apparatus D. Jaw Musculature E. Tongue V. FEEDING FUNCTION A. Overview of Feeding B. Feeding Stages C. Feeding in Sphenodon D. Feeding in Iguania E. Feeding in Scleroglossa F. Biomechanics of Lingual Prey Capture G. Function of Cranial Kinesis VI. SPECIALIZED FEEDING SYSTEMS A. Chameleons B. Amphisbaenians C. Komodo Monitor D. Snakes VII. THE EVOLUTION OF FEEDING IN LEPIDOSAURS A. Evolution of Ingestion Mode B. Post-Ingestion Feeding Stages C. Evolution of the Gape Cycle D. Tongue Evolution E. Dietary Specialization F. Feeding Systems, Functional Units, and Evolutionary Constraint VIII. FUTURE DIRECTIONS References

FEEDING (K. Schwenk, ed.)

This chapter considers the structure, function, and evolution of the feeding system in nonophidian lepidosaurs—tuatara, lizards, and amphisbaenians. The latter two groups comprise, along with snakes, the squamate reptiles (Squamata). Although snakes are cladistically nested within squamates, their feeding systems have diverged sufficiently from other taxa to merit separate treatment (Chapter 9). They are, however, considered in this chapter in a general sense, as in the discussion of evolutionary patterns within Lepidosauria. Lepidosaurs offer a number of attributes that make them attractive subjects for study in the context of tetrapod feeding mechanisms. First, they are phylogenetically well positioned to be informative about evolutionary trends and patterns in the tetrapod clade. Perhaps more to the point is that many of them apparently retain a relatively primitive, or at least generalized, phenotype as compared to other living amniotes and so provide better structural analogues for reconstructing the ancestral-feeding mode. For example, most lepidosaurs retain an unspecialized, welldeveloped hyobranchial apparatus and a mobile, complexly muscled tongue. The latter trait they share with mammals and turtles and so we can infer its presence in the common anmiote ancestor. The muscular tongue is of considerable intrinsic interest. Squamate tongues haveprovided part of the empirical basis for the development of the muscular hydrostatic model of movement (e.g., Kier and Smith, 1985; Smith and Kier, 1989) and, due to their relatively more predictable

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kinematics relative to mammal tongues, they are receiving increasing attention from modelers (e.g., Chiel et ah, 1992; van Leeuwen, 1997; van Leeuwen and de Groot, in preparation). Second, the feeding apparatus, particularly the tongue, is highly variable among lepidosaurs and so provides the grist for basic evolutionary studies, including phylogenetic analyses (e.g., Schwenk, 1988, and references therein), as well as studies of evolutionary pattern and process (e.g., Robinson, 1967; Schwenk, 1993b, 1995a,b; Bels et al, 1994; Kardong et al, 1997; Wagner and Schwenk, 2000). The lepidosaurian-feeding system is of particular interest in the latter case because there has been a fundamental shift in feeding mode within the group from tongue-based ingestion to jaw-based ingestion, corresponding cladistically to the origin of the Scleroglossa, one of two basal squamate clades (see later). The acquisition of jaw prehension, therefore, provides a model system for studying transitions in complex, functionally integrated systems (Schwenk, 1993b, 1995a, 2000b; Wagner and Schwenk, 2000). A related point is that the squamate tongue subserves two fundamentally different functions: feeding and vomeronasal chemoreception. A biomechanical consideration of tongue design suggests that a tongue phenotypically optimized for feeding is a poor chemoreceptor, whereas a tongue optimized for chemoreception is poorly designed for feeding function (Schwenk, 1993b, 1995a; Wagner and Schwenk, 1999). Hence, there is an evolutionary tension between these two functions that plays out in the evolution of tongue form. Clade-specific solutions to the "dilemma" posed by this evolutionary trade-off provide insight into underlying processes of phenotypic evolution (Schwenk, 1995a, 2000b, in preparation; Wagner and Schwenk, 2000).

IL LEPIDOSAURIAN PHYLOGENY A N D CLASSIFICATION Lepidosauria is a diverse clade of reptiles comprising approximately 7150 species of tuatara, lizards, snakes, and amphisbaenians (Pough et al, 1998). It is the sister group of Archosauria, which includes crocodilians, birds, and various extinct diapsid reptiles, such as the dinosaurs (Gauthier et al, 1988), or of turtles (Testudines) plus archosaurs (e.g.. Hedges and Poling, 1999; Kumazawa and Nishida, 1999) (Fig. 8.1). Lepidosauria is further divided into the Rhynchocephalia and Squamata, the former containing two species of tuatara, genus Sphenodon (Daugherty et al, 1990), and the latter, all remaining lepidosaurian species. Squamates are, themselves, divided into two basal clades.

the Iguania and Scleroglossa, and these, in turn, are subdivided into several suprafamilial groups (Fig. 8.1). A molecular study of nuclear and mitochondrial gene sequences suggested that Sphenodon is more closely related to archosaurs (+ turtles) than to squamates, thus splitting the Lepidosauria as presently construed (Hedges and Poling, 1999). Such a phylogenetic hypothesis is extremely unlikely in the face of morphological data. It would deny the 35 morphological synapomorphies identified by Gauthier et al (1988) uniting Sphenodon and Squamata relative to all other amniotes. Furthermore, one would find it very difficult to identify morphological synapomorphies uniting tuatara (+ fossil sphenodontids) with a clade including crocodilians, birds, and turtles. Morphology overwhelmingly supports a monophyletic Lepidosauria. Lepidosauria is an ancient group with fossil lizards known from the Upper Permian (approximately 250 mybp) and sphenodontids from the Triassic (Estes, 1983; Carroll, 1988b). Many Late Cretaceous (approximately 7b mybp) fossil species are assignable to modern families and some Late Jurassic (135+ mybp) taxa are recognizable as varanoids related to living monitor lizards and snakes (Estes, 1983). In traditional classifications, Lepidosauria is accorded the rank of subclass with Rhynchocephalia and Squamata as orders within it (e.g., Romer, 1956). Lizards (Lacertilia or Sauria), snakes (Serpentes or Ophidia), and amphisbaenians (Amphisbaenia) are given equal categorical ranking as suborders within the order Squamata, despite the fact that relationships among these groups remain poorly understood. Amphisbaenians were historically regarded as a family of "lizards" and called Amphisbaenidae in suit (e.g.. Camp, 1923), but later work suggested that these unusual, fossorial squamates were quite distinct from "typical" lizards and deserving of subordinal status in equality with lizards and snakes (e.g.. Cans, 1978; Crook and Parsons, 1980; Bellairs and Cans, 1982). Needless to say, such traditional classifications were crafted by workers in the context of "evolutionary taxonomy" rather than phylogenetic (cladistic) systematics, thus they were not overly concerned that the classification mirror phylogenetic relationships among the groups. Rather, recognition of Serpentes, Lacertilia, and Amphisbaenia as separate but equal ranks within Squamata calls attention to the relative morphological distinctness of each taxon. Indeed, this distinctness has been the basis for much of the ambiguity regarding the phylogenetic position of snakes and amphisbaenians relative to lizards. It has sometimes been suggested that each of these taxa is completely outside the others, i.e., monophyletic (e.g., Hoffstetter, 1968; Rieppel, 1978c, 1983; see Rieppel, 1988, for a review), but most

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SQUAMATA I FIGURE 8.1. (A) Phylogeny of Lepidosauria based on Estes et ah (1988). Amphisbaenia and Dibamidae are not included because their positions are uncertain; however, most evidence suggests placement of Amphisbaenia within Scleroglossa. Estes et al. (1988) declined to place snakes (Serpentes) in the phylogeny, but most data support varanoid affinities. (B) Squamate relationships based on Lee (1998). Taxa that differ in their placement relative to (A) are shown in bold type.

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studies suggest that snakes and amphisbaenians are nested within the "lizard" clade (e.g.. Camp, 1923; Estes et al, 1988; Schwenk, 1988; Caldwell and Lee, 1997; Lee, 1998; Caldwell, 1999), thus rendering "Lacertilia," as traditionally conceived, a paraphyletic taxon. "Lizard," however, remains useful as an informal term for nonsnake, nonamphisbaenian squamates. Current consensus accepts a monophyletic Squamata comprising two basal clades, Iguania and Scleroglossa (Estes et al., 1988), with snakes and probably amphisbaenians as members of Scleroglossa (Fig. 8.1). Unfortunately, molecular analyses of higher-level squamate relationships that might help resolve these issues are thus far unconvincing, having been poorly conceived and methodologically flawed [see Macey and Verma's (1997) reanalysis and discussion of Forstner et al. (1995)]. Despite general acceptance of Iguania and Scleroglossa as monophyletic taxa, details of relationships within each major clade remain contentious. Iguania, for example, is traditionally held to comprise three families, Iguanidae, Agamidae, and Chamaeleonidae, with the latter two sister taxa (Camp, 1923; Estes et al, 1988). However, morphological evidence for monophyly of Iguanidae was never compelling (Etheridge and de Queiroz, 1988; Estes et al, 1988; Schwenk, 1988; Frost and Etheridge, 1989) and the paraphyly of Agamidae relative to Chamaeleonidae has been suspected (Estes et al, 1988; Frost and Etheridge, 1989); hence, on the basis of a cladistic analysis. Frost and Etheridge (1989) dispensed with the traditional three-family taxonomy and erected nine separate iguanian families based on those taxa for which monophyly was strongly supported (Etheridge and de Queiroz, 1988; Frost and Etheridge, 1989; reviewed by Schwenk, 1994d). This resulted in a radical taxonomy that, unfortunately, has been widely adopted in the herpetological literature (e.g., Conant and Collins, 1998; Pough et al, 1998). Nonetheless, molecular evidence has provided strong support for iguanid monophyly and limited support for agamid monophyly, potentially vindicating the traditional taxonomy. I therefore choose to retain the threefamily system here, as I have elsewhere [see Schwenk (1994d) for additional arguments in favor of this system]. Nevertheless, it must be borne in mind that taxonomies are fluid and subject to change in accordance with the shifting weight of character evidence. The case of Scleroglossa is equally contentious, if not more so. The placement of several groups, notably Amphisbaenia, Serpentes, Dibamidae, and Xantusiidae, is especially problematic. Phylogenetic uncertainties are compounded by the fact that these taxa are limbless and/or fossorial and therefore prone to morphological convergence (Estes et al, 1988; Lee, 1998; Lee and Caldwell, 1998). Estes et al (1988) felt that

character evidence was too ambiguous to situate some taxa, so they designated Serpentes, Amphisbaenia, and Dibamidae as Scleroglossa incertae sedis, i.e., of uncertain position within the group. There is a growing consensus, however, that snakes are anguimorphans,. probably derived from within the varanoids and possibly the sister group of the living monitor lizards, Varanidae and Lanthanotidae (e.g., McDowell and Bogert, 1954; Schwenk, 1988; Caldwell and Lee, 1997; Lee, 1997, 1998). However, Caldwell (1999) suggested that snakes are the sister taxon of all other scleroglossans (although in some of his analyses, snakes are associated with various groups within Scleroglossa, including varanoids). Placement of other taxa remains even less certain [see Lee (1998) for one recent treatment]. Given these ambiguities, I illustrate two possible phylogenies for Squamata based on Estes et al (1988) and Lee (1998) that differ in their placement of some scleroglossan taxa (Figs. 8.1A and 8.1B, respectively). Throughout this chapter I use the former phylogeny, but the differences have little effect on interpreting major patterns of feeding evolution in Lepidosauria. Finally, it is worth noting that in recent, phylogenetic classifications of lepidosaurs, traditional Linnean ranks above the family level are rarely used (e.g., Pough et al, 1998). This reflects a current trend toward adopting the principles of "phylogenetic taxonomy" in classification, a system that assigns names according to shared ancestry, which does not, therefore, impose categorical "ranks." Such ranks are found to be unnecessary in a phylogenetic system (see de Queiroz and Gauthier, 1992,1994; de Queiroz, 1996,1997).

III. NATURAL HISTORY A. Diet Greene (1982) noted that lizard diets had not been reviewed to that time. Remarkably, this remains true today. Greene's brief treatment remains one of the best, single sources of lizard dietary information. Greer (1989) and Pianka (1986) summarized diets for the diverse Australian lizard fauna and desert lizard communities, respectively. However, to gain a complete picture of lepidosaurian diets, one must scour the primary, natural history literature through which relevant data are peppered. A coniplete review is far beyond the scope of this chapter; however, a short consideration of diet is required to place the analysis of feeding form and function in context. It can be said, first, that lepidosaurian diets are diverse—so diverse that the range of food types eaten is nearly as broad as the dietary breadth of tetrapods as a

8. Feeding in Lepidosaurs whole. Some individual species have very broad diets and eat a wide range of food (euryphagy), whereas others eat only one or a few things (stenophagy). One striking pattern of lepidosaurian feeding evolution is that dietary specialization is often not accompanied by phenotypic specialization in the trophic (feeding) apparatus (Greene, 1982). Phenotypic specialization for stenophagy is infrequent among lepidosaurs, in contrast to mammals and birds (see later and Chapters 12 and 13). For a given specialized diet, such as ants, some taxa are highly derived and phenotypically specialized [e.g., Phrynosoma (Iguanidae) and Moloch (Agamidae)], whereas others remain generalized in form [e.g., Liolaemus monticola (Iguanidae)]. The reasons why some organisms become trophically specialized while others do not remains a fundamental question in evolutionary morphology (e.g., Greene, 1982; Lauder, 1983a,b). The question of dietary specialization is pursued further in Section VII. Iguania and Scleroglossa differ little in the breadth of diets they encompass, with one exception—no iguanian regularly eats prey items that are very large relative to its body size, whereas within Scleroglossa, several taxa are specialized in this way. The evolution of macrostomatan snakes, in particular, is characterized by adaptations that enhance their ability to subdue and ingest prey, which, in some cases, are larger than the snake itself (Greene, 1997; Chapter 9). Komodo dragons (Varanus komodoensis) kill large mammals and reduce them to sizable chunks, which are bolted with minimal processing (Auffenberg, 1981; see Section VI, C). A few other lepidosaurs regularly consume vertebrates (e.g., Sphenodon punctatus, Walls, 1981; Gambelia wislizenii, Tanner and Krogh, 1974; ToUestrup, 1979; Parker and Pianka, 1976; some Chamaeleo, Loveridge, 1953; Bourgat, 1970; Burrage, 1973; Eremiascincusjam.es and Losos, 1991; Heloderma, Bogert and Martin del Campo, 1956; Pregill et al, 1986; Lialis, Patchell and Shine, 1986; most Varanus, Shine, 1986; Losos and Greene, 1988; James et al, 1992; see also Greene, 1982), but for most of these species vertebrate prey are rare or occasional dietary items and few evince morphological specialization of the feeding apparatus for carnivory (the pygopodid, Lialis, specializes on skinks and may be the most trophically specialized). Otherwise, the vast majority of lepidosaurs feed frequently on relatively small, invertebrate prey. This is true even for some of the largest lepidosaurs, the varanid lizards (Losos and Greene, 1988), and it may be the single generalization that can be made about lepidosaurian diets. In a highly influential paper, Pough (1973) suggested a relationship between lizard size and diet such that small species (< 100 g) are nearly all carnivorous/insectivorous and large species (> 300 g)

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are nearly all herbivorous, a pattern he attributed to the greater relative mass-specific energy requirements of smaller lizards. Pough suggested that the capture of small, active prey items is energetically untenable for large lizards and found that those groups that do maintain carnivory at a large body size have physiological, morphological, or behavioral adaptations which apparently circumvent this putative energetic constraint (see also Wilson and Lee, 1974). Pough suggested that juveniles of large species should show a dietary shift from carnivory/insectivory to herbivory as they achieve larger body sizes and found some support in the literature for this contention. Pough's (1973) conclusions can no longer be considered valid, however, except in broadest outline. Several factors mitigate against accepting the generality of his principal findings: (1) The study was done before phylogenetic awareness had infiltrated comparative ecological studies, hence it failed to take into account the effects of phylogeny on the observed correlation; in fact, many large, herbivorous species are closely related, hence represent single origins of herbivory and large body size, and the phylogenetic retention of this correlation within a clade, rather than multiple, independently evolved correlations. Thus, the apparent evolutionary "connection" between large size and herbivory was inflated falsely. (2) Many exceptions to the body size-diet correlation have since been noted. In particular, many very small species have been found to be purely, or mostly, herbivorous (e.g., Greene, 1982; Iverson, 1982; Schoener et al, 1982; Jaksic and Schwenk, 1983; Whitaker, 1968, 1987; Rocha, 1989, 1998; Schall and Ressel, 1991; Troyer, 1991; PerezMellado and Corti, 1993,1997; Vitt and Morato de Carvalho, 1995; Vitt and de la Torre, 1996; Vitt et al, 1997a). (3) Some putative ontogenetic dietary shifts from insectivory to herbivory have not been supported. For example, Swanson's (1950) report of diet switching in Iguana iguana, cited by Pough (1973), was speculative rather than empirical, and subsequent studies have found that even juvenile iguanas are fully herbivorous (Troyer, 1984). (4) Pough (1973) believed that lizard herbivores mostly lacked phenotypic specializations that would make them more efficient at digesting plant matter, but subsequent work has documented several adaptations for herbivory, notably hindgut fermentation systems for cellulose digestion (e.g., Iverson, 1982; McBee and McBee, 1982; Troyer, 1991; Bjorndal, 1997). In conclusion, although many large lizards are herbivorous, many are not. Most small lizards are insectivorous, but many are herbivorous. Certainly the number of small species for which plant matter constitutes a substantial portion of the diet is legion and grossly underestimated in the literature historically.

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It has been generally assumed that the ancestral lepidosaurian diet was insectivory (e.g., Carroll, 1977, 1988a); however, this conclusion was based on the presumption of a correlation between tooth form and diet (e.g., Hotton, 1955; Montanucci, 1968), body size and diet (see earlier discussion), and fossil evidence showing that the earliest lepidosaurs were small with generalized teeth. However, the correlation between diet and tooth form is now known to be tenuous at best (see Section IV, B) and, as noted, the correlation between diet and body size is unsupported, hence one cannot assume that small, fossil lepidosaurs with generalized dentitions were insectivorous (Greene, 1982). Nonetheless, it remains true that by sheer weight of species number, the "typical" lepidosaur is a small, generalized insectivore that feeds opportunistically. Only comparative, phylogenetic analyses of diet in specific lepidosaurian clades will provide reasonable inferences about ancestral diets. Such analyses have yet to be done and their absence represents a large gap in our knowledge of feeding evolution in lepidosaurs. 1. Sphenodon Diet in tuatara has been studied by Walls (1981). Sphenodon is almost entirely insectivorous or carnivorous, but fecal pellet analysis showed more than an incidental quantity of plant matter (seeds) in a small percentage (approximately 10%) of individuals (Walls, 1981; I. C. Southey, in Whitaker, 1987). One fossil species shows convincing morphological evidence for herbivory, but virtually all other known fossil sphenodontids are presumed to have been insectivorous or carnivorous (Throckmorton et al, 1981). Tuatara forage at night and feed opportunistically on whatever they encounter and can capture, with certain noxious and fast-moving prey absent from their diet. Unlike most lizards, however, a powerful biting apparatus and specialized dentition (e.g., Robinson, 1967, 1976; Rosenberg et ah, 1982; see later) permit them to process relatively large prey items, including whole petrel (sea bird) eggs and chicks. Large chicks are killed by biting and are reduced to manageable pieces by the teeth. Although eggs and chicks are seasonally very important components of the diet, large beetles and other invertebrates are consistently the most important prey types. Tuatara showed some preference for forest, as opposed to open area, prey species. 2.

Amphisbaenians

Natural diets of amphisbaenians are poorly known. Most data are available for the genera Amphisbaena (Riley et al, 1986; ColH and Zamboni, 1999; White et al, 1992; Cabrera and Merlini, 1990; Cruz Neto and Abe,

1993; Cusumano and Powell, 1991) and Blanus (Lopez et ah, 1991; Gil et ah, 1993), with some information on Cercolophia (Cruz Neto and Abe, 1993), Monopeltis and Dalophia (Broadley et al, 1976). An association between ants and amphisbaenians has long been assumed but rarely proven. However, such an ecological relationship has been established for Amphisbaena alba in Trinidad, with some evidence suggesting that the pattern holds for mainland South America as well (Riley et al, 1986). These workers found that A. alba follows the pheromone-marked foraging trails of leaf-cutter ants {Atta) across the surface to the nest where the amphisbaenian occupies the refuse chamber. Within this chamber it feeds primarily on arthropods, especially beetle larvae, without attracting the attention of resident soldier ants. Surprisingly, relatively few ants were found in the diet and many of these were individuals of a raiding species. The most important dietary items were beetle larvae and other insects that are, themselves, inhabitants of ant nests. Colli and Zamboni (1999)'s study of Brazilian A. alba did not determine whether the amphisbaenian occupied ant nests, but it did reveal a large number of ants in stomachs of preserved specimens. Termites were the most numerous item, however, but unidentified insect larvae were the most important items by volume. This study, therefore, agrees with Riley et al. (1986) in identifying insect larvae as the most important food type, but differs in finding large numbers of termites and ants, suggesting that the Brazilian population exhibits more opportunistic foraging. Other Amphisbaena species were also found to consume large numbers of termites (Cabrera and Merlini, 1990; White et al, 1992; Cruz Neto and Abe, 1993). Cruz Neto and Abe (1993) collected many of their specimens next to fallen trees where termite nests were abundant. These studies also found that ants and insect larvae were important food items. Termites were also the most frequent prey type for the African genera Monopeltis and Dalophia, although both taxa also consumed significant numbers of ants and beetle larvae as well (Broadley et al, 1976). Blanus cinereus was found to consume a variety of soil invertebrates that tend to be most dense and diverse under rocks (Lopez et al, 1991; Gil et al, 1993). However, large insect larvae (particularly dipterans) are preferentially selected, presumably because of their higher caloric payload. Ants are also frequently taken, but not in proportion to their environmental abundance. Riley et al (1986) reviewed the meager amphisbaenian dietary literature at that time and concluded that most amphisbaenians feed opportunistically on fossorial arthropods encountered within their own fixed tunnel systems, although some species, including

8. Feeding in Lepidosaurs A. alba, may also occupy ant nests. Dietary data published since seems to confirm this view, although it increasingly appears that termites and, to a lesser extent, ants are important prey types. The predominance of termites in amphisbaenian diets may reflect dietary specialization or it may result from chance discovery of clumped prey items in shared habitat (Cabrera and Merlini, 1990). The latter interpretation is supported by Colli and Zamboni's (1999) finding that a few individuals ate very large numbers of termites, but most individuals had consumed few or none. White et at. (1992) noted a single unidentified vertebrate in one specimen of A. gonavensis, and Colli and Zamboni (1999) found evidence for only three vertebrate prey items (a small lizard limb, a small anomalepid snake, and some hair) in 116 specimens of A, alba. These findings do not support the hypothesis that the imposing biting apparatus of amphisbaenians is an adaptation for eating large prey (Cans, 1966,1969a, 1974; see Section VI). 3. Other Squamates Although snake diets are diverse, there are no herbivorous species (Pough, 1983; Greene, 1997), which is also true for all other limbless tetrapods (Cans, 1975). Pough (1983) speculated that this pattern might obtain from a constraint in gut size relative to body mass in an elongate body. It should be kept in mind, as well, that snakes evolved from insectivorous/carnivorous lizards and went on to evolve specialized, jaw-based prehension mechanisms adapted for capturing animal prey. Thus, snakes were committed early in their ancestry to a specialized, highly integrated feeding apparatus that might have limited their phenotypic (and therefore, dietary) options—the loss of a hyolingual transport mechanism (see later), alone, may prevent the effective transport and processing of most plant foods. In any case, under the rubric of "animal prey," snake diets comprise an astonishing variety of food types, including foamy nests of frog eggs, worms, slugs, ant eggs and larvae, bird eggs, fish, frogs, lizards, other snakes, antelope, and even the occasional human (see Greene, 1997; Chapter 9). Although "advanced" (macrostomatan) snakes are clearly specialized for the consumption of extremely large prey (in some cases >100% body mass), basal scolecophidian snakes eat many tiny prey (ant eggs and larvae, and termites), thus there are few generalizations one can make about snake diet. Nevertheless, diet and feeding habits appear to be central to understanding the origin of snakes and patterns of diversification within the group (Greene, 1983, 1997; Savitzky, 1983; see Chapter 9).

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The diversity of lizard diets has already been treated in the introduction to this section. Little need be added other than to reiterate a few important points. Although the "typical" lizard, in the sense of species number, is a small, opportunistic insectivore, numerous exceptions exist. Some taxa are dietary specialists, including herbivorous (plant-eating), myrmecophagous (ant- and termite-eating), carnivorous (vertebrateeating), and oophagous (egg-eating) types. Within each of these dietary categories further specialization is often represented. For example, some herbivores eat primarily fruit (frugivory; e.g., Varanus olivaceous, Auffenburg, 1988), others leaves (folivory; e.g., I. iguana, Troyer, 1984; Rand et al, 1990), nectar (nectivory; e.g., some Hoplodactylus, Whitaker, 1987; Podarcis lilfordi, Perez-Mellado and Casas, 1997), or seeds [e.g., Angolosaurus skoogii and Meroles (Aporosaura) anchietae, Greene, 1982], and one species eats marine algae (Amblyrhynchus cristatus. Carpenter 1966). Importantly, however, diets often vary temporally, ontogenetically, or individually (e.g., Burrage, 1973; Jackson and Telford, 1975; Capel-Williams and Pratten, 1978; Vitt et al, 1981; Bauer et al, 1989; Dessem, 1985; Pianka, 1986; Shine, 1986; James, 1991; Perry and Brandeis, 1992; PerezMellado and Corti, 1993; Brown and Perez-Mellado, 1994; Rocha, 1996, 1998; Perez-Mellado and Casas, 1997; Whiting and Greeff, 1997; Znari and Nagy, 1997; Duffield and Bull, 1998). Thus, stenophagy may be seasonal or opportunistic. In some cases, of course, a narrow diet is maintained throughout life. It is therefore important to recognize that diet analyses based on samples limited geographically or temporally do not necessarily reveal the actual (complete) diet of a population or species. Undiscovered temporal shifts in diet driven by seasonality of food resources may explain why some putative dietary specialists fail to become phenotypically specialized. In other words, some species regarded as specialists based on inadequate dietary sampling might actually manifest serial, or opportunistic, stenophagy so that they remain functional generalists. Finally, there is the possibility that in some herbivorous species, stenophagy may be entrained in an individual, i.e., it is a phenotypically plastic trait. Although I know of no equivalent example in lizards, it has been shown that, as a species, green sea turtles (the only herbivorous marine turtle) are capable of eating both marine algae and sea grasses, but individuals eat only one or the other, even when both are available (Bjorndal, 1980, 1985). According to Bjorndal this pattern probably reflects individual specialization of the hindgut fermentation (cellulose-digesting) system for one or the other food type. Once established, a particular hindgut microbial fauna may be suitable for digesting only one type of food. Alternatively, variation in

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food preferences among individuals within a species could be genetically determined, as has been shown for some garter snakes (e.g., Arnold, 1981). Although as a general rule dietary types characterize larger taxonomic groups, closely related species occasionally differ radically in diet. For example, virtually all monitor lizards (Varanus) feed exclusively on other animals (Losos and Greene, 1988), but, as noted earlier, V. olivaceous is one of the most highly frugivorous lizards in the world (Auffenberg, 1988)! Nearly all lizards of the genus Cnemidophorus (Teiidae) are insectivorous and large species are sometimes carnivorous, but a few species are primarily herbivorous (e.g., C. aruhensis, Schall and Ressel, 1991; C. lemniscatus, Vitt et ah, 1997a). Likewise, the vast majority of tropidurine iguanids, genus Liolaemus, are insectivores, but a few species (e.g., L. magellanicus, Jacksic and Schwenk, 1983; L. lutzae, Rocha, 1989; L. fitzingeri; Troyer, 1991) are mostly, or entirely, herbivorous and others are known to include fruits in their diets (e.g., L. pictus; Willson et al, 1996). Often the dietary shift in close relatives is not attended by apparent phenotypic specializations, but such differences can be cryptic. For example, although there are no obvious, diet-related differences in the cranial feeding apparatus of the Liolaemus species, Troyer (1991) showed that L. fitzingeri has an expanded large intestine as compared to its insectivorous relatives, suggesting the presence of a hindgut fermentation system for cellulose digestion (Troyer, 1991; Bjomdal, 1997).

B. Foraging Ecology The literature on foraging ecology of lepidosaurs is an area of ambiguity and contention that I am loathe to enter, but its obvious relevance to feeding biology requires at least a cursory treatment. As for other tetrapods, lepidosaurs are generally regarded as either "ambush" ("sit-and-wait") or "active" ("wide") foragers (e.g., Pianka, 1966, 1986; Schoener, 1971; Regal, 1978, 1983; Huey and Pianka, 1981). In their extreme expressions these foraging modes are qualitatively distinct: ambush foragers remain more or less motionless in position and wait for active prey to come within reach of a strike, whereas active foragers move more or less widely through their environments in search of prey that may be stationary, clumped, or cryptic. Thus diets tend to differ between ambush and active foragers living in the same habitat (e.g., Huey and Pianka, 1981). In general, active foragers have higher field metabolic rates and higher rates of energy expenditure than ambush foragers, but their food (energy) intake rates are significantly greater (Huey and Pianka, 1981;

Anderson and Karasov, 1981; Nagy et al, 1984; Waldschmidt et al, 1987). However, active foragers suffer from a higher risk of predation and lower relative clutch volumes (e.g., Huey and Pianka, 1981). Active foragers tend to rely more heavily on vomeronasal chemoreception than ambush foragers and are putatively capable of distinguishing prey from nonprey using chemosensory cues (Cooper, 1994, 1995a). They are also more proficient at following pheromonal trails than ambushers and consequently are often equipped with forked tongues (Schwenk, 1994e; see later). This dichotomy in foraging modes, as for most biological dichotomies, is oversimplified. The reality is far more complex and the biological correlates presented do not universally apply (see Perry, 1999). Many workers have suggested that ambush and active foraging modes represent extremes of a continuum, or have introduced additional qualitatively distinct or intermediate foraging modes (e.g.. Regal, 1978,1983; Magnusson et al, 1985; Pietruszka, 1986; Waldschmidt et al, 1987; Perry et al, 1990; Cooper, 1994, 1995a; Werner et al, 1997; Perry, 1999). There is little agreement on how to define terms precisely and what the relevant criteria for such definitions are. This disagreement has led to a lack of uniformity in the attribution of foraging modes among studies and among taxa. The latter case may be especially problematic; a study of a closely related species might score one as an ambush forager on a relative, dichotomous scale, but in an absolute (quantitative) sense, the same species would be considered an active forager in the context of a broader phylogenetic sample [see discussion of Perry's (1999) study later]. Further, some studies have identified significant among-individual variation, as well as ontogenetic, diurnal, and seasonal variation in foraging mode within a species (e.g., Taylor, 1986; Pietruszka, 1986; Perry et al, 1990; Duffield and Bull, 1998). Some taxa simply defy categorization. For example, nearly all iguanid lizards studied conform to our expectations for ambush foragers, but most horned lizards (Phrynosoma) do not (e.g., Huey and Pianka, 1981). This seems to be related to dietary specialization on ants, which are a clumped and unpredictable prey of the sort usually preyed on by active foragers. Thus horned lizards move widely through their environments seeking locations with active ants. Once found, however, they station themselves in place, behaving like typical ambushers. Nonetheless, they restrict themselves to short feeding bouts so that nests remain active (high predation rates cause ant nests to become inactive for days) and to avoid incurring the wrath of soldier ants (Whitford and Bryant, 1979; Rissing, 1981; Shaffer and Whitford, 1981), hence they soon move on again in search of other locations, behaving once again

8. Feeding in Lepidosaurs like an active forager. This pattern may also apply to Phrynosoma's agamid counterpart, Moloch (Pianka and Pianka, 1970). Likewise, herbivorous iguanids and agamids appear to be qualitatively distinct from their typical ambush foraging relatives, for which Cooper (1994) erected a third, diet-based foraging mode. Scincids, as a rule, do not conform to expectation (Regal, 1983), although they are embedded in a typically wide-foraging, clade. Regal (1978, 1983) suggested an intermediate category of "cruising'' to indicate the relatively slow-moving, stop-and-go nature of skink foraging. In any case, scincids are so incredibly diverse that they are likely to vary significantly in foraging mode (e.g., Greer, 1989). Finally, I note that most snakes do not conform to simple categorization. Many caenophidian snakes, such as vipers, would appear to be archetypal ambush foragers because they sit nearly motionless beside prey trails for hours, days, or even weeks until a prey animal comes within striking distance (e.g., Greene, 1997). Nonetheless, such a snake initially moves extensively through its habitat, seeking chemical-laden prey trails and appropriate ambush sites. Similarly, scolecophidian snakes move widely through their environments until they locate ant trails, which they follow to the nest wherein they feed on eggs and larvae (e.g., Gehlbach et al, 1971; Webb and Shine, 1992). For these reasons (among others), snakes exhibit extreme chemosensory prowess, deeply forked tongues, and unsurpassed trailing abilities (Halpern, 1992; Schwenk, 1994e), traits typically associated with wide foragers (see earlier discussion). These examples hint at the complexity of foraging mode among lepidosaurs and explain why many taxa exhibit characteristics of both typical ambush and active foragers. Finally, a study using a broad taxonomic base and comparative (phylogenetically controlled) methods rejected the notion of bimodality in foraging mode among lizards and supported a foraging continuum (Perry, 1999). However, Perry's (1999) data reveal that the continuum of foraging modes is not uniformly distributed among clades—iguanians (only iguanids were included) and gekkotans lie overwhelmingly toward the "ambush" end of the foraging spectrum whereas the remaining taxa (Autarchoglossa) span the entire range. The continuum emerges from the summation of these two patterns. As such, there are no iguanians or gekkotans at the high (active) end of the foraging spectrum and there are relatively few autarchoglossans at the low (ambush) end. Thus I would interpret Perry's data more generously to indicate a continuum of foraging modes that are not randomly distributed among clades, with ambush strategies probably primitive for squamates. Autarchoglossans apparently have evolved features that permit, but do not require, active foraging modes.

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In any case, there remain exceptions to all of these generalizations, as noted. Tuatara are characterized as "passive" (ambush) foragers (Walls, 1981); however. Walls implied that individuals move around seeking appropriate prey. For example, because eggs and hatchlings of nesting shorebirds form an important part of the diet (see earlier discussion), tuatara must search actively through the birds' underground nest burrows. Among lizards, most iguanians and gekkotans are ambush foragers (Cooper, 1995b; Perry, 1999), as noted, but there are exceptions. The case of herbivores and the myrmecophagous genus Phrynosotna were discussed earlier. In addition, Pietruszka (1986) found that the carnivorous iguanid Gambelia exhibited rates of foraging movement equivalent to active foraging Cnemidophorus (Teiidae) and Perry (1999) identified several other actively foraging iguanid species ("phrynosomatids" or sceloporines). Although most autarchoglossan species are active foragers, there are numerous exceptions, particularly among cordylids (Cooper, 1994) and lacertids (Huey and Pianka, 1981; Nagy et al, 1984; Perry et al, 1990). Scincids are certainly unusual active foragers, if they are active foragers at all. The unusual case of snakes was also discussed earlier; other anguimorphans, such as Komodo dragons (Varanus komodoensis), often exhibit a similar pattern of searching widely for ambush sites (e.g., Auffenberg, 1981). Despite these exceptions and cautionary statements, some general remarks can be proffered. There is a strong phylogenetic component to foraging mode so that large taxa (e.g., families) tend to be relatively uniform in this regard (e.g., Huey and Pianka, 1981; Cooper, 1994, 1995a; Perry, 1999). Tuatara, and iguanian and gekkotan squamates, are primarily ambush foragers, but within this mode a range of variation exists so that some species approach an active foraging style. It is noteworthy that three of the exceptional iguanian taxa cited earlier are all dietary specialists: herbivores, anteating Phrynosotna, and lizard-eating Gambelia. Chemosensory prey discrimination also putatively evolves in conjunction with foraging mode (Cooper, 1994,1995a). These observations suggest, unsurprisingly, that diet and foraging mode are coevolved, integrated components of a lepidosaur's phenotype, although foraging mode is usually presented as a determinant of diet (e.g., Huey and Pianka, 1981). Autarchoglossans are primarily active foragers, but again, many exceptions are known. What remains most unclear is whether a given scleroglossan species characterized as an ambush forager would be comparable, both qualitatively and quantitatively, to an iguanian ambush forager. Perry's (1999) study is the first to approach this issue globally.

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Kurt Schwenk C. Sensory Basis of Food Location and Identification

Lepidosaurs have at their disposal a full arsenal of sensory systems to employ in the detection, identification, and capture of food. These include, in most cases, well-developed systems of vision, audition, touch, and chemoreception. Some snakes have specialized systems for thermo (infrared) reception as well. Among these sensory modes, vision and chemoreception are denionstrably the most important for feeding and foraging in most lepidosaurs. There is a long-standing dogma in the herpetological literature suggesting that "ascalabotans" [Camp's (1923) paraphyletic group comprising Iguania and Gekkota] are primarily visual and that autarchoglossans are primarily chemosensory Schwenk (1993a,b, 1994a) reviewed this issue in the context of squamate phylogeny and the merits of cladistic vs paraphyletic classifications and showed that the dichotomy is unsupported, even if updated to contrast the strictly monophyletic taxa Iguania and Scleroglossa. Like the dichotomy in foraging mode, however, this simple view does have merit in broad outline. Certainly it is heuristically useful as a starting point from which one might elaborate the exceptions. 1. Vision Lepidosaurian eye structure and function have been comprehensively reviewed by Walls (1942), Underwood (1970), and Peterson (1992). Reperant et ah (1992) treated the central projections of the visual system. Lepidosaurs, with the exception of most snakes, are unique in possessing a retina with a single layer of photoreceptor cells. All other tetrapods have what is known as a "duplex" retina with two layers of sensory cells. The functional significance of this difference is unknown. In any case, most lizards have an otherwise typical tetrapod eye with the exception that the retina apparently comprises only cones and no true rods. However, the notion of "rods" and "cones" is based on mammalian models and it is not clearly applicable to most reptiles. Some nocturnal lepidosaurs have rodlike receptor cells that have been interpreted alternatively as true rods or as modified cones. In particular, some geckos and snakes have very rod-like receptors (Underwood, 1970; Peterson, 1990), but the homology of these photoreceptors to other tetrapod rods is unlikely and has not been critically evaluated. In general, a high density of cones is taken to indicate high visual acuity (sharpness of vision) and the presence of color vision (Walls, 1942). Although it is generally assumed that diurnal lizards possess color vision, this is not certain. The neurophysiology of color vision is complex and poorly un-

derstood (Goldsmith, 1990; Fleishman et a/., 1998). It depends minimally on the varying spectral sensitivities of different pigments within classes of photoreceptor cells. Pigmented oil droplets within the cones may contribute to color vision by acting as filters (Peterson, 1992). Consistent with this observation is that the cones of nocturnal lizards (presumably lacking the need for color vision) usually lack oil droplets or the droplets are unpigmented (Underwood, 1970). Limited experimental evidence suggests that oil droplets do contribute to color vision in an agamid lizard (Peterson, 1992). In any case, chromatic information might also be encoded in the pattern of depolarization and hyperpolarization of the receptors or their connecting interneurons (e.g., Solessio and Engbretson, 1993). Only recently have the techniques become available to measure directly the absorption spectra of individual photoreceptors (e.g., Fleishman et al., 1993; Solessio and Engbretson, 1993; EUingson et al, 1995). These studies show that at least some diurnal lizards possess the anatomical basis for wavelength discrimination, although direct proof that they perceive colors is still lacking. Behavioral evidence does indicate that most diurnal lizards employ color vision, but most of this evidence is anecdotal or without convincing controls. Importantly, Fleishman et al. (1998) pointed out that colors vary not only in frequency, but in brightness (i.e., perceived intensity) contrast with the background and such differences confound the assumption of color discrimination in most experimental designs. Nonetheless, the evidence is suggestive. Numerous studies demonstrate, for example, that conspecific color cues are used by lizards in social contexts to assess sex, age, and breeding status (reviewed by Cooper and Greenberg, 1992; see also Watkins, 1997). However, the use of color cues in feeding is less well supported. Several studies show preferences of some lizards for foods of certain colors, especially yellow, orange, and red, which they differentiate from other colors (e.g., Benes, 1969; Rand et al, 1975; McGovern et al, 1984; Cans et al, 1985; personal observation). Two iguanian taxa, Anolis (Iguanidae) and Chamaeleonidae, show extreme adaptations for vision and visually directed predation that are worth exploring as exemplars. Anoles are extraordinary in their possession of a second fovea in the retina (Underwood, 1970; Fleishman, 1992). They are the only vertebrates other than some birds to have dual fovea (Underwood, 1970). The fovea is a specialized zone of the retina containing unusually high photoreceptor (usually cone) density (e.g., Makaretz and Levine, 1980; Fite and Lister, 1981) and other attributes that enhance visual acuity When an object of interest is spotted, the visual axis is usually

8. Feeding in Lepidosaurs adjusted so that it falls on the fovea. The typical, central fovea of anoles provides a zone of acuity for wide-field, monocular vision, whereas the second (novel) temporal fovea comes into play when the eyes fixate binocularly on a prey item directly in front of the lizard (Fite and Lister, 1981). Use of the temporal fovea in anoles is very similar to that in raptors (Sillman, 1973; Fite and Lister, 1981). Other nonavian tetrapods with welldeveloped binocular vision, including some squamates (e.g., the Asian vine snake, Ahaetulla) and humans, have a single fovea in the temporal position (Walls, 1942). The peripheral retina of anoles is extremely sensitive to certain kinds of movement so that even minute prey movements elicit monocular fixation with the fovea, potentially followed by binocular fixation and a predation attempt (Fleishman, 1986, 1992). A prey item that lies within a threshold distance will be approached and attacked, and this distance is modulated depending on prey size and abundance (Shafir and Roughgarden, 1998). The visibility of a prey item to an anole (and presumable other lepidosaurs) depends largely on the extent to which its movement differs from random background motion (Fleishman, 1986, 1988,1992; Persons et al, 1999). Anoles have also been shown to have visual sensitivity to ultraviolet light, which is used by some species in the detection of conspecific dewlap displays (Fleishman et ah, 1993). It is unknown whether ultraviolet cues play a role in predatory behavior, however. Chamaeleonids also exhibit unusual eyes and specialized, visually mediated predatory behavior. Upper and lower eyelids are fused and the eyeball is positioned extraorbitally so that the eyes are "turreted,'' each capable of independent movement and 360° of rotation. Although chameleons are certainly extreme in this regard, it is seldom appreciated that nearly all lizards, as well as other nonmammalian tetrapods, are capable of independent eye movement (Walls, 1942, 1961; Kirmse, 1988). Furthermore, some lizard species, particularly anoline iguanids and some agamines, have partial turreting of the eyes (e.g., Abel, 1952; personal observation). In Chamaeleolis, for example, an anoline form convergent with chameleons in many respects, upper and lower eyelids are fused and turreting is pronounced so that independent eye movement is clearly evident (personal observation). Chameleons scan their environments using saccadic (rapid, stop-go) movements of each eye independently. Only one eye at a time is in focus, however, alternating at approximately 1-sec intervals (Ott et al, 1998). Thus, a wide area of the environment can be scanned monocularly for prey, but apparently only one eye's image is processed at a time. When a prey item is spotted, the

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head is turned and the eyes rotate forward to fixate it binocularly (Ott et al., 1998). Prey movement is then tracked with head, rather than eye movement (Flanders, 1985). In preparation for prey capture, the distance to the prey item is visually determined. Chameleons depend entirely on accommodation (focusing) cues to do this and thus differ from most mammals, and probably other tetrapods, which principally employ binocularity (stereopsis) for depth perception (Harkness, 1977; CoUett and Harkness, 1982; Ott and Schaeffel, 1995). The speed of accommodation is among the fastest of any vertebrate measured (Ott and Schaeffel, 1995; Ott et al, 1998). This nearly instantaneous and highly accurate assessment of prey distance is used to modulate precisely tongue projection distance for lingual prey capture (Harkness, 1977; Ott et ah, 1998; see Section VI, A). Another unique feature of the chameleon eye is that the lens is negatively powered; in conjunction with corneal refraction, the visual system is telephoto, i.e., it magnifies the image on the retina (Ott and Schaeffel, 1995; Land, 1995). Land (1995) suggested that the peculiar lens arrangement creates monocular disparity so that objects at different distances in the visual field move across the retina at different speeds as the eye is rotated. This might help chameleons to distinguish prey at varying depths within the complexly threedimensional, arboreal environment they inhabit. It is noteworthy that both anoles and chameleons are arboreal species with extremely reduced vomeronasal chemosensory function (Haas, 1937, 1947; Armstrong et al, 1953; Gabe and Saint Girons, 1976). Although arboreality has often been associated with visual predation and reduced chemoreception, other arboreal species, such as green iguanas and most geckos, are, in fact, highly chemosensory, thus there is no necessary, causal relationship between the two traits (see Schwenk, 1993a). Nonetheless, some shared component of anoline and chamaeleonid environments, or similarities in predatory behavior, might have driven the acquisition of analogous adaptations. Alternatively, ancestral reduction of chemoreception, for whatever reason, might strongly predispose any lepidosaurian lineage toward compensatory enhancement of its visual system, no matter what the environment. 2.

Chemoreception

Most squamates rely heavily on chemosensory, as well as visual, cues during foraging and feeding. There are at least three separate chemosensory systems available to most species: gustation, nasal olfaction, and the vomeronasal system (for reviews see Burghardt, 1970,1980; Halpern, 1992; Schwenk, 1995b; Font, 1996).

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A possible fourth, trigeminal chemosensory system remains mostly unexplored in lepidosaurs (Tucker, 1971). Gustation is mediated by taste buds, which, in reptiles, are restricted to the oral cavity and pharynx, and are innervated by cranial nerve IX, the glossopharyngeal (e.g., Willard, 1915). Tuatara are well supplied with lingual taste buds and are unique among lepidosaurs in having specialized "gustatory papillae" (Schwenk, 1986). Although snakes lack lingual taste buds, many species have them within the oral mucosa, particularly along the tongue sheath (Schwenk, 1985; Young et ah, manuscript in preparation). Taste buds reach extremely high densities on the foretongues of some lizards, particularly iguanians (Schwenk, 1985; Herrel et ah, 1998c). They are stimulated by chemically diverse substances introduced to the surface of the tongue or into the mouth (see Schwenk, 1985), but the significance of taste in the biology of lepidosaurs remains almost wholly unexplored (Burghardt, 1970; Schwenk, 1985; see later). Olfaction is mediated by the nasal epithelium covering the nasal conchae and other surfaces within the nasal cavities. Volatilized chemicals inspired through the external nares stimulate the olfactory sensory cells, which project directly to the olfactory bulb of the brain. Air moves through the nasal cavities and exits posteroventrally through the palate via the internal nares (choanae) and into the glottis to the lungs. Inspiration is usually driven by typical rib-based ventilation of the lungs, but in some lizards a buccal or gular pumping mechanism drives airflow through the nasal cavities with or without lung ventilation (e.g., Schwenk, 1993a, personal observation; Dial and Schwenk, 1996; Owerkowicz et al, 1999). Hence, some lizards may employ an olfactory behavior analogous to mammalian "sniffing" (Dial and Schwenk, 1996). The vomeronasal system is served by paired vomeronasal (or Jacobson's) organs (VNO) that lie above the anterior palate, encapsulated by bone and cartilage within the nasal cavities. Each VNO has a sensory epithelium, the neurons of which project to the accessory olfactory bulb (at the base of the olfactory bulb in squamates). In Sphenodon, the VNO are tubular chambers open to the nasal cavities, but not directly to the mouth (Hoppe, 1934; Parsons, 1970). VNO stimulation is presumably by means of nasal inhalation, but virtually nothing is known of vomeronasal function in tuatara. In squamates, the VNO are sequestered from the nasal cavity and open directly to the mouth via two tiny openings in the palate, the vomeronasal fenestrae (Parsons, 1970). They are stimulated by chemicals brought into the oral cavity by the tongue and then drawn through the vomeronasal fenestrae (Halpern, 1992). Environmental chemicals are gathered by the tongue

during tongue flicking, a behavior characteristic of virtually all squamates. Tongue flicks vary from simple downward protrusion toward the substrate to rapid, multiple oscillations of the tongue in the air (e.g., Gove, 1970; Bels et al, 1994). In general it is presumed that VNO function is distinguished from nasal olfaction by its sensitivity to relatively nonvolatile, heavy molecular weight molecules (e.g.. Tucker, 1971); however, aerial tongue flicks can also saniple volatiles for VNO scrutiny (e.g., Halpern et al., 1997), thus confounding the biological roles of the two senses (Schwenk, 1995b). Similarly, the presence of taste buds on the tongue tip in most squamates makes it possible that tongue flicks directed to the substrate might be gustatory rather than serving to collect nonvolatile chemicals for the VNO, particularly in iguanians, which possess high taste bud densities on the tongue tip (Schwenk, 1985; Herrel et al, 1998c). However, strong circumstantial evidence supports the supposition that all tongue flicks, including substrate touches, mediate vomeronasal stimulation rather than gustation (Schwenk, 1993a; Dial and Schwenk, 1996). Gustation is most likely to be relevant for the assessment of palatability after a food item is held within the mouth (Schwenk, 1986,1995b). The manner in which the chemical senses are functionally and behaviorally interrelated remains poorly understood. Schwenk (1995b) proposed a heuristic model of chemically mediated predation in squamates consistent with current data: (1) Nasal olfaction initially senses a volatile food odor, which triggers tongueflicking behavior (Cowles and Phelan, 1958; Halpern et al, 1997). (2) Tongue flicking stimulates the vomeronasal system, which provides additional information about the odor or samples a different volatile component of the odor. (3) Exploratory and trailing behavior is initiated to localize the odor source using both aerial and substrate-directed tongue flicks; species with forked tongues can employ tropotactic mechanisms, but species with unforked tongues must rely on klinotactic mechanisms (see Schwenk, 1994e). (4) Tongue touches to a prey trail or the food item itself sample nonvolatile chemical components of the odor source for additional information. (5) Once the source is located, the chemical information gleaned so far may be sufficient to trigger ingestion, but often only in conjunction with appropriate visual cues (see later). (6) Following ingestion of the food item, taste buds provide gustatory assessment of palatability. Distasteful food is rejected at this point and a combination of visual and chemosensory cues associated with the prey item mediate learned avoidance in future encounters. This scenario clearly does not apply universally to all squamates, nor to any individual squamate during every feeding event. Some taxa have reduced or enhanced particular chemosensory modes, or empha-

8. Feeding in Lepidosaurs size nonchemosensory cues. For example, geckos and some other groups may substitute nasal olfaction for vomeronasal function at any point in this sequence (Schwenk, 1993a; Dial and Schwenk, 1996). Chameleons and anolines have reduced both nasal olfactory and vomeronasal senses and are heavily dependent on vision during all stages of feeding (see earlier discussion). Locomotion and exploratory behavior are typically attended by tongue flicking in most squamates, hence initial olfactory stimulation of the vomeronasal system may be unnecessary. Ambush predators have no need to trail and localize food sources, but rather assess the quality of prey items as they approach, both visually and by tongue flicking. It is well documented that many squamates, particularly scleroglossans, use chemosensory cues during foraging, primarily to locate hidden or cryptic prey. Burghardt (1970) and Halpern (1992) have reviewed much of this evidence. Bogert and Martin del Campo (1956), for example, found that Gila monsters (Varanoidea, Heloderma) could follow the scent trail of an egg dragged across the substrate and find where it was buried. In general, active foragers search for cryptic prey in leaf litter, under covering objects, or buried within the substrate by constantly probing with the snout and tongue flicking (e.g.. Fitch, 1935,1954,1958; Taylor, 1986; Vitt and Cooper, 1986; Vitt, 1991; Vitt and Blackburn, 1991). Most snakes are well known to follow scent trails left by prey species using their forked tongues and vomeronasal systems (Schwenk, 1994e). In addition to use of chemosensory cues to locate food during foraging in squamates, vomeronasal chemoreception is implicated in food/prey identification and discrimination (summarized by Cooper, 1994, 1995a). Cooper showed that herbivorous and actively foraging lizards are able to use chemical cues gathered by tongue flicking to distinguish among odors and to discriminate food from nonfood odors. These tests were based on the number of tongue flicks and attacks directed to cotton swabs saturated with test odors and hence did not involve food-specific visual cues. Although there are problems with this experimental method (Halpern, 1992; Dial and Schwenk, 1996), the results are suggestive. The ability to discriminate food odors is apparently a labile trait that is tightly associated with foraging mode; Cooper has suggested that phylogenetic transformations in foraging mode are always accompanied by a gain or loss of discriminatory ability. 3. Sensory

Integration

Although, as noted, some squamates apparently emphasize one sensory mode or another, it is clear that in nearly all species feeding behavior is a multisensory

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undertaking. The interplay of chemical senses may occur as outlined earlier and, more importantly, these systems are integrated with vision and other sensory cues to complete a foraging and feeding sequence. For example, although prey location and identification are almost entirely visual in the extremist anolines (Curio and Mobius, 1978, and references earlier), even they are well endowed with lingual and oral taste buds to assess food palatability once ingested (Willard, 1915; Schwenk, 1985). Conversely, actively foraging taxa usually assumed to be chemosensory specialists almost certainly use visual cues at some point in a feeding sequence. Indeed, in most cases it is a visual cue, usually movement, that triggers an attack (e.g.. Fitch, 1954,1958; Burghardt, 1964; Rand et al, 1975; Boyden, 1976; Curio and Mobius, 1978; Dial, 1978; Cooper, 1981; McGovern et al, 1984; Nicoletto, 1985a,b; Vitt and Cooper, 1986; Kaufman et al, 1996; personal observation). Kaufman et al (1996) showed that visual cues were sufficient for distinguishing among prey types in highly chemosensory monitor lizards (Varanus). Among snakes, acknowledged vomeronasal specialists, some species rely on visual cues for prey identification and elicitation of a strike (e.g., Drummond, 1979). Lizards clearly modulate their attack based on visual cues (Schwenk and Throckmorton, 1989; unpublished observation). During lingual feeding attempts, tongue protrusion distance is adjusted according to prey movement or behavior, or sometimes an attack is aborted altogether if prey movement ceases. Mathias Ott (personal communication) has found that horned lizards {Phrynosoma) adjust the trajectory of the rapidly protruding tongue during a capture attempt by slightly turning the head; the behavior is so rapid that visual feedback must occur within a few milliseconds (Schwenk and Throckmorton, 1989; Schwenk, unpublished; M. Ott, personal communication). Boyden's (1976) study of butterfly predation in several populations of Ameiva exemplifies the sensory interplay undoubtedly typical of most squamates. Ameiva are highly chemosensory teiid lizards with deeply forked tongues; virtually all teiids studied are active foragers (e.g.. Fitch, 1958; Anderson and Karasov, 1981; McGovern et al, 1984; Pietruszka, 1986; Vitt, 1991; Vitt and de la Torre, 1996; Vitt et al, 1997a,c) and are capable of chemosensory trailing (Schwenk, 1994e). Nonetheless, Boyden (1976) showed that visual cues alone were used by experienced individuals to distinguish palatable from unpalatable species of butterfly. Naive lizards, however, readily attacked unpalatable species, but subsequently avoided them. Thus, initial chemosensory assessment of palatability led to subsequent visual discrimination of prey species and learned avoidance of distasteful types. Fossorial squamates usually have reduced vision

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and, in some cases, the eye is lost or entirely nonfunctional as a photoreceptor (Underwood, 1970). In such species, vision obviously can play little or no role during feeding behavior and chemoreception is well developed in compensation. It is suggestive that in many fossorial species nasal olfaction seems to be relatively enhanced, as it is in the nocturnal geckos (Schwenk, 1993a); however, the precise interplay of the three chemical senses remains largely unexplored in these, as in other taxa. 4. Sensory Ecology of Sphenodon Most of what is known about the sensory ecology of feeding in tuatara is anecdotal. Tuatara are nocturnal foragers and their retinas are dense with rod-like photoreceptors (Underwood, 1970). As noted earlier, vomeronasal organs are present, but not exceptionally well developed and they do not open to the oral cavity. Not surprisingly, tuatara do not tongue flick (Walls, 1981; Gillingham et al, 1995). Their nasal, olfactory system also appears to be only moderately developed (Gabe and Saint Girons, 1976). However, they are very well supplied with lingual taste buds (Schwenk, 1986). Gillingham et al (1995) showed convincingly that visual cues alone are both necessary and sufficient during all tuatara social behaviors. Visual cues, especially movement, are also sufficient to elicit predatory attack; even inanimate objects moved within sight are attacked and bitten (Farlow, 1976; Walls, 1981). Walls (1981:92) suggested that "rounded, dark, smooth, shiny objects" were most effective in provoking attack in captive feeding experiments—a result consistent with the finding that rounded, dark, smooth, shiny beetles were the most frequent prey items in the study population! In captivity, naive tuatara were observed to capture certain, apparently noxious, prey and then reject them. Diet analysis showed that wild individuals avoided such readily available prey. It is therefore likely that gustation is used by tuatara to assess the palatability of food items and distasteful prey are rejected, subsequently discriminated visually, and avoided (Schwenk, 1986). Meyer-Rochow (1988) tested young tuatara in a darkroom. In the absence of light, or with a photographic safety light, the tuatara showed no interest in mealworms placed 2 cm in front of them, even though the mealworms were active and making scratching sounds. As soon as light was present, however, the same tuatara readily ingested the mealworms. MeyerRochow (1988) concluded that olfactory and auditory cues were insufficient to elicit feeding and that visual cues were relied upon exclusively. These observations are consistent with those of Gorniak et al. (1982) who

found that tuatara only responded to moving prey. Nonetheless, Walls (1981) noted that tuatara sometimes investigate and ingest nonmoving food items, especially petrel eggs and carrion, and believed that this behavior indicates the occasional use of olfactory cues. Farlow noted that a dead cockroach placed in a tuatara's cage was eventually eaten. Similarly, Gorniak et al. (1982:351) contended that "olfactory cues mediate the prey attack response and visual cues are used to steer the capture of prey"; however, they presented no evidence in support of this statement. In conclusion, visual cues are predominant in identifying most prey types and eliciting prey attack, but olfaction may be important for locating and identifying immobile food items. Gustation probably mediates learned food preferences. However, controlled experiments are notably lacking and these are required to determine the interplay of the senses in tuatara foraging and feeding. 5. Other Sensory

Systems

Other sensory mechanisms are less commonly employed during feeding in some squamates. In particular, tactile, vibratory cues are probably important to a variety of fossorial species, such as amphisbaenians (e.g., Gans, 1960,1969a). Gans noted that amphisbaenians moved toward insects moving at the surface. The importance of vibratory cues for locating prey was also demonstrated for the sand-swimming skink, Scincus (Hetherington, 1989). Snakes may use ground-borne vibratory cues to sense the presence of prey (Hartline, 1971). Barnett et al. (1999) recently showed that some chameleons use twig-borne vibrations as social signals. If chameleons are sensitive to such vibratory stimuli, conceivably they could use them for prey detection as well. I have virtually ignored the possible role of hearing in prey detection, but this is only because there is no information indicating it to be of widespread significance. Nonetheless, it is likely that audible cues associated with prey movement contribute to the triggering of prey attack. One species of Hemidactylus (Gekkonidae) has been shown to orient to and approach recorded cricket (prey) calls (Sakaluk and Belwood, 1984), suggesting that phonotaxis might be an important part of foraging in this species, at least. The unusual use of vocal communication by many gekkonids (Marcellini, 1977) might preadapt them for use of audition in prey detection; however, it is unknown how prevalent the behavior is in the family. The use of vibratory cues by amphisbaenians might actually be a form of low-frequency hearing rather than a strictly tactile sense. Most amphisbaenians have a unique ear morphology in which a tympanum is lacking, but an extremely long extracolumella extends anteriorly from

8. Feeding in Lepidosaurs the stapes along the mandible within a specialized zone of skin (Wever, 1978). Wever (1978:784) concluded that "the extracolumella functions in the conduction of vibrations set up in the skin of the face through the action of aerial sounds." Nonetheless, the position of the receptive area on the lower jaw and the sensitivity of the inner ear to low frequencies suggest that the amphisbaenian auditory system might actually be specialized for the reception of ground-borne, rather than aerial, vibrations.

IV. MORPHOLOGY OF THE FEEDING APPARATUS A. Skull and Mandible As reviewed in Chapter 2, the head skeleton comprises the skull, proper, as well as the mandible (lower jaw) and hyobranchial apparatus (tongue and throat skeleton). This section considers basic features of the head skeleton in tuatara and nonophidian squamates. The snake skull is treated in Chapter 9. Tables 8.1 and 8.2 list selected references for the morphology of the head skeleton in lepidosaurs. In general, lepidosaurian skulls comprise a system of bony plates and struts perforated by frequent, large vacuities. Particularly in some squamates, the skull becomes a gracile, almost delicate network of slender struts and kinetic joints. This trend reaches its maximal expression in macrostomatan snakes, but it is approached to some degree in several lizard groups. A lepidosaurian trend toward reduced cranial ossification, extensive fenestration, and cranial kinetism is in stark contrast to basal archosaurs, turtles, and many fossil reptile groups. Some of these changes relate directly to feeding system adaptation. One's impression of a typical lepidosaurian skull is of an extremely strong structure that minimizes weight and material. 1. Sphenodon Tuatara retain what is generally regarded as a primitive skull pattern (Glinther, 1867; Romer, 1956). This is most evident in the retention of a true diapsid pattern of temporal fenestration (see Chapter 2). As such, there are two, large temporal openings in the skull with a complete lower temporal arch formed by the jugal and quadratojugal bones (Fig. 8.2). The posterior rim of the lower fenestra comprises fused squamosal, quadratojugal, and quadrate bones, with the quadrate projecting ventrally below the level of the arch to articulate with the mandible (the jaw joint). In dorsal view, the temporal region is very wide due to capacious upper temporal fenestrae, but the dermal

189

roof of the braincase is narrowly constricted. Sphenodon also retains the primitive condition in having the entire anteroposterior series of medial, dermal roofing bones paired (premaxillae, nasals, frontals, parietals). A small parietal foramen is present in the midline for the parietal eye. The orbits are large. An unusual feature of the skull is the presence of a prominent, lateral notch between the maxilla and the premaxilla. The premaxillae are slightly elongate and in adults bear two, often prominent, acrodont teeth each. The effect is to create the impression of a "beak," hence the taxon name Rhynchocephalia, meaning "beak head." The posterior end of the braincase is wholly ossified and formed from an occipital series of bones surrounding the foramen magnum. Large paroccipital processes of the opisthotic bones extend laterally to articulate with the posterior rim of the lower temporal arch (at the dorsal end of the quadrate). Between these processes and the upper temporal arcades are posterior openings called the posttemporal fenestrae. Dorsally, a supraoccipital bone forms a median crest that extends toward the roofing parietal bones. It gives rise to an anteriorly directed, median process (ascending process or processus ascendens) that is "clamped" between the paired parietals. Ventrally, the basisphenoid forms the floor of the braincase. It extends anteriorly on each side to form two basipterygoid processes, which articulate with the deep, posterior wings of the pterygoid bones. Although Romer (1956) described these joints as "movable," each condylar process is held within a bony socket of the pterygoid that would seem to preclude movement here. Anteriorly, the braincase remains membranous throughout life (de Beer, 1937; Romer, 1956). Paired vomers, palatines, and pterygoids form most of the broad, bony palate that is much less fenestrated than in squamates. A derived feature of the palate is the presence of palatal teeth arrayed linearly along the lateral margin of the palatine bone parallel to the marginal, maxillary tooth row (Fig. 8.2B). During jaw closure, mandibular teeth lie within the cleft between the two upper tooth rows. As noted, the premaxillae and maxillae bear the marginal teeth (see later). Palatal fenestra are little more than longitudinal slits between palatine and maxillary bones due to the close juxtaposition of their tooth rows. The lower jaw, or mandible, comprises two halves (hemimandibles or mandibular rami) that are joined anteriorly by a loose connective tissue joint (Robinson, 1976). The looseness of this articulation is surprising given that Meckel's cartilage completely fuses anteriorly in the embryo, implying the formation of a true, symphyseal (fibrocartilage) joint (de Beer, 1937). However, Bellairs and Kamal (1981) observed late-stage

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Kurt Schwenk TABLE 8.1

Selected References Treating the M o r p h o l o g y of the Feeding S y s t e m in Lepidosaurs Exclusive of Snakes and Chameleons"" Scleroglossa

Sphenodon

Iguania

Bellairs and Boyd (1950) Bellairs and Kamal (1981) Broom (1903,1925) de Beer (1937) Gorniak et al (1982) Giinther (1867) Howes and Swinnerton (1901) Lakjer (1927) Malan (1946) Pratt (1948) Rieppel (1993) Romer (1956) Save-Soderbergh (1947) Schauinsland (1900,1903) Verluys (1936) Werner (1962) Wettstein (1931)

Avery and Tanner (1964, 1971) Bellairs (1984) Bellairs and Boyd (1950) Bellairs and Kamal (1981) Blanc (1965) Broom (1903,1925,1935) Camp (1923) de Queiroz (1987) Engelbrecht (1951) George (1954) Greer (1989) Hallermann (1992,1994) Harris (1963) Herrel et al (1998a) lordansky (1990b, 1996) Jenkins and Tanner (1968) Kamal and Zada (1970) Kraklau (1991) Lakjer (1927) Lang (1989) Malan (1946) Oelrich (1954) Paranjape (1974) Parker(1881) Pratt (1948) Ramaswami (1946) Rieppel (1978d, 1993) Romer (1956) Stimie (1966) Throckmorton (1976) Verluys (1936) Zaluskyeffl/. (1980)

Gekkota

Scincomorpha

Anguimorpha

Bellairs (1984) Bellairs and Boyd (1950) Bellairs and Cans (1982) Bellairs and Kamal (1981) Bels et al (1993) Broom (1903,1925,1935) Camp (1923) Dalrymple (1979) de Beer (1937) El Toubi and Kamal (1959a,b) Fisher and Tanner (1970) Cans (1960,1974,1978) Greer (1989) Herrel et al (1998a) lordansky (1990b, 1996) Kamal (1965) Kesteven (1957) Kritzinger (1946) Lakjer (1927) MacLean (1974) Malan (1940,1946) Montero et al (1999) Nash and Tanner (1970) Parker(1880) Presch (1976) Rao and Ramaswami (1952) Rice (1920) Rieppel (1978d, 1981c, 1984a,c, 1992b, 1993) Romer (1956) van Pletzen (1946) Verluys (1936) Wineski and Cans (1984) Zangerl (1944)

Auffenberg (1981) Bahl (1937) Barrows and Smith (1947) Bellairs (1949,1950,1984) Bellairs and Boyd (1950) Bellairs and Kamal (1981) Bogert and Martin del Campo (1956) Broom (1925,1935) Camp (1923) Criley (1968) Frazzetta (1962) Greer (1989) lordansky (1990b, 1996) Lakjer (1927) Malan (1946) McDowell and Bogert (1954) Rieppel (1978b,d, 1983, 1984a, 1993) Rieppel and Labhardt (1979) Romer (1956) Smith (1980) Verluys (1936)

Camp (1923) Dalrymple (1979) Dessem (1985) Edmund (1969) Estes and Williams (1984) Fisher and Tanner (1970) Cans (1960,1978) Greer (1989) MacLean (1974) Mateo and Lopez-Jurado (1992,1997) Peyer(1929) Presch (1974) Rocek (1980a) Romer (1956)

Bogert and Martin del Campo (1956) Camp (1923) Cooper (1966) Edmund (1969) Estes and Williams (1984) Greer (1989) Lonnberg (1903) McDowell and Bogert (1954) Peyer(1929) Rieppel (1978f, 1979a) Rieppel and Labhardt (1979) Rocek (1980b) Romer (1956)

Skull Bauer (1990) Bellairs and Boyd (1950) Bellairs and Kamal (1981) Broom (1935) Camp (1923) Greer (1985,1989) lordansky (1990b, 1996) Kluge (1962,1987) Lakjer (1927) Malan (1946) Rieppel (1984a,b, 1992a, 1993) Romer (1956) Stephenson (1962) Underwood (1957) Verluys (1936) Webb (1951) Wellborn (1933)

Dentition Edmund (1969) Gorniak et al (1982) Harrison (1901a,b) Robinson (1976) Romer (1956)

Avery and Tanner (1964) Blanc (1965) Camp (1923) Cooper and Poole (1973) Cooper et al (1970) Edmund (1969) Estes and Williams (1984) Greer (1989) Hotton (1955) Kline (1983) Kline and Cullum (1984, 1985) Lang (1989) Montanucci (1968) Oelrich (1956) Robinson (1976) Robison and Tanner (1962) Romer (1956) Throckmorton (1976,1979)

Bauer (1990) Bauer and Russell (1990) Camp (1923) Edmund (1969) Estes and Williams (1984) Greer (1985,1989) Patchell and Shine (1986c) Rieppel (1984b) Romer (1956) Sumida and Murphy (1987)

(continues)

191

8. Feeding in Lepidosaurs TABLE 8.1 (continued) Scleroglossa Sphenodon

Iguania

Gekkota Hyobranchial

Scincomorpha

Anguimorpha

apparatus

Edgeworth (1935) Furbringer (1922) Osawa (1898) Romer (1956) Tanner and Avery (1982)

Avery and Tanner (1964, 1971) Beebe (1944) Beddard (1905) Bels (1990b, 1992) Bels et al (1994) Blanc (1965) Camp (1923) Capel-Williams and Pratten (1978) de la Cerna de Esteban (1965) de Queiroz (1987) Edgeworth (1935) Font and Rome (1990) Furbringer (1922) Gnanamuthu (1937) von Geldern (1919) Harris (1963) Jenkins and Tanner (1968) Kraklau (1991) Lang (1989) Oelrich (1954) Richter (1932) Robison and Tanner (1962) Romer (1956) Smith (1984,1988) Tanner and Avery (1982) Throckmorton et al. (1985)

Bauer (1990) Bels et al. (1994) Camp (1923) de la Cerna de Esteban (1965) Furbringer (1922) Gnanamuthu (1937) Greer (1985) Richter (1932) Rieppel (1981a) Romer (1956) Tanner and Avery (1982) Underwood (1957)

Edgeworth (1931,1935) Gorniakeffl/. (1982) Haas (1973) Kesteven (1944) Lakjer (1926) LightoUer (1939) Lubosch (1933) Ostrom (1962) Poglayen-Neuwall (1953) Wettstein (1931)

Avery and Tanner (1964, 1971) Bradley (1903) Capel-Williams and Pratten (1978) Edgeworth (1935) George (1948) Haas (1973) Herrel et al. (1998a, 1999a) lordansky (1970,1990b) Jenkins and Tanner (1968) Kesteven (1944) Kraklau (1991) Lakjer (1926) Lang (1989) Lubosch (1933) Oelrich (1954) Poglayen-Neuwall (1954) Rieppel and Gronowski (1981) Robison and Tanner (1962) Throckmorton (1976,1978)

Bradley (1903) Edgeworth (1935) Gasc (1968) Haas (1973) lordansky (1970,1990b) Kesteven (1944) Lakjer(1926) Lubosch (1933) Poglayen-Neuwall (1954) Rieppel (1984a, b) Rieppel and Gronowski (1981)

Beebe (1945) Bels et al. (1994) Camp (1923) de la Cerna de Esteban (1959,1965) Edgeworth (1935) Cans (1978) Fisher and Tanner (1970) Furbringer (1922) Gnanamuthu (1937) Harris (1985) MacLean (1974) Montero et al. (1999) Nash and Tanner (1970) Richter (1932) Rieppel (1981a) Romer (1956) Smith (1984) Tanner and Avery (1982)

Bels et al. (1994,1995) Camp (1923) Furbringer (1922) Gnanamuthu (1937) McDowell and Bogert (1954) Richter (1932) Rieppel (1981a) Romer (1956) Smith (1986) Sondhi (1958b) Tanner and Avery (1982)

Bradley (1903) Edgeworth (1935) Fisher and Tanner (1970) Cans et al. (1985) Haas (1973) Herrel effl/. (1996,1998a, 1999b) lordansky (1970,1990b) Kesteven (1944,1957) Lakjer(1926) LightoUer (1939) Nash and Tanner (1970) Poglayen-Neuwall (1954) Rieppel (1979b, 1980, 1981c, 1984a) Rieppel and Gronowski (1981) Throckmorton (1982) Wineski and Cans (1984)

Bradley (1903) Edgeworth (1935) Haas (1973) lordansky (1970,1990b) Kesteven (1944) Lakjer (1926) LightoUer (1939) Poglayen-Neuwall (1954) Rieppel (1978a, 1984a) Rieppel and Gronowski (1981) Smith (1980,1982,1986)

Jaw musculature

(continues)

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Kurt Schwenk

TABLE 8.1 (continued) Scleroglossa Sphenodon

Iguania

Gekkota

Scincomorpha

Anguimorpha

Bayer(1899) Bels et al (1993) Bendz (1840) Bogert (1964) Camp (1923) Chieleffl/. (1992) Corning (1895) de la Cerna de Esteban (1959,1965) Dornesco and Andrei (1966) Duges (1827) Edgeworth (1935) Ferdinand (1884) Gabe and Saint Girons (1969) Cans (1978) Gnanamuthu (1937) Harris (1985) Iwasaki and Kobayashi (1992) Iwasaki and Miyata (1985) Kallius (1901) Kochva (1978) MacLean (1974) Minot (1880) Presch (1971) Renous (1977) Richter (1932) Schwenk (1985,1988,1994, 1995; 2000a) Sewertzoff (1929) Smith (1984) Taib and Jarrar (1986) Tanner and Avery (1982) von Seiller (1891,1892) Wagner and Schwenk (2000) Zanno (1974)

Camp (1923) Ferdinand (1884) Gabe and Saint Girons (1969) Gnanamuthu (1937) Kallius (1901) Kochva (1978) McDowell (1972) McDowell and Bogert (1954) Richter (1932) Schwenk (1985,1988, 1994,1995, 2000a) Sewertzoff (1929) Smith (1986) Smith and Mackay (1990) Sondhi (1958a,b) Tanner and Avery (1982) Toubeau et al (1994) von Seiller (1891) Wagner and Schwenk (2000)

Tongue Edgeworth (1935) Gabe and Saint Girons (1964,1969) Kochva (1978) Osawa (1897) Rieppel (1978e) Schwenk (1986,1988) Sewertzoff (1929) Tanner and Avery (1982)

Bendz (1840) Camp (1923) de la Cerna de Esteban (1965) Delheusydfl/. (1994) Edgeworth (1935) Ferdinand (1884) Gabe and Saint Girons (1969) Gandolfi, H. (1908) Gnanamuthu (1937) Herrel et al (1998c) Kochva (1978) Kraklau (1991) McDowell (1972) Oelrich (1954) Rabinowitz and Tandler (1986,1991) Richter (1932) Schwenk (1985,1988, 1994,1995, 2000a) Sewertzoff (1929) Smith (1984,1988) Taib and Jarrar (1985a,b) Tanner and Avery (1982) Wagner and Schwenk (2000) Willard (1915)

Camp (1923) de la Cerna de Esteban (1965) Edgeworth (1935) Gabe and Saint Girons (1969) Gnanamuthu (1937) Greer (1985) Iwasaki (1990) Kochva (1978) Ping (1932) Richter (1932) Schwenk (1985,1988, 1994,1995,2000a) Sewertzoff (1929) Tanner and Avery (1982) Underwood (1957) Wagner and Schwenk (2000) Zavattari (1909)

^See Chapter 9 and Table 8.3, respectively. For convenience, references for Dibamidae and Xantusiidae are included under Gekkota (as per Lee, 1998), and those for Amphisbaenia under Scincomorpha (as per Schwenk, 1988); otherwise the taxonomic content of each column follows Estes et al (1988). The primary literature is heavily emphasized, but important reviews or secondary sources are included. Major surveys, summaries, or overviews are shown in bold type.

regression of Meckel's cartilage in Lacerta, suggesting the likelihood of late-stage remodeling of the mandibular joint. Robinson (1976) suggested that the looseness of this joint permits rotation of each hemimandible and deformation of mandibular shape that allows propalineal movement of the lower tooth rows between the dual, parallel tooth rows of the upper jaw (see Section V). The only dentigerous element in each hemimandible is the dentary bone, which is also the largest and most anterior element. A series of smaller bones

form its posterior end. Notable among these is a dorsally projecting coronoid bone that serves as the attachment site for the adductor mandibulae musculature and an articular bone (fused with the prearticular) that articulates with the quadrate of the upper jaw to form the jaw joint. The articular facet is shallow and somewhat elongated anteroposteriorly, thus permitting anteroposterior sliding of the mandible on the quadrates (Robinson, 1976). A very small retroarticular process of the articular extends posterior to the jaw joint. On the

193

8. F e e d i n g in L e p i d o s a u r s TABLE 8.2 Selected References Treating Form and Function of the Feeding Apparatus in C h a m e l e o n s Morphology

Functional inference

Functional analysis

Bell (1987,1989) Briicke (1852) Edgeworth (1935) Duvernoy (1836b) Fineman (1940,1943) Fiirbringer (1922) Cans (1967) Gnanamuthu (1930,1937) Houston (1828) lordansky (1973) Kathariner (1895) Lubosch (1932,1933) Minot (1880) Mivart (1870) Owen (1866) Perrault (1676) Rice (1973) Rieppel (1981b, 1987) Rieppel and Crumly (1997) Sewertzoff (1923) van Leeuwen (1997) Wainwright and Bennett (1992a)

Bell (1989) Briicke (1852) Cuvier (1805) Dewevre (1895) Dumeril (1836) Duvernoy (1836a,b) Cans (1967) Gnanamuthu (1930,1937) Houston (1828) Kathariner (1895) Owen (1866) Perrault (1676) Schwenk (1983) van Leeuwen (1997)

Altevogt (1977) Altevogt and Altevogt (1954) Bell (1990) Dischner (1958) So et ah (1992) Schwenk and Bell (1988) Wainwright effl/. (1991) Wainwright and Bennett (1992a,b) Zoond (1933)

medial surface of the mandible, an open, Meckelian sulcus is apparent (Romer, 1956). 2.

Squamata

Squamates have introduced one very important novelty in skull form relative to Sphenodon and related, extinct taxa: the diapsid condition has been modified so that the lower temporal arch is absent due to loss of the quadratojugal bone and the quadrate process of the jugal (Figs. 8.3-8.6). Furthermore, the posterior margin of the lower temporal fenestra is formed entirely from the quadrate bone, which articulates somewhat loosely with the temporal arch above. In most cases, it also forms a loose joint with the pterygoid wing on its medial surface. A functional consequence of these modifications is that the quadrate is potentially free to rotate anteroposteriorly, a condition known as streptostyly (Versluys, 1912; Robinson, 1967). I emphasize "potentially" because actual streptostylic motion of the quadrate during feeding has been functionally documented only rarely (see later). Streptostyly (in the sense of potential quadrate mobility) is a diagnostic character of Squamata. Robinson (1976) thought that quadrate mobility was the initial source of selection pressure for reduction of the lower temporal bar, but Rieppel and Gronowski (1981) argued that it was expansion and thickening of a superficial adductor muscle (see later) that drove the loss.

In most squamates, the quadrate is emarginated posterolaterally and a prominent anterolateral rim supports the anterior margin of the tympanum. A minute, slender stapes runs from the tympanum across the anatomical space of the middle ear to the braincase (Fig. 8.4). Some scleroglossan taxa have no tympanum, but retain the middle ear cavity and a stapes, which attaches to the skin via a cartilaginous extracolumella. Due to expansion of the braincase in some burrowing forms, the middle ear space is virtually obliterated (Fig. 8.6). In the snout, paired septomaxillae are sometimes visible in dorsal view within the external nares (nostrils), most notably in varanids (Fig. 8.4). The septomaxilla forms part of the floor of the nasal cavity and, importantly, the roof of the skeletal capsule containing the vomeronasal organ. The complete isolation of these organs from the nasal chamber is unique to squamates (see earlier discussion). a. Iguania In general, iguanians resemble Sphenodon in skull form (Fig. 8.3). They tend to have large upper temporal fenestrae and thus are similarly broad across the temporal region. Unlike Sphenodon, however, the premaxillae, frontals, and parietals are virtually always fused into single, median bones; the premaxillae are paired in a few iguanids (Romer, 1956). The nasals remain paired, except in a few chamaeleonids (Rieppel and

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Kurt Schwenk

FIGURE 8.2. Skull of a tuatara, Sphenodon punctatus, in dorsal (A), ventral (B), lateral (C), and posterior (D) views, a, angular; art, articular; bo, basioccipital; d, dentary; ect, ectopterygoid; eo, exoccipital; ept, epipterygoid; f, frontal; j , jugal; m, maxilla; n, nasal; opis, opisthotic; p, parietal; pal, palatine; pf, postfrontal; pm, premaxilla; po, postorbital; prf, prefrontal; pro, prootic; ps, parasphenoid; pt, pterygoid; ptf, posttemporal fossa; q, quadrate; qf, quadrate foramen; qj, quadratojugal; sa, surangular; so, supraoccipital; sq, squamosal. From Vertebrate Paleontology by Carroll © 1998 by W. H. Freeman and Company. Used with permission.

Crumly, 1997). The orbits are large to accommodate well-developed eyes. A "parietal" foramen is present, except in some chamaeleonids (Rieppel, 1981b); however, its position is variable. It is most often within the frontoparietal suture (Fig. 8.3), but is sometimes completely within the frontal or parietal bones (e.g., Estes et al, 1988; Lang, 1989). The snout is usually broad and short in iguanians. In dorsal view it is most often blunt and rounded, but it is sometimes quite triangular and pointed anteriorly (particularly in some agamids). Some taxa, notably the sceloporine iguanids ('Thrynosomatids"), or sand lizards, have flattened, wedgelike snouts with countersunk lower jaws to facilitate head-first burial in loose sand. In most chamaeleonids and some basciliscine igua-

nids, the parietal region of the skull forms a welldeveloped median crest (Fig. 8.7). The crest is formed from a blade of the parietal bone that extends posterodorsally, and in chameleons and most of the basciliscines, the jaw adductor musculature takes its origin along its length (e.g., Schwenk, 1980; Rieppel, 1981b, 1987; Rieppel and Crumly, 1997; Lang, 1989). The parietals also have ventral extensions that meet the supraoccipital. In some taxa, lateral flanges of the parietal extend partly or completely over the upper temporal fenestrae, forming a cranial "casque." This is often continued anteriorly by lateral extensions of the frontal, prefrontals, and other dermal roofing bones. Cranial casques are also common among anoloid iguanids ("Polychrotidae"). Typically in casque-headed forms.

8. Feeding in Lepidosaurs

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F I G U R E 8.3. Skull of an iguanian lizard, Brachylophus vitiensis (Iguanidae), in dorsal (A), ventral (B), posterior (C), and lateral (D) views. (E and F) One ramus of the mandible in lateral (labial) and medial (lingual) views, respectively, aiaf, anterior inferior alveolar foramen; amf, anterior mylohyoid foramen; an, angular; ap, angular process; ar, articular; bo, basioccipital; bs, basi(para)sphenoid; cor, coronoid; den, dentary; ect, ectopterygoid; eo, exoccipital-opisthotic; ept, epipterygoid; fr, frontal; ju, jugal; la, lacrimal; mf, mental foramina; mx, maxilla; na, nasal; oc, occipital condyle; pal, palatine; par, parietal; pmf, posterior mylohyoid foramen; pmx, premaxilla; pre, prearticular; prf, prefrontal; pro, prootic; ps, parasphenoid process; ptf, postfrontal; pto, postorbital; ptr, pterygoid; q, quadrate; rap, retroarticular process; slf, supralabial foramina; smx, septomaxilla; soc, supraoccipital; sp, splenial; sq, squamosal; st, supratemporal; sur, surangular; vo, vomer. From de Queiroz (1987), with permission.

there is extensive co-ossification of the skin with the skull roof. Chameleons, in particular, show highly "sculpted'' dermal roofing bones indicative of this condition. Some chameleons have additional cranial ornamentation in the form of horns and other projections from the snout, cranium, and supraorbital region. Chamaeleo hifidis, for example, has paired, blade-like projections of the prefrontal and maxillary bones extending anteriorly from the rostrum (Rieppel and Crumly, 1997). Horns are primarily keratinous projections of the integument with a shorter, bony core projecting from the parietal and/or premaxilla. They are sometimes sexually dimorphic (e.g., de Witte, 1965) and used in male-male combat (e.g.. Bustard, 1958; Parcher, 1974), but most types of chamaeleonid cranial ornamentation are implicated in species recognition (Rand, 1961). Some anoline iguanids and agamid lizards also have elaborate, sometimes bizarre, cephalic ornaments, but these are mostly integumental. As in Sphenodon, the braincase is ossified posteriorly

and membranous anteriorly. Posttemporal fenestrae are well developed, and a median ascending process (usually cartilaginous) of the supraoccipital penetrates the parietal bone. Strong paroccipital processes extend laterally from the braincase and articulate with the temporal arches near to the quadrate's dorsal articulation (Fig. 8.3C). Basipterygoid processes of the basisphenoid are pronounced and extend anterolaterally to the medial, concave surfaces of the pterygoid wings (Fig. 8.3B). An articular cartilage is often present here. Although widely reputed to be a sliding joint in conjunction with skull kinesis (see later), in most iguanians the processes abut the pterygoid in such a way that anterior movement on the pterygoids would be impossible (Schwenk, unpublished observations). The palate is generalized and comprises, from front to back, paired vomers, palatines, ectopterygoids, and pterygoids. The premaxilla and maxillae contain the marginal teeth and contribute palatal shelves. Palatal teeth are often present on the pterygoid bones. Well-

n^DowcuL F I G U R E 8.4. Skull of a scleroglossan lizard, Varanus varius (Varanidae), in ventral (A), dorsal (B), and lateral (C) views. (D and E) One ramus of the mandible in lateral (labial) and medial (lingual) views, respectively. Note the laterally constricted temporal fenestrae and the mandibular joint posterior to the dentary evident in (D). The dentition is pleurodont and the teeth are blade-like, ang, angular; art, articular; boc, basioccipital; bsp, basisphenoid; cor, coronoid; den, dentary; ecp, ectopterygoid; epp, epipterygoid; exo, exoccipital; fro, frontal; jug, jugal; lac, lacrimal; max, maxilla; nas, nasal; pa, prearticular; pal, palatine; pap, palpebral; par, parietal; pof + poo, fused postfrontal and postorbital; prf, prefrontal; prm, premaxilla; pro, prootic; ptd, pterygoid; qut, quadrate; sep, septomaxilla; spl, splenial; squ, squamosal; sta, stapes; suo, supraoccipital; sur, surangular; tab, supratemporal; vom, vomer. From McDowell and Bogert (1954), courtesy of the American Museum of Natural History.

8. F e e d i n g in L e p i d o s a u r s

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F I G U R E 8.5. Skulls of two scleroglossan lizards showing loss of the temporal fenestrae. Both species exhibit typical, unicuspid, pleurodont dentition. (A) Coleonyx variegatus (Gekkonidae). (B) Cordylus giganteus (Cordylidae). In Coleonyx the temporal fenestra has been eliminated by loss of the upper temporal arcade, whereas in Cordylus it has been lost through overgrowth of dermal roofing bones. Abbreviations as in Fig. 8.4. From McDowell and Bogert (1954), courtesy of the American Museum of Natural History.

developed palatal fenestrae are found between the palatines medially and the maxillae laterally. Anteriorly, another pair of narrow fenestrae lie between the vomers medially and the maxillae laterally. The vomeronasal ducts open through these anteriorly and the internal nares (choanae) posteriorly. The continuity of these openings in iguanians and some other lizards is considered primitive and is called the "paleochoanate" condition (Lakjer, 1927; Bellairs and Boyd, 1950). Posteriorly, a wide interpterygoid vacuity is pierced in the midline by a slender parasphenoid process projecting forward from the basisphenoid. The iguanian mandible is similar to that of Sphenodon with several exceptions (Figs. 8.3E and 8.3F). The mandibular joint is much tighter and typically forms a fibrocartilage symphysis. In most taxa, Meckel's cartilage persists within a mandibular canal throughout life and is continuous anteriorly at the symphysis, but it is lost in some chameleons (Bellairs, 1984). A large splenial bone is present, sometimes extending quite far anteriorly along the medial surface of the dentary and

covering the Meckelian canal so that no sulcus remains. The coronoid bone is variously developed, but is often much more pronounced than in Sphenodon. The articular facet of the jaw joint is generally more restrictive than in Sphenodon and does not permit translational movement of the mandible. Finally, the retroarticular process is also highly variable. It is small to moderate in length in iguanids, virtually absent in chamaeleonids, and often exceptionally long in agamids (Schwenk and P. Hall, unpublished results). b. Scleroglossa Skull form among scleroglossans is diverse (Figs. 8.4-8.6). It conforms generally to the pattern established previously, but certain variations are notable. Major departures include diversity in the form of the temporal region and radical modification of the skull in numerous fossorial taxa. In the latter types, the skull has been transformed into a solid, unitary structure capable of withstanding the reaction forces obtaining from head-first locomotion through the substrate.

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ot-oc

pm

purposes of burrowing (Cans, 1974). Some amphisbaenians have vertically keeled snouts to enhance the displacement of soil during ramming and burrowing, whereas others have dorsoventrally compressed, wedge-like snouts for the same purpose. Amphisbaenians also have unusually complex, deeply interdigitating sutural patterns, reflecting enhanced strength and rigidity of the skull in these forms (e.g., Zangerl, 1944; Cans, 1960) (Fig. 8.6). Most important, many scleroglossan taxa have reduced or lost the upper temporal fenestrae. When present, the fenestrae are narrower than in iguanians so the temporal region of the scleroglossan skull is relatively less broad (Fig. 8.4). Loss of the fenestrae results either from obliteration by overgrowth of the surrounding bones or by loss of the arch itself (Romer,

FIGURE 8.6. Amphisbaenian skulls. (A) Amphisbaena alba (Amphisbaenidae) in lateral view. (B and C) Pachycalamus brevis (Trogonophidae) in dorsal and ventral views, respectively. Note loss of the temporal fenestrae and expansion of the braincase. Sutures are often elaborate to strengthen the skull for burrowing. Amphisbaena has large, pleurodont teeth, but the trogonophid has acrodont teeth with dental occlusion. The single, median tooth at the anterior end of the tooth row (C) is a unique feature of the amphisbaenian dentition. (A) from Rieppel (1979), (B) and (C) from Cans (1960), courtesy of the American Museum of Natural History.

including head ramming to widen or create tunnels (Cans, 1961, 1969a, 1974; Wake, 1993). With the exception of burrowing forms, however, scleroglossan skulls are typically less robust and more kinetic than in iguanians. The medial series of dermal roofing bones are variably paired or fused among scleroglossans. The premaxillae, which are fused in nearly all lizards, are paired in young individuals and adults of some scleroglossans (e.g., some gekkotans, Kluge, 1987; some skinks, Romer, 1956), and the nasal bones, usually paired, are sometimes fused (e.g., some Varanus, Greer, 1989). Skull form and snout shape are highly variable. Gekkonids, for example, typically have broad, flat skulls with relatively short snouts (Fig. 8.5A), whereas varanids often have pointed, elongate snouts that are wedge-like in profile (Fig. 8.4). Fossorial forms tend to have relatively small heads and skulls that are somewhat elongate, probably to reduce head diameter for

FIGURE 8.7. Skull and jaw musculature of a chameleon, Bradypodion pumilus. Note the parietal crest typical of many cham.eleons and some iguanid lizards, amam, adductor mandibulae medialis; amep (3a-3c), adductor mandibulae externus profundus, heads 3a to 3c; ames (lb), adductor mandibulae superficialis, head lb; bo.ap, bodenaponeurosis; dm, depressor mandibulae; lao, levator anguli oris; map, adductor posterior; m.pt, pterygoideus; ps.p, pseudotemporalis profundus; ps.s, pseudotemporalis superficialis; r.pl, rictal plate {Mundplatt). From Rieppel (1981b), with permission.

8. Feeding in Lepidosaurs 1956). Overgrowth occurs by posterior expansion of the postfrontals, medial expansion of bones forming the arch (postorbital and squamosal), fusion of the squamosal to the parietal, or some combination of these (Fig. 8.5B). Romer (1956) noted that overgrowth of the upper temporal fenestrae occurs in taxa with well-developed osteoderms and other integumental ossifications, such as the supraorbital plates found in some cordylids (e.g., van Pletzen, 1946), to which he attributed a causal basis. Fiowever, given that the function of the temporal fenestrae is poorly understood (Chapter 2), the reason for this interesting correlation remains unknown. Finally, some scleroglossan taxa have lost the upper fenestra through loss of the arch so that the widest part of the skull is across the orbits with the temporal region constricted to the width of the braincase (in small burrowing forms the posterior end of the braincase is often laterally expanded). This condition can be seen in gekkotans (Fig. 8.5A), the varanoids Heloderma and Lanthanotus, and virtually all fossorial taxa (e.g., Dibamidae, Amphisbaenia, and the small, burrowing skinks; Fig. 8.6). In such forms the jaw adductor musculature originates entirely on the side and roof of the braincase and, to some extent, from the overlying skin (e.g., Rieppel, 1979b, 1981c, 1984a,b). Ossification of the braincase is more extensive in scleroglossans than in iguanians, primarily through expansion of the prootics anteriorly along the lateral walls (Romer, 1956). In varanoids (McDowell and Bogert, 1954) and gekkotans (McDowell and Bogert, 1954; Kluge, 1987), ventral downgrowths of the frontal bones surround the olfactory bulbs of the forebrain. In fossorial forms, the braincase is further ossified and solidified, completely so in amphisbaenians (Romer, 1956; Cans, 1960), as in snakes. In these species the braincase is often "swollen" so that it closely approaches the quadrates (Fig. 8.6). As such, the paraoccipital processes are very short or absent. In most scleroglossans, however, they are well developed, as are the basipterygoid processes of the basisphenoid. The latter articulate with the pterygoid bones within medial, longitudinal grooves. The nature of this joint and the presence of a cartilaginous meniscus suggest that some sliding motion occurs here during kinetic movements of the skull in most species. The palate is generally similar to the condition described for Iguania, with some variations. The palatal fenestrae vary in size and are virtually absent in some species. In many scleroglossans, the anterior openings of the vomeronasal ducts are separated from the more posterior choanae, a condition termed "neochoanate" (Lakjer, 1927; Bellairs and Boyd, 1950). In such forms the vomeronasal openings are little more than tiny slits between the vomers and the palatal shelves of the max-

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illae. The choanae may also be narrow. Surprisingly, a number of lizards have evolved a secondary palate in which the airway is partially or completely separated from the oral cavity by ventromedial extensions of palatal bones. In some scincids a secondary palate is merely suggested, but in others it is complete and forms a "tunnel" by downgrowths of the palatine and pterygoid bones, which extend medially over the choanae (Goppert, 1903; Greer, 1989). This would act to channel airflow posteriorly to the oropharynx in the vicinity of the glottis. Secondary palates are also found in gymnopthalmids (so-called "microteiids"; Presch, 1976), dibamids (Greer, 1985), and some amphisbaenians (Zangerl, 1944; Kritzinger, 1946; Gans, 1978). The functional significance of the secondary palate in lizards is unknown; it may be more important in strengthening the facial skeleton than in respiratory function (see discussion of the secondary palate in mammals. Chapter 2), a hypothesis consistent with its occurrence in several lineages of small burrowers. The mandible is similar to the condition described for iguanians (Figs. 8.4 and 8.5). The retroarticular process is usually moderately developed, but is sometimes reduced to a nubbin or somewhat elongated. The coronoid process is variable in size, and in some taxa the splenial extends very far anteriorly along the medial surface of each hemimandible, almost reaching the symphysis. One striking variation of the mandible is evident in varanoid lizards {Heloderma, Lanthanotus, Varanus, and the extinct mosasaurs) and snakes: each hemimandible is divided into anterior and posterior moieties that are separated by a movable, fibrous joint (McDowell and Bogert, 1954; Lee et ah, 1999) (Fig. 8.4). In Lanthanotus, Varanus, and some snakes, the joint is almost vertical, forming a simple hinge that permits mediolateral bending of the mandible and probably some torsion as well. In Varanus the mandibular joint is loose and strictly fibrous (Bellairs, 1984), as it appears to be in Lanthanotus as well (Schwenk, unpublished results). 3. Morphological Basis of Cranial Kinesis Cranial kinesis in lizards has been reviewed by Frazzetta (1962, 1983), Condon (1987), Rieppel (1993), Smith (1993), and Arnold (1998). It is important to distinguish between the inference of cranial kinesis based on skull anatomy and the actual demonstration of kinetic movements determined by functional analysis (Kardong et ah, 1997). Fiere I limit discussion to the anatomy of cranial kinesis. Its function and relevance to feeding are treated later (see Section V). Cranial kinesis refers to any intracranial mobility of the skull and therefore excludes mandibular and

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hyobranchial movement. The concept derives from the early anatomical studies of Versluys (1912; reviewed in 1936) and others (e.g., Bradley, 1903; Lakjer, 1924) who noted that certain joints within the lizard skull appear to allow movement between bones. This has been confirmed by manual manipulation of fresh specimens (e.g., Frazzetta, 1962) and histological analysis of some putatively kinetic joints (e.g., van Pletzen, 1946; Condon, 1998; Schwenk, unpublished results). Versluys (1912) identified three ''types" of cranial kinesis in lizards: streptostyly refers to mobility of the quadrate bone (see earlier discussion), metakinesis refers to mobility of the dermatocranium on the braincase, and mesokinesis refers to mobility of the upper jaw or snout relative to the posterior, parietal portion of the skull. Skulls that exhibit both meta- and mesokinesis are said to be amphikinetic. Based on anatomical considerations alone, Frazzetta (1962) regarded most lizard skulls as amphikinetic. Although streptostyly is, in a general sense, a type of cranial kinesis, in most usage "cranial kinesis" refers to kinetic movements of the skull exclusive of streptostyly, which is usually discussed separately. In streptostyly, the quadrate moves on its dorsal articulation with the squamosal. This motion is primarily anteroposterior, but some lateral flexion might be possible in some species (e.g., Condon, 1987). Taxa vary considerably on the potential extent of streptostylic motion, depending on the nature of the quadratesquamosal joint (lordansky, 1990). In nearly all squamates the quadrate also articulates on its medial surface with the posterior "wing" of the pterygoid bone. This joint is also loose, but is variable in the degree of movement it allows [e.g., compare Ctenosaura, an iguanian, with very limited movement (Oelrich, 1956) and Cordylus, a scleroglossan, with significant movement (van Pletzen, 1946)]. Metakinesis implies flexion around a transverse axis defined by the lateral articulations of the paroccipital processes with the upper temporal arches. A median joint between the supraoccipital and parietal(s) also joins the braincase to the dermal skull roof. Metakinetic flexure, if it occurs at all, must be fairly complex due to the nature of these joints. Usually the axis of rotation is posterior to the medial supraoccipital-parietal joint, implying that sliding must occur at the latter point (Frazzetta, 1962), but this interpretation is problematic. In most taxa, a cartilaginous peg (ascending process) of the supraoccipital projects into a socket of the parietal bone; however, in the few taxa examined histologically, the joint would seem to permit little, if any, movement due to the nature of the collagenous fibers connecting the bones, hooking of the process, or, in some cases, actual fusion of the elements (Condon, 1998; Schwenk, unpublished

results). In mesokinesis, the principal locus of flexure is at the frontoparietal suture in the skull roof. In some species, the highly kinetic nature of this joint is indicated by significant erosion of the bones along the ventral side of the suture (Schwenk, unpublished observations). Flexure here, however, requires concomitant flexure of the palate and sliding of the pterygoids on the basipterygoid processes. Posterior movement of the pterygoids during ventroflexion of the snout on the mesokinetic joint would tend to push the quadrates backward, depending on the tightness of this joint (see earlier discussion). In addition, mesokinetic flexure requires bending in the bones of the upper temporal arcade (e.g., postorbital, prefrontal, squamosal) lateral to the frontoparietal suture. This movement is potentially distributed along the arcade in the connective tissue articulations among bones (e.g., Arnold, 1998). Finally, some flexion of the palatal bones (both dorsoventral and lateral spreading) is also implicit. Experimental evidence for streptostyly and mesokinesis in some taxa is relatively strong, but direct evidence of metakinesis is lacking. Most of the kinetic joints of the skull are fibrous. However, the basipterygoid joint and the dorsal articulation of the quadrate bone with the paroccipital process in some species are synovial (van Pletzen, 1946; Rieppel, 1978d, 1993). The quadrate-pterygoid joint sometimes develops a cartilaginous meniscus (Oelrich, 1956) or a synovial-like space (van Pletzen, 1946). The degree of movement permitted by the latter articulation varies considerably among species (e.g., Throckmorton, 1976). The potential movements of the amphikinetic lizard skull were modeled two dimensionally by Frazzetta (1962) as a quadric crank-chain system (see Fig. 2.6 in Chapter 2). This model divides the skull into several rigid, mechanically distinct moieties that are interconnected by four joints. The model demonstrates particularly how cranial kinesis permits elevation and depression of the snout (muzzle unit) relative to the braincase. In effect, the dentigerous upper jaw can be elevated and depressed as well as the lower jaw. The model also shows how the skull can be somewhat flattened by dorsoflexion of the snout relative to the rest position (see Arnold, 1998). As noted, the specifics of some of these movements are in question. In particular, the model implies that quadrate movement is coupled to snout flexion, but experimental studies suggest that these movements can be decoupled (see later). It is increasingly evident that there is significant variation in the presence, degree, and nature of skull kinesis in lizards (e.g., Rieppel, 1993; Arnold, 1998; Schwenk, unpublished results), thus, Frazzetta's (1962) model is not universally applicable. Other models are possible (e.g..

8. Feeding in Lepidosaurs lordansky, 1996). In any case, there is no doubt that streptostyly and dorsoventral movements of the snout do occur in some lizards (see later). B. Dentition The dentigerous bones of the upper jaw are the premaxilla(e) and maxillae, and in the lower jaw, the dentaries. In addition, there are small palatal teeth in some species, typically a short, somewhat transverse row of teeth across the pterygoid in squamates and a well-developed longitudinal row along the palatine in Sphenodon (see earlier discussion). Occasionally, palatine teeth occur in squamates as well. Lepidosaurs exhibit two principal types of marginal teeth: acrodont and pleurodont (see Fig. 2.7 in Chapter 2). Acrodont teeth are ankylosed directly to the apical surface of the jaw (Figs. 8.2, 8.6C, and 8.8), whereas pleurodont teeth lie along the medial side of the tooth-bearing bone, forming a rib-like pattern (Figs. 8.3-8.5). Acrodont teeth are added posteriorly to the tooth row during growth and are worn throughout life, but are not replaced. In contrast, pleurodont teeth frequently break and, in most cases, are replaced throughout life. However, the rate of replacement sometimes slows (e.g., Mateo and Lopez-Jurado, 1997) and in some pleurodont species tooth wear is significant in older individuals (e.g., Rocek, 1980b). Acrodont teeth are characteristic of Sphenodon and the iguanian families Agamidae and Chamaeleonidae, as well as one amphisbaenian family, the Trogonophidae. All other squamates have pleurodont teeth. Curiously, the anteriormost teeth in most agamids are pleurodont and some of these are usually long and "caniniform" (e.g.. Cooper et ah, 1970). The posterior, molariform teeth in some large teiids {Dracaena, Tupinambis) have a very broad base that extends well away from the lateral margin of the dentary and mandible (e.g., Peyer, 1929; Presch, 1974; Dalrymple, 1979). These have been variously described as "subpleurodont" (e.g., Dalrymple, 1979), "subacrodont," or ''acrodont" (MacLean, 1974), but are clearly a modified type of pleurodont dentition with replacement, albeit at a reduced rate (e.g., Edmund, 1969; Dalrymple, 1979). 1. Pleurodont

Dentition

In general, upper and lower pleurodont teeth bear no special positional relationship to one another except that the lower tooth row generally fits inside the upper toothrow. As such, there is no functional requirement to maintain precise alignment between upper and lower teeth as there is in mammals (Chapters

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2 and 13). Frequent breakage and replacement of teeth along the tooth row result in a slight, but constant shifting of functional tooth position, but this has no functional consequence. Teeth are replaced in maturational waves along the tooth row called Zahnreihen (Edmund, 1960, 1969). There are two distinct types of tooth replacement in pleurodont squamates: the "iguanid method" and the "varanid method" (reviewed by Rieppel, 1978f). In the iguanid method, a replacement tooth grows into the pulp cavity of the functional tooth from below as the latter is resorbed. In the varanid method, a replacement tooth grows in an interdental position posterior to the functional tooth and no resorption is evident. The iguanid pattern is typical of most pleurodont squamates and is believed to be primitive, whereas the varanid pattern is found only in varanoid lizards and snakes. An intermediate type of tooth replacement occurs in basal anguimorphans, teiids, and some amphisbaenians. Rieppel (1978f) argued that the similarity between snakes and varanoids is superficial and suggested that similar tooth replacement methods have evolved independently in several groups. Crown shape is highly variable in pleurodont squamates, although the "typical" tooth is unicuspid and peg-like to sharp. It has been suggested that there is a fairly tight correlation between diet and crown shape in lizards (e.g., Hotton, 1955; Montanucci, 1968); however, these studies did not take into account the strong phylogenetic component of tooth crown variation. On a broad scale there appears to be little diet-related variation in crown form. The vast majority of pleurodont squamates have numerous, relatively small, unicuspid to tricuspid teeth. These tooth forms are associated with a variety of invertebrate prey types as well as some percentage of plant food (see Section III,A). However, invertebrate prey types are extremely diverse in size, hardness, and behavior, and no clear adaptive patterns emerge. Two dietary types, however, seem to promote strong adaptive modification in the teeth. In many herbivorous lizards the teeth are laterally compressed and multicuspate. The number of cusps and therefore the width of the spatulate teeth roughly correspond to the degree of herbivory (Hotton, 1955; Montanucci, 1968). Throckmorton (1976) noted the such teeth lie at a slight angle relative to the axis of the jaw and each tooth slightly overlaps the succeeding one. With the jaws closed, upper and lower tend to alternate in line. This pattern results in a clean and continuous bite to remove a section of leaf or other vegetable matter, as opposed to a series of individual punctures. This is especially evident in iguanine iguanids (Figs. 8.3D-8.3F), but has also evolved

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independently in other taxa that include a high proportion of plant matter in their diets. Second, species that consume hard food items (durophagy), such as shelled molluscs, tend to form molariform teeth at the back of the tooth row (Peyer, 1929; Dalrymple, 1979; Rieppel, 1979a; Rieppel and Labhardt, 1979; Edmund, 1969; Estes and Williams, 1984). These are typically very broad based with blunted cusps and are especially well developed in several large teiids (especially the caimen lizard, Dracaena guianensis) and the Nile monitor, Varanus niloticus, which feed frequently on hard-shelled, aquatic molluscs and crustaceans. Limited dentitional adaptation to diet may have occurred in some clades. Sumida and Murphy (1987) and Bauer and Russell (1990), for example, suggested a correlation between tooth crown form and diet in geckos. However, Sumida and Murphy (1987) offered no dietary data and their conclusions were purely speculative. Bauer and Russell (1990) argued that several dentitional types accommodate an insectivorous diet in the genus Rhacodactylus, but large, caniniform teeth in R. auriculatus and several other species are adapted to vertebrate (and other soft-bodied) prey. Limited dietary data support their view. In some lacertid lizards there is an ontogenetic change in tooth crown form that is correlated with a dietary shift (Rocek, 1980a; Mateo and Lopez-Jurado, 1992, 1997). Juveniles have a very regular tooth row with small, tricuspid teeth and eat a relatively diverse, but mostly soft-bodied diet. In adults the tooth crowns become unicuspid and caniniform and vary in size along the tooth row. Adult prey diversity is higher and hard-bodied prey predominate. Mateo and Lopez-Jurado (1997) suggested that adult dentition is adapted to puncturing tough insect cuticle. Finally, the skink-eating specialist, Lialis (Pygopodidae), has sharp, recurved teeth that can fold posteriorly due to fibrous bases (Patchell and Shine, 1986c). These modifications parallel those found in some skink-eating snakes (Savitzky, 1981) and help prevent these notoriously hard and slippery lizards from escaping the jaws' grasp. Varanoid lizards typically have very sharp unicuspid teeth that are subcorneal to flattened and slightly recurved (e.g., McDowell and Bogert, 1954) (Fig. 8.4). These are often quite snakelike in appearance. Although such tooth form is usually attributed to carnivory, most varanids primarily consume a variety of invertebrates (Losos and Greene, 1988). The teeth of varanids that include vertebrates in their diets are particularly flattened mediolaterally (i.e., bladelike) and have minute serrations along their posterior margins, or both anterior and posterior margins (e.g., Auffenberg, 1981; Greer, 1989; Abler, 1992). Similar teeth occur in the dinosaur Tyranosaurus; mechanical tests

showed that they cut through flesh like a serrated steak knife using a "grip-and-rip" mechanism (Abler, 1992). Other functional ramifications of these teeth for Komodo monitors (and other varanids) are considered in Section VI. In the only venomous lizards, Heloderma, anterior and posterior grooves occur along the length of most teeth, apparently to enhance venom introduction. These are best developed in the mandible near to the point of venom discharge and are accompanied by ridges interpreted as "cutting edges'' (Bogert and Martin del Campo, 1956). Helodermatids also frequently consume vertebrates (Pregill et al, 1986). 2. Acrodont

Dentition

The most significant aspect of acrodont dentition is that it is not replaced during life. Rather, new teeth are added during growth while existing teeth wear down (Cooper ei al, 1970; Cooper and Poole, 1973; Robinson, 1976; Throckmorton, 1979). An important functional consequence of this is the stability of tooth position and the potential for upper and lower tooth alignment, or occlusion (as in mammals; see Chapters 2 and 13). Occlusion is characteristic of agamid lizards and, to a lesser extent, amphisbaenians, but not Sphenodon. In agamids, the lower tooth row fits tightly within the upper tooth row, with upper and lower teeth alternating (Fig. 8.8). The triangular form of agamid teeth in occlusal view and the tight fit of uppers and lowers produces a cutting mechanism that has been compared to the "pinking shears" used in sewing (Edmund, 1969). Importantly, as the teeth slide past one another they are worn so that fit is enhanced and sharp cutting edges are produced. Over time wear can be extreme so that all enamel on the abraded side is worn away, exposing the pulp cavity. The pulp cavity fills with bone or calcified tissue and the bone beneath the tooth changes from cancellous to compact (Cooper and Poole, 1973; Throckmorton, 1979). As tooth wear progresses, the teeth begin to cut into the bone of the jaw, with most wear concentrated on the lower jaw. In some old individuals of Uromastix, the teeth are completely worn away, but the apical margins of the dentaries have been worn into serrations and continue to function as tooth analogues (Cooper and Poole, 1973; Throckmorton, 1979, Robinson, 1976)! Loss of the premaxillary teeth through wear creates a beak-like appearance in some Uromastix and the bony edge of the premaxilla is used to crop vegetation (Throckmorton, 1979). Such wear is not as pronounced in most other agamids, nor in chamaeleonids. Uromastix evinces two adaptations of the enamel related to tooth wear and function. First, the enamel is relatively thicker than in other agamids. Second, it is

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FIGURE 8.8. Acrodont dentition and dental occlusion in agamids and amphisbaenians. (A) Ctenophorus decresii (Agamidae) showing anterior, caniniform, pleurodont teeth and marginal acrodont teeth in lateral view. (B) Upper (white) and lower (black) tooth occlusion in Agama agama (Agamidae) in occlusal view. (C) Similar view in an acrodont amphisbaenian. (A) From Greer (1989), (B) from Cooper et al. (1970) with the permission of Cambridge University Press, and (C) after Cans (1974), with permission.

unique among living reptiles in having prismatic microstructure similar to that of mammals (Cooper and Poole, 1973). However, very few lizards have bee examined in this regard, so there may be others with similar enamel structure. The potential to develop prismastic enamel is considered a mammalian synapomorphy (Wood et ah, 1999), thus its occurrence in a lizard is of interest. Functionally, it suggests that the mechanical properties of Uromastix enamel are isotropic, i.e., the same in all direction, as opposed to the typically anisotropic nature of reptile enamel, which might suggest a greater complexity of forces acting on the teeth (Cooper and Poole, 1973). Robinson (1976) argued that streptostylic movements of the quadrates permit slight adjustments of lower jaw position to maintain precise occlusion in agamids. This hypothesis is supported by the observa-

tion of streptostyly during food processing in Uromastix, but not in the pleurodont Iguana (Throckmorton, 1976). Herrel and De Vree (1999) also documented streptostylic movements in Uromastix. However, streptostyly was not observed in Agama {Plocederma) (Herrel et al, 1996a). It is possible that precise occlusion is more important in the herbivorous Uromastix than in other acrodonts due to the necessity of cropping fibrous plant food (see Section V). In Sphenodon the acrodont teeth do not function as in agamids and occlusion does not occur. Rather, the lower tooth row fits precisely into the groove between parallel, upper tooth rows (see earlier discussion) (Fig. 8.2). During food processing, the lower jaw slides anteroposteriorly along the upper jaw (Gorniak et ah, 1982) so that food trapped between upper and lower teeth is effectively sheared. Propalineal movement is permitted by sliding of the mandible on the quadrate at the jaw joint and bending of the mandibular rami at the symphysis, and is not the result of streptostyly (Robinson, 1976). Based on limited fossil evidence, Robinson (1976) argued that the condition in Sphenodon is derived from an agamid-type pattern of acrodont occlusion. Amphisbaenians also exhibit limited dental occlusion (Fig. 8.8). This is true for both pleurodont and acrodont species (Gans, 1969a, 1974), but presumably greater opportunities for wear and the production of cutting facets are available to the acrodont trogonophids. Gans suggested that amphisbaenians use their occluding tooth rows to bite pieces out of large prey items. The bite is often accompanied by axial twisting to tear off chunks. As noted earlier, however, there are no dietary data to support this adaptive scenario (see Section VI).

C. Hyobranchial Apparatus 1. Hyobranchial Skeleton The lepidosaurian hyobranchial apparatus is exceptionally variable in form and has not been meaningfully reviewed since Fiirbringer (1922). I will not challenge this trend here. Clearly, this is an area badly in need of a comparative, phylogenetic synthesis. I suspect that a careful analysis of hyobranchial form, including microscopic anatomy and development, could provide a rich source of phylogenetically informative characters, not to mention a clearer understanding of hyobranchial function during feeding and other behaviors. The hyobranchial apparatus is the remnant of the ancient pharyngeal skeleton of tetrapods' piscine ancestors. Along with the primary (nondermatocranial)

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jaw elements and their derivatives, the hyobranchium constitutes the splanchnocranial portion of the head skeleton (see Chapter 2). Most nonophidian lepidosaurs possess a generalized hyobranchial apparatus retaining some of the ancestral patterning of the visceral arches. In lepidosaurs, as in other tetrapods, it supports the tongue and the musculature of the throat. In most species the hyobranchium lies far anterior in the buccal floor between the mandibular rami. In Varanus it is positioned farther back in the throat, posterior to the mandible (e.g.. Smith, 1986). This shift is correlated with a specialization of neck and throat morphology related to derived respiratory and display functions (Bels et al, 1995; Owerkowicz et al, 1999,2000). The entire apparatus is free-floating within the buccal and gular musculature. It is heuristically useful to describe an "archetypal" lepidosaurian hyobranchial apparatus based on its most generalized adult form (e.g., Langebartel, 1968; Rieppel, 1981a) and its development (see especially Kallius, 1901; also El-Toubi and Kamal, 1959a,b), and then consider departures from this pattern. The "archetypal" condition is roughly characteristic of Sphenodon and most iguanid, agamid, gekkonid, lacertid, and scincid squamates (Fig. 8.9). Its presence in basal lepidosaurian clades suggests that it represents the primitive condition. The generalized lepidosaurian

F I G U R E 8.9. Generalized hyobranchial apparatus (Pogona muricatus, Agamidae) shown in ventral view relative to the mandible. Stippling indicates cartilage, ap, anterior process of basihyal; bh, basihyal; cbl, ceratobranchial 1; cb2, ceratobranchial 2; ch, ceratohyal; m, mandible. After Throckmorton et al (1985), with permission of Wiley-Liss, Inc., a subsidiary of John Wiley and Sons, Inc.

hyobranchium consists of a cartilaginous hyoid body, or basihyal which lies in the ventral midline. The basihyal has three anterior, cartilaginous projections: a median lingual (entoglossal) process and paired anterior processes. The lingual process projects anteriorly into the muscular body of the tongue for one-half to threequarters or more of its resting length (Schwenk, unpublished results). A laryngohyoid ligament runs posteriorly from its middle or anterior end to the ventral surface of the larynx (Oelrich, 1954; Schwenk, 1986, 1988; see later). The anterior processes (hypohyals) project anterolaterally and dorsally. The ends of these articulate by means of fibrous joints to large ceratohyals which extend posteriorly and dorsolaterally, wrapping around the sides of the throat. Medial to these are the first ceratobranchials, which project posteriorly from the posterolateral corners of the basihyal, distally curving dorsolaterally around the throat. They are the only hyobranchial elements to be consistently ossified and they typically join the basihyal at a synovial joint. Finally, second ceratobranchials are cartilaginous extensions of the basihyal that project posteriorly, in parallel, near the midline. They are closely apposed and elongated in species with extensible dewlaps (e.g., von Geldern, 1919; Font and Rome, 1990). The ceratohyals, first ceratobranchials and occasionally the second ceratobranchials, sometimes have small, cartilaginous distal elements appended to their tips called epihyals and epibranchials (e.g.. Tanner and Avery, 1982). The basihyal, lingual process, hypohyals and ceratohyals are derivatives of the second visceral arch. The first ceratobranchials are third arch derivatives and the second ceratobranchials are fourth arch derivatives (Kallius, 1901). The most common variant of the archetypal hyobranchial form is loss of the second ceratobranchials. The remaining ceratobranchials are assumed to be the first pair because they are usually positioned somewhat laterally on the basihyal, are ossified and articulated by synovial joint to the basihyal, and serve as the origin for the hyoglossus muscles (e.g., Langebartel, 1968). Circumstantially, it is also most likely that the most posterior, fourth arch elements would be lost given the general tendency in tetrapods to reduce and lose posterior visceral arch elements first. Beyond this, the hyobranchial form is remarkably variable, as noted. Virtually all (nonophidian) taxa retain vestiges of the basihyal and entoglossal process, but all other elements are reduced or lost in various and sundry patterns. As is typical in other cranial elements, small fossorial scleroglossans show the greatest divergence in hyobranchial form with reduction and loss of elements rampant (e.g., Rieppel, 1981a). Some (e.g., the burrowing skink, Acontius) approach the highly reduced snake condition in which the hyobranchium is little more

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8. Feeding in Lepidosaurs than a Y-shaped element. The paired, posterior elements are presumed to be the first ceratobranchials. In teiids and gymnopthalmids the entoglossal process is detached from the basihyal (Beebe, 1945; Tanner and Avery, 1982; Harris, 1985). The basihyal retains the base of the process and is connected to the detached portion by a "tubular membrane" (Harris, 1985). In at least one small sphaerodactyline gecko {Gonatodes), the lingual process does not extend into the tongue, but into the floor of the mouth instead (Schwenk, unpublished results). Although most iguanians retain the archetypal hyobranchial form, chameleons have diverged significantly from this pattern (e.g., Fiirbringer, 1922; Gnanamuthu, 1930, 1937; Lubosch, 1932; Fineman, 1943; Tanner and Avery, 1982; Wainwright and Bennett, 1992a). This is not surprising in light of extensive modification of the hyolingual apparatus for ballistic tongue projection (see Section VI). The basihyal is reduced to little more than the posterior end of a robust lingual process. The lingual process is remarkable for its thickness, length, and cylindrical, parallel-sided form. The latter feature is particularly important to tongue function during projection (e.g., van Leeuwen, 1997; see later). The ceratohyals are lost, but the anterior processes remain as independent elements movably articulated with the basihyal. Robust first ceratobranchials, likewise, articulate with the minute basihyal. At rest they extend anterodorsally along the back of the skull, a position very different from other iguanians. There are no second ceratobranchials. 2. Hyobranchial

Musculature

As for the hyobranchial skeleton, hyobranchial musculature is complex and extremely variable. The extreme variation in this musculature makes generalizations difficult and the homologies of some muscles questionable. Excellent treatments of individual taxa include Rieppel (1978e) for Sphenodon, Oelrich (1956) for an iguanid {Ctenosaura), and Smith (1986) for Varanus. Reviews can be found in Camp (1923; superficial throat musculature only), Gnanamuthu (1937), Kesteven (1944), and Tanner and Avery (1982); however, evolutionary patterns remain virtually unexplored. Hyobranchial musculature is divisible into intrinsic and extrinsic components, and the latter into prehyoid and posthyoid muscles. All muscles are paired. Intrinsic muscles are those that run from one element of the hyobranchium to another. This musculature is limited in most taxa, but in Varanus and other taxa with elaborate hyobranchia it may be more extensive and complex. The principal intrinsic muscle is the ceratohyoideus (branchiohyoideus), which generally runs between the second ceratobranchial and the ceratohyal. In some

species (notably iguanines) it runs between the two ceratobranchials (Avery and Tanner, 1971). According to Tanner and Avery (1982), a stout ceratohyoideus runs from the basihyal anterodorsally to the anterior process (hypohyal), but other references do not mention this. The ceratohyoideus is innervated by the glossopharyngeal nerve (c. n. IX) (Oelrich, 1956). The principal extrinsic, prehyoid muscle is the mandibulohyoideus (geniohyoideus). There is some confusion about its name. Early authors tended to use the name geniohyoideus, which is taken from mammalian anatomy, but most recent workers prefer mandibulohyoideus, which more accurately describes the muscle in lepidosaurs. Some, however, have described both muscles in lepidosaurs (e.g., Sondhi, 1958b; Tanner and Avery, 1982). Usually, "geniohyoideus" is reserved for the most medial, longitudinal portion of the muscle. In any case, the mandibulohyoideus represents a broad series of slips originating along the posteromedial margin of the mandible and running posteriorly to the hyobranchium where fibers insert primarily onto the first ceratobranchial, but also on the ceratohyal and the second ceratobranchial. Along the way these sheetlike muscle slips often interdigitate with transverse fibers of the intermandibularis muscle running between the mandibular rami (e.g., Oelrich, 1956; see later). Fiber orientation suggests that this muscle protracts the hyobranchium (and the tongue) and abducts the hyobranchial horns. It is innervated by the hypoglossal nerve (c. n. XII), as are the lingual muscles (Oelrich, 1956). Two large posthyoid muscles attach the hyobranchial apparatus to the sternum and shoulder girdle. The sternohyoideus runs near the midline from the anterior margin of the sternum to the first ceratobranchial (e.g., Oelrich, 1954; Rieppel, 1978e). In some species, part of it originates from the clavicle and insertion can occur on the basihyal and/or ceratohyal (Tanner and Avery, 1982). A separate sternothyroideus is recognized by Tanner and Avery (1982), who suggest that in some taxa it is distinct from the sternohyoideus, but in others it is variously fused. Finally, an omohyoideus originates on the clavicle, interclavicle, and/or sternum and curves anteromedially to insert on the first or second ceratobranchia and/or the basihyal. In some species it has two heads that join anteriorly before inserting onto the hyobranchium. These muscles are innervated by motor fibers of the first spinal nerve (Oelrich, 1956). D . Jaw Musculature The jaw musculature is an ill-defined set of muscles that act directly on the jaws or which potentially affect jaw movements. These muscles can be placed into four general groups based on their innervation (and

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Kurt Schwenk TABLE 8.3 Muscles Related to Feeding Function in Lepidosaurs" Muscle group (innervation)

Connections

Muscle

Superficial throat (c. n. V, VII)

Intermandibularis ant. Intermandibularis post. Constrictor colli

Superficial transverse fibers linking the mandibular rami and forming a sling around the throat beneath the hyobranchium

Hyobranchial: intrinsic (c. n. IX)

Ceratohyoideus

links second ceratobranchial and ceratohyal, or both ceratobranchials

Hyobranchial: prehyoid (c. n. XII)

Mandibulohyoideus

Mandible to first ceratobranchial (± ceratohyal and second ceratobranchial)

Hyobranchial: posthyoid (1st spinal n.)

Stemohyoideus (+ stemothyroideus) Omohyoideus

Sternum (± clavicle) to first ceratobranchial (± basihyal, ceratohyal)

Constrictor internus dorsalis (c. n. V)

Levator pterygoideus Protractor pterygoideus Levator bulbi

Skull roof (parietal) to pterygoid Ventrolateral braincase to posterior pterygoid Braincase or skull roof to lower eyelid (or pterygoid)

Adductor mandibulae externus (c. n. V)

Levator anguli oris A. m. e. superficialis A. m. e. medialis

Upper temporal arch (lower in Sphenodon) to rictal plate at corner of mouth Upper temporal arch (± quadrate) to lateral surface of mandible Lateral surface of parietal and posterior margin of upper temporal fenestra to lateral surface of basal aponeurosis attaching to coronoid bone of mandible Posterior wall of upper temporal fenestra to posteromedial surface of basal aponeurosis

A. m. e. profundus

Clavicle, interclavicle (± sternum) to first or second ceratobranchial (± basihyal)

Adductor mandibulae internus (c. n. V)

Pseudotemporalis

Adductor mandibulae posterior (c. n. V)

A. m. posterior

Anteromedial margin of upper temporal fenestra and epipterygoid bone to basal aponeurosis and coronoid bone of mandible Ectopterygoid, pterygoid and quadrate to posterior end of mandible + retroarticular process + lateral surface of mandible Quadrate to medial surface of mandible

Lingual: "extrinsic" (c. n. XII)

Genioglossus Hyoglossus

Mandible near symphysis to tongue First ceratobranchial to tongue + intrinsic fibers in tongue

Lingual: "intrinsic" (c. n. XII)

Verticalis Transversalis Longitudinalis Circular

Unpaired: floor of tongue beneath lingual process to dorsal transverse septum From midline laterally above dorsal transverse septum At base of papillae dorsal to transversalis Surround hyoglossus bundles; confluence of transversalis and verticalis fibers

Pterygoideus

"^See text for description, and text and Tables 8.1 and 8.2 for references. All muscles are paired, except the intrinsic lingual muscle, verticalis, which lies in the midline of the tongue. Terminology primarily follows Haas (1973), with additional reference to Oelrich (1956) and Schwenk (1986).

segmental derivation) (Table 8.3): (a) the trigeminal group (c. n. V, first visceral arch) includes the adductor musculature, the constrictor internus dorsalis muscles associated with cranial kinesis, and the anterior intermandibularis muscle of the throat; (b) the facial group (c. n. VII, second visceral arch) includes the depressor mandibulae muscle and the posterior intermandibularis and constrictor colli throat muscles; (c) the hypoglossal group (c. n. XII, hypobranchial muscles), including the lingual and prehyoid muscles; and (d) a posterior group (spinal nerves) comprising the posthyoid muscles. Here I limit discussion to muscles that act more or less directly on the jaws—the trigeminal nerve musculature associated with jaw closure and cranial kinesis and the facial nerve musculature, which

serves to open the jaws and constrict the pharynx. Preand posthyoid muscles of the hyobranchium were described earlier and the lingual musculature is described later. The cervical system is also of potential importance during some feeding functions, but is not treated here. Cervical musculature was reviewed, to some extent, by Versluys (1898) and its condition in helodermatids was described by Herrel and De Vree (1999b), who correctly pointed out its importance in generating inertial feeding thrusts in some squamate taxa (see later). The cervical epaxial muscles are also undoubtedly important in elevating the cranium at the atlanto-occipital (neck) joint, both to raise the head and to elevate the upper jaw during mouth opening (see Section V).

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Haas (1973) and Gomes (1974) provided benchmark syntheses of lepidosaurian jaw musculature. Some more recent literature is listed in Table 8.1. These studies provide ample information on the extensive taxonomic variation evident in the jaw muscles, but such detail is largely beyond the scope of this review. Rather, I attempt to distill the features of the system to a form salient to interpreting feeding function. I follow primarily the terminology of Haas (1973), which is based largely on the work of Lakjer (1926). Haas (1973) provided an extensive list of muscle synonymies. 1, Muscles Innervated by the Trigeminal Nerve The traditional basis for recognizing and naming different trigeminal muscles is on the basis of their position relative to the three principal rami of the trigeminal nerve: medial opthalmic ramus, middle maxillary ramus, and lateral mandibular ramus (Lakjer, 1926; Save-Soderbergh, 1945; Haas, 1973). Nonetheless, there is significant variation in the extent to which these muscle masses are separated from one another and the extent to which they are internally subdivided. In many cases, muscles are separate at their origins but fuse distally near their insertions. Thus, patterns of splitting and fusion in the trigeminal muscles often obscure homologies of individual muscles, as they do elsewhere in the body. Furthermore, variation in the form and extent of the upper temporal arcade and fenestra among squamate taxa is accompanied by differences in muscle origin. Most of the major trigeminal adductor muscles attach to an extensive insertional tendon called the bodenaponeurosis (Fig. 8.7). The bodenaponeurosis inserts onto the coronoid bone and its vicinity on the mandible. In most taxa it extends as a sheet some distance into the muscle mass, variously separating the muscles. Table 8.3 lists the principal lepidosaurian jaw muscles based on Haas (1973). These groups are briefly described here and illustrated, in part, in Figs. 8.7 and 8.10. a. Constrictor Internus Dorsalis Group These muscles lie very deep within the skull, medial to the opthalmic ramus of the trigeminal nerve. Two are implicated in kinetic movements of the skull (e.g., Frazzetta, 1962; lordansky, 1970; Haas, 1973). A protractor pterygoideus muscle originates on the prootic and basisphenoid, including the basipterygoid process, and runs posteriorly and ventrolaterally to insert along the posterior end of the pterygoid wing (lamina). The levator pterygoideus muscle runs vertically from the ventral surface of the parietal bone, along the epipterygoid, to the pterygoid wing lateral to the protractor. These muscles are widely presunied to participate in

adms

pte

FIGURE 8.10. Superficial jaw musculature in a generalized lizard, Ctenosaura (Iguanidae). adms, adductor mandibulae externus superficialis; admm, adductor mandibulae externus medialis; ang, angular; ar, articular; cor, coronoid; dmd, depressor mandibulae; es, extracolumella (extrastapes); ju, jugal; po, postorbital; pst, pseudotemporalis; pte, pterygoideus; q, quadrate; rp, retroarticular process; sq, squamosal; sur, surangular; ty, tympanum. From Bellairs (1970).

dorsoflexion of the snout (e.g., Frazzetta, 1962; lordansky, 1970), although Smith and Hylander (1985) disputed this interpretation and suggested that they serve to resist movement at the basipterygoid joint. Ventroflexion is putatively affected by muscles of the adductor complex (e.g., Borsuk-Bialynicka, 1985). A third muscle in this group, the levator hulhi, is associated with the eyeball in most lepidosaurs, but in amphisbaenians and snakes it inserts onto the dorsal surfaces of palatine and pterygoid bones to become a functional retractor pterygoideus, in opposition to the protractor (Haas, 1973). Rieppel (1981b) noted that the levator is absent in chameleons, but that the protractor is well developed in some, with a strong head to the quadrate bone. He suggested that the latter muscle functions as a protractor quadrati, a hypothesis consistent with the fact that chameleons are akinetic but streptostylic. Due to the presence of a complete lower temporal arch, Sphenodon is presumably akinetic; however, it has been suggested that juveniles with incomplete ossification might evince some kinesis (e.g., Frazzetta, 1983). Ostrom (1962) found that the levator and protractor pterygoideus muscles were variably developed in adults and completely absent in some individuals. He suggested that individual variation reflected variation in the degree of cranial kinesis, speculating that dietary differences among individuals or populations might underlie the difference. However, there is no support for this supposition, nor any functional evidence of skull kinesis in adult tuatara (Gorniak et ah, 1982).

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b. Adductor Mandibulae Externus The external muscle group lies between or lateral to the mandibular and maxillary branches of the trigeminal nerve. It is divided into superficial, medial, and lateral portions. The superficial part is, itself, usually subdivided into at least two parts: a levator anguli oris and an adductor mandibulae externus superficialis, sensu stricto. The levator anguli oris originates on the lower temporal arcade in Sphenodon, but in squamates it has shifted to the upper arch, or from the dorsolateral fascia overlying more medial muscles in taxa with the upper arch reduced. It inserts into the tough connective tissue at the corner of the mouth called the rictal plate, or Mundplatt. The superficialis lies more or less posterior to the levator and arises primarily from a quadrate aponeurosis, running anteroventrally (slightly posteroventrally in Sphenodon) to the lateral surface of the mandible behind the coronoid bone, with some fibers occasionally inserting onto a lateral portion of the bodenaponeur osis. The adductor mandibulae externus medialis is often the largest of the temporal adductor muscles, nearly filling the temporal fossa in some taxa. It is highly variable in form due, in part, to variation in the upper temporal arcade. In general, it arises from the posteromedial portion of the upper temporal arch, or the side of the braincase, and lies lateral to the bodenaponeurosis into which it most often inserts. Occasionally it attaches along the mandible posterior to the coronoid. The adductor mandibulae externus profundus lies deep to the medialis alongside the braincase. It inserts onto the medial surface of the bodenaponeurosis, which separates it from the medialis. Some fibers take origin from the anterior surface of the quadrate and bypass the bodenaponeurosis, inserting directly into a trough in the surangular bone of the mandible (posterior to the coronoid). In some cases, fibers of the profundus arise from the posterior margin of the temporal arcade and bulge posteriorly through the posttemporal fenestra. c. Adductor Mandibulae Internus The two muscles of this group are anatomically distinct, but share innervation by the mandibular ramus of the trigeminal. The pseudotemporalis has two parts in most squamates (superficialis and profundus: lateral and medial, respectively). The superficialis is often a large muscle that lies in the anteromedial portion of the temporal fossa. It arises from the anterior portion of the parietal bone and the top of the epipterygoid and runs quite vertically to the coronoid bone and the medial surface of the bodenaponeurosis, in some cases. It is lost in gekkotans (Haas, 1973). The profundus por-

tion lies lateral to the epipterygoid bone and levator pterygoideus muscle. It originates on the ventral end of the epipterygoid, fans out as it runs posteroventrally, and has a fleshy insertion on the coronoid bone. The two parts of the pseudotemporalis are sometimes fused at the point of insertion (e.g., Oelrich, 1956). The pterygoideus (pterygomandibularis) is a complex muscle that is the largest jaw adductor in some species. It runs laterally, posteriorly, and ventrally from the ectopterygoid and pterygoid bones to the posterior end of the mandible, including the retroarticular process, which it wraps in a kind of sling. The muscular "bulb" it forms around the posterior end of the mandible is sometimes referred to as the "masticatory cushion." It is often sexually dimorphic and hypertrophied in males, giving them a characteristic "jowly" appearance. The skin overlying the muscle is sometimes associated with enlarged scales (e.g.. Iguana) or seasonally bright coloration (e.g., Eumeces), suggesting that hypertrophy of these muscles may be related to display behavior. However, there may be mechanical and ecological consequences of sexual dimorphism for feeding function as well (Herrel et ah, 1996b; Lappin and Swinney, 1999). The pterygoideus is also usually divided into superficialis (lateralis) and profundus (medialis) portions. The latter lies more dorsally and its fibers are shorter and more transverse. The agamid, Uromastix, is unique in its possession of a third pterygoideus slip (e.g., Haas, 1973; Throckmorton, 1976; Herrel et al, 1999a). The pterygoideus is complexly pinnate with a central tendon. It is also functionally complex because it acts on the mandible both anterior and posterior to the jaw joint. Its position suggests that it can function as a jaw opener as well as a jaw closer (e.g., Oelrich, 1956; lordansky, 1970; Throckmorton, 1976; Schwenk and Hall, unpublished observations) and Throckmorton (1978,1980) showed that the pterygoideus profundus is indeed active during jaw opening in Uromastix; however, it may be most important in mandibular protraction (Throckmorton, 1976, 1978). Herrel et al (1997a) and Gorniak et al (1982) also found differential activity in the pterygoideus muscle in Agama and Sphenodon, respectively. Differential fiber recruitment in portions of a single, complex muscle, as evident in the lepidosaurian pterygoideus (and other muscles), is usually viewed as a mammalian trait (see Chapter 2). d. Adductor Mandibulae Posterior This is a relatively small muscle lying deep to the adductor mandibulae externus profundus. However, it takes its origin from the quadrate bone (and, in some cases, the pterygoid and paroccipital process) and runs anteroventrally to insert on the posteromedial surface of the mandible.

8. Feeding in Lepidosaurs e. Intermandibularis Anterior A more or less continuous series of transverse fibers cover the floor of the mouth and pharynx. The most anterior of these thin muscle sheets is the intermandibularis anterior (mylohyoideus). Note that the name "intermandibularis'' is preferred over "mylohyoideus/' the latter being derived from mammalian anatomy. It runs across the floor of the buccal cavity between the mandibular rami just beneath the skin. It is somewhat arbitrary to describe this muscle separate from its serially homologous portions just posterior (described in the next section), but due to its anterior position it is derived from the first visceral arch and shares its trigeminal innervation with the adductor and internus dorsalis musculature. Contraction of the intermandibularis is presumed to elevate the floor of the mouth. 2. Muscles Innervated by the Facial Nerve a. Intermandibularis Posterior This muscle lies immediately posterior to the intermandibularis anterior and is usually separated from it by an interdigitating slip of the mandibulohyoideus (Camp, 1923; see earlier discussion). b. Constrictor Colli Posterior to the mandible and the intermandibularis, the constrictor (sphincter) colli muscle comprises a third set of transverse fibers, forming a superficial sling beneath the hyobranchium and around the pharynx. Fibers arise from the neck near the dorsal midline immediately posterior to the head. Contraction of this muscle elevates the hyobranchium and constricts the pharynx which may be especially important during swallowing. c. Depressor Mandibulae This muscle depresses the mandible and is presumed to be the principal jaw opener. However, the pre- and posthyoid muscles may contribute to jaw opening in many cases and the pterygoideus muscle is also implicated in some taxa (see earlier discussion). Like the constrictor colli muscle, which often overlies it, the depressor mandibulae is a superficial neck muscle. It originates on the posterior margin of the parietal bone and upper temporal arch at the back of the skull, and from the fascia overlying the neck at the dorsal midline. It typically forms a fan-shaped muscle that runs ventrally to insert on the retroarticular process of the mandible. Haas (1973) considered the posterior, cervical portion a separate muscle, the cervicomandibularis. The cranial part of the depressor is clearly divided in some species, notably in agamids with well-

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developed retroarticular processes, in which there is an accessory head of the depressor running from the lateral surface of the temporal arcade. Gorniak et al. (1982) identified anterior and posterior portions of the depressor in Sphenodon as indicated by different fiber lengths and orientations, but not a septal plane. Nonetheless, each portion exhibited distinct activity patterns (see later). 3. Structural and Functional Aspects of the Adductor Musculature In general, the adductor muscles of lepidosaurs are highly pinnate. Presumably this reflects the need to generate as much jaw closing force as possible given limited cranial space. By packaging more fibers in a given volume, pinnate muscles have a larger physiological cross section than parallel-fibered muscles and therefore achieve greater contractile force (Cans et al., 1985). However, muscle pinnation comes at the cost of excursion distance, i.e., the distance through which a muscle can shorten. Lizards typically exhibit reasonably large gape angles (see later), so excursion limitations imposed by highly pinnate muscles are potentially serious. Gronowski and Rieppel (1981) pointed out that there is usually a transition in adductor form from back to front that should mitigate this problem. In comparison to other tetrapods, the lepidosaurian adductor muscle mass is exceptionally subdivided. The functional, evolutionary basis for this subdivision is unclear. It is tempting to relate it to streptostyly and cranial kinesis, which endow the lepidosaurian skull with more degrees of freedom than most tetrapod skulls, thus requiring a highly differentiated musculature to control (and resist) its varied movements. However, this hypothesis is weakened by two facts: Sphenodon (and presumably ancestral lepidosaurs) lack streptostyly and kinesis but share the complex musculature, and most of the main adductors insert onto a single, large, basal aponeurosis (the bodenaponeurosis) that connects them to the mandible. Presumably this shared attachment would have the effect of summing their separate forces into a single resultant vector. Thus, anatomical complexity is not apparently mirrored in the complexity of action. However, despite a shared attachment site, the individuated muscles differ in fiber length, degree of pinnation, and angle of insertion onto the bodenaponeurosis. They therefore vary in the degree to which they are stretched during jaw opening and in their line of action at different gape angles. Anterior adductors are longest, have the most parallel fiber arrangement, and are stretched the most during jaw opening, whereas posterior adductors are the most pinnate, with the shortest fibers, and are

210

Kurt S c h w e n k

stretched the least during jaw opening. Thus there is a correspondence between effective excursion distance and degree of stretch during jaw opening such that sarcomeres of all muscles remain within their lengthtension optima. Thus, maintaining an effective bite across a wide range of gapes may be the most compelling explanation for adductor subdivision in lepidosaurs (Rieppel and Gronowski, 1981; Gans et al, 1985). A related factor is that because individual adductors differ in the histochemistry and contractile characteristics of their constituent fibers, different muscles, or portions of muscles, can be recruited differentially depending on gape angle and the type of contraction needed (see later; Throckmorton and Saubert, 1983; Herrel et ah, 1999a). Finally, it is noteworthy in this context that most snakes, with their highly kinetic skulls and jaws, lack a bodenaponeurosis (Haas, 1973), thus the "degrees of freedom" argument may be most applicable to them, if not to lizards. 4. Jaw Muscle

Histochemistry

Although squamate skeletal muscle fiber histochemistry has been well studied, most studies have considered locomotory muscles (e.g., Putnam et ah, 1980; Gleeson, 1983,1985; Gleeson and Harrison, 1986; Gleeson et al, 1980; Young et al, 1990; Mirwald and Perry, 1991). Jaw muscles have been histochemically characterized in only three lizard species (Throckmorton and Saubert, 1982; Herrel et al, 1999a). In general, three fiber types are typical of squamates: fast-twitch glycolytic (FG); fast-twitch oxidative or oxidative-glycolytic (FOG); and slow-twitch fibers (Gleeson and Johnston, 1987). Slow fibers are often identified as "tonic" fibers because they are hard to distinguish histochemically (Gleeson, 1983), but Gleeson and Johnston (1987) found that, in squamates, such muscles corresponded to slow twitch rather than true tonic fibers. FG and FOG are rapidly contracting fibers that vary in the degree to which they depend on aerobic respiration. FG fibers are very fast contracting, but fatigue rapidly. FOG fibers can sustain longer bouts of activity. Slow fibers are oxidative, can sustain long contractions, and are slow to fatigue, but they are also slow to contract. Glycolytic muscles are usually associated with rapid, powerful movements of short duration, whereas oxidative fibers are associated with sustained activity, support, and postural maintenance. Whole muscles vary in the percentage of fibers contributed by each fiber type and in their distribution within the muscle; in some muscles, fiber types are scattered or mixed throughout, but in others they are segregated into distinct "compartments." Table 8.4 summarizes known fiber type composition

TABLE 8.4 Histochemical Profile of Jaw Muscles in Lizards^ Muscle^

Species

MLAO

Tn

MAMES

Tn

MAMESA

Ua

MAMESP

Ps Ua

MAMEM

Tn Ps Ua

MAMEP MPsS

MPs? MPtS (lat) MPtP (med)

Ps Ua

Tonic FO/FOG

+ + + +

+

-

+

+ + + + + + /+ + + +

FG

Mixed

Comp

+ +

+

-

-

+

+ +

?

?

?

?

-

+

-

?

?

-

-

-

+

?

?

-

?

?

-

+

-

-

-

?

?

-

+

?

?

-

Tn Ps Ua

-

Tn Ps

+

-

+ + + +

Tn Ps

+ /+

+ /+

Tn Ps Ua

-

-

+

-

+ + +

+ + +

-

?

?

+ +

-

-

+ +

+

-

-

+

+ +

+

-

MPtE

Ua

MAMP

Tn Ps Ua

MDM

Tn Ps Ua

+ +

-

+

-

+

+ + +

-

~

?

-

?

+

-

?

?

^Muscles with a single fiber type are homogeneous. In muscles with more than one type, fibers are either mixed (Mixed) or grouped into discrete compartments (Comp). FG, fast twitch, glycolytic; FOG, fast twitch, oxidative glycolytic; Ps, Plecoderma (Agama) stellio (Agamidae); Tonic, tonic, oxidative (or possibly slow twitch, oxidative); Tn, Tupinambis nigropunctatus (Teiidae); Ua, Uromastix aegyptius (Agamidae). Data for Tupinambis from Throckmorton and Saubert (1982); data for both agamids are from Herrel et al. (1999a). ^Muscle names in listed order: MLAO, levator anguli oris; MAMES, adductor mandibulae externus superficialis (unspecified); MAMESA, a. m. e. superficialis anterior; MAMESP, a. m. e. superficialis posterior; MAMEM, a. m. e. medialis; MAMEP, a. m. e. profundus; MPsS, pseudotemporalis superficialis; MPsP, pseudotemporalis profundus; MPtS, pterygoideus superficialis (or lateralis); MPtP, pterygoideus profundus (or medialis); MPtE, pterygoideus externus; MAMP, adductor mandibulae posterior; MDM, depressor mandibulae.

of lizard jaw muscles. In most respects the jaw muscles are histochemically similar to other squamate muscles. All three fiber types have been identified and exist in varying proportions in different muscles (note that numbering of fiber "types 1, 2, and 3 " does not correspond between Throckmorton and Saubert (1982) and Herrel et al (1999a). However, Throckmorton and

8. Feeding in Lepidosaurs Saubert (1982) found that their "tonic'' fibers were less oxidative than in lizard locomotory muscles and that their fast-twitch oxidative fibers lacked a glycolytic capacity, so they classified them FO rather than FOG. Some muscles are composed of a single fiber type, whereas others have two or three fiber types that are either mixed or compartmentalized. Both studies found that compartmentalized muscles are divided into an inner oxidative and an outer glycolytic region. In Tupinambis the glycolytic regions comprise only FG fibers, but the oxidative compartments are a mixture of two or three fiber types (Throckmorton and Saubert, 1982). Herrel et ah (1999a) found a similar pattern in two agamid species with the exception that no more than two fiber types were ever found within a single muscle. Interestingly, no FG fibers were identified in any Uromastix muscles. A perusal of Table 8.4 reveals a high degree of variation in muscle fiber composition both among species and among muscles, rendering generalizations impossible. One notable similarity is that the pseudotemporalis superficialis comprises a single fiber type in all three species (FOG in the agamids and FG in the teiid). This muscle is also one of the most anterior adductors with long, nearly parallel fibers that insert almost perpendicularly onto the mandible in most species (see earlier discussion). The predominance of fast-twitch fibers with high glycolytic capacity in this muscle suggests its importance in generating rapid, powerful jaw closure with the mouth fully open. This muscle may be responsible for the initiation of fast close during a gape cycle (see Section V). In any case, the high degree of histochemical variation among muscles suggests the possibility of differential fiber recruitment during a feeding sequence, supporting the functional specialization hypothesis of adductor subdivision discussed earlier (Throckmorton and Saubert, 1982). E. Tongue Schwenk's (1988) study is the most phylogenetically comprehensive overview of lepidosaurian tongue morphology to date, but its focus is on phylogenetically informative characters, thus it does not review some aspects of tongue form. Comparative studies more limited in taxonomic scope include Sewertzoff (1929), Gnanamuthu (1937), de la Cerna de Esteban (1965) and Tanner and Avery (1982). A reasonably full set of references is listed in Tables 8.1 and 8.2, but key sources include Sphenodon (Schwenk, 1986); Squamata: Iguanidae (Oelrich, 1956; McDowell, 1972; Schwenk, 1988; Delheusy et al, 1994); Agamidae (Gandolfi, 1908; Sewertzoff, 1929; Gnanamuthu, 1937; Schwenk, 1988; Smith, 1988; Herrel et al, 1998c, 1999a); Chamaeleoni-

211

dae (Gnanamuthu, 1930, 1937; Lubosch, 1932; Bell, 1989); Amphisbaenia (de la Cerna de Esteban, 1959; Schwenk, 1988); Gekkota (Zavattari, 1909; Sewertzoff, 1929; Gnanamuthu, 1937; Ping, 1931; Schwenk, 1988; Schwenk and Rehorek, in preparation); Scincomorpha (Sewertzoff, 1929; Gnanamuthu, 1937; de la Cerna de Esteban, 1965; Schwenk, 1988); and Anguimorpha (Sewertzoff, 1929; Sondhi, 1958b; McDowell, 1972; Smith, 1986; Schwenk, 1988; Smith and MacKay, 1990; Tobeau et al, 1994). Due to radical variation in superficial form (Fig. 8.11), the lepidosaurian tongue has provided a historically important source of characters for systematic studies (Camp, 1923; Schwenk, 1988, and references therein). Although highly variable overall, tongue form is nonetheless conservative within higher taxa so that families tend to be relatively uniform and well differentiated one from another. This pattern of variation is significant for feeding studies because it indicates that tongue evolution is not tied to ecological radiations within groups, but rather reflects deeper-level divergences. As such, tongue anatomy is practically uncorrected with diet (Schwenk, 1988), a surprising pattern given its centrality to feeding function (some exceptions are noted later). Lingual diversity also reflects the tongue's essential role in vomeronasal chemoreception. These patterns are discussed further in Section VII. 1. Superficial Form In most taxa the tongue at rest fills the oral cavity (exceptions are the varanids and snakes). It lies within a depression in the floor of the mouth that is bordered laterally by mucosal ridges (sublingual plicae) containing the sublingual salivary glands. These converge anteriorly and the tongue tip usually rests on or between them. Sublingual plicae are extremely well developed in agamids so that the tongue appears to lie within a deep well (Schwenk, unpublished observations), but they are lacking in most gekkotans (Schwenk, 1988; Filoramo and Schwenk, 1998, in preparation). In most iguanians and gekkotans, the tongue is relatively broad and short with a wide, rounded apex and wide base that extends posteriorly on each side of the larynx as two lobes called the posterior limbs (McDowell, 1972) (Figs. 8.11d, 8.11f, and S.llg). The posterior limbs are lost in chamaeleonids, some teiids, and some varanoids, usually in conjunction with development of a lingual sheath. In many squamates the foretongue tapers significantly so that the tongue is triangular in shape. This is especially true in autarchoglossans where the foretongue is often very slender. In many scincomorphans the hindtongue is reduced as well. In

212

Kurt Schwenk

FIGURE 8.11. Superficial form of the tongue in squamates (dorsal view), (a) Xantusia (Xantusiidae), (b) Abronia (Anguidae), (c) Podarcis (Lacertidae), (d) Coleonyx (Gekkonidae), (e) Varanus (Varanidae, (f) Gonocephalus (Agamidae), (g) Crotaphytus (Iguanidae), (h) Cnemidophorus (Teiidae), (i) Cordylus (Cordylidae), and (j) Dasia (Scincidae). From Schwenk (1995b), with permission.

varanids, the tongue is extremely narrow and parallelsided (Fig. S.lle). It is withdrawn into a sheath anterior to the larynx and is superficially similar to snake tongues, but is histologically distinct (Schwenk, 1988; Smith and MacKay, 1990). In snakes the lingual sheath and overlying larynx are situated far forward in the floor of the mouth so that the tongue at rest is completely covered except, perhaps, for the very tips. The anterior position of the larynx and glottis in snakes presumably permits respiration during the sometimes slow process of consuming very large prey. In contrast, the sheath and larynx in varanids lie posteriorly in a more typically lepidosaurian position, and at rest a substantial part of the tongue is evident lying in the floor of the mouth. It is convenient to divide the tongue into anterior and posterior portions referred to as the "foretongue" and "hindtongue," respectively, due to the potentially different morphological and functional attributes of each. However, the shape and extent of the tongue's mucosal surface provide only a partial picture of its

full extent. Some lingual musculature extends posteriorly beneath the oral mucosa to the hyobranchium, and virtually all other oral landmarks, such as the position of the larynx or the insertion point of the genioglossus muscle, potentially vary among species. Therefore, foretongue and hindtongue are descriptive terms that do not necessarily imply precise homologies among taxa. To a first approximation they represent comparable regions in most species, but in taxa with highly modified tongues, such as snakes, varanids, and chamaeleonids, comparisons are most problematic. The tongue tip is highly variable in form (Schwenk, 1988,1994e, 1995). It is rounded and uncleft in Sphenodon, some chameleons (Schwenk, unpublished results), and reportedly in Dibamidae (Greer, 1985; however, unpublished data suggest a slight notch in Dibamus). In all other squamates it is variously bifurcate: in iguanians, gekkotans, and some scincomorphans it is slightly notched; in most scincomorphans it is significantly cleft, and in the lacertoids, especially teiids, it is forked. The tongue is deeply forked in amphisbaenians and angui-

8. F e e d i n g in L e p i d o s a u r s

morphans show a morphocline from modestly cleft to deeply forked (McDowell and Bogert, 1954; Schwenk, 1994e). The presence of a forked tongue is tightly correlated with the ability to follow scent trails using the vomeronasal system mediated by tongue flicking (Schwenk, 1994e). The tongue tips in most species are underlain by thickened, keratinous pads (ventral pallets) that in notch-tongued forms rest on top of the sublingual plicae (Fig. 8.12B). In most fork-tongued forms the pallets curl around to the dorsal surface and are drawn out into long tines (McDowell, 1972) (Fig. S.llh). In varanoids the ventral pallets are not evident, al-

213

though they occur in basal anguimorphans. There is often a striking, male-female correspondence between the form of the tongue tip and the mucosal surface of the palate around the vomeronasal fenestrae. The tongue is free anteriorly and along its lateral margins. The posterior limbs are sometimes slightly undercut so that they are partially free of the buccal floor as well. The foretongue is attached to the floor of the mouth by a frenulum, which contains the genioglossus muscles (Fig. 8.12B). The point of attachment of these muscles determines the extent of the free part of the tongue anteriorly. However, this is deceptive because the foretongue is nearly always capable of some hydrostatic elongation, the extent of which is determined by histological features. Thus the degree of lingual liberation from the buccal floor is only roughly correlated with protrusibility in life. 2. Surf ace Morphology

B

F I G U R E 8.12. (A) Transverse section through the foretongue of an iguanid lizard {Stenocercus sp.) showing the deep, muscular corpus of the tongue typical of iguanian lizards and its crown of long, glandular, filamentous papillae. The curved arrows indicate the dorsal transverse septum, and the small, straight arrow points to the origin of the laryngohyoid ligament dorsal to the lingual process. (B) Midsagittal section through the tongue of an agamid Hzard {Agama hispida) showing the kinked apex of the lingual process within the tongue and the extent of the laryngohyoid ligament. Note the reticular papillae and the penetration of lingual glands into the tongue musculature of the foretongue. The tongue tip on each side is underlain by a thick, lightly keratinized epithelium forming the ventral pallet. Small, straight arrows indicate the laryngohyoid ligament (which passes out of the plane of section posteriorly). The dark, longitudinal line demarcating the dorsal extent of the verticalis fibers is the dorsal transverse septum, g, genioglossus; h, hyoglossus; 1, larynx; m, mandible; p, lingual process of hyobranchium; t, transversalis; v, verticalis.

In all lepidosaurs except snakes and varanids (and the foretongue of Lanthanotus) the tongue's dorsum is papillose. Basal snakes retain some papillae along the lateral margins of the tongue (McDowell, 1972). Schwenk (1984,1988) identified several types of papillae, but the homology of similar papillary forms in different taxa is not certain. The following descriptions are based primarily on Schwenk (1988) and extensive unpublished data. Sphenodon and iguanids are characterized by long, filamentous papillae on the foretongue that are densely covered by a simple epitheliumi of columnar mucous cells, except at the tips (Figs. 8.12A and 8.13A). In general the papillae at the tongue tip are low and squat, but they rapidly become long and slender across the foretongue before shortening and thickening again toward the hindtongue and the posterior limbs. The posterior limbs often have large, conical papillae that point posteriorly. The papillary apices vary among taxa and across the tongue's surface (Fig. 8.14). Anteriorly they are covered by a stratified, squamous epithelium perforated by numerous taste buds (Schwenk, 1985). On the foretongue where they are longest, papillae are often capped by a stratified squamous epithelium, but in many iguanids, especially anoloids, sceloporines, and some tropidurines (Schwenk, 1984,1988, unpublished results), as well as some agamids (Herrel et ah, 1998c), the apex of each papilla is covered by a bizarre, pseudostratified epithelium in which the nucleated cell bodies hang free, tethered to the papillary apex by a slender stalk! Each so-called "plumose'' papilla (Rabinowitz and Tandler, 1986; "arborate" papillae of Schwenk, 1984) ends in a tuft of these free-floating cells (Figs. 8.13A and 8.14B). The distribution of plumose

Kurt Schwenk

their lengths to create a spongelike form (Fig. 8.12B). The intervening crypts are lined by a glandular epithelium and the papillary apices are most often squamous, but are dramatically plumose in anoles and some agamines. Reticular papillae are restricted to a narrow zone of the foretongue in anolines, but they often extend well onto the hindtongue in agamids. Variation in papillary height along the length of the tongue is similar to the iguanid condition. Stout, conical papillae on the posterior limbs are often particularly well developed in agamids. Uniquely in some agamids, glandular crypts penetrate deeply into the musculature of the foretongue (Gandolfi, 1908; Gnanamuthu, 1937; Smith, 1988; Schwenk, unpublished results) (Fig. 8.12B). There is taxonomic variation in this trait and in the particular muscles invaded, but too few species

F I G U R E 8.13. (A) Parasagittal section through the foretongue of an iguanid lizard {Sceloporus occidentalis), anterior to the left. Note the long, filamentous papillae crowned with plumose cells. Papillae are longest in the contact zone (cz). (B) Parasagittal section through the tongue of a gecko {Gonatodes antillensis), anterior to the right, showing the low-profile, scale-like papillae and the intrinsic origin of some hyoglossus fibers (arrows). Sublingual salivary glands are evident beneath the tongue to the right, cz, contact zone; G, genioglossus; H, hyoglossus.

papillae on the tongue corresponds to the area of prey contact during lingual ingestion (see later). Posteriorly the epithelium reverts to a stratified squamous type or sometimes an unusual, cuboidal type, as in Sphenodon (Schwenk, 1986). The lingual epithelium is never keratinized, except very lightly, in some cases, on the ventral pallets. The "typical" papilla contains collagenous connective tissue fibers that run its length, muscle fibers, and a vascular loop; however, some filamentous papillae are so slender they appear to contain nothing more than collagen fibers (although some vascular supply would seem to be necessary). Posteriorly, the papillae become increasingly inclined toward the pharynx, particularly on the posterior limbs, although this is not always evident. Agamids, chamaeleonids, and anoline iguanids possess a unique form of reticular papillae in which it appears that filamentous papillae are anastomosed along

F I G U R E 8.14. Scanning electron micrographs of the lingual surface in two iguanid lizards. (A) Papillary apices on the hindtongue of Sceloporus occidentalis. Note the relatively smooth epithelium at the ends of some papillae and the transition to plumose cells in others. Scale bar: 34 /xm. (B) Papillary apices in contact zone of the foretongue in Callisaurus draconoides showing extensive development of plumose cells. Individual papillae are difficult to discern. Anterior is to the top. Scale bar: 19 [xrcv.

8. Feeding in Lepidosaurs have been examined to deduce phylogenetic patterns. Gekkotans and xantusiids have unique, short, peglike papillae across the broad, spatulate surface of the foretongue (Figs. 8.11a and 8.lid). These are nonglandular, filled by large vascular sinuses and are very lightly keratinized. They form an exceptionally smooth pad that demarcates precisely the part of the tongue used in eye wiping (Schwenk et ah, manuscript in preparation). Posteriorly there is a sharp transition to long, glandular, filamentous papillae (although these remain quite short in diminutive gekkonids). On the posterior limbs these fuse progressively into transverse lamellae called lingual plicae. In xantusiids, the transition is from the peg-like papillae directly to lingual plicae so that virtually the entire hindtongue is plicate. Although the anterior papillae are perpendicular (i.e., normal to the tongue surface), the posterior papillae and plicae become imbricate posteriorly. Dibamids have a unique surface form of narrow transverse ridges that are slightly imbricate, but these

fMf

T^f}

M

215

are quite different from the lingual plicae of other taxa. The epithelium itself is aglandular, but deep glandular crypts penetrate into the tongue and open to the surface in the grooves between ridges, almost creating the appearance of reticular papillae. Scincomorphans and amphisbaenians never possess filamentous papillae, although in some cordylids the papillae can become quite long. Scincomorphan papillae typically have broad bases and flat apical surfaces that are imbricate posteriorly, most often taking the form of scales that are superficially similar to integumental scales (Figs. 8.15A and 8.16). On the lateral margins of the foretongue and across the hindtongue the scales often fuse into lingual plicae. The ventral surface of the foretongue in teiids is also plicate (Harris, 1985). Amphisbaenians lack plicae and the tongue is entirely scaled. Glandular epithelia are restricted to the crypts between scales and plicae in the hindtongue (nicely shown by von Seiller, 1892), but the amphisbaenian tongue is entirely aglandular, a condition found elsewhere only in snakes and varanids, which lack lingual papillae. The apical epithelium is a broad, flat expanse of stratified squamous cells that is lightly keratinized. The posterior margins of lingual scales are smooth, as in teiids (Fig. 8.16B), or scalloped, as in scincids and cordylids (and sometimes lacertids; e.g., Iwasaki and Miyata, 1985) (Fig. 8.16A). In cordylids the marginal projections are sometimes long and finger like. Anquimorphans are characterized by a bipartite, or diploglossan tongue (e.g., McDowell and Bogert, 1954; McDowell, 1972). The foretongue is often described as "retractile" within the hindtongue, but this is not accurate. Rather, the foretongue is specialized for hydrostatic elongation while the hindtongue is not (Schwenk,

B

FIGURE 8.15. Transverse sections through the foretongues of two scleroglossan species. (A) Cnemidophorus tigris showing lowprofile, scale-like papillae. Note the smooth, flat surface and the lack of a glandular epithelium between papillae. (B) Varanus indicus showing the absence of papillae and extreme reduction of the tongue. The hyoglossus muscle bundles are surrounded by a thick circular fiber system (arrows) implicated in hydrostatic elongation of the tongue. Compare to the iguanid shown in Fig. 8.12A. DL, dorsal longitudinal muscle fibers; H, hyoglossus.

FIGURE 8.16. Scanning electron micrographs of scale-like papillae in two scleroglossan species. (A) Scincella sp. (Scincidae) showing the broad, flat, smooth surface of a single papilla. Scale bar: 18 /nm. (B) Similar papillae in a teiid, Cnemidophorus tigris. Scale bar: 91 jmrn.. Anterior is to the top in both figures.

216

Kurt Schwenk

unpublished observations). As such, the foretongue is capable of considerable hydrostatic length change by the modulation of tongue diameter. Thus elongation and shortening are localized within the foretongue and there is no actual retraction, or telescoping, of the foretongue into the hindtongue. However, there is both an obvious break point in papillary form on the dorsal surface and a zone of epithelial folding laterally and ventrally to accommodate the length change, thus the foretongue appears superficially to be in a retracted state at rest. In other scleroglossan taxa, hydrostatic length change is more evenly distributed along the length of the tongue without a sharp transition zone. A consequence of the bipartite tongue form is a transition in papillary form along the length of the tongue. The foretongue is always relatively smooth, with very low-profile papillae or none at all (as in Lanthanotus and varanids). These are flat and squat anteriorly, but become progressively peg-like posteriorly. They are aglandular and have a lightly keratinized, stratified squamous epithelium. Proceeding posteriorly, they become slightly pointed and slightly imbricate. At the foretongue-hindtongue junction, there is a sudden transition to tall, filamentous, highly glandular papillae. These are typically capped by a sharply pointed, posteriorly directed epithelial apex. Posterior papillae are broad and conical. Thus, the bipartite tongue is divided into a highly extensible foretongue used exclusively for tongue flicking and vomeronasal chemoreception, and a papillose, glandular hindtongue used to support and manipulate prey items in the mouth (see Section VII,D). Although this division of labor is typical of most scleroglossans, its functional and morphological sharpness is unique among squamates. In varanids, the hindtongue is putatively lost and modified into the lingual sheath (McDowell, 1972; Schwenk, 1988). The remaining tongue is devoid of papillae and is covered by a thin, lightly keratinized epithelium (Filoramo and Schwenk, manuscript in preparation) (Figs. 8.11e and 8.15B). The histochemistry of the lingual glandular epithelium in lepidosaurs has been studied most extensively by Gabe and Saint Girons (1969) and more recently by Taib and Jarrar (1985a,b, 1986). Iwasaki (1991) and Rabinowitz and Tandler (1991) provided data on the ultrastructure of lingual glands with some indication of secretory product. In general, lingual mucocytes are serous, mucous, or bipartite (mucoserous or seromucous) (Gabe and Saint Girons, 1969). Mucous cells vary in their chemical constituents (Taib and Jarrar, 1985a,b, 1986). Only agamids and iguanids have purely serous cells on the foretongue (Gabe and Saint Girons, 1969; Rabinowitz and Tandler, 1991) and in Sphenodon they are mucoserous. Because these are all lingual feeders, it is tempting to relate the copious secretion of serous

fluids to the biomechanics of lingual prey adhesion (see later). Unfortunately, the functional attributes of the different secretory products are completely unknown. Furthermore, some scleroglossans also have mucoserous cells and the lingual feeding chamaeleonids have seromucous secretions. All we can say is that all lingual feeders have some serous secretion on the foretongue and none exhibit pure, mucus secretion here, as found commonly in scleroglossans. In most taxa the histochemical profile of secretory cells varies along the length of the tongue with the hindtongue being predominantly mucus secreting. 3. Connective Tissue

Organization

As described previously, in most taxa the muscular corpus of the tongue is penetrated to a varying extent by the lingual process, a hyaline cartilage rod continuous with the basihyal posteriorly. The anterior extent of the lingual process is greater in iguanians than in scleroglossans. In most species it is attached to the cricoid cartilage of the larynx by a laryngohyoid ligament (Oelrich, 1956; Schwenk, 1988) (Fig. 8.12). This ligament arises from near the anterior end of the lingual process in most iguanians, but farther posterior in others. In the former case it is often associated with a dorsoventral "kink" in the tip of the lingual process (Schwenk, unpublished observations) (Fig. 8.12B). The ligament runs posterodorsally through the verticalis musculature (later) to insert into the connective tissue matrix beneath the larynx in the midline. In some scleroglossans the posterior end of the ligament branches before it attaches to the larynx (Schwenk, 1988). Beneath its mucosal surface, the tongue is covered by a thin "tunic" of connective tissue fibers that appear to be entirely collagenous. There is so far no evidence for organized fiber winding (e.g., cross-helical arrays) around the tongue as is often found in muscular hydrostats, but this has not been examined explicitly. Smith (1986) implied helical winding of superficial fibers in Varanus (where one might most expect it), but did not provide supporting data. In a mammal (opossum), fibers of the lingual tunic form a "feltwork" that is highly elastic (Schwenk et ah, manuscript in preparation), and presumably this is the case in most lepidosaurs as well. The viscoelastic nature of the tunic allows stretching during elongation and shape change and may help restore the tongue to its resting conformation by elastic recoil. Various septae partition the tongue musculature internally. In Sphenodon the central core of the tongue is occupied by the verticalis musculature and is divided by a median septum (Schwenk, 1986). This is separated into dorsal and ventral parts where the lingual process penetrates the tongue. In all squamates there is partial

8. Feeding in Lepidosaurs or complete loss of this septum. It is complete in the posteriormost portion of the verticalis in some agamids (Gnanamuthu, 1937; Schwenk, 1988; Smith, 1988) and nearly complete in Varanus (Smith, 1986). In most squamates, however, the verticalis is undivided and its fibers cross the midline. There is usually a tiny, dorsal component of the median septum above the verticalis that serves as the point of origin for the transversalis fibers. In Sphenodon and most squamates, a dorsal transverse septum runs across the top of the tongue above the hyoglossus bundles and the verticalis (Fig. 8.12A). Longitudinalis and transversalis fibers run above it. In most squamates this septum is very short and, together with the dorsal bit of median septum noted earlier, it forms little more than an inverted "T.'' The transverse septum is absent in gekkotans, anguimorphans, some scincomorphans, and Dibamus. A ventral transverse septum is evident in Sphenodon, but not in squamates. 4.

Musculature

All lepidosaurs possess a highly mobile, muscular tongue, a trait they share with mammals and a few other tetrapods (Chapter 2). The functional complexity of lingual movement and shape change is underlain by extreme complexity in muscle fiber architecture. Recall that the tongue is essentially a solid mass of muscle without bones and joints to direct its movements. Some of these movements are affected extrinsically by muscles that literally pull the tongue forward or backward, but some movement, especially shape and length change, is generated intrinsically by means of a muscular hydrostatic mechanism (Kier and Smith, 1985; Smith and Kier, 1989; see Chapter 2). Muscular hydrostats usually have complex muscle architecture, the function of which is not necessarily intuitive given a traditional notion of musculoskeletal function. In lepidosaur tongues, muscle fiber architecture is sometimes so complex it defies precise description and authors sometimes disagree in their accounts. Fiber systems often interlace in intricate ways so that it is difficult or impossible to characterize discrete, individual muscles within the tongue. Thus most published descriptions of tongue muscular anatomy represent rather egregious simplifications. Tetrapod tongue muscles are classified as either ''extrinsic" or "intrinsic." The former are said to originate outside the tongue and to insert within it, whereas the latter are said to lie completely within the tongue. Several authors have suggested that this distinction is not always clear within the lepidosaurian tongue (e.g., Sondhi, 1958a,b; Smith, 1988). Schwenk (2000a) showed that nominal extrinsic muscles often have a large intrinsic component and that nominal intrinsic

217

muscles sometimes have an extrinsic component. He suggested that it was more accurate to talk about "fiber systems" within the tongue than discrete muscles. The complexity of fiber systems within the tongue manifests its functional nature as a muscular hydrostat and suggests that the tongue is best regarded as a "functional unit" not easily atomized into separate parts (Schwenk, 2000b). Nonetheless, for organizational clarity and historical continuity, I maintain the traditional distinction between extrinsic and intrinsic muscles here, but qualify muscle descriptions with more accurate accounts of their constituent fibers where known and appropriate. a. Extrinsic Muscles There are two, paired extrinsic muscles in lepidosaurian tongues. The genioglossus runs posteriorly from the mandible near the symphysis to insert on the ventral and lateral sides of the tongue (Figs. 8.12 and 8.13B). It is regarded as a protractor of the tongue (but see later). The genioglossus lies within the "frenulum" that attaches the tongue to the floor of the mouth. It is usually divided into two portions: a genioglossus medialis lies near the midline and inserts into the ventral side of the tongue. Its anteriormost fibers usually curl sharply anterior at the point of entry and run some distance forward along the ventrolateral surface of the tongue. In Sphenodon they reach nearly to the tongue tip and are undoubtedly an important tongue retractor (Schwenk, 1986). A genioglossus lateralis inserts into the tongue farther posterior. Its fibers run posterodorsally, forming the lateral wall of the hindtongue. In scincids and cordylids, some fibers of the lateralis also turn anteriorly and run into the foretongue lateral to the hyoglossus bundle (Schwenk, 1988). In scincids these fibers form a discrete bundle, but in cordylids they are diffuse. Fibers of the lateralis sometimes insert into the floor of the mouth as well (e.g., Schwenk, 1986; Bell, 1989). A genioglossus internus is found in agamids (Smith, 1988) and anoline iguanids (Schwenk and E. Williams, unpublished results). It lies medially and inserts into the tongue anteriorly along the ventral midline between the hyoglossus bundles. The genioglossus varies among taxa in its posterior point of attachment (e.g.. Smith, 1984). Generally, the farther posterior it inserts the greater the amount of foretongue extension possible. Scleroglossans usually exhibit relatively more posterior genioglossus attachment than iguanians due to their heavier reliance on extensive tongue protrusion for chemosensory tongue flicking. However, in the myrmecophagous iguanian genus Phrynosoma, the genioglossus lateralis remains detached from the side of the tongue until it reaches the posterior limbs (Schwenk, 1994c; in preparation). The hindtongue is therefore narrow in comparison

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Kurt Schwenk

to related taxa, and genioglossus lateralis muscles form large ridges alongside the tongue until they join with it posteriorly. Presumably this is an adaptation for increasing tongue protrusion distance for lingual feeding—Phrynosoma has one of the longest relative protrusion distances measured in an iguanian during ingestion (Schwenk and Throckmorton, 1989). In Varanus, the genioglossus medialis attaches far back on the tongue at its origin on the hyobranchium (Gnanamuthu, 1937; McDowell, 1972; Smith, 1986). The genioglossus lateralis is reduced to a tiny slip that inserts into the lingual sheath. In chameleons, medial fibers of the genioglossus insert into the buccal floor ventral and lateral to the tongue (medialis?) and small lateral slips insert into the mucosa overlying the back of the tongue (lateralis?) (Gnanamuthu, 1930; Bell, 1989), which, in effect, constitutes a lingual sheath. The hyoglossus muscle arises as a broad sheet along the first ceratobranchial of the hyobranchium and runs forward into the corpus of the tongue alongside the lingual process (Figs. 8.12A, 8.13B, and 8.15). It is the principal tongue retractor. Within the tongue the paired hyoglossus muscles form two cylindrical or subcylindrical columns of mostly longitudinal fibers running nearly to the tongue tip. They constitute the bulk of the tongue's volume. For most of their extent within the tongue they are separated medially by the lingual process and the intervening fibers of the verticalis system (below) (Figs. 8.12A and 8.15). Each bundle is usually very deep, occupying most of the tongue's vertical height, although in some taxa there is a reasonably thick layer of intrinsic musculature dorsally between it and the base of the papillae. Sondhi (1958a,b) suggested that hyoglossus fibers in Varanus turned and twisted within the tongue to form the various intrinsic muscles, although Smith (1986) did not agree. She found that hyoglossus fibers are oblique rather than longitudinal and suggested that they form a spiral along the bundle. Schwenk (2000a) showed that in most squamate taxa each hyoglossus bundle is clearly subdivided into two or more zones that differ in fiber orientation and that the pattern of this subdivision changes along the length of the tongue. Subdivision is least evident anteriorly. Sagittal sections reveal that, minimally, the lizard hyoglossus comprises an extrinsic component that arises from the hyobranchium and an intrinsic component that arises within the hindtongue from the dorsal transverse septum (Fig. 8.13B). Intrinsic fibers loop anteroventrally, becoming confluent with extrinsic fibers anteriorly as they curve anterodorsally into the foretongue (Schwenk, 2000a). Where they join the fibers are essentially longitudinal, but posteriorly their orientation is variable, accounting for the internal subdivision.

Gekkotans share a striking pattern of hyoglossus form in which the paired bundles split once or several times to produce multiple, longitudinal bundles in the foretongue (Schwenk, 1988). These are visible externally as longitudinal ridges along the tongue's ventral surface and presumably are related to hydrostatic control of the broad, spatulate foretongue during eyewiping behavior (Schwenk et al, manuscript in preparation; see discussion of lingual papillae). Limited subdivision of the hyoglossus bundles occurs in some anguids as well (Edgeworth, 1935; Smith and MacKay, 1990). In Dibamus (Schwenk, 1988) and two of three species of amphisbaenian studied {Amphishaena, Anops; de la Cerna de Esteban, 1959), there is a medial bundle of the hyoglossus that runs along with the lingual process {hyoglossus medialis and perientoglossus, respectively). There are slight differences in the anatomy of these muscles so their homology is uncertain (Schwenk, 1988). In chameleons the hyoglossus is greatly elongated to accommodate the travel of the tongue during projection and at rest it is kinked into accordion-like folds. It attaches to the lateral surface of the accelerator muscle (see later), but a histologically distinct portion extends anteriorly to insert beneath the glandular surface, which is folded and invaginated at rest [Lubosch, 1932; Bell, 1989; Schwenk, unpublished results; Gnanamuthu (1930) and Bell (1989) considered the latter part a separate muscle, the longitudinalis linguae]. In the foretongue of some agamids, the hyoglossus muscle is perforated by glandular crypts that penetrate from the surface (see earlier discussion). Although not a lingual muscle strictly speaking, the mandibulohyoideus is closely allied with the tongue physically and developmentally. It forms longitudinal bundles or sheets beneath and lateral to the genioglossus muscles. As noted earlier in the description of hyobranchial musculature, in most squamates it comprises multiple, sheet-like slips that arise along the mandibular rami and run posteromedially to the hyobranchium. However, it is also true that there is usually a particularly well-developed medial pair of bundles with longitudinal fibers that arise from the mandible near the symphysis and therefore most closely approximate the mammalian notion of a true geniohyoideus muscle. h. Intrinsic Muscles The verticalis fiber system lies in the midline of the tongue surrounding the lingual process of the hyobranchium and completely separating the hyoglossus bundles in squamates (Figs. 8.12 and 8.15). Verticalis fibers arise from the lingual tunic at the floor of the tongue and insert dorsally into the transverse septum. In Sphenodon, however, the hyoglossus bundles are

219

8. Feeding in Lepidosaurs quite triangular in transverse section and throughout most of the tongue their upper corners meet in the midline above the verticalis, separating it from the transverse septum (Schwenk, 1986). Verticalis fibers insert, instead, on the median septum. This is also the case in the "ring" portion of the verticalis in some agamids, which retains a complete median septum. In gekkotans and anguids with multiple hyoglossus bundles in the foretongue, there is no discrete verticalis. Rather, vertical fibers run from the dorsum and form a loop or sling around each hyoglossus bundle. In most squamates, verticalis fibers take a curving path from the ventral surface on one side, around the lingual process and vertically on the opposite side. Thus fibers from both sides cross and interlace. In some (agamine) agamids, the posterior end of the verticalis is hypertrophied into a muscular sleeve that completely surrounds the lingual process. These fibers run circumferentially from ventral median septum to dorsal median septum, forming a sphincter-like arrangement, hence this portion of the verticalis has been called the "ring muscle" (e.g., Gandolfi, 1908; Smith, 1988). In chameleons the verticalis is extremely modified into a muscular tube that surrounds the entire length of the robust lingual process at rest. It provides the propulsive thrust for ballistic tongue projection (see later) and thus is called the accelerator muscle. Much has been made of the agamine ring muscle's putative similarity to the chamaeleonid accelerator muscle. However, this similarity is purely superficial: the striking feature of the chameleon accelerator is that its fibers are radial rather than circumferential, i.e., it is not a sphincter. They take a curved path from inner to outer membrane and fiber layers alternate in handedness (e.g., Gans, 1967; Bell, 1989; see van Leeuwen, 1997). In fact, the chameleon accelerator is far more similar in this regard to the iguanid condition in which verticalis fibers are radial and curve in opposite directions around the lingual process (Schwenk, unpublished results) (Fig. 8.12A). Other than expansion of verticalis mass ventral to the lingual process to create a tubular form, there is no detailed similarity between agamid and chamaeleonid conditions. Transversalis fibers run from the midline laterally across the dorsum of the tongue (Fig. 8.12A). Some fibers terminate in the dorsolateral margins of the tongue and lingual papillae, but in most taxa a ventral group of fibers loops ventrally along the perimeter of the hyoglossus bundle. In Sphenodon these insert into the ventral transverse septum, but in squamates they join verticalis fibers at the base of the tongue to form a continuous ring around the hyoglossus. In many iguanians this ring is not complete throughout the length of the tongue and, when present, it can be very thin

(e.g.. Smith, 1988). However, in scleroglossans it is often a thick band of muscle. The confluence of transversalis and verticalis fibers around the hyoglossus bundle, particularly in those taxa lacking a transverse septum, has led to the description of this fiber system as a circular muscle (e.g.. Smith, 1984, 1986). Oelrich (1956) described a ventral transverse muscle, but this is simply part of the circular system. In most lepidosaurs the longitudinalis forms a layer of longitudinal fibers running the length of the tongue beneath its dorsal surface, but it is best developed in the foretongue (Fig. 8.15A). In some taxa it is diffuse, but in others it comprises a series of discrete bundles. These are well developed in the foretongues of gekkotans and exceptionally so in the varanoid, Lanthanotus (Schwenk, unpublished results). Some longitudinalis fibers insert into the papillae where in transverse section they are easily mistaken as intrinsic papillary fibers (e.g., de la Cerna de Esteban, 1959, 1965). The sling-like fibers of the verticalis/circular muscle in some scleroglossans also extend into the papillae, as do transversalis fibers. It remains possible, however, that there are some vertical, intrinsic papillary fibers distinct from other fiber systems. 5. Relationship

to the Hyobranchial

Apparatus

The question of tongue mobility relative to the hyobranchium is relevant to our interpretation of hyolingual function during feeding. It is generally assumed that the lingual process is surrounded by a fluid-filled, synovial-type chamber that permits the tongue to slide freely along its length (e.g.. Smith, 1984,1988; Schwenk and Bell, 1988; Herrel et ah, 1995, 1998c). This is certainly true for chameleons in which the tongue is projected off the lingual process, but its relative degree of development among squamates has not been assessed. In fact, anatomical evidence suggests that significant lingual translation along the lingual process might not be possible in many squamates, particularly iguanians (Schwenk, unpublished observations). First, along most or part of the length of the lingual process there is no evidence for a fluid-filled cavity. This is especially evident posteriorly (Fig. 8.12B). The base of the tongue near to the basihyal is tightly adherent to the lingual process in some, if not most, lepidosaurs. There is no anatomical space between the tongue and the base of the lingual process and collagenous fibers of the lingual muscle endomycium are continuous with the perichondrium of the basihyal and lingual process here. Anteriorly, some space usually develops, but it is not clear that it is always fluid filled. Often connective tissue fibers cross between the tongue to the process, suggesting that the intervening space is an artifact of

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Kurt Schwenk

shrinkage. Second, the intimate connection between the laryngohyoid ligament and the tongue would seem to prevent sliding of the tongue past the ligament (Fig. 8.12B). Thus, for the tongue to slide anteriorly on the lingual process it would either have to stretch the ligament significantly or pull the larynx forward along with it. Our films of Sphenodon show clearly that the larynx advances and retracts in lockstep with the tongue (Schwenk et ah, manuscript in preparation; see also Fig. 4 in Gorniak et ah, 1982). We have also observed this in Pogona, an agamid lizard (Schwenk and Throckmorton, unpublished results). Delheusy and Bels (1992) and Delheusy et ah (1994) speculated that the ligament is stretched during tongue protrusion and that its elastic recoil helps to retract the tongue, but this is not supported by the kinematics of the tongue (see Section V) or our film observations. It is unknown how extensible the laryngohyoid ligament is. Preliminary histological and histochemical analysis indicates that it is composed entirely of longitudinally arranged collagenous fibers, suggesting that it is virtually inextensible (Schwenk, unpublished results). Finally, in many iguanians there is a pronounced, hook-like flexure at the tip of the lingual process where the laryngohyoid ligament attaches, as noted earlier (Fig. 8.12B). Although the foretongue curls around the end of the process during lingual prey capture (see Section V), the arrangement would not seem to permit significant translation of the tongue along the process. V. FEEDING FUNCTION A. Overview of Feeding Nonophidian lepidosaurs can be characterized as hyolingual feeders because they manipulate and swallow food primarily by means of patterned movements of the tongue and hyobranchial apparatus. Of course the jaws are an essential part of the feeding apparatus as well, particularly during prey capture and processing. The participation of each morphological unit during a complete feeding sequence varies among taxa. Only in monitor lizards (Varanus) is the tongue largely excluded from participation in feeding, thus ' they are inertial, rather than hyolingual, feeders (see later; Bramble and Wake, 1985). In the following discussion the word "prey" is used for convenience to describe all food items, including plant material. Specific, food-related differences are noted where appropriate. Also note that references to 'Targe" or "massive" food items are always based on food size relative to lepidosaur size and not on absolute size. A selected bibliography of studies providing functional data on feeding in different clades is given in Table 8.5.

All prey capture in lepidosaurs involves the tongue or jaws, thus a food item must be approached very closely before feeding can commence. Chameleons are an exception and indeed the projectile tongue is an adaptation to circumvent this very problem. In most lepidosaurs, close approach is possible because the food item (a) is immobile (e.g., a plant or neonate animal); (b) is initially hidden, then uncovered by an active forager; (c) is in the open and overtaken by a short, rapid dash; (d) is in the open and is approached slowly and stealthily; or (e) unwittingly approaches an immobile lepidosaur waiting in ambush. Once in proximity, food items may be assessed for appropriateness (see Section III,C). This is accomplished visually and chemically with tongue flicking and, in experienced individuals, probably involves learned recognition of appropriate food types. Once a food item is deemed acceptable, a feeding sequence is initiated. There is likely to be strong selection on prey capture performance in taxa feeding on active prey because an initial miss usually results in loss of the prey item. With very few exceptions, ectotherraic lepidosaurs are physiologically unequipped for lengthy pursuits and rely, instead, on quick, glycolytically fueled strikes and rapid processing (e.g., Pough and Andrews, 1985; Andrews and Bertram, 1997). During a feeding sequence, most species are, themselves, vulnerable to predation, thus there is, presumably, also pressure to reduce handling time. Complete feeding bouts, from capture to swallowing, are typically very brief, on the order of several seconds to half a minute. There is usually a refractory period following each completed feeding bout during which accessible prey will not be taken, but this is modulated according to satiety and can be brief in hungry individuals (personal observation). A complete feeding sequence comprises a remarkably complex series of events that in most species occurs very rapidly. A prey item must be located and captured. If it poses a threat or might escape, it is killed or incapacited. If it cannot be swallowed immediately it must be reduced or processed until it can be. It must then be moved through the oral cavity and into the throat to pass on to the gut for digestion. This series of events is orchestrated by a series of cyclical, patterned movements involving primarily the jaws, tongue, and hyobranchial apparatus. In order to make sense of the behavior it is necessary to partition it into discrete stages corresponding to the different functional tasks required of the feeding apparatus from start to finish. This facilitates analysis and desciption and makes comparisons among species possible. The discrete functional events that occur during a single feeding event are identified in the following feeding stages: prey capture, ingestion, processing, intraoral transport, pharyngeal

221

8. Feeding in Lepidosaurs TABLE 8.5

Selected References Treating Feeding Function and Cranial Kinesis in Lepidosaurs

Exclusive of Snakes and Chameleons'^ Scleroglossa Sphenodon

Iguania

Gekkota

Scincomorpha

Anguimorpha

Cranial kinesis

Gorniak et al (1982) Frazzetta (1983) Ostrom (1962) Versluys (1912, 1936)

Arnold (1998) Borsuk-Bialynicka (1985) Frazzetta (1962) Hallermann (1992) Herrel and De Vree (1999) lordansky (1966,1973,1990a, 1996) Rieppel (1978d) Throckmorton and Clarke (1981) Versluys (1912,1936)

Arnold (1998) Borsuk-Bialynicka (1985) Frazzetta (1962) lordansky (1966, 1996) Patchell and Shine (1986a) Versluys (1912, 1936)

Arnold (1998) Borsuk-Bialynicka (1985) Bradley (1903) De Vree and Cans (1987) Frazzetta (1962) lordansky (1966,1990a, 1996) Kritzinger (1946) MacLean (1974) Rieppel (1978d) van Pletzen (1946) Versluys (1912,1936)

Arnold (1998) Boltt and Ewer (1964) Borsuk-Bialynicka (1985) Condon (1987) Frazzetta (1962,1983) lordansky (1966,1996) Rieppel (1978a,d, 1979a) Smith (1980) Smith and Highlander (1985) Versluys (1912,1936)

Feeding function

Bramble and Wake (1985) Gorniak effl/. (1982)

Bels (1990a) Bels and Baltus (1988) Bels and Goosse (1989,1990) Bels et al. (1994) Bramble and Wake (1985) Delheusy and Bels (1992) Delheusyeffl/. (1994) Kraklau (1991) Herrel and De Vree (1999a) Herrel et al. (1995,1996a, 1997a, 1998a,b) Lappin (1999) Schwenk and Throckmorton (1989) Smith (1984) Throckmorton (1976,1978,1980) Throckmorton and Clarke (1981)

Bels et al. (1994) Bramble and Wake (1985) Delheusy et al. (1995) Patchell and Shine (1986a,c)

Bels and Goosse (1990) Bels et al. (1994) Bramble and Wake (1985) Dalrymple (1979) Elias et al. (2000) Cans et al. (1985) Cans and De Vree (1986) Goosse and Bels (1992) Herrel et al. (1996b, 1998a,b, 1999b) MacLean (1974) McBrayer and White (manuscript) Smith (1984) Smith et al. (1999) Urbani and Bels (1995)

Bels et al. (1994) Bramble and Wake (1985) Condon (1987) Elias et al. (2000) Frazzetta (1983) Herrel et al. (1997b) Smith (1982,1986)

''See Chapter 9 and Table 8.3, respectively. Studies listed here are primarily functional analyses of living animals; however, some significant morphological studies with functional inferences are also included, particularly for cranial kinesis. The primary Hterature is heavily emphasized, but important reviews or secondary sources are included (in bold). The taxonomic content of columns follows Table 8.1.

packing, and pharyngeal emptying. These are reviewed here and in Chapter 2. Not every stage occurs in every species or in every feeding bout, nor is each stage necessarily discrete—some are combined and others overlap. Fiowever, they represent a heuristically important starting point because each stage has a different functional outcome and therefore makes different mechanical demands on the structural elements of the system. Thus, to elucidate the functional bases of the extensive morphological diversity reviewed earlier, it is necessary to consider the varying role of the structural elements in each feeding stage (Schwenk and Throckmorton, 1989). The term "ingestion" is sometimes used in the literature generically to refer to the entire process of feeding.

from start to finish, with "swallowing" often used in a similar way in reference to snakes. In the context of tetrapod feeding, because these terms have specific, technical meanings as defined later and in Chapter 2, such usage is undesirable. Feeding stages are characterized by kinematic patterns of jaw, tongue, and hyobranchial movement (e.g.. Bramble and Wake, 1985). The cyclical nature of these movements is consistent with the notion of motor control by a central pattern generator (CPG) (see Chapters 2 and 13). I note anecdotally that the refractory period following a feeding sequence, mentioned earlier, gives the impression of a neural "switch" or transition period during which the CPG-controlled behavior of feeding is turned off and a more alert or conscious state

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1.5

TIME (SEC) F I G U R E 8.17. Jaw and tongue kinematics during lingual ingestion and intraoral transport in Sphenodon punctatus. Solid vertical lines demarcate the phases of each gape cycle. A discrete SO II is only evident in the transport cycle. Note that the tongue makes contact with the prey item over an extended period of time as the prey is pushed into the papillary surface. As the prey was pinned to the substrate, it pushed the mandible down, as indicated by a momentary increase in gape angle (at second dotted line). A stationary phase intervenes between gape cycles. Based on high-speed (300 fps) 16-mm film (Schwenk, Frazzetta and Jenkins, in preparation). FC, fastclose; FO, fastopen; SC-PS, slow close-power stroke; SO, slowopen.

is initiated to control the more plastic behavior preceding a strike. However, CPG control of cyclicity does not imply immutability of the resulting kinematic patterns, which are found to vary among species, among stages, and within a stage according to food type and state of reduction. As such, there is circumstantial evidence for the modulation of feeding kinematics based on sensory feedback (see Chapter 2). During each feeding stage the jaws are repeatedly opened and closed. A single open-close sequence is known as a gape cycle and each feeding stage comprises one to many gape cycles. A covcvpXeie feeding sequence, or hout, includes several feeding stages, from ingestion to swallowing. A "model gape cycle" was proposed by Bramble and Wake (1985) based largely on kinematic patterns evident in lepidosaurs and other nonmammalian tetrapods (see Fig. 2.14 and discussion in Chapter 2). Its generality remains in dispute, but it at least provides a starting point for comparing gape cycles among species and among feeding stages. A single

gape cycle potentially comprises several phases determined by changes in the velocity of the jaws as they open and close (Fig. 8.17): slow open I (SO I), slow open II (SO II), fast open (FO), fast close (FC) and slow close (SC) or slow close power stroke (SC-PS). There is sometimes an intervening period between cycles known as a stationary phase. Gape cycles are reviewed in Chapter 2 and further discussed in Section VII,C.

B.

Feeding Stages

1. Prey Capture and Ingestion Prey capture is the apprehension and subjugation of a prey item and ingestion is its movement from the environment into the oral cavity (Chapter 2). In nearly all nonophidian lepidosaurs, prey capture (or prehension) and ingestion are accomplished by the mouth and combined into a single stage so that capture

8. Feeding in Lepidosaurs involves both the apprehension of a prey item and its immediate delivery into the mouth. Rare exceptions include the Komodo monitor {V. komodoensis) and, occasionally, amphisbaenians, whose unusual feeding behaviors are discussed in Section VI. Once captured, small prey are either transported and swallowed immediately or are killed by biting, shaking, or crushing against the substrate. In some venomous snakes, subjugation is further decoupled from prey capture. Prey are bitten, envenomated, and released to be located later after they are dead. Only then does ingestion begin. Snakes differ from other lepidosaurs in most aspects of their feeding and the traditional feeding stages used here do not clearly apply (see Chapter 9). A fundamental dichotomy is evident in the pattern

F I G U R E 8.18. Consecutive cine frames (48 fps) of a small agamid {Phrynocephalus helioscopus) during lingual ingestion. Note the conformation of the tongue during protrusion and the initial bite following retraction of the mealworm into the mouth.

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of ingestion of small food items (see Sections IV,E and VII,A): Sphenodon and all iguanians use the tongue as a prehensile organ to apprehend small prey and draw it into the mouth, whereas all scleroglossans use jaws and teeth (Schwenk, 1988; Schwenk and Throckmorton, 1989; Wagner and Schwenk, 1999) (Fig. 2.16 in Chapter 2). As prey size increases the dichotomy fades and jaw prehension is almost universally employed, although taxonomic differences remain. A few scleroglossan species use a type of lingual prehension of small prey items in certain circumstances. These exceptions are discussed later. Lingual ingestion involves protraction and protrusion of the tongue concomitant with hyobranchial protraction, with the tongue tip ventrally curled so that the dorsal, papillary surface of the tongue is presented toward the prey item (Figs. 8.18 and 8.19). Tongueprey contact usually occurs on the anterior third of the tongue where papillae are longest in iguanians (Fig. 8.13A). One advantage of lingual prehension is that the tongue is protruded at the same time the head advances toward the prey item, thus their approach velocities are summed and prehension is more rapid than would be possible with the jaws alone. Tongue-prey contact can be relatively light, but most often involves a forceful impact that pushes the prey item against the substrate, fitting the tongue to the prey surface (see later). Adhesion is remarkably effective and involves a combination of interlocking and wet adhesion; in chameleons it may also involve suction (Schwenk, 1983; see Section VI,A). Retraction occurs almost

F I G U R E 8.19. Lingual prehension in an agamid Hzard (Pogona barbata) based on a 35-mm photograph. Note how the dorsal, papillose surface is curled around the end of the protruded, muscular tongue. The right anterior process of the basihyal is evident posteriorly, bulging as the tongue is protracted. The larynx moves forward with the tongue, presumably pulled by the laryngohyoid ligament. Sublingual plicae containing salivary glands form the sides of a well in which the tongue sits at rest.

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FIGURE 8.20. Jaw prehension in a scleroglossan lizard (Varanus niloticus). Prey capture is with the tips of the jaws (more pronounced with smaller prey). Note complete retraction of the tongue. The apparatus on the lizard's head is a goniometer designed to measure mesokinetic flexion and the arrow in the upper left indicates the position of the gage (see Fig. 8.25). From Condon (1987), Exp. Biol 47, 73-87, © Springer-Verlag, with permission.

immediately following prey contact and is extremely rapid. The prey item comes to lie within the mouth on the surface of the tongue or between the tooth rows for transport or swallowing. Jaw prehension of prey involves grasping of the prey in the jaws with the anterior teeth (Fig. 8.20). Sometimes the side of the mouth is used, but grasping usually occurs with the jaw tips. Prey are moved into the mouth for further processing by the tongue or an inertial toss. Larger prey are usually pinned or dragged against the substrate or are subdued by violent shaking before subsequent feeding stages commence. 2. Processing Processing refers to the mechanical reduction or modification of food within the mouth before it is swallowed (Chapter 2). If a prey item is very small it is often transported and swallowed directly without processing. Conversely, large prey consumed by inertial feed-

ers (e.g., Varanus) are often oriented in the mouth and swallowed whole, without processing (although usually after subjugation or killing by biting or suffocating). However, in most cases some processing follows immediately upon ingestion. After ingestion a food item often comes to lie across a tooth row where it can be bitten immediately (Fig. 8.18), but sometimes it must be positioned between the teeth or shifted to a more advantageous bite point. Such manipulative cycles are usually mediated by lingual movement, including tongue twisting, but they are sometimes accomplished inertially with a lateral jerk of the head. Repositioning is also used to orient large prey items head first so that limbs, scales, or fur fold posteriorly, facilitating prey movement into the esophagus. Reduction usually involves repeated bites so that the teeth (or occasionally the palate) pierce, crush, or shear the prey item as it is coated in saliva, rendering it softened but usually whole. Most lepidosaurs are well supplied with oral salivary glands that produce a variety of secretory products (Gabe and Saint Girons, 1969; Kochva, 1978), but there is no indication thus far that these compounds initiate chemical digestion or do anything more than lubricate the bolus for swallowing (with the exception of venom glands in Heloderma, which are used primarily for defense). Such chewing behavior is called puncture-crushing in contrast to mammalian-type mastication in which a food item is reduced to tiny particles. As such, comminution of food is not a necessary outcome of most lepidosaurian chewing, although it sometimes occurs, whereas it is the raison d'etre of most mammalian mastication. This difference has a profound effect on the form and evolution of the feeding system in the two groups. Transverse movements of the mandible relative to the upper jaw and a "masticatory orbit" (e.g., Hiiemae et al, 1978; Chapter 13) are virtually never observed in nonophidian lepidosaurs and remain unique features of the mammalian masticatory mechanism (e.g., Davis, 1961; Throckmorton, 1980). Despite the absence of a masticatory orbit as in mammals, it is an unsung fact that many, if not most, lepidosaurs chew on one side at a time and often alternate between sides. Side switching is particularly evident in Sphenodon (Gorniak et al, 1982; Schwenk et al, manuscript in preparation) and iguanians, especially acrodonts (Schwenk and Throckmorton, 1989; personal observation), but it is also observed in scleroglossans (e.g.. Smith, 1984). Chewing asymmetry and the intraoral manipulation it requires have been regarded as exclusively mammalian traits associated with the presence of mobile, muscular cheeks and lips, and the absence of a lingual process within the tongue (e.g., Davis, 1961), thus its ubiquitous occurrence in

8. Feeding in Lepidosaurs lepidosaurs has significance for interpreting the evolution of mammalian mastication (see Throckmorton, 1976; Crompton, 1989). Chewing asymmetry also has implications for muscle activity patterns on active versus balancing sides, mandibular bending, the transmission of forces from one side to the other, the nature of joint reaction forces, and the position of the bite point (e.g., Druzinsky and Greaves, 1979; Gorniak et ah, 1982; Greaves, 1995). These factors have only rarely been considered in lepidosaur feeding. Chewing and intraoral transport cycles tend to be kinematically similar and are often not separated in functional analyses. The basis for such similarity is discussed in the following section. 3. Intraoral

Transport

Intraoral transport is the movement of food through the oral cavity to the pharynx for swallowing (Chapter 2). In many ways, intraoral transport is the "purest'' form of gape cycle in which the cyclical, coordinated movements of the jaws, tongue and hyobranchium are most apparent, unsullied by the mechanistic vagaries of prehension and reduction. Possibly for these reasons. Bramble and Wake (1985) based their model gape cycle on intraoral transport and suggested that it might represent an ancestral tetrapod pattern (see Chapter 2). However, Bramble and Wake (1985) also included "chewing'' or processing cycles here as well. In the vast majority of lepidosaurs, intraoral transport is accomplished by cyclical movements of the tongue and hyobranchial apparatus in coordination with the jaws (Bramble and Wake, 1985). Hyolingual transport involves anterior movement of the tongue and hyobranchial apparatus underneath the food item during SO I while it is held against the roof of the mouth. The tongue is usually deformed at the end this process (SO II) so that the bolus comes to lie within a depression in its surface, or the tongue is elevated in front of the bolus. Although the prey item is often oriented transversely across the tooth row in chewing cycles, in pure transport cycles it is oriented longitudinally on the tongue to clear the teeth and corners of the mouth (e.g., Delheusy and Bels, 1992). SO II may also be used to integrate sensory information on food position and condition to modulate the next cycle (Bramble and Wake, 1985). As the jaws are parted during FO, the bolus is freed from contact with the palate or teeth, and the hyobranchium and tongue rapidly shift posteriorly so that at jaw closure (FC and SC) the prey item has come to lie farther back in the mouth where it is once again fixed against the palate by the tongue. The tongue repeats its anterior movement beneath the prey item in preparation for the next cycle. According to

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Bramble and Wake (1985), the presence of SC, especially with high levels of adductor activity indicating a power stroke (SC-PS), is contingent on the teeth engaging the prey item at the end of FC. They thus describe a chewing cycle as construed here, rather than a "pure" transport cycle. Indeed, an SC phase is variably present during putative transport cycles (see later). However, an SC phase is sometimes apparent even when contact of the marginal teeth with the prey item does not occur. This may represent controlled slowing of jaw closure or contact of the prey item with the palate as the jaws engage. If the latter, the presence of an SC phase during intraoral transport should be related to bolus size and condition, implying that SC should be more evident with large prey items and in earlier cycles. In some taxa, head jerking and prey inertia are substituted for hyolingual movement (Gans, 1969b). During inertial transport the prey item is momentarily released while the animal rapidly shifts its head anteriorly. The prey item thus comes to lie farther back in the mouth as the jaws close. For smaller prey, head and jaw movements are imparted to the food item itself so that it moves back relative to the ground, whereas a larger prey item remains more or less stationary while the head moves forward over it. Among lepidosaurs, only varanids are obligate inertial feeders due to extreme reduction of the tongue for chemoreception and its limited participation in feeding (e.g.. Smith, 1986; Condon, 1987; Elias et al, 2000). Other large, carnivorous lizards (e.g., Tupinambis) frequently employ inertial feeding as well (e.g., MacLean, 1974; Smith, 1984; McBrayer and White, manuscript in preparation), but these also use hyolingual transport some or most of the time (e.g., MacLean, 1974; personal observation). Inertial transport is occasionally used by other taxa, particularly when feeding on relatively large prey items (e.g., Sphenodon, see later), but small species, such as gymnopthalmids, eating relatively small prey also use it (e.g., MacLean, 1974). It is possible that the frequency of inertial feeding by lepidosaurs has been overestimated in the literature. This is because virtually all functional analyses have been undertaken in the laboratory with captive animals often fed unnatural diets (see Chapter 1). Mice are frequently used in feeding trials with larger lepidosaur species, but such vertebrate prey are rarely eaten in the wild (see Section III,A). The vast majority of prey items for such species are small invertebrates that are more likely to be manipulated with hyolingual movements. Intraoral transport and chewing cycles often overlap temporally and are difficult to distinguish kinematically (Bels et al, 1994; see later). In most taxa, they grade one into the other so that many gape cycles are a combination of the two. A pure chewing cycle would

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involve no posterior movement of the prey item during the gape cycle and a pure transport cycle would involve no crushing of the prey by the teeth. However, in most cases, chewing cycles include hyolingual movement of the prey item to place it between the teeth for crushing at the end of each cycle. There is cyclical anteroposterior movement, but no net posterior translation, or some posterior movement of the prey item along the tooth row occurs between bites. Thus jaw and hyolingual movements during chewing cycles are likely to mimic transport cycles kinematically in most taxa. For these reasons, Schwenk and Throckmorton (1989) followed Bramble and Wake in suggesting that processing should be considered a type, or subset, of intraoral transport, a conclusion in which Bels et al (1994) concurred. However, functional work has shown that there may be important quantitative (e.g., Herrel 1997a; Smith, 1982; Cans et al, 1985; Cans and De Vree, 1986) and qualitative (e.g.. Smith, 1982,1984; Condon, 1987; So et al, 1992; Herrel et al, 1997b) differences between the two cycle types (see later). Given that chewing is a facultative behavior and that chewing and transport have different mechanical outcomes and can be kinematically decoupled (as in chameleons), it seems worth preserving the distinction between chewing and intraoral transport stages here, and in future functional analyses, insofar as possible. 4. Pharyngeal Emptying

(Swallowing)

Swallowing refers to the movement of food into the esophagus, where peristalsis takes over the process of transporting the bolus to the gut (see Chapter 2). In lepidosaurs, swallowing potentially comprises two separate substages: pharyngeal packing and pharyngeal compression. Although these stages serve the same function as deglutition in mammals, swallowing is so different mechanistically in the two groups that it is unlikely to be homologous in any meaningful sense (see Smith, 1992; Bramble and Wake, 1985; see Chapters 2 and 13). Pharyngeal packing occurs universally among nonophidian lepidosaurs, but not pharyngeal compression, which is most common in scleroglossans. Occurrence of the latter stage in some species may be facultative, presumably depending on bolus size and characteristics (personal observation). It is often difficult to observe, sometimes only evident as a single, brief compressive cycle without an accompanying gape cycle. Because of confusion about the mechanics and nomenclature of swallowing in lepidosaurs, it is usually not clear whether the failure to mention pharyngeal compression in literature accounts of swallowing reflects its actual absence or merely the failure to observe or document it. To complicate matters further.

terminal intraoral transport cycles sometimes grade into pharyngeal packing cycles so that kinematic distinctions between transport and swallowing stages can be blurred during the transition (see later). In part because of these ambiguities, the literature on lepidosaurian swallowing is inconsistent and sometimes muddled. Some authors do not consider pharyngeal compression at all, note it briefly in passing, or consider it "aberrant" (Herrel et al, 1997b:387). Bramble and Wake (1985), who set the tone for nearly all lepidosaurian feeding studies to date, considered pharyngeal compression to be exceptional and limited to specialized inertial feeders, such as varanids and large teiids. In some studies, the discussion of pharyngeal packing is included under intraoral transport, and a separate stage known as "cleaning" is identified, although cleaning is actually a part of pharyngeal packing (see later). The literature is also inconsistent in its application of technical terms. For example. Smith (1984) equated "swallowing" with pharyngeal compression and considered pharyngeal packing a separate, preswallowing stage, whereas Herrel et al (1999b) equated "swallowing" with pharyngeal packing and considered pharyngeal compression a postswallowing stage! Some studies (e.g., Urbani and Bels, 1995) erroneously apply the term "deglutition" to swallowing behavior in lizards, usually in the context of pharyngeal packing [see Smith (1994) and Chapter 2]. These problems make extraction of data for a comparative synthesis difficult. I have proposed a standard nomenclature here that should facilitate comparative studies. Future functional analyses should take care to watch for pharyngeal compression following pharyngeal packing and to distinguish these two components of swallowing when they occur. a. Pharyngeal Packing Pharyngeal packing is characteristic of lepidosaurs and possibly some turtles (Chapter 2). During this stage the bolus is pushed into the pharynx and the anterior part of the esophagus (Smith, 1984, 1992; Bramble and Wake, 1989). This is almost always accomplished by the tongue and may be the principal function of the tongue's posterior limbs, which serve to tamp the bolus into the pharynx. Typically (but not always) during pharyngeal packing cycles the tongue is protruded out of the mouth tip first and often appears to "lick" the labial scales and snout. A "cleaning" or "lip-licking" function is often attributed to this behavior (e.g., Throckmorton, 1980; Cans et al, 1985; Bels and Baltus, 1988; Goosse and Bels, 1992), but in most cases such tongue protrusion results from lingual positioning for asymmetrical tamping by the posterior limbs

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8. Feeding in Lepidosaurs and probably has nothing to do with cleaning the labial scales (Smith, 1984; personal observation). The extent of tongue protrusion varies depending on the size of the bolus and its position relative to the esophagus. Packing cycles with tongue protrusion push the bolus farther back into the pharynx than cycles in which protrusion does not occur (Delheusy and Bels, 1992). Although tip-first tongue protrusion clearly distinguishes some pharyngeal packing cycles from transport cycles, early packing cycles can blend temporally and kinematically with preceding intraoral transport cycles. Both transport and packing involve hyolingual movement of the bolus posteriorly, but they differ in the position of the bolus relative to the tongue; in the former it lies on the tongue, whereas in the latter it is posterior to it. Other kinematic variables distinguish them as well, but the two phases may be largely overlapping in quantitative attributes, at least in some taxa (e.g., Herrel et al, 1995). Smith (1984), however, found the cycle types to be "distinct" in their patterns of tongue-jaw coordination and the shapes of the orbits described by tongue and hyobranchium. In packing, the hindtongue moves upward and backward during SO rather than upward and forward, and the tongue orbits become elongate and largely anteroposterior. Gape profiles become small and spiked, losing their differentiation into discrete phases. The extent to which these disagreements reflect phylogenetic differences, experimental conditions, or criteria for identifying cycle types in the first place remains to be determined. The extent to which pharyngeal packing moves food into the esophagus must be variable. Smith (1984) found that during pharyngeal packing, food collected in the pharynx only and pharyngeal compression was necessary to squeeze the bolus into the esophagus (swallowing sensu stricto). In contrast, Herrel et ah (1996a) observed that packing moved food into the esophagus as well. Because pharyngeal compression often does not occur, pharyngeal packing must be sufficient in many cases to move food fully into the esophagus to initiate peristaltic transport. Undoubtedly, bolus size and condition influence swallowing behavior, as well as taxonomic differences.

tive in taxa with posterior limbs of the tongue reduced or missing (see Section VII,B). Lepidosaurs and all other nonmammalian vertebrates lack the pharyngeal musculature characteristic of mammals (Smith, 1992; see Chapters 2 and 13) and therefore cannot compress the pharyngeal cavity internally to squeeze the bolus into the esophagus. Thus, if pharyngeal packing fails to tamp food far enough into the esophagus to initiate peristalsis, lepidosaurs resort to external compression of the pharynx by means of cervical flexure and/or contraction of the constrictor colli muscle. The constrictor colli forms a sling around the pharynx and its contraction elevates the hyobranchium and constricts the gular region. Smith (1984) noted that in order for compression to succeed, the bolus must lie behind the basihyal so that it is squeezed posteriorly and not returned into the mouth. It is conceivable that anterior and posterior intermandibularis muscles join the constrictor colli during swallowing so that their serial contraction creates a compressive wave along the pharynx from front to back, squeezing it like a tube of toothpaste, but this is purely speculative. If the bolus is posterior enough, simple constriction of the pharynx would suffice. Neck flexure also is used to compress the pharynx in some species, alone or in addition to constrictor colli constriction. Its pattern and extent vary among taxa, but it can involve ventral bending (head tucking), lateral bending, or both. In short-necked forms the bending appears to be simple flexure at the atlanto-occipital joint, but in elongate forms, lateral neck bending is sinuous and sinusoidal, i.e., it appears that a propagated wave is generated rather than simple flexure (personal observation). Sinusoidal movements continue into the trunk in some species. It is possible that internal concertina movements also aid in pharyngeal emptying in long-necked forms, especially anguimorphans, as they do in some snakes (Kley and Brainerd, 1996; N. Kley, personal communication). Such movements involve sinusoidal bending of the body axis internally, including vertebral column and esophagus, independent of the outer body wall (see suggestive Xray photo of Varanus, Fig. 89 in Greer, 1989).

h. Pharyngeal Compression Accumulating evidence indicates that pharyngeal compression is widespread among lepidosaurs (and other reptiles) and is not restricted to inertial feeders, as suggested by Bramble and Wake (1985). It occurs in both iguanian and scleroglossan squamates and although undescribed, it may be present in Sphenodon as well. It is more common or pronounced in scleroglossans, which accords well with their generally reduced hindtongues—pharyngeal packing may be less effec-

C. Feeding in

Sphenodon

1. Ingestion Lingual ingestion in tuatara was noted anecdotally by earlier authors (e.g., BuUer, 1878; Dawbin, 1962; Farlow, 1975) and has been analyzed by Gorniak et al (1982) and Schwenk et al. (manuscript in preparation). Gorniak et al. (1982) found that lingual prey prehension was used when feeding on small prey (insects).

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but that large prey items (mice) were grasped directly by the jaws. Ingestion is usually initiated by prey movement (see earlier discussion). Movement elicits head cocking and visual fixation of the prey item. The head is moved toward the prey, usually forward and downward toward the substrate, but prey suspended by a thread above the head are also easily taken (Schwenk et ah, manuscript in preparation). As the head moves closer, the jaws begin to part as the tongue is protracted. Cineradiography shows that tongue protraction is caused by hyobranchial protraction (Gorniak et ah, 1982; Schwenk et al, manuscript in preparation). There is no evidence of hydrostatic elongation or sliding of the tongue along the lingual process. The tongue is slightly elevated initially and extended tip first. The initial tip-first orientation of the tongue differs from iguanians (see later). Immediately upon crossing the mandibular symphysis the tongue tip curls ventrally and is fixed to the mandible so that as the tongue continues to be pushed out of the mouth by the hyobranchium it becomes arched with its dorsal surface presented anteriorly toward the prey item. This kinematic pattern is consistent with the fact that anterior genioglossus medialis fibers run into the foretongue to the tongue tip; contraction of these fibers, or simply their inextensibility, would force the tongue tip downward and anchor it to the mandible (Schwenk, 1986; see Section V,F). As the tongue is protruded the larynx advances correspondingly (Fig. 4 in Gorniak et ah, 1982). This suggests that the laryngohyoid ligament is inelastic and when the tongue is protracted it pulls the larynx with it (see earlier discussion). Prey contact occurs on the dorsal surface of the foretongue, which is now directed anteroventrally. The zone of contact corresponds to the region of the tongue where filamentous papillae are longest (Schwenk, 1986). Differences in papillary height and orientation across the width of the tongue create a modest lingual sulcus in the midline. The sulcus may enhance the number of papillae making contact with the prey item. The prey item is usually only lightly contacted by the tongue surface, but this is sufficient to cause adhesion. In some cases, however, contact is forceful enough to push the mandible slightly downward (Fig. 8.17). Tongue-prey contact triggers tongue retraction, but the jaws continue to open as the tongue and adherent prey are rapidly withdrawn into the mouth. As tongue and prey clear the mandible, the jaws are snapped close. Tongue retraction is coupled to hyobranchial retraction. Ingestion of mice is accomplished by biting and lifting with the anterior teeth. According to Gorniak et ah (1982:337), "The tongue plays no role during capture nor is it protruded." Unfortunately, Gorniak and col-

leagues do not indicate the nature of tongue movement and conformation within the mouth during jaw prehension. It is possible either that the tongue is fully retracted to avoid prey contact, as in scleroglossans, or that it curls and contacts the prey item within the mouth concomitant with jaw prehension, as in iguanians (Schwenk and Throckmorton, 1989). Feeding studies on intermediate prey sizes are necessary. These would help determine whether the transition from tongue to jaw prehension is a graded response, as in iguanians, or a threshold response. Lingual ingestion gape cycles are highly variable in duration and kinematic pattern in a single individual (Schwenk et ah, manuscript in preparation). Most cycles roughly conform to the Bramble-Wake model and are similar to the iguanian pattern (Fig. 8.17). The tongue and hyobranchium are protracted during SO I and SO II, then retracted during FO and FC. SO II is characterized by a very high gape angle, perhaps more so than in iguanians (Schwenk and Throckmorton, 1989; see later), presumably to allow clearance for the tongue and prey as they are retracted. Thus the difference in gape between SO II and maximum gape at the end of FO is usually quite small. Herrel et ah (1995) suggested that Sphenodon exhibits no distinct SO, but this is not accurate. There is a tendency for SO I and SO II to be poorly differentiated and for SO II to blur into FO so that a distinct "plateau phase" (Schwenk and Throckmorton, 1989) during SO II is less frequently evident in Sphenodon than in iguanians. Nevertheless, an SO phase is evident in many ingestion cycles (Schwenk et ah, manuscript in preparation). A typical ingestion sequence is slow relative to most squamates (0.5 to 1.0 sec); however, tuatara are relatively large and this may be an effect of body size. Although most investigators dutifully report quantitative data on cycle duration and make comparisons among taxa, scaling effects on tetrapod-feeding kinematics are virtually unstudied. Absolute differences in cycle duration among taxa may have little biological significance. Gorniak et ah (1982) provided electromyographic (EMG) data for feeding in Sphenodon, but unfortunately did not sample hyolingual muscles. During ingestion the jaws are opened by the bilateral activity of anterior and posterior portions of the depressor mandibulae; however, the anterior part is most active earlier and the posterior part later. Both are silenced as jaw closing begins and the adductors become active, although there is some overlap. The anterior portion of the superficial external adductor is first active, followed by its posterior portion, the medialis, the pseudotemporalis superficialis, and several parts of the complex pterygoideus. Adductor activity is maximal when the teeth contact

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8. Feeding in Lepidosaurs the prey item and crush it. They are then silenced during a stationary phase when the mouth opens slightly, probably from recoil of the prey item between the teeth. 2. Processing Tuatara use a unique form of mandibular translation to shear their food rather than the typical puncture-crushing of lizards (Gorniak et al, 1982). After two or three manipulative or killing bites, an insect is moved by the tongue to the corner of the mouth on one side where it is chewed for two to four cycles. The prey item remains fixed relative to the upper tooth row during chewing. It is then moved by the tongue and placed between upper and lower teeth of the same or opposite side and the chewing cycles are repeated. Multiple chewing clusters are repeated (approximately 15 times) until the insect is "reduced to a saliva-covered, mushy mass" (Gorniak et al, 1982:333). Each reduction cycle includes a period of mandibular translation along the articular surface of the fixed quadrate so that the lower teeth slide between the two parallel, upper tooth rows (Fig. 8.2) (see Section IV,B), shearing the prey as well as crushing it. The gape profile is typical with all phases usually evident. However, the jaws usually continue to open during SO II so that there is usually no distinct "plateau phase." SO involves simple mandibular depression. During FO, however, the mandible slides posteriorly along the quadrate-articular joint. The jaws close during FC, but there is no mandibular translation. The prey item is crushed during SC-PS as the jaws are pulled into full closure. At the end of SC-PS, a distinct "shearing phase" occurs during which the mandible is translated anteriorly. Larger prey items are slightly rolled during translation. Shearing ends when the mandible is slightly depressed at the start of a stationary or resting phase. Typically, a resting or stationary phase is present between each chewing cycle. These vary in time, but can be as long as a second. After three to five cycles of chewing, insects are shifted laterally to the opposite tooth row with twisting movements of the tongue. As chewing progresses, cycle durations decrease. Chewing cycles blend into intraoral transport. When feeding on mice, Sphenodon follows ingestion with several crushing or killing bites. Inertial transport is used to position the mouse transversely across the tooth rows of both sides at the back of the mouth for the symmetrical killing bites. Lateral jerks of the head are then used to position the mouse inertially between the teeth on one side and a series of four to seven chewing cycles begin to reduce the mouth. Initially, side

shifts and prey manipulation are inertially based, but as chewing proceeds, the tongue becomes involved in manipulatory movements and reduction cycles resemble those for insects. This probably represents a transition from processing to intraoral transport (see later). If limbs or other parts of the mouse come to lie outside the tooth rows following ingestion and manipulation, these are bitten off and not consumed. EMG recordings (Gorniak et al, 1982) showed that initial jaw closure during chewing is driven by the adductor mandibulae externus superficialis, externus profundus, and pseudotemporalis superficialis. Crushing during SC is caused by the addition of the pseudotemporalis and the pterygoideus. The shearing phase is driven by a portion of the pterygoideus whose fibers insert on the mandible with a large anterior component so that they act as a protractor, as well as an adductor, of the mandible. Chewing is highly asymmetric in Sphenodon with frequent side switching. Working and balancing side muscle activity varied from bite to bite during reduction, apparently in response to prey position and texture. 3. Intraoral

Transport

It is difficult to separate chewing from transport cycles in Sphenodon as both occur simultaneously. As reduction proceeds, the bolus is moved farther and farther back in the mouth. Chewing cycles then grade into pure intraoral transport cycles that Gorniak et al (1982) referred to as "terminal movements." However, because these cycles seem to grade quickly into pharyngeal packing cycles, the distinctions are difficult to make, at least based on the descriptions of Gorniak et al (1982). Further analysis of our cineradiographic films may help clarify differences among cycle types (Schwenk et al, manuscript in preparation). Transport is hyolingual with high amplitude anteroposterior movements of the hyoid (Schwenk et al, manuscript in preparation; see Fig. 11.23 in Chapter 11). Transport gape profiles are typical, with welldefined phases (Fig. 8.17). The bolus is released from the marginal teeth and held centrally on the tongue. During SO the tongue and hyobranchium move slowly forward, then rapidly so during FO. At FC the tongue and hyoid reverse direction and the tongue's dorsal surface is arched so that it scrapes the palate as it is rapidly retracted, pushing the bolus behind it toward the pharynx. Palate scraping does not occur with mice, presumably because they did not tend to adhere to the roof of the mouth due to their greater mass. Gape angles tend to be larger during transport cycles than during reduction, and mandibular translation is minimal (Gorniak et al, 1982). Muscle activity levels are

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reduced during transport; however, EMG patterns are similar to reduction cycles with the exception of the pterygoideus muscle. The pterygoideus exhibits a great deal of regional heterogeneity, with some parts active during jaw opening. 4.

Swallowing

a. Pharyngeal Packing As noted earlier, Gorniak et al (1982) did not distinguish between late intraoral transport cycles and pharyngeal packing. However, during "terminal movements" the tongue tip is often slightly protruded between the anterior teeth prior to retraction. Gorniak ei al. (1982) interpreted this behavior as a method of "cleaning" the anterior portion of the tongue, but more likely it reflects the larger anteroposterior excursions typical of pharyngeal packing cycles in other lepidosaurs (see later). It seems to be a way of positioning the bolus as far back on the tongue as possible so that the posterior limbs of the tongue can be used to tamp the bolus into the pharynx. h. Pharyngeal Compression Unfortunately, Gorniak et al. (1982) did not describe compression cycles in Sphenodon, nor do our films continue long enough into the feeding sequence to include this stage (Schwenk et al, manuscript in preparation). Gorniak et al. (1982) implied that swallowing is accomplished by the "terminal movements" described earlier, interpreted here as intraoral transport and pharyngeal packing cycles based on comparison to other lepidosaurs (see later). Our cineradiographic films indicate that the bolus may not clear the pharynx during these cycles, thus it is possible that tuatara use pharyngeal compression and possibly cervical flexure to push the bolus fully into the esophagus to complete swallowing, but this remains undetermined. Knowledge of the presence or absence of a pharyngeal compression stage in Sphenodon would help clarify the evolution of swallowing mechanisms in lepidosaurs. D . Feeding in Iguania 1. Ingestion Lingual ingestion in chameleons is treated separately (see Section VI), but is mentioned briefly here in comparison to other iguanians. This section focuses on the more generalized iguanian families, Iguanidae and Agamidae. Lingual ingestion in these taxa was noted anecdotally in a number of studies (e.g., Abel, 1952; Cooper et al, 1970; lordansky, 1973; Smith, 1984; Frazzetta, 1986), but its universality in Iguania was pointed out by Schwenk (1988) and Schwenk and Throckmor-

ton (1989), who showed that lingual ingestion of small prey uniquely characterizes this monophyletic taxon in contrast to its jaw-feeding sister taxon, Scleroglossa. Functional treatments or complete descriptions of lingual ingestion are available for the following taxa: Iguanidae, Anolis (Bels and Baltus, 1989; Bels, 1990a; Bels and Goosse, 1990); Dipsosaurus (Schwenk and Throckmorton, 1989); Iguana (Throckmorton, 1976; Schwenk and Throckmorton, 1989); Opiums (Delheusy and Bels, 1992); Phrynosoma (Schwenk and Throckmorton, 1989); Sauromalus (Schwenk and Throckmorton, 1989); Agamidae, Agama (including Plocederma) (Kraklau, 1991; Herrel et al, 1995); Phrynocephalus (Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989); Pogona (Schwenk and Throckmorton, 1989); and Uromastix (Throckmorton, 1976; Schwenk and Throckmorton, 1989; Herrel and De Vree, 1999a). As noted earlier, lingual prehension is limited to relatively small food items, whereas larger prey are grasped in the jaws (Smith, 1984; Schwenk and Throckmorton, 1989), as in Sphenodon. Nonetheless, only one study has provided any functional data for iguanian jaw prehension (Bels and Goosse, 1990). Bels and Goosse (1990) asserted that the small iguanid, Anolis carolinensis, used jaw prehension for blowfly larvae, but they did not document the behavior photographically. It is possible that 1-cm larvae were too large for lingual prehension by the small lizards, but it is also possible that poor film resolution prevented its detection. Some lingual feeding sequences involve minimal tongue protrusion and close approximation of the jaws before tongue-prey contact (particularly when prey are relatively large; see later). In small taxa, such as A. carolinensis, this is very difficult to see, even in good films (personal observation). Furthermore, studies of other Anolis species (Bels and Baltus, 1989; Bels, 1990), as well as my own observations of A. carolinensis (unpublished), confirm the use of lingual prehension. In any case, the gape profile given for this sequence was typical of lingual ingestion sequences in other taxa. The ambiguity of this case only highlights the dearth of functional data for jaw prehension in iguanians. Cropping of plants by herbivorous species may be a form of jaw prehension in some cases, but it virtually always involves initial or simultaneous lingual prehension (Schwenk and Throckmorton, 1989). This is described further later. Jaw prehension may occur in other unusual circumstances. For example, streamside basilisk lizards (Basiliscus) have been observed to capture fish under water after a lunge from their perch (Echelle and Echelle, 1972). Although underwater lingual prehension does occur in some salamanders (Schwenk and Wake, 1988, 1993; S. Deban and J. Larsen, personal communication), it is more likely that the

8. F e e d i n g in L e p i d o s a u r s

basilisks use their jaws for prehension given the mechanics of lingual prehension (see later). Montanucci (1989) observed that some individuals of Phrynosoma solare, an extreme ant specialist, eventually "learned" to use the jaws to capture unnaturally large prey, but only after repeated attempts with the tongue failed. Schwenk and Throckmorton (1989) suggested that prey size-dependent differences in iguanian prehension mode are quantitative and not qualitative. As such, tongue-prey contact always occurs, but the distance the tongue is protracted and protruded is modulated according to prey size. As prey size increases, the tongue is protruded less and less until at large prey sizes tongue-prey contact occurs within the margins of the jaws at the same time as jaw-prey contact. This scenario is supported by Throckmorton's (1976) observations of Uromastix and my own observations of Gambelia (Iguanidae) feeding on lizards (unpublished results). It also suggests the way jaw prehension may have evolved in Scleroglossa from lingual-feeding ancestors (Wagner and Schwenk, 2000; see Section VII,A). Due to the lack of functional data on jaw prehension in iguanians, the following account is limited to lingual ingestion (references given earlier). The kinematics of lingual ingestion are very similar to those described for Sphenodon, with a few exceptions. Most lizards are more likely to charge active prey than are tuatara. Prey motion typically alerts the lizard and triggers monocular fixation of the prey so that the head is often first tilted to one side. A feeding sequence begins with orientation of the snout toward the prey item (and presumably binocular fixation in most species) and approach. If the prey item is already within range, the strike usually involves forward rotation of the body over the forelimbs with the head moving down and forward toward the prey. Sometimes tongue flicking and further observation precede the start of feeding, but often it is initiated immediately. As such, the jaws may begin to part and the tongue protruded as the lizard approaches, but before it is within striking range (e.g., Kraklau, 1991). If the prey item ceases motion or moves away, the lizard may remain with its tongue partially protruded for some time before the feeding attempt is completed or aborted; sometimes the tongue moves in and out while the prey moves in and out of range (Schwenk and Throckmorton, 1989). Variation in this phase of a feeding sequence is responsible for extensive variance in ingestion cycle duration. As protraction begins, the tongue tip is immediately curled ventrally and the dorsal surface arched (Fig. 8.18). This is in contrast to Sphenodon in which the tongue is pointed during the earliest stages of protraction. As it passes the mandibular symphysis, the

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tongue tip is more or less anchored, and as protrusion continues the arched dorsal surface of the tongue extends outside of the mouth and is presented anteroventrally (Figs. 8.18 and 8.19). Schwenk and Throckmorton (1989) found a taxonomic difference between iguanids and agamids in the orientation of the tongue tip during protrusion, but additional study has not supported a consistent dichtomy. Tongue-prey contact occurs at maximum tongue extension on the anterior third of the tongue's dorsal surface (Figs. 8.19 and 8.21). The contact zone corresponds to the region of greatest papillary length and epithelial rugosity (Figs. 8.13A and 8.14B). As contact is made the lizard usually continues to advance so that the prey item is pinned to the substrate. This behavior not only immobilizes the prey, but importantly, it forces the prey item into the deep, papillary cushion of the foretongue so that the lingual surface is literally "formed" to the prey item (Figs. 8.21A and 8.21B). This maximizes the surface area of contact and may help promote adhesion. It might further help to absorb impact energy so that the prey item is not pushed away, giving the tongue time to form an adhesive bond. The mechanism of lingual adhesion and prehension is developed in detail in Section V,F. Following upon tongue-prey contact, the jaws open rapidly, largely by means of cranial elevation at the atlanto-occipital joint, and the tongue is retracted. As soon as the tongue and adherent prey cross the tip of

FIGURE 8.21. Lingual prey capture in a horned lizard, Phrynosoma cornutum (Iguanidae). (A and B) A small cricket is first hit with the tongue and then pinned to the substrate. The cricket's body is pushed into the papillary cushion of the tongue's contact zone, maximizing the surface area of contact and ensuring interlocking of the tongue with the prey surface. (C and D) Sequential frames of retraction in another feeding bout. Note how the tongue's papillary surface is straightened and rolled around the end of the tongue like a conveyor belt. The cricket is "flipped" rapidly into the mouth on the tongue's dorsal surface. Both sequences filmed at 250 fps (4 msec between frames).

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the mandible the jaws snap closed. High-speed films of Phrynosoma reveal that, during tongue withdrawal, its dorsal papillary surface is quickly retracted by "rolling" around the stiff, protracted column of lingual muscle like a conveyor-belt (Schwenk, manuscript in preparation). The prey item is "flipped" around the end of the tongue and into the mouth, its retraction accelerated by summing the independent velocities of the papillary surface and whole-tongue retraction (Fig. 8.21C and 8.21D). Bell (1989) showed that the papillary surface is moved independently around the muscular column of the accelerator muscle in chameleons, and films of other iguanians suggest a similar pattern during retraction, hence this may be a general, iguanian trait. In herbivorous species that feed by biting pieces off of whole plants (e.g.. Iguana and Uromastix), lingual ingestion succeeds initially only in getting a part of the plant into the mouth. Once there it must be cropped by the teeth (Throckmorton, 1976, 1978; Schwenk and Throckmorton, 1989). Ingestion may require several cycles to get a sufficient portion of the plant into the mouth before it is cropped (Throckmorton, 1976,1978). Multiple ingestion cycles are unique to this situation. However, one might more accurately regard cycles subsequent to the first as part of intraoral transport, and cropping as a type of reduction. In some cases, a whole plant that is fixed in place can be regarded as a "large" food item that necessitates jaw prehension for cropping. For example, the Galapagos land iguana {Conolophus subcristatus) uses both lingual and jaw prehension when feeding on cactus pads. Pads are usually scraped clean of spines and tough outer cuticle first, then bitten (see Section V,D,2). Often the tongue draws the pad in for cropping by the teeth, but sometimes it is bitten directly (H. L. Snell, personal communication). Either way, initial cropping may not completely separate a piece from the cactus. In this case the exposed cactus flesh is scraped off the tougher, outer cuticle by the teeth. The related marine iguana {Amblyrhynchus cristatus) may use jaw prehension predominantly. It feeds underwater or in the intertidal zone by grasping algae in its jaws and cropping it with a twist and jerk of the head (Carpenter, 1966). This cropping action may be enhanced by an extremely foreshortened facial skeleton and procumbent (protruding), spatulate teeth (personal observation). However, it is possible that the tongue initially contacts the algae to draw it into the mouth for cropping (see later). Because feeding frequently occurs under water, lingual prehension is probably minimally important. Nonetheless, semidomesticated individuals were said to feed terrestrially on crickets (K. Angermeyer, in Carpenter, 1966) and it seems likely that lingual protrusion would be used then, but this is unknown.

Four possible mechanisms of tongue protrusion have been proposed (Smith, 1984, 1988; Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989): (1) The tongue is "pushed" out of the mouth by protraction of the hyobranchium, primarily through action of the mandibulohyoideus (geniohyoideus) muscles. (2) The tongue is "pulled" anteriorly by the genioglossus muscle. This would either slide the tongue along the lingual process or pull the hyobranchium simultaneously due to a tongue-hyobranchial linkage and inextensibility of the tongue. (3) Intrinsic verticalis contraction reduces the diameter of the central lumen around the lingual process, exerting pressure on the incompressible fluid there and causing the tongue to slide forward on the tapered process. (4) The tongue is lengthened hydrostatically by a reduction in its diameter. Clearly, these mechanisms are not mutually exclusive and they may combine to produce various tongue movements. Furthermore, they may vary in their importance along the length of the tongue. For example, the hindtongue may be more tightly coupled to hyobranchial movement than the foretongue, which might use hydrostatic lengthening to a greater extent (see Section VII,D). It is reasonably well established that lapping and tongue flicking involve primarily hydrostatic elongation of the foretongue in all squamates and that lingual movements during ingestion, intraoral transport, and swallowing in iguanians are coupled to hyobranchial movement, but the precise mechanism of tongue protrusion during lingual ingestion is problematic. The anatomy of the tongue-hyobranchial connection suggests that independent movement of the tongue should be limited in most iguanians (see earlier discussion). Schwenk and Throckmorton (1989) presented circumstantial cinegraphic data for Pogona (Agamidae) suggesting that tongue protrusion is coupled to hyoid protraction (model 1), as it is in Sphenodon and during intraoral transport in iguanians. In support of this, Herrel et al. (1995) showed that the mandibulohyoideus muscle is active during lingual protrusion in Agama and that the sternohyoideus is active during retraction, suggesting that tongue movement is coupled to hyobranchial movement. Films of lingual feeding in the iguanid Phrynosoma also indicate coupled tongue and hyobranchial movement during retraction (Schwenk, manuscript in preparation). However, Herrel et al. (1995) also found that the genioglossus and posterior verticalis ("ring" muscle) are active during lingual protraction in Agama with peak activities at maximum protrusion, thus indicating models 2 and 3. Together, data for Agama suggest that tongue protrusion occurs through a combination of models 1,2, and 3. Thus, current data suggest a combination of niechanisms for lingual protrusion during ingestion in iguanians, but so

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8. F e e d i n g in L e p i d o s a u r s

few species have been adequately studied that a great deal of functional diversity remains possible. Tongue protrusion occurs during SO (Figs. 8.22 and 8.23). SO II typically occurs at higher gape angles than in subsequent feeding stages, probably to accommodate the protruded tongue (Schwenk and Throckmorton, 1989). The difference in gape angle between SO II and maximum gape at the end of FO is correspondingly

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MILLISECONDS F I G U R E 8.22. Kinematics of lingual ingestion and transport in an iguanid lizard, Phrynosoma cornutum. Solid vertical lines indicate maximum and minimum gape angles, and the dotted vertical line indicates moment of tongue-prey contact. Note variation in the gape profiles of the two intraoral transport cycles. The first transport cycle following prey capture is often aberrant. During prey capture the head moves forward and down toward the prey item. Note that the head continues to move forward after tongue-prey contact, pinning the prey item to the substrate before it is retracted.

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protrude

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F I G U R E 8.23. Jaw and tongue kinematics during lingual prey capture in three iguanian lizards. In these plots the gape profile is shown inverted to facilitate comparison. In Chamaeleo the tongue is projected off the hyobranchium, but the timing of this behavior is similar to tongue protrusion in the generalized taxa, occurring at the end of SO II. The slight depression in gape at the end of SO II is unique to chameleons. (A) Dipsosaurus dorsalis (Iguanidae). Data from Schwenk and Throckmorton (1989). (B) Pogona barbata (Agamidae). Schwenk and Throckmorton, unpublished data. (C) Chamaeleo zeylanicus (Chamaeleonidae). Based on Bell (1990).

in several iguanids and agamids, including another species of Agama. Because prey size and type varied among these studies, it is not possible to separate treatment from species effects at this time. If the early part of ingestion is prolonged due to prey pursuit or lizard uncertainty (see earlier discussion), this is evident as a prolonged SO II phase. The distinction between SO I and SO II, and between the latter and FO, is sometimes vague so that jaw opening is more or less continuous before it is curtailed abruptly by FC (e.g., Bels, 1990, for Anolis). However, most ingestion gape cycles conform to the standard model with a pronounced "plateau phase" (Schwenk and Throckmorton, 1989) preceding rapid FO and FC phases (Figs. 8.22 and 8.23). SC or SCPS is generally short or sometimes absent depending on whether the prey comes to lie between the tooth rows or not (e.g., Herrel and De Vree, 1999a). There may be a short stationary phase before processing and transport cycles are initiated. Maximum gape angles vary radically within and among species (23° to 48°) without any clear pattern. Throckmorton (1976) showed that the lower jaw is protracted during tongue protrusion by means of quadrate rotation (streptostyly) in Uromastix, but not in Iguana. The gape cycle during ingestion in chameleons is remarkably similar to that described earlier for generalized iguanians, despite the addition of a ballistic projection interval to tongue protrusion (e.g., Bels and Baltus, 1987; Bell, 1990) (Fig. 8.23). The kinematics of ingestion in chameleons supports the notion that the projection interval has been inserted at the end of the SO phase in a generalized, ancestral ingestion cycle (Bramble and Wake, 1985; Schwenk and Bell, 1988; Schwenk and Throckmorton, 1989; see Section VI,A). EMG data for lingual ingestion are available only for Agama (Plocederma) stellio (Herrel et al, 1995). They sampled a variety of adductor and hyolingual musculature and found a mostly predictable pattern of activity. Low-level depressor mandibulae and pterygoideus profundus (lateralis) activity accompanies mouth opening during SO. Although the pterygoideus is usually regarded as an adductor, anatomical and functional data indicate that it may also function as a mandibular depressor and protractor (see discussion in Section IV,D). FO is initiated by a burst of depressor activity that is exactly coincident with tongue-prey contact, as the pterygoideus becomes nearly silent. Contraction of the spinalis capitis, a dorsal cervical muscle, also contributes to FO by raising the upper jaw through dorsal rotation of the skull at the neck. Pterygoideus activity spikes again during FC, along with the external and posterior adductors, as the depressor fades out. Pterygoideus activity fades out, in turn, during SC while the other adductors have a second, but lower burst of activity. The genioglossus muscle and

8. Feeding in Lepidosaurs the intrinsic "ring" muscle (posterior verticalis) are active throughout tongue protrusion during SO. As noted previously, this activity pattern is consistent with theoretical models of tongue protrusion in agamids. One noteworthy result of the EMG analysis of Herrel et al. (1995) is that the hyoglossus (tongue) muscle begins high levels of activity early in SO while the tongue is being protruded and continues throughout the gape cycle. Anatomically, the hyoglossus appears to be the principal lingual retractor (see earlier discussion), thus its activity during protrusion, with onset preceding significant genioglossus and verticalis activity, is unexpected. Herrel et al. (1995) suggested that hyoglossus activity causes hyobranchial protraction, but this could only occur if the tongue is held by antagonistic action of the genioglossus, which initially it is not. It is possible that genioglossus activity begins earlier in a part of the muscle not sampled (Herrel and colleagues did not specify whether the electrode was placed in the medialis or lateralis portion of the genioglossus). Continued activity of the hyoglossus during jaw closing is consistent with its putative role as a lingual retractor. A more plausible function of hyoglossus activity is provided by Herrel et al/s (1997a) study of intraoral transport and swallowing in the same species. They suggested that hyoglossus contraction during protrusion causes the tongue to shorten and "bulge." Such bulging, in conjunction with fixation of the tongue tip at the mandible by the genioglossus medialis (and internus in agamids) might contribute to the characteristic curled form of the tongue during prehension (Figs. 8.18 and 8.19). Indeed, lingual bulging is evident in the earliest stages of a prehension cycle. In any case, interpreting the action of lingual muscle activity is problematic because of the hydrostatic nature of the tongue (Schwenk, 2000a). Some activity might serve to stiffen the tongue or to deform it in ways that are not intuitive based on traditional musculoskeletal mechanics. 2. Processing Instances of preingestion processing are extremely rare in iguanians, as in all lepidosaurs. As noted earlier, the Galapagos land iguana (Conolophus) savors cactus pads, which it scrapes clean of spines and tough outer cuticle with the forelimbs before ingestion (Carpenter, 1969; Vagvolgyi and Vagvolgyi, 1978). In old accounts, the behavior of tongue-flicking prey before ingestion was often misinterpreted as preingestion lubrication! Food processing most often involves chewing with the marginal teeth following ingestion, but in many instances prey are not reduced at all before transport and swallowing. This happens when prey are very small (e.g., ants eaten by horned lizards; Schwenk,

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manuscript in preparation) or in herbivorous species that crop a mouth-sized portion of a plant during an initial ingestion cycle (e.g., Uromastix, Throckmorton, 1976; Sauromalus, Schwenk, unpublished observations). Iguanians specialized for vertebrate prey swallow it whole using a combination of inertial and hyolingual transport with minimal processing (personal observation). However, killing or crushing bites might be considered a kind of processing. For example, leopard lizards (Gamhelia) manipulate lizard prey until they are held by the neck and anterior torso transversely across the mouth. They are then killed by a series of small amplitude, crushing bites that probably cause death by interfering with cardiac function (Lappin, 1999). Killing bites and similar behaviors are hard to categorize. They usually follow ingestion but precede chewing in the strict sense, hence they might best be considered a separate class of manipulative cycle rather than processing per se. In most pleurodont and some acrodont species, chewing takes the form of simple puncture-crushing in which the food item is repeatedly crushed between upper and lower teeth with simple, vertical movements of the jaws. Throckmorton (1976, 1980) suggested the possibility of axial rotation of the mandibular rami during chewing in Uromastix, but this is unsubstantiated [Bradley (1903) suggested a similar movement in lizards, generally]. Asymmetrical chewing, a mobile joint between mandibular rami, and streptostyly all introduce the possibility of more complex chewing movements, but these have not been documented. Bels and Goosse (1989) speculated that lingual retraction of the food item during jaw closure might promote a shearing action by sliding it against the approaching teeth just before crushing. In agamids and chamaeleonids, tooth function during chewing may be more complex than simple puncture-crushing. This is because their acrodont dentition permits occlusion, i.e., the precise alignment of upper and lower teeth (see Section IV,B). In occlusal view, most acrodont teeth appear as a series of triangles, corner to corner, in a saw-tooth pattern. With jaws closed, the triangular upper and lower fit exactly between one another (Fig. 8.8B). The fit is so tight that wear facts develop, sharpening the edges. Such occlusion introduces a shearing action that may be more effective in reducing food, possible producing a greater degree of comminution than in pleurodonts. However, this has not been demonstrated. My own casual observations suggest no greater degree of comminution in acrodonts, but possibly the formation of a softer bolus than in iguanids feeding on identical prey. Functional analyses of chewing are available for the following taxa: Iguanidae: Anolis (Bels and Baltus, 1988, 1989; Bels and Goose, 1989); Ctenosaura (Smith,

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1984); Iguana (Throckmorton, 1976); Opiums (Delheusy and Bels, 1992); Agamidae: Agama (including Plocederma) (Kraklau, 1991; 1997a, 1998b); Pogona (Throckmorton and Clarke, 1981); Uromastix (Throckmorton, 1976,1978,1980; Herrel et al, 1998b); and Chamaeleonidae: Chamaeleo (So et ah, 1992). Schwenk and Throckmorton (1989), Herrel et al (1996a), and Herrel and De Vree (1999) did not distinguish between chewing and intraoral transport cycles sensu stricto in the several iguanid and agamid species they studied. According to Herrel et al. (1997a), in Agama these cycles differ mainly in the intensity of muscle activity rather than patterns of onset and offset, or other kinematic variables, and this may be a general phenomenon (but see Section V,B,2). In general, chewing cycles are kinematically similar to intraoral transport cycles (e.g., Herrel et al, 1996a); however, the single quantitative study of a chameleon found them to be distinct (So et al, 1992). Gape profiles are variable, as always, but typically show a pronounced SO interval that is usually, but not always, divisible into SO I and SO II phases. Surprisingly, an SC phase was not observed in chewing Anolis (Bels and Baltus, 1989; Bels and Goose, 1989). Smith (1984:129) found that during intraoral transport the tongue and hyobranchium moved anteriorly beneath the prey item in SO and were retracted in FO, in conformity with the model gape cycle, but during bite (chewing) cycles (interspersed between transport cycles), the tongue continued to move forward during FO "to place the food between the teeth in readiness for tooth contact in fast closing." Similar patterns were found by Bels and Goose (1989) in Anolis and Herrel and De Vree (1999a) in Uromastix, but Delheusy and Bels (1994) and Herrel et al. (1996a) found no difference in tongue movement between chewing and transport cycles for Oplurus and Agama, respectively, with retraction beginning at the start of FO. Based on superficial indications of hyobranchial position, Kraklau (1991) suggested that there was little hyobranchial movement associated with chewing cycles, but significant anteroposterior excursion during intraoral transport. In Chamaeleo, the principal difference between chewing and transport cycles is that the hyobranchium remains more or less stationary during the former, but follows a typical pattern of movement in the latter (So et al, 1992). However, So et al. (1992) noted that despite the stationary hyobranchium during chewing, prey items were manipulated by an independently mobile tongue (see Section VI). In general, the relationship between hyolingual movement and gape phase in different feeding stages is more variable than generally acknowledged, thus taxonomic differences are difficult to interpret. This issue is discussed further in Section VII. In any case, FC is virtually always accompanied by hyolingual retraction and

placement of the food item between the teeth. SC-PS begins with tooth-food contact as the prey item is crushed between upper and lower tooth rows. The number of chewing cycles is extremely variable and depends on species, prey type, and prey size (e.g., Bels and Baltus, 1988). Chewing cycles sometimes occur in clusters and sometimes are interspersed between transport cycles, but usually they occur early in a feeding sequence and are followed by an increasing number of transport cycles. In Chamaeleo, chewing cycles precede transport cycles (So et ah, 1992; Schwenk et al., manuscript in preparation). Maximum gape angles for reduction cycles are comparable to ingestion and transport with typical values in the range of 20° to 35°; however. So et al. (1992) found that maximum gape was greater in chewing than in transport in Chamaeleo (they did not specify a value). Feeding on large prey items incurs longer cycle times, but not larger excursion distances, in Agama (Herrel et al, 1996a); however, chewing cycles were not explicitly distinguished from transport cycles in this study. Muscle activity patterns during chewing cycles in Agama (Herrel et al, 1997a) are described later along with intraoral transport. Herrel et al. (1998a) modeled bite forces in two agamids, Agama (Plocederma) and Uromastix, and estimated bite forces of 6 to 10 and 8 to 14 newtons, respectively. Based on this and one other comparison of two scleroglossan species (see later), Herrel et al. (1998a) suggested that herbivorous species generate greater bite forces than related insectivores, but the study is not adequately controlled for phylogenetic effects and this conclusion is premature. Herrel et al. (1998b) modeled bite forces in the same taxa and concluded that the temporal ligaments serve to stabilize the quadrate for increasing bite force and that the jugomandibular modification of the ligament is particularly effective in maintaining joint alignment for resisting especially powerful bite forces in akinetic forms. There may be ontogenetic changes in the biting mechanism. Capel-Williams and Pratten (1978) found that allometric changes in jaw configuration during growth in Agama bibroni lead to a rapid bite that is two and a half times more powerful in adults than in juveniles. They suggested that these mechanical differences limit diet choice in juveniles and underlie an ontogenetic shift in diet. Rieppel and Labhardt (1979) found a similar ontogenetic transition in mandibular mechanics and diet in Varanus niloticus. 3. Intraoral

Transport

Functional analyses of intraoral transport are available for the following iguanian taxa: Iguanidae: Anolis (Bels and Baltus, 1988, 1989; Bels and Goosse, 1989);

8. Feeding in Lepidosaurs Ctenosaura (Smith, 1984); Dipsosaurus (Schwenk and Throckmorton, 1989); Iguana (Throckmorton, 1976; Schwenk and Throckmorton, 1989); Opiums (Delheusy and Bels, 1992); Phrynosoma (Schwenk and Throckmorton, 1989; Schwenk, manuscript in preparation); Sauromalus (Schwenk and Throckmorton, 1989); Agamidae: Agama (including Plocederma) (Herrel et ah, 1996a, 1997a); Phrynocephalus (Schwenk and Throckmorton, 1989); Pogona (Schwenk and Throckmorton, 1989); Uromastix (Throckmorton, 1976,1978,1980; Throckmorton and Clarke, 1981; Herrel and De Vree, 1999a); and Chamaeleonidae: Chamaeleo (So et ah, 1992). The account of a generalized, hyolingual transport cycle given earlier serves as an appropriate description for intraoral transport in most iguanians (Fig. 8.22), although Herrel et al (1996a) noted that the relative lengths of SO I and SO II phases are not always consistent with the Bramble and Wake (1985) model. The principal difference between ingestion and transport cycles may be that SO typically (but not always) occurs at a lower gape angle during transport because there is no need to accommodate a protruded tongue (Schwenk and Throckmorton, 1989). Smith (1984) showed that tongue and hyobranchial movements are tightly coupled during transport in Ctenosaura, as they are in Sphenodon. Kraklau (1991) observed significant hyobranchial excursions during transport in Agama. Delheusy and Bels (1992) found that the duration of the stationary phase was longer between transport cycles than chewing cycles and that the SO phase was proportionately longer. The latter observation is consistent with the suggestion that the tongue is formed to the prey item during transport SO II (Bramble and Wake, 1985). Light and cineradiographic films confirm this hypothesis, revealing considerable lingual shape change during SO that fits the lingual surface to the bolus in order to hold it for transport (Schwenk, unpublished observations). Bramble and Wake (1985) noted the presence of muscle fibers within the lingual papillae and suggested that active papillary movement might contribute to this process, but this is unconfirmed. Smith (1984) observed localized changes in tongue length such that the anterior part of the tongue elongated underneath the bolus and then contracted, followed by expansion of the posterior end relative to the hyobranchium. The posterior end then shortens toward the basihyal during retraction. The tongue usually arches dorsally and scrapes the palate in the early part of hyolingual retraction. The bolus is generally held on the posterior part of the tongue with the anterior part arched in front of it; however, sometimes the bolus simply adheres to the anterior part of the tongue as it is retracted. In Chamaeleo the dorsal surface of the glandular portion of the tongue forms a sigmoid curve with the bolus cupped in a posterior depression

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(Schwenk et ah, manuscript in preparation). In general, retraction is accompanied by considerable ventral movement of the tongue and hyobranchium. The ventral component of retraction is extremely pronounced in some taxa, such as Chamaeleo (Schwenk et ah, manuscript in preparation) and Phrynosoma (Schwenk, manuscript in preparation). At the end of retraction in these taxa the gular region forms a deeply distended pocket that is slowly elevated during hyolingual protraction of the next cycle. Ventral movement during retraction clears the bolus from any intraoral contact so that it can be moved far back into the pharynx. Herrel et ah (1996a) found that transport cycles were longer in duration in Agama feeding on large prey items but that there was no significant increase in maximal excursion distances of jaws and tongue. Food size and type also affect the number of transport cycles required to move the bolus into the pharynx (e.g., Bels and Baltus, 1988). Although it is likely that quantitative differences in transport cycles are related to differences in prey mass and the process of fitting the tongue to the bolus during SO II and the efficacy of the resulting adhesion (Bramble and Wake, 1985), this remains speculative. For example, Bels and Baltus (1988) found that some fruits took fewer cycles to transport than insects and related this to the lack of lingual adhesion due to expressed juices, but in fact, one would expect lowered adhesion to result in more transport cycles to compensate for the smaller posterior distance traveled by the bolus with each cycle. Alternatively, the fruit might have tended to liquefy and more or less flow into the pharynx, reducing the number of transport cycles (Bels and Baltus, 1988). Herrel and De Vree (1999a) found only minor kinematic differences in Uromastix feeding on two very different food types (endive leaves and locusts), but Herrel et ah (1996) found longer cycle times in Agama feeding on larger prey, which they interpreted as being consistent with the Bramble and Wake (1985) hypothesis. However, increased cycle times while feeding on more massive prey might be a general scaling effect on the entire feeding apparatus rather than a specific consequence of tongue fitting and adhesion. Although Herrel and De Vree (1999a) did not distinguish chewing from transport cycles in Uromastix, they seemed to imply that, in all such cycles, tongue protraction continues through FO and that retraction does not begin until FC (see Section V,D,2). Bels and Goosse (1989) found the same pattern in Anolis. This pattern is similar to biting cycles described by Smith (1984), but is inconsistent with the model gape cycle and kinematic patterns during intraoral transport in other taxa. As noted previously, there is considerable variation in these kinematic relationships with no functional or phylogenetic pattern discernible thus far (see Section VII).

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Herrel et al (1997a) provided EMG data for transport cycles in Agama. Muscle activity patterns were similar to "crushing" (chewing) cycles except that in the latter, muscle activity levels were significantly higher, particularly in the anterior part of the adductor mandibulae externus superficialis. During SO, as the tongue is protracted, virtually all lingual muscles are active (genioglossus medialis and lateralis, hyoglossus, posterior verticalis). Although activity of the genioglossus and verticalis muscles is consonant with models of tongue protrusion, activity of the hyoglossus muscle, a putative retractor, is unexpected. This pattern is discussed in Section V,D,1. Herrel et al. (1997a: 112) suggested that hyoglossus activity shortens the tongue and in conjunction with protraction "causes the tongue to bulge, thus pushing it against the prey item." They noted that Anolis exhibited the same activity pattern (J. Cleuren and F. De Vree, in Herrel et al, 1997a). Although the "bulging" hypothesis is consistent with tongue deformation during ingestion (see earlier discussion), its timing during transport is more critical. Initially the tongue is "slid" underneath the bolus and bulging could not occur until the end of SO II when the tongue is fitted to the food item and readied for retraction. The mandibulohyoideus is active, presumably to protract the hyobranchium, and the stemohyoideus is active at very low levels, possibly to keep the hyobranchium in tension during protraction for better control and to initiate a rapid reversal at FO for hyolingual retraction. Herrel et al. (1997a) also noted low levels of activity in several adductors during SO II. Mouth opening is primarily caused by mandibular depression with contraction of the depressor mandibulae, but at FO a burst of activity in the dorsal cervical muscles (spinalis capitis) causes elevation of the cranium as well. The adductors (adductor mandibulae externus superficialis anterior and externus medialis, adductor mandibulae posterior, pseudotemporalis, ptergoideus superficialis and profundus) are active almost simultaneously at the beginning of jaw closing, although peak activity in the adductor mandibulae externus and pseudotemporalis lags a few milliseconds behind. Several of the adductors show biphasic activity, especially the adductor mandibulae posterior and the pterygoideus superficialis, with the second burst associated with SC. A true power stroke (SC-PS) only occurs during chewing cycles. In chewing cycles, adductor activity becomes more synchronous, and the high levels of activity tend to blot out the biphasic pattern, except in the pterygoideus superficialis. Activity of the hyobranchial retractors (stemohyoideus and omohyoideus) begins just prior to FO and, along with a burst of activity in the hyoglossus, causes rapid retraction of the tongue and hyobranchial apparatus.

Limited inertial transport has been observed in several iguanians. Smith (1984) noted that Ctenosaura used inertial transport for large or heavy food items, as did Throckmorton (1976) for Iguana and Uromastix, but large prey or heavy items are not typical of the natural diet in these species. In contrast, leopard lizards (Gatnbelia) routinely consume extremely large lizard prey and one might expect inertial transport to predominate. However, Lappin (personal communication) observed that, "Inertial transport may play a minor role, but there is a lot of hyolingual activity, even with the largest lizard prey" (see Lappin, 1999). Delheusy and Bels (1992) found that Opiums used an inertial transport cycle immediately following ingestion to position the prey item posteriorly at the corner of the mouth for chewing. Subsequent chewing and transport cycles were all hyolingual. Manipulation, rather than transport per se, may be the most typical use of inertial movements in iguanians. 4.

Swallowing

As noted previously, swallowing in lepidosaurs potentially consists of two kinematic stages, pharyngeal packing and pharyngeal compression, but in some cases the former is sufficient to engage peristalsis and compression is unnecessary to complete the act of swallowing. Our films suggest that when feeding on small, naturalistic prey items, pharyngeal compression is rare in iguanians and when it occurs it is very subtle and brief (Schwenk, unpublished results; Schwenk and Throckmorton, unpublished results). Iguanians seem to rely primarily on pharyngeal packing for swallowing with pharyngeal compression more common in scleroglossans. a. Pharyngeal Packing Pharyngeal packing is frequently described in the literature as "swallowing," "cleaning," and "lip licking," as discussed earlier. In some studies it is clear that descriptions of terminal transport cycles are actually transitional packing cycles. Sometimes packing and cleaning are described separately, but again, the distinction seems to relate to the changing kinematics of pharyngeal packing during a sequence of cycles, with "cleaning" cycles the last of the series before pharyngeal compression, if it occurs. Consequently, my delimitation of pharyngeal packing (based partly on my own observations) does not always agree precisely with descriptions in the literature. In any case, as has been noted several times already, feeding stages tend to blend into one another functionally and kinematically.

8. Feeding in Lepidosaurs Functional accounts of pharyngeal packing are limited to the following taxa: Iguanidae: Anolis (Bels and Baltus, 1988); Ctenosaura (Smith, 1984); Opiums (Delheusy and Bels, 1992); Agamidae: Agama (including Plocederma) (Fierrel et ah, 1996a, 1997a); and Uromastix (Throckmorton, 1980; Herrel and De Vree, 1999a). Smith (1984) first described pharyngeal packing in Ctenosaura. She found that packing cycles differed from intraoral transport in having lower amplitude gapes and different tongue movements due to a shift of bolus position from the dorsal surface of the tongue to mostly behind it. During SO the tongue is positioned in front of and above the bolus. With the bolus so positioned, the tongue is able to push the bolus posterior to the basihyal so that pharyngeal compression will squeeze it into the esophagus and not back into the mouth. The posterior end of the tongue, presumably the posterior limbs, is used to "tamp" the bolus into the pharynx and/or the esophagus. This usually involves high amplitude anteroposterior excursion of the hyolingual apparatus and often includes tongue protrusion during the protraction phase, especially in terminal cycles. The tongue protrudes tip first, either straight ahead or to the side, and often 'Ticks" the labial scales from one side to the other. For example, after consumption of a cactus pad, a land iguana {Conolophus) initiated "a long series of gulping movements . . . at least 43 in number. After each gulp the iguana extended its tongue slightly and licked its labials" (Vagvolgyi and Vagvolgyi (1978:162). I interpret the asymmetry of these movements to indicate asymmetrical use of the posterior limbs during the retraction phase—possibly one limb is used at a time. The protrusion may help maximize the anterior excursion of the tongue and hyobranchium to position the bolus behind the tongue more effectively and also help orient the hindtongue and posterior limbs side to side. Herrel et al. (1996a) suggested that initial packing cycles move the bolus into the esophagus and that in later cycles the tongue moves anteriorly beyond the bolus, "bulges," and then pushes the bolus farther into the esophagus. Delheusy and Bels (1992) noted that packing cycles in which the tongue was protruded were more effective at moving the bolus posteriorly than cycles without protrusion. They speculated that intrinsic shape changes in the tongue might promote the storage of elastic strain energy in the laryngohyoid ligament such that the hindtongue would "snap" back to accelerate the bolus posteriorly (also see Bels et ah, 1994), but the nature of tongue deformation does not suggest the ligament is being stretched and therefore does not support their hypothesis. The hypothesis also assumes that the larynx remains fixed so that the ligament is stretched when the tongue is protracted, but our films

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show that this does not occur during ingestion in Pogona (Schwenk and Throckmorton, unpublished observations) nor in Sphenodon (see earlier discussion; also see description of the ligament in Section IV,E,2), suggesting that the tongue and the larynx are coupled anatomically and kinematically. However, it is unknown if laryngeal coupling via the laryngohyoid ligament maintains for other feeding stages and in other taxa. Herrel et al. (1996a) found the kinematics of pharyngeal packing to be roughly similar to transport cycles in Agama, but with a shorter FO phase, a lower maximum gape angle, and the absence of an SC-PS phase. They also noted that the distinction between SO I and SO II is weak or absent. They attributed this to the posterior position of the bolus, which implies that it does not require tongue fitting, the putative mechanistic basis of a pronounced SO II (Bramble and Wake, 1985). However, packing cycles are kinematically very distinct in Uromastix (Herrel and De Vree, 1999a). In comparison to transport cycles, packing cycles have smaller gape angles with virtually no contribution of cranial elevation to FO, a longer SO phase, and greater tongue excursions (Fig. 8.24). During retraction, "the posterior edge of the tongue" is used to push the bolus posteriorly. As in transport in this species (see earlier discussion), the tongue continues to move anteriorly during FO with maximum tongue protraction corresponding closely with maximum gape. There is a tendency for tongue retraction to be faster during pharyngeal packing. Delheusy and Bels (1992) also noted that terminal packing cycles with tongue protrusion had smaller gape amplitudes than earlier cycles, as did Smith (1984). Muscle activity patterns during pharyngeal packing are distinctly different from intraoral transport in Agama with differences concentrated in the adductor musculature (Herrel et ah, 1997a). Small differences occur in the relative timing of the hyolingual muscles, but the pattern is generally similar to transport (see earlier discussion). In late packing cycles, depressor mandibulae and spinalis capitis activity is often absent. Given the reduced gape angles in these later cycles it is possible that gravity and mechanical displacement by the bulging tongue during retraction are sufficient to depress the mandible. At jaw closing, the adductors become active as in transport, but only the "deeper parts" of the adductor mandibulae externus, adductor mandibulae posterior, and the pterygoideus remain active through the cycle. Hyolingual retraction is driven by activity of the sternohyoideus and hyoglossus. Herrel et ah (1997a) noted that activity patterns were highly variable among packing cycles. This presumably reflects the rapidly changing position and condition of the bolus as it is tamped, in contract to

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TIME (SEC) F I G U R E 8.24. Jaw kinematics during intraoral transport and pharyngeal packing. (Top) Uromastix acanthinurus (Iguania, Agamidae). Based on Herrel and De Vree (1999a). (Bottom) Tiliqua rugosa (Scleroglossa, Scincidae). Based on Herrel et al. (1999b).

the more stereotypical movements of chewing and transport. h. Pharyngeal Compression Accounts of pharyngeal compression in iguanians are restricted to the following references: Iguanidae: Ctenosaura (Smith, 1984); Gambelia (Lappin, 1999); and Agamidae: Agama (Herrel et al, 1996a). Schwenk (unpublished results) and Schwenk and Throckmorton (unpublished results) have film data for several other iguanids and agamids. Ctenosaura elevates the head and uses neck bending rather than hyobranchial elevation for pharyngeal compression, but only for large food items. The natural diet of Ctenosaura would rarely include large prey items, hence this behavior may be aberrant. This is in contrast to a scleroglossan, Tupinambis, which relies heavily on hyobranchial elevation for swallowing, presumably by constrictor colli contraction (Smith, 1984; see later). Gambelia eating large lizard prey uses lateral bending of the neck to force it farther posterior once the prey item is partially engulfed (Lappin, 1999). Her-

rel et al (1996a:1734) did not recognize pharyngeal compression as a separate component of swallowing in Agama, noting only that, "Once inside the esophagus, constriction of the throat region pushes the prey further down." Our films of various iguanians eating small insect prey suggest that pharyngeal compression of any kind is rare, occurring sporadically and unpredictably after pharyngeal packing, and is usually limited to a single, small compressive cycle evident as elevation of the hyobranchium. However, we did not test the animals with larger prey, although Iguana swallowing bulky lettuce leaves did not compress the pharynx.

E. Feeding in Scleroglossa 1. Ingestion Ingestion has been poorly studied in scleroglossans. This account is based on the following references, as well as my own observations: Gekkota: Lialis (Patchell and Shine, 1986; Murray et al, 1991); Eublepharus (Delheusy et al, 1995); Scincomorpha: Tiliqua {Trachydosau-

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