Feeding in Vertebrates: Evolution, Morphology, Behavior, Biomechanics [1st ed.] 978-3-030-13738-0;978-3-030-13739-7

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Feeding in Vertebrates: Evolution, Morphology, Behavior, Biomechanics [1st ed.]
 978-3-030-13738-0;978-3-030-13739-7

Table of contents :
Front Matter ....Pages i-xviii
Feeding, a Tool to Understand Vertebrate Evolution Introduction to “Feeding in Vertebrates” (Vincent Bels, Anthony Herrel)....Pages 1-18
Front Matter ....Pages 19-19
Functional Morphology of Vertebrate Feeding Systems: New Insights from XROMM and Fluoromicrometry (Elizabeth L. Brainerd, Ariel L. Camp)....Pages 21-44
What Does Musculoskeletal Mechanics Tell Us About Evolution of Form and Function in Vertebrates? (Emily J. Rayfield)....Pages 45-70
Food Capture in Vertebrates: A Complex Integrative Performance of the Cranial and Postcranial Systems (Stéphane J. Montuelle, Emily A. Kane)....Pages 71-137
Transitions from Water to Land: Terrestrial Feeding in Fishes (Sam Van Wassenbergh)....Pages 139-158
The Evolution of the Hand as a Tool in Feeding Behavior: The Multiple Motor Channel Theory of Hand Use (Ian Q. Whishaw, Jenni M. Karl)....Pages 159-186
Front Matter ....Pages 187-187
Feeding in Jawless Fishes (Andrew J. Clark, Theodore A. Uyeno)....Pages 189-230
Feeding in Cartilaginous Fishes: An Interdisciplinary Synthesis (Daniel Huber, Cheryl Wilga, Mason Dean, Lara Ferry, Jayne Gardiner, Laura Habegger et al.)....Pages 231-295
Functional Morphology and Biomechanics of Feeding in Fishes (Nicholas J. Gidmark, Kelsie Pos, Bonne Matheson, Esai Ponce, Mark W. Westneat)....Pages 297-332
Evolutionary Specialization of the Tongue in Vertebrates: Structure and Function (Shin-ichi Iwasaki, Serkan Erdoğan, Tomoichiro Asami)....Pages 333-384
Tetrapod Teeth: Diversity, Evolution, and Function (Peter S. Ungar, Hans-Dieter Sues)....Pages 385-429
Feeding in Amphibians: Evolutionary Transformations and Phenotypic Diversity as Drivers of Feeding System Diversity (Anthony Herrel, James C. O’Reilly, Anne-Claire Fabre, Carla Bardua, Aurélien Lowie, Renaud Boistel et al.)....Pages 431-467
Feeding in Lizards: Form–Function and Complex Multifunctional System (Vincent Bels, Anne-Sophie Paindavoine, Leïla-Nastasia Zghikh, Emeline Paulet, Jean-Pierre Pallandre, Stéphane J. Montuelle)....Pages 469-525
Feeding in Snakes: Form, Function, and Evolution of the Feeding System (Brad R. Moon, David A. Penning, Marion Segall, Anthony Herrel)....Pages 527-574
Feeding in Crocodylians and Their Relatives: Functional Insights from Ontogeny and Evolution (Paul M. Gignac, Haley D. O’Brien, Alan H. Turner, Gregory M. Erickson)....Pages 575-610
Feeding in Turtles: Understanding Terrestrial and Aquatic Feeding in a Diverse but Monophyletic Group (Patrick Lemell, Nikolay Natchev, Christian Josef Beisser, Egon Heiss)....Pages 611-642
Feeding in Birds: Thriving in Terrestrial, Aquatic, and Aerial Niches (Alejandro Rico-Guevara, Diego Sustaita, Sander Gussekloo, Aaron Olsen, Jen Bright, Clay Corbin et al.)....Pages 643-693
Feeding in Mammals: Comparative, Experimental, and Evolutionary Insights on Form and Function (Susan H. Williams)....Pages 695-742
Feeding in Aquatic Mammals: An Evolutionary and Functional Approach (Christopher D. Marshall, Nicholas D. Pyenson)....Pages 743-785
Evolution, Constraint, and Optimality in Primate Feeding Systems (Callum F. Ross, Jose Iriarte-Diaz)....Pages 787-829
The Masticatory Apparatus of Humans (Homo sapiens): Evolution and Comparative Functional Morphology (Christopher J. Vinyard, Mark F. Teaford, Christine E. Wall, Andrea B. Taylor)....Pages 831-865

Citation preview

Fascinating Life Sciences

Vincent Bels Ian Q. Whishaw Editors

Feeding in Vertebrates Evolution, Morphology, Behavior, Biomechanics

Fascinating Life Sciences

This interdisciplinary series brings together the most essential and captivating topics in the life sciences. They range from the plant sciences to zoology, from the microbiome to macrobiome, and from basic biology to biotechnology. The series not only highlights fascinating research; it also discusses major challenges associated with the life sciences and related disciplines and outlines future research directions. Individual volumes provide in-depth information, are richly illustrated with photographs, illustrations, and maps, and feature suggestions for further reading or glossaries where appropriate. Interested researchers in all areas of the life sciences, as well as biology enthusiasts, will find the series’ interdisciplinary focus and highly readable volumes especially appealing.

More information about this series at http://www.springer.com/series/15408

Vincent Bels Ian Q. Whishaw •

Editors

Feeding in Vertebrates Evolution, Morphology, Behavior, Biomechanics

123

Editors Vincent Bels Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA Muséum national d’Histoire naturelle Paris, France

Ian Q. Whishaw Canadian Center for Behavioural Neuroscience University of Lethbridge Lethbridge, AB, Canada

ISSN 2509-6745 ISSN 2509-6753 (electronic) Fascinating Life Sciences ISBN 978-3-030-13738-0 ISBN 978-3-030-13739-7 (eBook) https://doi.org/10.1007/978-3-030-13739-7 Library of Congress Control Number: 2019932703 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Cover credit: Amy Knowlton, New England Aquarium, NOAA Permit Number 15415 This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Foreword

This volume, assembled and edited by Bels and Whishaw, is a significant, scholarly, assessment of the current research on the evolution of vertebrate feeding systems in the context of the “form–function complex”. It constitutes a major contribution that: (1) illustrates the continuing integration across biological subfields to analyze complex systems, (2) celebrates technical advances, ranging from CT scanning and PIV to sophisticated analytical and statistical methodologies, (3) incorporates phylogenetic perspectives that are essential for evolutionary research, and (4) shows how diversity of methods and organisms is essential for advancing the field of evolutionary morphology. Anatomy/morphology reigned as the king of the biological sciences in the mid— to the late nineteenth century, where its dominance was evident in Germany in particular. But newer fields, especially physiology and development, gradually superseded the older approaches, which slowly declined in influence. By the 1960s and 1970s, the change was evident. Functional morphology—exploration of the form–function interaction—developed rapidly and the first glimmerings of biomechanics could be seen. Phylogenetics became a necessary component of comparative investigations, including a renewed focus on the relation of ontogeny to phylogeny. Hypotheses and tests were increasingly emphasized. Development, behavior, and ecology became major components of functional studies. A renaissance of morphology was evident by the early 1980s. Key to the rebirth was a new sharp focus on problems and solutions, rather than description for its own sake. Studies of trophic systems began to consider the links among perception, integration, and action. Integrative approaches, frequently including either/both ontogenetic and paleontological time dimensions, were increasingly utilized. Central to the new movements were the rebirth of venerable organizations, for example, the American Society of Zoologists, which became the Society of Integrative and Comparative Biology (SICB) near the end of the twentieth century, and the appearance of new international organizations, such as the International Congress of Vertebrate Morphology (ICVM), which reliably meets every third year at diverse sites around the world. The programs of these organizations offer amazingly rich and diverse arrays of speakers and workshops and attract large v

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Foreword

audiences of lively young people, as well as more seasoned researchers. We live in an age of excitement and opportunity for research in the field relevant to the present volume. We are delighted to see that this entire volume presents the advances in our science using cases to represent the diversity of research perspectives on major chordate and vertebrate lineages. By presenting these in such a broadly comparative framework, many new ideas and extensive new research into the functional biology, sensu lato, of feeding will be stimulated. This volume is a thoughtful, erudite, compendium of research formulation and ideas. The authors and editors have given researchers a forward-thinking overview. We predict that it will prove to be a resource for researchers in many subfields of biology, serving to integrate and synthesize new conceptions of the evolution and function of trophic systems. Marvalee H. Wake David B. Wake

Acknowledgements

The genesis of this book is based on the invitation of Lars Koerner from Springer to provide a new insight of our understanding of the evolution of the feeding behaviors and mechanisms in vertebrates. We would express our gratitude for his support and understanding through the approval process at Springer and the conceptual construction of the book. This book concerns our understanding of feeding in chordates and vertebrates and its role in the ecological and evolutionary processes. The book was conceptualized by Vincent Bels (Museum national d’Histoire naturelle, Paris, France), who then asked Ian Q. Whishaw (University of Lethbridge, Lethbridge, Canada) to join him as co-editor, providing them with an excellent opportunity to work together on this project devoted to the understanding of the evolution of feeding behavior. This volume would never have been possible without the contributions of experts, who covered a series of field of researches from anatomy, biomechanics, to neurobiology, and behavioral ecology to attempt to provide hopefully an integrative approach of feeding behavior of chordates and vertebrates. We are highly indebted to all of them, and acknowledge their wonderful work, patience, understanding, and comprehension to build this book that tries to integrate a variety of approaches for future researches. Such book would not be possible without the help of a lot of colleagues who reviewed one or more of the chapters, providing absolutely excellent insights substantially improve of all of the contributions: Peter Aerts, University of Antwerp, Antwerpen, Belgium; Elizabeth Brainerd, Brown University, Providence, USA; Chris Broeckhoven, University of Antwerp, Antwerpen, Belgium; Matthew McCurry, The Australian Museum, Sydney, Australia; Ariel Camp, University of Liverpool, Liverpool, UK; Andrew Clark, College of Charleston, Charleston, USA; Gregory M. Erickson, Florida State University, Tallahassee, USA; Lara Ferry, Arizona State University, Glendale, USA; Serkan Erdogan, Namik Kemal University, Terkirdag, Turkey; Egon Heiss, Friedrich-Schiller-University of Jena, Jena, Germany; Juan Pablo Gailer, Universität Hamburg—Zoologisches Museum, Hamburg, Germany; Paul M. Gignac, Oklahoma State University, Tulsa, USA; Anthony Herrel, Museum national d’Histoire naturelle, Paris, France;

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Acknowledgements

Fritz Hertel, California State University, Northbridge, USA; Jose (Pepe) Iriarte-Diaz, University of Illinois at Chicago, Chicago, USA; Patrick Lemell, University of Vienna, Vienna, Austria; Christopher D. Marsall, Texas A&M University, Galveston, USA; Rachel Menegaz, University of North Texas, Fort Worth, USA; Stéphane J. Montuelle, Ohio University, Warrensville, USA; Nicolas Natchev, Shumen University, Shumen, Bulgaria; Kiisa Nishikawa, Northern Arizona University, Flagstaff, USA; Matthew J. Ravosa, University of Notre Dame, Notre Dame, USA; Emily Rayfield, University of Bristol, Bristol, UK; Alejandro Rico-Guevara, University of California at Berkeley, Berkeley, USA; Callum F. Ross, The University of Chicago, Chicago, USA; Peter Ungar, University of Arkansas, Fayetteville, USA; Christopher J. Vinyard, Northeast Ohio Medical University, USA; Sam van Wassenberg, Museum national d’Histoire naturelle, Paris, France; Susan H. Williams, Ohio University, Athens, USA; Mark W. Westneat, University of Chicago, Chicago, USA. Finally, we are pleased to thank Arumugam Deivasigamani and Anette Lindqvist for their invaluable help in the editorial and production processes of the book.

Contents

1

Feeding, a Tool to Understand Vertebrate Evolution Introduction to “Feeding in Vertebrates” . . . . . . . . . . . . . . . . . . . . Vincent Bels and Anthony Herrel

Part I 2

3

4

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Overview: From Structure to Behavior

Functional Morphology of Vertebrate Feeding Systems: New Insights from XROMM and Fluoromicrometry . . . . . . . . . . . Elizabeth L. Brainerd and Ariel L. Camp

21

What Does Musculoskeletal Mechanics Tell Us About Evolution of Form and Function in Vertebrates? . . . . . . . . . . . . . . . . . . . . . . Emily J. Rayfield

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Food Capture in Vertebrates: A Complex Integrative Performance of the Cranial and Postcranial Systems . . . . . . . . . . . Stéphane J. Montuelle and Emily A. Kane

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Transitions from Water to Land: Terrestrial Feeding in Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sam Van Wassenbergh

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The Evolution of the Hand as a Tool in Feeding Behavior: The Multiple Motor Channel Theory of Hand Use . . . . . . . . . . . . Ian Q. Whishaw and Jenni M. Karl

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Part II 7

1

Anatomy, Biomechanics and Behavior in Chordate and Vertebrate Lineages

Feeding in Jawless Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Andrew J. Clark and Theodore A. Uyeno

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Contents

Feeding in Cartilaginous Fishes: An Interdisciplinary Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Daniel Huber, Cheryl Wilga, Mason Dean, Lara Ferry, Jayne Gardiner, Laura Habegger, Yannis Papastamatiou, Jason Ramsay and Lisa Whitenack Functional Morphology and Biomechanics of Feeding in Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nicholas J. Gidmark, Kelsie Pos, Bonne Matheson, Esai Ponce and Mark W. Westneat

10 Evolutionary Specialization of the Tongue in Vertebrates: Structure and Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Shin-ichi Iwasaki, Serkan Erdoğan and Tomoichiro Asami 11 Tetrapod Teeth: Diversity, Evolution, and Function . . . . . . . . . . . Peter S. Ungar and Hans-Dieter Sues 12 Feeding in Amphibians: Evolutionary Transformations and Phenotypic Diversity as Drivers of Feeding System Diversity . . . . Anthony Herrel, James C. O’Reilly, Anne-Claire Fabre, Carla Bardua, Aurélien Lowie, Renaud Boistel and Stanislav N. Gorb 13 Feeding in Lizards: Form–Function and Complex Multifunctional System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vincent Bels, Anne-Sophie Paindavoine, Leïla-Nastasia Zghikh, Emeline Paulet, Jean-Pierre Pallandre and Stéphane J. Montuelle 14 Feeding in Snakes: Form, Function, and Evolution of the Feeding System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Brad R. Moon, David A. Penning, Marion Segall and Anthony Herrel 15 Feeding in Crocodylians and Their Relatives: Functional Insights from Ontogeny and Evolution . . . . . . . . . . . . . . . . . . . . . Paul M. Gignac, Haley D. O’Brien, Alan H. Turner and Gregory M. Erickson 16 Feeding in Turtles: Understanding Terrestrial and Aquatic Feeding in a Diverse but Monophyletic Group . . . . . . . . . . . . . . . Patrick Lemell, Nikolay Natchev, Christian Josef Beisser and Egon Heiss 17 Feeding in Birds: Thriving in Terrestrial, Aquatic, and Aerial Niches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Alejandro Rico-Guevara, Diego Sustaita, Sander Gussekloo, Aaron Olsen, Jen Bright, Clay Corbin and Robert Dudley

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Contents

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18 Feeding in Mammals: Comparative, Experimental, and Evolutionary Insights on Form and Function . . . . . . . . . . . . . Susan H. Williams

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19 Feeding in Aquatic Mammals: An Evolutionary and Functional Approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Christopher D. Marshall and Nicholas D. Pyenson

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20 Evolution, Constraint, and Optimality in Primate Feeding Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Callum F. Ross and Jose Iriarte-Diaz

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21 The Masticatory Apparatus of Humans (Homo sapiens): Evolution and Comparative Functional Morphology . . . . . . . . . . . Christopher J. Vinyard, Mark F. Teaford, Christine E. Wall and Andrea B. Taylor

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Editors and Contributors

About the Editors Vincent Bels was born in Verviers, Belgium. His Ph.D., Ethology and Functional Morphology, at the University of Liège (Liège, Belgium), integrated theoretical concepts to morphology and behavior in feeding animals. He has used lizards as a model to clarify the process of behavioral ritualization in evolution. He was Research Fellow and then Assistant at the University of Liège (Belgium). Then taught Biology, Zoology, and Ecology and developed applied research methods for studying feeding behavior in domestic animals at Hautes Ecoles (Hainaut, Belgium) and the Associated Agronomic Centre (Belgium). He is now a Professor at the Muséum national d’Histoire naturelle (Paris, France), where he has served as joint director of one Research Mixed Unit (CNRS/MNHN, France). He has taught Functional Morphology at the University of Mons (Belgium). He belongs to the Scientific Committee of Muséum National d’Histoire Naturelle (Paris, France), and serves at Scientific Sections of the Centre National de Recherche Scientifique (CNRS, France). He has authored over 80 peer-reviewed articles, 10 chapters, and 6 books on feeding and locomotion in Vertebrates. In 1994, he edited “Biomechanics of Feeding in Vertebrates” in the series Advances in Comparative and Environmental Physiology (Volume 18) published by Springer. This volume provides a comprehensive description of the evolution of feeding behavior in vertebrates by integrating feeding in aquatic and terrestrial animals. Professor Bels’ research is dedicated to feeding, drinking, and displays in lizards, turtles, and birds but he has also studied feeding and the relation between feeding and locomotion in vertebrates. His research goal is to integrate behavioral, physiological, and morphological science into a comprehensive understanding of the “Form–Function” relationship of the trophic system in vertebrates.

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Ian Q. Whishaw received his Ph.D. from Western University and is a Professor of Neuroscience at the University of Lethbridge. He has held visiting appointments at the University of Texas, University of Michigan, Cambridge University, and the University of Strasbourg. He is a fellow of Clair Hall, Cambridge, the Canadian Psychological Association, the American Psychological Association, and the Royal Society of Canada. He is a recipient of the Canadian Humane Society Bronze medal for bravery, the Ingrid Speaker Gold medal for research, the distinguished teaching medal from the University of Lethbridge and the Donald O Hebb Prize. He has received the Key to the City of Lethbridge and has honorary doctorates from Thompson Rivers University and the University of Lethbridge. He is a coauthor of a major introductory textbook in Behavioural Neuroscience and a major senior textbook in Neuropsychology. His research addresses the neural basis of skilled movement and the neural basis of brain disease. The Institute for Scientific Information includes him in its list of most cited neuroscientists. His hobby is training horses for western performance events.

Contributors Tomoichiro Asami Faculty of Health Science, Gunma PAZ University, Takasaki, Gunma, Japan Carla Bardua Life Sciences Department, The Natural History Museum, London, UK Christian Josef Beisser Department of Integrative Zoology, University of Vienna, Vienna, Austria Vincent Bels Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA, Muséum national d’Histoire naturelle, Paris, France Renaud Boistel IPHEP, Université de Poitiers, UMR CNRS 7262, Poitiers, France Elizabeth L. Brainerd Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA Jen Bright School of Geosciences, University of South Florida, Tampa, USA Ariel L. Camp Department of Musculoskeletal Biology, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, UK Andrew J. Clark Department of Biology, College of Charleston, Charleston, SC, USA Clay Corbin Department of Biological and Allied Health Sciences, Bloomsburg University, Bloomsburg, PA, USA

Editors and Contributors

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Mason Dean Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany Robert Dudley Department of Integrative Biology, University of California, Berkeley, CA, USA Smithsonian Tropical Research Institute, Balboa, Republic of Panama Serkan Erdoğan Department of Anatomy, Faculty of Veterinary Medicine, Namık Kemal University, Tekirdağ, Turkey Gregory M. Erickson Florida State University, Tallahassee, FL, USA; National High Magnetic Field Laboratory, Tallahassee, FL, USA Anne-Claire Fabre Life Sciences Department, The Natural History Museum, London, UK Lara Ferry Math and Natural Sciences Division, Arizona State University, Glendale, AZ, USA Jayne Gardiner Division of Natural Sciences, New College of Florida, Sarasota, FL, USA Nicholas J. Gidmark Department of Biology, Knox College, Galesburg, IL, USA Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA Paul M. Gignac Oklahoma State University Center for Health Sciences, Tulsa, OK, USA Stanislav N. Gorb Department of Functional Morphology and Biomechanics, Christian-Albrechts-Universität Kiel, Kiel, Germany Sander Gussekloo Department of Animal Sciences, Experimental Zoology Group, Wageningen, The Netherlands Laura Habegger Biology Department, Florida Southern College, Lakeland, FL, USA Egon Heiss Institute Zoology and Evolutionary Research, Friedrich-SchillerUniversity of Jena, Jena, Germany Anthony Herrel Département Adaptations du Vivant, Muséum national d’Histoire naturelle, UMR 7179 C.N.R.S/M.N.H.N, Paris, France Daniel Huber Department of Biology, The University of Tampa, Tampa, FL, USA Jose Iriarte-Diaz Department of Oral Biology, College of Dentistry, University of Illinois at Chicago, Chicago, USA

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Editors and Contributors

Shin-ichi Iwasaki Department of Medical Technology and Clinical Engineering, Faculty of Health and Medical Sciences, Hokuriku University, Kanazawa, Ishikawa, Japan The Nippon Dental University, Tokyo, Niigata, Japan Emily A. Kane Georgia Southern University, Statesboro, GA, USA Jenni M. Karl Department of Psychology, Thompson Rivers University, Kamloops, Canada Patrick Lemell Department of Integrative Zoology, University of Vienna, Vienna, Austria Aurélien Lowie Department of Biology Evolutionary, Morphology of Vertebrates, Ghent University, Ghent, Belgium Christopher D. Marshall Department of Marine Biology and Department of Wildlife & Fisheries Sciences, Texas A&M University, Galveston, USA Bonne Matheson Department of Biology, Knox College, Galesburg, IL, USA Stéphane J. Montuelle Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Warrensville Heights, OH, USA Brad R. Moon Department of Biology, University of Louisiana at Lafayette, Lafayette, LA, USA Nikolay Natchev Department of Biology, Faculty of Natural Science, Shumen University, Shumen, Bulgaria Haley D. O’Brien Oklahoma State University Center for Health Sciences, Tulsa, OK, USA James C. O’Reilly Department of Biomedical Sciences, Ohio University, Cleveland, Ohio, USA Aaron Olsen Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA Anne-Sophie Paindavoine Laboratory of Histology, Faculty of Medicine and Pharmacy, Institute of BioSciences, University of Mons, Mons, Belgium Jean-Pierre Pallandre Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA, Muséum national d’Histoire naturelle, Paris, France Yannis Papastamatiou Marine Sciences University, North Miami, FL, USA

Program,

Florida

International

Emeline Paulet Laboratory of Histology, Faculty of Medicine and Pharmacy, Institute of BioSciences, University of Mons, Mons, Belgium

Editors and Contributors

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David A. Penning Department of Biology & Environmental Health, Missouri Southern State University, Joplin, MO, USA Esai Ponce Department of Biology, Knox College, Galesburg, IL, USA Kelsie Pos Department of Biology, Knox College, Galesburg, IL, USA Nicholas D. Pyenson Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA Jason Ramsay Biological Sciences Department, Westfield State University, Westfield, MA, USA Emily J. Rayfield School of Earth Sciences, University of Bristol, Bristol, UK Alejandro Rico-Guevara Department of Integrative Biology, University of California, Berkeley, CA, USA Callum F. Ross Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, USA Marion Segall Département d’Ecologie et de Gestion de la Biodiversité, UMR 7179 C.N.R.S/M.N.H.N., Paris, France Hans-Dieter Sues Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA Diego Sustaita Department of Biological Sciences, California State University San Marcos, San Marcos, CA, USA Andrea B. Taylor Department of Basic Science, Touro University, Vallejo, CA, USA Mark F. Teaford Department of Basic Science, Touro University, Vallejo, CA, USA Alan H. Turner Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA Peter S. Ungar Department of Anthropology, University of Arkansas, Fayetteville, AR, USA Theodore A. Uyeno Department of Biology, Valdosta State University, Valdosta, GA, USA Sam Van Wassenbergh Département Adaptations du Vivant, Muséum National D’Histoire Naturelle, UMR 7179 CNRS, Paris, France Department of Biology, University of Antwerp, Antwerp, Belgium Christopher J. Vinyard Department of Anatomy & Neurobiology, Northeast Ohio Medical University, Rootstown, OH, USA Christine E. Wall Department of Evolutionary Anthropology, Duke University, Durham, NC, USA

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Editors and Contributors

Mark W. Westneat Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA Ian Q. Whishaw The Department of Neuroscience, The University of Lethbridge, Lethbridge, Canada Lisa Whitenack Department of Biology, Allegheny College, Meadville, PA, USA Cheryl Wilga Department of Biological Sciences, University of Alaska Anchorage, Anchorage, AK, USA Susan H. Williams Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, Athens, OH, USA Leïla-Nastasia Zghikh Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA, Muséum national d’Histoire naturelle, Paris, France; Laboratory of Histology, Faculty of Medicine and Pharmacy, Institute of BioSciences, University of Mons, Mons, Belgium

Chapter 1

Feeding, a Tool to Understand Vertebrate Evolution Introduction to “Feeding in Vertebrates” Vincent Bels and Anthony Herrel

A major problem of evolution addressed by Darwin, in his Origin of Species (Darwin 1859) is the evolutionary relationship between complex structures and their function, colloquially referred to as form-function relationships. Many of the insights that Darwin contributed to our conceptual framework of evolution are based on careful observations of traits in diverse fossil and extant vertebrates. The morphology and ecology of organisms revealed by subsequent experimental work and detailed study of behavior have added to Darwin’s observations to shape our understanding of the evolutionary relations between form and function (Stauffer 1957; Schulter and Grant 1984; Liem 1990). Following this biological tradition, the present volume describes the trophic system, the body parts of animals, and their associated behaviors that are central to feeding. According to Dullemejier concluding the book Biomechanics of feeding in vertebrates (Bels et al. 1994), this book reports on “…the astonishing diversity of ways in which organisms cope with the problem of obtaining food…”. The structures and behaviors, and the mechanisms leading to form–function relationships under natural and sexual selection have been described in previous works (i.e., Thomson 1917, 1988; Dullemejer 1974; Gans 1974; Gould 1971; Lauder 1985; Hanken and Hall 1993; Reilly and Wainwright 1994; Wainwright 1994, 2007; Lauder and Thomason 1995; McGowan 1999; Dutta and Munshi 2001; Irschick and Higham 2016; Schwenk 2000; Alfaro et al. 2004; Cooke and Terhuve 2015; Mcnulty and Vinyard 2015; Saxena and Saxane 2015; Abzhanov 2017; Barnet 2017). In addition, over the last 50 years, many studies have addressed the interactions between phenotypic V. Bels (B) Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA, Muséum national d’Histoire naturelle, 57 rue Cuvier, 75005, Paris Cedex 05, France e-mail: [email protected] A. Herrel Département Adaptations du Vivant, Muséum national d’Histoire naturelle, UMR 7179 C.N.R.S/M.N.H.N, 55 rue Buffon, 75005, Paris Cedex 05, France e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_1

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traits and the function of the trophic system in vertebrates (i.e., Bels et al. 1994, 2003; Schwenk 2000; Bhullar et al. 2012, 2015). Schwenk (2000) provides a guide to the problem addressed in this volume “…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…”. He goes on to emphasize “…the relative functionality of the feeding system has, without a doubt, a large impact on individual survival and hence lifetime reproductive success…” as Gans (1994) highlights “The study of feeding types and ingestion patterns … consequently offers great opportunities for understanding evolutionary patterns”. The skull has been described in a plethora of studies documenting its relation to environmental, historical, development constraints acting on its morphology, and its biomechanics and function (i.e., Lauder and Shaffer 1993; Dial et al. 2015; Tseng and Flynn 2015; Wilga and Ferry 2015; Ledogar et al. 2016; Olsen and Westneat 2016; Abzhanov 2017; Fish 2017; Pestoni et al. 2018). Smith (1993) identifies a number of constraints that explain the characteristics of the form of the skull in vertebrates including: (i) physical constraints due to the basic physical (mechanical) processes, (ii) selective or compromise constraints that are produced by competing demands on the interdependent elements of the structure, (iii) phylogenetic constraints due to evolutionary modifications in lineages with a common ancestor, and (iv) developmental constraints produced by morphogenetic processes. To these constraints must be added epigenetic constraints (Smith 1993). Epigenetic constraints show that distinct morphs can be selected through regulating developmental and cellular differentiation processes within the bounds of the phylogenetic plasticity of the structure. The present volume describes the functional evolution of feeding in chordates and vertebrates in aquatic, terrestrial, and interface habitats. In the introduction to the volume “Biomechanics of Feeding in Vertebrates” edited by Bels et al. (1994) in the series Advances in comparative Environmental Physiology (Volume 18, SpringerVerlag), Gans (1994) wrote: “Feeding involves the development of hunger, the identification and positioning of the predator relative to the prey, and the acquisition of the entire or part of the prey” and emphasized “Finally it seems useful to remember why the magnitude of adaptation is of interest. The role is that functional aspect of the phenotype that enhances the survival or evolutionary fitness of the individuals” and “…analysis of adaptation always depends on a detailed characterization of suites of interactions…”. The present book “Feeding in Vertebrates” integrates the complex morphological, functional, and behavioral interactions of cranial and postcranial systems in the phylogenetic and ecological contexts of food exploitation. This endeavor involves linking various disciplines as emphasized by Ashley-Ross and Gillis (2002): “…those interested in animal form and function have recently begun branching out to incorporate approaches from experimental biomechanics and other disciplines (see accompanying symposium papers), and functional morphology now stands at the threshold of becoming a truly integrative, central field in organismal biology”. Obviously, this book raises empirical questions concerning the adaptive radiation of chordates and vertebrates derived from interactions in which the anatomical (and physiological)

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properties of the structures play a key role “…the morphological diversification that is functionally related to the utilization of different types of resources following the expansion into a variety of unoccupied ecological niches” (Tokita et al. 2017). The approach in this book is integrative and based on studies of the links between form and function in the tradition of functional morphology and evolutionary biology (i.e., Bock and Wahlert 1965; Dullemejer 1980, 1994; Lauder 1981, 1983; Bramble and Wake 1985; Reilly and Lauder 1990; Hiiemae and Crompton 1985; Hildebrand et al. 1985; Liem et al. 2001; Bout 2003; Homberger 2003; Kardong 2015; Wake 2015). In all of the chapters in this volume, the term “function” refers to the “biological role” of the morphological traits (Irschick and Higham 2016) in the broadest sense. “Biological role”, is defined by Irschick and Higham (2016) as “the action that natural selection has previously favored”. Thus, the biological role is viewed through the behavior (i.e., feeding, drinking, displaying, and chemical collection) that vertebrates use in order to respond to environmental stimuli. This is accomplished through the action of the various hard (e.g., skull, hyoid apparatus) and soft (e.g., musculature) elements of the trophic system. These responses are complex and involve not only the tropic system per se but also the whole body of the animal, and are governed by a complex physiological process such as satiation (Fig. 1.1). In the case of feeding “function”, the diversity of properties of the nutritious substances (i.e., living prey, meat, plants and fruits, nectar) selected by chordates and vertebrates have acted as one of the key selective pressures in the evolution of chordate and vertebrate lineages resulting in the evolution of the trophic system. The trophic system includes the tongue, head and skull, the teeth, as well as the rest of the body for all lineages considered in this book. The functional output of the trophic system can be quantified by its performance. For Wainwright (2007), performance is the ability of individuals to do the tasks that fill their lives. Feeding performance traits have a complex underlying basis in the size, shape, and various properties of the components of the trophic system (Bels et al. 1994; Schwenk 2000; Liem et al. 2001; Aerts et al. 2002; Dial et al. 2015), and the interactions between per-

Fig. 1.1 Typical feeding posture in vertebrates using cranial and postcranial systems during feeding behavior. The small felid uses only the jaw apparatus (a) while large felids use their forelimbs to manipulate carcasses and meat (b)

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formance and its underlying anatomical elements reveal a large number of complex evolutionary dynamics. The chapters in this book summarize the functional diversity of the trophic system from anatomy to performance and behavior (sensu, Wainwright 2007) and depict and interpret the complexity of this functional diversity in chordate and vertebrate lineages through empirical case studies. The role of feeding in evolutionary processes is evident at all levels, from individuals to communities, and in all lineages that, at different geological times, successfully occupied a diversity of aquatic and terrestrial ecosystems. Feeding, and especially predation, has had a major structuring effect on animal communities since the Cambrian (Bengton 2002; Marshall 2006; Vannier 2009). A large number of studies on cranial and postcranial musculoskeletal systems in vertebrates demonstrate that feeding behavior has played a key role in the theories of evolutionary biology. This is best illustrated by the biological diversity of the beak and feeding (behavioral ecology) of Galapagos finches noticed by Darwin. The form–function interaction exemplified through a “form-function complex” as suggested by Williams (Chap. 18) can be viewed as a trait with implications for our understanding of the evolution of these animals. All of the chapters in this book relate to one or more of the five levels of analysis (e.g., behavior, peripheral morphology or anatomy of the musculoskeletal system, motor pattern, central nervous system structure, and circuit), needed to study the relationships between trophic form function as suggested by Lauder (1991). These levels are approached in different ways in each of the chapters in the biological context of the relationships of form and function demonstrated for all lineages of chordates and vertebrates (Chaps. 7–21). These chapters refer to the “function”, “biological role” or “role-associated aspects” of the structure (Bock and Wahlert 1965; Gans 1994) as stated by Bock and Van Wahlert (1965): … Its function is its action or simply how the feature works, as stemming from the physical and chemical properties of the form; a feature may have several functions that operate simultaneously or at different times. A faculty is defined as the combination of a form and a function of a feature; it is what the feature is capable of doing in the life of the organism. The biological role is the action or the use of the faculty by the organism in the course of its life history. A biological role can be ascertained only by observation of the organism living naturally in its normal environment. As described throughout this book, the tentative correlation between form and function of the trophic system must be considered as hypothetical until functional principles are established to demonstrate that the observed “form” properties necessarily respond to one or several environmental constraints. This is a difficult approach. Before postulating an established relationship between the properties of a structure and its “function” or its biological role, it is necessary to determine the involvement of the structure studied in all behaviors, not only feeding, used by an organism to interact with its environment. In this context, two chapters (Brainerd and Camp, Chap. 2; Rayfield, Chap. 3) deal specifically with questions of structural complexity and the relationships between the properties (e.g., anatomical, mechanical) of the trophic musculoskeletal system in diverse vertebrates and the complexity of the performance traits and behaviors in which they are involved. Defining all of the performance traits

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involved in behaviors thus remains a central point. According to Schwenk (2000), “form and function, experiment and description, qualitative and quantitative data must be held as equally important, complementary, and ideally, “reciprocally illuminating” elements…”. All of the chapters in this book place the integrated form-function properties of trophic (and sometimes non-trophic) features into the evolutionary and ecological contexts to explain how chordate (Clark et al., Chap. 7) and vertebrate (all other chapters) organisms are able to feed and thus assure their survival and reproductive fitness. For this reason, this book can be viewed as continuing the work of Arnold (1983), modified by Garland and Losos (1994) and more recently by Irschick and Higham (2016), exemplifying the relationship between structures and individual fitness (Fig. 1.2). This paradigm makes it possible to situate studies related to the adaptive nature of feeding behavior by providing information on how factors (“stressors” after Arnold 1983) relate to behavior (i.e., prey/food availability and properties) to influence fitness. Garland and Losos (1994) refined the paradigm by associating two factors (environment and genotype) influencing morphological traits and by indicating that intraand interspecific interactions can influence behavior. Similarly, they propose that the environment (“habitat”) can directly influence performance and the resulting behaviors. Finally, they suggest that morphological traits can directly impact fitness through their effect on performance as emphasized by Johnson et al. (2008): “The

Epigenetical Variation

Genetical Variation

Design Variation

Performance Habitat variation

Behaviour Variation

Fitness Variation

Developmental Variation

Habitat Aquatic ó Interface - Terrestrial

Fig. 1.2 Oversimplified heuristic diagram showing factors influencing the relationships between morphology, performance, and fitness through feeding behavior in chordates and vertebrates (modified from Arnold 1983; Irschick and Higham 2016)

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outcome of species interactions (competition, predation, etc.) is determined not by traits directly but how traits affect performance in the whole organism (Arnold 1983). Performance, when integrated as a function of a trait’s contribution to fitness, can clarify how selection operates. In addition, unmeasured aspects of performance may be inferred by including direct pathways to fitness”. To understand how the complete evolutionary context of natural and sexual selection (e.g., the hyoid apparatus in Squamates) drive the evolution of the trophic system, an integrative view of the interaction between environment and development and how this influences morphology, performance, and fitness is essential. Therefore, all of the chapters of this book can be integrated into the paradigms determined by Arnold (1983), and modified by Garland and Losos (1994) and more recently by Irshick and Higham (2016). Conceptually all of the chapters of this book illustrate, at various levels, the effect of selection through the influences of environment, genetics, epigenetics, and development, and so help to clarify the selective forces in chordate and vertebrate lineages (Fig. 1.3). Epigenetic and developmental approaches are currently being developed with several models that link functional morphology, phylogeny, and the evolution of the relations indicated in this paradigm. For example, recent work done on the beaks of birds (Abzhanov et al. 2006, 2007; Bhullar et al. 2012, 2015; Abzhanov 2017) combines the diversity of form function (sensu Lauder 1996) with genetic control during development. Approaching questions pertaining to form-function diversification and evolution in the radiation of chordate and vertebrate lineages requires an integrated approach. Gans (1994) stated, “It has become common to start functional and biomechanical comparisons by mapping their states on phylogenetic diagrams”. Integrated studies are needed at several time scales, as demonstrated in the majority of the lineages studied (see Chaps. 7–21). Paleontology, comparative and functional anatomical studies, behavioral ecology studies, and comparative studies of trophic systems have all provided evidence that evolutionary changes in the feeding system have defined the success of every vertebrate lineage. Recent evidence that changes can occur very rapidly and be observed on a timescale “commensurate with ecological processes”

Fig. 1.3 The demands of feeding on various types of foods with different trophic designs are highly variable as demonstrated in many chordate and vertebrate lineages. a A whole fruit is transported without any kind of manipulation in Rhyticeros undulatus (Aceros undulates). b Crushing a snail in Dracaena guianensis requires the development of high bite forces and the control of a complex jaw musculature. c Lialis burtonis has to deal with large prey items

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as suggested by Stroud and Losos (2016) also shows that rapid changes in trophic systems and behavior result from the adaptive responses to environmental changes that can be extremely “brutal”. This volume shows how various forces (historical and environmental) drive this complex system. By using empirical and experimental approaches to establish functional micro- and macroevolutionary scenarios of the evolution of food acquisition in chordates and vertebrates, significant insights into the drivers of phenotypic diversity are gained. Lauder (1991) raised two important questions about the complexity of form— function relationships that depend on ecological constraints: (i) At what level of integration do complex systems exist in an organism? (ii) Does the change of a component of a complex system affect (necessarily or not) the other elements of the same system? These questions summarize the complexity of the integration of the different elements that make up the trophic system. Trying to understand the evolution of feeding through a view of the trophic system only is too restricted. Classically, the trophic system is viewed as the major unit associated with feeding (and drinking) with the postcranial structures being the secondary unit (Kardong 2015; Ken and Carr 2019). Although noting the need for integration, many previous reviews focusing on feeding behavior have not attempted to document the involvement of other body elements (Bels et al. 1994; Schwenk 2000) that Dullemeijer (1994) insisted on by stating “Therefore, one should bear in mind that not only the head, but also many other regions of the animal body, cooperate in the feeding mechanism”. Higham (2007) (in aquatic habitats) and Bels et al. (2019) (in terrestrial habitats), focus on the major functional and integrated role of locomotor and trophic designs in predator–prey interactions. For the predator, capturing and killing prey involves the postcranial musculoskeletal system as shown in several chapters of this volume. The biological role of the postcranial elements and their association in feeding is therefore not negligible (Marshal and Goldbogen 2015; Hocking et al. 2017). Efficient feeding requires the combined movements of cranial and postcranial elements. The use of the forelimbs and hands for feeding in many vertebrate species as described by Montuelle and Kane (Chap. 4) and Wishaw and Karl (Chap. 6) plays a key role in the success of feeding. For example, feeding behavior in carnivorous mammals (Fig. 1.1) is related to the involvement of two distinct modules: a cranial module and a limb module (Gatesy and Dial 1996, Meachen-Samuels and Van Valkenburgh 2009). Clark et al. (Chap. 7) also demonstrate that jawless hagfishes use their flexible bodies to create rigid structural support for their everted tooth plates to create an efficient prey capture. These authors demonstrate the hierarchy in movements to reach, grasp, and bring food to the mouth within their own phylogenetic history as explained for vertebrates by Whishaw and Karl (Chap. 6). Trophic form–function interactions need to investigate properties of a set of skeletal (including teeth as demonstrated by Ungar and Sue, Chap. 11) and muscular (Bels et al. 1994; Schwenk 2000; Kardong 2015; Abzhanov 2017; Diogo et al. 2018) organs under neuronal control (Filosa et al. 2016). Experimental methods such as electromyography, strain gauges, high-speed cinematography, can be used for describing feeding. Our knowledge of form–function relationships and the biological role of the structure are increased by methodological, technical, and conceptual

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advances. These allow the investigation of the properties of the anatomical structures while simultaneously describing and quantifying feeding. In part I of this book “From structure to behavior”, two chapters emphasize how several new methods such as X-ray Reconstruction of Moving Morphology (XROMM) and fluoromicrometry use images for revealing 3D form–function relationships of cranial and cervical musculoskeletal structures (Brainerd and Camp, Chap. 2) and deductions based on Finite Element (FE) analysis (Rayfield, Chap. 3). These approaches show promise in revealing the morphological and functional properties of the trophic systems in relationship to historical and environmental constraints. As demonstrated by Brainerd and Camp (Chap. 2), questions related to the biomechanics of the trophic system in aquatic and terrestrial environments such as cranial kinesis in squamates, jaw mechanics and tooth occlusion in mammalian mastication, and pharyngeal jaw mechanics in fishes can all be understood using these novel approaches. Combined with fluoromicrometry to measure activity in muscles with complex architectures in association with experimental devices gives one the opportunity to understand the intrinsic functioning of the trophic system within its adaptive and evolutionary contexts. How feeding and other behavioral activities take place, and the nature of form— function interactions of the trophic system, are reviewed in all of the chapters of part II “Feeding in vertebrate lineages” of this book. The new findings presented in these chapters emphasize the contribution of empirical, experimental, and field studies to integrating functional morphology and biomechanics with disciplines such as behavioral ecology, physiology, and biomimetics. The relationships between structure and fitness revealed by performance and behavior take place in specific environments, thus constituting the ecological context that impacts each of the relationships (Fig. 1.2). Three environmental constraints are summarized in the chapters of this part of the book: (i) aquatic habitats (Chaps. 7–9, 10, 12, and 19), (ii) the interface between aquatic and terrestrial habitats (Chap. 5), and (iii) the terrestrial habitat (Chaps. 10–18 and 20–21). The question of feeding in water (Fig. 1.4) is documented in chordates (Clark and Uyeno) and a series of vertebrate lineages as documented by Huber et al. (Chap. 8), Gidmark et al. (Chap. 9), Herrel et al. (Chap. 12), Gignac et al. (Chap. 15), Lemell et al. (Chap. 16), and Marshall and Pyenson (Chap. 19). These chapters show that understanding feeding in an aquatic habitat by the different vertebrate lineages provides examples of the form–function complex shaped by the physical constraints of feeding in water (Fig. 1.4). Clark et al. (Chap. 7) explain how hagfishes and lampreys, who have no jaws, use their dentation to feed by biting and causing damage to the tissue of large marine animals. They present the jawless feeding mechanism of these animals as a way to understand the evolution of chordate feeding behavior, and the evolutionary origins of jaw-driven feeding. Based on a comprehensive integrative review of the morphology, biomechanics, and performance, these chapters also show the complexity of the feeding behavior related to the diversity of chordates and conclude, “Because the jawless condition represents the primitive feeding apparatus for vertebrate animals, the biomechanics and functional morphology of jawless feeding in hagfishes can bear some insight into the selective and functional advantages of jaws…”.

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Fig. 1.4 Feeding in whale (Courtesy Amy Knowlton, New England Aquarium, NOAA Permit Number 15415)

Huber et al. (Chap. 8) provide a novel holistic approach of feeding in elasmobranchs or cartilaginous fishes, and develop an integrative synthesis of the relationship between structure, performance, and behavior. They bring an analysis of these relationships within a phylogenetic and ecological framework that permits them to emphasize that “…we are now beginning to understand the manner in which sensory perception guides the movements of the jaws, and how the biochemical composition of those jaws affects their mechanical performance. Developing this synthesis has also helped identify knowledge gaps that will hopefully be rectified as research on feeding in cartilaginous fishes continues into the 21st century”. Gidmark et al. (Chap. 9) describe the feeding of fishes and demonstrates the extensive progress made in describing their morphology, development, and feeding behavior within evolutionary and ecological frameworks. The authors propose integrative ways to understand the diversity of feeding mechanisms and to understand how animals respond to the constraints on feeding behavior: “The integration of musculoskeletal biomechanics with research approaches in neurobiology, such as neurophysiology and brain to behavior approaches, could potentially produce important insights and make fish feeding an important model system for neuromechanics”. Moreover, they confirm that an integrative approach of experimental biomechanics in fish model systems such as zebrafish or medakas within a phylogenetic context can bring new insights to the form–function complex of vertebrates in aquatic habitats. This a key point to understand how natural selection acts on form function. They emphasize that “... using phylogenetic frameworks to make informed choices

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for species selection in feeding studies is important in order to get maximal value out of often difficult to obtain biomechanical data. As our database on feeding traits and integrative form-function insights grows, this will empower a new generation of research on the diversity and evolution of fish feeding mechanisms”. Marshal and Pyenson (Chap. 19) describe feeding in aquatic mammals and illustrate the diversity of feeding phenotypes in response to changing environmental conditions in lineages with highly different phylogenetic histories, with all of the extant species departing from ancestors feeding in a terrestrial environment. They show the diversity of behavioral responses of animals exploiting various food resources with specialized trophic systems evolving from their terrestrial ancestors and note that “…. mechanisms and adopted novel ways of feeding are influenced by both phylogeny and ecology. Here we highlight feeding strategies as diverse as aquatic herbivory, raptorial biting, suction to filter feeding, each of which have evolved in numerous mammalian lineages” and conclude “Most aquatic mammals are multimodal trophic opportunists that have made substantial departures from the classic terrestrial process model of feeding. Major departures from the process model have focused on food acquisition, and for most, the loss of mastication and intraoral transport to teeth, homodonty and even the total loss of teeth in some lineages”. As for fishes, they make the case for an integrative knowledge of the neuromuscular and sensorimotor control of feeding behavior in a comparative context and emphasize that “discoveries of new fossils and the development of new phylogenetic tools will allow scientists to further clarify functional transitions from land-to-sea and provide new perspectives on the evolution of mammalian feeding”. The other chapters involving aquatic and terrestrial species include Gignac et al. (Chap. 15) and Lemell et al. (Chap. 16) who demonstrate the importance of comparing aquatic and terrestrial species in the context of the phylogeny of these lineages. In Crocodylians, Gignac et al. emphasize the need to understand the morphological and functional implications of food/prey selection on the trophic system: “What factors directly caused the many shapes of the suchian jaw, allowing their snouts to have been so evolutionarily variable? Perhaps ongoing studies focused on fluid flow and sub-aquatic hydrodynamics of the snout”. Turtles are one of principal groups that allow us to understand the effect of the transition from aquatic to terrestrial habitats in vertebrates as concluded by the authors: “As might be expected, the morphology of the turtle feeding apparatus is closely associated with feeding habitat. Aquatic species have flat skulls, a large ossified hyobranchial apparatus with a small tongue, whereas purely terrestrial species possess the opposite: a high skull, and a small cartilaginous hyolingual apparatus with a large muscular and movable tongue that allows active lingual transport of food objects from the environment to the esophagus. Since turtles are characterized by a very long evolutionary history within diverse habitats, they are one of the most suitable groups within vertebrates to present morphological and behavioral variations and adaptations related to feeding medium and food type”. The transition between aquatic and terrestrial habitats is one of the key points in understanding the evolution of tetrapods, as illustrated by feeding in amphibious fishes living at the interface between water and land. Van Wassenbergh and colleagues (Chap. 5) explain the mechanical challenges and functional solutions

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required to successfully feed in an environment that is key to the terrestrial transition in vertebrate evolution. Through their extensive studies, they generate hypotheses on the evolutionary history of early tetrapods. Again, this review shows how the integration of the cranial and postcranial elements to maintain body posture is essential to allow the capture of food in the terrestrial environment, and how the trophic system works to capture and transport the food for efficient digestion in air. They note, “When transitioning to a life on land, ancestrally aquatic organisms are faced with numerous challenges caused by the physical and chemical differences between water and air …Since air is about 800 times less dense and 50 times less viscous than water, buoyancy forces on an animal’s body become negligibly small relative to the opposing gravitational forces, and both frictional resistance of the air and the work needed to overcome inertia strongly decrease. This has drastic effects on the mechanics of movement: transitioning to the terrestrial environment requires morphological changes to support the body and to generate propulsive forces…Not only biomechanical problems need to be coped with by the musculoskeletal system, many other organ systems are challenged as well - such as vision, hydration/desiccation, CO2 retention and acidosis, and ion-balance regulation…”. Food/prey capture, reduction, transport, and swallowing need to be supported by integrative complex actions of the hard (skull including teeth, hyoid apparatus) and soft (muscles) tissues organized as coordinated trophic elements. Chapters 12–21 demonstrate these challenges in morphology, performance, and behavior in relation to the capture, transport, and digestion of food as soon as vertebrates were able to survive and reproduce in aerial conditions. Three chapters explain the diversity of two key elements of the trophic system: tongue and teeth. Iwasaki et al. (Chap. 10) describe comparative studies of anatomical and biomechanical traits of the tongue in tetrapods. They state the tongue “…plays a crucial role in many vital functions, such as food-uptake, mastication and swallowing. The morphological concept of the tongue is that of a voluntary muscle mass covered by a mucosal sheath. However, the tongues of amphibians, reptiles, birds and mammals have deviated in terms of general morphology and function”. Their review describes the diversity in “form” and “function” of the tetrapod tongue. The central role of this element of the trophic system is exemplified in chapters on amphibians, reptiles, birds, and mammals and demonstrated through examples such as the morphology and function of the tongues of specialized species such as frogs, chameleons among reptiles and nectar-feeding bats among mammals (part II of the book). Comprehensive studies of the lingual mechanism such as exemplified in amphibians (Herrel et al. Chap. 12) and lizards (Bels et al. Chap. 13) permits the modeling of tetrapod feeding and drinking functions. In a lot of tetrapods, “The ability to catch a diverse array of prey puts special demands on the adhesive performance of frog tongues. The attachment to the prey must be at least strong enough to prevent the prey from escaping before it is grasped by the jaws” as stated by Herrel et al. (Chap. 12) and highlighted for frogs, salamanders (Herrel et al., Chap. 12), and lizards (Bels et al., Chap. 13). As demonstrated by Ungar and Sues (Chap. 11), teeth play a key role in the success of tetrapods because, as stated by these authors: “Teeth provide an excellent model

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system for understanding evolutionary change and how it has led to adaptive diversity across tetrapods. Their durability over geological time scales and their ubiquity in the fossil record make teeth unique and allow direct comparison of dental structure for both extant and extinct species”. Ungar and Sues demonstrate the diversity of teeth (i.e., size, shape, and structure) and their central role in the adaptive radiation of a lot of tetrapod lineages to emphasize that teeth are “are the front line in Nature’s struggle for existence”. Their survey of all the morphological traits into ontogenetic and phylogenetic contexts opens clearly a lot of questions on feeding evolution as approached in all of the chapters in tetrapods (Chaps. 12–15, 18–21). The complex interaction form function of the whole trophic system in terrestrial habitat (and in some cases in comparison with aquatic habitat) is discussed in amphibians by Herrel et al. (Chap. 12), in reptiles including turtles by Lemell et al. (Chap. 16), crocodiles by Gignac et al. (Chap. 15), snakes by Moon et al. (Chap. 14), lizards by Bels et al. (Chap. 13), and in mammals by Williams (Chap. 18) and by Ross and Iriarte-Diaz (Chap. 20) and Vinyard et al. (Chap. 21). These chapters provide examples of the evolutionary trends of the trophic system to exploit food/prey from food identification (i.e., vomerolfaction as described by Moon et al. (Chap. 14) and Bels et al. (Chap. 13) to food transport. The salient point of all of these chapters is to reveal the complexity of feeding behavior and the need for integrative studies to discuss the form–function complex. In amphibians, Herrel et al. (Chap. 12) suggest that “…Future studies quantifying feeding performance across a wide range of species are likely to provide critical insights into the selective pressures underlying the evolution of the staggering diversity in feeding form and function observed in amphibians”. Snakes “characterized by a unique feeding system and other traits associated with elongation and limblessness” are described by Moon et al. (Chap. 14) who emphasize that these “gape-limited predators” are a key example of differences in head morphology linked to differences in diet. In the meantime, such differences are nested within the adaptive nature of head shape revealing striking evolutionary convergences in some clades of these vertebrates. Constriction present in various ‘basal’ (Henophidia) and ‘advanced’ snakes (Caenophidia) relates mechanisms associating trophic and axial systems in the evolutionary success. These authors also show the complexity of responses of vertebrates with highly specialized tongues in the behavioral and functional changes to morphological modifications associated with one key sensory function and conclude “The great diversity of snakes calls for many more studies of feeding biology, which are likely to lead to the discovery of new mechanisms, as recent research has shown. In addition, by further integrating robust phylogenies, detailed morphological data, functional mechanisms, and ecologically relevant performance measures in future research, we will surely gain important new insights into how feeding, locomotor, and other mechanisms may have driven evolution and diversification of snakes”. The diversity of the trophic system and its effect on the feeding behavior, particularly associated to morphological and functional tongue modifications is emphasized in some examples provided by Iwasaki et al. (Chap. 10) and exemplified for lizards (Chap. 13, Bels et al.). Bels et al. discuss trophic elements in light of the “ModalAction-Pattern” of feeding (sensu Barlow 1978). Their chapter evaluates the effect of trophic specialization on the modulation and mechanisms of feeding and drinking in

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lizards (e.g., prey adhesion in chameleons). Lizards represent a model of evolution of prey/food capture in all tetrapods because in this clade the two modes of prey/food capture (lingual vs jaw prehension) can be observed (i) across species along the squamate phylogeny and (ii) within a same species in response to proximal factors of the prey/food. Indeed, as demonstrated by all tetrapods (Chaps. 18, 20 and 21), in an aerial environment the capture of prey/food is related to the actions of the jaws (jaw prehension) and/or the tongue (lingual prehension) toward the food. Bels et al. also show that the mechanisms of water collection are not constrained by tongue specializations until a “level” of morphological transformations observed in some clades “specialized” in vomerolfaction (Teiidae and Varanidae). Questions related to the complexity of morphological, functional, and behavioral responses also drive Lemell’s et al. description of turtles (Chap. 16). They argue that turtles “are one of the oldest known reptile orders, appearing about 240 million years ago. Within the vertebrates, they have evolved the most unusual body plan, with most of their body inside a protective box made of bone and keratin. This peculiar morphology has persisted since the late Triassic, but has allowed them to adapt to very diverse ecological habitats, ranging from marine and freshwater to purely terrestrial environments, from temperate to tropical regions of all continents except Antarctica”. These authors focus on the adaptive morphological, functional, and behavioral traits of these tetrapods which feed in water and in air. They demonstrate that the morphology of the turtle feeding apparatus is “closely associated with feeding habitat”. Crocodylians with a “wide range of snout shapes, tooth forms, and diets” are “exceptional ambush predators in near-shore environments”. Gignac et al. (Chap. 15) synthetize new knowledge on their feeding behavior and describe how feeding performance has shaped their head and jaws. Gignac et al. demonstrate that an in-depth knowledge of the fossil record reveals how form–function complexes and the subsequent feeding behavior in these reptiles evolved. They emphasize that biomechanical and functional questions still remain including, “What factors directly caused the many shapes of the suchian jaw, allowing their snouts to have been so evolutionarily variable?”. Rico et al. (Chap. 17) provide a form-function description of the trophic system in birds. Based on morphological traits, these authors review biomechanical and functional characteristics of feeding behavior in a wide diversity of bird species from hummingbirds to ostriches. From a comparative point of view, they “explore the vast diversity of bird feeding environments by grouping foraging (searching) and feeding (handling – consumption) mechanisms that birds use on land, air, and water”. They associate “what birds eat” and “how they feed” through an understanding of the convergences, radiations, trade-offs, etc., that have shaped the feeding apparatus. As in the chapters on snakes (Moon et al., Chap. 14) and lizards (Bels et al., Chap. 13) they explain the drinking mechanism which often involves different actions than the ones used to feed. Finally, Rico et al. raise new questions about the competing selective pressures on the beak and head form–function complex; i.e., morphological novelties like casques or the de novo origin of muscles. As can be observed in all of the chapters, they also emphasize how new insights can come from methodological

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and conceptual approaches explained by Brainer and Camp (Chaps. 2) and Rayfield (Chap. 3). Three chapters explore the evolutionary and adaptive nature of the trophic form— function complex in terrestrial mammals. Williams (Chap. 18) synthetizes integrated morphological, functional, and behavioral traits of mammalian feeding, from ingestion to swallowing, from comparative point of view of the clade. Various examples explain the complex interactions of the trophic elements (e.g., tongue) and solid food eating versus liquid food drinking to show the ability of this organ to play with proximal properties of the food. Williams highlights our understanding of how the tongue, lips, cheeks, jaw, soft palate, and hyoid are involved in feeding behavior. As exemplified in several chapters of the book, this chapter shows that some aspects of the interactions of form and function (i.e., muscles of mastication) in some models (e.g., primates) are becoming well understood. The motor control of structures such as the tongue, which plays a critical role in bolus manipulation and formation during chewing, remains to be explored not only in model organisms but also in the wide diversity of mammals exploiting different food resources. All these potential studies based on methodological and conceptual advances (Chaps. 2 and 3) will show what is called by Williams “…novel form-function links… expanding our understanding of functional diversity, but may also bring to the forefront unexpected constraints and limitations on function and behavior in mammalian feeding”. Feeding in primates (Fig. 1.5) is probably one key evolutionary model to explain the links between morphology, performance, behavior, and fitness (Ross and IriarteDiaz, Chap. 20, and Vinyard et al., Chap. 21). Ross and Iriarte-Diaz (Chap. 20) describe the evolution of feeding in primates and explain “several ways in which integration of results from new and improved methods for experimental study of primate feeding biomechanics will significantly enhance our understanding of the biomechanical determinants of primate feeding performance”. Integration of data on high-resolution jaw kinematics in these model animals with the investigation of properties and mechanics of jaws and dentition provides an understanding of the role of diet, grit, and feeding behavior in evolution of primates and identifies the drivers of their craniomandibular diversity that play a key role in their adaptive radiation. As suggested in all of the chapters in part II of the book, Ross and Iriarte-Diaz emphasize “One of the most exciting areas for future work is the integration of data on wild primate feeding behavior with the geometric and material properties of the foods they exploit”. In the suite of chapters on the diversity of form–function interactions in mammals, Vinyard et al. (Chap. 21) conclude, when considering feeding in humans, that feeding “played key roles in human evolution”. These authors pose questions on the evolution of feeding in humans and discuss “…the functional consequences of gracilization and functional relationships within the human masticatory apparatus using nonhuman primates for comparison”. They conclude “…that any performance deficits in the human masticatory apparatus are primarily related to gracilization. Humans possess a relative masticatory apparatus configuration that compares similarly to many other primates suggesting the evolution of humans has not unraveled the basic

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Fig. 1.5 Feeding in primates is one of the major models to understand the complexity of form— function relationship in vertebrates (Courtesy Emmanuelle Pouydebat, Muséum national d’Histoire naturelle, UMR7197 CNRS/MNHN)

functional relationships within the masticatory apparatus that characterize most primates”. In summary, this book provides an exposé of feeding in chordates and vertebrates. Each chapter reveals the complexity of morphological, functional, and behavioral traits and their interactions, and as such provides a tutorial of how natural selection has acted and still acts on the trophic system.

References Abzhanov A (2017) The old and new faces of morphology: the legacy of D’Arcy Thompson’s ‘theory of transformations’ and ‘laws of growth’. Development 144:4284–4297 Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442(7102):563 Abzhanov A, Rodda SJ, McMahon AP, Tabin CJ (2007) Regulation of skeletogenic differentiation in cranial dermal bone. Development 134:3133–3144 Aerts P, D’aout K, Herrel A, Van Damme R (2002) Topics in functional and ecological vertebrate morphology. Shaker Publishing, Maastricht Alfaro ME, Bolnick DI, Wainwright PC (2004) Evolutionary dynamics of complex biomechanical systems: an example using the four-bar mechanism. Evolution 58(3):495–503 Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23(2):347–361 Ashley-Ross MA, Gillis GB (2002) A brief history of vertebrate functional morphology. Integr Comp Biol 42(2):183–189 Barnett SA (2017) The rat: a study in behavior Routledge. Taylor and Francis, Oxford

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Bels VL, Chardon M, Vandewalle P (1994) Biomechanics of feeding in vertebrates. In: Advances in Comparative and Environmental Physiology, vol. 18. Springer, New York Bels VL, Gasc JP, Casinos A (2003) Vertebrate biomechanics and evolution. BIOS Scientific Publishers Limited, Trowbridge, UK Bengtson S (2002) Origins and early evolution of predation. Paleontol Soc Pap 8:289–318 Bhullar BAS, Marugán-Lobón J, Racimo F, Bever GS, Rowe TB, Norell MA, Abzhanov A (2012) Birds have paedomorphic dinosaur skulls. Nature 487(7406):223 Bhullar BAS, Morris ZS, Sefton EM, Tok A, Tokita M, Namkoong B, Abzhanov A (2015) A molecular mechanism for the origin of a key evolutionary innovation the bird beak and palate revealed by an integrative approach to major transitions in vertebrate history. Evolution 69(7):1665–1677 Bock WJ, Von Wahlert G (1965) Adaptation and the form–function complex. Evolution 19(3):269–299 Bout RG (2003) Biomechanics of the avian skull In: Bels VL, Gasc JP, Casinos A (eds) Vertebrate biomechanics and evolution. BIOS Scientific Publishers Limited, Trowbridge, UK, pp 229–242 Bramble DM, Wake DB (1985) Feeding mechanisms of lower vertebrates In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology, vol 13. Harvard University Press, Massachusetts, London, Cambridge, pp 230–261 Cooke SB, Terhune CE (2015) Form function and geometric morphometrics. Anat Rec 298(1):5–28 Darwin C (1859) On the origin of species. John Murray, London Dial KP, Shubin N, Brainerd EL (2015) Great transformations in vertebrate evolution. University of Chicago Press, Chicago Diogo RJ, Zierman JM, Molnar J, Siomava N, Abdala V (2018) Muscles of chordates: development homologies and evolution. CRC Press, New York Dullemeijer P (1980) Functional morphology and evolutionary biology. Acta Biotheor 29(3–4):151–250 Dullemijer P (1994) Conclusion: a general theory for feeding mechanics. In: Bels VL, Chardon M, Vandewalle P (eds) Biomechanics of feeding in vertebrates. Advances in comparative and environmental physiology, vol 18. Springer, New York, pp 347–358 Dutta HM, Munshi JD (2001) Vertebrate functional morphology: horizon of research in the 21st century. Science Publishers, Inc Filosa A, Barker AJ, Dal Maschio M, Baier H (2016) Feeding state modulates behavioral choice and processing of prey stimuli in the zebrafish tectum. Neuron 90(3):596–608 Fish JL (2017) Evolvability of the vertebrate craniofacial skeleton S1084-9521(17). Semin Cell Dev Biol 13:30284-7 Gans C (1974) Biomechanics: an approach to vertebrate biology. University of Michgan Press, Ann Arbor Gans C (1994) Introduction. In: Bels VL, Chardon M, Vandewalle P (eds) Biomechanics of feeding in vertebrates. Comparative and environmental physiology, vol 18. Springer, Berlin, pp 1–4 Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302 Gould SJ (1971) D’Arcy Thompson and the science of form. New Lit Hist 2(2):229–258 Hanken J, Hall BK (1993) The Skull, vol 1–3, University of Chicago Press, Chicago Hiiemae KM, Crompton AW (1985) Mastication, food transport and swallowing morphology. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology, vol 13. Harvard University Press, Massachusetts, London, Cambridge, pp 262–290 Hildebrand M, Bramble DM, Liem KF, Wake DB (1985) Functional vertebrate morphology. Harvard University Press, Cambridge Hocking DP, Marx FG, Park T, Fitzgerald EM, Evans AR (2017) A behavioural framework for the evolution of feeding in predatory aquatic mammals. Proc R Soc B 284:20162750 Homberger DG (2003) The comparative biomechanics of a prey-predator relationship: the adaptive morphologies of the feeding apparatus of australian black-cockatoos and their food as a basis for reconstruction of the evolutionary history of the psittaciformes. In: Bels VL, Gasc JP, Casinos A

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(2003) Vertebrate biomechanics and evolution. BIOS Scientific Publishers Limited, Trowbridge, UK, pp 203–228 Irschick DJ, Higham TE (2016) Animal athletes: an ecological and evolutionary approach. Oxford University Press, Oxford Johnson JB, Burt DB, DeWitt TJ (2008) Form function and fitness: pathways to survival. Evolution 62(5):1243–1251 Kardong KV (2015) Vertebrates: comparative anatomy function evolution, 7th edn. McGraw-Hill, New York Kent G, Carr R (2019) Comparative anatomy of the vertebrates, 9th edn. McGraw-Hill Publishers, New York Lauder GV (1981) Form and function: structural analysis in evolutionary morphology. Paleobiology 7(4):430–442 Lauder GV (1983) Food capture. In: Webb PW, Weihs D (eds) Fish biomechanics. Praeger Publishers, New York, pp 280–311 Lauder GV (1985) Functional morphology of the feeding mechanism in lower vertebrates. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Feeding mechanisms of lower vertebrates, vol 13. Harvard University Press, Massachusetts, London, Cambridge, pp 230–261 Lauder GV (1991) Biomechanics and evolution: integrating physical and historical biology in the study of complex systems. In: Rayner JMV, Wootton RJ (eds) Biomechanics in evolution. Cambridge University Press, Cambridge, pp 1–19 Lauder GV, Shaffer HB (1993) Design of feeding systems in aquatic vertebrates: major patterns and their evolutionary interpretations. The Skull 3:113–149 Lauder GV, Thomason JJ (1995) On the inference of function from structure. In: Thomason JJ (ed) Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge, pp 1–18 Ledogar JA, Dechow PC, Wang Q, Gharpure PH, Gordon AD, Baab KL, Richmond BG (2016) Human feeding biomechanics: performance variation and functional constraints. PeerJ 4:e2242 Liem KF (1990) Aquatic versus terrestrial feeding modes: possible impacts on the trophic ecology of vertebrates. Am Zool 30(1):209–221 Liem KF, Bemis WF, Walker (2001) Functional anatomy of the vertebrates: an evolutionary perspective. Harcourt College Publishers, New York Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Annu Rev Earth Planet Sci 34:355–384 Marshall CD, Goldbogen JA (2015) Feeding mechanisms marine mammal physiology: requisites for ocean living, pp 95–118 McGowan P (1999) A prectical guide to vertebrate mechanics. Cambridge University Press, Cambridge Mcnulty KP, Vinyard CJ (2015) Morphometry geometry function and the future. Anat Rec 298(1):328–333 Olsen AM, Westneat MW (2016) Linkage mechanisms in the vertebrate skull: structure and function of three-dimensional parallel transmission systems. J Morphol 277(12):1570–1583 Pestoni S, Degrange FJ, Tambussi CP, Demmel Ferreira MM, Tirao GA (2018) Functional morphology of the cranio-mandibular complex of the Guira cuckoo (Aves). J Morphol 279(6):780–791 Reilly SM, Lauder GV (1990) The evolution of tetrapod feeding behavior: kinematic homologies in prey transport. Evolution 44(6):1542–1557 Reilly SM, Wainwright PC (1994) Conclusion: ecological morphology and the power of integration. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press. Chicago, pp 339–354 Saxena RK, Saxena S (2015) Comparative anatomy of vertebrates, 2nd edn. Viva Books Private Limited, Anshan Schluter D, Grant PR (1984) Ecological correlates of morphological evolution in a Darwin’s finch Geospiza difficilis. Evolution 38(4):856–869

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Schwenk K (2000) Feeding: form, function and evolution in tetrapod vertebrates. Elsevier, London Smith KK (1993) The form of the feeding apparatus in terrestrial vertebrates: studies of adaptation and constraint. The Skull 3:150–196 Stauffer RC (1957) Haeckel Darwin and ecology. Q Rev Biol 32(2):138–144 Stroud JT, Losos JB (2016) Ecological opportunity and adaptive radiation. Annu Rev Ecol Evol Syst 47:507–532 Thompson DW (1917) On growth and form, 1st edn. Cambridge University Press, Cambridge UK Thomson KS (1988) Morphogenesis and evolution. Oxford University Press, Oxford Tokita M, Yano W, James HF, Abzhanov A (2017) Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin’s finches and Hawaiian honeycreepers. Phil Trans R Soc B 372(1713):20150481 Tseng ZJ, Flynn JJ (2015) Are cranial biomechanical simulation data linked to known diets in extant taxa? A method for applying diet-biomechanics linkage models to infer feeding capability of extinct species. PLoS One 10(4):e0124020 Vannier J (2009) L’Explosion cambrienne ou l’émergence des écosystemes modernes. CR Palevol 8(2–3):133–154 Wainwright PC (1994) Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 42–59 Wainwright PC (2007) Functional versus morphological diversity in macroevolution. An Rev Ecol Evol Syst 38:381–401 Wake MH (2015) Hierarchies and integration in evolution and development. In: Conceptual change in biology. Springer, Dordrecht, pp 405–420 Wilga CA, Ferry LA (2015) Functional anatomy and biomechanics of feeding in elasmobranchs. In: Fish physiology, vol 34. Academic Press, pp 153–187

Part I

Overview: From Structure to Behavior

Chapter 2

Functional Morphology of Vertebrate Feeding Systems: New Insights from XROMM and Fluoromicrometry Elizabeth L. Brainerd and Ariel L. Camp

Abstract Investigations in the form–function relationships of vertebrate feeding systems have a long and illustrious history of inferring function from anatomical structure and specimen manipulation, and a shorter but highly successful history of measuring function directly in living animals with sophisticated methods such as electromyography, bone strain gauges, high-speed cinematography, and cineradiography. Two new methods, X-ray Reconstruction of Moving Morphology (XROMM) and fluoromicrometry show great promise for revealing the 3D form–function relationships of cranial and cervical musculoskeletal structures. XROMM has been applied to measure 3D jaw kinematics and tooth occlusion in mammalian mastication and 3D pharyngeal jaw mechanics in fishes. The form–function relationships of the temporomandibular and other cranial joints are being explored with XROMM, including cranial kinesis in squamates, birds, and fishes. Muscle strain can be measured with fluoromicrometry by implanting small radio-opaque beads and tracking them with biplanar fluoroscopy. Fluoromicrometry has been used to measure muscle strain in muscles with complex architectures, such as the axial muscles during suction feeding in fishes and tongue deformation during swallowing in mammals. XROMM, fluoromicrometry, and buccal pressure measurements together have been used to measure the instantaneous power required for suction feeding and relate required power to the available muscle power. In the future, some systems that may benefit greatly from XROMM and fluoromicrometry are tooth–food interactions during mastication, food transport and swallowing, and the form–function relationships of feeding muscles with complex muscle-tendon architecture, such as the mammalian muscles of mastication and the multi-part adductor mandibulae of fishes.

E. L. Brainerd (B) Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA e-mail: [email protected] A. L. Camp Department of Musculoskeletal Biology, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool L7 8TX, UK e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_2

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2.1 Introduction Some of the form–function relationships between head structures and feeding performance are fairly obvious and quite satisfying. Teeth, in particular, are often unmistakably the right tools for the job at hand: herbivorous vertebrates tend to have flat, ridged teeth for grinding plant matter, carnivores have knife-like blades for slicing flesh, and durophagous vertebrates have flat teeth for breaking prey without breaking their teeth. Teeth are a prominent component of the vertebrate fossil record, extending these form–function inferences into the deep past. Analogies with human tools also suggest inferences about jaw shape and biting, with short jaws being analogous to pliers generating high bite forces and long jaws analogous to hedge trimming shears with rapid closure at the tips. The mechanical functions of feeding systems, such as those mentioned above, traditionally were inferred from morphology and manipulation of dead specimens, but extensive work to measure function directly in live animals began in the middle of the twentieth century and grew rapidly. Electromyography (EMG), high-speed cinematography, and cineradiography were applied to both aquatic and terrestrial feeding systems, and particularly to suction feeding in ray-finned fishes (e.g., Anker 1974; Grobecker and Pietsch 1979; Osse 1969) and mastication in mammals (e.g., Ardran et al. 1958; Becht 1953; Moyers 1950; reviewed in Gans et al. 1978). Highspeed film was replaced with high-speed video in the late 1980s, and then digital highspeed video in the 1990s, greatly speeding up the pace of research on animal motion (Lauder and Madden 2008). In the late 1970s, researchers began surgical implantation of strain gauges by adhering them to the bone surface to measure mandibular strain during mastication in mammals (e.g., Hylander 1977; Weijs and De Jongh 1977). Sonomicrometry has been applied extensively to measure muscle strain, i.e., the change in a muscle’s length relative to its initial length, during locomotion, and has seen some use in feeding systems for measuring muscle strain (e.g., Carroll 2004; Konow et al. 2010) and other distances through liquids or soft tissues (Sanford and Wainwright 2002). In sonomicrometry, two or more piezoelectric crystals are implanted within the muscle, and can send and receive pulses of sound. The distance between two crystals, and thus the length of the muscle, can be calculated based on the time required for a sonic pulse to travel between the crystals and the speed of sound in an aqueous medium. In the early 2000s, transducers for measuring bite force gained prominence and have been used in studies of many terrestrial and aquatic vertebrates (e.g., Herrel et al. 2001 and reviewed in Anderson et al. 2008). In addition to all of these methods for measuring feeding behavior in vivo, the methods for three-dimensional (3D) quantification of morphology ex vivo have developed rapidly and gained widespread use in the past two decades. X-ray computed tomography (CT) scanning was adapted for 3D skeletal morphology in extant vertebrates and fossils in the 1980s and 1990s (e.g., Conroy and Vannier 1984; Cranford 1988; Rowe et al. 1995, 1999), and later, the methods were developed for staining soft tissues to create X-ray contrast for CT (Gignac and Kley 2014; Jeffery et al. 2011; Metscher 2009). Microsource CT (microCT) produces high-resolution scans

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of small animals, and recent efforts to standardize CT data management and open data practices promise to vastly increase the value of CT data for comparative studies (Davies et al. 2017). Other biomedical imaging modalities, such as magnetic resonance imaging (MRI) and positron emission tomography (PET), have found some use in comparative morphology (e.g., Berquist et al. 2012; Gold et al. 2016; Montie et al. 2007). The advent of contrast-enhanced CT has made the use of MRI for static soft tissue imaging less attractive, but MRI and PET offer some exciting possibilities for functional imaging (Gold et al. 2016; MacCannell et al. 2017; Phelps 2000). The availability of 3D musculoskeletal morphology has led to great advances in 3D modeling of form–function relationships in feeding systems, particularly through finite element analysis (FEA) models of skeletal strain (reviewed in Grosse et al. 2007; Rayfield 2007), multi-body dynamics analysis (MDA) models of bite force (e.g., Gröning et al. 2013; Watson et al. 2014), and computational fluid dynamics models of suction feeding in fishes (e.g., Van Wassenbergh and Aerts 2009). A review of these modeling methods is beyond the scope of this chapter, but they are providing fundamental new insights into the functional morphology of feeding systems. They also show great promise for expanding the reach of functional morphology beyond in vivo measurements, such as to large datasets containing many species, to extinct vertebrates, and to in silico exploration of morphologies that may or may not actually occur in nature. For studies of feeding in vivo, two new methods have been developed in recent years: X-ray Reconstruction of Moving Morphology (XROMM) and fluoromicrometry (Brainerd et al. 2010; Camp et al. 2016; Knörlein et al. 2016). Below, we review and discuss the applications of these new methods to feeding systems, and consider some research questions that may particularly benefit from the study with XROMM and fluoromicrometry.

2.2 Applications of X-ray Reconstruction of Moving Morphology (XROMM) to Feeding Systems Much of what happens inside the oropharyngeal cavity during feeding is hidden by cheeks and other tissues. Cineradiography has revealed some of the actions of fleshy tongues, pharyngeal jaws, and teeth in the oral and pharyngeal regions, but cineradiography has historically provided only 2D views of complex 3D motions. A relatively new method, XROMM, is showing great promise for form–function studies of feeding because it yields simultaneous data on 3D skeletal kinematics and 3D bone shape. The 3D bone morphology usually comes from a CT scan, and 3D motion from biplanar videofluoroscopy. Polygonal mesh bone models from an individual animal are animated with motion from videofluoroscopy to match precisely, typically within 0.1 mm, the in vivo motions of the animal (Brainerd et al. 2010; Gatesy et al. 2010). The exact precision of an XROMM animation depends on multiple factors including the imaging volume, marker placement and tracking, and CT reconstruction

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Fig. 2.1 Yaw of the mandible in alternating left–right chewing cycles in a miniature pig. a Joint coordinate system is used to measure motion of the mandible relative to the cranium (not shown) as rotation about a dorsoventral axis (yaw, green dotted axis), a mediolateral axis (depression and elevation, blue dashed axis), and a rostrocaudal axis (roll, red solid axis). b Mandibular rotation about each axis (colors as in panel a) during chewing cycles, along with the occlusal phase (gray bars) (modified from Menegaz et al. 2015)

(Knörlein et al. 2016), and is often better than 0.1 mm (e.g., Camp and Brainerd 2015; Dawson et al. 2011; Gidmark et al. 2012; Konow et al. 2015). The 3D kinematics of jaws is an excellent subject for XROMM analysis. Many studies are ongoing, but to date, only a few have been published. In juvenile miniature pigs feeding on pig chow, XROMM demonstrated that the lower jaw yaws about a dorsoventral axis (Fig. 2.1) to produce the observed alternating left–right chewing cycles responsible for food reduction (Menegaz et al. 2015). This yaw of the entire lower jaw is produced by asymmetrical protrusion at the left and right temporomandibular joints (TMJs). By contrast, in ferrets and kinkajous, lateral motions of the mandible are produced primarily by lateral translation of the mandibular condyles relative to the mandibular fossae, not yaw of the entire jaw (Davis 2014). In the shorttailed opossum, long-axis rotation of the hemimandibles occurs in each chewing cycle, with a smaller counter-rotation during tooth occlusion (Bhullar et al. 2019). In three species of nonhuman primates, helical axis analysis of jaw depression and elevation showed that the axis of rotation of the mandible is located inferior to the TMJ, and this location varies among species (Iriarte-Diaz et al. 2017). In fishes, the pharyngeal jaws of grass carp were shown to grind grasses with an oblique grinding stroke shaped by the upper occlusion surface, a keratinous chewing pad (Gidmark et al. 2014). These studies demonstrate the ability of XROMM not only to reveal motions previously hidden by cheeks and other tissues, but also to describe quantitatively that motion using anatomically relevant axes.

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Temporomandibular joint shape varies substantially among mammals, and XROMM has the potential to reveal TMJ form–function relationships that could then be used to infer mandibular motion across many extant and extinct species. Thus far, the expected general patterns have held: omnivorous pigs and primates have broad, flat TMJs and show substantial bilateral and unilateral protrusion at the TMJ (Iriarte-Diaz et al. 2017; Menegaz et al. 2015), whereas carnivores, such as ferrets, have cylindrical TMJs that restrict motion to depression, elevation and lateral translation (Davis 2014). The functional significance, if any, of smaller differences in TMJ morphology among more closely related species remains to be explored with XROMM. The broader form–function relationships of cranial joints are also being studied with XROMM (Olsen et al. 2017a, b). In this approach, using channel catfish as a beginning model system, joint fitting routines extract the joint type, such as ball and socket, saddle or hinge, from large XROMM motion datasets of diverse motions from individual animals. Sets of joints in kinetic skulls, such as those of birds and fishes, can then be linked into 3D mechanisms that further determine the degrees of freedom of the system (Olsen and Westneat 2016). This approach has the potential to provide new insights into the form–function relationships of bones, joints, and linkage mechanisms that could then be applied to large-scale studies of museum specimens of extant and extinct vertebrates. The nature of tooth occlusion in mammals is particularly hard to study with traditional methods because, necessarily, during occlusion, the chewing surfaces are visually occluded preventing any standard video analysis. The power of XROMM for studying tooth occlusion is that the mesh model from the CT scan includes all the details of tooth morphology. The XROMM animation then includes the position of every location on every tooth at all times. For example, in miniature pigs feeding on pig chow, XROMM demonstrated that the yaw of the mandible produces a grinding motion between upper and lower premolars that includes a substantial mesiodistal component, in addition to the expected buccolingual component, resulting in an oblique power stroke (Fig. 2.2). The evolutionary origin of jaw yaw as it relates to tooth occlusion and the muscles of mastication has recently been explored (Grossnickle 2017). These results from miniature pigs demonstrate that XROMM can be used to study the details of tooth–tooth interaction during tooth occlusion in mammals, a potentially fruitful direction for continuing to explore the form–function relationships of teeth. Another finding from work on miniature pigs is that XROMM can reveal some information about the breakdown of the food bolus (Menegaz et al. 2015). Jaw kinematics from processing a Brazil nut in the shell showed evidence of when the nut broke, and then a gradual decrease in the distance between upper and lower teeth, as indicated by increasing jaw elevation (Fig. 2.3), as the size of the nut and shell fragments were reduced. These findings drive home the point that teeth in living animals work with food between them, not with the teeth occluding directly. Depending on the nature of the food, the form–function relationships of the teeth may be changing constantly during a bout of mastication as the particle size, consistency, and bolus size change. With XROMM, these tooth–food interactions can be studied

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Fig. 2.2 Oblique stroke of lower premolars against upper premolars during occlusion in a miniature pig. a Spheres were fitted to the cusp of a left (blue) and right (red) lower premolar to trace their motion as part of the XROMM-animated mandible model. b Ventral view of the cranium, showing the positions of the corresponding upper premolars. c Ventral view of the cranium showing path of the lower premolars as superimposed spheres, with arrows indicating the direction of the stroke during occlusion (modified from Menegaz et al. 2015)

directly, although work is needed to develop methods for radio-opaque marking of the food that will not obscure the teeth and may provide discrete information about food breakdown. Unlike mammals, most vertebrates have many mobile skeletal elements within the skull and substantial intracranial kinesis. However, these motions are often threedimensionally complex, involve structures not visible externally, or both, making them difficult to study in vivo with traditional video analysis. In squamates, mesokinesis has long been postulated from morphology and manipulation of dead specimens and has recently been confirmed in living Tokay geckos with XROMM (Montuelle and Williams 2015). In Tokay geckos, the snout rotates dorsally relative to the braincase during wide gape display behaviors and ventrally during defensive and feeding bites. In birds, the quadrate bone is the central junction of kinesis, suspending the lower bill and articulating via the palatal bridge to the upper bill. In ducks, an XROMM study showed that 3D motions of the quadrate include mediolateral motions associated with lateral spreading of the hemimandibles and rostrocaudal motions associated with upper bill elevation and depression (Dawson et al. 2011). Ray-finned fishes are the champions of cranial kinesis with more than 20 mobile cranial and hyoid bones that contribute to food acquisition, transport, and processing

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Rotations (deg)

0

-5

-10 elevation

-15 depression

0.2

0.4

0.6

0.8

1.0

1.2

1.4

Time (s)

Fig. 2.3 Rotations of the mandible during breaking and reduction of nut and shell pieces in a miniature pig. Mandible rotation, relative to the cranium, was measured about a dorsoventral axis (yaw, green dotted line), a mediolateral axis (depression and elevation, blue dashed line), and a rostrocaudal axis (roll, red solid line) (see Fig. 2.1). Zero elevation of the mandible indicates zero gape (teeth in occlusion), and the mandible can be seen to elevate more and more toward occlusion with each chewing cycle. The time of the nut breaking is indicated by the black arrow (modified from Menegaz et al. 2015)

(Liem 1980). These cranial elements are linked in mechanisms, such as the opercular linkage, which is thought to contribute to lower jaw depression. Planar 4-bar linkage models have been shown to fit this mechanism poorly (Van Wassenbergh et al. 2005b; Westneat 1990, 1994), with XROMM demonstrating up to 50% overestimate of lower jaw depression from opercular rotation in largemouth bass (Camp and Brainerd 2015). Working from 3D XROMM data, the best-fit model for the opercular mechanism was found to be a 3D, 3-DoF 4-bar linkage, achieving rotational errors of less than 5% (Olsen et al. 2017a, b). In studies of suction feeding in fishes, a long-standing problem has been our inability to make empirical measurements of the rate of expansion of the oropharyngeal cavity during this rapid behavior. Excellent work has been done modeling this expansion as an increasingly complex set of expanding cones or elliptical slices for fluid dynamic and computational fluid dynamic models of suction feeding (e.g., Muller and Osse 1984; Muller et al. 1982; Van Wassenbergh and Aerts 2009; Van Wassenbergh et al. 2005a) (Fig. 2.4). Now, we can also measure the rate of volume expansion directly with XROMM, by marking most of the cranial bones with tiny (0.5–0.8 mm) radio-opaque spheres, tracking them with biplanar videofluoroscopy, and animating the bones with XROMM. These bones then define the outer shell of the oropharyngeal cavity, and a deformable polygon can be fit within the space to yield a dynamic digital endocast of the instantaneous volume at each time step (Fig. 2.5). The soft tissues within the mouth are not included, so the absolute volume of the endocast will always be larger than the true volume, but the change in volume per time will be correct. Combined with the pressure measured in the buccal cavity, the instantaneous suction power can be calculated throughout the suction-feeding strike (Camp et al. 2015).

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(a)

r2

initial mouth volume

r1

mouth aperture opercular cavity

(b) caudal r4

middle r3

rostral r2

r1

(c)

Fig. 2.4 Methods for measuring mouth volume changes during suction feeding in fishes. a Volume change of the mouth cavity was initially modeled as a single expanding cone, with two radii representing the change in the mouth aperture (r1) and opercular cavity (r2) during suction feeding. The cone is shown at its initial position prior to the strike (solid lines, white region), at the maximum expansion of the mouth aperture (dashed lines, light gray region), and at the maximum expansion of the opercular cavity (dashed lines, dark gray region) (after Muller and Osse 1984). b A modified model consisting of three truncated cones, with four radii (r1–r4) to allow different rostrocaudal regions of the mouth to expand at different times and rates, as is observed in live fish (after Van Wassenbergh et al. 2006). c The ellipse method (Drost and Vandenboogaart 1986) is used to calculate static mouth volume by representing the mouth cavity as a series of ellipses and summing the volumes of each to calculate total mouth volume, for example, before the strike (solid lines, white region) and at peak mouth expansion (dashed lines, gray region). It can also be used to model mouth volume changes by dynamically changing the major and minor axes of each ellipse based on the kinematics of mouth expansion (after Van Wassenbergh et al. 2006)

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Fig. 2.5 Digital dynamic endocast for measuring mouth volume during suction feeding in largemouth bass. a The endocast (purple polygon) is fit to XROMM-animated models of the bones defining the left side of the mouth cavity, shown here prior to suction expansion. b As the bones move during suction expansion, the endocast deforms and expands to fill the growing mouth cavity. The endocast and skeleton are shown here at peak expansion. c The volume of the endocast, shown here without the skeletal models, can be measured at every time point and doubled to calculate total mouth volume by assuming bilateral symmetry (modified from Camp et al. 2015)

In some circumstances, XROMM can also be used to measure in vivo changes in muscle length. In muscles with fairly straight fascicles, simple architecture and no tendon, the attachment points of the muscle fascicles can be mapped onto the mesh models of the bones, the bones animated with XROMM, and then the lengths of the fascicles measured at each time step (Fig. 2.6). This technique was used for the pharyngeal jaw levator muscle of the black carp, a durophagous cyprinid specializing on snails and other hard-shelled prey (Gidmark et al. 2013). The in vivo muscle lengths from XROMM were combined with in situ length–tension curves and in vivo shell-crushing performance to show that pharyngeal bite force drops off at both small and large pharyngeal jaw gapes resulting from small and large prey shell sizes. In this study, muscle strain in vivo could be measured from XROMM due to the levator muscle being a simple, fan-shaped muscle with no tendon (Fig. 2.6). The lack of fixed-end compliance, as would be found with a tendon or other series elasticity in the muscle, was confirmed with the in situ force-length recordings (Gidmark et al. 2013).

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Fig. 2.6 Pharyngeal levator muscle in the black carp. The fan-shaped muscle (fibers in dashed lines) attaches directly to the dorsal process of the pharyngeal jaw and to the interior of the large levator fossa in the neurocranium, without tendons that would introduce series elastic compliance (modified from Gidmark et al. 2013)

Muscle strain was also measured from XROMM animations for some of the muscles of the head in largemouth bass (Camp et al. 2015) and bluegill sunfish (Camp et al. 2018): the levator operculi, dilator operculi, sternohyoideus, and levator arcus palatini. These muscles also have fairly simple architecture and little or no tendon, and in one muscle, length measurements were also confirmed with radio-opaque beads implanted into the muscle belly (i.e., fluoromicrometry) (Camp et al. 2015). However, when a free tendon or other source of fixed-end compliance is present, XROMM provides only the distance between attachment points on the bones, which is the length of the whole muscle-tendon unit (MTU) and not the length of the muscle fascicles. In these cases, muscle length changes should be measured directly with fluoromicrometry: implanting radio-opaque beads into the muscle belly, recording marker motion in vivo with biplanar fluoroscopy, and tracking markers in 3D to measure muscle length changes from the intermarker distance changes. Fluoromicrometry can yield muscle length measurements with a precision of 100 µm (Camp et al. 2016), although as with XROMM, the precision may vary with the imaging setup and marker placement and tracking (Knörlein et al. 2016). Fluoromicrometry can be combined with XROMM to measure both muscle and tendon length by determining MTU length from XROMM, and then subtracting muscle fascicle length changes from MTU length to get tendon length. In theory, fluoromicrometry could be used to measure tendon strain directly, but radio-opaque beads tend to get squeezed out of tendons when simply injected into the tissue (Camp et al. 2016), although beads sutured to an aponeurosis can yield aponeurosis strain (Azizi and Roberts 2009). The combination of fluoromicrometry and XROMM to measure MTU length, muscle strain, and tendon strain has been applied to jumping frogs and flying bats (Astley and Roberts 2012; Konow et al. 2015), but not yet to feeding systems.

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2.3 Applications of Fluoromicrometry to Feeding Systems Fluoromicrometry has been used to measure axial muscle strain during suction feeding in fishes and tongue deformation during swallowing in rhesus macaques (Camp and Brainerd 2014; Camp et al. 2015, 2017, 2018; Orsbon et al. 2017). As described above, the length changes in some cranial muscles of fishes can be measured directly from their attachment sites and the XROMM animations of cranial bones (Camp et al. 2015). The epaxial and hypaxial muscles of fishes, however, do not have discrete bony attachment sites. Instead, multiple tantalum beads (0.5–0.8 mm diameter) can be injected into the musculature to measure axial muscle strains throughout the epaxial and hypaxial muscle masses (Fig. 2.7). For studies such as this requiring many markers, fluoromicrometry offers an advantage over sonomicrometry, which can only simultaneously measure a limited number of pairwise distances and the maximum available sampling rate goes down with more crystals. The additional advantages of fluoromicrometry for measuring axial muscle strain are that radio-opaque tantalum beads can be placed by percutaneous injection with a hypodermic needle, no wires emerge from the animal and many pairwise distances can be measured simultaneously (Camp et al. 2016). Tantalum beads can also be injected medially, close to the axial skeleton to define a body-reference plane that can be used to measure cranial movements relative to the body (Fig. 2.7a). In mammalian mastication, the rapid 3D motions of the tongue and cheeks are extremely difficult to see and track, yet these motions are critical for bolus formation, bolus management, and swallowing. Fluoromicrometry combined with XROMM and contrast-enhanced CT (DiceCT; Gignac et al. 2016) is starting to be applied to measure hyoid and jaw kinematics, hydrostatic tongue deformation, and muscle length changes (Orsbon et al. 2017, 2018). This work on complex jaw, hyoid, and tongue motions emphasizes a great advantage of fluoromicrometry over sonomicrometry. Sonomicrometry yields only 2D distances, or at best a set of 3D distances relative to each other, but with no other anatomical context. Fluoromicrometry combined with XROMM yields both 3D bone kinematics and 3D soft tissue marker motions simultaneously, providing actual 3D soft tissue deformations with reference to bone positions. Such data will be essential for discovering the remarkable neuromotor coordination of tongue, jaws, and cheeks that allow mammals to chew and swallow so precisely and prevent tongue and cheek biting (usually) and choking (Orsbon et al. 2017, 2018).

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Fig. 2.7 Fluoromicrometry marker placement and muscle strain distribution during suction feeding in largemouth bass. a Placement of radio-opaque beads (black circles) used in fluoromicrometry to measure length changes along the epaxial (dorsal) and hypaxial (ventral) muscles. Six beads are also used to define a body-reference plane (gray rectangle) that can be used to measure cranial movements relative to the body. b Mean (±s.e.m.) muscle strain at peak neurocranium elevation in each region of the epaxials, and at peak pectoral girdle retraction in each region of the hypaxials for three fish (N = 10 strikes for each fish). Positive strain values indicate muscle shortening. The x-axis position of each bar represents the approximate rostrocaudal position of that muscle region (modified from Camp and Brainerd 2014)

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2.4 XROMM and Fluoromicrometry Case Study: Measuring Suction-Feeding Power in Fishes Suction feeding in fishes is an amazing behavior because it is lightning fast and, to the naked eye, prey seems to just disappear into the predator’s maw. Suction is produced by expansion of the entire oropharyngeal cavity (buccal and opercular cavities), sucking water and prey in through the mouth aperture. The water then flows out the gill openings, and the captured prey is retained in the pharynx and then swallowed. Accelerating a mass of water into the mouth requires substantial force, so suction feeding is both fast and forceful and therefore requires considerable muscle power (Carroll and Wainwright 2006; Van Wassenbergh et al. 2005a). Where does all that muscle power come from? One might expect feeding to be powered by cranial muscles, but in most fishes, these muscles are relatively small and may be insufficient to supply the power required for suction feeding (Fig. 2.8). We have known for a long time that epaxial muscles immediately behind the head contribute some power (e.g., Liem 1967; Osse 1969). Axial muscles are large in relation to cranial muscles, and evidence from empirical studies and modeling indicates that axial muscles must be contributing substantial power in many suction-feeding fishes (Carroll and Wainwright 2006; Gibb and FerryGraham 2005; Oufiero et al. 2012; Van Wassenbergh et al. 2008). But how much of the axial muscles (which extend from head to tail) contribute to feeding, and what proportion of suction expansion power do they generate?

Fig. 2.8 Cranial and axial musculature in largemouth bass. The four muscles of the head (dilator operculi, levator operculi, levator arcus palatini, and sternohyoideus) that can contribute to suction expansion are much smaller than the two massive axial muscles (epaxialis, hypaxialis) that can also contribute to mouth expansion during suction feeding (modified from Camp et al. 2015)

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Fig. 2.9 Methods for calculating the mechanical power required for mouth expansion during suction feeding and estimating the power the cranial and axial muscles are capable of contributing to that suction expansion. a Instantaneous buccal pressure is estimated from a pressure transducer, then multiplied by the rate of volume change to yield instantaneous suction power. b Fluoromicrometry is used to measure axial muscle shortening and the extent of shortening along the body, which in turn determined the mass of axial musculature that contributes to suction feeding. c Cranial muscle shortening is measured from muscle fascicle attachment points mapped onto the animated cranial bones. Optimum (i.e., assuming all contractile properties are optimized to maximize power production) muscle power capacity (Popt ) and velocity-corrected muscle power capacity (Pvc ) are calculated from muscle mass and measured shortening velocities, respectively

Answering these questions requires simultaneous measurements of axial and cranial muscle shortening and instantaneous suction expansion power (Fig. 2.9). As described above, XROMM and the dynamic endocast method can be used to measure instantaneous buccal expansion rate (Fig. 2.5). Instantaneous buccal pressure can be measured with a miniature pressure transducer, and pressure times rate of volume change yields instantaneous suction power (Fig. 2.9a). Fluoromicrometry can be used to measure axial muscle shortening and the extent of shortening along the body (Fig. 2.9b). The extent of shortening is needed to determine the mass of axial musculature that contributes to suction feeding, as only actively shortening muscles can generate power. Cranial muscle shortening can be determined from fluoromicrometry or muscle fascicle attachment points mapped onto the animated cranial bones (Fig. 2.9c). The maximum amount of power that could be generated by the cranial and axial muscles can be estimated from their masses, assuming optimal activation and shortening rate, yielding optimal muscle power capacity (Popt ). Actual muscle shortening rates from XROMM and fluoromicrometry (Fig. 2.10) can then be taken into account to estimate velocity-corrected power capacity (Pvc ), which is a best estimate of the actual maximum power available from each muscle during any given strike (Fig. 2.9c). Using these methods, we compared suction power to muscle power capacity and showed that at least 95% of the power for high-performance strikes comes from axial muscles in largemouth bass (Figs. 2.11 and 2.12). The epaxials and hypaxials have by far the largest Popt , due to the large mass of muscle employed, and they also shorten

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Fig. 2.11 Comparison of suction expansion power and cranial muscle power capacity for three individual largemouth bass. Mouth expansion power of all strikes (black lines) are graphed as a function of time for each individual. The optimal power capacity (Popt , red dashed line) and median of the velocity-corrected power capacity (Pvc , pink solid line) of all of the cranial muscles summed together are shown for each individual (from Camp et al. 2015)

consistently during peak power production (Fig. 2.10). In contrast, the Popt of the cranial muscles can hardly be seen on the same scale as the axial muscles (Fig. 2.12). Only the sternohyoideus shows substantial potential for power generation, Popt , but in fact, on average, it does not shorten during peak power production (Fig. 2.10), and hence realizes near zero Pvc (Fig. 2.12). These results indicate that largemouth bass use the bulk of their axial muscles for high power strikes, transferring power from the axial to the cranial systems. This power transfer is analogous to athletic feats in many human sports: just as baseball pitchers transfer power efficiently from their legs and core to their throwing arms, so largemouth bass transfer power from body to head. Our finding that most of the axial muscle mass is recruited for suction feeding suggests that we may need to reconsider the structure and function of these body muscles in fishes. While the red musculature along the lateral sides of the body and the musculature near the tail may function for swimming only, the bulk of the white axial musculature likely has dual functions in feeding and swimming. In the past, axial muscles and the vertebral column in fishes have been analyzed primarily for their role in swimming. Viewing them as feeding structures, or at least dual-function structures, offers a new framework for understanding the form–function relationships of the axial musculoskeletal system. Similarly, viewing the cranial musculoskeletal system as a power transmitter, rather than solely a power generator, may yield new insights into its evolutionary and functional morphology. To date, this suction power analysis has been published for just two species, largemouth bass and bluegill sunfish, and it remains to be determined whether axial musculature is the primary source for power in fishes with different mouth and body forms and/or distant phylogenetic relationships to these two centrarchid fishes. There are several reasons to predict that axial power is widespread: (1) in ray-finned fishes, the mass of the axial musculature greatly exceeds that of the cranial musculature; (2) cranial elevation and epaxial and hypaxial muscle activity are primitive

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Fig. 2.12 Optimal (Popt ) and velocity-corrected (Pvc ) muscle power capacities of largemouth bass. a For all three individuals (n = 29 strikes), gray bars show Popt and unfilled box plots show Pvc . The power required for buccal expansion is shown in a box plot on the extreme right, and all box plots represent the 25th and 75th percentiles of the data (bottom and borders), the median (black line) and 1.5 times the interquartile range (whiskers). b The inset shows the same data, but with the y-axis limited to 0.5 Watts to visualize the power capacities of the smallest three cranial muscles (modified from Camp et al. 2015)

for Actinopterygii (Lauder 1980); and (3) largemouth bass and bluegill sunfish have substantially different cranial morphologies and feeding kinematics (Higham et al. 2006), suggesting axial-powered suction feeding is not limited to a single set of morphologies or behaviors. If, as we expect, axial power does turn out to be widespread, then we’ll have a new framework for studying morphology and biomechanics of ray-finned fishes. This new framework will facilitate the study of form–function relationships throughout the entire fish body. Since the vast majority of the more than 30,000 species of ray-

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finned fishes feed at least partially by suction, we may be on the verge of a powerful new understanding of overall body shape, of axial form and function, and of cranial form and function in over half of all vertebrate species.

2.5 Potential Future Applications of XROMM and Fluoromicrometry to Feeding Systems XROMM will continue to yield fundamental insights into feeding systems through the measurement of 3D motion at joints and determining the relationship of jaw kinematics to the function of teeth during chewing. XROMM will also be key for exploring the sources of muscle power for suction feeding in diverse species of fishes. The use of XROMM and fluoromicrometry to study tongue and cheek kinematics in mammals has just begun and shows great promise. In aquatic animals, food handling during transport and processing is generally controlled by precise water motions known as the hydrodynamic tongue. With the exception of some work on lungfish (Bemis and Lauder 1986), form–function relationships of the hydrodynamic tongue have hardly been explored at all. In general, the study of food transport and swallowing across all vertebrates are areas that XROMM and fluoromicrometry have particular potential to revolutionize in the near future. In studies of food processing, XROMM has the potential to start to show how teeth actually interact with the food and each other. Tooth form and function have often been studied from the perspective of upper and lower teeth interacting, but of course, teeth rarely interact directly because there is food between them. The effects of food bolus breakdown on jaw kinematics and tooth occlusion can be quantified with XROMM (Fig. 2.3). Food breakdown requires putting some energy (work) into the food to create more surface area. XROMM and fluoromicrometry together have the potential to link muscle work to work done on the food via 3D jaw and tooth kinematics. Another area that would be exciting to explore with XROMM and fluoromicrometry is the form–function relationship of muscles and tendons in feeding systems. In studies of locomotion, a great deal of experimental and conceptual work has been done to develop principles of muscle-tendon function. The roles of muscles and tendons in producing force, work, and power have been clearly defined, as have their roles in energy conservation, power amplification, and power attenuation (reviewed in Roberts and Azizi 2011). The effects of fundamental muscle properties, such as length-tension and force-velocity, have been explored in many forms of locomotion (reviewed in Biewener 2016). Such principles of muscle and tendon function have not been so clearly defined for feeding systems, but XROMM and fluoromicrometry have the potential to provide in vivo data toward such a synthesis. In particular, integrating detailed muscle architecture data from DiceCT, in vitro muscle mechanics data, and in vivo muscle and tendon length changes from XROMM and fluoromicrometry may be a powerful combination. Similar XROMM work

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showed that the length–tension properties of the pharyngeal jaw levator in black carp limits both the largest and smallest mollusk shells that can be crushed (Gidmark et al. 2013). But the architecture of the levator muscle is very simple, with no tendon introducing series elastic compliance into the system (Fig. 2.6). The multipennate masseter muscle of mammals offers a much more complex problem. The masseter must have one or more aponeuroses for pennate fiber attachment, and the fact that these tendinous tissues introduce series compliance can be easily felt in one’s own masseter (and temporalis): bring your teeth into occlusion and then bite gradually harder and you’ll feel the muscles bulging out as their fibers shorten with no change in jaw position. The fibers can only shorten because the tendons are lengthening, and increasing force increases the fiber shortening, tendon lengthening and muscle bulging. Muscle bulging is known to feedback into force and speed of shortening through dynamic architectural changes in fiber orientation (Azizi et al. 2008; Brainerd and Azizi 2005). The complex architecture of some feeding muscles, such as the mammalian muscles of mastication and the multi-part adductor mandibulae of fishes, are ripe for exploration with DiceCT, fluoromicrometry, and XROMM. Lastly, these emerging techniques offer the opportunity to study the feeding roles of structures outside the head: the vertebral column, shoulder girdle, and neck. While feeding studies may predominantly focus on the head alone, the head and body are connected anatomically—either directly (in non-tetrapod fish) or via the neck (in tetrapods)—and likely mechanically as well. This connection can be seen most clearly in ray-finned fishes where the body muscles generate power for suction feeding, and the vertebral column and pectoral girdle transmit that power to the feeding apparatus. While flexion of the vertebral column has not yet been measured during suction feeding, XROMM studies of ray-finned fishes have confirmed that the pectoral girdle swings caudally to help expand the mouth cavity (Camp and Brainerd 2014; Camp et al. 2015, 2018). Pectoral girdle motion has also been found to contribute to mouth expansion in a suction-feeding shark (Camp et al. 2017), even though it lacks any skeletal articulation with the skull. These results demonstrate that, like the body muscles, the pectoral girdle can have a dual role in feeding and locomotion, and both these roles have likely influenced its evolution and morphology. XROMM and fluoromicrometry are excellent tools for investigating how widespread these roles are among ray-finned and cartilaginous fishes, and whether the neck may perform similar functions during feeding in tetrapods. One final advance that will also be critical for moving the field forward is data archiving and sharing. Comparative biology depends on comparing species, but for too long, we have tended to collect and store data without much thought of sharing and reuse. The functional morphology research community, and feeding researchers in particular, is leading the way toward open data sharing in organismal biology. A database for EMG studies of mammalian feeding has been established, the FEED database (Wall et al. 2011), as well as standards and databases for X-ray video and standard video management (Brainerd et al. 2017), and standards for CT data management (Davies et al. 2017). The ability to synthesize results collected from many species, combined with new in vivo and in silico methods, suggests exciting years ahead in the functional morphology of vertebrate feeding systems.

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Acknowledgements The preparation of this chapter was supported in part by the US National Science Foundation under grant number 1655756 to ALC and ELB and number 1661129 to ELB and by the UK Biotechnology and Biosciences Research Council under a Future Leader Fellowship to ALC.

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Grosse IR, Dumont ER, Coletta C, Tolleson A (2007) Techniques for modeling muscle-induced forces in finite element models of skeletal structures. Anat Rec (Hoboken) 290:1069–1088. https:// doi.org/10.1002/ar.20568 Grossnickle DM (2017) The evolutionary origin of jaw yaw in mammals. Sci Rep 7:45094 Herrel A, De Grauw E, Lemos-Espinal JA (2001) Head shape and bite performance in xenosaurid lizards. J Exp Zool A 290:101–107 Higham TE, Day SW, Wainwright PC (2006) Multidimensional analysis of suction feeding performance in fishes: fluid speed, acceleration, strike accuracy and the ingested volume of water. J Exp Biol 209:2713–2725. https://doi.org/10.1242/jeb.02315 Hylander WL (1977) In vivo bone strain in the mandible of Galago crassicaudatus. Am J Phys Anthropol 46:309–326 Iriarte-Diaz J, Terhune CE, Taylor AB, Ross CF (2017) Functional correlates of the position of the axis of rotation of the mandible during chewing in non-human primates. Zoology 124:106–118 Jeffery NS, Stephenson RS, Gallagher JA, Jarvis JC, Cox PG (2011) Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. J Biomech 44:189–192 Knörlein BJ, Baier DB, Gatesy SM, Laurence-Chasen JD, Brainerd EL (2016) Validation of XMALab software for marker-based XROMM. J Exp Biol 219:3701–3711. https://doi.org/10. 1242/jeb.145383 Konow N, Thexton A, Crompton A, German RZ (2010) Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing. J App Physiol 109:439–448 Konow N, Cheney JA, Roberts TJ, Waldman JR, Swartz SM (2015) Spring or string: does tendon elastic action influence wing muscle mechanics in bat flight? Proc Biol Sci 282:20151832. https:// doi.org/10.1098/rspb.2015.1832 Lauder GV (1980) Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. J Morphol 163:283–317 Lauder GV, Madden PG (2008) Advances in comparative physiology from high-speed imaging of animal and fluid motion. Annu Rev Physiol 70:143–163 Liem KF (1967) Functional morphology of the head of the anabantoid teleost fish, Helostoma temmincki. J Morphol 121:135–157 Liem KF (1980) Acquisition of energy by teleosts: adaptive mechanisms and evolutionary patterns. In: Ali MA (ed) Environmental physiology of fishes. NATO advanced study institutes series (Series A: Life science), vol 35. Springer, Boston, pp 299–334 MacCannell A, Sinclair K, Friesen-Waldner L, McKenzie CA, Staples JF (2017) Water–fat MRI in a hibernator reveals seasonal growth of white and brown adipose tissue without cold exposure. J Comp Physiol B 187:759–767 Menegaz RA, Baier DB, Metzger KA, Herring SW, Brainerd EL (2015) XROMM analysis of tooth occlusion and temporomandibular joint kinematics during feeding in juvenile miniature pigs. J Exp Biol 218:2573–2584. https://doi.org/10.1242/jeb.119438 Metscher BD (2009) MicroCT for comparative morphology: simple staining methods allow highcontrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9:11 Montie EW, Schneider GE, Ketten DR, Marino L, Touhey KE, Hahn ME (2007) Neuroanatomy of the subadult and fetal brain of the Atlantic White-sided Dolphin (Lagenorhynchus acutus) from in situ magnetic resonance images. Anat Rec 290:1459–1479 Montuelle SJ, Williams SH (2015) In vivo measurement of mesokinesis in Gekko gecko: the role of cranial kinesis during gape display, feeding and biting. PLoS ONE 10:e0134710. https://doi. org/10.1371/journal.pone.0134710 Moyers RE (1950) An electromyographic analysis of certain muscles involved in temporomandibular movement. Amer J Orthod 36:481–515 Muller M, Osse J (1984) Hydrodynamics of suction feeding in fish. Trans Zool Soc Lond 37:51–135 Muller M, Osse J, Verhagen J (1982) A quantitative hydrodynamical model of suction feeding in fish. J Theor Biol 95:49–79

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Olsen AM, Westneat MW (2016) Linkage mechanisms in the vertebrate skull: structure and function of three-dimensional, parallel transmission systems. J Morphol 277:1570–1583 Olsen AM, Camp AL, Brainerd EL (2017a) The opercular mouth-opening mechanism of largemouth bass functions as a 3D four-bar linkage with three degrees of freedom. J Exp Biol 220:4612–4623 Olsen AM, Hernandez LP, Camp AL, Brainerd EL (2017b) Linking morphology and motion: testing multibody simulations against in vivo cranial kinematics in suction feeding fishes using XROMM. FASEB J 31:90.91–90.91 Orsbon CP, Gidmark NJ, Ross CF (2017) Analysis of the primate “squeeze-back” swallowing mechanism using X-ray reconstruction of moving morphology and fluoromicrometry. FASEB J 31:393.391–393.391 Orsbon CP, Gidmark NJ, Ross CF (2018) Dynamic musculoskeletal functional morphology: integrating diceCT and XROMM. Anat Rec 301:378–406 Osse JWM (1969) Functional morphology of the head of a perch (Perca fluviatilis L.): an electromyographic study. Neth J Zool 19:289–392 Oufiero CE, Holzman RA, Young FA, Wainwright PC (2012) New insights from serranid fishes on the role of trade-offs in suction-feeding diversification. J Exp Biol 215:3845–3855. https://doi. org/10.1242/jeb.074849 Phelps ME (2000) Positron emission tomography provides molecular imaging of biological processes. Proc Natl Acad Sci USA 97:9226–9233 Rayfield EJ (2007) Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu Rev Earth Plant Sci 35:541–576. https://doi.org/10.1146/ annurev.earth.35.031306.140104 Roberts TJ, Azizi E (2011) Flexible mechanisms: the diverse roles of biological springs in vertebrate movement. J Exp Biol 214:353–361 Rowe T, Carlson W, Bottorff W (1995) Thrinaxodon: digital atlas of the skull CD-ROM (Second Edition, for Windows and Macintosh platforms). University of Texas Press, Austin, Texas, 547 Rowe T, Brochu CA, Kishi K (1999) Cranial morphology of Alligator mississippiensis and phylogeny of Alligatoroidea. Northbrook, III, Society of Vertebrate Paleontology Memoir 6. J Vertebr Paleontol 19(supplement to 2):1–100 Sanford CP, Wainwright PC (2002) Use of sonomicrometry demonstrates the link between prey capture kinematics and suction pressure in largemouth bass. J Exp Biol 205:3445–3457 Van Wassenbergh S, Aerts P (2009) Aquatic suction feeding dynamics: insights from computational modelling. J R Soc Interface 6:149–158. https://doi.org/10.1098/rsif.2008.0311 Van Wassenbergh S, Aerts P, Herrel A (2005a) Scaling of suction-feeding kinematics and dynamics in the African catfish, Clarias gariepinus. J Exp Biol 208:2103–2114 Van Wassenbergh S, Herrel A, Adriaens D, Aerts P (2005b) A test of mouth-opening and hyoiddepression mechanisms during prey capture in a catfish using high-speed cineradiography. J Exp Biol 208:4627–4639. https://doi.org/10.1242/jeb.01919 Van Wassenbergh S, Aerts P, Herrel A (2006) Hydrodynamic modelling of aquatic suction performance and intra-oral pressures: limitations for comparative studies. J R Soc Interface 3(9):507–514 Van Wassenbergh S, Strother JA, Flammang BE, Ferry-Graham LA, Aerts P (2008) Extremely fast prey capture in pipefish is powered by elastic recoil. J R Soc Interface 5:285–296. https://doi.org/ 10.1098/rsif.2007.1124 Wall CE, Vinyard CJ, Williams SH, Gapeyev V, Liu X, Lapp H, German RZ (2011) Overview of FEED, the feeding experiments end-user database. Integr Comp Biol 51:215–223 Watson PJ, Groning F, Curtis N, Fitton LC, Herrel A, McCormack SW, Fagan MJ (2014) Masticatory biomechanics in the rabbit: a multi-body dynamics analysis. J R Soc Interface 11. https://doi.org/ 10.1098/rsif.2014.0564 Weijs W, De Jongh H (1977) Strain in mandibular alveolar bone during mastication in the rabbit. Arch Oral Biol 22:667–675

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Westneat MW (1990) Feeding mechanics of teleost fishes (Labridae; Perciformes): a test of four-bar linkage models. J Morphol 205:269–295. https://doi.org/10.1002/jmor.1052050304 Westneat MW (1994) Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei: Perciformes). Zoomorphology 114:103–118. https://doi.org/10.1007/bf00396643

Chapter 3

What Does Musculoskeletal Mechanics Tell Us About Evolution of Form and Function in Vertebrates? Emily J. Rayfield

Abstract Functional loading generates stress and strain within the skeleton. Deducing how the skull stresses and strains has the potential to inform on what feeding and other behavioural loads the skeleton can withstand and the functional consequences of changes to shape. When applied in deep time, mechanical analysis of the skeleton may be used to determine the function of extinct organisms but also higher level questions such as niche partitioning, the evolutionary relationship between form, function and disparity, rates of functional evolution and the influence of constraints on morphological evolution. One method for deducing stress and strain in complex structures is finite element (FE) analysis. FE models have the potential to address questions of the evolution of form and function in vertebrates, but it is important to consider the assumptions and potential errors involved in creating and analysing FE simulations of function and behaviour. Currently lacking is an understanding of phylogenetic variability in various FE model input parameters such as bone material properties, muscle stress and adductor muscle pennation and fibre lengths. How within-species mechanical function relates to across-species function is still largely unknown. However, if the accuracy of an FE model can be estimated, then it is possible to frame appropriate questions to test long-standing functional hypotheses and deduce pattern and process in the relationship between form and function.

3.1 Why Study Function in the Fossil Record? Insight into Pattern and Process The interplay between form and function has been studied for millennia and is a central concept in the fields of design and engineering, as well as the evolutionary sciences (Blits 1999; Padian 1995). With respect to the fossil record, the study of organismal form can be used to infer the function of extinct animals, whose behaviour leaves little in the way of hard evidence, save trace fossils and typically, the hard parts E. J. Rayfield (B) School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UK e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_3

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of the skeleton. Functional studies of individual taxa provide insight into questions of diet, behaviour, ecological role, answering the ‘how did it work?’ question. Studies may focus on body plans not realised in extant taxa, such as multi-tonne sauropod or theropod dinosaurs (Bates et al. 2016; Sakamoto 2010), or the function of convergently acquired features not realised in extant taxa, such as sabre teeth or bizarre elongate manual claws (Andersson et al. 2011; Lautenschlager 2014; McHenry et al. 2007; Slater and Van Valkenburgh 2009). Given that most organisms that ever existed are extinct, these functional studies provide a much broader picture of the range of solutions available to environmental or evolutionary challenges, and what may be the extremes of morphological specialisation. Functional studies of individual taxa are important and interesting in their own right, but are also the foundation for further downstream ecological and macroevolutionary questions. These are best captured by Witmer’s ‘pyramid of inference’ (Witmer 1995; Fig. 3.1). Beginning with osteological data—the fossils themselves—soft tissues are then inferred, leading to an estimation of functional morphology, and subsequently mode of life. Repeating this process for numerous contemporaneous taxa may provide insight into palaeoecological interactions. By recording functionally relevant metrics such as limb or tooth proportions or aspects of jaw design, and using ordination methods, it may be possible to capture a measure of the ‘functional diversity’ of a community or a clade (Anderson et al. 2011; Stubbs et al. 2013). For example, sauropod dinosaurs that coexist in the Late Jurassic Morrison Formation occupy different regions of a functionally derived morphospace, suggestion variance in jaw function and evidence for niche partitioning (Button et al. 2014, 2017). A temporal approach can also be taken, studying the evolution of function, perhaps coincident with the appearance of novel morphologies (Anderson et al. 2011; Peterson and Müller 2018), major transitions, rates of functional evolution (e.g. Piras et al. 2018) or environmental perturbations and extinction (e.g. Grossnickle and Newham 2016).

Fig. 3.1 Modified version of Witmer’s inverted pyramid of inference, demonstrating how inference of soft tissue, and then function from fossils can lead to downstream inferences of ecology and functional evolution. The pyramid also serves to illustrate how mistakes in soft tissue inference are magnified in larger-scale inferences. Modified from Witmer (1995)

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These pattern-based studies aid in reconstructing the functional landscape of feeding in vertebrates. To deduce process we need to explore the relationship between form and function further. What forms are possible dictates what mechanisms can be created from morphological characters, such as systems of bony levers and tendinous and muscular pulleys (Fig. 3.2). The nature of what controls form itself is a matter of some debate. Form, and morphological diversity, is subject to potential constraints: historical/phylogenetic (the genetic material available to the organism); developmental; physical/architectural (there are a finite number of constructions available to perform a particular function); material (only biological materials are available—bone, cartilage, enamel, muscle, etc.); and the need to perform multiple functions (feeding, respiration, housing the brain and sense organs, display, fighting, locomotion) (Alexander 1985; Gould and Lewontin 1979; Maynard Smith et al. 1985; Smith 1993). The study of form and function permits the assessment of the role of extrinsic factors such as adaptation by natural selection against such constraints (Mayr 1983; Smith 1993). On this basis, do form and function share a predictive relationship, and indeed, why should they? What about the role of drift, multiple adaptive peaks, exaptation (Gould and Lewontin 1979) and integration and modularity (Goswami et al. 2015) in controlling the relationship between form and function? Available mechanisms, in turn, dictate what functions are possible (Fig. 3.2). What functions are possible determines how well an organism performs a particular function, task or role. We may ask, is form optimally constructed to perform this particular task, and if not, why not? Is the relationship between form and function an exclusive relationship? Can different forms perform the same function (a many-toone relationship), or the same form perform many different functions (one-to-many)? Evidence suggests both scenarios can be realised (Lauder 1995; Wainwright 2007). Function can be quantified via performance metrics such as speed of movement (of a jaw, a limb, a whole organism), output forces (bite force, joint forces) or other

Fig. 3.2 The relationship between morphology and ecology. Line indicates the hierarchy from morphological form to ecology. Increasing complexity at the level of mechanism and function weakens the one-to-one relationship between morphology, function and ecology

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kinematic parameters (e.g. moment arms of lever systems) or mechanical parameters (bone stress and strain, susceptibility to fracture or failure). Performance controls how well the organism carries out a biological role (biting, running), which in turn links to its overall behaviour (carnivory, cursoriality, etc.). How well the organism performs influences the phenotype, which determines which variants (and therefore forms) will survive, contingent also on environmental conditions and chance. A major question that has been asked is how function promotes diversification, in studies of extant and extinct taxa (Alfaro et al. 2004, 2005)?

3.2 How to Study Function in the Fossil Record? One solution to the study of function in the fossil record is to assume that morphology is representative of function and ecology, so-called ecomorphology. Assuming morphology is a direct representative of function discards intermediate evidence of mechanism, function and performance that may be subject to variation (Fig. 3.2). As a result, morphology may not be a reliable predictor of function and ecology. Functional complexity of the component structural parts may play a key role in defining the correlation between form and function. For example, traits or structures with low functional complexity (number of moving elements, degrees of freedom of movement) are predicted to share a more exclusive relationship between form and function (Irschick et al. 2013). Increasing functional complexity may lead to a more complex relationship between form and function, and the breakdown of a direct, predictive relationship between form and function (and ecology) leading to one-to-many, or many-to-one mapping of form to function. In organisms where the structure–function relationship is complex (three or more component parts), it would be prudent to take a detailed approach to deducing soft tissue anatomy, kinematics, perhaps reconstructing morphology in an extinct organism, before using biomechanical methods to calculate metrics of function (Fig. 3.2). This approach is time-consuming, but considers morphology, mechanism and function before recording comparative performance metrics that dictate ecology (Fig. 3.2). These performance metrics are assumed to confer a fitness advantage to the individual—for example, faster speed, greater bite force or lower bone deformation or susceptibility to fracture are considered advantageous and by inference, subject to selection. It’s important to distinguish these performance metrics from the measurement of functionally relevant morphological traits. These traits, such as proximal versus distal limb proportions, body fineness ratios, tooth cusp angle, depression of jaw joint, are a step removed from the performance indicator and fitness characteristic they emulate (cursoriality/speed, drag, tooth pressure, jaw kinematics) (e.g. Maclaren et al 2017; Gignac and Erickson 2015). While the measurement of functional traits offers a means to capture larger amounts of data, it carries the assumption that the chosen metrics are representative of functional performance and confer a fitness benefit to the individual.

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In both circumstances, functional or performance metrics from extant and extinct animals may be used to explore variance in functional characteristics, within clades, overtime and across key events in vertebrate evolutionary history (e.g. Neenan et al. 2014). Using comparative phylogenetics, it is possible to explore the evolution of functional traits, observing the tempo and mode of functional trait evolution (e.g. Broeckhoven and du Plessis 2017). These pattern-based approaches have so far largely focused on assessing functional rather than performance trait metrics. Process-focused studies in the fossil record are less common. To better understand the pattern and process of functional evolution in the fossil record, we need to estimate function in extinct animals. How can we do this, and how reliable is this process? Other chapters in this volume consider in detail ways in which function can be measured and recorded in extant animals such as direct observations and recording: EMG to record muscle activity; force plates and transducers to record loading; gauges and interferometry to record bone strain; dissection (physical and digital) to record soft tissue anatomy; and static imaging technology (CT, MRI) and dynamic imaging technology (XROMM and fluoromicrometry). The reader is directed to Chaps. 2, 8–21 for further information. Of course, the problem with extinct animals is that they are dead, and their remains are decayed and mostly mineralised. Soft tissues are commonly absent, leaving only the hard parts (which may themselves be incomplete) remaining. Without soft tissues, the mechanistic pulleys that control skeletal levers are absent (Fig. 3.2). Furthermore, the petrifaction process renders the study of the material properties of the skeleton impossible. The fossilisation process, therefore, makes studying the historical context of form and function problematic (and notwithstanding bias in the fossil record itself, which lends further complexity to evolutionary influences of form and function (Benson and Butler 2011; Benton et al. 2011)). Witmer (1995) and Bryant and Russell (1992) approached the problem of missing data due to fossilisation and provided a parameterised approach to the inference of soft tissues in fossils. Osteological correlates—hard tissue features that indicate the attachment of muscles or tendons—are identified in living taxa that bracket the fossil of interest (the ‘extant phylogenetic bracket: EPB’). The presence of similar osteological correlates in extinct taxa, or the likelihood of such features appearing in fossil taxa given their occurrence in living bracketing taxa, is used to infer soft tissue structures in fossils. The approach is not without issue: apomorphies and synapomorphies are given lower confidence weighting than plesiomorphic characters, yet the EPB approach has introduced a level of rigour and repeatability to the study and reconstruction of soft tissue that has been expanded upon by subsequent authors (notably Holliday 2009; Holliday and Witmer 2007; Lautenschlager 2016). This testable approach provides hypotheses of muscle placement, lines of action and volume, but there are still outstanding questions concerning our ability to estimate tendon: muscle length ratios, the degree of muscle pennation, muscle fibre length and the neurogenic control of muscular tissues (Lauder 1995; Bates and Falkingham 2012, 2018).

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3.3 The Relationship Between Bone Shape and Function Given that fossilisation typically renders all but the hard tissues of the skeleton lost, what can the skeleton alone tell us about organismal function? During function, the skeleton experiences external forces such as those generated by muscle contraction, bite or joint force, or ground reaction force (Fig. 3.3). This leads to the skeleton experiencing stress (a load per unit area) and strain (stretch per unit length). Loads may deform the skeleton and in extreme cases lead to yield and eventually fracture. How the skeleton responds to external loads is dictated by skeletal material properties (Young’s modulus, mineralisation) and structural organisation (gross shape, cortical and trabecular microstructure, osteon orientation and structure). There is a general consensus that the internal and external shape of the skeleton, at least in some way, reflects the load it experiences during function (Carter and Beaupré 2001; Meakin et al. 2014), although the extent to which loading controls bone form is contentious (Bertram and Swartz 1991) and likely varies across the skeleton, with different functions, and has a phylogenetic component (Erickson et al. 2002; Currey 2003). Similarities between the trabecular orientation in the head of a human femur and the principal orientation of tensile and compressive stress trajectories in a curved beam under vertical load led Wolff (1892) to propose his famous ‘law of bone transformation’ (also known as the trajectorial theory), stating that a change in form and/or function of a bone leads to changes in internal architecture that reflect the external loading environment. Frost’s later ‘mechanostat’ model forms the foundation for our understanding of how bones respond to changes in loading (Frost 2003; Fig. 3.4). During normal, everyday function, bone sits within an ‘adaptive state’. This was previously termed the ‘lazy zone’, although evidence suggests that bone remodelling does still occur within this adaptive state (e.g. Sugiyama et al. 2012). When bone falls into disuse (change in behaviour, injury) bone stress and strain

Fig. 3.3 How external forces are accommodated within a bone. Understanding structural organisation and estimating stress and strain within a bone may indicate the types of external loads the bone can withstand, providing hypotheses of function. Modified from Thomason (1995)

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Fig. 3.4 Revised ‘mechanostat’ model. Modified from Frost (2003) to accommodate evidence for bone turnover and deposition in the adapted zone and to remove the so-called ‘lazy zone’ of the adapted state

magnitudes decrease, thereby triggering a remodelling response where excess bone tissue is removed and the strain signal returns to the adaptive state (Fig. 3.4). Should bone loading increase (recovery post-injury, adoption of a more intensive activity, a new loading regime), bone strain is increased. Bone tissue is deposited in response, thereby lowering bone stress and strain back to the adaptive state (Fig. 3.4). In vivo studies provide evidence for the ability of bones to remodel in response to changes in load. Such studies comprise exercise or immobilisation experiments (e.g. Woo et al 1981) or more invasive excision experiments where typically one of the two distal limb bones is excised, and the functional response to increased loading in the remaining limb quantified (e.g. Goodship et al. 1979) or non-invasive loading experiments (e.g. Gross et al. 2002). Bone is able to compensate by increasing surface area and mass but material properties are not altered; bone does not get stiffer when accommodating increased functional loads. For practical reasons, immobilisation studies are performed on the postcrania rather than the skull, although medical studies of the human temporomandibular jaw joint demonstrate pathologies when the joint is damaged or immobilised due to disease or injury (Betti et al. 2018; Sun 2010). Mechanical loads are also shown to be important for normal skeletal development. Mutant mouse and zebrafish strains lacking muscle and embryonic immobilisation experiments demonstrate that bone and joint formation is disrupted and gene expression modified, in the absence of muscular loads in zebrafish, chick and mouse models (Rolfe et al. 2013; Roddy et al. 2011; Nowlan et al. 2008) including in the chick skull (Hall and Herring 1990), zebrafish jaw (Brunt et al. 2015) and mouse

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mandible (Enomoto et al. 2014). How mechanical loads influence skeletal morphology during ontogeny is a matter of some debate. For example, Renaud and Auffray (2010) demonstrated that post-weaning mice fed on hard versus soft food diets develop differently shaped jaws, that function in different ways, with similar shape trajectories to island morphs that shift diets. Hard food eaters have more efficient jaws that are better resist bending and torsional loads (Anderson et al. 2014). Similar diet-manipulation experiments on rabbits and rats also demonstrate diet-induced plasticity in musculoskeletal anatomy, but with varying strength of correlation of morphological characteristics to feeding behaviour (Menegaz et al. 2010; Ravosa et al. 2015). For example, the mechanical advantage of the masseter correlates with diet in mice but does not in rabbits. The link between skeletal form and biological function is subject to the same general constraints mentioned above. How well bone can physically adapt to loading may be limited by extrinsic constraints. A classic example of the constraint acting on the gross skeletal morphology is the skull of extant crocodilians that experience the conflicting functional demands of hydrodynamic drag imposing a flattened, streamlined cranial morphology, versus the need in some taxa to exert high bite forces to take down large-bodied mammalian prey, thought to require more arch or domed shaped skulls to resist feeding-induced bending loads (Busbey 1995; McHenry et al. 2006; Rayfield et al. 2007; Rayfield and Milner 2008; Walmsley et al. 2013, McCurry et al. 2017) (Fig. 3.5).

3.4 Evolutionary Adaptation to Mechanical Loads Bone mechanical adaptation as a process is usually considered within the lifetime of an individual. However, there are multiple examples of bones, or assemblies of bones such as skulls, that are seemingly well adapted in terms of overall shape and microstructure, to the functions they perform. The crania of mammals provide an obvious example—the short deep faces of felids for carnivory, the tubular snouts of anteaters, deep faces and high-crowned teeth of hypsodont grazers, and so on. Some studies have suggested that the proportion of stiffer cortical bone to more compliant trabecular bone is also selected for in carnivorans (Chamoli and Wroe 2011). Suture morphology may be selected for to accommodate different strain regimes in the skull. Interdigitate sutures tightly bind bones together and the collagen fibres that span the sutural contact may resist tensile and compressive loads. Simpler sutures may indicate simple strain regimes: overlapping scarf sutures in regions of tension and butt-jointed sutures for resisting compression (Rafferty and Herring 1999). Other aspects of bone structure may also be subject to selection. Material properties may be an obvious property ripe for selection. From the limited data we have, bone material properties, whilst variable, appear not to be adapted to particular functions (Currey 2002; Erickson et al. 2002). The exceptions are highly modified bone tissue. Low calcium content makes antlerless stiff but very tough, while high calcium content makes the whale tympanic bone extremely stiff (Currey 2003). Yet carnivores do not

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Fig. 3.5 Constraints on crocodilian skull morphology. a, b Tall, domed, ‘oreinirostral’ skull morphology, common to ornithodiran archosaurs and terrestrial crocodylomorphs. c, d Broad flat ‘platyrostral’ skull morphology, common to many neosuchian crocodyliformes. Oreinirostral skulls are hypothesised to be better at resisting bending (bilateral biting) than platyrostral skulls of the same size. Hydrodynamic constraints may impact crocodilian skull morphology, resulting in a tradeoff between minimising drag and resisting feeding loads in platyrostral skulls, although broad, flat skulls may be more effective at resisting compression and axial torsion during aquatic rolling feeding behaviours, particularly by development of the secondary palate and loss of the antorbital fenestra (Busbey 1995; figure modified from Rayfield et al. 2007 indicating potential zone of weakness at hypothetical antorbital fenestra)

have stiffer bone than nectar feeders, and convergences in bone material properties for function are not seen, although broad phylogenetic sampling of material property data across vertebrate clades and across the vertebrate skeleton has not yet been performed. More comprehensive and phylogenetically targeted material property studies are required to understand selection (or lack of) in bone material properties. Another possible target of selection is response to the strain stimulus. According to the mechanostat model, bone should remodel when experiencing low strains. There are circumstances where it is advantageous to retain bone tissue at low strains, for example to act as bone ballast in near-shore marine animals. Likewise, tissue deposition at high strains may be counterproductive to the maintenance of a lightweight skeleton in flying taxa (see Skerry 2006). The classic study by Currey and Alexander (1985) demonstrated extremely thick cortices in manatees and exceptionally thin bones in pterosaurs, supporting the idea of selection to the strain stimulus, but again, this remains to be explored in a targeted phylogenetic manner.

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3.5 Methods to Deduce Stress and Strain Within the Skeleton: Finite Element Analysis Given the relationship between function and bone mechanics, deducing stress and strain within the skeleton offers a way to: (i) infer loads the skeleton can accommodate; (ii) determine the comparative performance of the skeleton; or, (iii) provide a way to test the relationship between form and function. Aim (i) assumes a relationship between form and function. Aim (iii) instead aims to test the relationship between form and function. Aim (ii) may take either standpoint depending on the question asked. Underpinning the aim to deduce stress and strain in skeletons of fossils is the understanding that while animals and the environments they inhabited may have changed, the bone remodelling response has not altered. Furthermore, the basic cellular and tissue level building blocks of life (osteoblasts, chondrocytes, bone, tendon, cartilage) remain unchanged, as do tissue material properties, as far as we can infer from studies on living relatives. Strain gauges are a useful although technically challenging way to record bone strain in vivo or ex vivo. Small resistive wires glued to the surface of bone emit a voltage change when bones strain. As most fossil bone is petrified or mechanically altered in some way, gauges are not an appropriate method to record strain in the bones of extinct animals. Bone strains can be calculated from simple analytical models, such as beam models, and this method has worked well in structures such as long bones with relatively simple geometry and orthotropic material properties (Biewener 2003). Where geometry and material properties become more complex such as in the skull, these simpler models are unable to capture spatial complexity. An alternative method is finite element analysis (FEA). FEA is a mathematical approach that computationally calculates the stress, strain and deformation response of a structure to applied loads, given its geometry and user-defined material properties. It achieves this by dividing the structure into a large number of interconnected elements, each with simple geometric properties that together comprise a composite, complex geometric structure.

3.5.1 Description of FEA A comprehensive review of FEA in vertebrate morphology including the history of the method in non-medical biological studies can be found in Rayfield (2007), Panagiotopoulou (2009) and Bright (2014). For this reason, a simple explanation is provided here. The first step in finite element analysis is to create a digital model of the structure of interest, with data captured via tomography, or less commonly (as internal features are not detailed) via surface scanning or photogrammetry. Digital models can also be created in CAD packages, and sometimes 2D models are used (e.g. Marcé-Nogué et al. 2017). The digital model is imported into mesh generation software, where the finite element mesh is created—a series of discrete 2D or 3D

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elements joined at their apices by nodal points (with nodes also along the edges in quadratic elements). Each element is assigned a value of Young’s modulus to reflect its stiffness. Material property values can vary in magnitude and orientation across the structure. Boundary conditions—loads and constraints—are then applied to the model. Boundary conditions may represent loads generated by a simulated function or behaviour, or a hypothetical or comparative loading regime. The analysis computes the displacement of each node in response to the applied boundary conditions, taking into account the geometry and material properties of the structure. Displacements are then converted to nodal and element strain and stress. A comprehensive reconstruction of stress and strain and deformation across the structure is therefore generated by an FE analysis. Outputs are typically displayed as numerical values of average or peak stress and strain or deformation, or values at selected elements or nodes, and/or as coloured contour maps of stress and strain across the structure. Reaction forces, such as joint loading or bite forces, can also be estimated.

3.5.2 What Can the Results of FEA Tell Us? Rayfield (2007) discusses the various approaches FEA can take: inductive versus deductive (what was the function of this feature, versus what can we deduce about performance or the relationship between form and function), and hypothesis-driven studies (for example, what happens when this feature is removed, or modified). Studies can be performed in an individual taxon, usually an inductive approach to determine function (Fig. 3.6a). Comparative studies of several specimens or taxa may determine the performance of the skeleton or a certain feature, through time, or across a phylogeny (Fig. 3.6b). This could be mechanical performance of a structure, or the effect of evolutionary modification of a feature (Fig. 3.6c). As models become quicker to construct and solve, and as we understand better what parameters we need to include in our models and what can be omitted, comparative FE analysis are becoming more commonplace. Such studies have the potential to assess deep time evolutionary questions of how skeletal mechanical performance may adapt to new environmental conditions, modify across mass extinction events, or across major morphological transitions. The relationship between form and function and diversity and disparity can also be explored, particularly when combining FE results with quantitative shape analysis such as geometric morphometrics (O’Higgins et al 2010; Polly et al. 2016). Such pattern-based approaches are hugely informative, but it may also be possible to use finite element approaches to infer hypotheses of process: such as the role of function in dictating realised and theoretical skeletal morphologies and ultimately, the role of mechanical loads in skeletal evolution.

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Fig. 3.6 Examples of finite element analysis studies. a Model of a single specimen (the ornithischian dinosaur Psittacosaurus) to determine skull function and in this case, the effect of different hypothesised muscle arrangements. b Comparative feeding performance of primate jaws across phylogeny. c Effect of introducing different hypothesised features—simulating the effect of introducing an antorbital fenestra in extant archosaurs. Modified from a Taylor et al. (2017); b Marcé-Nogué et al. (2017); c Rayfield and Milner (2008)

3.6 Using FEA to Compare Feeding Performance and Behaviour in Extinct Taxa Although FE models of extinct skulls still take substantial time and effort to generate, due to the frequent need for restoration of missing elements and some retrodeformation, along with potential difficulties digitally segmenting fossil from surrounding matrix, comparative studies of skull function in extant taxa using FEA are becoming more common. As a case study example, Button et al. (2014, 2016) compared the mechanical performance of the skulls of extinct sauropodomorph dinosaurs.

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Sauropodomorpha, and particularly the sub-clade Sauropoda, present an interesting palaeobiological problem. These herbivorous taxa are notable for achieving large multi-tonne body masses and would have been required to process large quantities of plant fodder daily. Although the gymnosperm flora that dominated for the majority of sauropodomorph existence may not have been as unnutritious as previously estimated (Gill et al. 2018), saurpodomorphs lacked sophisticated tooth–tooth occlusion or dental batteries to effectively process resistant plant matter (Barrett 2014). The Late Jurassic Morrison Formation of North America presents an additional challenge as evidence suggests it was a seasonally arid environment with limited primary productivity (Button et al. 2014 and references herein). Despite this, the Morrison contained at least 10 multi-tonne sauropod dinosaur taxa, along with other herbivorous ornithischian dinosaurs and carnivorous theropod taxa. Previous studies had suggested that Morrison sauropods partitioned niches on the basis of differences in feeding ecology (Upchurch and Barrett 2000). Two of the most commonly found taxa have a noticeable different skull or tooth morphologies. Camarasaurus has a relatively short, tall skull with broad-crowned teeth whereas Diplodocus has an elongate skull with procumbent narrow-crowned teeth found in the anterior tooth row only (Chure et al. 2010). In deducing differences in feeding mechanics between these taxa, Button et al. (2014) used the extant phylogenetic bracket approach of Witmer (1995) to infer adductor muscle origination and insertion points on the skull and mandible, respectively (Fig. 3.7a). The adductor muscles were then digitally ‘fleshed out’ to create 3D muscle bodies. Physiological cross-sectional area (PCSA) was calculated by dividing the muscle volumes by muscle length, the latter being a proxy for muscle fibre length. PCSA multiplied by standard muscle stress generates a value for muscle force. Here assumptions must be made about muscle architecture—muscle anatomy and volumes, but also fibre lengths (which can impact notably on muscle force estimates; Bates and Falkingham 2018) and muscle stress. Many FE studies use a value of muscle stress of 0.3 Nmm−2 , taken from Thomason (1991) although how vertebrate muscle stress varies with function and phylogeny is little explored. The digital scan datasets were then used to create a finite element mesh of 3D tetrahedral elements. These finite elements are a discrete approximation of the continuum structure of the skull, so the finer the mesh, the better the elements approximate the continuum. Creating a mesh that is too coarse risks generating inaccurate results, as the resolution of the mesh is not sufficient to accurately capture the mechanical behaviour of the structure. Element size therefore should be reduced. However, at some point, further decreases in element size and mesh refinement will not alter model results. There is no rationale for further decreasing element size beyond this point, as computational processing power increases for no material gain. The process of determining optimal mesh size is known as convergence testing (Bright and Rayfield 2011) and should be a standard step in FE model creation. The FE model is then given material properties to reflect the stiffness/elasticity of the skeleton and teeth. In the case of the sauropod models, properties of extant vertebrate enamel, dentine and bone were applied to the teeth.

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Fig. 3.7 Using finite element models to determine niche partitioning in sauropod dinosaurs. Digital adductor muscle reconstruction in a Camarasaurus lentus; d Diplodocus carnegii. Finite element mesh and finite element analysis results in b, c Camarasaurus lentus; e, f Diplodocus carnegii, respectively. Units  MPa, megapascals; metric  von Mises stress. a, c, d, f Modified from Button et al. (2014)

Estimated muscle forces are then applied to the model at the location of muscle origination and insertion in the orientation of the estimated line of muscle action. Additional boundary conditions, to anchor the structure from moving are also applied. The sauropod models were fixed from translational movement in all three degrees of freedom at the quadrates to mimic the stabilising effect of the jaw joint. Fixing the biting teeth from movement simulates the impact of the tooth into a non-compliant foodstuff and allows the calculation of reaction forces at the tooth, which is used as a proxy for bite force. Running simulations of sauropod feeding—all muscles contracting, the animal biting at the front or rear of the tooth row—generates comparative patterns of stress and strain within the skull (Fig. 3.7). The results of the sauropod comparative study suggested a greater adductor muscle mass in the Camarasaurus skull, with the ability to generate greater bite forces. Scaling the Camarasaurus and Diplodocus skulls to the same surface area, Camarasaurus still exhibits a lower bony stress than Diplodocus, and by inference has a stronger skull—meaning it can withstand greater loads than Diplodocus before failure. These results suggest the potential for niche partitioning, and also corroborate data on differences in tooth isotope analysis (Tütken 2011), tooth microwear, enamel thickness and tooth replacement rate (D’Emic et al. 2013) and multivariate analysis of functionally relevant morphological characters (Button et al. 2014), that all suggest differences in feeding performance and behaviour and support the niche partitioning hypothesis.

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3.7 Limitations of This Approach There is potential for FEA to elucidate and address questions of morphological and mechanical evolution of the skeleton. The success of this enterprise depends on the ability of FEA to reliably determine aspects of function and performance and the appropriateness of the question being addressed of the data to hand. Validation studies (how accurately does the model represent reality) and sensitivity analysis (how does variation in model parameters impact model output) are two ways to address the utility of an FE model in deducing skeletal function. The usefulness of the model to address the question to hand is a different issue that must be considered by the researcher. Validation studies determine how accurately FE models represent the stress and strain environment of a structure experiencing a particular load. Typically, these studies are performed in vivo or ex vivo, usually by attaching gauges to the bone surface and recording strain while the animal performs a function, or a cadaver is loaded with external forces (Kupczik et al. 2007; Toro-Ibacache et al. 2016). Strain gauges only record strain at the point of attachment to the bone surface. More recently, digital speckle pattern interferometry (DSPI) has been employed to record whole surface strains, although this is currently restricted to ex vivo studies where a large (20–30 mm diameter) bone surface can be exposed (Groning et al. 2009, 2012; Bright and Groning 2011). Many studies have focused on the macaque cranium and/or mandible, where in vivo bone strains and bite forces are known from multiple experimental trails (Daegling and Hylander 2000; Ross et al. 2005; Strait et al. 2005) and material properties of the jaw have been characterised (Strait et al. 2005). The American alligator is also a useful non-mammalian validation case study (Porro et al. 2013) and the ostrich jaw has also been studied (Rayfield 2011; Cuff et al. 2015). Overall, validation studies have shown, perhaps unsurprisingly, that the more accurate the input parameters (geometry, bone material properties, muscle loads), the more accurately the FE model can reproduce experimentally derived strain (Ross et al. 2005; Strait et al. 2005; Fitton et al. 2012, 2015; Toro-Ibacache and O’Higgins 2016). Most FE models, even those with simple material properties, can reproduce strain patterns and modes of deformation recorded in experimental studies (see Stansfield et al. 2018 for a recent review). Some of the macaque jaw validation studies have found close congruence between in vivo or ex vivo and in silico strain magnitudes (e.g. Panagiotopoulou et al 2017). Studies on other taxa, particularly non-mammalian vertebrates, have shown that sutures exert an influence on the ability of model data to reproduce experimental strain (Curtis et al. 2013; Bright 2012; Reed et al. 2011; Wang et al. 2010). The lack of sutures in the mammalian mandible (comprising the singular dentary bone) avoids such problems, although there is debate over the role of the periodontal ligament in dissipating jaw strain (Gröning et al. 2011; Wood et al. 2011). Sensitivity analysis informs on which of the input parameters may be responsible for (a) the mismatch of experimental strain and in silico strains; or (b), in a model without reference to experimental data, which model parameters influence model

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outputs (stress, strain and deformation) most strongly. These may be input parameters chosen via assumptions on musculoskeletal anatomy and function, or variation due to human error (Table 3.1). Most sensitivity analysis studies focus on variation in input parameters in a single specimen and therefore consider sources of error and variability relative to each other. The use of geometric morphometrics to record shape variation in the loaded and deformed skull has proven to be a useful tool in comparing the results of comparative models in sensitivity analysis studies (O’Higgins et al. 2010; Polly et al. 2016). Bone stiffness (Young’s modulus) values exert a notable influence on FE model results (Strait et al. 2005; Cox et al. 2011), greater than bite position or bite angle and muscle orientation in the skulls of rodent crania (Cox et al. 2011). Bite position influences model results more than material properties in the skull and mandible of the ornithischian dinosaur Psittacosaurus (Taylor et al. 2017), yet material properties are almost as important. It is expected that different bite positions generate different patterns of stress and strain in the skull, and indeed documenting these differences may be an important aim. More pertinent to model reliability is how much unknown or assumed input parameters or sources of human error, influence model results. Variation in most input parameters will influence model behaviour to some degree. A key issue is whether this variation matters to the question asked. It is useful therefore in validation and sensitivity studies to consider: (a) whether input parameters or human error can be modulated in some way (‘Solutions’ in Table 3.1); and (b) what kind of model output data are required to address the question asked of the model. For the latter point, it may be helpful to consider a hierarchy of congruence between either model and

Table 3.1 Potential sources of error or assumptions in finite element models of skulls. Potential solutions are posed, in addition to a recommendation to perform sensitivity analysis to determine the scale of the error or assumption on model results where possible. EPB  extant phylogenetic bracket; MDA  multibody dynamics analysis Error or assumption

Influence

Potential effect on FE model outputs

Solution?

CT scan resolution (machine)

Lower resolution scans (CT, surface scans) may not sufficiently capture geometry

Inaccurate mode and/or magnitude of stress, strain or deformation

Generate higher resolution scans, or up-sample scan dataset

Segmentation error (human)

Some geometries not captured (thin bones), or other regions overemphasised

Inaccurate mode and/or magnitude of stress, strain or deformation

Manual segmentation of complex geometries; perform sensitivity study

Muscle location (error, assumption)

Places boundary conditions (simulated loads) at incorrect location

Inaccurate mode and/or magnitude of stress, strain or deformation

EPB approach; dissection of taxon or related taxa; perform sensitivity study (continued)

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Table 3.1 (continued) Error or assumption

Influence

Potential effect on FE model outputs

Solution?

Muscle size (error, assumption)

Larger or smaller muscles assumed or created in 3D

Muscle forces are exaggerated or underestimated—inaccurate magnitude of stress, strain or deformation

EPB approach; dissection of taxon or related taxa; simulation of muscle action via MDA; perform sensitivity study

Muscle line of action (error, assumption)

Incorrect placement of muscle forces

Muscle moments are exaggerated or under-estimated; Inaccurate mode but more likely magnitude of stress, strain or deformation

EPB approach; dissection of taxon or related taxa; perform sensitivity study

Muscle pennation (assumption)

Muscle incorrectly assumed to be parallel fibred; pennation not considered

Underestimation of muscle force as pennation increases PCSA of muscle body—underestimation of magnitude of stress, strain or deformation

EPB approach; dissection of taxon or related taxa; simulation of muscle action via MDA; perform sensitivity study

Muscle fibre length (assumption)

Muscle fibre length assumed  total muscle length

Underestimation of muscle force; fibres most likely shorter than total muscle body length—underestimation of magnitude of stress, strain or deformation

EPB approach; dissection of taxon or related taxa; simulation of muscle action via MDA

Convergence test absent (error)

Too coarse mesh resolution

Cannot approximate continuum condition and generates inaccurate results

Perform convergence test

Material property values (assumption)

Bone or other tissues assigned values that are too elastic or too stiff

Model returns inaccurately high or low strain magnitudes

Perform material property testing on taxon of interest or related taxa; perform sensitivity test (continued)

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Table 3.1 (continued) Error or assumption

Influence

Potential effect on FE model outputs

Solution?

Material property heterogeneity (assumption)

Variation in material properties across the skeleton is not accounted for

Inaccurate mode and/or magnitude of stress, strain or deformation

Perform material property testing on taxon of interest or related taxa; perform sensitivity test

Material property anisotropy (assumption)

Variation in orientation of material property stiffness is not accounted for

Inaccurate mode and/or magnitude of stress, strain or deformation

Perform material property testing on taxon of interest or related taxa; perform sensitivity test

Inaccurate boundary conditions

Model is constrained from movement at incorrect location or by incorrect degrees of freedom or inaccurate node choice

Inaccurate mode and/or magnitude of stress, strain or deformation

Consideration of kinematics of simulated behaviour; perform sensitivity test

Sutures

Model is lacking sutures or sutures are inappropriately modelled (relatively too thick, too thin, incorrect sutural junction properties)

Inaccurate mode and/or magnitude of stress, strain or deformation

In vivo/ex vivo studies to determine role of sutures in dissipating loading-induced strain; perform sensitivity test

Kinesis

Flexibly or actively mobile joints in the skull are not sufficiently characterised

Erroneous assimilation of stress and strain at joint location—inaccurate mode and magnitude of stress, strain and deformation

Simulation of joint, validated by comparison to mobility of joint in in vivo or ex vivo manipulation studies; perform sensitivity test

experimental data, or between models with different input parameters (Table 3.2). If the aim of the analysis is to record and compare strain magnitude data, and sensitivity analysis shows that variation in assumed input parameters influences strain magnitudes, then the model is not sufficiently constructed to answer the question, unless further validation study can refine model accuracy. On the contrary, if the hypothesis to be tested is whether skulls show similar modes of deformation between specimens (for example, do skulls bend in a similar manner) or test if patterns of stress or strain are similar, or to test the effect of introducing or removing features, and sensitivity

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Table 3.2 Is the FE model capable of producing data of sufficient accuracy to address the question? Hierarchy of congruence between model and experimental data, or when comparing models during sensitivity analysis. P1  principal stress or strain 1, typically tension; P3  principal stress or strain 3, typically compression Desired result

How determined

Metrics?

Computing and comparing stress, strain or deformation magnitudes

Maximum, averages, or specific location measurements of stress, strain or deformation; congruence between different models determined by user or experimentally (i.e. results of different models within 5% considered congruent)

Peak, mean, median, 95% mean, 95% median stress, strain (usually von Mises, P1 or P3) or deformation metric; correlation between stress or strain trajectories; variance between deformed models assessed via GMM and PCA

Reaction force magnitudes

Reaction force at constrained nodes, often simulating bite point or joint location

Recording of nodal values; statistical comparison

Stress, strain or deformation mode (quantitative)

Location of chosen nodes in loaded versus unloaded model; quantification of strain vectors

Variance between deformed models assessed via GMM and PCA; rose diagram or other comparison of strain vector orientation

Stress, strain or deformation mode (qualitative)

Visual assessment of patterns of stress, strain or deformation

Stress or strain (von Mises, P1, P3) or deformation patterns on model surface, on or within-model features (specific bones, cross section of ROI)

analysis shows that varying input parameters does not influence mode of deformation in a test case model, then the models are sufficient to address the question at hand. Performing sensitivity analysis on more than one specimen is important if we want to address whether potential sources of model variation are sufficiently large to obscure differences in mechanical function between different specimens. Few studies have yet to do this, probably due to the time-consuming nature of creating multiple FE models. Those studies that have achieved this aim have shown that the influence of model input parameters is not greater than the variation in mechanical function between mandible specimens, in this case of the same species, Homo sapiens (Stansfield et al. 2018).

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3.8 Perspectives There is still scope for further enquiry into how within-model variation due to input parameter assumptions relates to between model variation, either between different specimens of the same species, or specimens from different species. Performing these studies on a broad phylogenetic sample will also address if different clades are susceptible to different issues and biases in input parameter assessment. For example, clades with typically thin or flexible bone, such as extant birds, may be sensitive to material property variations and segmentation error, whereas clades with typically more robust skulls, the crania of crocodilians, or the mandibles of mammals, these issues may be less of a concern. There is much still to understand about the anatomical and phylogenetic basis of vertebrate cranial musculoskeletal anatomy (see Ginot et al. 2018, for example), and hence model input parameters in the case of feeding simulations. Is there a phylogenetic or functional signal in muscle stress, muscle pennation or muscle fibre length, for example? Likewise, phylogenetic and functional controls on material properties are unclear, due to current paucity of data exploring possible evolutionary or functional trends. The use of muscle simulations via MDA have potential to inform on most likely loading conditions to apply to FE models (Koolstra and van Eijden 2005; Curtis 2011) and assist in determining the interplay between muscle loads and kinetic movement in the skull (Jones et al. 2017), important when attempting to model a dynamic system with a static loading model. A combination of better understanding of input parameters and sensitivity analysis to understand how these parameters impact model outputs are key to uncovering the full potential of FEA on determining the diversity and disparity of skull mechanical function across the vertebrate fossil record. Process-based studies can also be realised—such as determining on evolutionary timescales how mechanical loads influence skeletal form, and the relationship between form and function, and the ability of functional adaptation to promote diversification. Other important factors that are worthy of consideration are whether the functional and mechanical metrics recorded via FEA are important for organismal fitness. How well a beak resists feeding-induced loads is important for birds that process seeds and other hard foodstuffs (Soons et al. 2015), yet factors other than resistance to feeding-induced loads may be selected for taxa that feed on insects (gape, speed of jaw closure), or nectar (elongation, curvature of the beak), or use their beaks in different ways during food procurement (skimming, probing etc., rather than biting). Many studies have considered the impact of bias in the fossil record on our understanding of taxonomic diversity through time (Benson and Butler 2011; Benton et al. 2011). If species and morphological diversity are biased, then it is logical to assume that the diversity of functions presented in the fossil record is also a biased sample of the true range of functional diversity in deep time. Few, if any studies have attempted to compensate for such bias. Finally, the outputs of finite element studies should not be considered in isolation. Many other techniques and methods are available to deduce function in the cranium,

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and to provide evidence of feeding or other types of behavioural ecology. For example, studies of trabecular orientation or compact to cancellous bone ratios, resistance to bending and torsion via beam theory, calculation of muscle moment arms and mechanical advantage are methods that can be recruited to test functional hypotheses, alongside FEA. Furthermore, studies of tooth microwear (Gill et al. 2014), or bone isotopic analysis (Angst et al. 2014) also provide additional lines of evidence that may support or refute functional hypotheses tested with or derived from finite element models. FEA is but one tool in the functional morphologist and biomechanists toolbox, but when applied to appropriate questions, can be a powerful means to recreate the mechanical function of the extant and extinct skeleton.

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Chapter 4

Food Capture in Vertebrates: A Complex Integrative Performance of the Cranial and Postcranial Systems Stéphane J. Montuelle and Emily A. Kane

Abstract Prey-capture behavior is unique because in many vertebrates, it requires the coordination between cranial and postcranial functional systems, which are traditionally defined by their separate contributions to feeding and locomotor performance, respectively. Such coordination is referred to as functional integration. First, this chapter reviews the current state of knowledge regarding cranial–postcranial integration during prey-capture behavior in aquatic and terrestrial environments, including quantitative data demonstrating cranial–postcranial coordination unequivocally, and promising qualitative observations and reports that remain to be tested explicitly. The evidence for cranial–postcranial coordination during prey capture in vertebrates are presented to show that (1) integration is an important biological phenomenon occurring across environments and (2) differences in integration can be hypothesized across and within clades. Second, the perspectives for investigating cranial–postcranial integration and its variability within and across vertebrate clades are discussed to assess the role of cranial–postcranial integration in the evolution of feeding. In particular, future research on food capture is suggested to focus on the flexibility of coordination patterns in response to food properties, as well as the sensorimotor control of cranial–postcranial coordination. The goal of this chapter is to inspire and promote future research on integration in order to extend the concept of food capture, and feeding behavior in general, beyond the cranial system in a more holistic approach to function.

S. J. Montuelle (B) Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, 4180 Warrensville Center Road, SPS349, Warrensville Heights, OH 44122, USA e-mail: [email protected] E. A. Kane Georgia Southern University, 8042-1, Statesboro, GA 30460, USA e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_4

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4.1 Introduction Feeding is traditionally defined as the behavior during which an organism transforms food resources into the energy and nutrients necessary for its body to operate, so that it can survive and reproduce successfully. Such behavior is not as simple as it encompasses a variety of performances and functions from different anatomical systems. Feeding involves searching for, approaching, capturing, processing, and assimilating the food item, and as such, in the context of this chapter, feeding will be described as a series of behaviors (Fig. 4.1). Each behavioral phase requires different levels of coordination between the cranial systems (such as the sensory organs and the feeding structures themselves; i.e., skull, jaws, and hyolingual apparatus) and the postcranial systems (such as the elements of the locomotor system; i.e., axial skeleton, limbs). The first phase of feeding is searching during which organisms detect potential food items. During searching, sensory organs collect cues to identify and locate food while the postcranial system generates the locomotor performance allowing for the reduction of the distance between the organism and the food item. The searching phase ends when the organism has found suitable food resources. Once located, the food item that is targeted may not yet be reachable. Thus, following the searching phase, the second phase of feeding can be referred to as the approach phase. The approach is based on the locomotor performance that enables the predator to position itself at the distance where it can reach or establish contact with the food item (e.g., Ford et al. 2005). The searching and approach may be absent in organisms that wait for their prey to become within reach. Once at reaching distance, the food capture phase begins during which organisms use a variety of anatomical structures to establish contact with the food item for the first time (thereafter referred to as the prehensile structures). Usually, the prehensile structure is a part of the cranial system like the tongue or the jaws, but some organisms are also capable of using postcranial elements such as the autopods of the anterior and posterior limbs in the case of primates and birds, respectively. However, food capture is not limited to prehension only. Not only does food capture require contact between an organism and the food item that is targeted, but prey items can also attempt to escape, or may have defense mechanisms such as spines that can be employed facultatively. Therefore, the predators require continual maneuvering to position themselves and the prehensile structure(s) at the precise time and location that will ensure the success of food capture (Kane and Higham 2014). Accordingly, food capture can be supported by the actions of the rest of the body, especially those of the locomotor system (e.g., axial skeleton and limbs), and by the sensory organs that continually collect physical, positional, and behavioral cues from the food item. Once contact between food and organism is established, the food processing phase starts, if present. During this phase, food is transported through the oral cavity where its properties are altered until the bolus reaches swallowability. This is typically achieved by the actions of the cranial elements such as the jaws, the teeth, and the hyolingual apparatus. The food processing phase also involves the continuous monitoring of food properties by numerous sensory organs and is

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Fig. 4.1 Feeding behavior as a sequence of behavioral phases. Each phase relies on a variety of performances and functions from different anatomical systems. Within this series, food capture is unique because, in many vertebrates, it requires the coordination of movements between cranial and postcranial structures to ensure the successful contact between an organism and the food resources that are targeted

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thus based on complex sensorimotor integration as the feeding movements must constantly respond and adjust to changes in food properties. Once food physical attributes (e.g., size, texture) matches the capabilities of the digestive system, the food is swallowed (i.e., transferred to the digestive tract) and digestion starts. Note however that the food processing phase may be very limited if not totally absent in organisms that swallow their prey whole. Digestion is the last phase of feeding behavior during which the different organs of the digestive tract (e.g., esophagus, stomach, intestine, etc.) allow for the extraction of nutrients and energy. In this context, this chapter will focus on the food capture phase because the success of the whole feeding behavioral series depends on the initial success of food capture. Specifically, before food can be processed and nutrient extracted, the food needs to be located and captured. The function of the prehensile structure is obviously critical to capture behavior, but the role of the rest of the body cannot be ignored. Covering the distance that separates an organism from its food resources is a key aspect of feeding behavior (Huey and Pianka 1981; Webb 1984b) and many organisms are characterized by anatomical structures or behaviors that help to reach food resources. For example, the extensibility of the hyolingual apparatus of various lizards and anurans allows them to project their tongue outside of the oral cavity to cover the distance between the animal and its prey, then retracting it to bring the prey in the oral cavity (Gans and Gorniak 1982; Wainwright et al. 1991; Ritter and Nishikawa 1995; Larsen et al. 1996; Nishikawa and Gans 1996; Herrel et al. 2001; de Groot and van Leeuwen 2004; Meyers et al. 2004; Anderson 2016). Primates use the extensibility of their forelimbs and the dexterity of their fingers to reach, grasp, and bring food items to their mouth, and therefore the prey capture is solely achieved through postcranial movements. Consequently, cranial–postcranial integration can be understood to be absent from hand prehension; and therefore will not be discussed in the context of this chapter. In contrast, many aquatic vertebrates feeding underwater are able to generate a suction flow in front of their mouth that traps the prey item and draws it inside the oral cavity (e.g., Muller and Osse 1984; Westneat 2006; Wainwright et al. 2007; Marshall et al. 2008, 2015; Van Wassenbergh and Aerts 2009; Hocking et al. 2013; Day et al. 2015). However, these mechanisms are only useful and efficient as long as the food item is in reaching distance of the prehensile structures (i.e., at relatively close range). Instead, to cover longer distances, or for organisms that can’t utilize these structures, many vertebrates have to move the cranial system toward the food item in order to capture it. This distance is usually covered by locomotor performance and/or behavior of the postcranial system. Without the contributions of the postcranial system, the food resources may not be reached and thus may not be taken to the oral cavity to be processed (Drost 1987; Kane and Higham 2014). Although locomotor and feeding systems can act independently (as in the searching or the processing phase), their coordinated use during food capture suggests an interdependency, or integration, of the two behaviors during this specific phase. Elements are integrated when their respective movements are coordinated in time and magnitude, which can be assessed by testing the correlation between kinematic variables (Higham 2007b; Wainwright et al. 2008; Kane and Higham 2015).

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Coordination of movements can stem from mechanical linkages or similarity in control or regulatory patterns (Wainwright et al. 2008), but in the case of integration during food capture, it is likely the result of a codependence that is necessary for achieving a common goal (Higham 2007b). The role of the postcranial elements during food capture has been demonstrated by showing that the positioning of cranial elements is actively supported by the actions of postcranial elements in a variety of aquatic and terrestrial organisms (e.g., Webb and Skadsen 1980; Rand and Lauder 1981; Geerlink 1987; Gerstner 1999; Van Der Leeuw et al. 2001; Hörster et al. 2002; Drucker and Lauder 2003; Montuelle et al. 2008, 2009, 2010, 2012a, b). However, cranial and postcranial movements during food capture are not merely added to one another, but rather are coordinated in time and space (e.g., Young et al. 2001; Higham et al. 2005; Higham 2007a; Holzman et al. 2007; Rice 2008; Rice and Westneat 2005; Rice et al. 2008; Kane and Marshall 2009; Montuelle et al. 2009, 2010, 2012a, b; Kane and Higham 2011). Because of this coordination, it is likely that integrated performance traits comprise a trade-off that must be mitigated (Ghalambor et al. 2003; Walker 2007, 2010; Irschick et al. 2008). For example, fishes cannot simultaneously optimize swim speed and the use of suction during prey capture (Higham et al. 2006), and neither measure of system-level performance adequately describes the emergent level of performance when both systems act together (Kane and Higham 2015). This is a unique type of coordination that is dynamic and can respond to the physical, positional, and behavioral attributes of the food item that is targeted. Because food capture behavior is at its core a complex interaction between an organism and its environment, investigating the role and contribution of cranial–postcranial integration during food capture can improve our understanding of predator–prey interactions. Therefore, integration across system-level performance measures could be used as a more holistic and ecologically relevant measure that encompasses the interrelationships and trade-offs present across systems. Our objective is to present and discuss recent research that highlights the fact that food capture is not restricted to the movements of cranial structures (e.g., the jaws, the hyolingual apparatus), but also includes the coordinated movements of postcranial structures such as the vertebral axis, limbs, or fins. This chapter will show that food capture behavior is based on a whole-body performance that integrates cranial and postcranial elements in a variety of aquatic, terrestrial, and aerial vertebrate organisms. To date, feeding behavior, and food capture, in particular, is too often considered in the vacuum of describing, comparing, and discussing cranial performance and morphology. This chapter aims to extend the concept of food capture to include reporting the role and the contribution of postcranial elements during food capture. This will promote a more integrative and organismal perspective for future research on feeding behavior and predator–prey interactions.

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4.2 Review: Evidence for Cranial–Postcranial Integration 4.2.1 Aquatic Food Capture Fishes are the archetypal aquatic vertebrate, having evolved in this media for over 400 million years and are the group from which all other vertebrate classes arose, making them a model system for understanding aquatic prey-capture mechanisms (Wainwright and Richard 1995; Ferry-Graham and Lauder 2001; Grubich 2001; Holzman et al. 2012; Day et al. 2015). In addition, several terrestrial vertebrate lineages are able to permanently or temporarily exploit aquatic environments to find food resources. These organisms often acquired second-derived anatomical and functional attributes enabling them to feed under water. The return to a full- or semiaquatic life mode from terrestrial ancestors can be observed in all classes of tetrapods: Mammalia (e.g., whales, dolphins, walrus, seals, sea lions, otters), Amphibia (e.g., salamanders, frogs), Reptilia (e.g., crocodiles), Aves (e.g., seabirds), and all of these lineages share the challenge of acquiring food in a dense and viscous media and prey capture is often highly convergent with fishes. Aquatic food capture can be classified into three modes: ram feeding, suction feeding, and biting (Ferry et al. 2015). These modes differ based on how water and prey move relative to the mouth cavity (Liem 1980; Ferry et al. 2015; Kane and Higham 2015). Modes like suction are considered specialized, requiring conserved morphological and kinematic traits (Jacobs and Holzman 2018), while others like biting may be more generalized and can be utilized in a variety of circumstances (Mehta and Wainwright 2007a). Ram feeding refers to a reliance on swimming to overtake the prey and is synonymous with use of the postcranial system. Therefore, ram is the only mode that can be performed in isolation of other modes, whereas suction and biting are often combined with ram to generate forward body movement to close large distances from prey (Ferry et al. 2015). Despite these differences in capture modes, the characteristics inherent to a fish’s ability to propel itself in the water can have direct consequences for food capture independent of what mode is used. Body shape is a characteristic typically thought of as having a direct relationship with swimming performance because of its relationship with friction drag (Webb 1984b, c). However, during food capture, this parameter is important for allowing water to flow smoothly into the predator’s mouth with little resistance (i.e., minimize pressure drag). Once the mouth begins to open, during any feeding mode, body shape and mouth size both play a role in defining the streamline that separates water flowing around the predator from water entering the predator’s mouth (Muller et al. 1982; Muller and Osse 1984). These hydrodynamic interactions at the cranial region of a predator can also result in the generation of a bow wave ahead of the predator that can be detected by their prey (Stewart et al. 2014). In addition to these external hydrodynamic forces that must be mitigated, body shape is also a product of internal physiological demands. The lateral epaxial and hypaxial muscles are responsible for generating force to power movement and the geometry of these muscles affects their performance during swimming (Altringham et al. 1993;

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Wakeling and Johnston 1998). These same muscles power acceleration of the body toward prey (Johnston et al. 1995; Schriefer and Hale 2004) but also power burst movements of the head and jaws during suction feeding (Camp and Brainerd 2014, 2015; Camp et al. 2015, 2018). This overlap in function means that coordinated timing of acceleration of the body and expansion of the head is necessary to prevent suboptimal muscle contraction during one or both behaviors. This may be facilitated through functional regionalization of the muscles, so that the caudal region powers acceleration while the anterior region powers feeding (Schriefer and Hale 2004). In these ways, postcranial morphology contributes to aquatic food capture by influencing physical and functional features that have direct consequences for the ability to utilize the feeding system. In addition to its morphology, postcranial performance also has consequences for the ability to capture food, but in this case, the consequences may differ as a result of differences between feeding modes.

4.2.1.1

Ram Feeding

Ram feeding is perhaps the most basic aquatic-feeding mode as it is the only mode that can be performed in the absence of other modes (Ferry et al. 2015). The term “ram” is synonymous with swimming and refers to behaviors that close predator–prey distance by actively moving the predator toward the food item. These behaviors can be classified as slow-velocity pursuit, high-velocity pursuit, and high-acceleration lunge. In all cases, food capture involves overrunning or grabbing the prey whole within the jaws.

Slow-Velocity Pursuit Slow-velocity pursuit requires that prey are not able to actively evade the predator at a speed greater than the predator’s approach. For this reason, this type of ram behavior will be most effective for small or planktonic prey in combination with filter or suspension feeding. Many aquatic vertebrates that filter prey typically use continuous, slow-velocity movement where the mouth is held open while they swim steadily through the prey items. This feeding mode is exemplified by bony fishes such as paddlefish, anchovy, and herrings such as menhaden (Rosen and Hales 1981; Friedland et al. 1984; James and Probyn 1989), cartilatinous fishes such as basking and whale sharks (Sims 2000; Taylor 2007), and cetaceans (Table 4.1). Whithin the mouth, the prey are then filtered using structures such as gill rakers or baleen to separate them from the surrounding, outflowing water (Motta et al. 2010; Paig-Tran et al. 2013; Werth and Potvin 2016). In this case, the filtering structures are the functional prehension mechanisms, and not the jaws. In secondary aquatic mammals such as right and bowhead whales that lack gill openings allow a continuous unidirectional flow of water out of the mouth cavity, anatomical adaptations such as a grooved channel and posterior opening allow unidirectional flow in and out of the mouth to facilitate continuous forward movement (Werth and Potvin 2016).

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Table 4.1 Summary of the secondarily aquatic mammalian taxa for which prey capture under water is documented to include significant postcranial movements during suction feeding, ram feeding and/or biting CLADE and TAXA

Common name

References

Ram

Suction

Biting

Walrus

Kastelein and Mosterd (1989); Kastelein et al. (1994, 1997); Born et al. (2003)

X

Arctocephalus pusillus doriferus

Australian fur seals

Hocking et al. (2014); Volpov et al. (2015)

X

Callorhinus ursinus

Northern fur seals

Marshall et al. (2015)

Eumetopias jubatus

Steller sea lions

Skinner et al. (2009); Viviant et al. (2010); Marshall et al. (2015)

Cystophora cristata

Hooded seals

Suzuki et al. (2009)

Erignathus barbatus

Bearded seals

Marshall et al. (2008)

Hydrurga leptonyx

Leopard seals

Edwards et al. (2010); Hocking et al. (2013)

Leptonychotes weddellii

Wedell seals

Davis et al. (1999); Sato et al. (2002); Watanabe et al. (2003)

Lobodon carcinophaga

Crabeater seals

Klages and Cockcroft (1990)

X

Phoca vitulina

Harbor seals

Bowen et al. (2002); Marshall et al. (2014)

X

X

Delphinapterus leucas

Belugas

Kane and Marshall (2009)

X

X

Eschrichtius robustus

Gray whales

Woodward et al. (2006); Johnston and Berta (2011)

ARCTOIDEA Odobenus rosmarus

Otariidae X

X NR

X

X

Phocidae X X NR

X

X

CETACEA

SVP

X

(continued)

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Table 4.1 (continued) CLADE and TAXA

Common name

References

Ram

Kogia sp.

Pygmy sperm whales

Bloodworth and Marshall (2005, 2007)

Balaena mysticetus

Bowhead whales

Simon et al. (2009); Werth and Potvin (2016)

SVP

Eubalaena glacialis

Right whales

Woodward et al. (2006)

SVP

Balaenoptera musculus

Blue whales

Nowacek et al. (2001); Woodward et al. (2006); Cade et al. (2016)

SVP, HAL

Megaptera novaeangliae

Humpback whales

Woodward et al. (2006); Simon et al. (2012); Cade et al. (2016)

SVP, HAL

Globicephala melas

Pilot whales

Werth (2000a, b); Kane and Marshall (2009)

Lagenorhynchus obliquidens

White-sided dolphins

Kane and Marshall (2009)

HVP, CS

Tursiops sp.

Bottlenose dolphins

Bloodworth and Marshall (2005)

HVP

Suction

Biting

X

Balaenidae

Balaenopteridae

Delphinidae X

X

HAL: high-acceleration lunge; HVP: high-velocity pursuit; NR: neck ram; SVP: slow-velocity pursuit. Taxa are listed alphabetically in their respective clades, references are listed chronologically

Despite a lack of obvious cranial movements as the mouth is held open, cranial–postcranial integration is likely common during filtering behaviors using slowvelocity pursuit. In filter-feeding cetaceans, jaw opening is associated with significant postcranial movements, especially those of the forelimbs, in order to maneuver and control strike velocity (Simon et al. 2012). Additionally, the reliance on sustained locomotion in whales results in postcranial elements specialized for cruising (Woodward et al. 2006). However, increased drag due to the open mouth during filtering hinders the metabolic efficiency of this feeding mode, requiring sufficient prey density or reduced swim speeds to be a cost-effective strategy (Webb 1982; James and Probyn 1989; Sims 2000). The small size of prey relative to the predator in combination with a unidirectional flow of water prevents the formation of a bow wave in front of the predator and minimizes the prey’s ability to escape capture. Therefore,

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the predator movement alone dictates food capture success. Many filter designs are dependent on hydrodynamic interactions with the filter, rather than direct mechanical sieving, such that changes in the flow inside the mouth chamber can have dramatic effects on the filter’s ability to trap prey items. For example, swim speed can modulate the speed of water flowing into the mouth, which then modulates the size-selective properties of the filter (Paig-Tran et al. 2011). In paddlefish, undulating postcranial movement during swimming is used to modulate the pressure gradient formed at the gills, to minimize filter clogging by sloughing prey toward the esophagus at coordinated intervals (Haines and Sanderson 2017). Therefore, during slow-velocity pursuit and filter feeding, coordination likely shifts to involve structures other than the jaws themselves, and this integration occurs both spatially and temporally to maximize capture success.

High-Velocity Pursuit and High-Acceleration Lunge High-velocity pursuit and high-acceleration lunge behaviors are used when food items are overtaken rapidly by swimming through the prey. These food items are larger than what could be effectively captured using suction (see below), but small enough to fit within the jaws whole (e.g., Liem 1980; Norton and Brainerd 1993; Porter and Motta 2004). In anchovy, for instance, particulate feeding by means of pursuit is a more energetically efficient food capture behavior than filter feeding (James and Probyn 1989). This may be especially true when food items are less densely packed, requiring the predators to target individual items. The larger size of these prey means that they are often capable of responding to and escaping an approaching predator. Pursuit (including chasing) and ambush attack strategies are therefore useful to prevent or overcome the prey’s response (Webb and Skadsen 1980). Depending on the prey size, food items can either be swallowed whole or trapped by the jaws and teeth (Porter and Motta 2004), making the jaws the prehensile structure during food capture. This behavior is common in fishes such as salmon, spikedace, pike killifish, chain pickerel and relatives, needlefish, and barracuda (Webb and Skadsen 1980; Rand and Lauder 1981; Harper and Blake 1991; Porter and Motta 2004; Ferry-Graham et al. 2010; Ferry et al. 2015) as well as a variety of secondary aquatic vertebrates (Table 4.1). During high-velocity and high-acceleration capture behaviors, the postcranial structures play a vital role in closing the distance with the prey as well as maintaining an accurate strike relative to prey position. Postcrasnial movements such as those of the tail and fins contribute to maintaining momentum during the strike, braking, and turning maneuvers (e.g., Harper and Blake 1991; Gosline 1994; Higham 2007a, b; Wöhl and Schuster 2006, 2007; Rice 2008). A number of seabirds use a diving behavior to propel themselves into the water, using their momentum to travel in the water with their beak open to catch food (Table 4.2). In this behavior, propulsion using postcranial movement is categorized based on the use of the flippers or wings (e.g., penguins, auks, and petrels) or movements of the feet (e.g., cormorants). In addition, imperial cormorants and European shag are capable of using these struc-

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tures to modify body orientation during food capture, which they do according to the microhabitat (e.g., rocky vs. sandy) (Gomez-Laich et al. 2015; Watanuki et al. 2008). These various postcranial movements occur during mouth opening so that the oral cavity is open when the predator overtakes the prey. Because ram feeding relies on the locomotor capabilities of the postcranial elements, postcranial morphology has been shown to be adapted for ram feeding (Gosline 1994; Higham 2007b; Collar et al. 2008). Due to the rapid intermittent nature of lunge strikes, these behaviors often require the recruitment of behaviors used during escape responses to (i.e., S-start or C-start) to quickly generate thrust toward the prey (Webb 1978; Rand and Lauder 1981; Webb and Skadsen 1980; Harper and Blake 1990, 1991; Norton 1991; Porter and Motta 2004; Ferry-Graham et al. 2010; Schreifer and Hale 2004). However, these behaviors are usually slower in duration and decreased in magnitude compared to when they are used to escape predators (Harper and Blake 1991; Schreifer and Hale 2004). For both pursuit and ambush behaviors, the postcranial system is responsible for closing the distance with prey and the mouth is primarily used to grab prey as the body overtakes it. However, cranial–postcranial integration is likely not fixed across predators that use these strategies, and two further examples suggest that the magnitude of coordination and the type of traits that are correlated during high-performance ram behaviors may be adaptable. First, balaenopterid whales, such as blue and humpback whales, are intermittent lunge feeders whose food capture behavior is based on multiple bursts of forward motion per dives (Croll et al. 2001; Acevedo-Gutierrez et al. 2002; Woodward et al. 2006; Goldbogen et al. 2006, 2008, 2012; Calambokidis et al. 2008; Simon et al. 2012; Hazen et al. 2015). This lunge behavior utilizes the dynamic pressure of water to passively and rapidly expand the mouth cavity (Goldbogen et al. 2007; Simon et al. 2012). However, the opening of the jaws increases the projected area of the body, thus drag, which forces the body to decelerate during the jaw opening phase (Goldbogen et al. 2006, 2007; Cade et al. 2016). This rapid deceleration is used to differentiate lunge and continuous filter-feeding modes in cetaceans (reviewed in Goldbogen et al. 2017). During this engulfment phase, the body glides forward using the momentum generated by the acceleration phase, but significant overlap indicates that the lunge may be actively sustained by postcranial movements throughout the first part the engulfment phase (Cade et al. 2016). Indeed, coordination between flipper strokes during jaw opening has been observed so that (i) jaw opening occurs at the instant of maximum forward velocity and (ii) maximum engulfment capabilities coincide with maximum body deceleration (Goldbogen et al. 2007; Simon et al. 2012; Cade et al. 2016). Additionally, the use of the postcranial system to power lunges has resulted in postcranial elements specialized for quick acceleration (Fish 2002; Goldbogen et al. 2006; Woodward et al. 2006). As demonstrated with filter-feeding paddlefish (Haines and Sanderson 2017), movement of the postcranial body and the tail can also affect the flow of water through the mouth, requiring coordination during the engulfment phase (Potvin et al. 2009). However, due to the complex interactions with mouth expansion, cranial–postcranial integration may be more complex and stronger during high-acceleration lunge feeding in cetaceans than in other aquatic vertebrates such as fishes.

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Table 4.2 Summary of the avian taxa for which prey capture under water and on land is documented to include significant postcranial movements CLADE and TAXA

Common name

References

Ram Feeding under water

Suction feeding under water

Beak prehension on land

Alle alle

Little auks

Enstipp et al. (2018)

Ana sp.

Ducks

Koolos and Zweers (1991); Van Der Leeuw (2001); Guillemain et al. (2002)

X

X

Diomedea sp.

Albatros

Prince (1980); Hedd et al. (1997)

X

X

Egretta garzetta

Little egrets

Lotem et al. (1991); Johansson and WetterholmAldrin (2002)

X

X

Egretta gularis scbistacea

Reef herons

Katzir and Intrator (1987); Prince and Jones (1992); Bocher et al. (2000)

X

X

Fratercula arctica

Atlantic puffins

Watanuki et al. (2008)

X

X

Pelecanoides sp.

Diving petrels

Navarro et al. (2014)

X

X

Phalacrocorax Cormorants sp.

Lotem et al. (1991); Watanuki et al. (2008); GomezLaich et al. (2015)

X

X

Pygoscelis sp.

Kokubun et al. (2011); Watanabe and Takahashi (2013)

X

X

Semi-aquatic birds

Penguins

X

(continued)

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Table 4.2 (continued) CLADE and TAXA

Common name

References

Ram Feeding under water

Suction feeding under water

Beak prehension on land

Calidris alpina

Dunlins

Martins et al. (2013)

X

Columbia livia

Common pigeons

Zweers (1982); Klein et al. (1985); Hörster et al. (2002); Theunissen et al. (2017)

X

Gallus domesticus

Chickens

Bout (1997); Van Der Leeuw (2001)

X

Phasianus colchicus

Common pheasants

Whiteside et al. (2015)

X

Phoeniconaias Lesser minor flamnigos

Martin et al. (2005)

X

Ramphastos sp.

Toucans

Baussart et al. (2009)

X

Rhea Americana

Greater rheas

Beaver (1978)

X

Streptoplia risoria

Ring doves

Deich and Balsam (1993)

X

Taeniopygia guttata

Zebra finches

Bischof (1988)

X

Terrestrial birds

Taxa are listed alphabetically, references are listed chronologically

Second, aquatic-feeding snakes lack limbs and their associated propulsive capabilities. Consequently, the vertebral axis itself generates the movement that is coordinated with the strike. This coordination varies among species and may be related to prey density, illustrating the role of postcranial movements during predator–prey interactions in aquatic snakes (Table 4.3). For example, Thamnophis couchii and T. elegans coil and extend the entire length of its vertebral axis during the strike whereas Nerodia rhombifer rarely use the most posterior section of the vertebral axis (Alfaro 2003). Additionally, peak head acceleration generated by the extension of the trunk occurs prior to the start of jaw opening in T. couchii, whereas it occurs after jaw opening in T. rufipunctatus and T. sirtalis (Alfaro 2002). These patterns demonstrate interspecific differences in the coordination of jaw movements with

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Table 4.3 Summary of the aquatic tetrapod taxa for which prey capture prey under water is documented to include significant postcranial movements during suction and/or ram feeding (e.g., lunge movements, assistance from the forelimbs, neck extension) CLADE and TAXA

Common name

References

Inertial Suction

Hymenochirus boettgeri

Dwarf clawed frogs

Sokol (1969); McCallum (1997); Deban and Olson (2002); Dean (2003); Carreño and Nishikawa (2010)

X

Lankanectes corrugatus

Sri Lankan wart frogs

Pethiyagoda et al. (2014)

X

Pipa pipa

Suriname toads

Carreño and Nishikawa (2010)

X

Pseudhymenochirus merlini

Merlin’s dwarf gray frogs

Carreño and Nishikawa (2010)

X

Telmatobius sp.

Titicaca frogs

Barrionuevo (2016)

X

Xenopus laevis

African clawed frogs

Avila and Frye (1978); McCallum (1997); Carreño and Nishikawa (2010)

X

Mole salamanders

Reilly and Lauder (1992)

X

Neck ram compensatory biting only suction

ANURANS

URODELES Ambystoma sp.

(continued)

those of the vertebral axis, thus emphasizing the importance of cranial–postcranial integration pattern in the evolution of prey-capture behavior even in tetrapods that lack postcranial paired appendages such as limbs.

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Table 4.3 (continued) CLADE and TAXA

Common name

References

Amphiuma tridactylum

Three-toed amphiuma

Erdman and Cundall (1984); Reilly and Lauder (1992)

X

Andrias davidianus

Chinese giant salamanders

Heiss et al. (2017)

X

Cryptobranchus sp.

Hellbenders

Reilly and Lauder (1992); Elwood and Cundall (1994)

X

Dicamptodon sp.

Pacific giant salamanders

Reilly and Lauder (1992)

X

Siren sp.

Sirens

Reilly and Lauder (1992)

Desmognathus sp.

Dusky salamanders

Deban and Marks (2002)

X

Eurycea widerae

Two-lined salamanders

Deban and Marks (2002)

X

Gyrinophilus porphyriticus

Spring salamanders

Deban and Marks (2002)

X

Pseudotriton ruber

Red salamanders

Deban and Marks (2002)

X

Stereochilus marginatus

Many-lined salamanders

Deban and Marks (2002)

Ichtyosaura alpestris

Alpine newts

Denoël (2004); Heiss et al. (2013)

X

Notophthalmus viridescens

Eastern newts

Reilly and Lauder (1988, 1992)

X

Plethodontidae

Inertial Suction

Neck ram compensatory biting only suction

X

Salamandridae

(continued)

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Table 4.3 (continued) CLADE and TAXA

Common name

References

Inertial Suction

Neck ram

Chelodina longicollis

Snakenecked turtles

Van Damme and Aerts (1997); Aerts et al. (2001)

Chelonia mydas

Green sea turtles

Bels and Renous (1992)

X

Chelydra serpentina

Snapping turtles

Lauder and Prendergarst (1992); Summers et al. (1998)

X

Chelus fimbriatus

Mata mata

Lemell et al. (2002)

Cuora amboinensis

Malayan box turtles

Natchev et al. (2009)

Dermochelys coriacea

Leatherback turtles

Bels and Renous (1992); Bels et al. (1998)

X

Heosemys grandis

Giant Asian pond turtles

Summers et al. (1998)

X

Kinosternon leucosternum

Whitelipped mud turtles

Summers et al. (1998)

X

Manouria emys

Asian forest tortoises

Natchev et al. (2015a)

Pelusios castaneus

West African mud turtles

Lemell and Weisgram (1997)

Platysternon megacephalum

Big-headed turtles

Summers et al. (1998)

Sternotherus odoratus

Musk turtles

Natchev et al. (2011)

Spectacled caimans

van Drongelen and Dullemeijer (1982)

compensatory biting only suction

CHELONIA X

X

X

X X

X

X

X X

CROCODYLIA Caiman crocodilus

X

(continued)

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Table 4.3 (continued) CLADE and TAXA

Common name

References

Inertial Suction

Neck ram

Crocodylus sp

Freshwater crocodiles

Johnstone (1973); Pooley and Gans (1976); Taylor (1987)

X

Gavialis gangeticus

Gharials

Thorbjarnarson (1990)

X

compensatory biting only suction

SERPENTES Agkistrodon piscivorus

Cottonmouths Kardong (1975); Vincent and Hedges (2005)

X

Erpeton tentaculum

Tentacled snakes

Smith et al. (2002)

X

Natrix sp.

Water snakes

Bilcke et al. (2006)

X

Nerodia sp.

Water snakes

Alfaro (2003); Bilcke et al. (2006); Vincent et al. (2006)

X

Thamnophis sp.

Garter snakes

Alfaro (2002, 2003)

X

Taxa are listed alphabetically in their respective clades, references are listed chronologically

The Use of Jaw and Neck Ram From large distances, closing the distance between predator and prey is accomplished by postcranial structures such as the body and fins, but at short distances, some predators have the ability to thrust their cranial structures toward the prey independently. For example, many fishes combine jaw opening with jaw protrusion (also referred to as jaw ram) to approach and capture food items (Lauder and Liem 1981; Wilga and Motta 2000; Ferry-Graham et al. 2001a, b; Wainwright et al. 2001). This behavior allows the fish to rapidly move a portion of its body closer to the prey item, reducing the visual cue of a strike and the probability of triggering an escape response, as well as maneuvering the capture mechanism into a more effective position relative to the prey (in the case of suction feeding; Holzman et al. 2008a). This ability has been a significant innovation in the diversification of suction-feeding fishes (Wain-

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wright et al. 2015), and is used as an alternative to body ram when prey are located at close distances (Longo et al. 2015). Fishes also use jaw ram in combination with high-speed attacks to enhance the distance covered by the body (Oufiero et al. 2012) suggesting that the ability to move the mouth independent of the body is an efficient strategy for closing the distance to the prey. Seahorses and pipefishes use a unique form of jaw ram that relies on the elastic recoil in tendons of the postcranial muscles (Van Wassenbergh et al. 2008) to power rapid cranial elevation, pivoting the jaws toward the prey in an angular jaw ram motion (Longo et al. 2015) during what has been termed “pivot feeding” (Muller 1987; de Lussanet and Muller 2007; Flammang et al. 2009). Secondary aquatic vertebrates have lost the kinetic function of most skull bones, thereby losing the ability to use jaw ram. However, many of these animals have gained flexibility of the head and neck through modification of the cervical vertebrae and occipital condyles of the skull, thereby permitting an analogous ram motion of the entire cranium toward prey (herein termed neck ram) (Table 4.1). Jaw prehension on land relies on postcranial movements, especially those of the neck, to thrust the skull and the jaws forward toward the prey and position them accurately in time and space with respect to the prey (see Sect. 4.2.2.2), thereby likely facilitating the use of these same movements after secondary transitions to the water. For example, penguins and imperial cormorants move their head independent of their body while foraging on the benthos (Kokubun et al. 2011; Gomez-Laich et al. 2015). Additionally, in penguins and sea lions, acceleration along the surge axis can be used to discriminate food capture events from other activities, such as food processing and regular swimming (Viviant et al. 2010; Kokubun et al. 2011; Watanabe and Takahashi 2013). The postcranial movements of aquatic turtles are constrained due to the derived shell, such that the neck ram is common and may be the primary form of ram used during prey encounters (Table 4.3). However, the role of the neck in generating strike velocity varies between and within species (Lauder and Prendergarst 1992; Lemell and Weisgram 1997; Natchev et al. 2009), demonstrating that postcranial movements may provide an axis of diversity among aquatic turtle food capture behaviors. Contrary to these examples, neck ram is likely absent in toothed whales where neck vertebrae are shortened and fused (Hocking et al. 2013). When present, neck ram is likely useful for (i) aiming the jaws at prey since the neck and head are potentially more maneuverable than the rest of the body and (ii) closing the distance between the jaws and prey since the neck and head present a smaller profile than the body and can minimize a prey reaction. This second idea is convergent with the use of jaw ram in fishes except for three important points: (i) neck ram is directionally flexible whereas jaw ram only occurs in the forward direction, (ii) neck ram may be an ancestral trait in secondary aquatic vertebrates but a derived trait in fishes, and (iii) coordination of head thrusting and jaw opening requires cranial–postcranial integration in secondary aquatic vertebrates but only integration within the cranial system in fishes. One exception may be seahorses, where the angled orientation of the postcranial system may be the key to resisting the powerful ventral recoil due to rapid cranial elevation during pivot-feeding, enhancing stability and food capture performance (Van Wassenbergh et al. 2011). Otherwise,

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these differences between the jaw and neck ram likely result in a novel and potentially significant form of cranial–postcranial integration in secondary compared to primary aquatic species.

Compensatory Suction In water, the forward motion of the head and body induces a bow wave in front of the predator’s snout that can push the prey away from the mouth (Lauder and Prendergarst 1992; Van Damme and Aerts 1997; Summers et al. 1998). Such bow wave induces consistent failure of food capture performance (Van Wassenbergh et al. 2010; Stewart et al. 2014; Natchev et al. 2015a). However, since water is incompressible, any degree of mouth opening can be used to generate suction. Therefore, even a small amount of suction is likely generated by any animal opening its mouth, and this suction may be used to compensate for the bow wave ahead of the swimming predator. In other words, while postcranial movements push the food item away, cranial movements draw it toward the oral cavity to counteract the effect of this forward movement. This use of compensatory suction is common in aquatic turtles where the term has been widely used (Table 4.3), but is also present in other aquatic animals. In bony fishes, this behavior been referred to as “hydrodynamic stealth” in zebrafish (Danio rerio; Gemmell et al. 2014) but has not been as widely applied otherwise. However, compensatory suction is likely also common in these fishes and is likely associated with the suction component during feeding strikes that contain ram, suction, and biting, as in opaleye (Girella nigricans; Ferry et al. 2015). Due to the need to counteract a bow wave, compensatory suction is likely common in aquatic vertebrates that rely on high performance ram prey-capture strategies and represents a further degree of coordination between cranial and postcranial movements to maintain the absolute positioning of the food item (as demonstrated by the fact that the food item remains stationary; Lauder and Prendergarst 1992; Van Damme and Aerts 1997; Summers et al. 1998; Natchev et al. 2009).

4.2.1.2

Suction Feeding

Many aquatic vertebrates utilize some form of suction generation to capture the food (Wainwright et al. 2007, 2015; Higham, this volume). This behavior involves expansion of the oral cavity to generate a pressure differential that pulls a volume of water into the mouth, carrying the food item along with it (e.g., Muller and Osse 1984; Westneat 2006; Wainwright et al. 2007; Holzman et al. 2007, 2008a, b; Van Wassenbergh and Aerts 2009; Day et al. 2015) (Fig. 4.2). In this case, the anteriorly projected suction volume created by mouth expansion is the element responsible for food capture, not the jaws. This feeding mode is usually used to capture individual prey items, but can also be used during suspension-feeding in whale sharks to move water and suspended prey into the mouth (Sanderson and Wassersug 1993; Motta et al. 2010). Although once considered along a continuum with ram (Norton and

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Fig. 4.2 Schematic representation of suction feeding in fishes. First, the predator approaches its prey using the locomotor movements of the postcranial elements. Once it is at a distance from the prey that position the prey within the potential suction volume, the rapid expansion of the mouth and gill chambers creates the suction volume. The suction volume traps the prey item and draws it into the oral cavity. This corresponds to our definition of the food capture phase. Dotted lines and arrows represent water flow during suction; solid lines indicate locomotor movements; center of mass is indicated with a checkered circle

Brainerd 1993), suction rarely occurs in isolation of ram (Longo et al. 2015). In fact, fishes as different as bichirs, mollies, and freshwater sunfish rely on similar hydrodynamic patterns when using suction (Jacobs and Holzman 2018) such that the degree of reliance on swimming describes patterns of feeding diversity better than traits associated with suction-feeding (Wainwright et al. 2001; Oufiero et al. 2012; Ferry et al. 2015; Longo et al. 2015). Therefore, suction-feeding more likely exists along a continuum of slow versus fast swimming, or inertial (pulling the prey) versus compensatory (overrunning the prey) suction. Below, we limit our discussion to inertial suction-feeding since compensatory suction is discussed above. Inertial suction is an efficient capture behavior underwater because of the high density and viscosity of water, but this comes at a cost to the reach of the suction field. Therefore, selection pressures for suction and the coordinated use of the postcranial system are likely strong in aquatic environments, and accordingly, the role of postcranial movements has been noted in a variety of aquatic organisms (Table 4.2). The same properties of water that make suction useful also make it short-lived, both temporally and spatially (Svanbäck et al. 2002; Ferry-Graham et al. 2003; Day et al. 2005, 2007; Higham et al. 2005, 2006; Holzman et al. 2008a). Therefore, the timing of predator position with mouth expansion is critical and translation toward prey via locomotor movements of the postcranial system is essential for closing this gap (Fig. 4.2) (Van Leeuwen and Muller 1984; Wainwright et al. 2001; Higham et al. 2005; Longo et al. 2015). Coordination with locomotion also ensures that the position of the suction volume is accurate with respect to the food item that is targeted (Nyberg 1971; Drost 1987; Flynn and Ritz 1999; McLaughlin et al. 2000; Higham et al. 2005, 2006; Kane and Higham 2014). In addition to its role in the positioning of the suction field, the postcranial system also has a more direct role in defining the suction volume itself. Hydrodynamic interactions with the surrounding water influence the volume and rate of water sucked

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in and predator displacement influences these interactions. Forward swimming allows the predator to ingest a larger and more elongate volume of water, but the greater volume is at the cost of suction velocity and strength (Weihs 1980; Higham et al. 2005, 2006). This contrast between high-velocity and high-volume suction (Muller et al. 1982; Muller and Osse 1984; Higham et al. 2006; Holzman et al. 2012) is due to the constraint that water movement can only be initiated when the mouth opens but before the gills open so that water does not backflow through the gill openings. Achieving a unidirectional flow through the mouth to generate suction requires opening the gill chamber at a precise time such that fishes ingesting a larger volume as they swim require opening this chamber earlier, compromising suction velocity (Bishop et al. 2008). Alternatively, if a predator moves quickly while the gill chamber is closed, the chance of pushing water away instead of pulling water toward the mouth increases (Muller and Osse 1984). Therefore, postcranial movements can hinder the efficiency of high-velocity suction feeding and a high-volume suction-feeding strategy may become more effective at high speed. Additionally, since suction reach is constant (Ferry-Graham et al. 2003; Day et al. 2005; Jacobs and Holzman 2018), predators that approach prey at faster speeds likely overrun the suction volume and suction may become more compensatory than inertial. The changes in suction with swim speed outlined above suggest a trade-off between suction velocity and swim speed, which has been supported in a variety of fishes (Higham et al. 2007; Oufiero et al. 2012; Kane and Higham 2015). Additionally, differences between marine and freshwater ecomorphs in sticklebacks suggest that divergence within suction-feeding fishes may be constrained along this trade-off (Higham et al. 2017). However, this trade-off may only be apparent above a given speed (Higham et al. 2005) or above a threshold of specialization for prey capture such that it is not ubiquitous to all suction-feeding events. Therefore, assessing how the constraints of two systems functioning together to achieve a common behavior might be involved in evolutionary processes presents a promising area for future research. Insight into the role of the postcranial system during suction feeding may be gained by considering transitions back to the aquatic environment by terrestrial vertebrates that result in convergence with fishes in the use of inertial suction (Table 4.1). Similar to fishes, suction feeding in secondary aquatic vertebrates is characterized by (i) a small mouth opening to increase suction flow velocity and (ii) significant hyoid depression to increase volume of the oral cavity (Shaffer and Lauder 1985; Reilly and Lauder 1992; Bloodworth and Marshall 2005, 2007; Marshal et al. 2008, 2014, 2015; Kane and Marshall 2009; Stinson and Deban 2017). However, the gill chambers have been lost, so water flow is bidirectional, and the suction volume is limited to that of the mouth cavity, likely constraining the use of high-volume suction. At the same time, high-velocity suction is also likely compromised due to a bidirectional flow of water (Lauder and Schaffer 1985), limited dimensions of cranial expansion relative to fishes, and a large, notched gape opening (Skorczewski et al. 2010). On the other hand, body size, and therefore absolute mouth volume, or morphological adaptations to increase suction performance, may play a role in mediating these

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constraints (Adam and Berta 2002; Jones and Goswami 2010; Kienle and Berta 2016; Stinson and Deban 2017; Jacobs and Holzman 2018). As with fishes, body movement in aquatic tetrapods toward prey is often observed in combination with suction feeding (Tables 4.1 and 4.3). For example, hind limb extension powers a lunge toward the prey item in aquatic amphibians (Erdman and Cundall 1984; Hoff et al. 1985; Elwood and Cundall 1994; Deban and Wake 2000; Deban and Marks 2002; Dean 2003; Deban 2003; Carreño and Nishikawa 2010; Barrionuevo 2016). Even more so than just lunging on the prey, many amphibians use forelimb movements to corral prey into the mouth in combination with suction (Sokol 1969; Avila and Frye 1978; Robinson and Cappo 1989; McCallum 1997; O’Reilly et al. 2002; Carreño and Nishikawa 2010; Pethiyagoda et al. 2014; Barrionuevo 2016). In dolphins, the flippers are used for maneuvering and braking during food capture and a strong interaction between postcranial (i.e., swim velocity) and cranial (i.e., mouth opening) variables have been observed (Werth 2000a; Bloodworth and Marshall 2005; Kane and Marshall 2009). As in fishes, suction strikes likely fall along a continuum between high velocity and high volume except that the magnitude of each of performance may be reduced compared to fishes of similar size (if they exist). Despite the aquatic environment imposing strong selection in favor of suction generation, vertebrates that secondarily capture aquatic prey are morphologically constrained by their terrestrial ancestry. This constraint may affect their ability to generate suction. If suction capability is also constrained relative to fishes, then integration with the postcranial system may be more prominent. Reduced ability to pull prey toward the mouth may mean that a greater degree of accuracy is required during suction prey capture, imposing constraints on the use of locomotion. Specifically, the trade-off between swimming and suction is likely more dramatic in these organisms, such that suction will be most effective in the complete absence of swimming. In fact, the greatest suction pressures have been recorded from secondary aquatic tetrapods during behaviors that constrain locomotion (i.e., feeding from a stationary device) or when forward velocity is significantly reduced (Marshall et al. 2008, 2014, 2015; Kane and Marshall 2009). Alternatively, some species may compensate for reduced suction capacity by using other structures to prevent prey escape. Given the speed of suction feeding in many of these organisms, the postcranial movements involved can be hypothesized to be coordinated at least in time with the cranial movements responsible for the rapid expansion of the oral cavity. While these vertebrates may be convergent with fishes in the use of suction during prey capture, the strength and nature of the relationship between cranial and postcranial movements during suction behaviors may not be.

4.2.1.3

Biting

Biting, also referred to as raptorial, grip and tear, or pierce feeding, is based on the prehensile capabilities of the jaws to grip onto the prey item and occurs during the mouth closing portion of a food capture event (Ferry et al. 2015). In this food capture mode, the jaws and teeth (if present) are the effective mechanisms of prehension.

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Although a small amount of suction can be generated by the opening movements of the jaws, biting does not rely on water flow to draw the food item inside the oral cavity (Alfaro et al. 2001). In fact, prey items are usually large enough that suction force cannot overcome drag forces on the prey and suction is ineffective (Ferry et al. 2015). Biting encompasses a range of behaviors including: (i) using the jaws to grab and retain prey, such as in gar, needlefish, moray eels (Porter and Motta 2004; Mehta and Wainwright 2007b) and other secondary aquatic vertebrates such as gharial, cetaceans, and pinnipeds (Table 4.1), (ii) removing pieces from a large prey item, such as in sharks (Tricas and McCosker 1984; Shirai and Nakaya 1992) and scale-eating fishes (Sazima 1983), (iii) scraping attached food item from a surface, as observed in parrotfishes, cichlids, armored catfishes, and cyprinodontiform fishes (Ferry-Graham et al. 2002; Rice and Westneat 2005; Van Wassenbergh et al. 2007, 2009; Gibb et al. 2008; Rice 2008; Hernandez et al. 2009; Rupp and Hulsey 2014), and (iv) picking behavior that is based on precise movements of the upper and lower jaws to individually select small prey from the water column, as described in Poeciliid fishes such as mollies, mosquitofish, and guppies (Ferry-Graham et al. 2008; Hernandez et al. 2008, 2009; Copus and Gibb 2013). All of these behaviors require the predator to close the distance with the prey, but each may require different levels of integration with the postcranial system depending on how it is used. In most cases, the animal moves the whole body forward toward the prey and many of the constraints discussed for ram feeding are also applicable during biting, such as the consequence of generating a bow wave. For this reason, biting behaviors may be observed in combination with both ram and compensatory suction behaviors (Ferry et al. 2015). Ram behaviors are usually achieved through body movements, but there are some exceptions. Sideways snapping or sweeping in gar, needlefish, snakes, crocodiles, and gharial (Thorbjarnarson 1990; Porter and Motta 2004) can be classified as a form of jaw ram. Raptorial biting in pinniped feeding underwater is based on the significant forward acceleration of the skull (Suzuki et al. 2009; Hocking et al. 2014; Marshall et al. 2015; Volpov et al. 2015), which is hypothesized to be generated using neck ram (Davis et al. 1999; Werth 2000b; Bowen et al. 2002; Sato et al. 2002; Watanabe et al. 2003). Similar to both suction and ram behaviors, biting can occur as a single discrete event, such as during grabbing behaviors, but can also occur in continued and repeated bout feeding (Alfaro et al. 2001; Rupp and Hulsey 2014). In this case, use of the postcranial system is likely divergent from other forms of continuous feeding such as slow pursuit ram filter feeding. To successfully position between bouts, accurate positioning of the jaws onto the food item depends on postcranial movement for maneuvering and braking in coordination with movement of the jaws (Alfaro et al. 2001; Rice and Westneat 2005; Rice 2008; Rice et al. 2008; Rupp and Hulsey 2014). During bout feeding in substrate-feeding cichlids, a significant correlation between fin beat rate and bite rate was observed (Rupp and Hulsey 2014), indicating that the locomotor system is critical for positioning and repositioning the fish between bites. In cases such as this where prey items are large and non-elusive relative to the predator, constraints imposed by hydrodynamic interactions may be weaker than during suction or ram behaviors (Ferry et al. 2015), potentially allowing greater

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flexibility of cranial and postcranial movements during prey capture. In fact, the cranial and postcranial systems may be more coordinated in time than in magnitude during these behaviors. In wrasses that capture food by scraping it from a substrate body, velocity is more coordinated with the timing of feeding variables than to mouth size (Rice 2008) and the postcranial system may be under greater demand for positioning capabilities than for swim velocity itself (in contrast to ram and suction behaviors). This potential flexibility allowed by biting behaviors may have implications for cranial–postcranial integration and the ability for organisms to diversify and exploit aquatic environments. Compared to suction feeding (Camp and Brainerd 2014, 2015; Camp et al. 2018), biting may not rely on postcranial epaxial muscle contractions for forceful jaw opening (Alfaro et al. 2001), releasing constraints due to coordination among muscle contractions. Additionally, biting requires less integration among cranial components than suction, allowing for a loss of morphological integration among skull features, loss of coordination in cranial kinematics, and increased skull diversification in moray eels (Mehta and Wainwright 2007a, b; Collar et al. 2014). Therefore, biting behaviors may release the constraints on cranial and postcranial systems that are observed during suction behaviors, making this behavior more of a generalist strategy that provides evolutionary lability. The ability to capture aquatic food using biting may have been an exaptation for using jaw prehension on land during the vertebrate transition to terrestrial environments (Heiss et al. 2018). Additionally, terrestrial jaw prehension likely facilitated the use of raptorial biting (body/neck ram in addition to anterior or lateral biting) as a transitional feeding mode in the secondary adaptation of mammals back to aquatic lifestyles and prey-capture modes (Johnston and Berta 2011; Hocking et al. 2014; Marshall et al. 2015). Therefore, food capture using biting may present the greatest diversity in cranial–postcranial integration strategies compared with other aquatic-feeding modes and represents a significant area for future research on cranial–postcranial integration.

4.2.2 Terrestrial Food Capture Aquatic vertebrates that use suction take advantage of the forces associated with the density and viscosity of water to draw food into the oral cavity. In comparison, the low density and viscosity of air make suction impractical for capturing food on land. Instead, similar to aquatic vertebrates that cannot use suction feeding, terrestrial vertebrates have to cover the distance between themselves and the food item. The ability to reach for food is thus critical to the success of food capture on land. This section will review our knowledge of food capture behaviors observed in terrestrial organisms (i.e., tongue prehension, jaw prehension, and hand prehension). Most studies of food capture on land focus on understanding the movements of the cranial elements (see Schwenk 2000a for a review), but here our objective is to extend our perspective on food capture by considering the contribution of the postcranial elements. First, we will discuss the role of postcranial movements into reaching for

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food and covering predator–prey distance. Second, we will present the contribution of postcranial movements not only as a mere addition to the cranial movements, but rather how their coordination in time and magnitude benefits the various food capture behaviors known to be used by terrestrial organisms.

4.2.2.1

Tongue Prehension

Some terrestrial organisms use their tongue to reach and contact food items. This is the case of most amphibians (reviewed in Nishikawa 2000; O’Reilly 2000), as well as some non-ophidian squamates (reviewed in Bels et al. 1994; Schwenk 2000b; Bels 2003) and some chelonians (e.g., Bels et al. 1997, 2008; Wochesländer et al. 1999), but also myrmecophagous mammals such as echidnas, pangolins and anteaters (reviewed in Reiss 2000; e.g., Naples 1999; Lin et al. 2015; Asahara et al. 2016; Casali et al. 2017). The ability of the hyolingual apparatus to protrude or indeed project forward outside of the oral cavity allows for covering predator–prey distance. Even though most of the literature focuses on the morphology and/or the movements of the cranial elements (i.e., the hyolingual apparatus and the jaws), many authors report postcranial movements during tongue prehension so that the body also extends forward toward the food item (Tables 4.4 and 4.5). In particular, postcranial movements during tongue prehension in various amphibians and squamate lizards are usually reported as “lunge movements” which are described as the extension of the hindand/or forelimbs pushing the trunk forward toward the food item during jaw opening and tongue protrusion. In chamaeleons, food capture is characterized by tongue projection up to a distance equal to over one body length (e.g., Wainwright et al. 1991; Wainwright and Bennett 1992a, b; Meyers and Nishikawa 2000; Herrel et al. 2001; de Groot and van Leeuwen 2004; Anderson and Deban 2010; Anderson 2016) while the body remains stationary (Wainwright et al. 1991). This indicates that no cranial–postcranial integration occurs in organisms in which the hyolingual apparatus is morphologically adapted for tongue projection like chameleons (Fig. 4.3d). Contrary to chamaeleons, where the tongue is capable of ballistic projection and therefore capable of covering long predator–prey distance, tongue prehension in many other lizards is supplemented by postcranial movements. In these animals, lunge movements vary as much as to be described by a full repertoire of locomotor strategies ranging from a distinct strike posture to a fully fleshed jump, as is the case in Anolis lizards (Moermond 1979, 1981; Jenssen et al. 1995; Montuelle et al. 2008). This demonstrates that postcranial movements are a key component of food capture performance in these organisms. However, the amplitude of postcranial movements in Anolis carolinensis is found independent from cranial movements (Montuelle et al. 2008), providing evidence that cranial and postcranial movements are not coordinated during food capture in this species. In contrast, postcranial and cranial movements are coordinated in time and amplitude during tongue prehension in another lizard, Broadleysaurus major (Montuelle et al. 2009, 2010). Contrary to Anolis lizards that catch food using tongue prehension exclusively, B. major uses the tongue to capture only a subsample

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Table 4.4 Summary of the lepidosaur taxa for which tongue prehension is explicitly documented to involve postcranial movements during prey capture behavior (e.g., neck movements, lunge movements) CLADE and TAXA

Common name

References

Sphenodon punctatus

Tuatara

Gorniak et al. (1982)

Green anoles

Moermond (1979, 1981); Montuelle et al. (2008)

IGUANIA Anolis carolinensis Agamidae Moloch horridus

Thorny devils

Meyers and Herrel (2005)

Pogona vitticeps

Bearded dragons

Meyers and Herrel (2005); Schaerlaeken et al. (2007)

Pseudotrapelus sinaitus

Sinai agamas

Meyers and Nishikawa (2000)

Stellgama stellio

Starred agamas

Kraklau (1991); Herrel et al. (1995)

Phrynosoma platyrhinos

Desert horned lizards

Meyers and Herrel (2005)

Sceloporus undulatus

Fence lizards

Meyers and Nishikawa (2000)

Broadleysaurus major

Plated lizards

Reilly and McBrayer (2007); Montuelle et al. (2009, 2010, 2012a)

Karusasaurus polyzonus

Karusa lizards

Broeckhoven and Le Mouton (2013)

Lacerta viridis

Green lizards

Urbani and Bels 1995

Ouroboros cataphractus

Armadillo girdled lizards

Broeckhoven and Le Mouton (2013)

Tiliqua scincoides

Blue-tongued lizards

Smith et al. 1999

Uma notata

Fringe-toed lizards

Meyers and Herrel (2005)

Zonosaurus laticaudatus

Girdled lizards

Urbani and Bels 1995

Phrynosomatidae

AUTARCHOGLOSSA

Taxa are listed alphabetically in their respective clade, references are listed chronologically

of its dietary range (i.e., small and/or motionless food items; Reilly and McBrayer 2007; Montuelle et al. 2009, 2010; similar to closely related species; Urbani and Bels 1995; Smith et al. 1999; Broeckhoven and Le Mouton 2013). In summary, reliance on postcranial movements during tongue prehension in lizards vary from no movement, thus no coordination, to the movement that either is or isn’t coordinated with cranial movement, and this is proposed to be linked with tongue specialization. Indeed, closely related species (B. validus and B. nigrolineatus) have been observed to engage in tongue-flicking behavior (Cooper 1992; Cooper and Steele 1999), indicating that in these species the tongue is not only used for food prehension but also for food detection and localization using chemoreception (although other species in the same clade are reported to use tongue prehension to not be able to discriminate between odors by using chemoreception; Le Mouton et al. 2000). Therefore, contrary to the tongue of A. carolinensis whose morphology is solely adapted to its prehensile function, the morphology of the tongue of B. major species is a trade-off between

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Table 4.5 Summary of the amphibian taxa for which tongue prehension is documented to include significant postcranial movements (e.g., lunge movements) CLADE and TAXA

Common name

References

Ascaphus truei

Tailed frogs

Nishikawa and Cannatella (1991)

Bufo sp.

Toads

Gans and Gorniak (1982); Nishikawa and Gans (1992, 1996); Deban and Lappin (2011)

Cyclorana novaehollandiae

New Holland frogs

Robinson and Cappo (1989); Valdez and Nishikawa (1997)

Discoglossus pictus

Painted frogs

Nishikawa and Roth (1991)

ANURANS

Dyscophus guineti

False tomato frogs

Monroy and Nishikawa (2009)

Hemisus marmoratus

Marbled snout-burrowers

Ritter and Nishikawa (1995); Nishikawa et al. (1999)

Hyla cinerea

Green tree frogs

Deban and Nishikawa (1992)

Hymenochirus boettgeri

Dwarf clawed frogs

Sokol (1969)

Pachymedusa dacnicolor

Leaf frogs

Gray and Nishikawa (1995)

Phrynomantis bifasciatus

Banded rubber frogs

Meyers et al. (2004)

Rana pipiens

Leopard frogs

Comer and Grobstein (1981); Anderson (1993); Anderson and Nishikawa (1993, 1996)

Spea multiplicata

Spadefoot toads

O’Reilly and Nishikawa (1995)

Xenopus laevis

African clawed frogs

Avila and Frye (1978)

URODELES Hynobius sp.

Asian salamanders

Larsen et al. (1989, 1996)

Ambystoma sp.

Mole salamanders

Larsen and Guthrie (1975); Larsen et al. (1996)

Bolitoglossa mexicana

Climbing salamanders

Larsen et al. (1989)

Desmognathus sp.

Dusky salamanders

Larsen et al. (1989); Deban and Dicke (1999); Deban and Marks (2002)

Ensatina eschscholtzii

Yellow-eyed ensatinas

Larsen et al. (1989); Deban (1997); Deban and Scales (2016)

Gyrinophilus porphyriticus

Spring salamanders

Deban and Marks (2002)

Plethodon sp.

Woodland salamanders

Maglia and Pyles (1995); Larsen et al. (1989); Deban and Dicke (1999); Deban and Scales (2016)

Pseudotriton ruber

Red salamanders

Deban and Dicke (1999)

Plethodontidae

(continued)

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Table 4.5 (continued) CLADE and TAXA

Common name

References

Cynops pyrrhogaster

Fire belly newts

Miller and Larsen (1990)

Ichtyosaura alpestris

Alpine newts

Denoël (2004); Heiss et al. (2013)

Paramesotriton hongkongensis

Warty newts

Miller and Larsen (1990)

Salamandra salamandra

Fire salamanders

Miller and Larsen (1990); Reilly (1996)

Taricha torosa

California newts

Findeis and Bemis (1990)

Salamandridae

Taxa are listed alphabetically in their respective clade, references are listed chronologically

two functions; i.e., prehension and chemoreception. Tongue morphology in lizards differs depending on its primary function as prehensile tongues are bulky and fleshy whereas chemoreceptive tongues are slender and flattened (Schwenk 1993, 1994, 2000b). The slender and flattened morphology of chemoreceptive tongues decreases their prehensile capabilities, whereas the bulky and fleshy morphology of prehensile tongues is a hindrance to the efficiency of tongue-flicking behavior necessary to chemoreception; even though some prehensile tongues remain able to tongue flick (e.g., Herrel et al. 1998). In this context, the success of tongue prehension in lizards with chemoreceptive tongue cannot rely solely on the prehensile capabilities of the hyolingual apparatus, but instead requires the integration of postcranial elements (Montuelle et al. 2009). It thus appears that tongue prehension in lizards is linked to various degree of cranial–postcranial integration (Fig. 4.3). In lizards whose hyolingual apparatus is specialized for tongue projection, such as in chamaeleons, tongue movements are so efficient that the rest of the body can remain stationary (e.g., Wainwright et al. 1991; Meyers and Nishikawa 2000; Herrel et al. 2001; de Groot and van Leeuwen 2004; Anderson and Deban 2010; Anderson 2016; Fig. 4.3c) and consequently no cranial–postcranial integration occur. In other lizards that use tongue prehension, but whose hyolingual apparatus is not specialized for tongue projection, tongue movements are assisted by lunge movements that are powered by postcranial structures such as the limbs and the vertebral columns (Montuelle et al. 2008, 2009). Among these species, cranial and postcranial movements are decoupled from each other in taxa with strong prehensile capabilities of the hyolingual apparatus (Montuelle et al. 2008; Fig. 4.3b) whereas, in taxa whose tongue is characterized by limited prehensile capabilities, cranial and postcranial movements are coordinated in time and magnitude (Montuelle et al. 2009; Fig. 4.3a). Consequently, cranial–postcranial integration during tongue prehension in squamate lizards is hypothesized to compensate for the reduced prehensile capabilities of the tongue. The phylogenetic framework of these observations allows for the development of forging hypotheses related to the role of cranial–postcranial integration during the evolution of tongue prehension in squamate lizards. In the squamate lineage, the

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Fig. 4.3 Changes in relative contribution of cranial and postcranial movements, and their integration, during food capture behavior in response to changes in the prehensile capabilities of the tongue. a In organisms whose tongue is only capable of catching small food items, postcranial movements are coordinated with both jaw and tongue movements to produce successful food capture performance, essentially compensating for the limited prehensile capabilities of the tongue. This is the case of Gerrhosaurus major (Montuelle et al. 2009, 2010). b In organisms whose tongue is used consistently and exclusively to catch food, postcranial movements are involved but decoupled (i.e., independent) from jaw or tongue movements. This is the case of Anolis carolinensis (Montuelle et al. 2008). c In organisms whose tongue is specialized for extreme prehensile capabilities, postcranial movements during food capture is unnecessary (i.e., the body remains stationary) and no cranial–postcranial integration occurs. This is the case of Chamaeleo oustaleti (Wainwright et al. 1991). d In organisms whose tongue lacks any prehensile capabilities, jaw prehension is used for all sort of food items, basing food capture performance on the coordination of jaw movements with postcranial movements such as those of the neck and of the forelimbs. This is the case of lizards with chemoreceptive tongue like Tupinambis merianae and Varanus sp (Montuelle et al. 2012a, b). e In organisms whose tongue lacks any prehensile capabilities and that lost limbs, jaw prehension relies on the coordination of jaw movements with neck movements. This is the case of food capture in snakes. The relative contribution of the cranial and postcranial movements during food capture is represented by color: tongue movements in green, jaw movements in blue, neck movements in yellow, and limb movements in red

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closest relative of the ancestral condition is Sphenodon punctatus, which has been observed to use tongue prehension only to capture small elusive prey (i.e., crickets and cockroaches; Gorniak et al. 1982; Schaerlaeken et al. 2008). This condition is similar to what is observed in Broadleysaurus major and other scincomorphan lizards that use tongue prehension only to capture small food items (Urbani and Bels 1995; Montuelle et al. 2009, 2010; Broeckhoven and Le Mouton 2013). Based on molecular evidence, the scincomorphan clade is nested close to the root of the squamate lineage (Townsend et al. 2004; Lee 2005; Vidal and Hedges 2005) and thus limited the prehensile capabilities of the hyolingual apparatus, and the associated cranial–postcranial integration during tongue prehension, may be the plesiomorphic condition within the squamate lineage. Molecular evidence further shows that iguanian and autarchoglossan lizards are derived (Townsend et al. 2004; Lee 2005; Vidal and Hedges 2005), suggesting that the morphofunctional evolution of the hyolingual apparatus is characterized by two different trajectories: specialization for prehension or for chemoreception. On one hand, as the prehensile capabilities of the tongue increase, the contribution of the postcranial movements during food capture decreases, first by being decoupled (as in Anolis lizards; Montuelle et al. 2008; consider transition between Fig. 4.3a, b) until a point where postcranial movements are unnecessary and thus the body remains stationary (as in chamaeleons; Wainwright et al. 1991; Meyers and Nishikawa 2000; consider the transition from Fig. 4.3a, b and ultimately c). In other words, cranial–postcranial integration during tongue prehension in squamate lizards is hypothesized to have disappeared in response to the morphofunctional specialization of the hyolingual apparatus for food prehension. On the other hand, the specialization of the hyolingual apparatus for chemoreception led to significant changes in its morphology which rendered it ineffective for prehension. As a result, squamate taxa with chemoreceptive tongues are only able to catch food using their jaws exclusively. As will be explained in the next section, jaw prehension clearly relies on extensive cranial–postcranial integration (Fig. 4.3d, e). Interestingly, this integration hypothesis is supported by the trade-off observed between lunge movements and tongue prehensile capabilities in amphibians that use tongue prehension to capture food items. Lunge movements during food capture have been documented in several anuran and urodele taxa (Table 4.5). Unfortunately, these reports are for the most part qualitative, and the quantification of postcranial movements has been limited to measuring lunge distance (Larsen et al. 1989; Nishikawa and Cannatella 1991; Nishikawa and Roth 1991; Anderson 1993; Gray and Nishikawa 1995; Maglia and Pyles 1995; Anderson and Nishikawa 1996; Larsen et al. 1996; Deban 1997; Valdez and Nishikawa 1997; Deban and Marks 2002). Nevertheless, many of these authors agree that cranial and postcranial movements during tongue prehension in amphibians are at least related temporally (Anderson and Nishikawa 1996, p. 758) if not coordinated temporally and spatially (Nishikawa and Gans 1992, p. 250). Interspecific differences in lunge movements in amphibians have been proposed to be associated with variability in distance, velocity and acceleration of tongue protraction (Roth and Wake 1985; reviewed in Wake and Deban 2000; Deban et al. 2001; Deban and Marks 2002) and anurans (Nishikawa et al. 1992; reviewed in Nishikawa 2000; Deban et al. 2001). In detail, amphibian taxa

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that lunge the most are the ones characterized by limited tongue protraction (Larsen et al. 1989, 1996; Nishikawa and Cannatella 1991; Nishikawa and Roth 1991; Deban and Nishikawa 1992; Gray and Nishikawa 1995; Deban and Dicke 1999; Deban and Marks 2002), whereas taxa with extensive tongue protraction are the ones that lunge the least (Gans and Gorniak 1982; Findeis and Bemis 1990; Nishikawa and Gans 1992, 1996; Nishikawa et al. 1999; Deban and Marks 2002). In particular, the absence of lunge movements has actually been documented in amphibian taxa whose hyolingual apparatus is specialized for tongue projection (in anurans: Gans and Gorniak 1982; Nishikawa and Gans 1992, 1996; Ritter and Nishikawa 1995; Larsen et al. 1996; Meyers et al. 2004; Deban and Lappin 2011; in urodeles: Larsen et al. 1989; Miller and Larsen 1990; Maglia and Pyles 1995; Deban and Dicke 1999; Deban and Marks 2002; Deban et al. 2007; Deban and Richardson 2011). Therefore, similarly to squamate lizards, in amphibian taxa whose tongue is able to protrude outside of the oral cavity to reach for food item, lunge movements are unnecessary, and thus are reduced if not totally absent, and cranial–postcranial integration can be hypothesized to be reduced if present at all. In contrast, in taxa whose tongue cannot protrude as much, lunge movements contribute to covering the distance between the predator and the food item, thus ensuring the success of food capture. Accordingly, cranial— postcranial integration during food capture can be expected to be strong in amphibian taxa whose hyolingual apparatus is characterized by poor tongue prehensile capabilities and limited in amphibian taxa whose hyolingual apparatus is specialized for prehension. According to our hypothesis that lunge movements during tongue prehension in amphibians are also based on cranial–postcranial integration, the evolutionary pattern of cranial–postcranial integration observed in squamate lizards may be mirrored in the amphibian lineage as well.

4.2.2.2

Jaw Prehension

In the context of this chapter, we propose to use the term jaw prehension to describe food capture performance during which (i) initial predator–prey contact is completed by the jaws and (ii) tongue protraction–retraction movements are absent. Jaw prehension is observed in a wide variety of terrestrial vertebrates, including: amphibians (Miller and Larsen 1990; Deban 1997; O’Reilly 2000; Deban et al. 2001; Deban and Marks 2002), squamate lizards (reviewed in Schwenk 2000b; Bels 2003; Table 4.6), snakes (reviewed in Cundall and Greene 2000), crocodylians (reviewed in Cleuren and De Vree 2000), chelonians (Bels et al. 1997, 2008; Natchev et al. 2009, 2015a; Heiss et al. 2010; Stayton 2011), mammals (e.g., Allen 1950; Robinette et al. 1959; McManus 1970; Adamec 1976; Biben 1979; Gorniak and Gans 1980; Van Valkenburgh and Ruff 1987; Smallwood 1993; Van Valkenburgh 1996, 2007; Table 4.7), and birds (e.g., Deich and Balsam 1993; Hörster et al. 2002; Table 4.2). Jaw prehension has also been reported to be used in a couple of anuran taxa feeding on large prey (i.e., Cyclorana novaehollandiae and Rana pipiens; Anderson 1993; Anderson and Nishikawa 1996; Valdez and Nishikawa 1997). In those cases, the tongue is only used to subdue and immobilize the prey, which is subsequently grasped

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with the jaws. Jaw prehension in frogs remains significantly different than tongue prehension because the tongue is “not used to return the prey to the mouth” (Anderson and Nishikawa 1996). Jaw prehension requires the whole cranial apparatus to be moved toward the food item because the jaws cannot move independently from the skull like the tongue can. The positioning of the skull onto the prey is achieved by the movements of the postcranial elements such as the vertebral axis and the limbs during jaw opening so that the jaws can close onto the food item and secure it. Therefore, the success of jaw prehension can be hypothesized to be dictated by the reach capabilities of the postcranial system, especially the extension capabilities of the neck and the limbs. Neck movements have indeed been noted to be key to jaw prehension in chelonians (Bels et al. 1997, 2008; Natchev et al. 2009, 2015a), squamate lizards (Montuelle et al. 2009, 2012a, b), snakes (Kardong 1975, 1986; Greenwald 1978; Janoo and Gasc 1992; Kardong and Bels 1998; Cundall and Deufel 1999; Young et al. 2001; Vincent et al. 2005; Young 2010; Herrel et al. 2011; Table 4.6) and carnivorans (reviewed in Van Valkenburgh 2007; Table 4.7). Inaccurate or incorrect postcranial movements may fail to position the skull correctly with respect to the food item, thus translating into an unsuccessful attempt at capturing food. Even more so than just a matter of positioning in space, the coordination of cranial and postcranial movements must also occur in time. Without coordination between the movements of the jaw and those of the postcranial elements, the jaws may be opened too widely or conversely not open enough at the time of predator–prey contact, thus resulting in an unsuccessful food capture attempt.

Jaw Prehension in Squamates Most autarchoglossan lizards use jaw prehension to capture prey, which is completed by the upper and lower jaw securing first contact with the food item by closing onto it rapidly (reviewed in Schwenk 2000b; Bels 2003). In addition, jaws opening–closing movements have been shown to be coordinated in amplitude and timing with those of the neck and the forelimbs in a handful of autarchoglossan taxa: Broadleysaurus major, Salvator merianae, Varanus niloticus, and V. ornatus (Montuelle et al. 2009, 2012a). The taxonomic range of these observations shows that the evolution of the chemoreceptive capabilities of the tongue decreased its prehensile capabilities from a condition where the tongue is only capable to catch small prey (as in cordylids; Urbani and Bels 1995; Smith et al. 1999; Reilly and McBrayer 2007; Montuelle et al. 2009; Broeckhoven and Le Mouton 2013) to a condition where the tongue is not involved at all in the capture of any kind of prey and jaw prehension is used to capture all food (as in monitor lizards and many snakes; Cundall and Greene 2000; Montuelle et al. 2012a, b; Fig. 4.3d). According to the observations that jaw prehension in squamate lizards relies on cranial–postcranial integration, jaw prehension in snakes can be hypothesized to be characterized by the coordination of jaw movements with those of the vertebral axis. Even though no quantitative data are available yet, this hypothesis appears to be

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Table 4.6 Summary of the lepidosaur taxa for which jaw prehension is documented to include significant postcranial movements (e.g., neck movements, lunge movements) CLADE and TAXA

Common name

References

Sphenodon punctatus

Tuatara

Gorniak et al. (1982)

Ablepharus kitaibelii

Copper skinks

Natchev et al. (2015b)

Broadleysaurus major

Plated lizards

Reilly and McBrayer (2007); Montuelle et al. (2009, 2010, 2012a)

Karusasaurus polyzonus

Karusa lizards

Broeckhoven and Le Mouton (2013)

Ouroboros cataphractus

Armadillo girdled lizards

Broeckhoven and Le Mouton (2013)

Salvator merianae

Black and white tegus

Montuelle et al. (2009, 2012a)

Varanus niloticus

Nile monitors

Montuelle et al. (2009, 2012a, 2012b)

Varanus ornatus

Ornate monitors

Montuelle et al. (2009, 2012a, 2012b)

Agkistrodon piscivorus

Cottonmouths

Kardong (1975); Vincent et al. (2005)

Erpeton tentaculum

Tentacled snakes

Smith et al. (2002)

Nerodia sp.

Water snakes

Alfaro (2003); Vincent et al. (2006)

Thamnophis sp.

Garter snakes

Alfaro (2002, 2003)

AUTARCHOGLOSSA

SERPENTES Semiaquatic snakes

Terrestrial snakes Bitis arietans

Puff adders

Young (2010)

Boa constrictor

Common boas

Cundall and Deufel (1999)

Corallus hortulanus

Tree boas

Cundall and Deufel (1999)

Crotalus sp.

Rattlesnakes

Kardong (1986); Kardong and Bels (1998); Young et al. (2001)

Liasis mackloti

Freckled pythons

Cundall and Deufel (1999)

Morelia sp.

Pythons

Cundall and Deufel (1999)

Natrix tessellata

Dice snakes

Van Wassenbergh et al. (2010)

Piluophis melanoleucus affinitis

Pine snakes

Greenwald 1978

Python sp.

Pythons

Cundall and Deufel (1999)

Trimeresurus albolabris

White-lipped pit vipers

Herrel et al. (2011)

Vipera ammodytes

Nose-horned vipers

Janoo and Gasc (1992)

Taxa are listed alphabetically in their respective clade, references are listed chronologically

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Table 4.7 Summary of terrestrial non-primate mammalian taxa for which prey capture is documented to include significant postcranial movements during jaw prehension (e.g., neck movements, forelimb assistance) CLADE and TAXA

Common name

References

Treeshrews

Joly et al. (2012)

Dendrolagus sp.

Tree kangaroos

Iwaniuk et al. (1998)

Monodelphis domestica

Short-tailed opossums

Ivanco et al. (1996)

Beavers

Whishaw et al. (1998)

EUTHERIA Tupaia belangeri MARSUPIALS

RODENTS Castor sp. Cavia porcellus

Guinea pigs

Whishaw et al. (1998)

Cynomys parvidens

Prairie dogs

Whishaw et al. (1998)

Meriones unguiculatus

Mongolian gerbils

Whishaw et al. (1998)

Mesocricetus auratus

Golden hamsters

Whishaw et al. (1998)

Mus musculus

House mice

Whishaw (1996); Whishaw et al. (1998)

Rattus norvegicus

Brown rats

Whishaw and Pellis (1990); Whishaw et al. (1992); Ivanco et al. (1996); Whishaw (1996); Whishaw and Coles (1996); Whishaw et al. (1998); Alaverdashvili et al. (2008)

Sciurus carolinensis

Grey squirrels

Whishaw et al. (1998)

Urocitellus richardsonii

Ground squirrels

Whishaw et al. (1998)

Tamiasciurus hudsonicus

Red squirrels

Whishaw et al. (1998)

Cheetahs

Kruuk and Turner (1967); Van Valkenburgh (1996); Russel and Bryant (2001)

CARNIVORANS Acinonyx jubatus

Felis catus

Domestic cats

Biben (1979)

Hyena hyena

Striped hyenas

Spoor and Badoux (1986)

Lynx lynx

Lynx

Viranta et al. (2016)

Panthera leo

Lions

Kruuk and Turner (1967); Van Valkenburgh (1996)

Panthera pardus

Leopards

Kruuk and Turner (1967); Martin (1980); Karanth and Sunquist (2000)

Panthera tigris

Tigers

Martin (1980); Karanth and Sunquist (2000) (continued)

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Table 4.7 (continued) CLADE and TAXA

Common name

References

Procyon lotor

Raccoons

Iwaniuk and Wishaw (1999)

Puma concolor

Cougars

Robinette et al. (1959); Smallwood (1993)

Common marmosets

Singer and Schwibbe (1999); Vinyard et al. (2001, 2003, 2009); Vinyard and Scmitt (2004); Dumont et al. (2011)

Cheirogaleus sp.

Dwarf lemur

Ward et al. (1993); Ward (1995)

Euoticus elegantulus

Bushbaby

Vinyard et al. (2003)

Microcebus murinus

Gray mouse lemur

Reghem et al. (2011); Scheumann et al. (2011); Toussaint et al. (2013, 2015)

PRIMATES Callithrix jacchus

Otolemur sp.

Greater galago

Ward et al. (1993); Ward (1995)

Phaner furcifer

Masoala lemur

Vinyard et al. (2003)

Taxa are listed alphabetically in their respective clades, references are listed chronologically

supported by promising qualitative reports and observations of food capture behavior in snakes (Table 4.6). As noted by multiple researchers, jaw prehension in snakes is achieved by coils in the body which quickly extend to propel the head and the open jaws onto the prey (reviewed in Cundall and Greene 2000; Young et al. 2001; Vincent et al. 2005; Young 2010; Herrel et al. 2011). These studies report significant differences in postcranial movements during jaw prehension between taxa (Cundall and Greene 2000; Young et al. 2001; Vincent et al. 2005; Young 2010). In a terrestrial species, Bitis arietans, three patterns of postcranial recruitment have been observed: snapping (i.e., only the cranial-most body coil is extended, no other coil is extended), lunging (i.e., the cranial-most body coil is extended first, followed by the second body coil, no other coil is extended), and projecting (i.e., body coils extend in a craniocaudal sequence; Young 2010). Western diamondback rattlesnakes (Crotalus atrox) are also capable of switching between coiled strikes (i.e., more than 50% of the body is formed into coils) or extended strikes (i.e., less than 50% of the body is formed into coils), with the former associated with larger gape size (Young et al. 2001), suggesting cranial–postcranial coordination in amplitude. However, in Bitis arietans (the puff adder), trunk extensor muscles are not active during body extension, indicating that head displacement is due to the elastic extension of body coils (Young 2010). This suggests that postcranial movements during jaw prehension in snakes may not be as finely controlled as postcranial movements generated by muscle contractions in other animals. In addition, snakes may represent a taxa in which uncontrolled postcranial movements may be coordinated in time and/or amplitude with well-controlled cranial movements.

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Jaw Prehension in Birds Beak prehension in birds can be considered functionally homologous to jaw prehension because the first contact with the food item is achieved by the keratinized upper and lower jaws without the tongue playing any role. To our knowledge functional and/or biomechanical data on food capture in birds are scarce as most of the research focused on the food processing stage of feeding behavior (reviewed in Tomlinson 2000). Neck movements during food capture in terrestrial birds have been described, or at least reported, in a variety of taxa (Table 4.2). Unfortunately, most of these reports are qualitative description but a handful of studies provide promising quantitative data. Beak prehension, also referred to as pecking, is used to pick up food on the ground by the tips of the beak and is achieved by the movements of the neck to orient, angle, and thrust the head toward the food item (Beaver 1978; Zweers 1982; Klein et al. 1985; Deich and Balsam 1993; Van Der Leeuw et al., 2001; Hörster et al. 2002). Neck mobility in birds has been demonstrated to be the core of the diversity of neck and head postures, explaining, and predicting those used during food capture (Bout 1997; Van Der Leeuw et al. 2001). The degree to which such mobility in the cervical region is correlated to beak opening–closing movements will provide unequivocal evidence of cranial–postcranial integration during beak prehension in birds. During pecking in adult chicken, mallard ducks, and pigeons, head movements are observed to be induced by the movements and the deformation of the neck (Zweers 1982; Klein et al. 1985; Bout 1997; Van Der Leeuw et al. 2001; Hörster et al. 2002). Pecking in pigeons may even involve “a downward bow of the body itself” (Hörster et al. 2002, p. 30) probably because the neck is too short for the head to reach the ground. However, variability in cranial and postcranial movements is explicitly noted (Hörster et al. 2002, p. 39), and thus neck–head correlation can be hypothesized to be variable as well. Finally, in adult ring doves, cranial movements (i.e., gape distance) are correlated with postcranial movements (i.e., head thrust velocity; see Fig. 1 in Deich and Balsam 1993); although no statistical test of such correlation was conducted. Interestingly, this study also observed pecking behavior in newborn doves and reported that “neither gape nor the coordination of gape and thrust appear to be close to their adult patterns” (Deich and Balsam 1993; p. 272). Finally, note that such changes in neck–head coordination throughout ontogeny are also reported during drinking in chicken (Heidweiller et al. 1992). These observations suggest that cranial–postcranial integration may vary throughout ontogeny in birds. Overall, given the high velocity and rhythmicity of pecking behavior in granivorous birds, cranial–postcranial integration can be hypothesized to minimize beak-substrate impact to prevent injuries to the beak tips by controlling the lowering of the head toward the ground as the beak opens and closes rapidly. Other studies quantify the role of neck movements during food capture indirectly by measuring the depth and the angle of the head of birds probing the substrate for food items (Lotem et al. 1991; Martins et al. 2013). Food capture in dunlins is characterized by three distinct patterns of head depth which indicates variability in neck movements (Martins et al. 2013). This variability is shown to respond to

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changes in food and in the time of the year, and likely relates to food availability. Similarly, the success of food capture in egret depends on strike angle with more acute angle being the most successful food capture attempts, emphasizing the critical role of postcranial movements during beak prehension, especially those of the neck (Lotem et al. 1991). The importance of neck movements for food capture in birds is illustrated by the extreme examples of food capture in flamingos where the neck allows the skull to be completely inverted during feeding (Martin et al. 2005), or in skimmers that “forage with the lengthened lower mandible trailing in the water as the bird flies a level straight course” (Fig. 4 in Martin 2007). Finally, in birds feeding on items anchored in a substrate, such as scavenging carnivorous or herbivorous birds, for instance, cranial–postcranial integration can be hypothesized to contribute to the success of the pulling force that is necessary for detaching food from its substrate. In conclusion, the role of the cervical region of the vertebral axis can be hypothesized to be key to the success of beak prehension in birds and thus, similarly to jaw prehension in other terrestrial vertebrates, beak prehension may be hypothesized to involve the integration of the cranial and postcranial elements so that neck and beak movements are coordinated in time and/or amplitude.

Jaw Prehension in Mammals Jaw prehension is also used by a variety of mammals, in particular rodents and carnivorans (Table 4.7; reviewed in Van Valkenburgh 2007). In carnivorans especially, biting has been mentioned to be supported by the action of the craniocervical system as well as those of the forelimbs (Table 4.7). Because the prey-capture behavior of carnivorans relies on biting, the capabilities of the cranial elements to generate bite force apply significant selective pressures on cranial morphology (Christiansen and Adolfssen 2005; Christiansen and Wroe 2007; Christiansen 2008; Slater et al. 2009; Hartstone-Rose et al. 2012). In Canids, differences in cranial morphology are associated with various aspects of biting behaviors depending on dietary specializations (Slater et al. 2009). According to our hypothesis that jaw prehension relies on cranial–postcranial integration, Canids with different diets may be characterized by different coordination patterns between jaw and neck movements. Canids feeding on small and evasive prey are characterized by long and narrow jaws allowing quick jaw movements (Slater et al. 2009), and thus the timing of neck extension projecting the head forward toward the prey can be expected to be coordinated to match the speed of jaw opening and closing movements. In contrast, canids feeding on large prey are characterized by strong short jaws allowing greater bite force (Slater et al. 2009), the pulling force generated by neck movements can be expected to be coordinated in time and amplitude with bite force generation. Jaw prehension in other carnivorans also relies on more postcranial movements than just those of the neck. In particular, the role of the forelimbs during jaw prehension is well documented in felids (Table 4.7). Overall, most of these taxa jump on their prey with their jaw open and with their forepaws contributing to securing a grip on the prey in various degrees. On one hand, the use of jaw prehension in

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felids is associated with variation in the morphology of the jaw apparatus, which relates to diet (e.g., Hartstone-Rose et al. 2012). On the other hand, food capture in some felids relies so much on grasping the prey item with the forepaws that the forelimbs are actually considered to be the main prehensile elements (Gonyea and Ashworth 1975; Gonyea 1978; Van Valkenburgh 2007; Meachen-Samuels and Van Valkenburgh 2009). In these species, the extent of the contribution of the forepaws during prey capture is such that the morphology of the forelimbs is understood to be influenced by feeding behavior (e.g., Viranta et al. 2016), whereas that of the vertebral column is not (Randau et al. 2016). The selective pressure associated with prey capture influences the morphology of the claws, especially their retractability (Gonya and Ashworth 1975; Gonyea 1978), but also that of the elbow in terms of degree of freedom at the joint (Andersson 2004), and the muscle architecture of the forelimbs in general (Cuff et al. 2016). The extended role of the forelimbs during prey capture in felids can be hypothesized to reduce the selective pressure on the skull and the jaws to generate and resist bite force. In accordance with this hypothesis, the mandibular corpus of felids is less resistant to bending than that of canids which food capture behavior relies more heavily on the capacity of the jaws and the skull to generate bite force (Biknevicius and Ruff 1992). Based on the reports and observations available to date, food capture behavior in felids involves the movements of cranial and postcranial elements, but evidence of coordination remain purely qualitative. Without quantitative evidence of coordination between the movements of the jaws with those of the neck and/or the forelimbs, the hypothesis that cranial–postcranial integration occurs during jaw prehension in felids remains speculative. Contrary to the rest of the primate lineage that typically uses hand prehension (see Whishaw and Karl, this volume), some primates use jaw prehension to capture food (Table 4.7). Most of these observations focus on the tree-gouging behaviors that these organisms perform to scrape the bark and scoop out food pieces. During tree-gouging, animals open their mouths widely, anchor their upper incisors on the trunk of a tree, and use the lower incisors to scrape upward through the bark (Vinyard et al. 2001, 2009; Dumont et al. 2011). As much as tree-gouging relies on jaw movements, it involves extensive postcranial movements. Indeed, recordings of forces applied to the substrate show that gouging performance combines bite force with forces generated by the neck and the forelimbs (Vinyard and Schmitt 2004; Vinyard et al. 2009). First, neck and forelimb movements allow the animal to push downward and into the substrate in order to anchor the upper teeth into the substrate. Second, bite force is assisted by the neck and the forelimbs pulling the skull away from the bark to facilitate scooping pieces. Finally, the neck extends to expand “the space between the […] cervical anatomy and the mandible” (Forsythe and Ford 2011, p. 2137). These observations clearly point at the fact that jaw prehension performance during tree-gouging is based on the coordination of the jaw–neck–forelimb movements, suggesting that food capture in these animals depends on cranial–postcranial integration. However, quantifying neck and forelimbs movements and testing their correlation in time and amplitude with jaw movements remains to be done to fully assess the role of cranial–postcranial integration during tree-gouging behavior.

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4.3 Perspectives: A Deeper Look into Cranial–Postcranial Integration The previous sections of this chapter have focused on identifying the presence of integration in a range of vertebrate prey-capture behaviors. However, our understanding of the role of cranial–postcranial integration during food capture can benefit from research beyond the mere testing of correlation between movements. Indeed, progress should also extend into understanding the mechanisms driving patterns of integration, such as sources of variation in integration and/or how these patterns are controlled. For example, predators can often alter their capture strategy depending on variation in the physical and textural properties of the food item (e.g., Deban 1997; Nemeth 1997b; Valdez and Nishikawa 1997; Ferry-Graham 1998; Dumont 1999; Ferry-Graham et al. 2001c; Montuelle et al. 2010, 2012b; Monroy and Nishikawa 2011). What effects do these changes in food properties have on the coordination pattern between cranial and postcranial movements? In other words, what is the extent to which cranial–postcranial integration is flexible within an organism with a given set of component traits in response to changes in food properties (sensu Wainwright et al. 2008)? If flexibility is supported, then how are these changes modulated and controlled by the sensorimotor system? Answers to these questions will be critical for understanding how animals can adapt and respond to changing feeding demands across both spatial and temporal gradients.

4.3.1 Flexibility in Response to Food Properties Kinematic integration between two anatomical elements is defined as the coordination in time and amplitude of their movements (Wainwright et al. 2008) and is traditionally exposed by testing the correlation between movements (Fig. 4.4a; reviewed in Kane and Higham 2015). Therefore, flexibility in integration will be demonstrated by significant variation in the correlation parameters within an animal and between prey types and/or properties (Fig. 4.4). For example, a bivariate correlation may become weaker (Fig. 4.4b), tighter (Fig. 4.4c), or absent (Fig. 4.4f) when compared between contexts. Multivariate and bivariate correlation-based methods have been preferred for these analyses over regressions because they are symmetric and do not assume that one trait predicts the other (e.g., Olson and Miller 1951; Berg 1960; Zelditch et al. 2004). However, correlations do not provide information about the orientation of the relationship between traits, such as the slope and intercept that can be obtained using a regression, and these additional metrics may be important for understanding nuanced differences in integration. For example, the correlation parameter may be similar across contexts, but the orientation may be divergent such that (i) the amount of change in the postcranial system that is associated with change in the cranial system might increase or decrease, resulting in differences in regression slope (Fig. 4.4d) or (ii) the use of kinematic traits may shift in magnitude for one

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or the other systems, resulting in differences in regression intercept (Fig. 4.4e). In these cases, the amount of integration (represented by a correlation coefficient) is similar, but the functional consequence may be different based on differences in orientation. Therefore, we suggest that future studies of cranial–postcranial integration also consider symmetric regression analyses, such as reduced major axis regression (Smith 2009), or analyses based on changes in the variance–covariance matrix of traits (Lande and Arnold 1983; Walker 2007) that can capture differences in correlation structure (e.g., Schluter 1996; Roff et al. 2012). These analyses could provide novel information about the ability of integration to change based on the composition of underlying traits and their correlation, as well as how the shape of the correlation structure may be influenced by factors such as specialization. Below, we discuss how each of these factors may affect the potential outcome of cranial–postcranial integration.

4.3.1.1

Flexibility of Cranial and Postcranial Movements

Because it corresponds to the first physical contact between an organism and its food, movements involved during food capture must match food properties to make the capture attempt successful. If movements are not adjusted according to food properties, the food capture attempt may fail. For example, vertebrates can modulate cranial and postcranial movements based on variation in the ability to use a given food capture method, such as when feeding above or below the water or when prey size renders prehension by an extended structure ineffective (discussed further below). Additionally, when feeding in the dark and vision is compromised, largemouth bass reduce approach speed, relying more on inertial suction to pull prey into the mouth (Gardiner and Motta 2012). These physical and sensory constraints are likely primary determinants of an animal’s flexibility during food capture, but flexibility can also be a factor of variation in properties of the prey that affect their ability to be captured. Anchovy switch from ram-filtering to high-velocity ram pursuit, increasing approach speed as well as changing whether the mouth is opened continuously or intermittently, when prey density decreases (James and Probyn 1989). Similarly, suspension-feeding sharks are predicted to switch from ram-filtering to suction prey capture, decreasing approach speed and increasing reliance on mouth expansion, when high-density prey are located in a concentrated patch rather than being more widely dispersed (Ferry et al. 2015). Finally, swimming performance during lunge capture in cetaceans is also noted to be flexible in response to food density (e.g., Hazen et al. 2015). Flexibility is also required if the prey varies in their ability to be removed from a substrate or their ability to respond to and evade a predator (discussed further below). Each of these conditions (among others) could affect the ideal strategy a predator should use to capture a food item, thereby influencing the flexibility of cranial and postcranial movements. The physical differences between water and air have been cited as a mechanism explaining a switch in feeding modes from suction underwater to biting on land in a variety of vertebrates, including amphibious fishes (Van Wassenbergh 2013; Michel

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Fig. 4.4 Hypothetical patterns of flexibility in cranial–postcranial integration during food capture behavior in response to changes in food properties. a A reference cranial–postcranial coordination pattern is characterized by three parameters defining the correlation between a cranial and a postcranial kinematic variable: slope (R), intercept (on the y-axis) and scatter (R2 ). b Compared to the reference pattern (in gray), the observations are scattered in a wider cloud (i.e., lesser R2 -coefficient; in black), indicating that the strength of the correlation between cranial and postcranial kinematics decreases. This illustrates loosened or relaxed integration. c Compared to the reference pattern (in gray), the observations are more correlated (i.e., greater R2 -coefficient; in red), indicating that the strength of the correlation between cranial and postcranial kinematics increases. This illustrates improved integration. d Compared to the reference pattern (in gray), the slope of the correlation is steeper (i.e., greater R coefficient; in green), indicating that the direction of the coordination between cranial and postcranial kinematics is modified. This illustrates modulation in the direction of the integration pattern. Note that, modulation in direction can also occur with a shallower slope of correlation (i.e., lesser R coefficient; not shown). e Compared to the reference pattern (in gray), the intercept of the correlation pattern is increased (in yellow), indicating a shift in the coordination between cranial and postcranial kinematics. Shift in cranial–postcranial integration is illustrated during jaw capture in Varanus sp whose jaw–neck coordination pattern is adjusted in response to changes in food size (see Fig. 6A in Montuelle et al. 2012b). Note that, shift in integration can also occur with a lesser intercept on the y-axis, and similarly with the intercept on the x-axis (not shown). f Compared to the reference pattern (in gray), no significant correlation is found between cranial and postcranial kinematics (i.e., R coefficient = 0; in blue). This illustrates the loss of the reference integration pattern, as in the case of Varanus sp whose cranial and postcranial movements are only coordinated during the capture of evasive prey, but not during the capture of immobile prey (Montuelle et al. 2012b). Note that, flexibility in cranial–postcranial integration pattern can fit into any of these cases or be a combination of any

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et al. 2015), salamanders (Shaffer and Lauder 1988; Reilly 1996), turtles (Summers et al. 1998; Natchev et al. 2009), snakes (Vincent et al. 2005), and mammalian pinnipeds (Marshall et al. 2008, 2014, 2015; Hocking et al. 2014). More rapid feeding movements are seen underwater where the use of suction (inertial or compensatory) is viable. Some species use biting and jaw prehension regardless of the media and movements are more similar (Stayton 2011; Marshall et al. 2015), suggesting that flexibility of cranial movements may not be required to capture food across environments. Changes in postcranial movements during food capture across environments are less often described but suggest that these may also be important for maximizing food capture. For example, a more vertical posture was observed during terrestrial feeding in catfish (Van Wassenbergh 2013). During nonfeeding behaviors, salamanders switch propulsive structures when transitioning from water to land, relying on their tail for swimming and their limbs for walking (O’Reilly et al. 2000; AshleyRoss and Bechtel 2004), suggesting a similar switch in propulsive structures may be apparent during food capture. Therefore, differences in the physical properties of air and water likely dictate flexibility of cranial and postcranial movements to account for differences in both the ability to move the mouth and body toward prey, as well as the ability to move prey toward the mouth for capture. Animals may also switch food capture modes when they are feeding within a given environment. In this case, switches between modes that require a protrusible structure to pull prey may occur when the prey become too large for these mechanisms to be effective. Some anurans, as well as Sphenodon and other cordylid lizards switch between tongue and jaw prehension capture modes depending on food size: small items are captured using tongue prehension, whereas large items are captured using jaw prehension (Gorniak et al. 1982; Anderson 1993; Anderson and Nishikawa 1993, 1996; Urbani and Bels 1995; Valdez and Nishikawa 1997; Smith et al. 1999; Reilly and McBrayer 2007; Montuelle et al. 2009; Broeckhoven and Le Mouton 2013). These switches may be due to the fact that as prey gets bigger (by weight or volume), the tongue contact surface area does not increase proportionally and prehensile force may not be sufficient to pull the prey into the mouth (Anderson 1993). A similar phenomenon is observed during prey capture in fishes, where fishes that capture larger prey tend to do so with a greater reliance on ram-feeding modes rather than using suction (Wainwright et al. 2007). For fishes relying on suction, a small mouth size is advantageous for creating a steeper pressure gradient, increasing the pulling force experienced by prey (Wainwright et al. 2007; Wainwright and Day 2007). Although the cranium can be expanded to some degrese to increase suction force and capture similar, larger prey (Ferry-Graham 1998), as the prey approach equivalency with mouth diameter, handling time increases and capture efficiency decreases exponentially (Werner 1974; Werner and Hall 1974). This can be explained by the fact that larger prey impedes the flow of water into the mouth, decreasing the effectiveness of the suction volume for pulling the prey toward the mouth (Skorczewski et al. 2010). Therefore, to capture larger prey, both fishes and terrestrial vertebrates decrease the reliance on a protrusible structure and increase the reliance on body propulsion toward or through the food item during food capture.

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In addition to prey size, and potentially confounded with this trait, prey morphology and behavior can alter the effectiveness of capture modes, resulting in changes in cranial and postcranial movements involved in food capture. For example, for aquatic predators to capture grasping or attached prey, they must either contact prey directly with the jaws using a biting strategy (e.g., Gibb et al. 2008; Hocking et al. 2014) or generate sufficient suction force to overcome the force of attachment (Holzman et al. 2007, 2012). This is in contrast to evasive prey where minimizing the deformation of the water ahead of the predator (bow wave; Holzman and Wainwright 2009) or minimizing visual cues (Domenici 2002) are used to prevent an escape response. If an escape is attempted, the predator must then overcome the swimming force of the escaping prey to successfully capture it. This is exemplified by piscivorous asp (Aspius aspius) that increase the duration and magnitude of mouth opening when prey attempt an escape response (Van Wassenbergh and De Rechter 2011). These differences in prey type demands result in differences in cranial kinematics to optimize the chances of capture. For example, a large mouth is better for capturing large evasive prey, whereas a small mouth is useful for small evasive prey, and mouth size is unrelated to capturing attached prey where demand depends on the force of attachment (Holzman et al. 2012). Additionally, postcranial kinematics can also vary in response to prey type. Food elusiveness, usually approximated with prey velocity, induces greater swimming performance of the postcranial system (e.g., Webb 1984b; Nemeth 1997b). Kelp greenling (Hexagrammos decagrammus), for instance not only modulate suction generation, but also the attack speeds and approach distance used to capture elusive and non-elusive prey types (Nemeth 1997a, b). Additionally, frogs and salamanders increasingly recruit lunge behaviors to ensure the capture of large, evasive prey (Hoff et al. 1985; Reilly et al. 1992; Anderson 1993; Maglia and Pyles 1995; Deban 1997; Valdez and Nishikawa 1997) and turtles as well as pinnipeds increase the amplitude and velocity of neck movements in response to increased prey velocity (Lauder and Pendergast 1992; Lemell and Weisgram 1997; Suzuki et al. 2009). However, head acceleration is inflexible between food types in the Australian Fur Seals (Arctocephalus pusillus doriferus; Volpov et al. 2015). Similarly, during pecking in pigeons, cranial movements (i.e., gape distance) and neck movements (i.e., head velocity) are flexible in response to pellet size (see Fig. 2 in Klein et al. 1985), demonstrating that the success of food capture in this bird species relies on the flexibility of postcranial movements. In summary, there is overwhelming evidence suggesting that many vertebrates can modify cranial and postcranial movements in response to the different contexts within which food capture might occur, but the extent of the flexibility of postcranial movements during food capture varies at the specific level and may, therefore, be a key in our understanding of the evolution of food capture. How such flexibility in postcranial and cranial movements and kinematics relate to changes in cranial–postcranial integration is less clear.

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Flexibility in Cranial–Postcranial Integration Patterns

Because integration is an emergent property of each part of the animal working in cooperation, changes in kinematics of one or more part may not equate to the flexibility of integration (Fig. 4.4d, e). Alternatively, integration may be flexible without observable changes in underlying kinematics (Fig. 4.4b, c, e). We envision two primary ways in which cranial–postcranial integration may be flexible, which are outlined below. First, animals may be flexible in whether integration is present or absent (Fig. 4.4f). In other words, animals may be flexible in the composition of cranial–postcranial integration, such that the parts that contribute to integration can be added or subtracted as necessary. For instance, in Varanid lizards, jaw–postcranial coordination was only significant during the capture of mobile prey, indicating that Varanus sp. is able to switch cranial–postcranial integration on and off depending on whether they are targeting an evasive or motionless prey item, respectively (Montuelle et al. 2012b). Other lizards and frogs are known to use tongue prehension to capture small prey items only (Gorniak et al. 1982; Anderson 1993; Anderson and Nishikawa 1993, 1996; Urbani and Bels 1995; Valdez and Nishikawa 1997; Smith et al. 1999; Montuelle et al. 2009; Broeckhoven and Le Mouton 2013). In those cases, the coordination between the tongue and postcranial movements is only activated for the capture of a subset of their dietary breadth. To capture bigger prey, the tongue— jaw–postcranial integration pattern is dropped and only jaw-postcranial integration is observed. In these animals, each prehension mode is characterized by a unique cranial–postcranial coordination pattern: during tongue prehension, the amplitude of jaw opening movements are coordinated with the amplitude of neck elevation, but during jaw prehension, the timing of head positioning is coordinated with that of forelimb flexion (Montuelle et al. 2009). Therefore, the ability to switch between tongue and jaw prehension is based on the flexibility of the tongue–jaw–neck–forelimbs coordination pattern. Similarly, a species of primate, Microcebus murinus, switches between hand prehension and jaw prehension depending on food mobility (Reghem et al. 2011; Scheumann et al. 2011; Toussaint et al. 2013, 2015). Postcranial reach and grasp movements are independent from cranial movements whereas jaw prehension relies on cranial–postcranial integration between the jaws and neck. Therefore, in this primate species, integration may be turned off during hand prehension and turned on during jaw prehension. A similar pattern might be present in aquatic vertebrates that switch between feeding modes. For example the size of the prey relative to the predator results in differential use of the postcranial components during ram feeding. With planktonic prey slow-velocity pursuit is used to filter prey from the water (Sanderson and Wassersug 1993), with small prey high-velocity pursuit is used to overrun prey (Van Leeuwen 1984), and with large prey, high-acceleration lunge is used to ambush prey (Webb and Skadsen 1980). Not only do these changes result in a shift in the use of cranial and postcranial systems, but the role of the filtering apparatus (if present) may be added or subtracted to the cranial–postcranial integration pattern depending on swim speed or prey properties (James and Probyn 1989; Haines and Sanderson 2017). Additionally,

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during suction behaviors, cranial–postcranial integration primarily involves coordination among magnitudes of mouth expansion and swim velocity (Higham 2007b; Higham et al. 2007; Tran et al. 2010; Kane and Higham 2015), whereas during biting behaviors, coordination among timing variables may be more important (Rice 2008). In this way, the changing roles of each part likely exist along a gradient, such that changes in integration rely more or less heavily on contributions from the postcranial system. Second, animals may be flexible in the magnitude and/or orientation of cranial— postcranial integration (Fig. 4.4b, c, d, e). When lizards use tongue prehension (vs. jaw prehension) or capture mobile prey (vs. immobile prey) they demonstrate tighter integration between the timing and magnitude of movements related to the head, neck, and forelimbs (Montuelle et al. 2009, 2012a, b). Additionally, during jaw prehension in Varanus, capture of both small and large prey items are characterized by similar direction of correlation between the timing of neck elevation and jaw movements, but the correlations are offset to accommodate wider jaw openings and delayed neck elevation when capturing large prey (Fig. 6A in Montuelle et al. 2012b; as illustrated in Fig. 4.4e). Similar patterns are also likely present in fishes. In both serranid and cichlid fishes, faster attack speeds and a shorter duration of the capture event (high performance) results in increased coordination within the feeding system (Liem 1978; Oufiero et al. 2012) and in centrarchids, the correlation between mouth size and swim speed is stronger in a high speed predator (Higham 2007a, b). The ability to modify the coordination pattern of cranial and postcranial movements in response to food properties may be advantageous for organisms feeding on food items varying in properties, and thus flexibility in cranial–postcranial integration may be considered a part of the suite of functional characters associated with a generalist diet (as in Nemeth 1997a, b). Flexibility in cranial–postcranial integration would indicate that different patterns of coordination may be more effective for a specific type of food. Alternatively, patterns of coordination between cranial and postcranial movements may not vary between food types and/or properties, indicating either that a single pattern of coordination allows for the successful capture of different food, or that integration at the functional level may be constrained. In fishes, specialization for feeding behaviors may constrain the range of available locomotor behaviors (Webb 1984b; Kane and Higham 2015; Ferry et al. 2015) but this may or may not be the case in other vertebrates. Therefore, specialization may result in strong patterns of integration, which could impede flexibility to respond to new feeding situations (i.e., new food properties). In contrast, animals using more flexible feeding movements may be characterized by reduced level of integration. If this is supported, then modulation of cranial or postcranial movements in response to prey properties may come at the cost of integration (Kane and Higham 2015). Assessing the flexibility of cranial–postcranial integration will be important for understanding dietary specializations within and between species.

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4.3.2 Sensorimotor Control of Integration Quantifying the pattern of correlation between cranial and postcranial movements during food capture provides evidence for the integrative nature of food capture behavior but the study of integration cannot be limited to investigating patterns, and indeed their variability. It has a lot to gain from the study of the processes allowing integration. Integration between two or more body parts necessitates neural pathways allowing for the coordination of the positioning and the movements of each element with respect to each other. Consequently, we propose that integration between two anatomical elements can be demonstrated by studying the effects of sensory deprivation from one element on the movements of the other elements. The coordination between movements of two anatomical elements implies that at any point in time, each element is dependent on the position of the other element(s), as well as on the characteristics of the movements they are engaged into. Thus, an integrative performance can be proposed to rely on the constant exchange of sensory and motor information between elements. As such, integration can be hypothesized to depend on the sensorimotor control of coordination. According to this hypothesis, we propose that the loss of sensorimotor information from at least one of these elements can be expected to negatively affect integrative performances and behaviors. Such an approach has been conducted by testing the effects of the transection of the different nerves innervating the hyolingual apparatus on the movements of the tongue but also those of the jaws in anurans and squamate lizards (e.g., Comer and Grobstein 1981; Nishikawa and Roth 1991; Deban and Nishikawa 1992; Nishikawa and Gans 1992; Anderson and Nishikawa 1993, 1996; O’Reilly and Nishikawa 1995; Meyers and Nishikawa 2000; Schaerlaeken et al. 2007). This series of the paper explains that nerve transection investigates the hypothesis that “a particular muscle is either necessary or sufficient for the performance of a given motor behavior. A muscle is necessary for a given movement if denervation of that muscle alters the kinematics of the movement or eliminates the movement entirely. A muscle is sufficient for a given movement if denervation of other relevant muscles has no effect on the kinematics of the movement” (Nishikawa and Roth 1991, p. 218). In these studies, focusing on food capture in anurans, sensory loss from the hyolingual apparatus (experimentally generated by nerve transection) is shown to not only affect the movements of the tongue itself but also those of other cranial elements such as those of the jaws. The conclusions of this wealth of literature are twofold. First, it shows that tongue muscles alone are not sufficient for food capture in anurans, and neither are jaw muscles alone. Second, both tongue and jaw muscles are necessary for food capture behavior. Even more so, some of these studies noted that nerve transection affects the timing of jaw movements with respect to those of the tongue, thus suggesting that sensory information from the hyolingual apparatus “coordinates” movements from the other cranial elements such as the jaws (Anderson and Nishikawa 1996, p. 760). Consequently, in these organisms, integration with the cranial system is understood to rely on the sensory information from the tongue. As the effects of sensory loss from the tongue on jaw–tongue coordination shows

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integration within the cranial system, we propose that this approach can be extended to the study of cranial–postcranial integration during food capture. Supporting this is the fact that sensory loss from the hyolingual apparatus (i.e., sensory loss from a cranial element) affects head rotation in anurans (Anderson and Nishikawa 1996). We hypothesize that in organisms whose food capture performance is based on cranial–postcranial integration, the coordination of cranial and postcranial movements is made possible by the exchange of sensory information between cranial and postcranial elements. Based on this hypothesis, the study of sensory loss can demonstrate cranial–postcranial integration during food capture. Indeed, we argue that cranial–postcranial integration will be demonstrated in cases where (i) neither cranial or postcranial movements are found sufficient on their own for food capture performance and (ii) both cranial and postcranial movements are found necessary to food capture performance. Alternatively, if movements from one element (i.e., either cranial or postcranial) is immune to sensory loss from another element, then it will indicate that (i) movements of the former are sufficient to food capture performance and (ii) movements of the latter are not necessary, thus invalidating the integrative nature of food capture in this case. Accordingly, we suggest removing the sensory pathways from one element and study whether, and if so, to what extent, the positioning and movements of other anatomical elements cope with the lack of sensory information. In particular, we expect sensory loss from the cranial elements responsible for identifying food properties to be critical. The integrative nature of food capture performance will be demonstrated in the case sensory loss from the cranial elements will alter (i) the movements of the postcranial elements themselves, as well as (ii) the coordination pattern between the cranial and postcranial movements. Alternatively, food capture performance will be shown to not rely on cranial–postcranial integration if the postcranial movements and the cranial–postcranial coordination pattern are similar (i.e., not significantly different) with or without the sensory information from the cranial elements.

4.4 Synthesis and Conclusions This chapter presents the state of our understanding of cranial–postcranial integration during food capture behavior in vertebrates. Cranial–postcranial integration may not be a generalized phenomenon across vertebrates, but the review of quantitative data and qualitative observations shows that in a large variety of aquatic and terrestrial vertebrates, food capture behavior is not solely based on cranial movements but rather benefits from the contribution of postcranial movements in a coordinated manner. For instance, all modes of aquatic food capture seem to include a component performed by the postcranial system. The fin and tail movements are indeed used to generate acceleration, maneuvering and/or braking while being finely coordinated in time and amplitude with the jaw movements responsible for ram feeding, suction, and biting in fishes, as well as in many secondary aquatic organisms that feed underwater. For food capture in terrestrial organisms, cranial–postcranial integration may play a key

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role for the success of lunge movements during tongue prehension in organisms in which hyolingual apparatus is not specialized for reaching over long distance, such as in anurans and squamate lizards. In contrast, the organisms in which hyolingual apparatus is specialized for prehension, lunge movements are not necessary and thus no cranial–postcranial integration may occur. Organisms using jaw prehension to capture food are arguably the most likely to benefit from cranial–postcranial integration because the accurate positioning in time and space of the skull thus the jaws with respect to the food item can be hypothesized to rely heavily if not entirely on postcranial movements such as those of the neck, of the forelimbs and of the hind limbs. Regarding secondary aquatic organisms, how cranial–postcranial integration is convergent with aquatic food capture in fishes, given the constraints of the food capture modes of their terrestrial ancestors, remains to be further investigated. The study of cranial and postcranial movements during food capture, and indeed whether they are coordinated in time and/or in amplitude, in secondary aquatic organisms will further our understanding of the role of cranial–postcranial integration in the evolution of food capture behavior in vertebrates. In organisms in which food capture relies on cranial–postcranial integration, several questions arise for our understanding of the evolutionary relevance of such functional characteristics. At the morphological level, the main function of postcranial elements is locomotion and as such, it can be expected that the selective pressure associated with locomotion are the ones affecting postcranial morphology the most. However, in organisms which postcranial elements are also involved in food capture performance, how do the locomotor and feeding functions of the postcranial morphology coexist? In other words, how do locomotor and feeding functions compete with and/or support each other? Are postcranial traits modular, so that some parts contribute to locomotor behaviors whereas others are dominant in feeding behaviors? In aquatic vertebrates especially, the locomotor function of the postcranial morphology to generate swimming velocity may directly support feeding purposes during ram feeding by closing the distance with prey. On the other hand, forward movement underwater generates a fluid wave in front of the mouth that pushes the food item away from the predator, potentially decreasing feeding success, unless the cranial system can compensate for this effect by generating compensatory suction. As such, a trade-off may be revealed between the locomotor and feeding function of the postcranial system. If so, how, and to what extent, do changes in locomotor functions affect feeding functions, and vice versa. At the performance level, integrating the movement capabilities of the postcranial elements with those of the cranial elements may expand the range of food types and properties that one individual is able to exploit to survive or may increase the effectiveness of the cranial elements on a particular food type. As such, cranial–postcranial integration during food capture can provide individuals with an advantage over their competitors within and outside of their own species. This suggests that cranial–postcranial integration may play a role in selection and adaptation associated with new dietary niches. Alternatively, relying on the movements of multiple elements in a coordinated manner may be a constraint at the evolutionary level because it can hinder the ability to change rapidly,

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and thus adapt, in response to changes in environmental conditions (e.g., changes in the availability of one or more particular food types and/or properties). To date, the feeding system has been considered to be mostly synonymous with the cranial system. In this chapter, we argue that feeding behavior should be more of an organismal concept that includes elements of the cranial and postcranial systems. Extending this idea provides insight into the constraints that organisms may be faced with during prey capture. Diet has been shown to have significant consequences on the shape and function of the cranial elements to a point that various patterns of morphofunctional adaptations in response to dietary specialization have been demonstrated in the cranial system in multiple vertebrate lineages (reviewed in Schwenk 2000a; e.g., Sacco and Van Valkenburgh 2004; Werth 2007; Mori and Vincent 2008; Huber et al. 2009; Figeirido et al. 2013; Jones et al. 2013; Gutzwiller and Hunter 2015; Kienle et al. 2015; Dumont et al. 2016; Fabre et al. 2016; Dollion et al. 2017; Melstrom 2017; Solé and Ladévèze 2017). If postcranial movements contribute to the success of food capture behavior, then one can hypothesize that postcranial elements may also carry adaptation in response to diet. Accordingly, the morphology of postcranial elements has been shown to carry an adaptive signal corresponding to different prey-capture behavior in a limited array of vertebrates (e.g., Gonya and Ashworth 1975; Gonya 1978; Webb 1984a, b; Russel and Bryant 2001; Drucker and Lauder 2002; Argot 2003; Andersson 2004; Higham 2007b; Collar et al. 2008; Meachen-Samuels and Van Valkenburgh 2009; Figueirido and Janis 2011; Janis and Figueirido 2014; Viranta et al. 2016). Adaptive pressures associated with diet may thus not be restricted to the cranial system only, but rather apply at the organismal level. Widening the breadth of our understanding of food capture behavior, and feeding behavior in general, and beyond the cranial system, it is likely to provide fellow researchers with exciting new research avenues to understand the evolution of feeding in vertebrates. Acknowledgements We would like to thank Prof. Vincent L. Bels for inviting us to contribute to this volume. Preparation of this manuscript by S. J. Montuelle was supported by grants from the National Science Foundation (MRI DBI 0922988 and IOS 1456810), the National Institute of Health (1R15DE023668-01A1), and the Heritage College of Osteopathic Medicine Research & Scholarly Affairs Committee to Prof. S. H. Williams and Prof. S. M. Reilly at Ohio University. Preparation of this manuscript by E. A. Kane was supported by the National Science Foundation Postdoctoral Research Fellowship in Biology (DBI-1401560) to E. A. Kane while at Colorado State University.

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Werner EE (1974) The fish size, prey size, handling time relation in several sunfishes and some implications. J Fish Res Board Can 31:1531–1536 Werner EE, Hall DJ (1974) Optimal foraging and the size selection of prey by the bluegill sunfish (Lepomis macrochirus). Ecology 55:1042–1052 Werth AJ (2000a) A kinematic study of suction feeding and associated behavior in the long-finned pilot whale, Globicephala melas (Traill). Mar Mammal Sci 16:299–314 Werth AJ (2000b) Feeding in marine mammals. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 487–526 Werth AJ (2007) Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat Rec 290:546–568 Werth AJ, Potvin J (2016) Baleen hydrodynamics and morphology of cross-flow filtration in balaenid whale suspension feeding. PLoS ONE 11:e0150106 Westneat M (2006) Skull biomechanics and suction feeding in fishes. In: Shadwick RE, Lauder GV (eds) Fish biomechanics. Elsevier, San Diego, pp 29–75 Whishaw IQ (1996) An endpoint, descriptive, and kinematic comparison of skilled reaching in mice (Mus musculus) with rats (Rattus norvegicus). Behav Brain Res 78(2):101–111 Whishaw IQ, Coles BL (1996) Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behav Brain Res 77:135–148 Whishaw IQ, Pellis SM (1990) The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component. Behav Brain Res 41(1):49–59 Whishaw IQ, Dringenberg HC, Pellis SM (1992) Spontaneous forelimb grasping in free feeding by rats: motor cortex aids limb and digit positioning. Behav Brain Res 48(2):113–125 Whishaw IQ, Sarna JR, Pellis SN (1998) Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res 96:79–91 Whiteside MA, Sage R, Madden JR (2015) Diet complexity in early life affects survival in released pheasants by altering foraging efficiency, food choice, handling skills and gut morphology. J Anim Ecol 84:1480–1489 Wilga CD, Motta PJ (2000) Durophagy in sharks: feeding mechanics of the hammerhead Sphyrna tiburo. J Exp Biol 203:2781–2796 Wochesländer R, Hilgers H, Weisgram J (1999) Feeding mechanism of Testudo hermanni boettgeri (Chelonia, Cryptodira). Neth J Zool 49:1–13 Wöhl S, Schuster S (2006) Hunting archer fish match their take-off speed to distance from the future point of catch. J Exp Biol 209:141–151 Wöhl S, Schuster S (2007) The predictive start of hunting archer fish: a flexible and precise motor pattern performed with the kinematics of an escape C-start. J Exp Biol 210:311–324 Woodward BL, Winn JP, Fish FE (2006) Morphological specializations of Baleen whales associated with hydrodynamic performance and ecological niche. J Morphol 267:1284–1294 Young BA (2010) How a heavy-bodied snake strikes quickly: high-power axial musculature in the puff adder (Bitis arietans). J Exp Zool 313A:114–121 Young BA, Phelan M, Jaggers J, Nejman N (2001) Kinematic modulation of the strike of the Western diamondback rattlesnake (Crotalus atrox). Hamadryad 26(2):288–321 Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists: a primer. Elsevier academic Press, San Diego, CA Zweers GA (1982) Pecking of the Pigeon (Columba livia L.). Behaviour 81(2):173–230

Chapter 5

Transitions from Water to Land: Terrestrial Feeding in Fishes Sam Van Wassenbergh

Abstract Several species of fish live at the interface between water and land, and have evolved ways to cope with the problems of an ancestrally aquatic feeding system that needs to function on land. Studies of the kinematics of terrestrial feeding by these amphibious fishes allow us to identify the mechanical challenges and solutions to successfully make this environmental transition. In turn, this can help us to generate hypotheses on the evolutionary history of early tetrapods related to their transition to terrestrial feeding. In this chapter, an overview is given of the results of studies that have analyzed the kinematics of terrestrial feeding in four amphibious fishes. These studies showed how these fishes establish and maintain a stable body posture to allow the capture of food in the terrestrial environment, how their jaws grab the groundbased food, and how this food is transported to the back of the mouth cavity. Finally, in the light of these findings, an overview is provided of the current hypotheses on how terrestrial feeding could have evolved in early tetrapods.

5.1 Introduction When transitioning to a life on land, ancestrally aquatic organisms are faced with numerous challenges caused by the physical and chemical differences between water and air (e.g., Dejours 1975; Liem 1990; Graham 1997; Laurin 2010; Wright and Turko 2016). Since air is about 800 times less dense and 50 times less viscous than water, buoyancy forces on an animal’s body become negligibly small relative to the opposing gravitational forces, and both frictional resistance of the air and the work needed to overcome inertia strongly decrease. This has drastic effects on the mechanics of movement: transitioning to the terrestrial environment requires morphological changes to support the body and to generate propulsive forces (e.g., Pace and Gibb 2009; Gibb et al. 2013). Not S. Van Wassenbergh (B) Département Adaptations du Vivant, Muséum National D’Histoire Naturelle, UMR 7179 CNRS, 57 rue Cuvier, Case Postale 55, 75231 Paris Cedex 05, France e-mail: [email protected] Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Antwerp, Belgium © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_5

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only biomechanical problems need to be coped with by the musculoskeletal system, many other organ systems are challenged as well—such as vision, hydration/desiccation, CO2 retention and acidosis, and ion-balance regulation (Wright and Turko 2016). Despite these numerous challenges, evolution within one group of lobefinned fishes, the Tetrapodomorpha including iconic ‘transitional’ fossils such as Eusthenopteron, Tiktaalik, Ichthyostega, and Acanthostega, have successfully overcome these challenges to give rise to the four-legged animals (Tetrapoda), presumably in the upper Devonian (George and Bliek 2011). This transition of early tetrapods from living in water to living on land was a critical event in the evolution of vertebrates, as it subsequently resulted in the radiation and worldwide colonization of tetrapods (Clack 2002a; Long and Gordon 2004; Laurin 2010). In search for the morphological characteristics that allowed the early tetrapods to become terrestrial, this transition has been given plenty of attention in paleontological studies (e.g., Jarvik 1980; Coates and Clack 1995; Ahlberg et al. 2005; Daeschler et al. 2006; Niedzwiedski et al. 2010; Shubin et al. 2014; Porro et al. 2015). Other ancestrally aquatic vertebrate taxa have also evolved ways to cope with life on land. These are the amphibious fishes, i.e., fish that naturally spend part of their life on land. A recent review article counted more than 200 extant species of amphibious fishes spanning 40 families and 17 taxonomic orders (Wright and Turko 2016). Given the challenges for transitioning from water to land, the large number of independent evolutions toward partly terrestrial life in fishes is impressive. However, the terrestrial life of many of these species is limited to brief emersions to migrate over land. In contrast, some species of blennies (Blenniidae) can be considered true land animals as they spend the majority of their time on land (Ord and Hsieh 2011). In order to transition to a fully terrestrial life, not only the locomotor system needs to suit the new environment, but also the feeding system. A typical ancestrally aquatic feeding system, as observed in a fish with a generalized morphology (e.g., a cichlid or a trout), will be confronted with several problems to function in the terrestrial environment (Heiss et al. 2018). In the aquatic environment, virtually all fish generate suction to transport food toward, into, and through the mouth cavity (i.e., the buccopharyngeal cavity). Suction involves a flow of water into the mouth that is powered by a coordinated sequence of movements that results in anterior-to-posterior waves of expansion and contraction of the buccopharyngeal cavity (e.g., Muller and Osse 1984). More details on how a generalized suction-feeding apparatus works in a fish can, for example, be found in the recent review article by Day et al. (2015). On land, however, flows of air are too weak to transport food. It is calculated that the buccopharyngeal expansion has to be 28 times faster to produce a flow of air with the same kinetic energy than a flow of water (Van Wassenbergh 2013). Muscles simply cannot reach such a large increase in speed (Hill 1938). Consequently, we can safely consider the terrestrialization of aquatic vertebrates to be importantly constrained by the biomechanical problems of aquatic feeders to transition to terrestrial feeders (Heiss et al. 2018). Consequently, due to challenges of terrestrial feeding for a fish, it is not surprising that only a fraction of the many species of amphibious fishes have been observed

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to capture their food on land. Records of terrestrial feeding exist for the reedfish (Erpetoichthys calabaricus, Polypteridae; Sacca and Burggren 1982), the four-eyed fishes (Anablepidae; Zahl et al. 1977), the eel catfish (Channallabes apus, Clariidae; Van Wassenbergh et al. 2006; Van Wassenbergh 2013), blennies (Blenniioidei; Rao and Hora 1938; Nieder 2001), and mudskippers (Oxudercinae; Stebbins and Kalk 1961; Sponder and Lauder 1981). Studies of how these amphibious fishes manage to feed on land and underwater provide us with valuable information on the potential solutions to feed in both the aquatic and terrestrial environments. In turn, this can help us to generate hypotheses on the evolutionary history of early tetrapods related to their transition to terrestrial feeding (Ashley-Ross et al. 2013).

5.2 Mudskippers Mudskippers (Gobiidae: Oxudercinae) are typically found in close association with tidal sand flats from mangrove borders and estuaries of the Indo-West Pacific region (Stebbins and Kalk 1961; Murdy 1989) where they opportunistically feed on diverse invertebrates (e.g., Colombini 1996; data for Periophthalmus sobrinus). Foraging takes place entirely out of the water (Colombini et al. 1995). Aspects of the kinematics of terrestrial prey capture were first analyzed by Sponder and Lauder (1981) for Periophthalmus koelreuti. Later, Michel et al. (2014) focused on the function of the jaws during prey capture in Periophthalmus barbarus. These studies showed how the mudskipper takes up a position at only a few centimeters in front of the prey. Its head is lifted off the ground by the support from both the pectoral fins and the pelvic fins (Fig. 5.1a). Next, the mudskipper pivots forward on its pectoral fins (Fig. 5.1b) to bring the opening mouth down toward the substrate where the prey lies (Fig. 5.1c). The jaws then close on the prey while the mouth is still held against the ground (Fig. 5.1d). Finally, the pectoral fins are moved forward to take over the support from the pelvic fins, and the head is elevated to the rest position (Fig. 5.1e). Michel et al. (2015a) noted for P. barbarus that from the moment the mouth opens (Fig. 5.1b), a convex meniscus of water becomes visible at the mouth aperture (Fig. 5.2a). This water further protruded out of the mouth, and just before the jaws were placed around the prey, the water contacted the prey and spread along the surface surrounding the prey (Fig. 5.2b). While the jaws were closing and the prey was engulfed, part of the expelled water was sucked back into the buccal cavity (Fig. 5.2c).

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Fig. 5.1 Overview of the different successive stages during prey capture by Periophthalmus. Drawings are based on Michel et al. (2015a)

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Fig. 5.2 Sequence of motions illustrating the hydrodynamic tongue function in Periophthalmus barbarus in lateral view (top row) and ventral view (bottom row). Gray areas denote the water that is protruding out of the mouth. Drawings are based on Michel et al. (2015a)

The expelling of water is more than just a side effect of opening the mouth when water is retained in the buccopharyngeal cavity on land: water is actively protruded and retracted to assist the capture and transport of the prey (Michel et al. 2015a). Before the lunge at the prey, the small, valvular slits at the dorsoposterior side of the opercula are closed (Fig. 5.2a). Consequently, the connected opercular and buccal volumes could be regarded as a vessel with a small opening at the side of the mouth. While the mudskipper accelerates forwards and pivots down toward the prey, the left and right gill covers are adducted (Fig. 5.2a), and the hyoid is elevated (Fig. 5.2b). Because water is incompressible, the decrease in volume resulting from these motions resulted in a flow of water anteriorly toward the mouth. After this, the head volume increased by hyoid depression and opercular abduction (Fig. 5.2c) causing suction to be generated. As this ‘protrusion’ and ‘retraction’ of buccal water shows kinematic and functional resemblance to tongue movement during feeding in lower tetrapods, it is referred to as a ‘hydrodynamic tongue’ (Michel et al. 2015a). X-ray videos showed that this hydrodynamic tongue allows P. barbarus to engulf and transport prey to the pharyngeal jaws in a single cycle of the gape and hyoid. As field observations showed that the mudskipper’s snout often temporarily disappears in the mud during feeding (Stebbins and Kalk 1961), sucking mud along with the water retained in the mouth cavity can help to transport prey deep into the buccopharyngeal cavity (mud and detritus were found in stomachs; Ravi 2013). The mudskipper’s capacity to terrestrially transport the food to the esophagus also explains why mudskippers can eat multiple prey items without needing to return to the water for swallowing (Sponder and Lauder 1981; Michel et al. 2015a). Although Sponder a Lauder (1981) observed in P. koelreuti that water drained out of the open mouth onto the ground during feeding, they attributed the intraoral transport capacity during terrestrial feeding on worms exclusively to the anterior–posterior movement of the pharyngeal jaws. X-ray video images of P. barbarus, in contrast, show that the pharyngeal jaws always stay

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posterior to the orbits (Fig. 7 in Michel et al. 2014), and are therefore not used to transport the prey from the oral jaws. Field observations suggest that variation exists between species in the amount of water carried on land in the buccopharyngeal cavity as well as the frequency of water intake (Stebbins and Kalk 1961 vs. Gordon et al. 1968). Interspecific variability in the usage of the hydrodynamic tongue may thus exist, but further investigations would be needed to confirm this. The movement of the oral jaws of mudskippers is also important to effectively, and quickly, grab or scoop up prey from the ground. As for most Perciform fishes, both the upper jaw (premaxilla, maxilla, and palatine bones) and lower oral jaw (anguloarticular, retroarticular, and dentary bones, and Meckel’s cartilage) are mobile (Fig. 5.3a). Early during the launch at the prey, the premaxilla rotates dorsally (Fig. 5.3b) and protrudes downward over the prey (Fig. 5.3c). Meanwhile, the dentary is rotated ventrally over an angle exceeding 90° (Fig. 5.3b, c), which most likely involves bending in Meckel’s cartilage that connects the dentary with the anguloarticular (Michel et al. 2014). The mouth aperture plane is now approximately parallel with the ground surface, and is moved vertically down over the prey (Fig. 5.3c). Finally, a fast-closing rotation of the lower jaw will close the mouth and scoop the prey into the mouth. Coupled with this action, the upper jaw returns back into its resting position (Fig. 5.3d).

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Fig. 5.3 Motion sequence of the oral jaws during terrestrial prey capture in Periophthalmus barbarus. Drawings are based on Michel et al. 2014. AARA  anguloarticular and retroarticular, BC  braincase, DENT  dentary, F  food, MAX  maxilla, PAL  palatine, PREM  premaxilla, SUS  suspensorium

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5.3 Eel Catfish Within the family of air-breathing catfishes (Siluriformes: Clariidae), several species from Central and West Africa have an eel-like, elongated body (Boulenger 1907; Cabuy et al. 1999). Channallabes apus is the most extremely anguilliform species of all eel-like Clariidae, has no pectoral fins, and is commonly named as the eel catfish. This species inhabits muddy swamps, and, like other Clariidae, has long dorsal and anal fins, and a dorsoventrally flattened head. A study showing that the natural diet of C. apus mainly consisted of terrestrial insects (Huysentruyt et al. 2004) was quickly followed by the discovery of its terrestrial feeding capacity (Van Wassenbergh et al. 2006). A more detailed analysis of the kinematics of terrestrial feeding in C. apus followed later (Van Wassenbergh 2013). Laboratory observations of terrestrial feeding also exist for a closely related species, Gymnallabes typus (Van Wassenbergh et al. 2017). After leaving the water, when food touches one of the tactile barbels of C. apus (Fig. 5.4a, arrow 1), the front part of the body is lifted (Fig. 5.2b, arrow 2) and the head is bent downwards (Fig. 5.4b). Alternatively, the eel catfish will scan the ground surface by moving the open mouth and barbels over the ground while already taking the posture of Fig. 5.4b (Van Wassenbergh 2013). While maintaining this characteristic head-down posture, the mouth opening is increased (Fig. 5.4c, arrow 4) and the hyoid starts to depress the floor of the mouth cavity (Fig. 5.4c, arrow 3). The hyoid continues its expansive movement (Fig. 5.4d, arrow 6), while the mouth is closing to grab the prey in between its upper and lower jaw (Fig. 5.4d, arrow 5). Finally, the catfish abandons the trunk-lifted posture (Fig. 5.4d) and slips back into the water where it sucks the food further into the buccopharyngeal cavity. Unique videos of this species moving and capturing prey on a sandy substrate were shown in the wildlife documentary Wild Congo—River of Monsters released in 2014 by Blue Planet Film (directed By Thomas Behrend). The oral jaws of clariid catfish (Fig. 5.5a) is mechanically simpler than those of mudskippers (Fig. 5.3). The premaxilla of the catfish is firmly attached to the mesethmoid of the braincase (Devaere et al. 2001), while the maxilla serves as the base support of the maxillary barbel (Diogo et al. 2003). Consequently, the upper jaw does not have the capacity to protrude: it moves along with the braincase. The lower jaw consists of the same skeletal elements as those observed in the mudskipper (Fig. 5.3a), but no noticeable sagittal-plane bending could be observed on X-ray videos of C. apus or other clariid species during aquatic feeding (Van Wassenbergh et al. 2007). Despite these simplified mechanics, C. apus manage to firmly grasp food with its numerous teeth of the upper jaw (premaxilla and vomer) and the lower jaw (dentary). Yet, it takes sometimes a few repetitive mouthopening cycles before the bite is successful (Van Wassenbergh 2013). The widest mouth opening is achieved only when also the hyoid and cleithrum are retracted (Fig. 5.5b). This motion sequence strongly resembles that of aquatic suction feeding (Van Wassenbergh 2013).

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Fig. 5.4 Sequence of events during terrestrial capture of an upside-down beetle by the eel catfish Chanallabes apus. The total duration is about 0.25 s. Forward movement of about one head length occurs from a to d. The animal is moving back into the water in e and onwards. The arrows indicate the following events: 1. contact between prey and barbel; 2. lifting of the trunk; 3. start of hyoid depression; 4. start of increased opening of the mouth; 5. maximal hyoid depression; 6. mouth closing. Drawings are based on Van Wassenbergh (2013)

Two aspects of the postcranial system are assumed to be critical to allow the eel catfish to put the body into its typical, lifted-trunk, nose-down posture. First, a certain degree of dorsoventral flexibility in the postcranial system is needed (Van Wassenbergh et al. 2006). There does not appear to be a single joint or region that is specifically responsible for the nose-down pitching of the head: it is caused by accumulation of bending from a relatively long region (certainly more than one head length) behind the head (Van Wassenbergh 2013) (Fig. 5.5a). Second, in order to make a dorsoventral arc in the anterior part of the body, maintaining balance will become a problem. To cope with this (without strong pectoral fins as in mudskippers), support is provided by the posterior end of the body (not shown in Fig. 5.5a). This part of the body is still in contact with the ground and/or water. Consequently, the fact that eel catfish have a relatively long body with respect to the head (Van Wassenbergh et al. 2017), seems essential to provide the support to stably attain and maintain its terrestrial feeding posture (Fig. 5.5).

5.4 Reedfish Reedfish Erpethoichthys calabaricus are known to be able to capture prey on land in a simulated natural environment (Sacca and Burggren 1982). Together with the Polypterus species (bichirs), it belongs to the family of Polypteridae. Since Polypteridae are the most basal family in the phylogeny of ray-finned fishes (Actinopterygii) (Near et al. 2012), these are the extant fish that are closest to the common ancestor

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Fig. 5.5 Lateral view on the bony skeleton of Channallabes apus (anterior body part) in the typical nose-down feeding posture, indicating the functional units of the jaw system a. The movement of these functional units during mouth opening are drawn in b. Drawings are based on Van Wassenbergh et al. (2006). AA  anguloarticular, BC  braincase, BR  branchiostegal rays, CH  ceratohyal (hyoid), CL  cleithrum, DENT  dentary, MAX  maxilla, OP  operculum, SUS  suspensorium, UJ  upper jaw

of actinopterygians and sarcopterygians. For this reason, they are of special interest in the light of the early evolutionary history of sarcopterygians the first tetrapods (Standen et al. 2014). Reedfish inhabit swamps and rivers in Western Africa. Their elongate, eel-like body shape (Cleason et al. 2007) resembles that of the eel catfish. In contrast to the eel catfish, they do have relatively small pectoral fins which they use during slow aquatic locomotion, but not during terrestrial locomotion (Pace and Gibb 2011). Although a detailed quantitative kinematical analysis of terrestrial capture of prey by the reedfish is not available in the literature, a recent study presented a quantitative description of the motion sequence observed based on high-speed videos (Van Wassenbergh et al. 2017) (Fig. 5.6). These descriptions were sufficient to conclude that terrestrial prey-capture behavior in reedfish is similar to that of the eel catfish (Van Wassenbergh et al. 2017): the reedfish uses a lifted trunk and downward inclined head to capture ground-based prey. Buccal expansion and compression during mouth opening are also present. Reedfish thus similarly use the ground support and flexi-

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Fig. 5.6 Typical, inclined head posture during searches for prey on land by Erpethoichthys calabaricus. Drawing based on Van Wassenbergh et al. 2017

bility of an eel-like body to perform the trunk elevation and dorsoventral flexion of the anterior trunk region (Van Wassenbergh et al. 2017).

5.5 Largescale Foureyes The largescale foureyes (Anableps anableps) are known to jump and feed on mudbanks (Zahl et al. 1977; Brenner and Krumme 2007). In contrast to the previously described amphibious fishes, this South-American cyprinodontiform species does not have an eel-like body like the eel catfish or reedfish, nor does it have the strongly developed pectoral fins of a mudskipper. Cyprinodontiforms, the group that also includes popular aquarium fishes like guppies (Poecilia reticulata), have a fusiform body with pectoral fins that do not have the capacity to be depressed ventrally to interact with the ground (Boumis et al. 2014). How then does A. anableps manage to capture food on land? Michel et al. (2015b) showed that A. anableps completely relies on the movement of its jaws. Similar to the mudskipper, the lower jaw rotates over a large angle (sometimes up to 90°; Michel et al. 2015b). In contrast to the mudskipper, however, the upper jaw manages to protrude forward and then downward to meet the depressed lower jaw at a ventral position (Fig. 5.7). This jaw movement causes the plane of the mouth aperture to be reoriented to become approximately parallel with the ground, and allows A. anableps to swiftly grab ground-based prey. Next, A. anableps will always return to the water for further intraoral transport of its food (Michel et al. 2015b). Cyprynodontiformes are known to use their protrusible premaxilla to capture individual prey items from the water column or of the substrate (Hernandez et al. 2008; Ferry-Graham et al. 2008). Their jaw protrusion mechanism differs from the perciform type illustrated earlier for the mudskipper (Fig. 5.3) where the anterior tip of the premaxilla was first rotated dorsally, and the retraction during mouth closing was caused by linkages to the adducting lower jaw. In cyprinodontiforms, the premaxilla is first pulled forward by its ligamentous connection with the depressing lower jaw. Next, the mouth-closing action by the premaxilla can be controlled independently from the adduction of the lower jaw because part of the adductor mandibulae complex, the A1 division, inserts on the maxilla. In turn, the maxilla is connected by

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Fig. 5.7 Motion sequence of the terrestrial capture of a piece of fish by largescale foureyes (Anableps anableps) from lateral view. The names of the displayed bones are given in the enlarged drawing on the bottom. Drawings are based on Michel et al. (2015b)

a ligament to the ventral part of the premaxilla. This system gives cyprinodontiforms more flexibility to aim their bite without having to move their entire body. Aided by stretchable, initially folded skin between the maxilla and the premaxilla, a more extreme anterior–ventral protrusion of the premaxilla is possible in A. anableps compared to other cyprinodontiform species (Michel et al. 2015b).

5.6 Evolution of Terrestrial Feeding in Early Tetrapods 5.6.1 Inferences from Tetrapodomorph Fossils When and how tetrapods first evolved the capacity to feed on land remains an open question. During the last decade, however, several studies on this topic were published based on comparative functional morphology. First, patterns of sutural morphology of the skull roof, the fibrous joints between skull bones, were linked to feeding modes (Clack 2002b; Markey and Marshall 2007). Basing on the hypothesis that taxa that perform aquatic feeding should exhibit similar sutural morphologies, and that at least some of these sutures would be quantitatively different from those found in terrestrial taxa, skull sutures from tetrapodomorph fossils Eusthenopteron and Acanthostega from the Devonian age were analyzed. The primitive ray-finned fish Polypterus endlicherii (Polypteriidae) was used as a reference for aquatic suction feeder (Markey et al. 2006), and the Permian terrestrial temnospondyl Phonerpeton (Dissorophoidea) as a terrestrial tetrapod. Whereas, the finned tetrapodomorph Eusthenopteron showed resemblance with Polypterus, the limbed tetrapodomorph Acanthostega resembles Phonerpeton. This analysis suggests that a shift from suction feeding to biting occurred (presumably in the water or near the water’s edge; Markey and Marshall 2007) around the fin-to-limb transition (Fig. 5.8b).

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Fig. 5.8 a Change trough time of the total disparity (sum of variances of 10 scale-independent variables) in the mechanical characteristics of the mandible based on a large sample of fossils from the time of the rise of tetrapods (see Anderson et al. 2013). The gray envelope denotes the 95% confidence interval. Note that, the variation in the mechanical properties of the mandible remained approximately constant up to about 315 million years ago, which includes a relatively long period after the origin of weight-supporting limbs in the late Devonian age. Below, a partial disparity graph shows the relative contributions of five groups (tetrapodomorph fishes, digited stem tetrapods, temnospondyls, lepospondyls, and amniotes) to the overall disparity (top graph) over time (after Anderson et al. 2013). The increase in jaw disparity during the Pennsylvanian is caused by evolution within the amniotes, and is hypothesized to be linked to the origin of herbivory (Anderson et al. 2013). b Shows a comparison of the mechanical properties of the skull roof sutures of a basal actionopterygian fish (Polypterus), a tetrapodomorph fish (Eusthenopteron), a presumably aquatic stem tetrapod (Acanthostega), and a Permian temnospondyl (Phonerpeton) (after Markey and Marshall 2007). This study showed that the suture morphologies of Acanthostega are inconsistent with the hypothesis that it captured prey primarily by means of suction (as in Polypterus), which suggests that it may have bitten prey directly at or near the water’s edge. In contrast to (A), sutural morphology does suggest a shift in feeding mechanics (presumably toward a ‘biting’ mode of feeding) already emerging in aquatic stem tetrapods

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It would be logical to see this presumed shift from suction feeding to biting as inferred from cranial sutures to be reflected in the morphology of the mandible. However, Anderson et al. (2011, 2013) surprisingly found that diversification the tetrapod mandible lagged behind the evolution of terrestriality. Relatively little changed in the mandible over the ~70–80 million years interval following the origin of the digit-bearing limb until the time when herbivory evolved in amniotes (Fig. 5.8a). These results were supported by a study on the outline shape (2D in lateral projection) of mandibles from around the fish-to-tetrapod transition: Devonian tetrapods share similarities in lower jaw morphology with Carboniferous aquatic/semiaquatic tetrapods and with Eusthenopteron and Panderichthys and are morpohologically distinct from anthracosaurs, temnospondyls, rhizodonts, and megalichthyids (Neenan et al. 2014). Consequently, depending on which structure is analyzed, skull roof sutures, or mandibles, different predictions exist on the evolution of biting performance at the transition to a terrestrial lifestyle in early tetrapods. The current sarcopterygian fossil that is most closely related to tetrapods is Tiktaalik roseae. This fossil shows several features that have been interpreted to be related to the way it feeds. The establishment of a neck is assumed to be important to position the mouth toward prey in a shallow-water setting (Downs et al. 2008). Adaptations for dorsoventral flexion of the presacral vertebral column are present in both Tiktaalik (Daeschler et al. 2006) and Ichthyostega (Ahlberg et al. 2005), which could be useful to attain a head-down posture to feed on ground-based prey (Van Wassenbergh et al. 2006). A reduction in size of the hyomandibula (which forms the jaw and hyoid suspension at the lateral sides of the head) in Tiktaalik compared to the more basal-finned tetrapodomophs is linked to a reduced reliance on water flows through the mouth cavity (Downs et al. 2008). However, the latter could also be linked to a dorsoventral flattening of the head, for which expansions and compressions in the dorsoventral direction become more useful for generating water flows than lateral expansions (Alexander 1970; Van Wassenbergh et al. 2009). Yet, the dorsoventral flattening of the head itself can be regarded as an adaptation for a benthic lifestyle (Adriaens 2003).

5.6.2 Functional Insights from Amphibious Fishes Lifting of the pectoral region is repeatedly observed during the terrestrial capture of prey by amphibious fishes. The only exception is the four-eyed fish (Anableps anableps), which uses a specialized type of jaw protrusion to pick prey from the ground. Since there is no indication of protrusible upper jaws in the tetrapodomorph fossils, this probably implies that a lifted trunk is needed for effective terrestrial capture of prey in the early tetrapods and their closest ancestors (Van Wassenbergh et al. 2017). This lifting of the pectoral region allows the gape to be pointed toward the ground, and to place the jaws around ground-based prey. Could this lifting of the pectoral region be achieved in the Devonian tetrapodomorphs with or without weight-bearing support from the pectoral

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fins/limbs? This question was recently asked following the description of the terrestrial feeding mechanism of the reedfish Erpethoichthys calabaricus (Fig. 5.6), which showed a striking resemblance to that of the other eel-like species Channallabes apus (Fig. 5.4) (Van Wassenbergh et al. 2017). These two species use the support from the posterior part of their long body and their tail to allow a curling of the anterior body without losing postural balance and stability. However, a comparison of the length of the head relative to the body indicated that the selected tetrapodomorphs are considerably less elongated, and closely resemble the mudskipper in this respect (Fig. 5.9). If we conclude from this that the capacity to lift the trunk without needing pectoral fins or limbs is unlikely to work in stem tetrapods because of their relatively short body and tail with respect to the anguilliform fishes, development of weightbearing capacity by the pectorals is probably essential for the evolution of terrestrial capture of prey. This would mean that the selective pressure to exploit ground-based terrestrial prey may have been an important factor in the evolution of pectoral fins to limbs in early tetrapods (Van Wassenbergh et al. 2017). It can thus be expected that species like Tiktaalik, Ichthyostega, and Acanthostega were capable to capture prey on land as soon as their pectoral support could sufficiently lift the trunk off the ground to tilt the head down toward the ground.

5.6.3 Evolution of the Tongue After the amphibious fishes have captured the prey between their oral jaws, the feeding event continues with the intraoral processing and transport toward the esophagus. Except for the mudskipper, all species studied needed to return to the water to swallow their food. While remaining on land, the mudskipper was able to get its prey in between the pharyngeal jaws with the help from a hydrodynamic tongue (Fig. 5.2), and to capture and swallow a second prey on land (Michel et al. 2015a). The mudskipper’s feeding behavior can, therefore, be considered to be at a higher level of terrestrialization compared to the other amphibious fishes in our sample. Yet, relying on water to swallow, it is still at an intermediate stage of terrestrialization compared to animals that can feed repeatedly on land without the use of intraoral water. As a solution to this problem, a sticky, muscular tongue supported by the hyobranchial skeleton evolved in tetrapods. However, this evolution seems to have occurred later than the evolution of digited limbs, as paleontological studies found that early tetrapod evolution happened in water and most early tetrapods had gills and a hyobranchial system similar to that in sarcopterygians as well as salamander larvae (Reilly and Lauder 1988; Schoch and Witzmann 2011). A metamorphosis and true terrestrial forms evolved much later but changes of the hyobranchial system that accompanied such terrestrial transitions that led to the evolution of a functional tongue are virtually unknown (Schoch 2001). Fossil records of hyoid arch skeletal elements remain scarce (but see Schoch and Witzmann 2011; Downs et al. 2011; Witzmann and Schoch 2013) especially for the earliest tetrapods (but see Downs et al. 2008), perhaps because these originally cartilaginous elements do not often

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ossify in course of ontogeny and therefore do not fossilize (similar to many extant lissamphibians). As a result, paleontologists cannot answer many important questions about tongue evolution (what age, which group, how many times did a tongue evolve). This also implies that we have to rely on mechanistic scenarios using information from modern systems that have been subjected to similar selection pressures (e.g., Reilly 1996; Michel et al. 2015a). The classical hypothesis about the evolutionary transformation series that occurred to evolve terrestrial feeding independent of water in early tetrapods is that first terrestrial prey transport by the tongue evolved, and that prey capture by a protruding tongue is hypothesized to be gained subsequently (Reilly and Lauder 1990; Gillis and Lauder 1995; Reilly 1996). This hypothesis is based on the kinematic analogy/homology between the externally observable hyoid depressions performed by suction-feeding fish and the depressing hyoid region of terrestrial salamanders during intraoral transport of prey. Later, it appeared that the hyoid motions of a fish living at the interface between water and land more closely resemble those of the tongue protrusion phase of salamander, where the hyoid is lifted toward the opening mouth (Michel et al. 2015a). Furthermore, Michel et al. (2015a) points out that the

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Fig. 5.9 Comparison of head length to total length ratios between three anguilliform species that terrestrially capture prey (reedfish Erpethoichys calabaricus, eel catfish species Channallabes apus and Gymnallabes typus), two other terrestrially feeding fish (mudskipper Periophthalmus barabarus, and largescale foureyes Anableps anableps), with four upper Devonian tetrapodomorph fossils (simplified cladogram on top). Note that, these tetrapodomorphs are less elongated than reedfish eel catfish, and more closely resemble the average actinopterygian (axis baseline). Error bars denote standard deviation. After Van Wassenbergh et al. (2017)

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tongue-based intraoral transport by modern terrestrial salamanders is moving a prey that is already brought fairly deep into the mouth cavity during the capture phase that involves protrusion and retraction of the salamander’s tongue. This means that the scenario proposed by Reilly and Lauder (1990) for the evolutionary steps in the evolution of the vertebrate tongue is incomplete: it leaves unanswered how the prey is moved from the jaws to the level of the hyoid inside the mouth cavity. Two more complete scenario’s for the evolution of a functional tongue were proposed by Michel et al. (2015a), as explained below. The first scenario is a completion of the abovementioned hypothesis that stated that the tongue evolved first to transport the prey inside the mouth cavity (Reilly and Lauder 1990). Kinetic inertial transport would have been evolutionarily gained to move prey from being held by the jaws to the level of the hyoid inside the mouth cavity. This feeding mechanism is used by extant crocodiles (Cleuren and De Vree 1992) and monitor lizards (Elias et al. 2000; Montuelle et al. 2009), and involves a posterior shift of the prey by performing a forward acceleration of the head by extending the neck. A tongue evolved to perform salamander-like prey-transport cycles to complete the final stages of intraoral transport without using water, thereby retaining the ancestral hyoid motion patterns of aquatic suction feeding (Reilly 1996). In the light of the functional morphology of the stem tetrapod fossils, this scenario makes sense: the early tetrapod fossils and tetrapodomorphs are generally of large size, and possess a mobile neck (in Tiktaalik and the more derived species; Daeschler et al. 2006), just as crocodiles and monitor lizards. Although this hypothesis is probably the most plausible scenario, some aspects do not entirely fit this gradual evolutionary transition, and justify considering alternative scenarios. Fishes that live at the interface between water and land, and have access to water to assist in intraoral transport and swallowing, may not experience the selective pressures to evolve this entirely novel behavior, i.e., kinetic inertial transporting of food from the jaws to the hyoid region of the mouth cavity. None of the amphibious fishes analyzed to date shows this type of motion, despite that the morphology of the locomotor system of species like the mudskipper or eel catfish could theoretically allow them to launch their head and (part of) their body forward, coordinated with shortly releasing the jaw’s grip on the prey. In contrast, as mentioned above, the hyoid of the most terrestrial of the currently analyzed amphibious fishes, the mudskipper, shows a kinematic pattern similar to that of the hyobranchium of a salamander performing a protrusion of the tongue out of the mouth (Michel et al. 2015a). Therefore, the evolution of a fleshy tongue directly as an adaptation to fulfill the complete phase of food transport, either transport from being grabbed between the oral jaws or through direct adhesive prehension, should still be considered as an alternative evolutionary scenario. While factors such as the stable lifting of the anterior trunk and downward headtilting allowed the benthic capture of food to be performed in the terrestrial environment, further independence of water for swallowing can be attributed to the evolution of the hyolingual system. The appearance of an adhesive tongue can safely be regarded as a key factor in the colonization of land away from amphibious habitats. Future studies on the morpohology of the hyobranchial skeleton of early tetrapod

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fossils will be important for our understanding of the evolutionary history of the vertebrate tongue (Witzmann and Schoch 2013), but identification of transitional patterns in the hyobranchial system that can be linked to the drastic change in function during feeding have yet to be discovered.

5.6.4 Conclusion Amphibious fishes show a range of solutions to the mechanical problems they face when feeding out of the water. To reorient the gape toward terrestrial food, lifting of the pectoral region is consistently observed. This can either be achieved with (e.g., mudskippers) or without support from the pectoral fins (in fishes with elongated bodies). Although some species make use of a specialized type of jaw protrusion to pick prey from the ground, others manage without. The origin of a mobile neck in early tetrapods was probably an important factor to allow the capture of terrestrial food, while the jaws itself required little modifications. How the mode of intraoral transport of food precisely evolved from the ancestral, hydrodynamic mechanism, to the usage of a strongly remodeled hyobranchial system with a fleshy tongue, as in extant tetrapods, remains one of the great mysteries in our evolutionary history. Acknowledgements I thank Anthony Herrel, Peter Aerts, Dominique Adriaens, Egon Heiss, and Krijn Michel for their help in my research on the biomechanics of feeding in amphibious fishes. I also thank the reviewers of this chapter, and the editor for his invitation to write this chapter. This work was supported by a New Research Initiative grant from the Special Research Fund (NOIBOF) of the University of Antwerp, and by a grant from the Agence Nationale de la Recherche (ANR-16-ACHN-0006-01) to S.V.W.

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Chapter 6

The Evolution of the Hand as a Tool in Feeding Behavior: The Multiple Motor Channel Theory of Hand Use Ian Q. Whishaw and Jenni M. Karl

Abstract Skilled hand movements allow us to acquire and prepare food, make and use tools, create art, and communicate. These abilities are central to the human experience and we perform them effortlessly. Yet, the evolutionary history of the control of the hands is complicated and poorly understood. Progress has been impeded by a lack of information concerning the use of the hands in most species of vertebrates. A predominant view, as espoused by the Primate theory, is that skilled hand movements evolved only recently, in the primate lineage, largely as a consequence of visually-guided adaptations to an arboreal habitat. We will discuss several limitations of the Primate theory and present an alternate theory of how skilled hand movements evolved, Multiple Motor Channel (MMC) theory. MMC theory posits that there is not a single evolutionary history or neural control system for the human hand. Rather, neurobehavioral control of the hand can be best understood by viewing it as a recent coalescence of discrete neurobehavioral systems that served different functions and were mediated by different sensorimotor circuits throughout their different evolutionary histories. MMC theory proposes that flexible coordination of the constituent movements used during feeding—the reach, the grasp, and the withdraw—enable the various skilled hand movements used by nonhuman animals as well as humans.

6.1 Introduction Many animal species, in many animal orders, use their hands to aid in feeding (Iwaniuk and Whishaw 2000; Sustaita et al. 2013). The construction of phylogenies from these observations suggests that hand use for feeding dates back to the first terrestrial vertebrates. It is probable that the origin of hand use in feeding has even earlier antecedents. For example, some species of bony fish use the pectoral fins for a variI. Q. Whishaw (B) The Department of Neuroscience, The University of Lethbridge, Lethbridge, Canada e-mail: [email protected] J. M. Karl Department of Psychology, Thompson Rivers University, Kamloops, Canada e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_6

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ety of purposes, including positioning their mouth for grazing (Drucker and Lauder 2002). Although behavioral observations provide a rich source of information on the use of the hand in feeding, there are problems (Sustaita et al. 2013; Wise and Donoghue 1986). The largest order of mammals, rodents (Rodentia), consists of about 2,277 species, yet there has been but one comparative study of their hand use in feeding (Whishaw et al. 1998). The second largest order of mammals, bats (Chiroptera), consisting of over 1,240 species, have a hand that has evolved into a wing and they use their hand to grasp food and place it into their mouth when flying and when sedentary, yet the feeding behavior in only a few species has been described (Fenton et al. 2015; Kalko and Schnitzler 1989; Webster and Griffin 1962). There are about 4,800 species of frogs and toads (Anura) and although studies of their hand use are exemplary, hand use in feeding has been studied in only a comparatively small number of species (Gray 1997; Sustaita et al. 2013). The study of hand use for feeding in other orders, including marsupials, carnivores and primates similarly provides detailed information on only a few species (Iwaniuk and Whishaw 2000). What these numbers mean is that we have an incomplete dataset from which to draw conclusions about how skilled hand movements evolved. Although a strong case is made that hand anatomy results from homology (Fitch 2000), it is more difficult to ascertain the contribution of behavioral homology (Whishaw et al. 1992; Sacrey et al. 2009). The genetic basis of hand use is completely unknown. One way to cope with incomplete information about hand use in feeding in vertebrates is to pose a theory that can organize behavioral observations and generate testable hypotheses. Here we suggest that the Multiple Motor Channel theory (MMC) of hand use is a useful beginning. The MMC theory of hand use proposes that hand use for feeding is a composite of at least 3 independently evolved movements, the reach, the grasp, and the withdraw, each with its own evolutionary history, function, and sensory control. In the following sections, we will describe an early competitor to MMC theory—the Primate theory, also sometimes called the fine-branch niche theory. We will then elaborate on the origin of MMC theory. Finally, we will conclude by describing how MMC theory can be used to generate and test hypotheses regarding the evolution of hand use in feeding.

6.2 The Primate Theory Early literature on hand use for feeding is primate-centric (for a summary see Karl and Whishaw 2013). There are six primary tenants of the Primate theory of hand use for feeding (Cartmill 1974; Heffner and Masterton 1983; Jones 1916; Le Gros Clark 1963; McNeilage 1990; Napier 1960, 1993). (1) Primates are unique in having hands, as defined by the presence of fingernails, whereas many non-primate species have paws, as defined by the presence of claws. (2) Having been subjected to the evolutionary pressure of climbing through small tree branches, primate hands

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are unique in having evolved prehension, the ability to reach out and grasp a food item with a single hand. (3) The evolution of an upright posture freed the hands from the servitude of locomotion posture and forward-facing eyes facilitated further prehensile sophistication in hominids. (4) Free hands facilitated the evolution of independent finger movements to construct and use tools to assist in gathering, preparing, and eating food. (5) The epitome of independent finger use is the pincer grasp in which an item is held between the distal pads the thumb and index finger. (6) The neuroanatomical change that enables independent finger use is the evolution of direct projections of the corticospinal tract onto motor neurons in the spinal cord, an anatomical feature unique to primates. A recent proponent of the primate theory dismisses evolutionary continuity by arguing that, “Other mammalian lineages have evolved similar mechanisms in parallel” (Murray et al. 2017, pp. 192).

6.3 Not just Primates It is necessary to re-examine each of these claims. (1) Whereas the Primate theory emphasizes that hand use in feeding is a specialized primate behavior, in actuality both primate and non-primate species use their hands to assist in feeding. With respect to the hand versus paw dichotomy related to the presence of nails or claws, primates do have nails but some non-primates display a mixture of both claws and nails. As is illustrated in Fig. 6.1, the Norway rat (Rattus norvigicus), which is widely used for experimental research on hand use, has a nail on its thumb, and claws on fingers 2 through 5 (Green 1963). There are also other exceptions to the primate exclusionary nail hypothesis (Sargis 2002; Spearman 1985). Proponents of the Primate theory argue that claws are a functional impediment to prehension. Thus, animal species with large claws should not be able to perform single-handed prehension. For example, the American red squirrel (Tamiasciurus hudsonicus) is proposed to only hold an object with both hands as a person might hold a beach ball between the palms of the hand (Napier 1993). Yet, examination of the claw claim gains little support (Iwaniuk et al. 1998, 2001). Members of the tree kangaroo genus (Dendrolagus) and bear family (Ursidae) have large and distinctive claws. Yet, these species display a variety of hand configurations and grasp postures when engaging in feeding, and the presence of claws does not seem to be a limiting factor. Other species of vertebrates have large claws as an adaption for various behaviors, e.g., for digging by ground squirrels or for climbing by tree squirrels (f. Sciuridae). With respect to the red squirrel, when it holds objects, it is not between the palms but between the tips of the fingers, including its two large thumb pads and the tips of its other fingers (Whishaw et al. 1998). It would seem that animals with claws display skilled manipulation movements, finger-based grasping, as well as single-handed prehension.

162 Fig. 6.1 Precision grasp and thumb nail of the Norway Rat (Rattus norvigicus). a The rat is presenting a piece of spaghetti to its mouth using its right hand and is positioning the end of the spaghetti using its left hand. b A precision grip in which the pasta is held between the first finger (thumb) and second finger (index finger) is used by the left hand. c Finger 1 has a nail and fingers 2–5 have claws. The use of a precision grip and they presence of a nail on the thumb suggest that thumb, although small, receives considerable use in grasping objects (after Whishaw and Coles 1996)

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(2) With respect to the idea that the evolution of skilled hand use is derived from climbing in trees, an explicit test using a carnivore data set suggests that animals in this order display little difference in hand structure or hand use as a function of an arboreal versus non-arboreal lifestyle. Flexibility in the use of the upper arm, however, is related to arboreality, suggesting that aspects of the reach, but not the grasp, may have evolved in an arboreal habitat (Iwaniuk et al. 2000). Clearly, the movements involved in brachiating, an ape specialization, are put to good use in various kinds of reaching behavior by apes in general. (3) The idea that a bipedal stance and forward-facing eyes are prominent factors in the evolution of skilled hand movements also receives little support. There are many more quadrupedal species that use the forelimbs to assist in reaching, grasping, and feeding, than there are bipedal species that do so. While research on the sensory control of the forelimbs in non-primates is limited, available research suggests that visual guidance of prehension in these animals is not prominent. In species that have been studied, lack of visual guidance, due to the lateral position of the eyes or the presence of a long snout, does not seem to impede single-handed prehension, which can be directed by tactile, olfactory or auditory cues (see Whishaw and Karl 2014). (4) Even the idea that independent finger use is a useful behavioral category is beset by the problem of definition (Häger-Ross and Schieber 2000). What comprises an independent finger movement? To be cheeky about it, horses (Equus ferus caballus) walk and paw the snow for food using a single finger, the primate homologue of finger 3, epitomizing a high degree of specialization of a single independent finger for feeding. Indeed, various kinds of independent finger use are displayed by a number of primate and non-primate species. For example, the Aye-Aye (Daubentonia madagascariensis) uses a single finger, finger 3, to perform sophisticated tapping movements on logs to locate insects and skillfully engages finger 4 in order to acquire and extract an insect through the hole that the insect itself has bored into the wood (Milliken et al. 1991). It also displays competency in using its thumb for holding food (Pellis and Pellis 2015). (5) The Primate theory also proposes that only hominids can perform a true pincer grasp of holding a food item between the pads of the thumb and finger 2, but other primates have been observed to use this and other precision grips, including holding objects between the pads of the thumb and the other fingers (Butterworth and Itakura 1998; Fragaszy and Crast 2016; Pouydebat et al. 2009; Spinozzi et al. 2004). It is also suggested that the rat also uses a pincer grasp when holding food as is illustrated in Fig. 6.1 (Whishaw and Coles 1996). (6) There have been investigations into the role of the corticospinal tracts, and other brain regions, in the control of the forelimb and hand. One proposal is that the rubrospinal tract, which projects from a midbrain nucleus to the spinal cord, controls arm movements whereas the corticospinal tract, which projects from the neocortex to the spinal cord, controls independent finger movements (Lawrence and Kuypers 1968a, b). Yet, selective lesions of these tracts fail to abolish the aforementioned movements. At best, they only seemingly impair

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these movements. Indeed, similarly impaired but preserved reaching movements are reported in rats when both pathways are removed together (Whishaw et al. 1998). Furthermore, damage to the cortical motor areas that give rise to the direct projections of the corticospinal tract in the primate do not abolish the independent finger movements as defined by the formation of a pincer grasp. Monkeys with such injury quickly recover the ability to use a pincer grasp to take a raisin offered by hand and to pick up a raisin from a surface in order to eat it (Darling et al. 2014).

6.4 A New Approach: Call a Hand a Hand Now is an appropriate time to reconsider the Primate theory as an explanation for how feeding-related functions of the hand evolved. But what would a reconsideration look like? First, we propose to extend the use of the term ‘hand’ and “fingers” to species other than primates (a suggestion first put forward by G. Cameron Teskey, personal communication). A shift in terminology allows one to move from a primate-centric view of the forelimb and its feeding functions to a vertebrate view. This, in turn, opens up the possibility of studying hand use in all vertebrates from the perspective of a comprehensive evolutionary framework. Second, results from brain lesion studies suggest that it is unlikely that hand use depends on a single brain region. Although primates have direct corticospinal projections to motor neurons and can use their hands to feed, so too can rodents that have no direct corticospinal projections to motor neurons, so too can marsupials that have no cortical tracts descending into the spinal cord, and so too can some reptiles and frogs that have no cortex at and no corticospinal tracts. Mendyk and Horn (2011) describe reaching behavior in an arboreal monitor lizard Varanus beccarii. The animals reached through a slot and reached into tree crevices and holes to obtain food. These movements must be guided and performed by subcortical brain regions. Third, although no one would doubt that a number of different brain regions make a contribution to hand use, it is unlikely that a primate-centric view of hand use will uncover all contributions. To transition from a primate-centric to a vertebrate view of hand use is useful because it allows us to directly address the behavior that is the topic of this chapter, the evolution of the hand as a tool in feeding. As we have suggested, there is not a single evolutionary history of human hand function as posited by the Primate theory. The evolutionary history of the human hand can be better understood by viewing it as a sophisticated interplay between different movements and the multiplicity of functions that the forelimb has been adapted to perform throughout vertebrate evolution. Of these, the movements used in feeding—the reach, the grasp, and the withdraw—are prominent. There is little doubt that some primates became specialist in controlling some of these movements, especially the reach and the grasp, using vision, but antecedent evolutionary adaptations gave these primates a lot to work with. In the following sections of this chapter we elaborate on the contribution that MMC theory makes to understanding the evo-

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lution of hand use in feeding and describe how this theory can be applied when investigating the diverse feeding-related behaviors of the hand in vertebrates.

6.5 Development of the Multiple Motor Channel Theory MMC theory has its origins in two ideas. The first idea is the description of human pointing as a composite of two movements; a large “initial adjustment” that brings the hand close to the target and a smaller “later adjustment” that focuses in on the target (Woodworth 1899). The idea is that even seemingly simple movements are composites of still simpler units. The second idea is that behavior is constrained by neural channels that specify the input-output relations of neural circuits and their functions (Jeannerod 1981). For example, different neural circuits are required for actions that respond to the extrinsic properties of objects (e.g., their location) versus their intrinsic properties (e.g., color, size or form) and their perceptual qualities (e.g., edibility). These two ideas gave rise to Dual Visuomotor Channel (DVC) theory, a theory that proposes that human reach-to-grasp movements consist of a reach that directs the hand to the location of a target object, and a grasp that shapes the hand for appropriate target purchase (Jeannerod 1995). Jeannerod’s theory has been extended to non-human primates and to the investigation of the brain anatomy subserving reach-to-grasp movements. The theory has successfully predicted that reach and grasp movements are subserved by different neocortical networks (see Binkofski et al. 1998; Caminiti et al. 2010; Cavina-Pratesi et al. 2010a, b; Culham et al. 2006; Ferrari-Toniolo et al. 2015; Graziano et al. 2002; Greulich et al. 2017; Jeannerod 1981; Jeannorod et al. 1995; Kaas and Stepniewska 2016; Karl and Whishaw 2013; Kastner et al. 2017; Krauker and Ghez 2000; Vesia and Crawford 2012; Vesia et al. 2013). Still, hand use in feeding involves at least one additional movement that has received relatively less attention. Once an object is grasped in the hand, it must be placed into the mouth for eating. This movement, termed the withdraw, mainly uses somatosensory rather than visual control (Sacrey and Whishaw 2012). Thus, Jeannerod’s theory does not have the explanatory breadth required to account for all of the movements of the hands in feeding (Whishaw and Pellis 1990; Whishaw et al. 2002). The utility of MMC theory is that it includes the three main hand movements and their differing sensory control. The first hypothesis generated by MMC theory is that there are at least three different evolutionary histories that can account for hand use in feeding, one for the reach, one for the grasp, and one for the withdraw (Karl et al. 2018; Karl and Whishaw 2013; Whishaw and Karl 2014).

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6.6 Multiple Motor Theory and Human Hand Use By far, the majority of studies investigating hand use have been conducted using human participants. Therefore, an appreciation of some of the movements of feeding by the human hand is useful for understanding what motor abilities evolved. Imagine a food item, such as a raisin, on a table before you. The reach transports the hand to the raisin whereas the grasp shapes the digits for purchase. The reach is performed using largely proximal musculature of the upper arm. It is an egocentrically directed movement in that it is made with respect to body coordinates. The reach is directed by the extrinsic properties (spatial location) of the target and its function is to bring the hand to the target. In more colloquial terms, the cognitive correlate of the reach reflects “where” the target object is. The grasp is made using largely distal musculature. It is an allocentrically directed movement in that it is made with respect to the target object. It is directed to the intrinsic properties of the target (size, shape) and its function is to shape and orient the hand and fingers to grasp the target. In colloquial terms, the cognitive correlate of the grasp is “what” the target object is. The reach and the grasp have distinctive kinematic features. A kinematic description of hand shaping during prehension shows that the fingers transition through a number of shaping postures as the reach transports them to a target food item. If a participant’s hand starts in an open position on the lap, the fingers first close and flex as the hand is lifted, in a configuration referred to as collect. The minimum hand aperture of collect occurs at about the time that the movement of the hand is aimed towards the target, usually from a position just above the target. The hand aperture at collect is proportional to the size of the target (Saling et al. 1996). It is as if the hand is ‘sighting’ the target. This is an essential transitional function. Although vision detects the sensory properties of the target, the visual metric must be converted to a somatomotor metric to be useful for the hand. It is possible that collect, by representing the visual perception of object location and size as a motor metric, consummates this translation. As the hand then advances toward the target from the sighting position, the aperture between the thumb and one of the other fingers, usually the second finger, increases to form an overgrasp, a finger aperture that is larger than, but proportional to, the size of the target. As the finger tips reach the target, they close and envelope the target for purchase (Jeannerod 1995). Many human reaching studies do not use a food item as a target object, but for studies that do, it is clear that to consummate the reach, the food item must be brought to the mouth for eating. This act is different from reaching in a number of ways (Whishaw et al. 2002). First, it involves an interplay between the hand and the mouth. Whereas reaching is guided by vision, the withdraw depends largely on somatosensory cues—cues from the mouth that tell the hand where to go, and cues from the hand that inform the mouth of the intrinsic properties of the food item (De Bruin et al. 2008; Karl et al. 2012b; Quinlan and Culham 2015). Converging evidence from brain imaging studies support the view that the reach, the grasp, and the withdraw are produced by different neocortical pathways (Fig. 6.2).

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Fig. 6.2 Motor channels of the human neocortex. Step/Locomotion pathway (yellow); reach pathway (blue); handling/hand-to-mouth pathway (pink); grasp/manipulate pathway (green). Note the proximity and partial overlap of the step/locomotion and reach pathways as well as the proximity and partial overlap of the food handling/hand-to-mouth and grasp/manipulate pathways. Adapted from Gharbawie et al. (2011b), Grafton (2010), and Kaas et al. (2011) (aIPS—anterior intraparietal sulcus, M1—primary motor cortex, PRR—parietal reach region, PMd—dorsal premotor cortex, PMv—ventral premotor cortex, S1—somatosensory cortex, SMA—supplementary motor area, SPOC—superior parieto-occiptal cortex, V1—visual cortex, *—intraparietal sulcus, **—parietooccipital sulcus)

For primates, the reach is enabled by a network of cortical areas that form a pathway that projects from primary visual cortex, through dorsomedial parietal cortex, to the dorsal premotor and motor cortices. The reach pathway is just beside a visuomotor channel that mediates stepping (Kaas et al. 2011), a relevant point later on in this chapter. The grasp is enabled by a pathway from primary visual cortex that projects through the ventrolateral parietal cortex to ventral premotor and motor cortex, motor regions that represent the fingers. A portion of the grasp pathway may represent the qualitative properties of the target, e.g., the item is good to eat (Murata et al. 2016; Perry and Fallah 2014; van Polanen and Davare 2015). A pathway that mediates hand to mouth movements connects ventral parietal cortex and ventral premotor cortex, a region representing the mouth and hands, and this pathway does not receive inputs from cortical visual areas (Stepniewska et al. 2009).

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6.7 Cortical Organization and Multiple Motor Channel Theory Brain stimulation in nonhuman primates support the idea that separate neuroanatomical substrates enable the reach, the grasp, and withdraw. Graziano (2009) describes locations in dorsal premotor cortex that, when electrically stimulated with relatively long duration stimulation, cause a monkey to adopt a posture of reaching out for something. What is important in this description is that the movement is not a reachto-grasp movement, but a “reach-as-if-to-grasp” movement: In our stimulation studies, when we stimulated in the cortical zone that we termed the “reachto-grasp” zone, we tended to evoke the first process of extension of the arm, pronation of the forearm, extension of the wrist, and opening of the grip. In this sense the term reach-to-grasp is misleading because there was no grasp at the end of the reach. Rather, we seemed to evoke a reach in preparation for a grasp, with the grip open (Grazanio 2009, p. 145).

In the same experiments, Graziano finds that stimulation in ventral premotor cortex and ventral motor cortex elicited hand-closing movements, as if the monkey were taking food in its hand or holding food in preparation to place it in the mouth: In contrast, when we stimulated in the cortical areas that we termed the “manipulation” zone and the “hand-to-mouth” zone, we tended to evoke the second process of retraction of the arm toward the body, supination of the forearm, flection of the wrist, and closure of the grip (Grazanio 2009, p. 145).

Similar electrical stimulation of primate parietal cortex finds that there are areas that elicit a reach, areas that elicit a grasp, and still other areas that produce a withdraw movement of the hand to the mouth. Each behavior is obtained from an anatomically different location. The reach region is located in dorsal parietal cortex and the grasp and withdraw regions are located more ventrally. Furthermore, the reach, grasp, and withdraw regions of parietal cortex project to the reach, grasp, and withdraw regions of motor cortex (Stepniewska et al. 2011). These regions and their connections form the three sensorimotor channels for the reach, the grasp, and the withdraw. Since the publication of Graziano’s studies on the function of the motor cortex in primates, there have been a number of studies in which the sensorimotor cortex of rats and of mice have been mapped using similar long trains of either electrical stimulation or optogenetic stimulation. These studies reveal a topography of elicited movements that is surprisingly similar to that described for monkeys. Stimulation of the more rostral areas of motor cortex elicit grasping movements and movements of the hand directed toward the mouth while stimulation of the more caudal area of motor cortex elicit movement in which the hand is advanced as if reaching or retracted as if withdrawing (Bonazzi et al. 2013; Brown and Teskey 2014; Guo et al. 2015; Hira 2015; Wang et al. 2017). Clearly, just as the motor cortex of primates is in part organized to produce movements of feeding so too is the motor cortex of rodents. A difference between rodents and primates relates to an absence of visual projections to the parietal and motor cortex pathways mediating hand use (Zhang et al. 2016). The rat has somatosensory (S) to motor cortex (M) projections but does not have

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Fig. 6.3 Motor channels of the mouse (Mus domesticus) cortex. Note that the pathway for locomotor guidance and head orientation (ACA-anterior cingulate area) receives a projection from the primary visual cortex (V), whereas Reach, Grasp, and Withdraw channels have only projections between somatosensory cortex (S) and motor cortex (M). Based in part on behavioral research (Whishaw 2003) and pathways described by Zhang et al. (2016)

a channel from visual cortex to these regions. There are visual projections that are directed into anterior cingulate cortex and these likely mediate head orientation and guidance for locomotion (Fig. 6.3). The absence of a visual projections to sensory and motor cortex is consistent with behavioral results that indicate that although a rodent may use vision to walk to a food item, it uses olfaction and not vision to reach (Whishaw 2003). In summary, although the reach, the grasp, and the withdraw are interwoven during feeding as a seamless movement, the three movements are behaviorally and anatomically dissociable in primates and in rodents. Our description of hand use to this point is a caricature of the hand movements used in feeding. We do many things with our forelimbs that could be categorized as variations of the reach, grasp, or withdraw movement. We do more than perform reach movements, we push, pull, wave, throw and so forth. We do many things with our grasp movement too. We grasp with one hand, between two hands, between a hand and our body, between our various fingers and so forth. We also perform a variety of withdraw movements when we scratch our head or brush our teeth. All of these movements are associated with various finger configurations and rotatory movements such as those that mediate supination and pronation of the hand used in reaching for and presenting a food item to the mouth. The reach, grasp, and withdraw categories of MMC theory

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provide a useful way to simplify human forelimb behavior in order to investigate the evolutionary history of its component movements. It is likely that the various uses of the hand are sufficiently specialized to require additional regions and connections of the somatosensory and motor cortex that are elaborations of the more fundamental reach, grasp, and withdraw movements (Gharbawie et al. 2011a).

6.8 Hand Use: Not just a Visual Behavior If a human participant, who starts with her hands open and resting palm down on their lap, is asked to reach for and eat a food item placed before her, she perform a characteristic series of movements (Fig. 6.4a). To review, she lifts the hand and closes the fingers in proportion to the size of the target (collect). Then, as she transports the hand to the target, she opens the fingers to an aperture that is slightly larger than that of the target (overgrasp). As the hand advances further, the fingers close to grasp (purchase). The target is then brought to the mouth (withdraw) and the fingers open to place the object in the mouth (release). Vision makes an important contribution to the reach portion of this feeding movement (de Bruin et al. 2008). At about the time that the hand begins to move, a participant visually engages the target and maintains visual fixation until approximately the point of purchase. Then the participant visually disengages the target by

Fig. 6.4 Visual reach and touch-then-grasp and visual reach strategies in a human. a Start, overgrasp, and grasp movement used to acquire a visible target. b Touch-then-grasp strategy used to acquire an unseen and unknown target. Note For the preshape structure the hand preshapes and orients to the intrinsic properties of the target before touching it. For the Touch-then-Grasp structure the hand shapes and orients to the intrinsic properties of the target after touching it (after Karl et al. 2012b)

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blinking and/or looking away. This visual fixation on the target during the course of the reach is called gaze anchoring (Reyes-Puerta et al. 2010). Blindfolding the participant disrupts the reach phase of the movement, but it has no effect on withdraw (de Bruin et al. 2008). Thus, the reach is importantly dependent upon vision, but withdraw is not and thus must be dependent upon somatosensation. For visually-guided reaching, the reach and the grasp are closely coupled during hand transport towards the target. They can, however, be behaviorally dissociated (Karl et al. 2012a). If a participant is blindfolded and asked to reach for a food item, grasp it, and place it into the mouth for eating, she first extends the hand with relatively open fingers in an attempt to locate the target. Once she locates the target by touching it, her fingers close to purchase the object. Often, after the first touch that locates the object, the participant withdraws the hand, shapes the digits, and only then makes a grasping movement in what is termed a touch-release-grasp movement. Thus, as illustrated in Fig. 6.3b, the apparently seamless reach-to-grasp action is dissociated into two movements, first a reach that locates the object and then a grasp that achieves purchase. What is extraordinary about the grasp movement of the blindfolded participant is that the hand shaping after touching the target is similar in every way to the hand shaping that a participant makes when sighted. Measurement of overgrasp aperture after initial target contact for a blindfolded participant shows that it is comparable to that of the sighted condition. Thus, the information acquired from touch is as useful for shaping the digits for purchase as is the information obtained from vision. These blindfold experiments indicate that a reach is not dependent upon vision but its accuracy is improved with vision whereas the hand shaping of the grasp can be accomplished with either vision or touch. There is evidence that the superior colliculus contributes to the reach. Nicholas Humphrey trained a female rhesus (Macaca mulatta) monkey, Helen, over a number of years on many visual tasks following a complete lesion of her primary visual cortex (V1). Helen’s size and shape discrimination were about what is expected of a fully sighted monkey. The tasks given to Helen included reaching for crickets or raisins located on the floor of a cage or on the surface of a table. Videos of Helen’s reaching behavior indicate that she gaze anchors the target during the reach and visually disengages as she grasps, just as a sighted person does. But, she is like a blindfolded person, although her reach is accurate, she displays no hand preshaping before her grasp. She only adjusts her fingers to grasp after she contacts the raisin with the palm of her hand (Whishaw et al. 2016). This finding suggests that an alternate visual pathway to the cortical reach circuit can enable the reach in the absence of cortical area V1. This pathway is likely a projection from the superior colliculus (Song and Peek 2015), or perhaps also the lateral geniculate nucleus (Tamietto et al. 2016), to the cortical reach channel that bypasses V1. Taken together these experiments show that although the primary cortical visual projections to parietal and motor cortex contribute importantly to human reach and grasp movements, both the reach and grasp can be performed quite well in the absence of vision or visual cortex. Such observations contribute to the idea that much of the sensory control of the arm and the hands for reaching and food handling evolved

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without cortical visual control and subsequently became coopted under the service of cortical vision. In short, vision is an app for the motor system.

6.9 Origins of the Reach, Grasp, and Withdraw MMC theory proposes that reaching for food by hand to place it into the mouth, although a smooth movement in primates, is a composite movement with each of the submovements, the reach, the grasp, and the withdraw, having a different evolutionary origin. Each of these submovements is also complex and variously depends upon the ability to make rotary movements of the hand, e.g., pronation and supination, and the ability to make a variety of intersegmental movements of the arm and hand relative to external cues, such as a food object, or to body cues, such as to the other hand and to the mouth. In the following sections, we provide some speculations within MMC theory about the evolutionary origins of these movements.

6.9.1 Stepping to Reaching Stepping must form part of the history of the reach. In most quadrupeds, the neural control of the forelimbs and hindlimbs is coupled in whole body locomotion (Grillner 1975). Nevertheless, even when stepping, a forelimb must have independence to accommodate individual steps on changing terrain (Armstrong 1988; Beloozerova and Sirota 1993; Georgopoulos and Grillner 1989; Krouchev and Drew 2013). One can imagine that this independence of forelimb movement can be adapted for a variety of non-locomotor functions such as pushing, swatting, digging, and reaching. For instance, a polar bear (Ursus maritimus) may extend a forelimb to pin a slippery fish to the ground, a cat (F. felidae) may extend a forelimb to swat at a fly or trip up prey, or a boar (Sus scrofa) may extend a forelimb to uncover a food item covered by soil. Gray et al. (1997) describe five hand movements used for feeding in Anurians and one of these movements has the appearance of a modified stepping movement, prey stretching, in which the hand holds the prey down while the mouth pulls at it. This is a feeding movement similar to that displayed by carnivores such as the polar bear when eating large food items (Iwaniuk et al. 2000). Thus, the wide range of independent forelimb movements produced by various animals to assist in their feeding behavior may be derived from stepping. Comparative studies examining behavioral and kinematic features of forelimb movements support the idea of a common origin for a step and a reach. In rodents and primates, and likely for animals of other orders, a forelimb stepping movement is initiated by flexing the elbow and lifting the hand from the substrate. The fingers and wrist then flex and close with the fingers in a collect posture as the limb is transported forward. The fingers open and extend as they approach the target. For contact, the hand pronates in the lateral to medial direction in what is described as the

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Fig. 6.5 Stepping and reaching compared. a The stepping hand of a rat collects on transport, the digits extend and open for placing, and pronate lateral to medial to make contact. b A reaching hand of the rat collects for aiming, the digits extend and open in preparation for grasping, and they pronate lateral to medial to grasp. c A reaching hand of a human collects for aiming, the digits extend and open for the overgrasp, and they pronate lateral to medial to grasp (after Whishaw et al. 2010; Karl et al. 2012b)

arpeggio movement (Fig. 6.5a). The movement of reaching for food in both rodents (Fig. 6.5b) and humans (Fig. 6.5c) is similar in that the digits are collected as the hand is lifted for action, the digits are open and extended with limb advancement, and an arpeggio movement is made to contact the target (Karl and Whishaw 2013; Sacrey et al. 2009; Whishaw et al. 2010). The similarities of collection and the arpeggio found in stepping and reaching suggest a common origin. Manzano et al. (2007) describe a similar stepping movement in tree frogs. The origin of this pattern of forelimb movement may be derived from the whisking of the pectoral fins of bony fishes, which collect during the transport phase of the whisk to reduce friction with the water and then re-open during the thrust phase. Sensory information makes an important contribution to the reach. For rodents, olfaction plays a role in identifying a target for which they may reach. As a rat sniffs a piece of food, it need only bring its hand to its snout to contact the food. In many formal tests of reaching that require a rat to reach through a slot for a food item, it must raise its head in order to clear a path for the hand, so the reach itself is ballistic (Whishaw and Tomie 1989). Thus, like a blindfolded human reaching for an unknown target, in the absence of vision, a rat, although making an accurate reach, does not preshape the hand prior to target contact and does not learn to do so even with extended training. Detailed information on the sensory control of the forelimb for most actions in most animal species is not available, but available evidence suggests that online visual guidance of the reach is not prominent in species other than some carnivores and most primates. Whereas both New World monkeys (catarrhines) and Old World monkeys (platyrrhines) are specialists in visually guided reaching, visual guidance for shaping the hand may be largely a specialization Old World monkeys (see also Preuss 2007).

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When vision contributes to locomotion, attention must be directed ahead of the limb’s target for placement. On difficult terrain, such as rocky or arboreal habitats, visual attention although briefly directed to the precise target location must then shift ahead for the next step (Patla and Vickers 2003; Wilkson and Sherk 2005). Therefore, the actual step is in part preplanned and ballistic. Human participants using a visuallyguided reach, also frequently visually disengage just before the reach movement is completed, suggesting that online vision is more engaged in bringing the hand to the target than contacting and purchasing the target. It could also be argued that were there some inaccuracy in the hand’s approach just before grasping, the time required for visual correction of the grasp is too long to be useful.

6.9.2 Food Handling to Grasping Food handling must form part of the history of the grasp. When grasping a food item as part of a reaching action, rodents use a whole hand grasp that is not shaped to target size as do those prosimians that have been carefully studied (e.g., Fox et al. 2019). By contrast, holding a food item in the hand and manipulating it with complex movements while eating is common in many animal species in many vertebrate orders (Iwaniuk and Whishaw 2000; Sustaita et al. 2013). After a food item has been grasped, a variety of specialized grip configurations and digit movements may be used to manipulate, explore, or stabilize the food item in relation to the mouth. Shaping of the hand during food handling can be quite complex depending upon the food item (Allred et al. 2008; Whishaw et al. 1998; 2017c). In rodents, these movements may aid in positioning a piece of pasta in the mouth (Fig. 6.6a, b), the removal of a hard shell from a sunflower seed by chewing (Fig. 6.6c, d), or biting (Fig. 6.6e, f). A large food item may be held in a fully open hand, but as the item is consumed the grip pattern may change so that the item is eventually held between the first and second fingers—and between the pads of thumb and the first finger. Thus, the movements of taking food from the mouth with the hands and returning food to the mouth with the hands is made in a relatively restricted space relative to the mouth. In primates, similar movements might aid in the removal of the fleshy peel from an orange or banana, or to rotate a cob of corn. For descriptions of primate hand movements see (Elliot and Connolly 1984; Lederman and Klasky 1998; Macfarlane and Graziano 2009; Reghem 2011). Interestingly, Desmurget et al. (2014) describe sites in human motor cortex that generate forelimb movements while receiving sensory inputs from the mouth. A cortical mechanism such as this could contribute to the coordinated hand-mouth food handling behaviors observed in non-primates, nonhuman primates, and humans (Whishaw et al. 2018). A sea of tactile receptors located on the wrists, hands, snout, teeth, lips, and tongue seem related to food manipulation at the mouth in rodents (Ivanco et al. 1996; Whishaw et al. 1998; Whishaw and Coles 1996). These receptors aid in manipulating food in relation to the intrinsic properties of the food item, its size and shape. As food

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items are passed between the hands or are passed between the mouth and the hands, both the mouth and the hands may preshape to receive the food item. Preshaping by the hands when reaching for a food item in the mouth is observed in both rodents and in humans (Karl et al. 2012b; Whishaw et al. 1992a). Tactile signals from the mouth thus inform the hands about the intrinsic properties of a food item held in the mouth (Fig. 6.7a). In humans, this tactile-mediated hand preshaping (Fig. 6.7b) is as precisely calibrated as it is in visually-guided prehension (Fig. 6.7c).

Fig. 6.6 Food handling movements of eating by rodents. a, b Rat eating a piece of spaghetti uses different grips by each hand. c, d Syrian Hamster (Mesocricetus auratus) eating a sunflower seed manipulates the seed while nibbling off the end of the seed. e, f Mongolian gerbel (Meriones unguiculatus) snaps the seed in half with its teeth and throws away the removed shell (after Whishaw and Coles 1996)

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Fig. 6.7 Hand preshaping by rat and human reaching to the mouth to take small, medium, and large food items. a A rat reaching to the mouth, b a human reaching to the mouth, and c human visually guided grasp. Note In all three situations online haptic (food handling) or visual (grasping) information is available to guide hand preshaping such that a large peak hand aperture is used to grasp a large food item, an intermediate peak hand aperture is used to grasp a medium-sized food item, and a small peak hand aperture is used to grasp a small food item (after Whishaw et al. 1992 and Karl et al. 2012b)

We suggest that hand preshaping for passing food between one hand and another as well as from the hand to the mouth and back again was likely co-opted by the visual system in Old World primates to enable the hand preshaping that accompanies visually-guided prehension.

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6.9.3 Pushing to Withdrawing The withdraw movement that carries a food item to the mouth is less studied than are the reach and the grasp. Freely moving rodents typically pick up a food item in the mouth and then display a distinctive “rodent-typical” pattern of eating and food handling (Whishaw et al. 1992). First, an animal sits back on the haunches with the food in the mouth. They then lift one or both hands to a position just lateral to the mouth. The hands are then moved to grasp the food by an adduction/abduction of the upper arm. A very similar hand to mouth movement is displayed by the marsupial Monodelphis domestica when bringing a cricket to the mouth for eating. The object is released into the side of the open mouth with no hand manipulation (Ivanco et al. 1996). The rodent-typical pattern of eating is also displayed in various forms by primates (Reghem 2011). Indeed, we humans usually adopt a similar sitting posture when eating. That eating involves posture is not always appreciated and this can be the cause of an observer to miss features of the evolutionary continuity involved in the use of the hand in feeding. Pushing a food item into the mouth with a hand is one of five movements of Anurians described by Gray et al. (1997). Nevertheless, withdraw of the hand to the mouth as an independent movement after a food item is grasped by the hand may not be completely developed in rodents (Whishaw et al. 2018). When a mouse (Mus domesticus) is trained to reach for food in a formal testing apparatus in which food can be obtained from a shelf by reaching through a slot, it first sniffs the food. Then, as it reaches through the slot to obtain food, it lifts its head to provide space for the advancing hand. Once it has grasped the food, however, it lowers its snout to contact the hand and it maintains this snout-hand contact as it withdraws the hand with the food and sits back on its haunches (Fig. 6.8a). The withdraw of the hand as a mouth-assisted movement is likely mediated by the motor cortex, as lesions to the motor cortex disrupt coupling of the snout with the hand (Gharbawie and Whishaw 2006). Observations of withdrawal of the hand with food in head fixed mice, who are unable to bring their head to the food and so must make an independent withdraw movement entirely with the forelimb, reveal that the movement is difficult for them (Fig. 6.8b). Their success seems to aided by extending their tongue to the food held in the hand while seemingly “licking the hand toward the mouth” (Whishaw et al. 2017a, b). Observations on feeding in a number of rodent species suggest that food grasping with the mouth typically precedes taking the food from the mouth with the hands, although occasionally the Mongolian gerbil (Meriones unguiculatus) and the North American beaver (Castor canadensis) are observed to pick up a food item with a hand (Whishaw et al. 1998). Cricket predation by the laboratory rat also features capture of the cricket with a hand and not the mouth (Ivanco et al. 1996). Interestingly, primates with lesions of the reach pathway revert to mouth feeding except for prey capture (for a summary see Whishaw et al. 2016). That freely moving rodents can position the hands beside the mouth for food handling while eating is enough to suggest that this movement is a step toward the

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Fig. 6.8 Hand withdrawal by the house mouse (Mus musculus). a After grasping food on a shelf, a mouse brings the mouth to the hand and carries the hand beside the mouth as it sits back to eat as is indicated by the digitized trajectory of the mouth and hand. b After a head fixed mouse grasps food, the withdrawal movement is made with difficulty as is indicated by the irregularity of hand trajectory (after Whishaw et al. 2017c)

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completely independent withdraw movement displayed by primates. Hand positioning beside the mouth to assist in feeding may have originated even earlier in vertebrate evolution as many anurans display a variety of hand-to-mouth type movements, including wiping, scooping, pushing etc., to assist in feeding (Gray 1997).

6.10 Conclusion, Where to Now? Many terrestrial vertebrates use the hand to assist with feeding. In doing so they display three fundamental actions: reach, grasp, and withdraw. There is little doubt that primates, and especially humans, are exemplary in making these movements, but the movements are sufficiently recognizable in many other animal species to suggest that they are evolutionarily conserved. In addition, it is likely that each movement has been elaborated in different ways in different species. Although much of the detail is lacking, MMC theory makes it possible to advance a number of predictions related to the evolution and control of hand movements. A principle in embryology, development, and evolution is the principle of rostrocaudal and mediolateral development (Eilam 1995). Similar evolutionary progression can be observed for hand use in feeding. The evolution of reaching may have begun with the body itself acting as the reaching organ and the mouth as a grasping organ, with subcortical visual and/or olfactory processing providing primary guidance. A fish, for example, propels itself to a food item and opens its mouth for capture. For this type of feeding, there may be little calibration of the mouth in relation to target size, as a fully open mouth is likely more effective for all food sizes than is a partially open mouth. This ‘capture’ strategy is conserved in terrestrial vertebrates as illustrated by a dog leaping mouth open to catch a small food item or a large item like ball. More nuanced movements of the mouth might be used for grazing on algae, grass, or leaves. In bony fishes, the pectoral fins contribute to orienting the mouth toward the target. With the evolution of limbs in terrestrial vertebrates the reach function of the mouth is passed along to the forelimb with the first reach act being a modified step to hold a food item against the ground, whereas the grasp function of the mouth is passed along to the hand. According to the principle of deep homology, the neural circuitry that mediates the earliest movements of the pectoral fins of fish would provide the substrate for the evolution of this complex control of hand use in feeding in terrestrial vertebrates (Gehrke et al. 2015). The examination of hand use as a function of feeding strategies suggests that more developed hand movements are found in species with the most generalized diet (Iwaniuk et al. 2000). This suggests that primates owe their prehensile forelimbs to the evolution of capture strategies that involve the reach as well as to the evolution of grazing strategies that involve the grasp. Indeed, it is not difficult to imagine that a largely terrestrial animal might find a sufficiently varied diet to engage the evolution of complex hand movements. This suggestion does not negate the suggestion that hand movements associated with climbing through branches might contribute to

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feeding behavior. Rather, is possible that hand movements that evolved for feeding and manipulating food items in relation to the mouth in turn became useful for climbing through branches. Evidence for the conservation of hand movements in vertebrates comes not only from the many descriptions that suggest functional similarities in different species, but also from descriptions of their maturation during development. One of the first reaching movements in developing human infants occurs as one-month-old infants gaze anchor a target object and reach for it by stretching forward and opening their mouth (Foroud and Whishaw 2012). Over the next months and years infants develop a reach and a grasp that are first responsive only to tactile cues and then later to visual cues (Karl et al. 2018; Thomas et al. 2015). In addition, visual control of the reach appears to mature at a faster rate than for the grasp (Karl and Whishaw 2014). Withdraw movements may also have their origins in early infant actions as witnessed by the movement of sucking a thumb in prenatal infants (Hepper et al. 2005). Nevertheless, a more mature withdraw movement associated with grasping first requires the development of a reach and a grasp. Further evidence for movement conservation comes from observations on the similarity of movements within orders and families. For example, the raccoon (Procyon lotor) is very adept at using its hands, so adept in fact, that early observers speculated that it was a carnivore outlier and had evolved hand movements similar to those of primates. Careful study of its hand movements suggest a different conclusion. The raccoon is skilled, but the forelimb and hand movements that it makes are characteristic of those of other carnivores. Thus, the raccoon is specialized, but not special (Iwaniuk and Whishaw 1999). Species similarities in hand use are sufficiently recognizable that they can receive labels as exemplified by Leyhausen’s description of “canid” and “felid” to describe hand holding patterns (Leyhausen 1979, see Fig. 8-3, p. 58). More systematic labeling of hand use in vertebrates, as we have included in this chapter, would likely go a long way to developing a taxonomy through which the evolution of hand use could be traced. For example, we are struck by the feeding behavior of many New World monkeys that hold a large food item relatively stationary position in their hands while making many complex visually guided head movements while eating. Linking features of this taxonomy to the evolution of neural systems would provide insights into the neural control of prehension. For example, we have suggested that the evolution of the direct projections of the corticospinal tract onto motorneurons, as is found in primates, could be better understood, not as an enabler of independent finger movements, but as part of a visuomotor channel that enables the visual control of skilled hand movements. This visuomotor channel includes the evolution of the fovea and the projections to visual cortex at the sensory end of the channel, ending with the direct projections of the corticospianl tract onto spinal cord motor neurons at the motor side of the channel (Karl and Whishaw 2013; Whishaw and Karl 2014). MMC theory brings a different opportunity for understanding behavior than does localization of function theory. According to localization of function, there are regions or centers of the brain that are responsible for specific behaviors. For example, centers in the motor cortex that represent the hand, the arm, and so forth

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and these centers are responsible for the movements of those body parts. Channel theory proposes that a functional unit of brain organization is a channel—a pathway from sensory receptors to muscles—which represents a biologically useful action. Channel theory is consistent with the idea of the connectome, that brain networks are an organizing feature of the brain (Hagmann 2005; Sporns et al. 2005). Comparative studies on hand use in the feeding behavior of vertebrates offers an opportunity to determine how the connectome evolves as well as to understand how the primate connectome represents the reach, the grasp, and the withdraw. Future work on the evolutionary history of hand use for feeding could also be directed towards the genetic origins of hand movements. At present, it is often necessary to speculate to what extent the movements of different species of animals reflects homology/homoplasy, but a better understanding of gene expression patterns associated with variations in hand use would go a long way to assessing putative behavioral similarity. Hand in hand with such studies, further insight into the comparative nervous systems controlling hand movements might aid in understanding how widespread use of the hand in feeding evolved.

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Part II

Anatomy, Biomechanics and Behavior in Chordate and Vertebrate Lineages

Chapter 7

Feeding in Jawless Fishes Andrew J. Clark and Theodore A. Uyeno

Abstract Hagfishes and lampreys are a peculiar minority of fishes that bite in the absence of jaws. Despite not being mounted to proper jaws, the dentition of hagfishes and lampreys can effectively incise the tissues of large marine animals. The jawless feeding mechanisms employed by hagfish and lamprey may prove insightful in our attempts to understand the evolutionary origins of jaw-driven feeding and, more broadly, the evolution of chordate feeding. These taxa appear to be descendants of the first chordates that possessed dentition, and thus potentially represent the earliest chordates to acquire prey through biting: the process of driving teeth into prey tissue by the means of a closed kinematic chain or loop. In this chapter, we demonstrate how hagfish and lamprey generate true biting movements and provide a comprehensive review of the anatomy and biomechanics of jawless feeding in both taxa.

7.1 Introduction to Jawless Feeding 7.1.1 Jawless Biting The jawless fishes (agnathans) account for only 0.2% of extant craniates; these include the hagfishes (Order: Myxiniformes) and lampreys (Order: Petromyzontiformes). Though jawless feeding is rare in vertebrates, the feeding apparatuses of hagfishes and adult (post-metamorphic) lampreys are nonetheless effective. Their keratinous teeth can be driven into the tissues of exceedingly large food items, and carve out, or render, morsels with similar effect as produced by jawed biting movements (Clark and Summers 2007). Where most vertebrates bear teeth on opposable, pincer-like jaws, the teeth of hagfishes and lampreys are attached to the surface of A. J. Clark (B) Department of Biology, College of Charleston, 66 George Street, Charleston, SC 29424, USA e-mail: [email protected] T. A. Uyeno Department of Biology, Valdosta State University, 1500 N. Patterson Street, Valdosta, GA 31698, USA © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_7

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eversible cartilaginous tooth plates, which are cyclically protracted and retracted to render and swallow pieces of food (Fig. 7.1a–d). The protraction and retraction of the tooth plates in hagfish is supported by an underlying basal plate or by the piston cartilage in lampreys. Many references for both taxa describe the tooth plates and their movements in terms of “rasping tongues”. One may also draw general morphological and functional parallels between these agnathan tooth plates and their supportive cartilages to the form and function of molluscan radulae and their supportive odontophore (Fig. 7.1e). Despite documented similarities in form and function of the hagfish and adult lamprey “rasping tongues” (Yalden 1985), these two groups employ considerably different approaches for rendering tissue. Lampreys use a prominent tooth-bearing oral disc that allows flesh-feeding (e.g., Lampetra fluviatilis) and hematophagous species (e.g., Petromyzon marinus) the ability to tightly adhere to the body surfaces of large and fast-swimming prey animals (Nichols and Tscherter 2011; Samarra et al. 2012). Once attached to the host, the lamprey employs cyclic protraction–retraction movements of its apicalis (or tooth plates) to draw blood and other tissues (Lanzing 1958; Hardisty and Potter 1971a). During this rasping movement, the drawing of blood is facilitated through the secretions from the buccal gland. The active component in these secretions is lamphedrin; an anticoagulant with cytolytic and hemolytic properties (Lennon 1954). Given the striking behavior of blood-sucking, predatory lampreys, the group, in general, is often referred to as ectoparasitic, however nonparasitic forms account for more than 50% (20 sp.) of the 38 extant lamprey species (Potter 1980; Renaud 1997; Gill et al. 2003). These nonparasitic species retain oral discs and tooth plates, albeit with reduced dentition, which are used for clinging onto surfaces like suction cups (Potter 1980; Gill et al. 2003). With 78 recognized species (Fernholm et al. 2013), hagfishes are approximately twice as speciose as lampreys. Hagfishes are strictly marine and generally known to be opportunistic scavengers that feed on dead or dying vertebrates and invertebrates (Martini 1998; Auster and Barber 2006). There is little evidence for dietary diversity across species, and within species (e.g., Eptatretus stoutii), little evidence for ontogenetic dietary shifts (Clark and Summers 2012). However, recent observations of foraging behaviors in wild hagfishes of the genus Neomyxine suggest that some species are active predators on living free-swimming prey (Zintzen et al. 2011, Fig. 7.2). In contrast to adult lampreys, hagfishes cannot firmly adhere to surfaces because they lack oral suction discs. Despite this, hagfishes attempting to render tissue are capable of generating retractile forces similar to the biting forces produced by comparably sized gnathostomes (Clark and Summers 2007). Where predatory lampreys use their rasping tooth plates to create an ulcer for the purpose of feeding on blood and small bits of other tissues, hagfish tooth plates are used to carve or shear ingestible chunks of flesh from animal carcasses that are bigger than can be immediately swallowed. These tooth plates are also effective at grasping and intraorally transporting whole food items, such as polychaete worms and burrowing fish (Zintzen et al. 2011, Fig. 7.2). An important difference between the feeding of hagfish and both parasitic lamprey and jawed vertebrates involves how these animals resist forces generated by

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Fig. 7.1 Arrangement of dentition and supportive cartilages in the feeding apparatuses of hagfish and lamprey. The biting motions in these agnathan tooth plates relative to their supportive cartilages resemble the motions of a molluscan radula relative to its supportive odontophore. a Left lateral view of a hagfish (above) and a closer view of the head region (below) showing the position of the tooth plates and basal plate. b Left lateral view of an adult lamprey (above) and a closer view (below) of the apicalis and piston cartilage. c Left lateral view of tooth plate protraction (top) and retraction (bottom) movements relative to the basal plate in the hagfish feeding apparatus. Images from panels (a) and (c) were modified from Clark and Summers (2012). d Apicalis protraction (top) and retraction (bottom) relative to the piston cartilage in the feeding apparatus of an adult lamprey. e General arrangement and rasping motions of a molluscan radula relative to its supportive odontophore. Like the basal plate and piston cartilage of hagfish and lamprey, the molluscan odontophore bolsters the protractile–retractile movements of the radula (dentition). Images from panel (e) were modified from Brusca and Brusca (2003)

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Fig. 7.2 Predatory behavior of a hagfish (Neomyxine sp.) on a red bandfish Cepola haastii. a, b Individual hagfishes actively searching for and identifying bandfish burrows. c A specimen of red bandfish attempting to exit the burrow when the hagfish enters. d The attack phase begins when the hagfish swims into the burrow and grasps the prey. Note the gyrations in the posterior region of the hagfish body during the attack. e The extraction phase begins with the formation of an overhand knot while the head of the hagfish remains in the burrow. f Manipulation of the body knot facilitates the extraction of the hagfish and grasped prey from the burrow. All images a–f were reproduced with the permission from Dr. Vincent Zintzen (Source Fig. 7.3 in Zintzen et al. 2011)

the dentition. Jawed vertebrates bite with teeth born on pincer-like beams that are connected by robust, compression-resistant jaw joints (Fig. 7.3a). This biting system forms a closed kinematic chain or loop, by which the skull, upper jaw, and dentition provide counteracting loads to the loads applied by the lower jaw and dentition. These applied biting forces and bite reaction forces, are transmitted along the upper and lower jaws to the jaw joints as compressive joint reaction forces. Parasitic lampreys use the adhering suction of their oral discs to close the kinematic chain, which counteracts the force applied by the apicalis to the prey’s body wall (Fig. 7.3b). In the

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Fig. 7.3 Closed kinematic chains in the feeding apparatuses of jawed vertebrates (gnathostomes) and jawless fishes (agnathans). As with the jawed biting mechanism, the jawless feeding mechanisms of lampreys and hagfish (top images) can be decomposed to a pair of rigid links (resembling upper and lower jaws) joined at a compression-resistant joint (bottom images). These images demonstrate how hagfish and lamprey can employ biting mechanisms. a In this closed kinematic chain, the input force produced by the jaw muscles are transmitted along individual “links” in the chain that collectively form a closed loop. These individual “chain links” include (1) the applied muscle force spanning the jaw joint, (2) lower jaw, (3) lower teeth, (4) food, (5) upper teeth, (6) upper jaws and skull, and (7) back to the jaw joint. Also illustrated, are the applied forces in this system and their counterbalancing reaction forces. b When adhering to the body of a prey item, the lamprey is capable of driving its dentition into the food by means of a closed kinematic chain. The parasagittal section of the lamprey head (illustrated at the top) illustrates how the retractile force of the tooth plates (or apicalis) is counterbalanced by the compressive force of the lamprey’s body (section modified from Hilliard et al. 1985). c Video image sequence (progressing from left to right) illustrating how the body knot of a hagfish can act like an opposing jaw to the tooth plates. As the stiffened body knot approaches and slides over and past the head, the rigid body applies a compressive knotting force against the food, which counteracts the tensile, retractile force (or jawless biting force) delivered by the tooth plates. Illustrations modified from Uyeno and Clark (2015)

lamprey feeding system, the counterbalancing suction-induced compressive loads and the apicalis-driven tensile loads are joined by prominent ligaments that connect the supportive piston cartilage to the robust cartilages of the cranium and branchial basket (Fig. 7.3b). Hagfishes do not have an obvious method of closing this kinematic loop; if they simply press their tooth plates to a surface, the resulting effect would be to simply push themselves away from the carcass upon which they are trying to feed. To counteract this effect, hagfish employ their whole bodies to resist the pressure of their tooth plates: they swim forward as they are pressing their tooth plates to the food item and backward to tear off a sheared portion; or they press their bodies against burrow surfaces in the ground or within a carcass; or they form and manipulate body knots (Fig. 7.3c). Notably, hagfishes use the loops of the knot as leverage in order

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to facilitate biting into whale carcasses and other oversized food items and generate enough force to defeat tough scaly body coverings with dense connective tissues (Clark and Summers 2012; Uyeno and Clark 2015). In the hagfish feeding system, a muscular hydrostat forms the compression-resistant joint between the counteracting retractile forces from the tooth plates and the whole body (Fig. 7.3c). Despite their jawless condition, the feeding systems of hagfish and lampreys are indeed capable of generating compressive forces that counteract the tensile forces produced by their retracting tooth plates (Fig. 7.3b, c). This effect is similar to the bite reaction forces produced by the upper jaw and teeth of a mammal that counteracts the bite forces applied by the lower jaw and teeth (Fig. 7.3a). Like gnathostomes, hagfishes and post-metamorphic lampreys possess dentition that can be driven into objects through the use of a closed kinematic loop, which means, like gnathostomes, these jawless fishes possess a biting system. Here, we introduce the term “jawless biting” to refer to the retractile movements of the tooth plates of hagfishes and lampreys.

7.1.2 Natural History Jawless fishes, or agnathans, were the most abundant vertebrates for over 140 million years until the end of the Devonian Period (approximately 360 million years ago) (Carroll 1988; Purnell 2002). During their 80 million-year coexistence with early jawed vertebrates, agnathans occurred in diverse forms. Ostracoderms, characterized by their rigid dermal body coverings made of bone and dentin, accounted for approximately 600 recognized species of the Paleozoic jawless fishes, with at least four distinct superclasses including the Pteraspidomorphi, Anaspida, Thelodonti, and the Osteostrachomorphi (Lingham-Soliar 2014). All species of these hard-bodied jawless fishes are known for possessing bony head and body armor covering a relatively unmineralized internal skeleton (Forey and Janvier 1993; Janvier 1993; LinghamSoliar 2014). The general morphology of hagfishes and lampreys appears to have remained largely conserved since the Paleozoic. Conserved aspects of their morphology include: soft, flexible, and elongated bodies that lack paired fins, integuments that are devoid of scales, and their feeding apparatuses (Bardack 1991; Janvier 1993; Gess et al. 2006). Most Paleozoic agnathan taxa are thought to be microphagous suspension feeders that used cilia to generate weak suction currents that were characterized by both low pressure and throughput relative to the powerful suction created by the rapid expansion of the buccal cavity in extant gnathostome fishes (Mallat 1984; Wainwright et al. 2015). Agnathan suspension feeding that involves relatively low-power suction currents continues to be used by larval forms of extant lamprey (Hardisty and Potter 1971b; Mallatt 1984). Macrophagy is known in a number of agnathans and related taxa; hagfishes (Dawson 1963), lampreys (Lanzing 1958), conodonts (Purnell 1993; Purnell and Donoghue 1997) and some thelodont fish species (van der Brugghen and Janvier 1993). Despite notable exterior differences between extinct and extant forms,

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the jawless feeding mechanisms of these fossil macrophagous taxa were probably similar to those of adult lampreys and hagfishes (Purnell 1993; Goudemand et al. 2011).

7.1.3 Evolution of Chordate Feeding Given the ancestral position of agnathans in the phylogeny of vertebrates, the jawless feeding mechanisms employed by hagfish and lamprey may provide insight into understanding the evolutionary origins of jaw-driven feeding and, more broadly, the evolution of chordate feeding. The evolutionary trend seems to be generally described as a transition from low-power suspension feeding that depends on ciliary action in basal chordates (e.g., urochordates and cephalochordates) to rapid, highpower suction in gnathostomes that is driven by a sudden drop in pressure induced by rapid expansion of the jaw and hyoid apparatus. Larval lampreys appear to use an intermediate approach, involving a feeding flow of moderate intensity produced by ciliary motion that is enhanced by the passive elastic expansion of an actively compressed buccal cavity in order to capture food particles from the water column (see Mallatt 1981). Extant agnathans appear to be descendants of the first chordates that possessed dentition, and thus potentially represent the earliest chordates to acquire prey through biting: the process of driving teeth into prey tissue through the use of a closed kinematic loop. Though histologically distinct and possibly phylogenetically independent from the enameloid teeth found in jawed vertebrates (Smith and Hall 1990; Smith et al. 1996), hagfish and lampreys can bite as forcefully as many jawed vertebrates. The keratinous dentition of these animals is highly effective in reducing large food items (Clark and Summers 2007). Biting is a prey-capture mode that has repeatedly evolved among jawed vertebrates, although it is second in frequency to suction feeding.

7.2 Jawless Feeding in Hagfishes 7.2.1 Biodiversity, Ecology, and Feeding Behaviors Hagfishes are thought to have evolved over 500 million years ago and represent one of the most ancestral lineages of craniates (Forey and Janvier 1993). All species of hagfishes occur in demersal marine habitats, the depths of which may range from 10 m to 5000 m (Fernholm 1974; Martini 1998). Hagfishes feed on a diversity of prey such as; crustaceans, polychaete worms, cephalopods, various small fishes (Gustafson 1935; Wakefield 1990; Johnson 1994), hagfish eggs (Worthington 1905; Holmgren 1946), and the remains of larger marine vertebrates, such as mackerel sharks, sturgeon, birds, whales, and other marine mammals (Strahan 1963; Shelton

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1978; Martini 1998). Hagfishes do not assemble in organized schools; however, when opportunities to feed on dead or moribund prey are presented, immense aggregations of hagfishes can result in spectacular feeding frenzies (Strahan 1963; Smith 1985; Martini 1998). When feeding on large prey items, hagfishes couple cyclic protractions and retractions of their tooth plates with violent whole body movements including knotting (Clark and Summers 2012). During an en masse foraging event, such as feeding on a whale fall, individuals will often cluster themselves around an open wound and proceed to aggressively bite into the prey while employing body knotting, shaking, and twisting. In these situations, the hagfishes will frequently bump into and rub against one another but nonetheless continue to feed unperturbed. Also frequently observed during en masse feedings is the formation of slime aggregates on prey tissue. This is thought to be a possible deterrent for other marine scavengers (Martini 1998; Zintzen et al 2011). Hagfishes are popularly portrayed as opportunistic scavengers on dead or dying marine animals, however, the diversity of their feeding niches is likely not fully characterized. Zintzen and colleagues (2011) have recently discovered that some hagfish species can actively hunt and capture living prey. Underwater video recordings revealed predatory behavior of a Neomyxine species hunting a burrowing Red Bandfish (Cepola haastii) (Fig. 7.2). These recordings showed several hagfishes searching for Red Bandfish burrows, with some individuals occasionally swimming into and out of burrows. This initial searching phase occurred during a relatively long time period (up to 118 min), while the subsequent attack and extraction phases lasted approximately 3 min. During the first minute of the attack, the hagfish drove its head (anterior third of the animal’s total length) into a burrow and proceeded to violently shake and spin the free swimming two-thirds of its body. It is hypothesized that during this period in the attack, the hagfish was deploying its tooth plates for grasping the prey. This active period was immediately followed by a one-minute inactive period, during which it is hypothesized that the hagfish suffocated its prey with slime until the prey stopped moving (Zintzen et al. 2011). Following this period of inactivity was the extraction phase, which began with intense body movements followed by knot formation and manipulation. Less than 30 s later, the hagfish withdrew itself from the burrow with the Red Bandfish secured in its tooth plates (Zintzen et al. 2011).

7.3 Morphology of the Hagfish Feeding Apparatus Myxinoid feeding morphology and behavior were initially observed by European zoologists in the mid to the late 1700s (Gunnerus 1766; Retzius 1790; Abildgaard 1792) and detailed anatomical descriptions have been known for more than a century (Ayers and Jackson 1901; Cole 1905, 1907; Dawson 1963). Morphological parallels are noticeable in the jawless feeding apparatuses of both hagfishes and

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adult lampreys, which has raised the possibility of these taxa sharing a monophyletic origin as cyclostomes (Yalden 1985). The jawless feeding apparatuses of lampreys and hagfishes are like those of jawed vertebrates in that they are comprised of teeth supported by stiff internal structural elements and powered by skeletal muscles (Clark and Summers 2007). In the feeding apparatuses of most gnathostomes, rigid tissues are represented by jaws that are predominantly composed of bone, while the stiffest elements in the jawless feeding apparatuses of hagfish (dentition and basal plate) and lampreys (dentition, piston cartilage, annular cartilage, and branchial basket) are made of unmineralized cartilage. Moreover, in hagfishes, these stiff elements are embedded in muscle and connective tissue that can account for up to 90% of the total mass of the feeding apparatus (Clark et al. 2010). However, the musculature itself is complexly arranged as a muscular hydrostat, and when activated, transforms the soft feeding apparatus into a surprisingly rigid structure that effectively accommodates forceful biting (Clark et al. 2010; Uyeno and Clark 2015). In all hagfish species, the cylindrical feeding apparatus is located in the anterior 15–20% of the body’s length and ventral to the esophagus (Fig. 7.4). In situ, the feeding apparatus is suspended dorsally from the diminutive cranial cartilages by delicate, sinuous arches of cartilage and thin sheets of muscle and connective tissues (Janvier 1993; Ziermann et al. 2014). Ventrally, the feeding apparatus is connected to the rectus muscle band (Fig. 7.5c), a component of the hagfish body wall musculature. When excised from the body, the feeding apparatus resembles a cylinder of muscle with a length roughly four times its width. The feeding apparatus from a 30 cm Atlantic hagfish can be casually described as looking almost exactly like a “Vienna sausage” (a short bite-sized sausage commonly served at parties in North America). Despite its soft tissue composition, and its lack of opposing jaw elements, the hagfish feeding apparatus is capable of creating strong shearing movements with its teeth (Clark and Summers 2007), especially when the tooth plate movements are supported by the leverage of coordinated whole body swimming and knotting movements (Uyeno and Clark 2015). Despite the similarity in overall construction, the morphology of the feeding apparatuses is surprisingly diverse across species: variation can be observed in the relative size of the feeding apparatuses and in the total number of teeth (Fernholm 1998; Clark and Summers 2007). Comparison of cross-sectional areas of discrete muscles within the feeding apparatuses also shows marked variation between species, especially between Eptatretus and Myxinines (Clubb et al. 2019). In the following descriptions, we summarize a generalized overall construction of the feeding apparatus components (the basal plate, dentition, and musculature).

7.3.1 Basal Plate The basal plate is formed of several cartilaginous structures that together represent the most robust of cartilages in the cranial skeleton and in the whole animal. Situated

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Fig. 7.4 Morphology of the hagfish feeding apparatus. (a) Ventral view of a specimen of Atlantic hagfish Myxine glutinosa with the position of the cylindrical feeding apparatus outlined. Magnified ventral (b), left lateral (c), and dorsal (d), views of the feeding apparatus showing the anterior and posterior hard and soft components, the position of the esophagus, the variable and complex orientations of muscle fibers, and the arrangement of the retractor muscle (lighter shading) relative to the tooth plates and cartilage (darker shading). To the right of these illustrations are photographs of the feeding apparatus of a Pacific hagfish Eptatretus stoutii from ventral (e), left lateral (f), and dorsal (g) views with the esophagus removed and the head intact. BP, basal plate; DPM, deep protractor muscle; ESO, esophagus; PC, perpendicularis cartilage; PM, perpendicularis muscle; CM, clavatus muscle; RT, retractor tendon; SPM, superficial protractor muscle; TM, tubulatus muscle; TP, tooth plates. h–j Three-dimensional illustrations of the hagfish feeding apparatus with the tooth plates (TP) in the retracted position. Illustrations are presented in ventral (h), left lateral (i), dorsal (j), anterior-three-quarter (k), and posterior-three-quarter (l) views to demonstrate the cylindrical shape and the complexity in the arrangements of muscle and connective tissues. In all drawings, the tubulatus muscle (TM) is semitransparent to show the deeper clavatus muscle (CM). Note that the PM and posterior fibers of the TM are connected to the perpendicularis cartilage. In contrast, connections between the CM and PC are absent. ABP, anterior basal plate; BP, basal plate; CTP; connective tissue patch (the insertion for the PM fibers); MBP, middle basal plate; PBP, posterior basal plate. Anatomical illustrations a–d were modified from Clark et al. (2010) with permission. Photo credits e–g Mr. Luke Clubb

at the base of the cranial skeleton, the basal plate provides attachment sites for feeding musculature and supports the protraction–retraction movement of the tooth plates. This composite structure can be divided into anterior, middle, and posterior segments, and when summed, the length of these cartilages (i.e., basal plate length) constitutes the anterior 40–50% of the feeding apparatus (Figs. 7.4 and 7.5). When we manipulate excised basal plates, we observe that the connections between these subdivisions allow the basal plate to conform to specific shapes. Both anterior and middle basal plates, which are sagittally subdivided into bars, resemble vertebrate hyaline cartilage and have been referred to as type I cartilage (Wright et al. 1984, 2001). The anterior basal plate consists of a pair of medial bars and a pair of lateral bars, which connect with the two bars of the middle basal plate (Fig. 7.5a, b). The articulations between these subdivisions in the anterior and middle basal plates can give the basal plate a trough-shaped cross-section that provides a supportive platform for the tooth plate movements and respective feeding musculature (Fig. 7.5d) (Cole 1905; Dawson 1963). It is possible that the suture-like joints within and between the anterior and middle basal plate can enable the basal plate to undertake some changes in shape (Uyeno and Clark, Personal Observations). The anterior and middle basal plates are the only parts of the feeding apparatus with cartilaginous connections to the cranial cartilages. Labial cartilages, which articulate with cartilages in the tentacles and palate, project from the anterolateral margins of the lateral bars of the anterior basal plate (Fig. 7.5a, b) (Cole 1905). Branchial arch cartilages, which project from the posterolateral margins of the middle basal plate, connect with the cartilages in the palate (Fig. 7.5a, b) (Cole 1905). Posterior segments of hagfish basal plates bear a more tendinous appearance than a hyaline cartilage appearance, and thus are referred to as type II cartilage (Wright et al. 1984, 1998). In contrast to the anterior and middle segments, the posterior basal plate

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Fig. 7.5 Morphology of the cranial skeleton and basal plate in the hagfish. a Illustration of the cranial skeleton of a hagfish from left lateral view. Note the thin, sinuous morphology of the labial and branchial cartilages that connect the basal plate to the remaining cranial cartilages. The darkest shaded tissues: the palatal tooth, tooth plates, anterior, and middle basal plates, represent the most rigid of tissues in the head and whole animal. b Photographs of the basal plate of a Pacific hagfish Eptatretus stoutii from dorsal view (anterior is left). These photos show the anterior, middle, and posterior divisions of the basal plate and its connection with the branchial arches (BA). In contrast to the anterior and middle divisions, the posterior basal plate resembles tendon or elastic cartilage more so than hyaline cartilage, and is considerably less stiff and more flexible. Photographs of the tubulatus muscle (TM) intact (top) and cut (bottom) demonstrate the attachment of the TM to the dorsolateral surfaces of posterior basal plate. c The ventral surface and keel of the basal plate provides the origin for the protractor muscles and one of the three major axial muscles, the rectus muscle. d 3D drawings of the basal plate and retracted tooth plates from anterior-three-quarter (top) and posterior-three-quarter (bottom) views. Note that the arrangements of the anterior and middle basal plate cartilages produce a trough-shaped cross-section, and on the ventral surface, the convexity and prominent keel of the more flexible posterior basal plate supports the protractor muscles. ABP, anterior basal plate; DPM, deep protractor muscle; LB, lateral bar; MBP, middle basal plate; MB, medial bar; PBP, posterior basal plate; SPM, superficial protractor muscle; TP, tooth plates

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is less stiff, lacks subdivisions, and is relatively elongate, narrow, and tapers caudally (Fig. 7.5). The length of the posterior basal plate accounts for the posterior 50–60% of the basal plate length. Although the posterior basal plate does not articulate with any cranial cartilages, it retains a trough-shaped transverse cross-section and provides attachment sites for some of the major feeding muscles (tubulatus and deep protractor muscles). Located on the dorsal surface of the posterior basal plate is a central longitudinal groove, above which the retractor tendon is positioned at rest and when the dentition is protracted. On the ventral surface of the posterior basal plate is a prominent longitudinal keel, which provides attachment for the deep protractor muscles (Fig. 7.5d). The posterior and lateral surfaces of the posterior basal plate provide attachment sites for the anterior fibers of the tubulatus muscle. While we have not been able to record direct, in situ visualizations of basal plate motions in a freely behaving hagfish, we hypothesize that the arrangement of basal plate cartilages and associated musculature described above likely permits some deformation of the basal plate. This ability to deform may enhance the possible motions of the dentition. For example, protraction and retraction of molluscan odontophore are known to facilitate the radular movements (Padilla 2004; Mikhlina et al. 2015) (Fig. 7.1e). Morphological variation between the anterior and posterior halves of the basal plate coupled with the presumptive differences in material properties could bear some important functional ramifications. Presumably, this would be much like the associated color and stiffness gradients occurring in cephalopod beaks are hypothesized to attenuate biting stresses (Miserez et al. 2008). In the case for the hagfish feeding apparatus, the posterior basal plate could buffer the transmission of stresses from the most rigid of tissues (teeth and anterior/middle basal plate) to the most flexible tissues (visceral, muscle, and connective tissues).

7.3.2 Dentition The tooth plates, a bilaterally symmetric series of teeth and supportive cartilages, represent the most dynamic structure in the hagfish feeding apparatus. Individually, the tooth plates bear two rows of dentition supported by two pairs of cartilages divided into anterior and posterior arches (Fig. 7.6). The anterior arch, which supports the dentition, is larger and more flexible than the posterior arch. Dentition of the tooth plates is supported by the anterior cartilaginous arch, which is fenestrated for the transmission of dental nerves, or nervus dentalis, and the attachment of connective tissues (Cole 1905). The deep protractor muscle, originating from the ventral surface of the basal plate, inserts onto the leading edge of the anterior arch. The smaller but stiffer posterior arch is the attachment site for the retractor muscle tendon (Cole 1905). The differential stiffness in the anterior and posterior tooth plate arches parallels the different muscle forces and stresses exerted by the retractor and protractor muscles on the tooth plates during feeding (Clark and Summers 2007). Projecting from the anterior arch of the tooth plates are two rows of smooth, curved, non-serrated keratinous teeth, which are sometimes referred to as “horny

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Fig. 7.6 Dentition of the hagfish. a Photograph of the feeding apparatus of a Pacific hagfish Eptatretus stoutii in dorsal view, with the white box indicating the position of the tooth plates. Photo credit: Mr. Luke Clubb. b Magnified photo of the tooth plates excised from the feeding apparatus of an Atlantic hagfish Myxine glutinosa. c Illustration of the anterior and posterior tooth rows and supportive cartilages (in gray) in the tooth plates of E. stoutii. d Posterior tooth row from M. glutinosa rotated to demonstrate its hollow morphology (e.g., gray surfaces are internal). e–j Diversity in the dentition of hagfishes, exemplified in Eptatretus cirrhatus and Myxine limosa. Magnified photos of the anterior (e) and posterior (f) tooth rows removed from the tooth plates of a specimen of E. cirrhatus. g Illustration of the teeth of E. cirrhatus highlighting the total tooth number and fusion patterns of the medial teeth (shaded) in both anterior and posterior tooth rows. Total tooth numbers and fusion patterns vary across different species of hagfishes (Fernholm 1998). Magnified photos of the anterior (h) and posterior (i) tooth rows from the tooth plates of M. limosa. (J) An illustration of the dentition of M. limosa demonstrates the smaller size and total number of teeth relative to the dentition of E. cirrhatus. Also indicated by the illustrations are the 2–2 tooth-fusion patterns in the anterior–posterior medial teeth of M. limosa (J) compared with the 3–3 tooth-fusion patterns of E. cirrhatus (g)

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cusps” or “horny teeth” in the literature (Fig. 7.6). In a given species, the total number of the teeth from the posterior row of the tooth plates are usually less than or equal to that in the anterior row. Depending on the species, the total number of teeth on the tooth plates from an individual can vary from 26 teeth (e.g., in M. paucidens) to 70 teeth (e.g., in E. carlhubbsi) (Fernholm 1998). The dentition on both rows of the tooth plates are progressively longer and broader in the medial direction and progressively shorter and narrower in the lateral direction (Clark and Summers 2012). On both anterior and posterior rows, the largest teeth are usually fused as pairs or trios. The shape of the teeth somewhat resembles the grasping dentition of piscivorous sharks and teleosts, and while the total number and fusion patterns of the dentition in the anterior and posterior rows vary across species (Fernholm 1998), the general morphology (e.g., sinuous shape and smooth surface devoid of serrations) of these teeth appears to be conserved (Fig. 7.6e–j). Situated in the roof of the mouth immediately anterior to the resting or retracted tooth plate is a single posteriorly curved tooth called the palatal tooth (Fig. 7.5a), which is usually larger than any of the dentition on the tooth plates. The anatomical position of the palatal tooth relative to the tooth plates, coupled with characteristic head depression movements, enable the palatal tooth to function like a ratchet in that precludes the kickback or expulsion of food during intraoral transport as the tooth plates are repeatedly protracted and retracted after food is ingested (Clark and Summers 2007).

7.3.3 Feeding Musculature The cylindrical hagfish feeding apparatus can be divided into an anterior “hard component” and a posterior “soft component” (Fig. 7.4). The basal plate and tooth plates are situated in this region, the hard component represents the more dynamic and rigid portion of the feeding apparatus. The bulk of the major feeding musculature is complexly arranged as a muscular hydrostat in the soft component (Clark et al. 2010; Clubb et al. 2019). The muscles described here (i.e., the ones that predominantly control tooth plate protraction and retraction motions) can be referred to as the major feeding muscles; all of which are innervated by the trigeminal nerve (Lindström 1949). In the following descriptions, we collectively use the terminology presented by Clark et al. (2010).

7.3.3.1

Protractor Muscle Group

The musculature that powers protraction of the tooth plates occurs in the relatively rigid anterior portion of the hagfish feeding apparatus. The Deep Protractor Muscles (DPM), or Musculus protractor dentium profundus (Cole 1907), originates from the ventral surface of the posterior basal plate and inserts onto the leading edge of the anterior cartilaginous arch of the tooth plates. The DPM possesses four tubular-

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shaped heads (a pair of lateral heads and a pair of medial heads) with longitudinally arranged fibers that span the length of the muscle. Each head of the DPM retains a conserved cross-sectional shape through its length, and connects with its skeletal origins and insertions via short tendons. The Superficial Protractor Muscles (SPM), or M. protractor dentium superficialis (Cole 1907), originates from the ventral surface of the posterior basal plate and inserts onto the oral mucosa anterior to the tooth plates. From a ventral perspective of the feeding apparatus, this thinner sheet of muscle becomes visible as its fibers sweep along and over the lateral and anterior surfaces of the DPM (Figs. 7.4 and 7.5c).

7.3.3.2

Retractor Muscle Group

Three muscles comprise the soft component of the feeding apparatus: (1) a retractor muscle (also known as the M. retractor mandibuli (Ayers and Jackson 1901), the M. longitudinalis linguae (Cole 1907), or the M. clavatus (Dawson 1963; Clark et al. 2010; Clubb et al. 2019)), (2) a vertical muscle (also known as the M. perpendicularis (Cole 1907; Dawson 1963; Clark et al. 2010), and (3) a sphincter muscle (also known as the M. constrictor musculi mandibuli (Ayers and Jackson 1901), the M. copulocopularis (Cole 1907), or the M. tubulatus (Dawson 1963; Clark et al. 2010; Clubb et al. 2019)). The smallest muscle, the M. perpendicularis (PM), possesses vertically oriented fibers packed within the mid-sagittal plane of the posterior 30% of the M. clavatus (CM). Overlying the PM are the semi-longitudinally arranged fibers of the CM. The anterior 65–75% of the CM is enveloped within an overlying array of circular fibers of the M. tubulatus (TM) (Fig. 7.4). Within this region of overlap, the CM progressively tapers in the anterior direction where it connects to the long, narrow retractor tendon at the anterior portion of the TM that interconnects with the posterior basal plate. This morphology has most recently been reviewed in Clubb et al. (2019).

7.4 Biomechanics and Functional Morphology of Hagfish Feeding Hagfishes are capable of forcefully and dynamically driving teeth into food items, despite a number of features that seem maladapted to forceful biting (Clark and Summers 2007). First, the hagfish feeding apparatus (HFA) is predominantly constructed of deformable muscle and connective tissues, and thus does not depend on stiff bones connected by joints. Second, the teeth of a hagfish come in the form of tooth plates, which, in effect, represent one half of a jaw. How can a hagfish forcefully use its teeth without having an opposing jaw element to crush and shear against? Third, the deformable biting system of a hagfish is mounted in the head of a similarly deformable body that can be easily be maneuvered in tight spaces (see

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Freedman and Fudge 2017). Indeed, with a flexible body, hagfish can vigorously tie themselves into a number of different knots. Is not such flexibility a shortcoming? Engineers that design man-made biting systems (e.g., Jaws of Life, table saws, etc.) strive to create housings that support the biting bits as rigidly as possible so that force generated can be directed to the biting surface rather than wasted in deforming the housing. The analysis of this seemingly contradictory relationship between form and function depends on understanding the biomechanics of the feeding apparatus movements and also the complex and integrated body movements.

7.4.1 The Hagfish Feeding Mechanism The bite produced by a hagfish can be decomposed to a cyclical three-step process: First, the tooth plates are protracted from the mouth. Second, the teeth are pressed into the food item. Third, the tooth plates, along with rendered bits of food, are retracted into the mouth (Fig. 7.7). While it is difficult to separate the forces generated within and outside the feeding apparatus, the strong biting force of a hagfish is likely generated by a combination of retractor muscle activity in the feeding apparatus and coordinated body movements. At rest, the retracted tooth plates are folded along their longitudinal axis and the left and right halves of the tooth plates resemble the covers of a book resting on its spine. Thus, the left and right rows of teeth are brought together like pages between the tooth plate covers such that the teeth point posteriorly (Fig. 7.8). The retracted tooth plates are covered by the soft oral mucosa contiguous with the esophagus (Figs. 7.4c and 7.6b). During protraction, the left and right halves of the tooth plates rotate laterally as the tooth plates protracted from the mouth. The end of the protraction phase is marked by the book cover-like halves of the tooth plate in an “open book” position that results in the rows of teeth oriented towards the food item. Protraction is coupled with simultaneous unveiling of the oral mucosa that exposes the teeth, and when the tooth plate is maximally protracted and unfolded, teeth apices point anteriorly in preparation for appropriate contact with the food item (Fig. 7.8). As retraction begins, the teeth are driven into and then become hooked on the food item. The rest of the retraction phase is marked by the tooth plates folding medially as they return into the mouth with dismembered food items in tow (Fig. 7.8). Upon entering the mouth, oral mucosa envelopes the tooth plates, which unhooks the food from the teeth and then works the food into the esophagus. The dislodging of captured food items from the tooth plates is also aided by the palatal tooth and cyclic head depression—elevation movements during subsequent protraction–retraction cycles (Clark and Summers 2007). Rotation of the tooth plates about the distal end of the basal plate resembles a simple pulley, and modeling the mechanism as a pulley has allowed us to generate predictions for the retractile forces of hagfishes (Clark and Summers 2007, 2012). If this simple pulley system were to be modeled in static equilibrium, the magnitude of the input force would equal the magnitude of the output force, therefore, the amount

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Fig. 7.7 Video image sequences and illustrations of the protraction–retraction cycles (bite cycles) in the Atlantic hagfish Myxine glutinosa. (a), Left lateral view of a hagfish gape cycle during the capture phase, when food is grasped and being engulfed. (b), Left lateral view of a hagfish bite cycle during the intraoral transport phase, which commences once food is swallowed. (c). Ventral view of the bite cycle during transport. Note, in ventral view, the bilateral unfolding of tooth plates as they exit the mouth during protraction, followed by the medial folding as they are retracted. The time at each event is indicated in the upper left corner of each video image. This figure was modified from Clark et al. (2010) with permission

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Fig. 7.8 Three-dimensional drawings of the tooth plate protraction–retraction cycles relative to the supportive basal plate in anterior-three-quarter view (a), ventral view (b) and frontal view (c) Note that in all views, the bilateral halves of the protracting tooth plates begin to part and unfold, like an opening book. When the tooth plates are maximally protracted, the apices of the teeth point in the anterior direction. Conversely, when the tooth plates are retracted, the halves of the tooth plates fold medially and the apices of the teeth point in the posterior direction when the tooth plates are fully retracted

of force produced by the protractor and retractor muscles would equal the amount of force applied by the tooth plates during protraction and retraction (Fig. 7.9). Thus, the retractile force of the hagfish tooth plate equals the maximum isometric force production (e.g., assuming 100% recruitment of motor units) of the retractor muscle (M. clavatus). In these studies, the physiological cross-sectional area of the M. clavatus (CSACM ) was determined using the methods described in Powell et al. (1984), by dividing the product of the M. clavatus mass (M CM ) and the cosine of the

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Fig. 7.9 The feeding mechanism of the hagfish can be modeled as a simple pulley. a Left lateral view of a hagfish head with the feeding apparatus highlighted to show the muscles that pull directly on the tooth plates. b The retractor muscle possesses a bipennate fiber arrangement and inserts onto the posterior margin of the tooth plate with a long narrow tendon, granting this muscle some resemblance to a human gastrocnemius muscle. LOA, line of action; θ, pennation angle. Kinematic profiles of protraction (c) and retraction (d) of the tooth plates, by which the forces acting on the tooth plates relative to the basal plate (middle) can be modeled with the simple pulley method (right). Images have been modified from Clark and Summers (2012)

pennation angle (θ) by the product of muscle’s density (ρ) and muscle fiber length (=L CM ). CSACM  (MCM cosθ)(ρ LCM )−1 The maximal isometric force production of the M. clavatus (F CM ) was calculated as the product of the CSACM and the specific tension of white muscle in hagfishes (K), which was substituted with the specific tension of elasmobranch Scyliorhinus canicula (L. 1758) white muscle (Lou et al. 1999). When applied to the static pulley, the force generated by the retractor muscle equals the retractile force (sensu Clark and Summers 2007) or jawless biting force in a hagfish.

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Jawless biting force  FCM  CSACM K Bite force is a significant measurement for feeding performance, as the force production relates to the hardness and size of the food that can be managed. These measurements are indicative of the morphology of the feeding apparatus, prey handling times, and more broadly, the natural diet and ecology of a species (Wainwright 1987; Hernandez and Motta 1997; Herrel et al. 2001; Huber et al. 2005; Herrel and Gibb 2006). Hagfishes can bite as forcefully as many fishes and tetrapods, and they do so in the absence of a stiff, robust internal skeleton and pincer-like jaws. The theoretical retractile forces of 30–40 cm long specimens of Atlantic and Pacific hagfish are approximately 7.0 N and 10.0 N, respectively (Clark and Summers 2007). In an ontogenetic series of E. stoutii Pacific hagfish (TL range  17.0–61.5 cm), the biting forces theoretically range from 3.0 N to >20.0 N (Clark and Summers 2012). When dissected from the feeding apparatus, the M. clavatus and tendon looks like a human M. gastrocnemius and Achilles tendon. The bipennate fiber arrangement of the clavatus muscle relative to its line of action grants it the capability to contract with greater force but less speed than comparable muscles (e.g., M. protractor dentium profundus) with longitudinal fiber arrangements. Furthermore, the long, narrow retractor tendon, which transmits the clavatus muscle force to the tooth plates, is as strong and stiff as gnathostome tendons (Summers and Koob 2002). These properties of the hagfish feeding apparatus grant it the capacity for handling a variety of possible food items, and renders it especially useful for grasping and transporting sizable chunks of flesh.

7.4.2 Tooth Plate Kinematics During Feeding The feeding bouts of hagfishes can be divided into four general stages: identification, positioning, ingestion (capture) and intraoral transport; all of which have been observed in the wild (Zintzen et al. 2011) and in laboratory settings (Clark and Summers 2007). Hagfishes rely on olfactory and tactile stimuli for identifying possible food items. Identification involves an independent movement of the barbels (or tentacles) as they contact the food. Simultaneously with or immediately following identification, the mouth is positioned onto or next to the food, followed by ingestion, which occurs when the tooth plates are repeatedly protracted and retracted until the food is engulfed (Fig. 7.7a). Once ingested, additional protraction–retraction cycles are used to facilitate the swallowing or intraoral transport of the food (Fig. 7.7b, c). Two-dimensional kinematics of tooth plates in hagfishes have been described in M. glutinosa Atlantic hagfish and in E. stoutii Pacific hagfish (Clark and Summers 2007). In this study, animals were presented with thin rectangular samples of squid mantle in order to stimulate tooth plate movements in the absence of excessive body movements and knotting. Despite differences in phylogenetic origins, the relative size of the feeding apparatuses (Fig. 7.10a, b), and bite force production, the kinematic profiles of the tooth plates were similar in both M. glutinosa and E. stoutii (Fig. 7.10c, d). The duration of each protraction–retraction cycle, or bite cycle, were approximately one

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second, with tooth plate protraction and retraction accounting the initial third and latter two-thirds of the bite cycle. Stereotypic cranial movements like head depression and elevation were also similar between both species (Fig. 7.10d).

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Fig. 7.10 Interspecific variation in the hagfish feeding apparatus, exemplified in Myxine glutinosa and Eptatretus stoutii. a Ventral views of M. glutinosa (top) and E. stoutii (bottom) of similar TL with their feeding apparatuses shaded to indicate position in the head. b Ventral views of the feeding apparatuses from a M. glutinosa (top) and a E. stoutii (bottom) of similar TL. Note the significantly robust morphology in E. stoutii relative to M. glutinosa. Despite these discrepancies, kinematic time variables (c) and angular variables (d) of both M. glutinosa and E. stoutii are similar between these species. GCT gape cycle time; HDA, head depression angle; HDT, head depression time; HET, head elevation time; MPA, maximum protraction angle; PT, protraction time; RT, retraction time. Images in (c, d) have been modified from Clark and Summers (2007). e–j Muscle activity in the hagfish feeding apparatus. e Composite block diagram showing kinematic time variables (PT and RT) and the relative onsets, durations, and offsets of activation in the major feeding muscles of hagfish during the capture phase of feeding. Muscles include: the perpendicularis muscle (PM), clavatus muscle (CM), tubulatus muscle (TM), and the deep protractor muscle (DPM). The inset showing burst presence, indicates that during capture phases, all muscles studied were activated during each protraction–retraction cycle. f Block diagram showing the relative timing of kinematic events and muscle activation events during the intraoral transport phase of feeding. Note that the burst presence in the PM, CM, and TM decline when ingested food is being swallowed. g Raw electromyographic recordings (EMGs) show muscle activity patterns during a single gape cycle occurring in the capture phase. Raw EMGs from the first (h), second (i) and third (j) gape cycles of the intraoral transport phase demonstrate the progressive decline in burst presence from the retractor muscles once food is ingested. Images have been modified from Clark et al. (2010)

7.4.3 Muscle Activity in the Hagfish Feeding Apparatus The soft component of the hagfish feeding apparatus (HFA) appears to function as both an actuator for the tooth plate and a skeletal support system for the retractor muscle pulling on the tooth plate. The soft component of the HFA is a cylindrical muscular hydrostat consisting of a three-dimensionally complex arrangement of connective tissues and muscle fibers with circular, bipennate (semi-longitudinal), and vertical orientations (Fig. 7.4) (Clubb et al. 2019). Clark et al. (2010) discovered that co-contraction of all three muscles comprising the hydrostat is what supports the M. clavatus as it pulls the tooth plates in the mouth (Fig. 7.10e–j). Synchronized video and electromyographic data from M. glutinosa Atlantic hagfish show that the M. clavatus, M. tubulatus (sphincter muscle), and M. perpendicularis stay inactive during protraction but fire when the tooth plates retract. These data also demonstrate that elastic recoil of the stretched retractor tendon, muscle, and connective tissues initiates the retraction of the tooth plates. This is evident from the absence of electrical activity during the initial 10–50 ms of tooth plate retraction (Fig. 7.10e, f). Instead of a bony or cartilaginous skeleton, the retractor muscle’s force production is supported by the hydrostatic pressures generated by the activated M. tubulatus, and M. perpendicularis. Simultaneous activation of the M. tubulatus, and M. perpendicularis effectively stiffens the origin of the retractor muscle, and therefore through pressurized myoplasm, transforms the soft component of the HFA into a rigid skeletal origin for the retractor muscle (Clark et al. 2010). The increased turgidity of this muscular hydrostat successfully resists deformations from applied loads, and thus facilitates the transmission of muscle-generated retractile force to the tooth plates.

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Synergism from these three muscles occur during the capture phase, however, the muscle activity in the hydrostat progressively decreases when food is transported intraorally (Fig. 7.10g–j). This progressive reduction to absence of bursts from the M. clavatus, M. tubulatus, and M. perpendicularis during retraction in the intraoral transport phase also indicates the use of passive elastic recoil mechanisms (Clark et al. 2010). During the bite cycles associated with swallowing, the release of the strain energy stored during protraction suffices for retracting the tooth plates (Clark et al. 2010). Passive retraction like this has recently been observed in the feeding apparatuses of E. stoutii electrically stimulated to maximally protracted states (Fuerte-Stone et al. 2016).

7.4.4 Jawless Biting Versus Jawed Biting The broader goal of the research conducted by Clark and Summers (2007) was, from the perspective of a jawless feeding system, to assess possible functional and selective advantages of jaws. By comparing biting force production, gape size, and biting speed of hagfishes with previously published data on various gnathostomes, Clark and Summers (2007) demonstrated that neither forceful bites nor large gapes are novelties presented by a jawed feeding apparatus. Despite their considerably soft and jawless condition, hagfishes are capable of generating as much biting force as a jawed vertebrate of similar size. The 180° gape angles achieved with maximally protracted tooth plates (Fig. 7.10d) enable hagfish to ingest large food items. Other than a few species of snakes and fishes, large gape angles as such are rarely implemented for prey capture among gnathostomes (Clark and Summers 2007). Delivering forceful bites and apprehending food with large gapes are beneficial for the rapacious foraging habits commonly observed in wild specimens (e.g., en masse feeding on a large carcass). The speed at which the bite is delivered, however, appears to be a major functional innovation allowed by jaws (Clark and Summers 2007). The parameter of feeding that hagfishes appear to fall short is the bite cycle or gape cycle time. At 1000 ms, the protraction–retraction cycle of the hagfish is an order of magnitude longer than any previously published gnathostome bite cycle time. The sluggishness of the hagfish bite can be attributed to its feeding mechanism and, perhaps, to its feeding ecology. Under a given amount of force, the amount of displacement and mechanical work achieved by a concentrically contracting muscle would be significantly enhanced if the muscle were to span one or multiple joints in a rigid lever or linkage system. These features are obvious in the gnathostome biting apparatus, which can be modeled as third-class levers or four-bar linkages typically geared to increase closing velocity at the expense of force (Frazzetta 1962; Muller 1987; Westneat 1990, 2004). The arthrodire placoderms, known for biting with heavy dermal cranial armor, likely avoided the problem of sluggishness by moving their heavy mouthparts with fourbar linkages geared for high kinematic transfer efficiencies (Anderson and Westneat 2007). Joints and rigid links are absent in the hagfishes, and even if modeled as a

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pulley, the hagfish feeding apparatus neither amplifies the speed nor the force of the end effector (tooth plates) as in the levers or linkages (Clark and Summers 2007). The slower delivery of bites from hagfish is nonetheless suitable for a diet consisting of dead or dying animals, in which the pressure of apprehending elusive prey is relieved. However, faster gape cycles could facilitate the predatory habits noted in Neomyxine (see Zintzen et al. 2011). Lampreys and even some extinct agnathan lineages possibly rely on a similar mechanism for feeding like the hagfish (e.g., Janvier 1993; Yalden 1985), and thus could be faced with the same limitations for producing rapid bites.

7.4.5 No Joints? No Problem! Many vertebrate biting systems can be represented by a simple mechanism including rigid upper and lower jaws that bear teeth anteriorly and are connected to each other posteriorly through a joint (Fig. 7.3a). Between the teeth and joint are jaw-adducting muscles that originate on the upper jaw and insert on the lower one. In this pincer-like organization, food is placed between the teeth, the jaw adductor muscles generate a force that is transmitted along the lower jaw to the lower teeth, which apply pressure (sensu Gignac and Erickson 2015) to the food that is subsequently transferred to the upper teeth, upper jaws, and jaw joints. In this closed kinematic chain, the upper jaws apply an opposing bite reaction force to the lower jaws (Newton’s Third Law). Less obviously, unless one suffers from a temporomandibular joint disorder, there is also an equal and opposite reaction force that loads the joint in compression (Fig. 7.3a). This mechanism represents a closed kinematic chain, in which the food rests on the teeth of the lower jaw, the lower jaw is connected to the upper jaw through a compression-resistant joint and the teeth of the upper jaw makes contact with the food. If the joint was not able to resist compression, or did not exist, then muscular contraction would simply result in bringing the loose ends of the jaws together rather than breaching the food. If one considers the hagfish feeding apparatus as simply an upper jaw with anteriorly pointing teeth, it can be simply modeled as a spear or spade. Perhaps the momentum of the forward swimming hagfish could be enough to drive the teeth into the prey, however, a model like this does not explain the strong retractile force that hagfishes can produce in order to tear off chunks of flesh. The hagfish mechanism must overcome two separate problems: (1) the feeding apparatus must be made into a rigid jaw structure, despite being composed of compliant muscle and connective tissue, and (2) the hagfish must create both an ad hoc temporomandibular-like joint and a lower jaw in order to close the kinematic chain. The musculature of the HFA is responsible for generating the force needed to move the tooth plates, while providing the structural stiffness needed to support the teeth as they are driven into the food. The first task, a muscle providing motive force, is quite conventional and depends on muscles pulling on tendons. However, the second and less obvious task depends on the muscle and connective tissues in the HFA to be arranged as a muscular hydro-

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stat that becomes turgid and thus provides the rigid structural support needed to effectively use the tooth plate. Muscular hydrostats are densely packed, three-dimensionally complex arrangements of muscle tissues that are composed of two or more muscle fiber orientations (Kier and Smith 1985). Fiber orientations may be arranged antagonistically to cause deformations, or, when co-contracting, may pressurize their myoplasm and lend a turgidity to the overall structure. This form of structural support contrasts the endoand exoskeletal systems of vertebrates and arthropods that make extensive use of rigid links. A simple example of a muscular hydrostat may be a cylinder composed of longitudinal muscle fibers contained within a wall of circumferential fibers. If the longitudinal muscle fibers contract while the circular fibers are relaxed, the entire cylindrical structure becomes shorter and fatter because no changes in volume are occurring. Conversely, the cylinder becomes longer and narrower when the longitudinal muscles relax and the circular muscles contract. Alternatively, simultaneous contraction of the two orientations of fibers results in pressurization of the cylinder rather than any shape change. Muscular hydrostats can also be comprised of more than two muscles or connective tissue fiber orientations and the fibers may be oriented radially, helically, circumferentially or at any oblique angle depending on the required function (Kier and Smith 1985; Smith and Kier 1989). EMG data from M. glutinosa reveal that these muscles relax during protraction of the tooth plates but simultaneously contract when the tooth plates are retracted (Clark et al. 2010; Fig. 7.9e–j). The co-contraction of these muscles effectively stiffens the soft component of the HFA, which (1) provides a necessarily rigid skeletal origin or anchor for the clavatus muscle that also facilitates the transmission of forces from the muscle to the tooth plates and (2) transforms the previously soft, deformable feeding apparatus into a turgid, deformation-resistant cylindrical block, or link, that stabilizes the motions of the tooth plates relative to the motions of the basal plate and whole body. This resistance to deformation by compressive bite reaction forces associated with tooth plate retraction and body movements precludes the feeding apparatus from buckling or collapsing while ingesting food. This resistance effectively counterbalances the retractile forces of the teeth and closes the kinematic loop in the hagfish feeding mechanism, like an anvil does to a hammer (Fig. 7.3c). The ability of this soft feeding apparatus to simultaneously employ the functional roles as an actuator and stabilizer of tooth plates resembles the control strategies used by many forcefully biting, soft-bodied invertebrates. We hypothesize that the functionality of the missing parts of the hagfish biting system (e.g., second jaw and joint) is supported by the complex muscular hydrostat that is the posterior soft tissue component of the hagfish feeding apparatus (Clubb et al. 2019). This muscular hydrostat must function as (1) the force generator for movement, (2) a rigid structure that allows the tooth plate to be supported, and (3) a joint that allows the teeth to be positioned so that the force generated by integrated body movements can be leveraged for an opposing bite (Uyeno and Clark 2015). These multiple functions of a muscular hydrostat may be a commonly recurring functional motif in soft-bodied invertebrate morphology and are known as “muscle articulations.” A fascinating example of a muscle articulation is the one associated with upper and lower beaks of cephalopods

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(Uyeno and Kier 2005, 2007). In contrast to the better-understood “sliding joints” occurring in many animals with rigid skeletons, in which the articulating surfaces of the rigid links (e.g. upper and lower jaws) are in direct contact with one another (Wainwright et al. 1982), muscle articulations are a type of “flexible joint” in which muscle and connective tissues arranged as multifunctional muscular hydrostats form a repositionable joint or pivot area between two disconnected rigid links (Uyeno and Clark 2015). Muscle articulations are multifunctional because they provide the force to move the biting elements, create the joint interconnecting the rigid links, and transmit bite reaction forces (Uyeno and Clark 2015).

7.4.6 Body Knotting in Hagfishes When a hagfish struggles to procure food with simple retraction or rearward swimming, it employs whole body knotting to close the kinematic loop and generate the necessary “biting” force. Here, perhaps counterintuitively, the extremely flexible body of the hagfish becomes an adaptation to creating leverage through the formation and deft manipulation of body knots (Fig. 7.11a). Elongate, limbless, gape-limited aquatic vertebrates are known for integrating head movements with body movements for reducing prey size or handling exceedingly tough prey. Knotting behaviors have evolved independently in hagfishes (Jensen 1966; Uyeno and Clark 2015), pelagic sea snakes Pelamis platurus (Pickwell 1971), and in some species of moray eels (Miller 1987; Barley et al. 2015), and considering its prevalence in hagfish feeding, body knotting may represent an ancestral vertebrate strategy for consuming oversized prey. Possible adaptations for knotting in hagfishes include a flexible, elongate body comprising a complex arrangement of body wall (body core) muscles and an incomplete vertebral column devoid of vertebrae; all of which are enveloped in a loose skin (Clark et al. 2016). The axial muscles of hagfishes include two distinct segmented muscle groups (the parietal and rectus muscles) positioned deep to a superficially overlapping unsegmented oblique muscle (Cole 1907; Jansen and Andersen 1963; Vogel and Gemballa 2000; Clark et al. 2016) (Fig. 7.11b). These arrangements of body core muscles grant a large range of motion by enabling a hagfish to twist its body along its longitudinal axis, bend its body bilaterally and dorsoventrally. The comparably slack skins of hagfishes likely enhance the flexibility of the predominantly decoupled body core (Clark et al. 2016; Freedman and Fudge 2017). This can easily be demonstrated by experimenting with sheath-core constructed ropes designed to possess different amounts of sheathing for cores of a fixed length and radius (Fig. 7.11c). Through these manipulations of rope sheath looseness, it is clear that the looser sheathed models are regularly flexible while tauter-sheathed ropes bear more flexural stiffness (Clark et al. 2016). Like the taut skins of other fishes, the skins of hagfishes are strong and stiff anisotropic biological composites; however, in contrast to other fish skins, the skins of hagfishes are more compliant to stresses

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Fig. 7.11 Body knot formation and manipulation in hagfishes. a Video image sequence of a specimen of Eptatretus stoutii feeding on tethered food. Note that the formation of the knot begins in the caudal end of the hagfish, and once formed, the knot is slid towards the head and pressed against the food surface to leverage an ingestible piece of food. b The loose skin and complex axial musculature of hagfish. (Left) Lateral view of a hagfish with its body core muscles enlarged to show variable fiber arrangements of the three muscle groups: the parietal, rectus, and oblique muscles. (Right) Transverse section of a E. stoutii (approximately at 50%TL) showing how the superficial sheet of unsegmented oblique muscle overlaps with the segmented rectus and parietal muscles. (Right-top) Anterior-three-quarter view of a hagfish body segment (three-dimensional drawing) to illustrate the loose skin and arrangement of muscle tissues comprising the body wall (body core). N, notochord; SC, spinal cord. c Sheath-core constructed ropes can serve as models for the hagfish body, with the core of the rope representing the animal’s body core, and the rope’s sheath representing the animal’s skin. Loose sheathed ropes (ropes with extra sheathing) are regularly flexible in contrast to ropes with tauter sheathes. d Two styles of knots commonly observed in hagfishes include the figure-eight (top) and trefoil, or overhand knot (bottom). e Video images of a E. stoutii (top) and a M. glutinosa (bottom) employed figure-eight and overhand knots, respectively. The hagfishes in these videos are employing body knots to free their heads secured within custom rubber membranes. Video images in (a) have been modified from Clark and Summers (2012). The two-dimensional drawings in (b) and the rope photos (c, d) have been modified from Clark et al. (2016). Austin Haney (VSU) provided the images in (e)

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and strains applied in the circumferential direction. This discrepancy is proposed to facilitate the torsional movements required for the knotting (Clark et al. 2016). To date, there are few studies that investigate the biomechanics and functional morphology associated with body knotting in hagfish (but see Haney et al. 2016). However, a large number of studies tangentially describe the function of body knotting based on qualitative observations (Jensen 1966; Zintzen et al. 2011; Clark and Summers 2012; Uyeno and Clark 2015; Glover and Bucking 2015; Clark et al. 2016). Generally, these functions fall into three categories: (1) Enhancing the retraction of the tooth plates while feeding on firmly tethered food (Clark and Summers 2012) and for extracting burrowing prey (Zintzen et al. 2011), (2) Removing potentially suffocating mucous from the body (Jensen 1966; Fudge 2001; Lim et al. 2006), and (3) Escaping predatory attacks (Jensen 1966). Knotting can be elicited in specimens restrained to rubber membranes (Haney et al. 2016), and by using this approach, we have been able to document the diversity in knotting kinematics across species in our laboratories (Fig. 7.11d, e). Despite being relatively thinner and longer than E. stoutii, M. glutinosa typically requires more time to form and manipulate knots does not bend its body into loops with small radii. As such, M. glutinosa usually produce and manipulate simple loops or overhand knots, while specimens of E. stoutii regularly form figure-eight knots or even more complex knots (Fig. 7.11d, e). A possible reason for differences in body stiffness (at least behaviorally) may be because the skin is built differently between the two species: while transverse skin sections in both species show a great amount of connective tissue, E. stoutii skin shows additional fibers that stain in a manner consistent with muscle (Patel et al. 2017). Furthermore, different knotting behaviors might be attributed to the variation in the material properties of the skins between these species (Patel et al. 2017). Preliminary analyses of knotting events of both species suggest some commonalities in the form of underlying movements that, together, form all loops and knots. We hypothesize that these may represent motor primitives and believe that further studies on this matter are required as a development of complex body movements through control of a relatively small set of motor primitives may be an efficient method of controlling a long sinuous body that may deform in three-dimensional space at any position.

7.5 Jawless Feeding in Lampreys 7.5.1 Introduction The jawless feeding mechanisms of lampreys can also give us some insight into the evolutionary trends of early vertebrate feeding. A notorious image of a foraging lamprey might be an adult parasitic species (e.g., Petromyzon marinus Sea lamprey) firmly attached to a fish or an aquarium glass wall (Fig. 7.12a). Adult P. marinus use keratinous teeth mounted on a “rasping tongue” like the hagfish feeding apparatus

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to bite into large food items, however, in addition to biting, the lamprey feeding apparatus generates the suction required to adhere to the prey’s body. Sea lampreys are highly recognized for their invasion of the North American Great Lakes and for their impact on endemic fishes at the individual and population levels (e.g., Smith and Tibbles 1980). There is a substantial literature on the gut contents of lamprey (e.g., Farmer 1980) and on the bite marks produced by parasitic lamprey on various prey (e.g., King 1980), however, studies on the functional morphology and biomechanics of lamprey feeding are comparably minimal. Among the earliest descriptions on the form and function of feeding and breathing in adult lampreys came from Dawson (1905a, b). Subsequent efforts to characterize the feeding morphology of lamprey included postulates for function (Reynolds 1931; Lennon 1954; Lanzing 1958; Gradwell 1972; Hilliard et al. 1985). The ability for lamprey to firmly cling to surfaces has inspired studies on intraoral pressure fluctuations during suction and ventilation (Gradwell 1972), during vibration-induced startle responses (Currie and Carlsen 1988), and during feeding (Kawasaki and Rovainen 1988). Within the past 30 years, advances in our understanding of the functional morphology and biomechanics of adult lamprey feeding came from efforts by Hilliard et al. (1985), Kawasaki and Rovainen (1988), Rovainen (1996), and Renaud et al. (2009).

7.5.2 Feeding in Larval Lampreys Lampreys have adopted different life history and feeding strategies to the hagfishes (Hardisty and Potter 1971a). Hagfishes only occur in marine environments and undergo direct development (Martini 1998), while lampreys develop as larvae, called ammocoetes, in freshwater environments for five to seven years (Hardisty and Potter 1971b). Most of the predatory, or parasitic lampreys are anadromous, taking on their post-metamorphic adult feeding habits in open-water marine environments. Following up to two years of this predatory stage, the lampreys migrate back to freshwater environments to spawn (Hardisty and Potter 1971b). Nonparasitic adults do not feed and remain in freshwater where they eventually spawn. Adults of all species die after mating (Hardisty and Potter 1971a, b). Ammocoetes burrow into the substrate and expose their heads during feeding. The feeding apparatus of ammocoetes bears more resemblance to the urochordates and cephalochordates than to adult lampreys. Instead of using teeth, all species of larval lamprey possess oral and branchial cilia that are used for suspending food particles via mucous cords, which are subsequently pulled into the gut via ciliary action. This ciliary action is facilitated by a moderate suction that draws water to the mouth. Mallatt (1981) posited that the dual-pump model for teleost ventilation (Hughes and Shelton 1958) also applies to larval lampreys, though in the case of larval lamprey, the expansion of the mouth is achieved by releasing elastic strain energy stored in the wall of the actively compressed oropharyngeal cavity. Urochordates and cephalochordates draw in water via pharyngeal ciliary action but do not use cyclic

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Fig. 7.12 The form and function of lamprey feeding. a Photograph of a post-metamorphic sea lamprey (Petromyzon marinus) attached to an aquarium wall showing the dentition of the oral disc and apicalis (Photo credit: Andrea Miehls). Names and arrangements of teeth: AF, anterior field; IO, infraoral lamina; LF, lateral field; LL, longitudinal lingual laminae; PF, posterior field; SO, supraoral lamina; TL, transverse lingual lamina. b Left lateral views of the cranial skeleton of the lamprey (Lampetra fluviatilis) with musculature removed (top) and with major feeding muscles included (middle). Names of cartilages: anc, Annular cartilage; arc, arcualia; bra, branchial basket; cpr, cornual process; lpa, anterior lateral plate; lpp; posterior lateral plate; nc, nasal capsule; nch, notochord; oc, otic capsule; pcc, pericardial cartilage; soa, subocular arch; stc, styliform cartilage; tea, anterior tectal cartilage; tep, posterior tectal cartilage; trr, trematic ring. Names of muscles: m.ang, annuloglossus; m.ann, annularis; m.bag, basilaroglossus; m.bas, basilaris; m.cap, cardioapicalis; m.ccs, constrictor cornualis superficialis; m.cgr, copuloglossus rectus; m. cgl, cornuoglossus; m.sta, styloapicalis. c Left lateral view of the dentition, cartilage, and muscles in the “rasping tongue” of a lamprey (L. fluviatilis). apc, apical cartilage; coc, copular cartilage; lig, piston ligament; m.cgo, copuloglossus obliquus d Left lateral views of a lamprey (Geotria australis) sectioned in the mid-sagittal plane to illustrate the position of the apicalis in protracted (left) and retracted states (right). HS, hydrosinus; OB, olfactory bulb; SC, spinal cord; ODT, oral disc teeth; vel, velum; br. tube, branchial tube. e, f Comparative feeding morphology in blood-feeding and flesh-feeding lampreys, illustrating variation in the oral disc (i, iv), apicalis (ii, v), and velar tentacles in ventral view (iii, vi). Anatomical illustrations and photos were modified from Miyashita (2012) (b, c), Hilliard et al. (1985) (d), and Renaud et al. (2009) (e, f)

pumping of the branchial (pharyngeal) cavity for generating feeding currents, though ascidians (urochordates) can reject food by compressing the pharyngeal wall (Orton 1913).

7.6 Morphology of the Lamprey Feeding Apparatus Most of our understanding of the morphology of the post-metamorphic lamprey feeding apparatus comes from parasitic species. The lamprey feeding apparatus is born on a cartilaginous cranial skeleton significantly more elaborate than the cranium of hagfishes (Fig. 7.12b), and the biting and suction achieved with both an oral disc and a tooth plate necessitates more muscles (e.g., Hilliard et al. 1985; Ziermann et al 2014; Miyashita 2015). Along with a piston cartilage and apicalis, major structures of the lamprey cranium involved in feeding include the annular cartilage, copula cartilage, branchial basket and pericardial cartilage (Hilliard et al. 1985). The relatively robust and numerous cartilages in the lamprey head form the rim of the oral disc (e.g., annular cartilage), drive biting movements (e.g., piston and apical cartilages), and support the muscle-generated forces during suction and retraction of the apicalis.

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7.6.1 Oral Disc A unique feature to the lamprey feeding apparatus is the oral disc, which facilitates attachment to a prey’s body. Throughout the surface of the oral disc are numerous keratinous teeth arranged in left and right lateral fields, anterior fields and posterior fields (Hubbs and Potter 1971) (Fig. 7.12a). During attachment, the teeth of the oral disc become embedded in the host like athletic cleats that work to prevent slippage along the prey’s body. Oral fimbriae and papillae are soft, filamentous structures lining the periphery of the oral discs in all lampreys (parasitic and nonparasitic), excluding species from Mordacia. These mucus-secreting soft tissue projections develop during metamorphosis and appear to have sensory functions (Lethbridge and Potter 1979; Khidir and Renaud 2003). Furthermore, mucus secretion around the rim of the oral disc has been proposed to aid in suction by producing a seal at the mouth (Lethbridge and Potter 1979). The oral disc is structurally supported by the annular cartilage and its movement or shape changes are largely controlled by the associated annularis muscles (Dawson 1905b) (Fig. 7.12b).

7.6.2 Apicalis and Piston Cartilage The tooth plates of a lamprey, or apicalis, can be observed from the oral aperture located at the center of the oral disc (Fig. 7.12a). Like the tooth plates of hagfishes, the apicalis bears serially arranged keratinous teeth that can be driven into prey tissue by cyclic protraction and retraction (Fig. 7.12c, d). The apicalis comprises a single transverse lingual lamina positioned anterior to a pair of longitudinal lingual laminae. In some species, the teeth on the transverse and lingual laminae are serrated and like the teeth on the oral discs, the teeth on the apicalis are diverse across species and appear to be functionally associated with diets (Potter and Hilliard 1987; Renaud et al. 2009). When the apicalis is cyclically protracted and retracted during feeding, its transverse lamina is most effective at puncturing the prey’s integument while the paired longitudinal laminae, which bilaterally unfold and medially fold like hagfish tooth plates, intraorally transport blood and fleshy tissues to the gut (Hilliard et al. 1985). Underlying the apicalis, oral and gut cavities, is the supportive piston cartilage: a robust, elongate cone-shaped structure spanning between the oral aperture and the branchial basket. The piston cartilage of lamprey supports the movements of the apicalis and the piston cartilage itself, like molluscan odontophore and hagfish basal plates, can be protracted and retracted (Fig. 7.1). However, in contrast to the anatomically decoupled tooth plates and basal plates of hagfish, the apicalis of lamprey is directly attached to the head of the piston cartilage by a stiff, fibrous piston ligament (Hilliard et al. 1985) (Fig. 7.12c, d).

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7.6.3 Major Feeding Muscles The feeding behaviors of lamprey include stereotypic movements of the oral disc, tooth plates, pharynx (oral cavity), and velum (Hilliard et al. 1985; Kawasaki and Rovainen 1988); all of which are controlled by muscles innervated by branches of the trigeminal nerve (Lindström 1949). Described here are the major components of the lamprey feeding apparatus involved in the protraction and retraction movements of the apicalis and piston cartilages. Particularly useful references for the anatomy of these muscles include the investigations conducted by Hilliard et al. (1985), Miyashita (2012), and Ziermann et al. (2014). The research conducted by Hilliard et al. (1985) included functional postulates based on anatomical descriptions (gross dissection and histology) and manipulations of the feeding apparatus from euthanized specimens of Southern Hemisphere Lamprey Geotria australis. Particularly beautiful anatomical illustrations of the lamprey feeding apparatus can be obtained from Miyashita (2012). The primary apicalis retractor muscle of a lamprey, the M. cardioapicalis, resembles the clavatus muscle of a hagfish in that it is connected to the apicalis by a long narrow tendon. In contrast to the clavatus muscle, the cardioapicalis muscle is born on a relatively robust pericardial cartilage, which forms the posterior surface of the branchial basket, and the associated sphincter muscle (M. constrictor glossae profundus internus) is substantially reduced relative to the robust tubulatus muscle of hagfishes and only encircles a portion of the cardioapicalis muscle and piston cartilage (Hilliard et al. 1985; Miyashita 2012; Ziermann et al. 2014). Constriction of the sphincter muscle is hypothesized to aid in protracting the piston cartilage (Hilliard et al. 1985). A putative synergist for the M. constrictor glossae profundus is the M. constrictor cornualis superficialis, which links the paired cornual processes adjacent to the posterior region of the piston and runs under the piston cartilage like a sling (Hilliard et al. 1985; Ziermann et al. 2014) (Fig. 7.12b). Additional protractor muscles of the piston cartilage include the M. annuloglossus and M. copuloglossus rectus (Hilliard et al. 1985). The M. annuloglossus spans between the annular cartilage and piston cartilage, and the M. copuloglossus Rectus spans from the posterior end of copula cartilage to the piston cartilage. The M. copuloglossus obliquus, which originates from the posteroventral side of the copula and inserts onto the head of the piston, was originally hypothesized to be a retractor of the piston cartilage (Hilliard et al. 1985). However, in Ichthyomyzon unicuspis the M. copuloglossus obliquus appears to be a protractor of the piston (Kawasaki and Rovainen 1988). The large M. basilaris that overlaps many of the cranial muscles are also hypothesized to support the piston cartilage. The anteroventral extension of the M. basilaris that inserts onto the lateral posterior surface of the piston head (Hilliard et al. 1985), and likely functions in the expansion or compression of the oral cavity (Kawasaki and Rovainen 1988).

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7.7 Biomechanics and Functional Morphology of Lamprey Feeding The efforts of Hilliard et al. (1985) and Kawasaki and Rovainen (1988) include the most recent and important contributions to our understanding of the functional morphology and biomechanics of feeding in adult lamprey. Hilliard et al. (1985) provided a detailed anatomical description of the feeding apparatus musculature of G. australis with associated functional hypotheses. Kawasaki and Rovainen (1988) conducted experiments on live specimens of Ichthyomyzon unicuspis, which included observations of apicalis movements and suction pressure measurements synchronized with EMG recordings from the M. basilaris, M. annularis and branchial muscles during feeding. A helpful review of the feeding and breathing in lamprey can be obtained from Rovainen (1996).

7.7.1 Protraction and Retraction of the Apicalis The adult lamprey feeding apparatus can generate biting movements through the cyclic protraction and retraction of the apicalis. These biting movements of the “rasping tongue” are coupled with biting and suction of the toothy oral disc being applied to the prey’s body. Retractile forces from the M. cardioapicalis are transmitted to the apicalis by a long narrow tendon and supported by the pericardial cartilage. Protraction appears to be driven by the activity of the M. copuloglossus rectus and M. copuloglossus obliquus and the ligamentous linkages between the copula, piston, and apical cartilages (Kawasaki and Rovainen 1988). Protraction–retraction cycles of the tooth plates in lampreys appears to be more restricted than the tooth plate movements of hagfishes. The limited motion of the tooth plate in adult lampreys can be attributed to the robust piston ligament connecting the tooth-bearing apical cartilage to the anterior edge of the supportive piston cartilage (Hillard et al. 1985; Fig. 7.12c, d). In the hagfish feeding apparatus, the tooth plates are free to move relative to the basal plate (see Clark and Summers 2007). Through manipulation of euthanized specimens of G. australis, Hillard et al. (1985) showed that the retraction of the tooth plates occurs during the protraction of the piston cartilage, and vice versa.

7.7.2 Feeding Modes of Parasitic Lampreys Parasitic lampreys feed on blood and other tissues from a larger living host, typically a bony fish (Hardisty and Potter 1971a; Khidir and Renaud 2003). Lampreys use their toothed oral discs (or suckers), “rasping tongues,” and volumetric fluctuations in the buccal (oral) and pharyngeal cavities to adhere to prey (Reynolds 1931; Lanzing 1958; Kawasaki and Rovainen 1988). The feeding morphologies and natural diets

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of parasitic lampreys are diverse, and their feeding modes have been categorized as flesh-eating (Genera: Ichthyomyzon, Petromyzon, and Mordacia), blood-eating (Genera: Eudontomyzon, Lampetra, Lethenteron, Geotria), intermediate or bloodand-flesh-feeding (Genera: Entosphenus and Tetrapleurodon), and carrion-feeding (Caspiomyzon wagneri) (Potter and Hilliard 1987; Rovainen 1996; Renaud et al. 2009). The relationships between feeding morphologies and phylogenetic patterns have been investigated by Hubbs and Potter (1971), Potter and Hilliard (1987), Salewski et al. (1995), Gill et al. (2003) and Renaud et al. (2009). Recent efforts by Renaud et al. (2009) provide an excellent description of the relationships between the diet and morphology of the dentition, buccal glands and velar apparatus in parasitic lamprey (Fig. 7.12e, f). Blood-feeding lampreys (e.g., Petromyzon and Ichthyomyzon) possess larger buccal glands than the flesh-feeding Lampetra, Lethenteron, Eudontomyzon and Geotria, which probably reflects the increased dependence that blood-feeding species have on anticoagulants (Renaud et al. 2009). Larger velar tentacles in fleshfeeding lamprey species relative to blood-feeding species are proposed to be useful in preventing larger food items from entering the branchial tube. In blood feeders, like P. marinus and Mordacia sp., the relatively narrow teeth born on the transverse lingual lamina and longitudinal laminae are proposed to be adaptations for rasping holes, while the stouter dentition in flesh feeders like Lampetra fluviatilis and G. australis are proposed to facilitate gouging tissue from the prey’s body (Renaud et al. 2009; Fig. 7.12e, f).

7.7.3 Adhesion to Prey Once a lamprey finds a place to cling to, it actively applies its oral disc, or sucker, onto the substrate until it successfully adheres to it. Manipulation of the sucker is achieved through contractions of the annularis muscle. Attachment of an adult lamprey to a substrate involves a vacuum created in the sucker cavity and oral (or buccal) cavity, accompanied by movements of the apicalis, piston, oral disc and whole body (Dawson 1905b). In addition to rasping and tearing flesh, the retracted apicalis appears to function like a valve between the oral cavity and sucker cavity, and prevents water in the oral cavity from leaking back into the sucker cavity (Kawasaki and Rovainen 1988). Thus, in addition to rasping and tearing flesh, the apicalis forms an intermittent seal between the sucker and oral cavity (Rovainen 1996). The velum functions like another valve that directs water flow from the oral cavity to the branchial tube or to the gut. If velar apparatus blocks passage of fluid to the branchial tube, the fluid will be directed to the esophagus. Separation of water flow enables a foraging parasitic lamprey to breathe while actively biting into the prey with its apicalis. Once attached to a substrate, water in the oral cavity and hydrosinus can be pressurized by constriction of the pharyngeal and basilaris muscles to flow into the branchial tube or into the esophagus (Reynolds 1931; Kawasaki and Rovainen 1988). Active muscle-generated expansion of the oral cavity induces a vacuum that draws

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fluid into the mouth. This expansion of the oral cavity can occur with relaxation of the apicalis (during pumping) or with maximal protraction of the apicalis (during feeding). During feeding, cyclic protraction reaction of the apicalis does not impede suction (Kawasaki and Rovainen 1988; Rovainen 1996).

7.8 Conclusions Because the jawless condition represents the primitive feeding apparatus for vertebrate animals, the biomechanics and functional morphology of jawless feeding in hagfishes can bear some insight into the selective and functional advantages of jaws (see Clark and Summers 2007). These studies also provide an informative perspective on the evolutionary trends in the form and function of feeding across the chordates, especially during those crucial transitional steps from suspension feeding with cilia to suction and biting with proper jaws. Despite their poor fossil record, some of the feeding mechanisms employed by many extinct taxa (e.g., conodonts and thelodonts) may be explained by careful observations and studies on the jawless feeding mechanisms of extant hagfishes and lampreys. There appears to be more diversity in the morphology and biomechanics of knotting and feeding across species that previously thought, given the progressive increase in the number of species and the advancements in our understanding of the phylogenetic relationships between hagfish species (see Fernholm et al. 2013). Hagfish are jawless fishes that use the muscular hydrostatic function of their feeding apparatus to create turgid structural support for their everted tooth plates (Clark et al. 2010; Clubb et al. 2019). When extra biting force is needed to procure a grasped food item, hagfishes can use their flexible bodies to create an ad hoc joint and lever system. The joint connects the feeding apparatus to loops of body knot that are then pressed against the food item (Uyeno and Clark 2015). This body contact with the food item creates a closed kinematic loop that can then be used to generate leverage needed for forceful bites. With a significantly more elaborate cartilaginous cranium, the biting system of the adult predatory lamprey might not rely on muscular hydrostatics for achieving motive and structural support for inducing a bite within a closed kinematic loop, and furthermore, are not known for creating and manipulating body knots. Instead, the biting forces and movements of the apicalis appear to be supported by the robust cranial, branchial and pericardial cartilages, and counterbalanced by the suction and dentition on the oral disc. Acknowledgements The authors are honored to contribute to this text on vertebrate feeding and we especially want to thank Dr. Vincent Bels for this opportunity. Our recent advances in the study of hagfish feeding biomechanics were funded by grants from the National Science Foundation (IOS1354788 awarded to TAU and AJC), the College of Charleston (awarded to AJC), and Valdosta State University (awarded to TAU). Luke Clubb (VSU) generously provided descriptions of the intraspecific variations in the morphology of the hagfish feeding apparatus, and some of the images in this chapter. Austin Haney (VSU) provided insightful comments on the interspecific differences in knotting behaviors and biomechanics of hagfishes, and provided some images for the chapter. Raj

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Patel (CofC) and Emily Kennedy (CofC) provided comments on the variation in material properties of integuments of Myxine and Eptatretus. We thank Dr. Vincent Zintzen for providing the artwork for Fig. 7.2. The collection and shipment of hagfish specimens to the authors’ laboratories were made possible by: Dean Grubbs (for the deep-sea fishing data and live E. springeri specimens), Donna Downs (WA Fish and Wildlife) and Port Angeles Fishing Co. for providing live E. stoutii specimens, Kim Penttila (CA Fish and Game Commission) for providing us with frozen specimens of E. stoutii and M. hubbsi, and Caleb Gilbert (NOAA NMFS) for providing live M. glutinosa specimens.

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Potter IC (1980) The petromyzoniformes with particular reference to paired species. Can J Fish Aquat Sci 37:1595–1615 Potter IC, Hilliard RW (1987) A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes). J Zool 212:713–737 Powell PL, Roy RR, Kanim P, Bello MA, Edgerton VR (1984) Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. J Appl Physiol 57(6):1715–1721 Purnell MA (1993) Feeding mechanisms in conodonts and the function of the earliest vertebrate hard tissues. Geology 21:375–377 Purnell MA (2002) Feeding in extinct jawless heterostracan fishes and testing scenarios of early vertebrate evolution. Proc R Soc Lond B Biol Sci 269:83–88 Purnell MA, Donoghue PC (1997) Architecture and functional morphology of the skeletal apparatus of ozarkodinid conodonts. Philos Trans Royal Soc London B 352:1545–1564 Renaud CB (1997) Conservation status of northern hemisphere lampreys (Petromyzontidae). J Appl Ichthyol 13:143–148 Renaud CB, Gill HS, Potter IC (2009) Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lamprey. J Zool 278:231–242 Retzius AJ (1790) Anmarkingar vid Slaget Myxine. Kgl. Vet Akad Nya Handl Stockh 11:104–108 Reynolds TE (1931) Hydrostatics of the suctorial mouth of the lamprey. Univ Calif Publ Zool 37:15–34 Rovainen CM (1996) Feeding and breathing in lampreys. Brain Behav Evol 48:297–305 Salewski V, Kappus B, Renaud CB (1995) Velar tentacles as a taxonomic character in central European lampreys. Acta Univ Carol Biol 39:215–229 Samarra FI, Fennell A, Aoki K, Deecke VB, Miller PJ (2012) Persistence of skin marks on killer whales (Orcinus orca) caused by the parasitic sea lamprey (Petromyzon marinus) in Iceland. Mar Mam Sci 28:395–401 Shelton RGJ (1978) On the feeding of the hagfish Myxine glutinosa in the North Sea. J Mar Biol Assoc UK 58:81–86 Smith BR, Tibbles JJ (1980) Sea lamprey (Petromyzon marinus) in Lakes Huron, Michigan, and superior: history of invasion and control 1936–78. Can J Fish Aquat Sci 37:1780–1801 Smith CR (1985) Food for the deep sea: utilization, dispersal, and flux of nekton falls at the Santa Catalina Basin floor. Deep Sea Res 32:417–442 Smith MM, Hall BK (1990) Developmental and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev Camb Philos Soc 65:277–374 Smith KK, Kier WM (1989) Trunks, tongues, and tentacles: moving with skeletons of muscle. Am Sci 77:28–35 Smith MM, Sansom IJ, Smith MP (1996) Teeth before armour: the earliest vertebrate mineralized tissues. Mod Geol 20:1–17 Strahan R (1963) The behaviour of myxinoids. Acta Zool 44:1–30 Summers AP, Koob TJ (2002) The evolution of tendon—morphology and material properties. Comp Biochem Physiol 133A:1159–1170 Uyeno TA, Kier WM (2005) Functional morphology of the cephalopod buccal mass: a novel joint type. J Morphol 264:211–222 Uyeno TA, Kier WM (2007) Electromyography of the buccal musculature of octopus (Octopus bimaculoides): a test of the function of the muscle articulation in support and movement. J Exp Biol 210:118–128 Uyeno TA, Clark AJ (2015) Muscle articulations: flexible jaw joints made of soft tissues. Integr Comp Biol 55:193–204 van der Brugghen W, Janvier P (1993) Denticles in thelodonts. Nature 364:107 Vogel F, Gemballa S (2000) Locomotory design of ‘cyclostome’ fishes: Spatial arrangement and architecture of myosepta and lamellae. Acta Zool Stockh 81:267–283 Wainwright SA, Biggs WD, Currey JD, Gosline JM (1982) Mechanical design in organisms. Princeton University Press, Princeton, NJ

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Wainwright PC (1987) Biomechanical limits to ecological performance – mollusk-crushing by the caribbean hogfish, Lachnolaimus maximus (Labridae). J Zool 213:283–297 Wainwright PC, McGee MD, Longo SJ, Hernandez LP (2015) Origins, innovations, and diversification of suction feeding in vertebrates. Integr Comp Biol 55:134–145 Wakefield WW (1990) Patterns in the distribution of demersal fishes on the upper continental slope off central California with studies on the role of ontogenetic vertical migration in particle flux. University of California, San Diego Westneat MW (1990) Feeding mechanics of teleost fishes (Labridae; Perciformes): A test of four-bar linkage models. J Morphol 205:269–295 Westneat MW (2004) Evolution of levers and linkages in the feeding mechanisms of fishes. Integr Comp Biol 44:378–389 Worthington J (1905) Contribution to our knowledge of the myxinoids. Amer Nat 39:625–663 Wright GM, Keeley FW, DeMont ME (1998) Hagfish cartilage. In: Jørgensen JM, Weber RE, Malte H (eds) The Biology of Hagfishes, Chapman and Hall, London, pp 160–170 Wright GM, Keeley FW, Youson JH, Babineau DL (1984) Cartilage in the Atlantic hagfish, Myxine glutinosa. Am J Anat 169:407–424 Wright GM, Keeley FW, Robson P (2001) The unusual cartilaginous tissues of jawless craniates, cephalochordates and invertebrates. Cell Tissue Res 304:165–174 Yalden DW (1985) Feeding mechanisms as evidence for cyclostome monophyly. Zool J Linn Soc 84:291–300 Ziermann JM, Miyashita T, Diogo R (2014) Cephalic muscles of Cyclostomes (hagfishes and lampreys) and Chondrichthyes (sharks, rays and holocephalans): comparative anatomy and early evolution of the vertebrate head muscles. Zool J Linn Soc 172:771–802 Zintzen V, Roberts CD, Anderson MJ, Stewart AL, Struthers CD, Harvey ES (2011) Hagfish predatory behaviour and slime defense mechanism. Sci Rep 1:131

Chapter 8

Feeding in Cartilaginous Fishes: An Interdisciplinary Synthesis Daniel Huber, Cheryl Wilga, Mason Dean, Lara Ferry, Jayne Gardiner, Laura Habegger, Yannis Papastamatiou, Jason Ramsay and Lisa Whitenack

8.1 Introduction Fishes, and elasmobranchs in particular, are often described as “opportunistic” predators meaning that they will take advantage of feeding opportunities as they arise. The implication of this term is that elasmobranchs are not selective about what they eat, which is a gross oversimplification of the complex interactions that shape diet, many of which are driven by interactions of an organism’s physiology, ecology, and behavior. These interactions typically are driven by a particular need that the organism must D. Huber (B) Department of Biology, The University of Tampa, Tampa, FL 33606, USA e-mail: [email protected] C. Wilga Department of Biological Sciences, University of Alaska Anchorage, Anchorage, AK 99508, USA M. Dean Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany L. Ferry Math and Natural Sciences Division, Arizona State University, Glendale, AZ 85306, USA J. Gardiner Division of Natural Sciences, New College of Florida, Sarasota, FL 34243, USA L. Habegger Biology Department, Florida Southern College, Lakeland, FL 33801, USA Y. Papastamatiou Marine Sciences Program, Florida International University, North Miami, FL 33181, USA J. Ramsay Biological Sciences Department, Westfield State University, Westfield, MA 01086, USA L. Whitenack Department of Biology, Allegheny College, Meadville, PA 16335, USA © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_8

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meet in order to maximize its fitness, here used in the Darwinian sense to represent the genetic contribution of an individual to the next generation. Fitness is affected by additional interactions such as competition, predator avoidance, prey acquisition, and reproduction, to name a few. These first three items can, and often do, relate directly to feeding because energy acquisition is paramount to organismal survival, and therefore to fitness. Such interactions are affected by the physiology of an organism as much as by its ecology. That is to say, the internal environment of the cartilaginous fish may dictate the nature of the interactions as much as the external environment. For example, the freshwater tolerance of a particular species or life history stage will determine how far upstream into the freshwater habitat it can range in its quest for food. Case in point, juvenile sharks of many oceanic species often selectively reside and therefore forage in estuarine habitats (e.g., Bethea et al. 2015). Similarly, visual acuity will affect how well an organism sees in low light conditions, and in turn how, when, and where it forages. For example, the white shark Carcharodon carcharias exhibits increased foraging effort and capture success when preying on seals at dawn and during a full moon (Fallows et al. 2016). Physiological constraints will also affect the distribution of prey items that the organism encounters, and therefore what ends up in its diet. This is true even if the predator is “opportunistic” and eating what it encounters indiscriminately. However, most cartilaginous fishes are not truly indiscriminate feeders (Munroe et al. 2014). While all elasmobranchs are carnivores, some will eat a broad range of food types, while others utilize a very narrow breadth of food resources. Prey selectivity, or specialization, is defined as utilizing only one or a few of the items available in the habitat (Ferry-Graham et al. 2002). The reasons for selectivity/specialization are often tied to the energetic reward of the prey item, but not exclusively so. A predator may be prevented from using other resources because it has been outcompeted, or excluded, from using the resource. Alternatively, the predator may have evolved constraints that limit its ability to utilize certain prey resources, which may or may not have been caused by competitive interactions such as the aforementioned. Furthermore, additional differences exist between a specialized diet and specialized behaviors and/or physiologies employed while acquiring that diet. In the coming sections, the major factors that influence feeding in cartilaginous fishes will be explored by investigating the sequence of events during a feeding bout from the predator’s perspective. First, you will read about how sensory systems are used to locate and target prey. You will then read about how the anatomy, mechanical properties, behaviors, and performance of the feeding mechanism influence what ends up in the diet. Finally, you will read about digestive physiology in order to understand how dietary items are utilized to meet the energetic demands of the organism. It is our hope that this integrative approach to understanding feeding in cartilaginous fishes will provide a holistic perspective on how these remarkable animals have maintained positions atop aquatic trophic systems for over 400 million years.

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8.2 Sensory Basis of Feeding Behavior 8.2.1 Sensory Cues in the Environment Feeding in cartilaginous fishes encompasses a suite of behaviors beginning with the initial detection of prey and culminating in the acquisition and digestion of food. Both live prey items and dead tissue produce an array of sensory cues including chemical odorants, hydrodynamic disturbances, sounds, visual cues, and/or weak electric fields, as well as specific tastes and textures, although the latter are only perceptible upon contact with the prey. Other cues are detectable by various sensory systems at various distances from the source (i.e., prey item), with differences in detection distance based on the physics of signal propagation in the aquatic environment and the detection threshold of the animal’s sensory systems (Figs. 8.1 and 8.2). Chemical cues produced by prey could include metabolic byproducts (urine, feces), pheromones, blood or hemolymph leaking from a wound, or, in the case of a dead prey item, the byproducts of tissue breakdown (Derby and Zimmer 2012). Single amino acids can stimulate feeding behaviors and the olfactory receptors of elasmobranchs are sensitive to minute concentrations of these compounds in the picomolar range (Hodgson and Mathewson 1971, 1978; Meredith and Kajiura 2010; Nikonov et al. 1990; Silver 1979; Silver et al. 1976; Tricas et al. 2009; Zeiske et al. 1986). Some studies have described comparatively stronger responses of olfactory neurons to more complex mixtures, such as extracts or rinses of prey items (Gilbert et al. 1964; Zeiske et al. 1986) and most behavioral studies rely on such mixtures to elicit robust food search responses (Dove 2015; Gardiner and Atema 2007, 2010; Johnsen and Teeter 1985; Kajiura 2003; Kajiura and Holland 2002), suggesting that compounds other than amino acids are also important to elicit feeding behavior. Studies have demonstrated that elasmobranchs are attracted not only to the blood and other bodily fluids released by injured prey, but also to the odor of undamaged prey, particularly when the prey is distressed (Hobson 1963; Tester 1963a, b). These chemical cues will diffuse from the source but a concentration gradient will exist only in a completely stagnant (motionless) environment, which rarely exists in nature as wind, tidal currents, and animal motions will cause water flow. Flowing water disperses odor simultaneously through advection (the transportation of odor filaments or patches) and turbulent mixing of the chemical concentrations (Atema 2012; Webster 2007; Webster and Weissburg 2001). Advection occurs at low Reynolds numbers (Re < 100) when flow is laminar, whereas at high Reynolds numbers (Re 100), turbulent mixing generates swirling packets, or eddies, that break up into a series of successively smaller eddies, creating a spatially and temporally chaotic structure known as an odor plume. As the distance from the source increases, intermolecular viscous forces dissipate turbulent energy until it is completely lost, and in this distant region (i.e., the odor far field) only very patchy odor information is available, carried by the bulk flow (Fig. 8.2). The distance over which this process occurs for biological signals is somewhat difficult to determine as it will vary with signal source strength and background noise. Hydrodynamic trails in quiet labora-

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Fig. 8.1 The general distribution of the sensory systems on the body of a a shark (bonnethead, Sphyrna tiburo), b a batoid (clearnose skate, Raja eglanteria), and c a chimera (spotted ratfish Hydrolagus colliei). Colors correspond to the sensory fields depicted in Fig. 8.2 (green  olfactory, mechanosenses  purple (light purple  lateral line system canals, dark purple dots  superficial neuromasts), red  eyes, orange  ampullae of Lorenzini). Taste buds (not shown) are located inside of the mouth and pharynx. Tactile cues are thought to be perceived by the non-pored canals of the lateral line system, free nerve endings in the skin (Roberts 1978), and by the vesicles of Savi, found in dasyatid, torpedinid, and narcinid batoids such as the lesser electric ray Narcine bancroftii (d). Based on Cornett (2006), Dider (1995), Johnson (1917), Maruska (2001), Raschi (1978), Tester and Nelson (1967)

tory environments have been estimated to be detectable at distances from the source that vary from the mm to cm range for the wake of an individual plankter to over a hundred meters for a herring (Dehnhardt et al. 2001; Yen et al. 1998). Hydrodynamic disturbances (e.g., turbulence, discussed above) might arise from prey movements, such as leg paddling, fin or tail beats, gill currents, or siphon jets, creating signals that can persist in the environment over considerable distances and durations (Hanke and Bleckmann 2004; Hanke et al. 2000). Passive wakes can also arise from ambient currents washing over an object such as a sedentary fish, and all of these signals are perceptible from the bulk flow (Dehnhardt et al. 2001; Hanke and Bleckmann 2004; Hanke et al. 2000; Coombs et al. 2007; Niesterok and Hanke 2013). Sounds could include the grinding of teeth or drumming of the swim bladder in fish, the stridulations, snapping, or rasping of crustaceans, or the vocalizations of

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Fig. 8.2 Sensory signals and their use by hunting sharks. Senses are indicated by capital letters (e.g., V  vision); asterisk (e.g., V*) denotes sense used to measure and orient to the bulk flow (i.e., by detecting environment features); no asterisk (e.g., V) denotes sense used to process prey cues; slashed (e.g., \ V ) indicates sensory block. Background colors in a–c indicate areas of signal availability corresponding to signal dispersal fields in a Behavioral phases in boxes occur at a discrete distance from the source; behavioral phases in boxed arrows occur over a distance; line arrows indicate transitions from one phase of the behavior to the next. a Physical model of prey signal fields (After Ajemian and Sanford (2007)). Prey emits a complex mixture of sensory stimuli that radiate and disperse into the habitat. Animals can detect the bulk flow vector (arrow) by measuring their drift along the walls and substrate, using vision (V*) or touch (T*) of the walls or bottom, or, by detecting turbulence in the bulk flow, with the lateral line (L). Bulk flow disperses prey odor downstream over large distances where it can be detected by olfaction (O, green); closer to the source, prey-generated wake turbulence becomes detectable by the lateral line (L, purple). Close to the source, the prey becomes directly detectable based on vision (V, red), lateral line imaging of the acoustic near field (L, delineated by purple dotted line), electroreception (E, orange), and touch (T, direct tactile contact with prey). b The blacktip shark, Carcharhinus limbatus. From downstream, the blacktip shark detects the presence of prey using O and, during the daytime, tracks the bulk flow upstream using OV* or OL. Seeing the prey, it switches to V to orient and strike from a distance (~2 m). Near the prey, the strike is adjusted using L. Then it switches to E to ram-capture the prey. With the lateral line blocked ( \ L ) it often misses the prey; successful captures involve increased ram. If \ E , it can capture prey using T; if \ T , it will miss. When approaching prey from downstream at night (under moonless conditions; \V* V \ ), it detects (O) and tracks (OL) the prey until it is at close range (~20 cm), then orients and strikes using L, but captures using less ram. If V* \ \ L , it detects the prey (O), but cannot track and ceases to feed. When approaching prey from upstream ( \ O ), it detects the prey using V and orients, strikes, and captures. If it approaches the prey from upstream at night ( \ O\ V ), it will not detect the prey and will not feed. c The bonnethead, Sphyrna tiburo. From downstream, the bonnethead detects prey using O and, during the daytime, tracks it using OV* or OL; it switches to V to orient and strike, but does so at a closer range (~1 m) than the blacktip shark, then switches to E to capture using ram-biting. When approaching prey from downstream at night ( \V* V \ ), it detects (O) and tracks the prey (OL), but cannot orient or strike and ceases to feed. If \ L , it detects prey (O), but cannot track, and ceases to feed. When V\ approaching prey from upstream ( \ O ), it detects prey using V, then orients, strikes, and captures. At night ( \V* V \ ), it detects (O) and tracks (OL) prey, but cannot orient and strike and ceases to feed. If \ E , it misses the prey even when touching it (T or \ T ). d The nurse shark, Ginglymostoma cirratum. From downstream, the nurse shark detects prey using O, then, during the daytime, tracks using OV*, OL, or OT*. At a close range, it switches to V, L, or E to orient and strike, then switches to E to suction capture the prey. At night ( \V* V \ ), it detects (O), tracks (OL or OT*), orients and strikes (L or E) as above, but modulates its capture by increasing suction and decreasing ram. When approaching prey from upstream ( \ O ), it does not detect the prey and does not feed. Like the blacktip shark, if \ E , it can still capture the prey if it touches it (T), but it misses when it does not touch ( \ T ) the prey. Nurse shark illustration copyright José Castro, with permission. Pinfish, shrimp, bonnethead, and blacktip shark illustrations copyright Diane Peebles, with permission. © 2014 Gardiner et al. 2014

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marine mammals, as well as sounds of prey movements, such as splashing, jumping, or the struggling movements of a wounded fish (Banner 1972; Kasumyan 2008; Reidenberg and Laitman 2010; Schmitz 2002). The near-field (i.e., particle motion) component of these acoustic cues extends up to one wavelength (e.g., tens to hundreds of meters), while the far-field (i.e., pressure) component may extend much further (e.g., kilometers) (Fig. 8.2). Near-field acoustic cues may be detected by the lateral line system over distances of 0.4–2.0 predator body lengths from the source (Palmer et al. 2005). Inner ear mechanisms for localization of sound cues are poorly understood for fish in general, but even more so for cartilaginous fish (Sisnero and Rogers 2016). Sharks are attracted to low-frequency sounds, particularly pulsed and/or biological sounds such as fish vocalizations, the sounds of fish feeding, and the sounds of wounded and struggling fish (Banner 1972; Myrberg et al. 1969, 1972; Nelson 1967; Nelson and Gruber 1963; Nelson et al. 1969; Richard 1968), and studies have reported cartilaginous fish responding to 25–50 Hz sounds from distances of over 400 m (Myrberg et al. 1972). However, the near-field component for such sounds would extend only tens of meters, and the manner in which cartilaginous fish detect the farfield component without a swim bladder or tympanic bladder to act as a pressure-toparticle motion transducer is unknown. Studies on elasmobranch attraction to sound in freely swimming animals have been limited to field-based work, where background noise is difficult to control and the distances from which the animals respond may be hard to accurately measure. Lab-based studies of feeding behavior have explicitly avoided considering acoustic cues, due to the issue of sound reverberation (Gardiner et al. 2014). Visual cues could include the coloration of the skin or shell, bioluminescence, or motion of the prey (Haddock et al. 2010; Rosenthal 2007). Elasmobranchs can visually discriminate between objects based on a number of different attributes, including shape, size, color, brightness, and pattern (Aronson et al. 1967; Clark 1963; Fuss et al. 2014; Graeber 1978; Tester and Kato 1966; Van-Eyk et al. 2011). Although the anatomy of the visual system has been extensively studied in elasmobranchs and holocephalans, and spectral ranges and visual fields of many elasmobranch species have been determined, the limits of visual detection are not well known (reviewed by Lisney et al. 2012). The distance from which visual cues can be perceived will be heavily influenced by the amount of available light and amount of scatter (Duntley 1963; Mazur and Beauchamp 2003), as well as the background contrast in intensity, polarization, and pattern of reflected light (Johnsen 2005; Johnsen and Sosik 2004). The general range of visual cues is thought to be on the order of tens of meters (Fig. 8.2). Bioelectric fields surround all living organisms, with direct current fields arising from the leaking of ions across the mucous membranes (mouth, pharynx, gill epithelium). These fields are modulated by respiratory movements, producing an alternating current component, and the leakage of ions may even produce electrical fields from dead organisms as well (Kalmijn 1972). The detection threshold for these signals has been measured at 0.1–5.0 nV/cm for marine elasmobranchs (Bedore et al. 2014; Haine et al. 2001; Jordan et al. 2009b, 2011; Kajiura 2003; Kajiura and

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Fitzgerald 2009; Kajiura and Holland 2002; Kalmijn 1982; Kempster et al. 2016; McGowan and Kajiura 2009; Wueringer et al. 2012), and based on the strengths of fields produced by marine prey, these cues can be detected at distances of less than a meter from the source (Bedore and Kajiura 2013; Haine et al. 2001; Kalmijn 1972) (Fig. 8.2). The sensitivity of the holocephalan electrosensory system has only been examined in one species, spotted ratfish Hydrolagus colliei, with a sensitivity threshold (0.2 μV/cm) suggesting that it uses electrical cues over distances of less than 10 cm from the source (Fields et al. 1993; Fields and Lange 1980). The electrosensory system of freshwater rays is approximately four orders of magnitude less sensitive, with thresholds ranging from 0.2–5.0 μV/cm, resulting in detection distances of 5 cm or less (Harris et al. 2015; McGowan and Kajiura 2009). Both freshwater populations of euryhaline species, which possess long, “marine-type” ampullary canals, and obligate freshwater species, which possess short ampullary canals, have similar sensitivity thresholds, suggesting that the medium has a greater effect on sensitivity than ampullary morphology. Due to the higher resistivity of freshwater, electrical signals decay more slowly than in seawater, resulting in fields that propagate further but dissipate with a shallower slope (Fig. 8.3). It is believed that elasmobranchs detect the relative change in voltage, rather than the absolute voltage, so the detection distances are longer in saltwater than in freshwater (Harris et al. 2015; McGowan and Kajiura 2009).

8.2.2 Use of Sensory Cues During Feeding The feeding sequence in cartilaginous fishes can be broken down into phases. The animal must initially detect and recognize the presence of prey, track long-distance cues to the vicinity of their source, orient to and strike at the prey through wholebody motion, move the jaws to capture the prey, and then transport the prey into the digestive system. As an animal approaches its prey and additional signals become available, the animal may perform sensory switching, focusing on the particular cue(s) that provides for the best performance in each phase of feeding (Gardiner et al. 2014). The use of sensory information during the complete behavioral sequence has only been examined in three species of sharks (Fig. 8.2b–d), but numerous studies have examined the use of sensory information during particular phases of feeding, providing partial information for a wide variety of species. The particular cues used for each behavioral task can be linked to the ecological niche of the animal because the environment in which the animal hunts and type of prey it seeks can influence the availability of sensory signals, while the manner in which it acquires food can influence how these cues are used. In many cases, elasmobranchs can substitute alternative sensory cues if their preferred cues are unavailable, allowing for successful prey capture. This behavioral plasticity may have contributed to the success of the elasmobranch fishes in a wide variety of habitats. Chemical cues can be combined in a nearly limitless number of ways, creating unique signatures that are useful for prey identification (Atema 2012). Because odor

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Fig. 8.3 Relationship between electric field strength and distance from an electrical dipole source in freshwater (left) and saltwater (right). Due to the higher resistivity of freshwater, electrical signals decay more slowly than in seawater, resulting in fields that propagate further but dissipate with a shallower slope. It is believed that elasmobranchs detect the relative change in voltage, rather than the absolute voltage, such that detection distances are longer in saltwater than in freshwater. Modified from McGowan and Kajiura (2009)

cues can be carried a great distance from the source, odor is often the first cue encountered. Numerous studies dating back to the nineteenth century (Bateson 1890) have recognized the importance of olfactory cues for feeding behavior in elasmobranchs. For some species olfactory cues are essential, and in their absence, prey may be detected but will not be recognized as food. Nurse sharks Ginglymostoma cirratum can detect and orient to the visual, electrical, hydrodynamic signals of live prey, but do not attempt to capture it unless they also perceive an attractive odor (Gardiner et al. 2014), and similar results have also been found for dusky smoothhound Mustelus canis and swell sharks Cephaloscyllium ventriosum (Sheldon 1911; Tricas 1982). In addition, the hydrodynamic trails produced by moving fish and crustaceans and the siphon jets produced by bivalves do not appear to be sufficient for prey recognition by sharks and batoids unless an attractive odor is also present (Jordan et al. 2009a; Montgomery and Skipworth 1997). Zooplankton produce fine-scale hydrodynamic wakes from swimming motions, as well as higher frequency vibrational cues from the movement of mouthparts, both of which are important signals used in prey recognition by bony fish (Montgomery 1989) and may be important for elasmobranchs that consume swimming zooplankton (Gardiner and Atema 2014), although

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this has not yet been evaluated. Many fish produce unique vocalizations, but to date, their use for prey recognition has not been assessed. Some species, such as blacktip Carcharhinus limbatus, bonnethead Sphyrna tiburo, lemon Negaprion brevirostris, blacktip reef Carcharhinus melanopterus, and gray reef Carcharhinus amblyrhynchos sharks, can recognize prey using visual cues alone (Gardiner et al. 2014; Gilbert 1963; Hobson 1963). Electrical field characteristics also differ among prey species (Bedore et al. 2014; Harris et al. 2015; Kalmijn 1972), but these cues do not appear to be useful for recognizing prey (Gardiner et al. 2014) or distinguishing between different prey species (Blonder and Alevizon 1988). Odor is often the first cue encountered by an animal approaching potential prey from downstream (Gardiner et al. 2014; Hobson 1963). To locate an odor source, animals cannot simply perform comparisons of concentrations at the two nostrils and move toward the stronger concentration (i.e., chemotaxis) because turbulence caused by random velocity fluctuations results in very steep concentration gradients that are irregular and unpredictable in both time and space (Moore and Atema 1991). Averaging the concentration of these peaks over time and moving toward the stronger average concentration would require sampling of this intermittent concentration field over several minutes, a process too slow to be of use to the animal. In fact, animals are capable of tracking odor plumes to their sources within tens of seconds, and this process appears to be due in sharks to the timing of odor cues (Moore and Atema 1991; Moore et al. 1991; Webster and Weissburg 2001; Weissburg et al. 2002). For example, dusky smoothhound sharks Mustelus canis respond to minute differences in the timing of arrival of odors at the two nostrils and turn toward the side that first receives the stimulus. This strategy steers the animal towards the center of an odor patch, from which it simultaneously uses flow and odor cues to find the source of the odor in a process known as odor-gated rheotaxis. During odor-gated rheotaxis animals determine the direction of the bulk flow and then turn upstream by assessing their drift in the flow via the lateral line, vision, or tactile cues from the substrate (Baker et al. 2002; Gardiner and Atema 2007; Gardiner et al. 2014; Hodgson and Mathewson 1971; Mathewson and Hodgson 1972; Peach 2001, 2003; Zimmer-Faust et al. 1995). This strategy would lead the animal to the vicinity of the odor plume source, at which point other sensory signals would be needed for precise localization of the prey. Animals can also follow the fine-scale structure of an odorous wake, a process termed eddy chemotaxis (Atema 1996; Gardiner and Atema 2007). Rather than simple upstream-directed swimming, animals using eddy chemotaxis follow the same path taken by their prey as they track the fine-scale eddies of the flavored wake. Such fine-scale wake tracking has been observed in sharks and other fish, as well as copepods and pinnipeds (Dehnhardt et al. 2001; Gardiner and Atema 2007; Pohlmann et al. 2001, 2004; Schulte-Pelkum et al. 2007; Yen et al. 1998). Hydrodynamic trails produced by aquatic prey can persist in the environment and remain detectable for some time, even against the background noise of the bulk flow (Niesterok and Hanke 2013). Eddy chemotaxis may be used until the predator is within the range of other sensory cues or may be used to track the odor plume to its source, a strategy that is particularly useful in the dark (Gardiner and Atema 2014; Gardiner et al. 2014).

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Acquiring prey requires precise coordination of whole body (i.e., striking) and jaw (i.e., capture) movements. Animals that have tracked an odor plume from downstream typically switch to other directional cues to precisely localize their prey prior to executing these tasks (Gardiner and Atema 2007; Gardiner et al. 2014; Hobson 1963; Hodgson and Mathewson 1971; Mathewson and Hodgson 1972; Tester 1963a). If an animal approaches the prey from a direction other than downstream, it will not encounter the odor field. In such cases, species that can recognize prey using nonolfactory cues can proceed to orient, strike, and capture the prey (Gardiner et al. 2014; Hobson 1963). Species that rely exclusively on odor for prey recognition may display indications of perceiving the presence of the prey, such as orientating the body or lifting the head, but will not initiate a strike in the absence of olfactory cues and therefore will not feed (Gardiner et al. 2014; Sheldon 1911; Tricas 1982). The cues utilized for these final phases of feeding behavior appear to be tightly linked to the feeding strategy of the animal. Species that rely on predominantly ram-based capture (i.e., forward motion of predator’s body overtakes prey) must use cues that can allow the animal to localize the prey from a sufficient distance for the animal to accelerate prior to reaching the target. Ram-based strikes are often initiated from a distance of one or more body lengths, necessitating the use of long-range directional cues. Vision appears to provide the best information for this task, allowing animals to orient to their prey from a distance of several body lengths (Gardiner et al. 2014; Gilbert 1963; Hobson 1963). Acoustic cues have been suggested to play a role, but studies involving live, dead, or artificial prey are complicated by the simultaneous presentation of visual and acoustic cues (Hobson 1963). Some species are also capable of orienting to the prey using the lateral line system, but since these cues can only be detected at shorter distances, the forward velocity of the strike will be reduced (Gardiner et al. 2014, 2016). For species that predominantly utilize suction-based capture (i.e., prey is drawn into the mouth via induced changes in fluid pressure), the striking phase of capture is reduced and may consist only of turning the head to align the mouth with the prey (Gardiner et al. 2014, 2016). These animals need only localize their prey from a short distance and can therefore rely either on long-distance directional cues (e.g., vision), intermediate-distance directional cues (e.g., near-field acoustic, detected by the lateral line) or very short-range cues (e.g., electrical) to accomplish this task (Fouts and Nelson 1999; Gardiner et al. 2014; Tricas 1982). Electrical cues have not been sufficient for ram-feeding sharks to orient to live prey in the water column (Gardiner et al. 2014), although several species of sharks will orient to and nudge or bite at the source of dipole electric fields presented on the substrate (Haine et al. 2001; Jordan et al. 2011; Kajiura 2003; Kajiura and Fitzgerald 2009; Kajiura and Holland 2002; Kalmijn 1971, 1982; Kempster et al. 2016), as well as live, buried prey (Kalmijn 1971). These results suggest that electrical cues may prove useful for ram-strikes from a close distance, particularly for benthic prey. Although studies of the entire sensory sequence of feeding in batoids are lacking, odor elicits food search behaviors in skates, rays, and sawfish, and these animals display behavioral patterns that are consistent with odor plume tracking in sharks (Bedore et al. 2014; Blonder and Alevizon 1988; Harris et al. 2015; Jordan et al.

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2009a, b; Kalmijn 1971; Kempster et al. 2016; Wueringer et al. 2012). Once excited by food odor, batoids will orient to and bite at the sources of hydrodynamic (Jordan et al. 2009a; Montgomery and Skipworth 1997) and electrical cues (Bedore et al. 2014; Blonder and Alevizon 1988; Harris et al. 2015; Kalmijn 1971; Kempster et al. 2016; McGowan and Kajiura 2009; Wueringer et al. 2012). The final phase of feeding requires that the animal correctly time jaw movements at the end of the strike in order to capture prey. Ram-feeding sharks generally decelerate slightly at the end of a high-speed strike in order to increase the accuracy of capture, which has also been observed in ram-feeding teleosts. Lateral line cues are essential for this behavior, likely because these final moments just prior to capture are not visually mediated as a result of the laterally positioned eyes (Gardiner and Atema 2014; Gardiner et al. 2014; McComb et al. 2009). Electrical cues can be perceived within this range, triggering jaw depression in species like bonnethead sharks Sphyrna tiburo, which relies so exclusively on the electrosensory system to initiate capture that it fails to move the mouth when electrical cues are blocked (Gardiner et al. 2014) (Fig. 8.2c). Other species such as blacktip sharks Carcharhinus limbatus, nurse sharks Ginglymostoma cirratum, and torpedo rays Torpedo marmorata will initiate jaw depression in response to tactile cues (Belbenoit 1986; Gardiner et al. 2014). The use of tactile cues, perceived by the non-pored canals of the lateral line system and possibly the vesicles of Savi, may also guide jaw movements in batoid species that trap their prey against the substrate prior to capture using a tenting behavior (Maruska and Tricas 1998, 2004; Mulvany and Motta 2014). Some species can adjust to the use of different sensory information in the striking phase by modulating the kinematics of prey capture, within their anatomical limits (Gardiner et al. 2016). Ram-feeding animals typically begin capture at the end of a high-velocity strike initiated using long-distance cues where the prey is typically positioned directly in front of the mouth. When blacktip sharks strike from proximity in the dark using lateral line cues, the prey is less precisely positioned, but the shark can overcome this by repositioning the head earlier and to a greater degree. It can also decrease the amount of ram used, but likely cannot increase the amount of suction because the small labial cartilages do not laterally occlude the gape, precluding effective suction generation. Suction feeding animals such as nurse sharks Ginglymostoma cirratum, which possess laterally occluded mouths, can actively increase the amount of suction used while simultaneously decreasing ram, which may aid in capturing prey that is less precisely positioned. Even though visual cues could allow this species to strike from a greater distance, its body shape is suited to slower, more maneuverable swimming, which may limit the degree to which it can increase forward ram, but may increase capture success if prey flees in a “zig-zag” fashion. Other species, such as bonnethead sharks Sphyrna tiburo, may have more rigid requirements for striking behavior (e.g., exclusive reliance on vision for prey in the water column) and the initiation of capture (e.g., exclusive reliance on electroreception); capture will either proceed in a fairly stereotyped fashion or will fail to occur when the required cues are unavailable. Species with more intermediate anatomical characteristics (e.g., body suited to reasonably rapid swimming, but also larger labial folds) typically use a combination

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of ram and suction to capture prey and may be capable of greater modulation than animals that specialize on one feeding modality or the other. For example, spiny dogfish Squalus acanthias and leopard sharks Triakis semifasciatus modulate prey capture with respect to prey size (Ferry-Graham 1998; Wilga 1997) and may be capable of modulation in response to changes in sensory information, although this has not been directly investigated. The ability to modulate feeding behavior with respect to sensory information may be linked to behavioral ecology as well. For example, blacktip sharks Carcharhinus limbatus are primarily diurnal hunters, but juveniles can be found in both clear waters and murky habitats where visibility may be limited to less than a meter (Bethea et al. 2015), thereby limiting the potential interplay between sensory modalities during a feeding event. Likewise, nurse sharks are nocturnal hunters that have been observed to suck prey from crevices in the reef, clearly relying on senses other than vision (Motta et al. 2008). After capture, an animal must decide whether to retain (swallow) a prey item or reject it. Taste buds, which are found in the oropharyngeal cavity of cartilaginous fishes (Atkinson and Collin 2012; Cook and Neal 1921; de Sousa Rangel et al. 2016; Ferrando et al. 2012; Tester 1963a; Whitear and Moate 1994a, b), are poorly understood but appear to function in this behavior. For example, sharks will reject prey items that have been stripped of taste cues, are non-food items, or are non-preferred food items (Gardiner and Atema 2007; Hobson 1963; Tester 1963a). Tactile cues have also been implicated in food acceptance, with sharks capturing and subsequently rejecting non-food items that have been soaked in food flavors, presumably based on texture (Gardiner and Atema 2007; Hobson 1963).

8.3 Prey Capture Providing that adequate sensory information has been obtained to localize prey items, the capture of those prey items by cartilaginous fishes is contingent upon the use of anatomical structures in diverse behaviors to mechanically capture, process, and ingest prey. Despite the relative lack of taxonomic diversity among cartilaginous fishes compared to bony fishes, they possess a considerable diversity of feeding mechanisms and strategies, which have been investigated through a wide range of anatomical, theoretical, experimental, and field-based studies.

8.3.1 Anatomy of the Feeding Apparatus Despite over 400 million years of evolutionary history and substantial morphological change from the ancestral condition (Figs. 8.4 and 8.5), the anatomy of the feeding apparatus of cartilaginous fishes remains composed of a relatively small number of structures interacting in a relatively simple mechanical arrangement. Unlike teleosts, which have approximately 60 bones within the head, chondrichthyan fishes possess

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Fig. 8.4 Left lateral view of the cranial skeletons of three Palaeozoic sharks. a Jaws of Cladodus elegans superimposed on the braincase of “Tamiobatis sp”. b Jaws and braincase of Cladodoides wildungensis. c Jaws and braincase of Orthacanthus. Not to scale. Reproduced with permission from Ginter and Maisey (2007)

only 10 cartilages in the head (Motta and Huber 2012; Motta and Wilga 2001). The two halves of the upper jaw, or palatoquadrates, and lower jaw, or Meckel’s cartilages, are connected to the chondrocranium via the hyomandibular cartilages, the dorsal components of the hyoid apparatus, and the nature of this connection both varies among clades and is pivotal in determining feeding modality (Fig. 8.5) (Wilga 2002; Wilga et al. 2007). The ceratohyal cartilages and interconnecting unpaired basihyal cartilage comprise the ventral hyoid apparatus, forming the ventral surface of the buccal cavity; these ventral elements connect to the hyomandibular cartilages in sharks and to the branchial cartilages in batoids. These elements are the primary actuators of prey capture, although the branchial arches, comprised of basibranchial, hypobranchial, ceratobranchial, epibranchial, and pharyngobranchial cartilages, function with the hyoid apparatus in the hydraulic transport of prey items into the digestive tract. Notably, cartilaginous fishes lack jaws on the pharyngeal apparatus, which are commonly used for prey processing by teleost fishes (Motta and Huber 2012; Wilga et al. 2007).

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Fig. 8.5 Left lateral views of cranial skeletons depicting the anatomy of various jaw suspension mechanisms including a autodiastyly (hypothetical ancestral state); b amphistyly (Pleuracanthus, Xenacanthida); c orbitostyly (Chlamydoselachus, Chlamydoselachida); d orbitostyly (Squalus acanthias, Squaliformes); e hyostyly (Sphyrna, Carcharhiniformes); f euhyostyly (Rhinobatos, Batoidea). C, ceratohyal; E, ethmoidal articulation; EP, epihyal; H, hyomandibula; O, orbital articulation; L, lower jaw; P, postorbital articulation; U, upper jaw. Reproduced with permission from Wilga (2002)

Jaw suspension, which has a considerable effect on jaw mobility, is determined by the degree to which the palatoquadrate articulates with the chondrocranium (e.g., via ethmoidal, orbital, and/or postorbital articulations), the degree of preservation of the hyoid apparatus (e.g., broken or intact), and the orientation of the hyomandibular cartilages (Wilga 2005; Wilga et al. 2007). All of these attributes vary with respect to phylogeny, ultimately resulting in phylogenetic variation in jaw mobility, which has generally increased over the course of evolutionary history (Schaeffer 1967). The ancestral condition for cartilaginous fishes may be an autostylic jaw suspension in which the palatoquadrate was connected to the chondrocranium through ethmoidal and orbital articulations, and the hyoid apparatus was intact, but not suspensory (Fig. 8.5) (Grogan and Lund 2000). The basal split among chondrichthyans into holocephalans (e.g., chimeras, ratfishes) and elasmobranchs (e.g., sharks, rays, skates) was largely associated with the fate of the jaw suspension. The holostylic condition,

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characterized by fusion of the upper jaw to the chondrocranium and a non-suspensory hyoid arch that is morphologically and functionally a branchial arch, evolved in holocephalans, while the hyostylic conditions, characterized by suspension of the jaws via the hyomandibular cartilages, evolved in elasmobranchs (Huxley 1876). Several hyostylic conditions have evolved, which differ in the nature of the articulations between the palatoquadrate and cranium. Basal sharks such as cladoselachians and Hexanchiformes evolved an amphistylic condition characterized by ethmoidal and postorbital articulations (Fig. 8.5) (Wilga 2002). Orbitostyly, characterized by a prominent orbital articulation and loss of the ethmoidal and postorbital articulations, is characteristic of squaliform sharks, which exhibit enhanced jaw kinesis relative to amphistylic species (Wilga 2002). However, hexanchiform sharks also have an orbital articulation, and are unique in having two jaw suspension types, orbitostyly and amphistyly (Wilga 2002). The hyostylic jaw suspension mechanism is found in sharks of the orders Heterodontiformes, Orectolobiformes, Carcharhiniformes, and Lamniformes, and is characterized by an ethmoidal articulation and loss of the postorbital articulation (Wilga 2002). Some lamniform species evolved an additional palatonasal articulation, while lamnid species subsequently lost the ethmoidal articulation (Wilga 2005). Finally, batoid elasmobranchs possess a euhyostylic jaw suspension (i.e., true hyostyly) in which the hyoid apparatus is not intact and the hyomandibular cartilages are the only connection between the upper jaw and chondrocranium (Gregory 1904). In accordance with this considerable change, the batoids exhibit the greatest degree of jaw kinesis among the cartilaginous fishes, with species such as lesser electric rays Narcine bancroftii able to protrude the jaws 100% of the head length during prey capture, as well as protrude the jaws asymmetrically (Fig. 8.6) (Dean and Motta 2004; Moss 1977; Wilga 2002; Wilga and Motta 1998b; Wilga et al. 2007). While multiple articulations between the palatoquadrate and cranium can limit jaw mobility, the length of the articular ligaments ultimately determines the extent of jaw kinesis (Wilga 2002). The evolutionary increase in the role of the hyomandibular cartilages in supporting the jaws and accommodating feedingrelated forces is reflected in reinforcement of these cartilages over evolutionary history through increased size, cortical mineralization, and trabecular reinforcement (Balaban et al. 2015; Dean et al. 2006; Huber 2006; Wilga et al. 2007). The muscles of the feeding apparatus have also remained fairly consistent in a relatively simple mechanical arrangement throughout the evolutionary history of cartilaginous fishes, with major changes occurring in the batoid radiation (Motta and Wilga 2001). While the morphological change in muscles naturally accompanies the evolution of the skeletal system, the majority of these changes in sharks are associated with the upper jaw (Motta and Wilga 2001); presumably, the critical role of lower jaw depression in feeding and breathing has limited musculoskeletal changes in the system. The coracomandibularis muscle depresses the lower jaw, while the coracoarcualis–coracohyoideus muscle complex depresses the hyoid arch, with minor variation in insertion, origin, and relative size among sharks (Fig. 8.7) (Motta and Wilga 2001; Wilga et al. 2001). The adductor mandibulae complex is comprised of the quadratomandibularis muscles, which extend between the upper and lower jaws, and the preorbitalis muscles, which extend from the cranium to the upper

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Fig. 8.6 Skeletal elements of the feeding mechanism of the lesser electric ray Narcine bancroftii depicted in anterior, dorsal, and ventral views in the resting state (left), symmetrically protruded state (center), and asymmetrically protruded state (right). The magnitude and asymmetrical ability of jaw protrusion in batoids is thought to be due to the euhyostylic jaw suspension mechanism in which in which the hyoid apparatus is not intact and the hyomandibular cartilages are the only connection between the upper jaw and chondrocranium. HYM, hyomandibula; MC, Meckel’s cartilage; NC, neurocranium; PQ, palatoquadrate. Reproduced with permission from Dean and Motta (2004)

jaw (Motta and Wilga 2001). There are at least two divisions (dorsal and ventral) of the quadratomandibularis muscles, with as many as five subdivisions within the dorsal division (Fig. 8.7) (Motta and Wilga 2001). The quadratomandibularis muscles typically adduct the jaws, but may also protrude the upper jaws, like the preorbitalis, if the lower jaw is held open (Wilga et al. 2001). Muscles of the upper jaw have subdivided multiple times, independently throughout phylogenetic history. These subdivisions have led to alterations in muscle orientation, although muscle origins, insertions, and functions have remained relatively

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Fig. 8.7 Cranial and pharyngeal musculature of the spiny dogfish Squalus acanthias in lateral view (top), superficial ventral view (bottom left), and deep ventral view (bottom right). AM, adductor mandibulae; BTC, branchial trematic constrictor; CC, coracoarcualis; CH, coracohyoideus; CM, coracomandibularis; CU, cucullaris; DHC, dorsal hyoid constrictor; DSBC, dorsal superficial branchial constrictor; EBM, epibranchial; HTC, hyoid trematic constrictor; HYP, hypoxia; IH, interhyoideus; IM, intermandibular; LH, levator hyomandibularis; LP, levator palatoquadrate; MC, Meckel’s cartilage; PO, preorbital; PQ, palatoquadrate; SP, spiracular; VHC, ventral hyoid constrictor; VSBC, ventral superficial branchial constrictor. Reproduced with permission from Fishbeck and Sebastiani (2008)

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consistent (Motta and Wilga 2001; Wilga et al. 2001). However, the lengthening and shortening of the jaws have caused some changes in muscle orientation that have brought about associated changes in muscle function (Wilga et al. 2001). For example, as the jaw and hyoid cartilages lengthened and the jaw joint moved to a more posterior position in the carcharhiniform clade, the vertical orientation of the upper jaw retractor muscle (i.e., levator palatoquadrate) became shifted horizontally, thereby functioning to protract the upper jaw (Fig. 8.7) (Wilga et al. 2001). In contrast, shortening of the jaw and hyoid cartilages in orectolobiform and heterodontiform sharks moved the jaw joint to a more anterior position, which also led to a horizontal orientation of the upper jaw retractor muscle, although in this case function was conserved (Wilga et al. 2001). The retractor muscles of the hyoid arch, the levator hyomandibular, has remained relatively consistent with minor changes of insertions onto surrounding elements (Fig. 8.7) (Motta and Wilga 2001). Multiple subdivisions have evolved in nearly every muscle of the batoids feeding apparatus. Perhaps the freeing of the upper jaw from the cranium combined with decoupling of the ventral hyoid elements from the jaw suspension released constraints on the jaws, allowing movement in directions not possible with an intact hyoid arch and palatocranial articulations (Kolmann et al. 2014, 2016; Wilga and Motta 1998a, b); unlike sharks, the jaws of skates and rays can depress and adduct asymmetrically (Fig. 8.6) (Dean and Motta 2004; Gerry et al. 2008, 2010). New muscles also evolved within batoids to move the cranium vertically (levator and depressor rostri), to depress and retract the hyomandibular cartilage (coracohyomandibularis, depressor hyomandibularis), and to depress the lower jaw (depressor mandibularis) (Fig. 8.8) (Miyake 1988; Miyake et al. 1992).

8.3.2 Prey Apprehension Despite the relative simplicity of the feeding apparatus, cartilaginous fishes have evolved a considerable range of prey capture modalities including ram, suction, filter, and bite, collectively enabling species of this clade to consume a tremendous breadth of food resources ranging from zooplankton to whales (Frazzetta 1994; Moss 1977; Motta et al. 1997; Motta and Wilga 2001). Bite and suction feeding are the two extremes in this continuum of feeding modalities, and differ by whether the predator directly contacts the prey with the jaws or the prey is drawn to the predator’s mouth via the induction of water flow. While some species are obligate bite or suction feeders (e.g., Motta et al. 2008; Tricas and McCosker 1984), many species employ varying degrees of both behaviors during prey capture and transport, the latter of which requires hydraulic movement of prey through the pharynx into the esophagus, even in bite feeders (Norton and Brainerd 1993; Wainwright 1999; Wilga and Motta 1998a). Biting, which is the process of seizing prey between the jaws and/or decreasing prey size to manageable pieces for ingestion (Wilga and Motta 1998a), is suggested to be the basal prey capture mode in elasmobranchs (Maisey 1980; Moy-Thomas

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Fig. 8.8 Cranial and pharyngeal musculature of the southern guitarfish Rhinobatos percellens in lateral view (left) and ventral view (right). AMM, adductor mandibulae medial; AML1, adductor mandibulae lateral 1; AML2, adductor mandibulae lateral 2; CC, coracoarcualis; CH, coracohyoideus; CHM, coracohyomandibularis; CM, coracomandibularis; CU, cucullaris; DHC, dorsal hyoid constrictor; DM, depressor mandibularis; DR, dorsal rectus; DSBC, dorsal superficial branchial constrictor; EP, epaxial; MC, LH, levator hyomandibulae; LVR, levator rostri; Meckel’s cartilage; PO, preorbital; PQ, palatoquadrate; RO, rostrum; SCC, scapulocoracoid cartilage; SP, spiracular; VHC, ventral hyoid constrictor; VSBC, ventral superficial branchial constrictor

and Miles 1971; Schaeffer 1967). While ram (i.e., swimming to prey) is typically used to get the predator close to the prey, most sharks use biting to apprehend the prey (Motta and Wilga 1999). For example, cookie-cutter sharks Isistius spp. have an oversized lower jaw with serially fused teeth, fleshy lips, and modified pharyngeal muscles that allow them to firmly impale the upper jaw into prey items then excising a circular flesh plug using the lower jaw (Compagno 1984; Shirai and Nakaya 1992). The geometry of these plugs is so characteristic that the feeding ecology of these rare sharks has largely been surmised from wounded prey such as whales and even humans (Dwyer and Visser 2011; Papastamatiou et al. 2010; Ribéreau-Gayon et al. 2016). Several elasmobranch species also use bite mechanisms to crush prey with specialized teeth (see Tooth Form and Function below). Suction feeding is widely represented in cartilaginous fishes, having evolved independently in virtually every lineage, with extreme specializations in horn sharks (Heterodontiformes) and carpet sharks (Orectolobiformes) (Motta 2004). Morphological specializations for suction feeding in elasmobranchs include a small mouth opening that is laterally occluded by folds of skin supported by large labial cartilages, small teeth, and hypertrophied hypobranchial muscles (Motta et al. 2002, 2008; Motta and Wilga 1999). Rapid buccal expansion draws a stronger influx of water when focused through a smaller mouth opening, and indeed horn sharks Heterodontus franscisi, bamboo sharks Chilosciyllum plagisum, and nurse sharks Ginglymostoma cirratum are capable of extreme suction performance, generating intraoral pressure as low as −110 kPa (Huber 2006; Motta et al. 2002, 2008; Wilga and Sanford 2008). Despite

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the undeniable power of suction feeders, this feeding modality is limited in that suction generation decreases as the inverse cube of distance (e.g., ~one mouth width distance into the water column). However, feeding next to a substrate triples the effective strike radius and decreases the degree of accuracy needed while striking (Nauwelaerts et al. 2007), perhaps explaining why most suction feeding species are benthic or feed in complex environments. Many species, like spiny dogfish Squalus acanthias (Squaliformes) and white-spotted bamboo sharks Chiloscyllium plagiosum (Orectolobiformes), initially acquire prey via suction and subsequently reduce prey via biting (Wilga and Motta 1998a). Ram feeding is probably the least common mode of prey capture in Chondrichthyes. This occurs when small prey is completely taken through the mouth opening and into the pharynx by the forward motion of the fish; if the jaws close on the prey as it passes through the mouth, then biting has occurred in addition to ram feeding. Ram feeding is the sole mechanism for prey capture by continuous filter feeders, which has evolved independently among the Orectolobiformes, Lamniformes, and Batoidea clades. The apprehension of zooplankton, squid, or schools of fish can be accomplished using ram or suction, after which prey are trapped by a variety of branchial filtering mechanisms (Fig. 8.9) (Motta et al. 2010; Paig-Tran et al. 2013; Wilga et al. 2007). Whale sharks employ surface or subsurface ram filter feeding (i.e., slow swimming at the water’s surface or below with an open mouth), as well as suction feeding (i.e., maintaining a relatively stationary position in the water column while suctioning) (Motta et al. 2010; Motta and Wilga 2001; Nelson and Eckerd 2007; Taylor 2007). Like whale sharks, megamouth sharks are thought to use suction to apprehend prey, although buccal expansion presumably increases drag that potentially can decrease the filtering rate below optimal filter feeding models (Heithaus 2004; Nakaya et al. 2008; Sims 2000). Basking sharks and manta rays use subsurface ram filter feeding, with the latter also using cephalic lobes to funnel prey into the mouth (Fairfax 1998; Motta and Huber 2012; Motta and Wilga 2001; Notarbartolo-Di-Sciara and Hillyer 1989; Sims 2000). Projections arising from the branchial arches vary in complexity among filterfeeding elasmobranchs. Megamouth sharks Megachasma pelagios and basking sharks Cetorhinus maximus possess filamentous gill rakers that are superficially similar to those of teleosts. Whale sharks Rhincodon typus and manta rays (Mobulidae) possess reticulated gill rakers in the shape of filtering pads covered by dermal denticles that may protect the filtration system from oversized food particles (Fig. 8.9) (Motta et al. 2010; Paig-Tran et al. 2011, 2013; Paig-Tran and Summers 2014). Beyond the variety of behaviors used to acquire planktonic prey, the mechanisms of prey accumulation on the gill rakers may vary among species (e.g., cross-flow filtration, vortex filtration, sieving, direct interception, inertial impaction, gravitational deposition, diffusion deposition) with respect to prey particle size, filtration rate, and gill raker anatomy (Motta et al. 2010; Paig-Tran et al. 2011, 2013; Rubenstein and Koehl 1977). Interestingly, most filter feeding predators have a relatively low number of electrosensory receptors on the head, likely owing to the lack of elusivity of zooplanktonic prey, and perhaps also to differences in the electrical signatures of these prey (Kempster et al. 2012; Mulvany and Motta 2013).

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Fig. 8.9 Filter feeding mechanism of the whale shark Rhincodon typus showing a the position of the filtering mechanism within the head; b gross morphology of the lower filtering pads (white ruler  15 cm); c an upper filtering pad of with inset showing representative 1 cm square area of the irregular shaped holes of the reticulated filtering mesh; d external view of an upper left pad with secondary vanes that direct water laterally into the parabrachial chamber and over the gill tissue (gt) before it exits the pharyngeal slit (not shown) (white square  1 cm2 ); and e a close-up of a section through a lower left filtering pad showing the reticulated mesh (rm), primary vanes (pv), secondary vanes (sv), and gill tissue (gt). Water flow is through the mesh, between the primary and secondary vanes, and over the gill tissue. (white square  1 cm2 ). Reproduced with permission from Motta et al. (2010)

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Feeding modes used by cartilaginous fishes appear to vary according to habitat use and prey type, rather than phylogenetic proximity (Ajemian and Sanford 2007; Wainwright 1999). Chain catsharks, Scyliorhinus rotifer (Scyliorhinidae), capture prey almost exclusively with suction in deep water habitats, while closely related swellsharks, Cephaloscyllium ventriosum (Scyliorhinidae), capture prey with the jaws in shallow habitats (Ajemian and Sanford 2007).

8.3.3 Jaw Kinematics The general mechanism for opening and closing the jaws is conserved, with variation in the timing and magnitude of kinematic events correlated with feeding modality (Motta 2004; Motta and Huber 2012). Suction capture events are relatively rapid, and typically last ~100–400 ms, while bite captures can take nearly 2 s to complete (Motta et al. 2008; Tricas and McCosker 1984). The mouth opening or expansive phase starts with depression of the lower jaw triggered by the coracomandibularis muscle and depression of the hyoid apparatus by the coracoarcualis and coracohyoideus muscles; these processes are independent and occur in parallel rather through a coupled linkage as in actinopterygian fishes (Wilga et al. 2007). In the mouth closing or compressive phase, the jaws are adducted and the upper jaw protruded by the quadratomandibularis and preorbital muscles, with assistance by the levator palatoquadrate muscles in Carcharhiniformes. By the end of the compressive phase in a successful capture event, the prey is either between the jaws or within the buccopharyngeal cavity. Finally, in the recovery phase, the upper jaw and hyomandibular are retracted back under the cranium by the levator palatoquadrate and levator hyomandibularis, and the other skeletal elements return to the resting position (Figs. 8.7 and 8.8) (Motta 2004; Motta and Wilga 1999; Wilga et al. 2001, 2007). A preparatory phase, which entails a decrease in buccal volume by jaw adduction and hyoid elevation prior to the expansive phase and functions to increase volumetric expansion of the feeding mechanism, may occur prior to mouth opening during suction capture and processing events, but may also occur after a missed strike, prior to a subsequent strike attempt (Motta et al. 2008; Wilga and Motta 1998a; Wilga et al. 2007). Upper jaw protrusion, the anteroventral movement of the palatoquadrate during jaw closure is a characteristic event during feeding in most cartilaginous fishes (Motta and Wilga 1999, 2001; Wilga et al. 2001). Various hypotheses exist regarding the efficacy of jaw protrusion, including reduced time to jaw closure, reorientation of the jaws to facilitate prey gouging, and changing the angle of tooth attachment to facilitate prey gouging (Frazzetta 1994; Tricas and McCosker 1984; Wilga 2005; Wilga et al. 2001). The extent of upper jaw protrusion varies among cartilaginous fishes and is related to the length of the craniopalatine ligaments more than the jaw suspension type (Wilga 2002; Wilga et al. 2007). For example, lemon sharks Negaprion brevirostris can protrude the upper jaw 18% of head length with their hyostylic jaw suspension, whereas spiny dogfish Squalus acanthias can protrude the upper jaw 30% of head length with their orbitostylic jaw suspension (Wilga 2002).

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Lesser electric rays Narcine bancroftii, have extreme jaw protrusion reaching up to 100% of head length, and batoids in general appear to be capable of modulating the direction and magnitude of protrusion (Fig. 8.6) (Dean Bizzarro and Summers 2007; Dean and Motta 2004; Gerry et al. 2010). Modulation of prey capture behavior based on food type or size appears to be more common in bony fishes than in cartilaginous fishes (Ferry-Graham 1998; Liem 1980). This seems to be especially true in specialized feeders like the nurse shark that requires rapid movements of the feeding apparatus to ingest prey (Matott et al. 2005). However, modulation based on prey type has been found among several species of batoids, where prey elusivity triggers changes in jaw opening times (Mulvany and Motta 2014). Modulation in prey capture kinematics is also found in blacktip sharks Carcharhinus limbatus and nurse sharks Ginglymostoma cirratum, which vary between bite and suction feeding based on selective elimination of sensory systems (Gardiner et al. 2016). Chewing or multiaxial movement of the jaws relative to each other used to break down food has historically been associated with mammals and the pharyngeal jaws of teleosts. However, a recent study reported this behavior in freshwater stingrays and the degree of jaw mobility needed to consume prey in this manner is likely facilitated by the presence of a euhyostylic jaw suspension mechanism (Kolmann et al. 2016).

8.3.4 Feeding Performance Bite force has been a widely used metric for the investigation of feeding in vertebrates, including cartilaginous fishes, as it is directly related to food acquisition and therefore to survival (Huber et al. 2005, 2006, 2008). High bite forces have been shown to reduce prey processing time, thereby increasing the efficiency of energy intake during feeding (Verwaijen et al. 2002), and facilitate enhanced understanding of feeding ecology by providing insights into dietary specialization, niche partitioning, and ontogenetic dietary variation (Dumont et al. 2012; Habegger et al. 2012; Huber et al. 2009; Kolmann and Huber 2009). Cartilaginous fishes offer an interesting model to investigate bite force owing to the simplicity of their feeding apparatus, a wide range of dietary guilds, and the large range of sizes achieved by this group (Huber et al. 2009; Motta 2004; Motta and Huber 2012). The study of bite force has been performed through a variety of methods ranging from voluntary in situ measurements and in vivo measurements during tetanic muscle stimulation to theoretical models based on jaw lever mechanics and computational simulations based on finite element analysis (Habegger et al. 2012; Huber and Motta 2004; Huber et al. 2005, 2006, 2008; Kolmann et al. 2015a; Mara et al. 2012; Wroe et al. 2008). Bite forces vary widely among cartilaginous fishes (from 12 N in velvet belly lantern sharks Etmopterus spinax to 6000 N in bull sharks Carcharhinus leucas). Although in some cases extremely high bite forces are more related to large body size than functional necessity (Habegger et al. 2012; Huber et al. 2009; Wroe et al.

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2008), other cases demonstrate linkages between biting performance and dietary specialization, such as in durophagous species (Huber et al. 2005, 2008; Kolmann and Huber 2009; Kolmann et al. 2015a). For example, horn sharks Heterodontus francisci, spotted ratfish Hydrolagus colliei, and cownose rays Rhinoptera bonasus produce high mass-specific bite forces in association with reinforced dentition, hypertrophied jaw adductor muscles, and high leverage jaws (i.e., high mechanical advantage) to consume hard prey such as sea urchins, gastropods, and bivalves (Huber et al. 2005, 2008; Kolmann and Huber 2009; Kolmann et al. 2015a; Summers et al. 2004). The armaments of these prey items may even exceed the stiffness of the cartilaginous jaws used to capture them, representing an intriguing biomechanical/ecological system (Motta and Huber 2012). Regardless of trophic specialization, bite force among vertebrates is influenced by a suite of morphological characteristics including adductor muscle size and architecture, head width, jaw length, and jaw leverage, with head width generally being the most predictive morphometric correlate of vertebrate bite force (Habegger et al. 2012; Herrel et al. 2005; Huber et al. 2009). Habegger et al. (2012) conducted a phylogenetic analysis of available chondrichthyan feeding biomechanics data and found that phylogenetic increases in bite force can be attributed to both size-independent and size-dependent factors. For example, phylogenetic increases in body size are correlated with absolute increases in bite force, head size, jaw length, and adductor muscle size, increased trophic level, and decreased consumption of benthic prey, thereby indicating that ascension to apex predator status is associated with an overall increase in absolute body and head size, and departure from the benthos. Alternatively, mass-specific increases in bite force, which have occurred in holocephalan, heterodontid, orectolobid, and carcharhinid lineages, are associated with relative increases in head size, adductor muscle size, and mechanical advantage (i.e., a measure of how the position of muscle attachment to the jaws affects the proportion of muscular force transmitted to the prey) (Habegger et al. 2012). These differences in absolute (size-independent) and relative (size-dependent) bite force reflect alternative evolutionary strategies for elevated trophic position and competition reduction via trophic specialization respectively, although these are not mutually exclusive (e.g., both occur in carcharhinid sharks). The scaling of bite force provides further examples of trophic specialization via enhanced feeding performance. Bite force scales isometrically over six orders of magnitude of body mass variation among cartilaginous fishes (Habegger et al. 2012; Huber et al. 2009), yet tends to exhibit positive allometry in young and/or small, benthic species. For example, durophagous horn sharks Heterodontus franciscsi, spotted ratfish Hydrolagus colliei, and cownose rays Rhinoptera bonasus all exhibit positive allometry of bite force which allows earlier access to the relatively competitor free niche of hard prey consumption (Huber et al. 2008; Kolmann and Huber 2009; Kolmann et al. 2015a). Blacktip sharks Carcharhinus limbatus and juvenile bull sharks Carcharhinus leucas also exhibit positive allometry of bite force, although in these cases it appears related to the consumption of relatively large, not hard, prey (Habegger et al. 2012; Huber et al. 2006). Notably, bull sharks exhibit isometry of bite force when all age classes are considered, which along with the previously noted

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inter-specific isometry, indicates that selection for high bite force is relaxed at very large body sizes, at which point additional force becomes functionally irrelevant (Habegger et al. 2012; Huber et al. 2009). While high bite forces are related to the consumption of mechanically challenging food, some studies have shown that unique behaviors (e.g., repetitive adductor muscle firing patterns, cyclical bite force application, multidimensional chewing behavior) can facilitate this process (Huber et al. 2005; Kolmann et al. 2016; Wilga and Motta 2000), and that tooth cutting performance may be far more influential a determinant of feeding success than bite force in non-durophagous species. Sharp teeth and rapid jaw movements apparently overcome bite force limitations in teleost predators such as king mackerel Scomberomorus cavalla and great barracuda Sphyraena barracuda, which happen to have among the lowest mass-specific bite forces of all fishes (Ferguson et al. 2015; Habegger et al. 2011).

8.3.5 Skeletal Composition and Mechanical Properties Successful prey capture is contingent upon the mechanical performance of the skeleton given its roles in transmitting forces from the musculature to the surrounding environment (e.g., bite forces) and in resisting the forces imposed upon it by the environment (e.g., prey reaction forces). Although the structure of the chondrichthyan skeleton is rather unique, it has the same chemical constituents as other vertebrate skeletons (e.g., water, proteoglycans, collagen, and a form of calcium phosphate mineral known as hydroxyapatite) and is a fascinating example of the hierarchical, composite design that is ubiquitous throughout biodiversity (e.g., Haversian bone, mollusk shell, arthropod skeleton) (Chen et al. 2008; Currey 2008; Dean et al. 2009; Eames et al. 2007; Liem et al. 2001; Omelon et al. 2014). Examination of these systems reveals emergent mechanical properties at larger scales (e.g., stiffness + toughness of whole skeletal elements) owing to the mixture of structural materials at smaller scales (e.g., mineralized cartilage + unmineralized cartilage) and the resulting interaction between their constituent properties (e.g., elasticity + viscosity). Most skeletal elements of the elasmobranch feeding mechanism (i.e., those other than teeth) are composed of tessellated cartilage, in which unmineralized cartilage is surrounded by a cortex of mineralized blocks known as tesserae and wrapped in a fibrous perichondrium (Fig. 8.10) (Dean et al. 2009; Maisey 2013). Tessellated cartilage, which is an apomorphic feature of the cartilaginous fishes, is thought to be a structural adaptation to facilitate the growth of mineralized skeletal elements that are incapable of remodeling at a large scale; tessellation allows for volumetric increase of the unmineralized cartilage core while tesserae grow via hydroxyapatite accretion within the perichondral surface of the unmineralized cartilage (Dean et al. 2009; Maisey 2013; Seidel et al. 2016). Holocephalans have lamellar sheets of mineralization that pass through, not around, skeletal elements, and the extent to which these structures are homologous to tesserae is unknown (Lund and Grogan 1997; Rosenberg 1998).

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Fig. 8.10 Structure of tessellated skeletal elements in the elasmobranch feeding mechanism. a CT reconstruction of the blue shark Prionace glauca with red boxes indicating imaging locations of b, c. (b) Cross-sectional structure of a tessellated skeletal element with mineralized tesserae [T(c)] surrounding a core of uncalcified cartilage [UC] and overlain by a fibrous perichondrium [PC]; the inset image provides a schematic view of the tissue relationships, as well as the fibrous joints between tesserae (Cryo-SEM image from the jaws of Urobatis halleri). (c) CT reconstruction of a jaw joint showing tesseral surface [T(s)] without the perichondrium (jaw joint CT scan from Urobatis jamaicensis). Reproduced with permission via Creative Commons user license (https:// creativecommons.org/licenses/by-nc-nd/4.0/) from Liu et al. (2014)

Unmineralized cartilage is a chondrocyte-rich tissue consisting of a gelatinous extracellular matrix (ECM) of water and proteoglycans, laden with Type II collagen fibers (Dean and Summers 2006; Enault et al. 2015; Liem et al. 2001). It is elastic in compressive loading owing to negatively charged glycosaminoglycan side chains on the proteoglycans (e.g., chondroitin sulfate, keratin sulfate), the hydrophilic natures of which maintain the turgidity of unmineralized cartilage in the unloaded state (Carter and Wong 2003; Liem et al. 2001). Uniaxial compression tests of unmineralized cartilage from the jaws of 10 shark species have found stiffness values (i.e., stress: strain ratio; indicative of the ability to resist deformation) ranging from 0.010–0.079 GPa, with a median value (0.050 GPa) that is just 0.3% of the stiffness of human Haversian bone (~20 GPa) (Fig. 8.11) (Currey 1998; Ferrara et al. 2013; Jagnandan and Huber 2010; Porter et al. Unpublished; Wroe et al. 2008). Similarly, the ultimate strength (i.e., stress at which complete structural failure occurs) of elasmobranch unmineralized cartilage (range: 0.008–0.042 GPa; median: 0.009 GPa) is just 4.2% that of human Haversian bone (~0.213 GPa) (Currey 1998; Porter et al. Unpublished). Although these values are generally greater than those of mammalian articular cartilage, they are extremely low compared to virtually any mineralized skeletal tissue (Currey 2008; Laasanen et al. 2003). Notably, variation in the stiffness and ultimate strength of elasmobranch unmineralized cartilage bears little correlation with feeding ecology (e.g., durophagous vs. piscivorous species), likely owing to the principal role of the mineralized jaw cortex in resisting applied stress (Ferrara et al. 2011).

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Fig. 8.11 Stiffness of elasmobranch skeletal tissues (no fill), materials (light gray fill), and elements (dark gray fill) in comparison to human Haversian bone (dashed line spanning all data). Lines with dots represent data for which there are single values. Rectangles represent ranges of values with inset dashed lines representing median values. Data compiled from Balaban et al. 2015 (a), Ferrara et al. 2013 (b), Li et al. Unpublished (c), Porter et al. Unpublished (d), Whitenack et al. 2010 (e), and Wroe et al. 2008 (f)

Tesserae contain unmineralized cartilage, as well as globular and prismatic mineralized cartilages. Globular mineralized cartilage is found on the endochondral surfaces of tesserae and consists of fused spherules of hydroxyapatite (~40–55 nm in diameter), whereas prismatic mineralized cartilage is found on the perichondral surfaces of tesserae and consists of aggregations of hydroxyapatite dense enough to spectrally refract light (Dean and Summers 2006; Kemp and Westrin 1979; Orvig 1951). Nanoindentation of prismatic mineralized cartilage has found stiffness values ranging from 20–40 GPa, comparable to human Haversian bone and a full three orders of magnitude greater than that of unmineralized cartilage. Stiffness variability appears related to local variation in hydroxyapatite mineral density, which can exceed that of mammalian bone and calcified cartilage (Fig. 8.11) (Currey 1998; Li et al. Unpublished). The concentric accretion of mineral appears to create periodic variation in stiffness which is believed to facilitate fracture resistance within tesserae by dissipating crack energy as it arrives at the interface of materials with different moduli. This correlation between local mineral density and local material properties (e.g., stiffness) is characteristic of mineralized elasmobranch skeletal elements such as vertebrae and hyomandibulae, in which small increases in mineral content yield dramatic gains in stiffness (Balaban et al. 2015; Currey 2008; Huber et al. 2013; Porter et al. 2006, 2007). This is perhaps best represented in the most heavily mineralized tissues of the chondrichthyan skeleton, enameloid (~98% hydroxyapatite

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by weight) and the two forms of dentine (~71% hydroxyapatite by weight), osteodentine, and orthodentine, which have stiffness values 70 GPa, 28 GPa, and 23 GPa respectively (Moyer et al. 2015; Vogel 2003; Whitenack and Motta 2010b). Given the composite nature of tesserae, it is no surprise that they have intermediate material properties relative to the unmineralized and prismatic mineralized cartilages of which they are composed. Nanoindentation studies of whole tesserae have found stiffness values ranging from 0.119 GPa in white sharks Carcharodon carcharias to 4.05 GPa in round stingrays Urobatis halleri (0.6–20.3% of human Haversian bone stiffness)) (Fig. 8.11) (Currey 1998; Ferrara et al. 2013; Wroe et al. 2008). The significant variation within these values is intriguing given that the associated studies utilized “nano”-indentation techniques. Variation in specimen preparation and indenter size seems to explain this variation, as these attributes ultimately determine whether the tests are investigating intrinsic material properties at the nanoscale, or something better approximating micro/mesoscale properties of the whole tesseral element. Interestingly, anisotropy (i.e., material property variation with respect to loading direction) has been found in both unmineralized cartilage and tesserae (Ferrara et al. 2013), suggesting variation in the distribution and function of ultraand microstructural constituents within these tissues. Although the functional implications of these variations for jaw function are unknown, it is possible that anisotropy could be related to the compression bias of tessellated cartilage, which distributes more stress to tesserae loaded in compression than to those loaded in tension (Liu et al. 2010). At a larger scale, anisotropy in tessellated cartilage from the jaws of blue sharks Prionace glauca loaded parallel to the tessellated layer yielded stiffness values approximately twice those of loading perpendicular to the tessellated layer (Liu et al. 2014). This greater stiffness during parallel loading is due to the compression of adjacent intertesseral joints, which are otherwise placed in tension during perpendicular loading, and indicates that the geometry and orientation of elasmobranch skeletal elements and their constituent tesserae will greatly affect their mechanical performance. For example, the major axis of blue shark jaws is aligned dorso-ventrally such that prey contact forces during feeding are applied parallel to the major axis along which the tessellated jaw cartilage exhibits greater stiffness (Fig. 8.10). Were the major axis to be oriented in the latero-medial direction, for example, prey contact forces would be applied perpendicular to the major axis and the mechanical performance of the jaw would be greatly diminished (Liu et al. 2014). The relationship between the orientation of a skeletal element and its mechanical performance is reflected in its structural properties, those which are dictated by material distribution; the material properties described above are those which are dictated by material composition. The most commonly investigated structural property in feeding biomechanics is the second moment of area, a cross-sectional attribute of skeletal elements that affects their ability to resist bending, the principal mode of jaw loading during prey capture (Summers et al. 2004; Wainwright et al. 1976). For a given volume of skeletal material, the farther that material is distributed from the central axis of a skeletal element in the direction of loading, the greater its second moment of area and ability to resist bending under that load will be. This is because

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stress increases with distance from the central (i.e., “neutral”) axis of a skeletal element. The effect of increasing second moment of the area can easily be envisioned by considering the flexion of a meter stick when loaded parallel or perpendicular to its major axis; much less flexion occurs during parallel loading when more material is distributed in the direction of loading. Second moment of the area can, therefore, be increased by lengthening the major (i.e., longer) axis of a skeletal element in the direction of loading (e.g., the blue shark jaw described above) and/or by thickening the tessellated cortex of the skeletal element (e.g., multilayered tesserae described below). Single-layered tesselation appears to be the ancestral condition for tessellated cartilage as it is the most widespread form throughout extant elasmobranchs and is present in some of the most basal fossil chondrichthyans (Maisey 2013). However, up to six layers of tesserae have been found in the jaw cartilages of extant sharks and rays which have high bite forces associated with either large body size or durophagous feeding habits (Fig. 8.12). This cortical reinforcement indicates adaptation to mechanical loading in that it increases the second moment of area, and thereby increases resistance to bending and torsion (Dingerkus et al. 1991; Summers 2000). Whereas the relationship between skeletal tissue material properties and feeding ecology is yet to be determined, elasmobranch jaw structural properties have clear associations with diet. Durophagous sharks and rays, such as horn sharks Heterodontus francisci and spotted eagle rays Aetobatus narinari, have cortical distributions of tesserae that resist bending 35X and 20X better than a solid rod of equivalent crosssectional area (i.e., “moment ratio”), respectively. These values are greater than those of various piscivorous lamniform sharks (e.g., goblin Mitsukurina owstoni, sand tiger Carcharias taurus, crocodile Pseudocarcharias kamoharai, salmon Lamna ditropis, shortfin mako Isurus oxyrinchus), which have moment ratios ranging from 5X–20X (Luger et al. 2015; Summerset al. 2004). All of these jaws also have peaks in second moment of area beneath the jaw joints and posterior teeth, both of which are regions that experience high compressive loads during feeding, suggesting predictable organization of jaw structure in sharks independent of phylogeny and ecology (Huber et al. 2005, 2008; Luger et al. 2015; Summerset al. 2004). These parameters clearly have a developmental component as well, as tessellated skeletal elements increase in mineralization during growth such that second moment of area increases by three orders of magnitude over ontogeny in H. francisci (Seidel et al. 2016; Summers et al. 2004). In addition to variation in jaw geometry and cortical thickening as means of increasing second moment of area, jaw structure is also reinforced in some species via trabeculation, the formation of mineralized struts that pass through the lumen of a skeletal element, connecting and transmitting stress between the cortical layers. Trabeculation, which is a common means of optimizing weight and strength in animal skeletons (e.g., mammalian spongy bone, echinoid test, porcupine quills; Currey 2008; Seilacher 1979; Vincent and Owers 1986), has been found in the jaw cartilages of myliobatid stingrays, jaw and hyomandibular cartilages of lesser electric rays Narcine bancroftii, and jaw and basicranial cartilages of Cretaceous hybodont sharks (Dean et al.2006; Lane and Maisey 2012; Summers 2000). In the myliobatid

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Fig. 8.12 Upper jaw (palatoquadrate cartilage) of the cownose ray Rhinoptera bonasus with tooth plates removed illustrating skeletal reinforcement via cortical thickening and trabeculation. The cortex (orange) of the jaws is thickened with multiple layers of tesserae, whereas trabeculae are also made of tesserae and span the lumen between the upper and lower surfaces of the jaw. Image courtesy of R. Seidel and M. Dean

stingrays, these struts form orthogonal to the tooth plates to resist jaw flexion during hard prey consumption, whereas those found in N. bancroftii are largely oriented parallel to the occlusal surface of the jaws to resist buckling during ballistic protrusion of the jaws into the sediment when capturing prey (Figs. 8.6 and 8.12) (Dean et al. 2006; Summers 2000). Although trabeculation can be induced as a plasticity response to mechanical loading in bony vertebrate skeletons (Barak et al. 2011), its presence prior to birth in cownose rays Rhinoptera bonasus and manta rays Manta birostris suggest at least some phylogenetic component to their presence (Summers 2000). A limited number of experimental and modeling studies have examined the mechanical performance of whole elasmobranch skeletal elements, finding additional evidence for the relationship between mechanical performance and feeding ecology. For example, the stiffness of hyomandibular cartilages from white-spotted bamboo sharks Chiloscyllium plagiosum (0.106 GPa), which are powerful suction feeders, was greater than that of spiny dogfish Squalus acanthias (0.042 GPa), dusky smoothhounds Mustelus canis (0.058 GPa), and sandbar sharks Carcharhinus plumbeus (0.050 GPa), with variation among species related to the percentage of mineralization in cross-sectional area (Fig. 8.11) (Balaban et al. 2015; Wilga et al. 2007; Wilga and Sanford 2008). Flexural stiffness of the hyoid arch elements in dusky smoothhound sharks Mustelus canis increases allometrically over ontogeny, in association with a shift in diet to increasingly hard prey (Wilga et al. 2016). Jaw viscoelasticity

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(i.e., tendency to exhibit rate-dependent material properties) decreases over ontogeny in the lesser spotted dogfish Scyliorhinus canicula, which is also correlated with an ontogenetic increase in the consumption of hard prey. Decreased viscoelasticity is likely related to the development of tesseral mineralization which should tend to mitigate the contribution of the viscoelastic unmineralized cartilage that dominates the skeletal elements of younger animals (Fahle and Thomason 2008; Liu et al. 2014; Seidel et al. 2016). Studies utilizing Finite Element Analysis (FEA), a computational modeling technique that integrates material and structural properties to calculate stress and strain distributions, have provided insights into elasmobranch jaw function. Simulations of the jaws of white sharks Carcharodon carcharias using heterogeneous cartilaginous models (i.e., mineralized cortex surrounding unmineralized core) and hypothetical bony models have been used to explore the mechanical consequences of the loss of bone in the chondrichthyan skeleton (Wroe et al. 2008). As expected, bony jaws exhibited higher stress and lower strain, but bite force was only 4.4% lower for cartilaginous jaws, suggesting that the adoption of a more compliant skeletal system has not compromised the biting performance of cartilaginous fishes (Wroe et al. 2008). Comparative FEA modeling of jaw performance in C. carcharias and sand tiger sharks Carcharias taurus has found that the tessellated cortex of the jaws experiences stresses up to an order of magnitude greater than the unmineralized cartilage core of the jaw, clearly identifying the cortex as the mechanically relevant component of the jaws (Ferrara et al. 2011). Additionally, jaw stress and bite force exhibited less variability with respect to gape angle in C. carcharias, indicating that its jaws are better suited to withstand the forces associated with consuming large prey such as marine mammals (Ferrara et al. 2011; Martin et al. 2005).

8.4 Tooth Form and Function 8.4.1 Tooth Structure and Morphology Chondrichthyan teeth are superficially composed of a thin layer of enameloid (0.2–0.9 mm thick) present in either a monolayer of randomly oriented hydroxyapatite crystals as in basal lineages, or as a triple-layered structure consisting of a layer of single-layered enameloid, under which are layers of parallel-fibered (i.e., tension resisting) and tangle-fibered (i.e., compression resisting) enameloid as in neoselachians (Gillis and Donoghue 2007; Preuschoft et al. 1974; Whitenack and Motta 2010b). The complexity of this enameloid microstructure in neoselachians is thought to facilitate more complex prey capture mechanisms and increase the mechanical integrity of serrations in more recent lineages (Andreev 2010; Duffin and Cuny 2008). The base of all elasmobranch teeth is comprised of osteodentine, which resembles bone in that the osteodentine forms tubules surrounding vascular canals comparable to the structure of osteons, whereas the crown may be composed

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Fig. 8.13 a Schematic of generalized osteodont (left) and orthodont (right) elasmobranch tooth histotypes (Moyer et al. 2015; Schnetz et al. 2016). EN, enameloid (dark gray); OR, orthodentine (white); OS, osteodentine (light gray); PC, pulp cavity (black). b Scanning electron micrograph of enameloid microstructure. Scale bar represents 100 μm. DEJ, dentine–enamel junction; OS, osteodentine; PFE, parallel-fibered enameloid; SLE, single-layered enameloid; TFE, tangle-fibered enameloid

of osteodentine or orthodentine, the latter of which has a much “smoother” appearance owing to the lack of vascular canals (Fig. 8.13) (Compagno 1988; Mertinene 1982; Moyer et al. 2015; Whitenack and Motta 2010b). These tissues are arranged into a stunning array of tooth morphologies among chondrichthyans, ranging from triangular blades, to teeth with multiple cusps or cusplets, to flat molar-like shapes (Fig. 8.14). Typically, extant elasmobranch teeth are categorized based on putative qualitative function and morphology together (Cappetta 1987, 2012; Frazetta 1988; Moss 1977; Motta and Huber 2012), though tooth morphology is also influenced by phylogeny. Teeth with triangular, lingolabially flattened cusps are categorized as “cutting type”, and may have serrations as well as inclined or notched cusps. Examples include many sharks of the family Carcharhinidae, particularly on the upper jaw, as well as white sharks Carcharodon carcharias. Teeth with tall, narrow cusps that are usually smooth are categorized as “tearing type” and are thought to function best in the puncture. Examples include many sharks of the order Lamniformes such as makos Isurus spp. and sand tiger sharks Carcharias taurus, as well as the lower jaw teeth of some Carcharhinus species. Small teeth, with or without lateral cusplets, are in the “clutching type” category and are typically used for grasping rather than damaging prey. These are often found in orectolobids, scyliorhinids, and male dasyatids and rajids (Cappetta 2012). Molariform teeth are either described as “crushing type” or “grinding type”, a distinction made by Cappetta (2012) based on the flatness of the cusp and tooth size; “crushing type” teeth are smaller, more numerous, and bulbous while “grinding type” teeth are larger, hexagonal, and flatter, forming a tooth plate. Examples of “crushing type” include many rajids, dasyatids, rhinobatids, and starry smoothhound sharks

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Mustelus asterias, while examples of “grinding type” include myliobatid stingrays (Fig. 8.14). Dentition also can vary with a jaw (monognathic heterodonty), between the upper and lower jaws (dignathic heterodonty), ontogenetically, and/or between the sexes. Cappetta (2012) places elasmobranchs with strong monognathic and/or dignathic heterodonty in subcategories under the morphotypes above. The “cutting-clutching subtype” (a subtype of cutting type), tend to have cutting-type teeth on one jaw and clutching type on the other, such as sixgill sharks Hexanchus griseus and squaliform sharks including dogfish Squalus spp., gulper sharks Centrophorus spp., and kitefin sharks Dalatias licha. Similarly, “clutching-grinding” is a subtype of “grinding type”, and is only represented by heterodontids which have clutching type teeth anteriorly and molariform teeth posteriorly. Alternatively, the “crushing-grinding subtype” encompasses batoids with monognathic heterodonty. Pastinachus is the only extant genus that fits into this category, with symphysial “crushing teeth” while the remainder of the jaw is filled with “grinding teeth” (Fig. 8.14) (Cappetta 2012). Holocephalans do not fit neatly into any of these categories. Each holocephalan has three pairs of tooth plates with the lower jaw bearing a mandibular set and the upper jaw bearing symphyseal and vomerine sets (Fig. 8.14) (Didier et al. 2012). Collectively, these plates create an anterior cutting edge and a posterior molariform surface used to cut and process prey, respectively (Didier 1995; Huber et al. 2008). Unlike elasmobranchs, which replace the teeth with varied frequency, the tooth plates of holocephalans continually grow throughout life without serial replacement (Luer et al. 1990; Moss 1967; Reif et al. 1978; Wass 1973).

8.4.2 Tooth Function Teeth are used to damage prey. This damage can occur to maintain a grip on the prey item to prevent escape, to divide prey into a manageable size for ingestion, or to process prey for digestion (e.g., chewing insects in ocellate river stingrays Potamotrygon motoro (Kolmann et al. 2016) or cracking crab carapaces in bonnethead sharks Sphyrna tiburo (Mara et al. 2010; Wilga and Motta 2000)). The three elements involved in damaging prey are cutting, puncturing, and breaking, with each of these modes of damage involving some degree of elastic stretching, viscoelasticity, and fracture (Schofield et al. 2016). For example, during the interaction between a shark tooth and a teleost fish, the tooth apex locally compresses the prey item as the shark bites down. The tissue surrounding the compressed area elastically stretches under tension, the magnitude of which is dependent on the velocity with which the tooth is applied to the prey item and the material properties of the prey item (e.g., stiffness (E), yield stress (σY ), fracture toughness (Gc )). This rate-dependent performance of the prey item represents its viscoelasticity and the combination of compression and tension creates an effective shear stress, which fractures the tissue if the shear stress is large enough to overcome the threshold determined by the material properties of the prey (Frazetta 1988; Schofield et al. 2016; Williams and Patel 2016). This model

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Fig. 8.14 Examples of chondrichthyan tooth types including “cutting type” (a, tiger shark Galeocerdo cuvier; b, white shark Carcharodon carcharias), “clutching type” (c, nurse shark Ginglymostoma cirratum), “tearing type” (d, sand tiger shark Carcharias taurus), “crushing type” (e, smoothhound shark Mustelus canis), “grinding type” (f, spotted eagle ray Aetobatus narinari), chimera tooth plates (g, spotted ratfish Hydrolagus colliei), “crushing-grinding subtype” (h, cowtail stingray Pastinachus sephen), “cutting-clutching subtype” (i, bluntnose sixgill shark Hexanchus griseus), and “clutching-grinding subtype” (j, Port Jackson shark Heterodontus portjacksoni)

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for puncturing soft tissues also works for crushing hard tissues such as mollusk shell, though less deformation tends to occur in these materials. For a tooth engaged in lateral cutting or draw, similar to that of a steak knife, much of the above applies. Shear stress still is generated due to compression under the tooth’s cutting edge and tension in the surrounding tissue, and a cut is generated if the prey’s failure threshold is overcome. This threshold will be determined by the prey’s material properties, as well as by the relative degrees of force applied in lateral (e.g., head shaking) and downward (e.g., biting) motions, represented by the “slicepush ratio” (ξ). The amount of downward force required to achieve fracture decreases as ξ increases (Atkins 2016), which is conceptually intuitive; cutting through meat with a steak knife is easier when the knife is drawn through the meat as it is pushed down, as opposed to only pushing down on the knife. The link between elasmobranch tooth morphology and function has only recently been investigated quantitatively. Cutting (unidirectional draw) and puncturing performance has been investigated in a variety of individual bladed selachian teeth on both soft and hard prey (Whitenack and Motta 2010a). While some “cutting-type” teeth, such as the notched teeth of tiger sharks Galeocerdo cuvier and the laterally inclined teeth of great hammerhead sharks Sphyrna mokarran, performed well in cutting and poorly in puncturing, few clear relationships were found between the cutting performance of individual teeth and their morphology (Whitenack and Motta 2010a). The majority of bladed teeth included in this study were able to puncture blue crab Callinectes sapidus carapace without breaking, despite the fact that many of those species do not include hard prey in the diet. Often, teeth that were categorized as “cutting-type” and “tearing-type” were able to cut through prey equally well, indicating that morphology cannot always be used to assign a single function. The exception were teeth that were distally inclined enough to present a flat surface during puncture, such as those of blue sharks Prionace glauca, great hammerheads Sphyrna mokarran, and tiger sharks Galeocerdo cuvier. These “cutting-type” teeth were not able to puncture prey consistently, but were able to perform well in draw, suggesting that the designated morphotype is predictive of function. Crushing performance of generalized “molariform” tooth models on snail shells has also been investigated (Crofts and Summers 2014). While domed (convex) and flat teeth performed better than concave teeth (i.e., they required less force to fracture shells), teeth with thin and tall central cusps actually performed best. While many chondrichthyans have convex or flat teeth (particularly batoids), no chondrichthyans have a morphology that matches the best performing engineered tooth model of Crofts and Summers (2014), begging the question of why this portion of tooth morphospace is unoccupied. The hazy relationship between tooth morphology and function is likely due, in part, to the balance between prey cutting/crushing performance and the structural integrity of the tooth (Crofts and Summers 2014; Whitenack and Motta 2010a; Whitenack et al. 2011). For example, if a tooth is easily broken or dulled on a shorter time scale than a species’ tooth replacement schedule, then performance is likely reduced, which can have fitness consequences owing to reduced prey capture ability. Furthermore, a tooth functions in concert with other teeth, both within

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a given jaw and with teeth from the opposing jaw, an attribute seldom accounted for in tooth performance studies. Dynamic testing of serial arrangements of teeth in bidirectional draw has been tested on four species of sharks that would be classified by Cappetta (1987) as “cutting type”, despite the fact that these teeth differ considerably (Corn et al. 2016). The teeth of three shark species (tiger Galeocerdo cuvier, sandbar Carcharhinus plumbeus, silky Carcharhinus falciformis) performed equally well in cutting, while those of bluntnose sixgill sharks Hexanchus griseus performed poorly. These multi-tooth findings are contrary to single-tooth results that found no difference in unidirectional draw performance between H. griseus and G. cuvier (Whitenack and Motta 2010a). The manner in which teeth are connected to the jaws can also affect tooth function. Elasmobranchs exhibit an acrodont form of dental attachment, in which the tooth bases lay on the occlusal surfaces of the jaws and are not set in a socket. Connection to the jaws occurs via a thick dental ligament composed of flexible collagen and elastin fibers (Ramsay and Wilga 2007). At a glance, attaching teeth to the jaws with flexible connections may seem counterintuitive, especially when teeth are being used to grip, impale, tear, and crush struggling prey. However, several possible advantages of this mode of attachment have been hypothesized. For example, the large blade-like cutting teeth of carcharhinids and Carcharodon spp. could be held flatter when not in use and become more erect during prey capture as tension increases in the dental ligament during mouth opening (Frazzetta and Prange 1987; Powlik 1995). These two positions would reduce the probability of self-inflicted injury and increase the chances of prey puncture, respectively (Frazzetta 1994; Frazzetta and Prange 1987; Powlik 1995). The benefits of flexible tooth attachment also extend beyond the initial event of prey contact. Processing of prey that has been seized by the jaws utilizes biting to drive teeth farther into the tissue or compress prey to the point of tissue failure, and lateral head-shaking to draw the mediolateral facing tooth blades through prey tissues in order to excise large chunks (Whitenack and Motta 2010a). Flexible tooth attachment may facilitate processing behaviors by allowing teeth with cutting and tearing-type dentitions to shift laterally or pivot anteroposteriorly while they are embedded into prey tissue (Frazzetta 1994; Powlik 1995). For example, white shark teeth may contact bone as they penetrate into a seal. If the teeth are unable to cut into the bone, or contact it an angle that would cause labiolingual pivoting of the tooth, the tooth may fracture under the load. However, if the teeth can shift laterally via a flexible attachment to the jaw, they would passively move slightly around the obstruction with less risk of fracture (Powlik 1995). Furthermore, Carcharodon jaws are curved, such that the labiolingual surfaces of the teeth at the jaw tips face more anteroposteriorly, but those of the more lateral teeth face more mediolateral. Anteroposterior pivoting of the lateral teeth would reduce the chance of binding in prey tissue and hindering the cutting action of the anterior teeth during head shaking (Frazzetta 1988, 1994). Flexible tooth attachment can increase the versatility of elasmobranch dentitions as well. Most orectolobiform sharks and narcinid rays possess clutching-type dentitions, thought to be useful for gripping soft-bodied prey such as fish (Cappetta

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1987). However, the clutching dentition of white-spotted bamboo sharks Chiloscyllium plagiosum is also used to crush tough prey such as crustaceans (Dean et al. 2008; Ramsay and Wilga 2007). During prey capture, the teeth are held erect due to tension in the dental ligament resulting from long axis rotation of the contralateral halves of the jaws and posterior pulling of the skin and connective tissues attached to the dental ligament during jaw protrusion and adduction (Ramsay and Wilga 2007). The erect teeth and lingually facing tooth cusps and cusplets will penetrate and secure soft prey in the mouth, especially if the prey is struggling to free itself from the jaws. However, if the prey is hard or tough and resists puncture, the flexible attachment allows for lingual rotation of the teeth at the bases to form a pavement of overlapping cusps. This tooth rotation moves the larger and flatter labial faces of the teeth into a more parallel position relative to the occlusal plane of the jaws, thus forming an uneven surface for crushing, reminiscent of the crushing type dentition (Fig. 8.15) (Dean et al. 2008; Ramsay and Wilga 2007). Finally, teeth are just one component of a larger tool, the jaws, and aspects of jaw anatomy such as the shape of the occluding surfaces, position of the jaw joint, and flexibility of the jaw symphyses can therefore also affect tooth function (Dean et al. 2008; Ramsay and Wilga 2007). For example, the jaw joint is ventrally offset from the occlusal planes of the jaws in bamboo sharks and most other orectolobiform sharks, allowing the occlusal planes to remain in a more parallel position relative to each other as the jaws open and close. This more parallel alignment of the occlusal planes facilitates the clutching and crushing ability of these species’ dentitions, as it allows many teeth to contact and grip prey simultaneously, reminiscent of a pair of channel-locking pliers. In batoids such as the lesser electric ray Narcine bancroftii, flexible tooth attachment, and jaw symphyses allow extensive medial rotation of the jaws and reorientation of the teeth during benthic feeding such that prey is grasped by the tooth cusps of the left and right halves of the jaws while sediment is hydraulically winnowed from the orobranchial cavity. Heterodontid sharks have enlarged occlusal planes in their anterior and posterior regions of the jaws, which bear clutching and molariform teeth respectively (Cappetta 1987). Molariform teeth in the enlarged posterior region reduce the probability of tooth failure owing to their expanded surface areas, which ironically also reduces the stress applied to hard prey items crushed by these teeth. However, heterodontids alleviate this issue by having their molariform teeth arranged as tight labiolingual-directed rows with the lingual side of each tooth in contact with the labial side of next tooth in the row, reminiscent of a masonry arch. The combined shape of the jaws and occlusal pattern of the molariform teeth create specific points of contact, thereby localizing the stresses applied to prey. Some batoids, such as Pastinachus and Rhina have undulating occlusal surfaces along the jaws with numerous small teeth, creating numerous points of contact with prey (Underwood et al. 2015). However, Kolmann et al. (2015b) found little difference in crushing performance when comparing different jaw curvatures in myliobatiform jaws. Laminform sharks, such as shortfin makos Isurus oxyrinchus which have tearing or cutting dentitions, have a jaw joint that is in-line with the occlusal planes of the jaws. As the jaws close, the teeth come together in a posterior to anterior progression

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Fig. 8.15 Normal clutching position (a, b) and the rotated crushing position (c, d) of the teeth of the white-spotted bamboo shark Chiloscyllium plagiosum. a, b Illustration and cross-sectional photograph of teeth on the occlusal surface of the palatoquadrate in the normal clutching position. c, d Illustration and cross-sectional photograph of teeth on the occlusal surface of Meckel’s cartilage in the rotated crushing position. DL, dental ligament; JC, jaw cartilage; RL, root lobes. Reproduced with permission from Ramsay and Wilga 2007

to shear tissue similar to a pair of scissors (Frazzetta 1988). In Isurus, the teeth on the anterior end of the jaws are not as flattened labiolingually as the posterior teeth. Thus, the anterior teeth have reduced mediolateral cutting edges with longer cusps that are angled lingually, but with the cusp tips recurved labially (Cappetta 1987; Frazzetta 1988). The posterior teeth are more flattened labiolingually, have finer cutting edges with central cusps that do not recurve labially, and may be at a slight posterior angle. The function of these two tooth shapes is revealed when out-levers and bite force vectors are calculated for the jaws and teeth. At the anterior teeth the steep angle

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between the tooth cusp and the surface of the jaws would reduce the alignment of the tooth cusps with the forces applied to the prey, but the labial recurving increases the alignment of the tooth cusp with the bite force. Furthermore, the lack of the labial recurves on the posterior teeth keeps bite force in-line with the cusp of the teeth in that area. Therefore, both tooth types can effectively penetrate prey, perforating the tissue to facilitate tearing.

8.4.3 Tooth Morphology and Diet Tooth morphology is clearly related to diet in some chondrichthyans, such as those durophagous taxa with molariform teeth. For example, the diet of horn sharks Heterodontus francisci consists of approximately 90% hard prey (e.g., echinoids, molluscs, crustaceans), while white-spotted eagle rays Aetobatus narinari and holocephalans such as spotted ratfish Hydrolagus colliei eat predominantly mollusks (Ajemian et al. 2012; Johnson and Horton 1972; Quinn et al. 1980; Schluessel et al. 2010; Segura-Zarzosa et al. 1997; Strong 1989; Wingert et al. 1979). However, these links can seldom be made for elasmobranchs with non-molariform teeth. The relationship between tooth shape and diet (presence/absence by taxon (e.g., cephalopod, gastropod, teleost)) from all of the non-filter feeding shark families have been investigated, and with the exception of the molariform-toothed durophages, there is no relationship (Whitenack and Kolmann, unpublished data). Tooth morphology may not correlate with diet because elasmobranchs tend to have taxonomically varied diets. For example, although tiger sharks Galeocerdo cuvier have cutting teeth with characteristic notches that facilitate sawing through sea turtle carapaces (Fig. 8.14), they also eat a variety of teleosts, elasmobranchs, birds, crustaceans, and other prey items for whom that infamous notch bears no relevance (Compagno 1984; Lowe et al. 1996; Papastamatiou et al. 2006). In fact, not a single shark species that eats only one taxonomic prey type (Whitenack and Kolmann unpublished). Even the bonnethead Sphyrna tiburo, which has been characterized as a blue crab Callinectes sapidus specialist, will also feed on shrimp, other crustaceans, and cephalopods (Bethea et al. 2007; Compagno 1984; Cortés et al. 1996). Little is known about the mechanical variation within taxonomic groupings of prey (e.g., teleost fishes) or across taxonomic groups. For example, Whitenack and Motta (2010a) found that some shark teeth could cut some fish prey, but not others, depending on scale thickness, skin thickness, and body stiffness; information on the material properties of prey items (e.g., hardness, toughness) are lacking for most “soft” prey. While a reclassification of prey types based on material properties may reveal links between chondrichthyan tooth morphology and diet, feeding is not the only biological role of teeth. Male elasmobranchs will grip females with their teeth during mating (Pratt and Carrier 2001; Springer 1967), and some elasmobranchs have sexually dimorphic dentitions including squaliform sharks such as Halaelurus and Deania, some scyliorhinids, Heterodontus portusjacksoni, and batoids such as Urolophus, Raja, Aptychoterma, and Dasyatis species (Bigelow and

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Schroeder 1953; Compagno 1984, 1988; Ellis and Shackley 1995; Fedducia and Slaughter 1974; Geniz et al. 2007; Gutteridge and Bennett 2014; Kajiura and Tricas 1996; McCourt and Kerstitch 1980; Powter et al. 2010; Pratt and Carrier 2001). Male Atlantic stingrays Dasyatis sabina seasonally change their tooth morphology from molariform to clutching-type shape during the mating season, and the teeth of male D. Sabina and male shovelnose rays Aptychoterma rostrata have higher fin-gripping strength than those of females (Gutteridge and Bennett 2014; Kajiura and Tricas 1996). Notably, sexual dimorphism of dentition in shovelnose rays and in rajids is not accompanied by dietary differences between the sexes, indicating that differences in tooth morphology are not related to feeding (Gutteridge and Bennett 2014; McEachern 1977; Taniuchi and Shimizu 1993). Ultimately, it is difficult to correlate form and function in structures that have multiple functions and it is unlikely that a structure would be optimized for one function at the cost of another (Domenici and Blake 2000; Koehl 1996; Lauder 1995; Reif 1983).

8.4.4 Tooth Performance and Paleoecology Chondrichthyans are well represented in the fossil record, thanks to the numerous teeth produced throughout life. However, the fossil record of teeth in situ, jaws, and the rest of the body are rare due to the fact that cartilage does not readily fossilize (but see Stahl and Parris 2004; Williams 2001 for examples), and stomach contents and definitive trace fossils of prey are also exceedingly rare (but see Kirwet et al. 2008; Schwimmer et al. 1997; Vullo 2011; Williams 1990 for examples). Therefore, much of what is inferred about how and what extinct chondrichthyans ate comes from tooth morphology (e.g., Cappetta 1987; Cicimurri 2000, 2004; Peyer 1968; Stahl and Parris 2004). Given the rather dubious relationship between tooth morphology, function, and diet discussed above, this inference is now recognized as problematic. However, biomechanical studies are emerging as a new way to elucidate the function of extinct chondrichthyan teeth. Cast aluminum versions of Cladodus, Xenacanthus, and Hybodus teeth exhibited comparable cutting performance to extant shark teeth in puncture tests. Furthermore, Cladodus and Xenacanthus teeth were able to puncture hard and soft prey items, whereas Hybodus teeth were only able to puncture hard prey (e.g., blue crab Callinectes sapidus) (Whitenack and Motta 2010a). Working on a system for which there is no extant analog, Ramsay et al. (2015) modeled the interaction of features of the newly discovered jaws of Helicoprion davisii, such as the jaw joint position, shape of the occlusal surface and the position of the tooth whorl. The disk-like tooth whorl and convex occlusal surface exhibited functional differences among the teeth based on their whorl position. Posterior teeth travel in a posterodorsal arc as the jaws close and function to puncture and pull food into the mouth. Anterior teeth first travel in an anterodorsal arc, which could initially hook prey, and then a posterodorsal arc which could puncture and pull prey further into the mouth, combining puncture and draw into one activity (Fig. 8.16) (Ramsay et al. 2015).

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Fig. 8.16 Feeding mechanism of the euchondrocephalan Helicoprion showing a the characteristic Helicoprion tooth whorl in comparison to b the generalized morphology of a bite-feeding shark illustrating functional and nonfunctional teeth. c, d Left lateral schematics of the Helicoprion jaws on a theoretical cranium generated from a closely related eugeneodontid chondrichthyan Caseodus. BF, basitrabecular fossa; BTP, basitrabecular process; CR, cranium; EC, encasing cartilage; EP, ethmoid process; FT, functional teeth; JC, jaw cartilage; LBC, labial cartilage complex; MC, Meckel’s cartilage; NT, new teeth (nonfunctional); OE, oral epithelium; PQ, palatoquadrate; RT, tooth root; TW, tooth whorl. Reproduced with permission from Ramsay et al. (2015)

8.5 Digestive Physiology and Energetics An animal’s digestive system is responsible for breaking down, absorbing, and assimilating ingested prey items, and the morphology and characteristics of this system underlie the efficiency with which it performs these tasks. Rather than being static, digestion is a dynamic process which from a theoretical standpoint can be examined in much the same way that a chemical engineer considers a reactor; reactants (prey) are placed into a vessel (digestive tract) in which chemical reactions occur (e.g., hydrolysis, enzymatic digestion, absorption). The goal of the chemical engineer is to optimize these reactions, and as such, it is expected that natural selection of the digestive system has optimized the net acquisition of energy or nutrients from particular types of prey. For these reasons, chemical reactor theory has been used to model animal digestive systems and predict how the digestive system is adapted to

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a particular lifestyle, as well as the short-term and long-term adaptations required to deal with changing conditions (Penry and Jumars 1987). Within this framework, elasmobranch digestive systems can be considered a combination of a batch reactor (i.e., stomach) where reactants are processed in discrete well-mixed batches (i.e. the animal does not feed continuously), and a plug-flow reactor (i.e., intestine/colon) through which there is a more continuous flow of material with little axial mixing. Chemical reactor theory generates several predictions regarding the general premise that as prey retention time in the digestive system increases, there will be a more extensive breakdown of food and digestive efficiency will increase (Hume 2005). Therefore, retention time is a potentially critical determinant of digestive efficiency which can be increased by either reducing flow rates via changes in gastric or intestinal motility (i.e., a short-term response) or by increasing gut volume (i.e., a long-term response) (Hume 2005). As both an efficient and flexible system, digestive homeostasis is maintained via the complex coordination of the batch and plug-flow reactors. Enzyme secretion rates are tailored to the presence/absence of different nutritional components (i.e., variable levels of proteins, lipids, and to a lesser extent carbohydrates), while pH optima varies within the different reactors relative to enzyme profiles, and patterns of motility in the stomach and intestine are coordinated to control retention times in response to meal size and chemical constituency. Chemical reactor theory will provide the framework for describing how the chemical reactions of chondrichthyan digestive systems proceed, as well as how these systems maintain performance under changing conditions.

8.5.1 Digestive System Sharks, as with most carnivorous fishes, largely exist on a “feast or famine” lifestyle with extended periods during which the stomach is empty, followed by times of gorging (Armstrong and Schindler 2011). Prey will often be consumed whole or with minimal mastication, making the stomach responsible for converting solid material into semi-liquid chyme (although see Kolmann et al. 2016 for an exception). Digestion in the stomach requires an enzymatic and chemical breakdown of prey, along with mixing of contents via gastric contractions. Enzymatic digestion of proteins in prey is accomplished by the secretion of pepsin, which is initially released in an inactive form, pepsinogen (Table 8.1). Pepsinogen requires highly acidic conditions in order to be cleaved and converted into pepsin, which the stomach accomplishes by secreting concentrated hydrochloric acid (HCl). Pepsin has been identified in shark gastric fluids, and in spotted catsharks Scyliorhinus canicula this enzyme had optimal activity at pH 2.5 (Guerard and Le Gal 1987; Papastamatiou 2007). In elasmobranchs, acid and pepsin are secreted by one cell type, the oxynticopeptic cells that are located in crypts of the gastric mucosa. However, bluntnose sixgill sharks Hexanchus griseus have mammalian-like separate parietal (acid) and chief (enzyme)

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Table 8.1 Diversity, function, and active sites of elasmobranch digestive enzymes Enzyme

Function

Pepsina

Digest proteins

Site of release Stomach

Gastrinb

Increase acid secretion

Stomach

Histaminec

Increase acid secretion

Stomach

Acetylcholined

Increase acid secretion

Stomach?

Ghreline

Acid secretion and motility?

Stomach

Somatostatinf

Decrease acid secretion?

Intestine

Cholecystokininf

Induce pancreatic secretions?

Intestine

Lipaseg

Digest lipids

Pancreas

Trypsing

Digest peptides

Pancreas

Maltaseg

Digest maltose

Intestine

Aminopeptidaseg

Digest proteins

Intestine brush border

N-acetyl-β-D-glucosaminidaseg

Digest structural carbohydrates?

Microbial?

a Guerard

and Le Gal 1987; Papastamatiou 2007 1983 c Hogben 1967 d Unknown e Kawakoshi et al. 2007 f Holmgren and Nilsson 1999 g Jhaveri et al. 2015 b Vigna

secreting cells, and the extent to which this occurs in other chondrichthyan taxa is unknown (Michelangelli et al. 1988). Acid costs energy to produce and secrete, as evidenced by the high density of mitochondria in the oxynticopeptic cells of Chilean catsharks Scroederichthys chilensis (Rebolledo and Vial 1979). Hence, acid secretion should be regulated so that HCl production only occurs at high levels when prey is in the stomach. Indeed, gastric pH is in the range of 7.0–8.2 when the stomachs of various shark and ray species are empty (Papastamatiou and Lowe 2005; Sullivan 1905). However, several species have shown gastric pH ranging from 1.0–2.5 on an empty stomach, suggesting a basal level of acid secretion (Anderson et al. 2010; Papastamatiou and Lowe 2004; Papastamatiou et al. 2007; Wood et al. 2006). Low pH in an empty stomach may serve an antimicrobial function by preventing bacterial growth on the stomach mucosa, but it is unclear as to why such a dichotomy exists among species. One possibility is that basal acid secretion enables the stomach to remain in a state of physiological readiness, which could be advantageous for frequently feeding species to allow more rapid completion of gastric digestion (Papastamatiou 2007). Such variability in gastric acid secretion patterns are not unique to sharks and can be seen in comparisons among and within reptiles and mammals as well (Secor and Carey 2016). It is also important to clarify the difference between pH and acid secretion rate; if the stomach is empty, a low secretion rate would be required for pH to be maintained at low levels,

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Fig. 8.17 Gastric acid secretion rates in leopard sharks demonstrating negative feedback in the physiological regulation of the digestive system. Gastric acid secretion rates are significantly higher when gastric pH > 2.5 (p < 0.003). Error bars represent standard deviations. Reproduced with permission from Papastamatiou 2007

whereas much higher secretion rates would be required to reduce the pH of a full stomach (Papastamatiou 2007). The initial stimulus for acid secretion is distention of the stomach wall as prey enters, followed by the action of secretagogues (i.e., hormones released by the stomach itself) and/or neurotransmitters (Table 8.1). In sharks, increased acid secretion has been induced by gastrin, histamine, and acetylcholine, although the response was more moderate than in mammals (Hogben 1967; Holmgren and Holmberg 2005; Vigna 1983). Although the mechanisms are not well understood, if sharks are similar to mammals in this regard then the regulation of acid secretion is primarily under the control of histamine release, with negative feedback likely playing a role as well (Holmgren and Holmberg 2005); as pH in the stomach drops below a certain level there is a reduction in acid secretion rate likely due to the inhibition of gastrin release (Bomgren and Jonsson 1996). Negative feedback in pH-dependent control of acid secretion occurs in teleosts and leopard sharks Triakis semifasciata, in which acid secretion rates following feeding declined when the pH decreased 50% tongue length), tapered lingual process (hyobranchial rod) to protrude the entire tongue beyond the jaws” (Wagner and Schwenk 2000). For these authors, this modality of tongue movement is different compared to the ancestral tongue prehension that is retained in Scincoidea and Gekkota. However, all kinematic studies show that arboreal and terrestrial Gekkota only use their jaw for solid (prey) food (see, for example, Delheusy et al. 1995; Delheusy and Bels 1999), but their tongue for liquid (i.e., nectar). The Gekkotan tongue is proposed to be morphologically specialized for drinking (see below) and eye licking or wiping, although Reilly and McBrayer (2007) also noted that: “…this (eye licking) is the primary function of the tongue and may actually conflict with direct aerial chemosensory and

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feeding function.” The ancestral mode of tongue prehension with dorsal surface of the fore tongue is retained in Gerrhosauridae (Urbani et al. 1995; Montuelle et al. 2012a) and Scincidae (Smith et al. 1999). Reilly and McBrayer (2007) discussed the question of the role of the tongue in this latter group. Tongue prehension is completely lost in three families of the Autarchoglossa (Lacertiidae, Teiidae, and Xantusiidae), in which tongue-based prehension capabilities probably diminished with the enhancement of vomerolfactive abilities to check their habitat, including finding prey and conspecifics. This hypothesis supports the conclusion of Bels (2003) who described four modes of prehension in lizards (Bels et al. 2019): (i) tongue pinning, (ii) tongue active retraction, (iii) ballistic tongue, and (iv) jaw prehension. Reilly and McBrayer (2007) suggested that the ancestral character state involves jaw prehension with fast opening. “Tongue active retraction” (Bels 2003; Bels et al. 2019) and “translational tongue protrusion” (Reilly and McBrayer 2007) correspond to a similar motor pattern (MAP, Figs. 13.10 and 13.11). Prey capture can be defined as a FAP or MAD defined in classical ethology (Tinbergen 1952; Bels 2003). Without active retraction of the prey, the prey/food is only pressed on the substratum and the jaws advance onto the prey when the gape is at its peak opening (Bels 2003). Tongue pinning occurs as a capture mode per se (Bels et al. 2019) and always occurs as soon as the mass of the tongue touches the prey (Fig. 13.5), but also likely occurs in any other modes of lingual prehension (Fig. 13.3 in Bels 2003; as shown in Figs. 13.6 and 13.7), since it allows the tongue to adhere to the prey. The role of the tongue in squamate ancestors probably was either to press the prey/food on the substratum and/or to slightly retract it into the buccal cavity (references). The properties of the selected prey probably play a key role in the tongue movement in relationship with its muscular characteristics (see Figs. 13.3 and 13.4). Behavioral specialization can modify the lingual motor pattern. This is evident in the study of Cordylidae showing that prey selection drives a major change in lingual movement. In this lizard family, Broeckhoven and Mouton (2013) concluded that: “the consumption of termites in O. cataphractus has resulted in the evolution of a novel lingual prehension mode, during which the ventral surface of the tongue is used to apprehend prey. This is in contrast to other lizards, which use the dorsal surface of the tongue to contact prey. Moreover, we demonstrated that this novel lingual prehension mode is accompanied by distinct morphological elaborations of the tongue surface.” However, the question of evolution of ventral tongue prehension in Cordilydae remains to be debated. Towsend et al. (2004) present one novel scenario on the evolution of capture per se (not feeding) in lepidosaurians based on their phylogenitc study. They suggest the prey/food capture is “more labile” along the squamate tree (Towsend et al. 2004). For these authors: “Lingual feeding evolved at least twice, once either in the lineage leading to Sphenodon or in a common ancestor of Sphenodon and squamates (allowing uncertainty in the outgroup designations), and once in an ancestor to Iguania.”

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13.6.2 Lingual Adhesion The properties of the mucus secreted by the fore tongue that contacts the prey are probably critical for successful prey capture. In the iguanian Oplurus cuvieri, Delheusy et al. (1994) confirmed that: “…The epithelium of the papillae is composed of cells filled with secretory granules. Each surface plays successive roles during food ingestion, intra-buccal transport, and swallowing. The mucous interpapillary spaces would serve the adherence between the tongue and the food.” A strong adhesion between the fore tongue and the prey is required during the retraction phase in all lizard species using lingual prehension. Tongue–prey adhesion in lizards can be explained by various mechanisms such as interlocking with self-adjustment between prey surface and tongue for physical crosslinks, suction mechanism, and wet adhesion (Schwenk 2000, Herrel et al. 2000; Vitt et al. 2003; Higham and Anderson 2013). Only a few experimental analyses provide data to explain prey–tongue adherence, however, and most focus on chameleons. Herrel et al. (2000) explained that: “It is generally thought that chameleons, like other iguanians, rely on serous and mucous secretions and on interlocking to hold the prey on the tongue after capture (Bramble and Wake 1985; Bels et al. 1994).” In addition, they confirmed that: “suction plays an important role in the mechanics of chameleon tongue prehension…. Clearly, a suction process is enabled by the rearrangement of the intrinsic tongue musculature in chameleons so that the tongue pad can be withdrawn to form a pouch-like structure. Interestingly, an evolutionary precursor for this unique arrangement of the intrinsic musculature (a modified arrangement of the fibres of the m. hyoglossus) may be present in agamid lizards (K. Schwenk, personal communication; note that this depends on the nature of the relationship between chameleons and agamids). The withdrawal of the tongue pad and the subsequent formation of a pouch not only create suction forces on the prey, but also increase the adhesive properties of the tongue considerably, presumably by increasing the contact surface area and possibly by reorientating the tongue papillae (resulting in increased interlocking).” Recently, a dynamic model for viscous adhesion has been proposed for prey capture in chameleons (Brau et al. 2016). This model is based on measurements of the viscosity of the mucus produced at the fore tongue (tongue pad), although this secretion remains to be biochemically characterized. In this model, the viscosity of the fore tongue secretion is about 400 times larger than that of human saliva. Using this model, the maximum prey mass that can be held by the fore tongue is calculated as follows (Fig. 13.12): m ∗p  ρV ∗ 

9 η2 Σ 4 64π2 kd 2 h 40

In this equation, V  the prey volume; ρ  typical prey density; η  0.4 ± 0.1 Pa. The morphological parameters, k, , and mt depend on the snout-vent (SVL) length, LSVL . For Chameleons, Brau et al. (2016) estimate SVL between 50 and 200 mm,

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Fig. 13.12 Chameleon schema of prey capture (modified from Brau et al. 2016) used to build the model proposed by Brau et al. (2016). h0 the initial thickness of the mucus; mp prey mass; mt tongue mass; d distance

and h0 the initial thickness  of the mucus layer  50 ± 10 mm. The authors suggest  4.8 (±1.2) 10−3 L2SVL , and the mass of the tongue that k  223 (±60) LSVL , 3 mt  0.45 (±0:09) LSVL (MKS units). The retraction force applied on the prey at a distance linearly scaling with chameleon LSVL is d  0.2 (±0.1)LSVL . Using these parameters, the equation can be written as a function of the animal body size: V ∗1/3  (1.2 ± 0.6)L 1.4 SVL Because the mass of the captured prey reported for various chameleon species is always under that calculated with this model, Brau et al. (2016) concluded that: “…Viscous adhesion alone is therefore largely sufficient to allow capture of very large prey.” The dynamic model based on viscoelasticity of the mucus remains to be tested in all other lizards using tongue prehension (Fig. 13.13). The role of tongue retraction for carrying the prey into the oral cavity can be hypothesized to be rather similar in all iguanian lizards (and possibly scleroglossans using lingual prehension), although it may also be affected by differences in morphological features such as the nature of secretion, the number of cells along the tongue papillae, the number and type of muscle fibers, etc. Comparative analyses of the surface of fore tongue suggest that production of various secretions can play a key role in such viscous adhesion. But how the tongue retracts the prey into the buccal cavity in Cordylidae and Scincidae remains to be investigated. Even more so, in the case of lizards using the ventral surface of the tongue to capture food (Broeckhoven and Le Mouton 2013), does viscoelasticity vary between dorsal and ventral surface?

13.6.3 A Scenario… Townsend et al. (2004) explained that: “lingual prehension is assumed to be the ancestral lepidosaurian condition, it is possible that the similar feeding behavior and tongue morphology of Sphenodon and iguanians represent homoplasy rather than

494 Fig. 13.13 Series of frames showing the deformation of the fore tongue during its expansion on the prey in Pogona vitticeps. The prey is presented to the lizard through a prism permitting images of the tongue at prey contact to be obtained. Only the dorsal surface of the fore tongue contacts the prism to show its potential deformation (instead of the prey). The mucus (black arrows) is produced by the fore tongue as soon as lingual contact occurs between the tongue and the prey. The arrows indicate the mucus produced by the lizard tongue

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homology.” Figure 13.14 proposes a schematic evolution scenario of prey capture in lizards based on morphological, functional, and behavioral data within the context of a recent phylogenetic relationship proposed for lizards (Reeder et al. 2015). In accordance with previous hypotheses (Bels 2003; Reilly and McBrayer 2007), we suggest that prey/food is captured either by lingual or prehension in ancestral lepidosaurians probably depending on prey/food properties. The MAPs of jaw opening present an opening–closing profile and head movement (lunge, see Figs. 13.8 and 13.9) toward the prey/food. The opening phase is controlled with regular gape increase at various speeds (called FO, Fig. 10.3, Reilly and McBrayer 2007) associated with various amplitudes of tongue protrusion, if any in the case of strict jaw prehension. This condition is proposed to be illustrated by several families including Scincidae, Cordylidae, and Gerrhosauridae. In Agamidae and Iguanidae, this condition is also retained with the tongue used to pin the prey and limited active retraction at various degrees (translational tongue protrusion, Reilly and McBrayer 2007). In all of these lizards, the tongue is slightly protracted to pin the prey on the substratum (Urbani and Bels 1995; Bels 2003) or is able to retract the prey/food as in Scincidae (Smith et al. 1999), Agamidae (i.e., Acanthosaura sp., Bels et al. 2019), and even Anolis (Fig. 13.6; Montuelle et al. 2008). The movements of the tongue outside of the buccal cavity can be understood to be in agreement with the morphological properties of the tongue in Agamidae (Smith 1982) and the scenario proposed by Schwenk and Bell (1988), who suggested that “protrusion with hyoid protraction and limited lingual translation caused by extrinsic muscles; little or no activity of verticalis musculature; only tongue tip curls ventrally (the primitive state).” Active tongue retraction (translational lingual protrusion, Reilly and McBrayer 2007) is probably related to some morphological and functional innovations as demonstrated by Reilly and McBrayer (2007). This is also supported by Reilly and McBrayer (2007) who stated that “…the key innovation of lingual translation varies within Iguania.” In most lizards that capture food with tongue prehension, the dorsal papilose surface of the tongue always touches the prey/food. However, some Cordylids have recently been reported to be able to use the ventral surface of their tongue (Broeckhoven and Le Mouton 2013). In contrast, all iguanian lizards used the dorsal surface of the tongue to drink and to collect chemical information from the substratum. Dynamic viscous adhesion probably limits the prey/mass selected by the lizards, but this mechanism appears to be sufficient for all prey selected as demonstrated in chameleons (Brau et al. 2016). This suggestion of the ancestral condition is not problematic, because both modes of prehension are variably present in the closest outgroups to lepidosaurs (i.e., birds, turtles, and crocodilians). During lizard evolution, the functional constraint associated with the ability to detect chemicals via chemoreception has a strong effect on tongue morphology and its functional and behavioral performance (Toubeau et al. 1994). In Lacertidae, Baeckens et al. (2017b) demonstrated: “co-variation between sampler and sensor, hinting towards an ‘optimization’ for efficient chemoreception” and concluded that “species’ degree of investment in chemical leading factor driving the diversity in vomeronasal-lingual morphology signalling, and not foraging behavior.” In some

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Fig. 13.14 Schematic cladogram showing a proposed evolutionary scenario in lizards. All lizards use their tongue for food transport (and reduction when it occurs). Some species (i.e., Tupinambis sp. and Varanus sp.) with a highly modified lingual morphology can use their tongue for prey transport at various degrees and are also characterized by inertial feeding (see text for explanations). Probably, the lizard ancestors were able to catch food/prey by using the jaws only or by pinning their food on the substratum (Bels 2003; Bels et al. 2019). They may be able to use “tongue prehension” (Fig. 10.5, p. 314, Reilly and McBrayer 2007) as recorded in Tiliqua sp. (Smith et al. 1999). Tongue pinning is a component of the lingual action on the food/prey in all modes of lingual prehension (ventral and dorsal lingual prehension). As soon as the tongue touches the prey on the substratum, the lizard uses active lingual prehension (transational tongue protrusion) can be viewed as a derived mode of the ancestral pinning with possible prey lingual retraction when jaws close on the prey (Bels 2003; Reilly and McBrayer 2007). Except Tupinambis sp. (and probably Varanus sp.) with highly modified tongue, all lizards use the dorsal surface of their protruded tongue to collect any liquid (water and nectar). Probably, the ancestral mode of drinking was based on this movement including lingual protrusion and fore tongue deformation to reach the liquid (i.e., drops of liquid). In contrast, vomerolfaction is related to contact of the ventral lingual surface on the substratum (the role of tongue flicking in air remains to be investigated, see Goosse and Bels 1992), except in all Iguania that use the dorsal surface of their tongue to collect chemicals. We suggest that lingual movement during tongue pinning, drinking, and vomerolfaction show similar MAP in the lizard ancestors (see text for more explanations). DAR Dorsal Active Retraction; DD Use of dorsal surface of the fore tongue in drinking; DV Use of dorsal surface of the fore tongue in vomerolfaction; J jaw capture; TP tongue pinning; VAR Ventral Active Retraction; VD Use of ventral surface of the fore tongue in drinking; VV Use of ventral surface of the fore tongue in vomerolfaction

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families, the anatomical specialization of the tongue modifies the deformation and elongation process and reduces its ability to catch any food/prey items (Smith 1982; Reilly and McBrayer 2007). In such cases, the tongue only plays a functional role during drinking (Bels et al. 1993). In contrast to Reilly and McBrayer (2007) who stated that “…The ground geckos, the Eublepharidae, are unique among the Gekkota in having lost tongue prehension….”, all Gekkonidae have lost lingual prehension but use their tongue for exploiting liquid food like nectars (Fig. 13.1; see below). Living prey and other solid foods (i.e., fruits) are captured with jaw prehension (Delheusy and Bels 1999). As suggested by Vitt et al. (2003) and Reilly and McBrayer (2007), several behavioral and functional constraints (i.e., noctuarity, eye licking/wiping) probably play a key role in explaining the loss of lingual prehension in Gekkonidae. This evolutionary scenario remains to be explored in association with comparative analysis of tongue morphology and performance in many families of lizards.

13.7 Reduction and Transport Studies in various lizard species with divergent trophic systems (e.g., skull and hyolingual system) demonstrate that patterns (FAP or MAP) of the intraoral food reduction and transport cycles show many motor similarities, but at the same time, many are modulated by food/prey properties (Throckmorton 1980; Smith 1982, 1984, 1986, 1994; Schwenk 1988; Bels and Baltus 1988, 1987; Schwenk and Throckmorton 1989; Delheusy and Bels 1992; Bels et al. 1994; Delheusy et al. 1995; Urbani and Bels 1995; Herrel et al. 1996, 1997a, b, 1999c, 2001a, b; Kardong et al. 1996; Delheusy and Bels 1999; Elias et al. 2000; Reilly et al. 2001; Montuelle et al. 2009b; Zghikh et al. 2014; Fitzsimons and Thomas 2016). Here, we only discuss the evolution of the transport cycle and not the number of cycles, which can vary between and within species in relationship with to prey properties (i.e., movement of the prey into the buccal cavity when crushing/killing, contact between the prey and the tongue, prey volume, and size). Figure 13.15 shows a typical cricket processing sequence by the agamid Acanthosaura capra showing that the position of the prey is the key factor that separates reduction and transport (Bels and Baltus 1987; Herrel et al. 1996). During reduction cycles, the prey is maintained between the teeth, whereas during transport cycles, it is moved by the protraction–retraction of the tongue through the buccal cavity toward the esophagus. A division of intraoral process into phases (reduction, intraoral transport, swallowing) has been reported in many species (Schwenk and Throckmorton 1989; Kraklau 1991; Herrel et al. 1997a, b; Delheusy and Bels 1992; Urbani and Bels 1995; Smith 1984; Bels and Baltus 1987; So et al. 1992). Sckwenk (2000) compares reduction (chewing) in iguanians and scleroglossans, and his detailed comparative analysis in relationship with morphology (e.g., dentition, tongue) concludes that: “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…”. It can be assumed that

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reduction cycles (crushing cycles in Agama stellio: Herrel et al. 1996, 1997a, b; chewing cycles in Schwenk 2000) derive or are a simple modulatory cycle response of food/prey transport. The motor pattern of the reduction and transport cycle has been conserved but is also modulated in response to change in prey type (Bels et al. 1994; Schwenk 2000; Herrel et al. 2001a, b). Herrel et al. (2001a) explain that: “Despite the large variability observed within and among species, some elements of the feeding cycle in lizards do appear to be conserved and corroborate parts of the Bramble and Wake (1985) model (Fig. 13.2).” In each cycle, the movements of the jaws and hyolingual apparatus show the classical division in slow opening (SO), fast opening (FO), fast closing (FC, and slow-closing-power stroke (SC-PS) as suggested for transport in all tetrapods (Bels 2003). The SO stage is often divided into SO I and SO II. Except in Phelsuma madagascariensis which exhibit long SO II phases between transport cycles, prey transport does not show a consistent SO II stage (Fig. 13.16). Herrel et al. (2001a) emphasize that: “…in all species examined slow opening phases are present, but this is clearly food type dependent and SO phases do not always occur in every cycle (e.g., see Delheusy and Bels 1992; Herrel et al. 1999a; Herrel and De Vree 1999; Schwenk 2000). During this phase the fitting of the tongue to the prey occurs (ensuring an effective subsequent backward prey transport), hence this phase is related to, and might even be determined by, anterio-dorsad tongue movements (see Bramble and Wake 1985; Herrel et al. 1997a)”. In their extensive review of kinematics of gape cycle, McBrayer and Reilly conclude that: “… all species had some transport gape cycles containing both the SO and FO phases, and overall, it was the predominant pattern observed in 79 kinematic models of prey transport in lizards…. An SO phase has been observed in at least some gape cycles in most lizards investigated to date (reviewed in Schwenk 2000), and the outgroup to lizards, rhynchocephalians, show a slow opening phase in reduction and repositioning movements (Figs. 13.6, 13.7, 13.8 and 13.9, Gorniak et al. 1982; simple transport cycles have not been analyzed in this taxon). … Therefore, lizards… not only retain the pleisomorphic open-close transport cycle but also commonly insert an SO phase during prey transport.” All studies based on X-ray films and EMGs demonstrate that the hyo-lingual protractor and retractor muscular activities produce movements of the tongue and the hyoid apparatus during prey transport. These lingual movements are based on a series of trophic muscles (associated or not with dorsal epaxial muscle activity) allowing synchronization with jaw opening and closing (Smith 1982, 1984, 1986; Herrel et al. 1997a, b, 1999a, b). In both phases, the tongue plays the key role to move the food/prey within the buccal cavity (Bels and Goosse 1990; Herrel et al. 2001a, b). Bels and Goosse (1990) determined the role of the tongue through the description of hyo-lingual movements during intraoral food (locust) transport in Anolis equestris: “When the food item (locust) is within the buccal cavity of the lizard, its mechanical reduction begins. During the SO and the main part of the FO stages, the hyoid elements move forward…. The movement of ceratobranchials I and ceratohyals is more rapid during the FO stage…. The ceratobranchials I move further anteriorly than the ceratohyals so that the two elements seem to be crossed in

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Fig. 13.15 During a typical feeding cycle in Acanthosaura capra, the captured prey is repositioned by the tongue a reduced, b transported, c and swallowed d lingual cyclic movement (protraction—retraction) within the buccal cavity is related to different modulation of lingual deformation. The lizard changes the body posture along the transport and the swallowing cycle. Time is given in ms

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Fig. 13.16 X-ray series of frames depicting mice transport in Tupinambis merianus. a. The tongue does not play any major role in food movement. b. The tongue acts on the movement of the prey as demonstrated by relative movements of markers placed into fore (a) and mid (b) tongue. c The two last frames of the transport cycle depicted in b show lingual deformation demonstrated by the movements of the intra-lingual markers at the end of this cycle. During this cycle, the prey begins to enter into the esophagus showing the difficulty to separate last transport cycle and first swallowing cycle

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their mid-portion…. The hyoid body is therefore forced upward …The hyoid elements cease to cross as they move backward at the beginning of the FC stage… The force exerted by the ceratobranchials I against the hyoid body should be greater than that exerted by the ceratohyals because the contracting m. ceratohyoideus and/or m. mandibulohyoideus I protract(s) the ceratobranchials I against the ceratohyals. This produces a forward and upward force acting on the tongue. The forward component results in the protraction of the lingual process and the tongue and the upward component elevates the lingual process… The tongue is then elevated during the FO stage …At the same time, the intrinsic musculature of the tongue would act to produce the hump-backed shape….” Regarding modulation of the transport cycles, Herrel et al. (2001a) showed that: “Some elements of the feeding cycle appear to be conserved across lizards. Notably, we see hyolingual protractor activity during slow opening, jaw opener and dorsal epaxial muscle activity during fast opening, bilateral contraction of all jaw closer groups during fast closing, and bilaterally simultaneous, co-activation of all jaw closers during the slow close phase (Smith 1982, 1984, 1986; Herrel et al. 1997a, b, 1999a, b). The limited amount of information available for jaw and hyolingual muscle activation patterns suggests that the overall amount of variation is larger for the jaw closer muscles compared to the hyolingual muscles. However, as quantitative data on hyolingual muscle activation patterns are scarce (Herrel et al. 1997a, unpublished) this should be confirmed by further research.” Food/prey properties are also known to modulate several characteristics of feeding cycles, including bite force (reduction) and jaw–tongue kinematics. For example, Metzger (2009) showed that prey mass has a more significant effect than prey hardness or mobility. His data confirmed that the SO phase of the gape cycle plays a key role in the contact (“physical conformation”, Metzger 2009) of the lingual surface with the food. Herrel et al. (2001b) discuss this modulation and concluded that: “Although most lizards respond to changes in the structural properties of food items by modulating the activation of the jaw and hyolingual muscles, some food specialists might have lost this ability. Whereas the overall similarity in motor patterns across different lineages of lizards is large for the hyolingual muscles, jaw muscle activation patterns seem to be more flexible. Nevertheless, all data suggest that both the jaw and hyolingual system are complexly integrated. The elimination of feedback pathways from the hyolingual system through nerve transection experiments clearly shows that feeding cycles are largely shaped by feedback interactions.” Furthermore, other analyses show differences among species. For example, in their comparative analysis of two closely related scincid species with highly different morphologies and diets (omnivorous Tiliqua scincoides and herbivorous Corucia zebrata), Herrel et al. (1999c) emphasize that both species respond to mobility and toughness of the food. For example in C. zebrata, the SO stage and the total duration of the cycle decrease while transporting leaves of endive. In T. rugosa, gape distance decreases and FC shortens for transporting grasshoppers. This demonstrates that these lizards are able to recruit jaw closers differently in response to the mechanical resistance of the food. For example, in the case of tough vegetables like endive, lizards recruit their jaw muscles maximally. In T. rugosa, the intensity of the jaw

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muscle recruitment is similar when feeding on endive and snails, but a very strong recruitment of the jaw closers is also recorded for mice and grashoppers. In this case, prey mobility is suggested to be the main factor affecting muscular recruitment. Herrel et al. (1999c) suggest that “…a quick killing of a potentially mobile prey is undoubtably the best way to assure that it will not escape. Indirect support for this is the observation that T. rugosa responds to grasshoppers by decreasing the gape distance, and thus the duration of the FC, during intraoral transport cycles. By decreasing the time that the prey is not in contact with the jaws (i.e. during FOs and FCs) the chances that a mobile prey can escape are likely to be reduced…”. In contrast, Herrel and De Vree (1999) showed only few food-type dependent differences in the herbivorous U. acanthinurus eating locusts and endive which are food items with large differences in terms of toughness, size, shape, and intra-buccal mobility. By comparing data from U. acanthinurus with the insectivorous Pogona vitticeps transporting grasshoppers, these authors explained that contact properties between the tongue surface and the prey can be a possible explanation for the differences recorded in the transport cycle stages. The medial fore tongue surface in P. vitticeps (see also Zhgikh et al. 1014) is covered by plumose papillae showing numerous secretory cells (Schwenk 2000), whereas this surface is covered by dense papillae in Uromastyx acanthinurus. This suggests that the tongue may fit better under the prey in the insectivorous Pogona. Interestingly, these authors also argue that prey reduction is not retained in the herbivorous Uromastyx. The effects of tongue movements on the modulation of the transport cycle dynamics have also been investigated in teiid and varanid lizards with their highly specialized tongue related to vomerolfaction (Elias et al. 2000; Schaerlaeken et al. 2012). These lizards use three types of prey transport modalities: (i) “pure” inertial transport performed during the beginning of the transport sequence (no tongue involvement), (ii) inertial transport with extension–retraction cycles of the tongue when the prey was positioned along the jaws, and finally (iii) a series of so-called “normal tonguebased” cycles when the prey was in the most posterior position in the buccal cavity. Based on high-speed films, Elias et al. (2000) show that the tongue is used variably along the transport sequence of killed mice, and that these cycles are “…with little or no inertial movement of the head.” By using X-ray films allowing visualization of the hyoid and some lingual movements, Schaelaeken et al. (2011) demonstrate that varanid lizards are able to modulate hyoligual movements in relationship to prey types. They found that transport of mice, as studied by Elias et al. (2000), required greater and longer feeding movements (e.g., gape distance, maximal jaw opening velocity, total hyoid displacement, durations of SO and FO stages).

13.8 Swallowing Swallowing is the last phase of the feeding sequence (see review by Schwenk 2000) and involves pharyngeal packing and compression. This feeding stage remains not well studied although clear differences have been recorded in the jaw and lingual

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Fig. 13.17 Series of frames depicting movement of the tongue out of the buccal cavity in Phelsuma madagascariensis. These movements at the end of the swallowing phase likely probably facilitate pushing of the prey into the esophagus. Time is given in s

kinematic profiles determining the MAP of this phase (Fig. 13.17). Interestingly, this MAP seems to be conserved in species with various lingual morphologies. The tongue plays a key role during this feeding stage but its role remains to be determined and probably is modulated by the food/prey properties and the amount of space between food/prey and buccal cavity (Fig. 13.18). Tongue protrusion–retraction cycles and deformation move the food into the pahrynx and the digestive tract. Clear differences are present in jaw and tongue movements when comparing intraoral transport and swallowing cycles (Schwenk 2000). A swallowing cycle is often characterized by a decrease in the importance of the FO phase, and an increase in the duration of the SO phase associated with pronounced tongue movements (Fig. 13.18).

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Fig. 13.18 Series of X-ray frames depicting two lingual and jaw cycles determining the MAP of swallowing in Lacerta viridis. The tongue deforms to move beneath the food and to facilitate its movement into the pharynx (frames 0–9) and into the esophagus (frames 12–37). Frames are separated by 0.004 s. P Prey; T tongue

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Fig. 13.19 Like the majority of lizards, Anolis carolinensis uses the dorsal surface of the tongue to collect water

13.9 Drinking Drinking is the principal behavior for intake of liquid food (e.g., nectar) and water (Fig. 13.19). In their extensive study of drinking strategies in living organisms, Kim and Bush (2012) define drinking as “…We loosely define drinking as fluid uptake required for the sustenance of life. …Finally, we note that drinking need not involve water; for example, many insects and birds ingest fluid primarily in the form of nectar, which serves also as their principal source of energy…”. All lizards occupying nonxeric terrestrial and arboreal habitats adopt several postures to be able to uptake water and many species exploit nectar as a source of food and water. In xeric lizards, postures are used to collect the limited water from the environment (Malik et al. 2014; Yemmis et al. 2016; Cotman 2018). Cotman (2018) concludes: “Although many species exhibit an accompanying behaviour—that is, active body movements—the actual process of water collection remains passive. The behaviour can instead be regarded as positioning the body surface towards the source from which water is obtained or to assist gravity-mediated water collection.” In the majority of lizards, water moves into the buccal cavity and the dorsal surface of the tongue plays the key role to acquire water in any kind of environment (Peterson 1998; Schwenk and Greene 1987; Sherbrooke 1990, 1993, 2004, Sherbrooke et al. 2007; Bels et al. 1993; Wagemans et al. 1999; Vesel`y and Modr`y 2002). In experimental conditions, lizards with various lingual morphologies approach the source of water, position the head a few millimeters (5–15 mm) above the substrate

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and the water source, and rhythmically protract and retract the tongue in and out of the buccal cavity to collect the liquid (Fig. 13.20). In all lizards studied, drinking behavior is divided into two phases: immersion and emersion. During immersion (Fig. 13.21), water is collected and moved to the pharyngeal cavity through buccal compartments (Bels et al. 1993) (Fig. 13.22). During emersion, water enters the digestive tract (Bels et al. 1993; Wagemans et al. 1999). The salient point is the role of the tongue during this behavior. Except Tupinambis and Varanus (see below), the liquid (water or nectar) is collected by the fore tongue alone. In all lizards studied, the tongue not only collects the liquid but also moves this liquid to the pharynx and the entrance of the esophagus. In contrast to the Sclerologossa, in the iguanians Anolis and Oplurus (Wagemans et al. 1999), the tongue is only slightly protruded (Fig. 13.20) when compared to the degree of tongue protrusion involved in prey capture (Delheusy and Bels 1992; Delheusy et al. 1994; Montuelle et al. 2008). This difference between iguanians and scleroglossans is even more marked for chameleons, which protrude the tongue only very slightly when drinking, compared to enormous tongue projection that occurs during food capture (Wainwright and Bennet 1992a, b; Herrel et al. 2000; Brau et al. 2016). The iguanian Oplurus cuvieri appears to be capable of drinking with its snout submerged in a large volume of water, and, in such circumstances, to use a buccal pumping mechanism (Wagemans et al. 1999) similar to that recorded for some varanids (Smith 1986) and snakes (Kardong and Haverly 1993; Berkhoudt et al. 1995; Cundall 2000). But the fore tongue always enters in contact with liquid in all lizards. The use of both mechanisms (lingual loading versus suction) for gathering water in squamates is seemingly related to the volume of water available, but this remains to be tested by using a similar experimental approach to that employed by Cundall (2000) for snakes. High-speed and X-ray films provide data to elucidate the drinking mechanism. Two mechanisms appear to be used by lizards. The first mechanism has been mainly revealed in lizards with highly different lingual morphologies using the fore tongue to gather water into the buccal cavity (Fig. 13.21). Water (and probably any other liquid) is collected by the dorsal surface of the fore tongue. Two major mechanisms seem to play in water collection: (i) presence of a film thickness of water on the tongue surface and (ii) capillary imbibition of water into the papillae (Kim and Bush 2012). These authors suggest the following formula to calculate the volume of the liquid (water) layer: e  lCa2/3 (l  the length of the tongue in contact with the liquid) with

Ca  u μ/σ∼10−4

(u  tongue velocity; μ  liquid viscosity; σ  surface tension) and the water intake rate is: Q  el2 f∼0.5 (f (Hz)  the recorded licking frequency during one immersion phase).

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Fig. 13.20 Drinking sequence showing lingual movements in Phelsuma madagascariensis. The tongue is expanded when moved out of the buccal cavity and contacts the liquid (time: 0.00–0.88 s). Only the dorsal surface of the fore tongue acts to transport water to the buccal cavity. Time is given in s

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Fig. 13.21 Schematic illustration of the drinking mechanism in lizards. Papillae are represented in gray. a A coating film is produced as suggested by Kim and Bush (2012). b Opening the spaces between the papillae occurs during tongue contact with the film (drop) of water on the substratum to enhance water filling of the tongue by facilitating capillary imbibition. c During tongue retraction out of the buccal cavity, the tongue returns to a less expanded shape and water of the film is entrained in the middle of the tongue. d In the meantime, interpapillary spaces are reduced, and the amount of water in these spaces is added to the water film on the tongue. e As soon as the tongue in the buccal cavity and jaws closes, the liquid fills the buccal compartments as determined in Lacerta viridis, Oplurus cuvieri, and Anolis carolinensis (Bels et al. 1993; Wagemans et al. 1999). The arrows indicate the possible movement of water

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Fig. 13.22 Series of X-ray frames illustrating the role of the tongue to gather water into the buccal cavity in Tupinambis merianae. These frames are only used to illustrate the mechanism of drinking recorded in lizards with highly specialized tongue. Time (ms) corresponds to the position of the tongue in one opening–closing cycle during the immersion phase. Two small markers are present in the tongue of the lizard (black boxes) to show the complex protraction–retraction movements of the tongue. One marker is also positioned on the head and two markers on the throat of the lizard. These last markers show that water is pushed into the pharyngeal cavity with the movement of the tongue as in previous studies (Bels et al. 1993). The arrows indicate the postion of the fore tongue. We, external water in the environment; Wi, water in the buccopharyngeal cavity

As soon as the tongue contacts the water, the fore tongue enlarges (Fig. 13.20). This change can modify the papillar organization. The papillae probably expand away from each other, opening spaces between them and then favoring imbibition of the fore tongue. When the tongue retracts, it recovers its initial shape and water flows into a central canal in the tongue. The tongue retracts into the buccal cavity and fills the first buccal compartment just at the level of the Jacobson’s organ as shown in Lacertidae (Bels et al. 1993) and Iguaniade (Wagemans et al. 1999). As soon as water has filled the pharyngeal compartment, the lizard begins the emersion phase allowing water to be swallowed (Bels et al. 1993). The mechanism used by Teiidae remains to be explored. In this lizard, the fore tongue is not used to collect water, but regular movements of the tongue on the water surface create a fluid movement from outside to the buccal cavity (Fig. 13.22; Bels et al. in prep.).

13.10 Conclusion This chapter summarizes the main data and hypotheses related to the evolution of feeding behavior in lizards. This review provides a rationale for why future investigations of our empirical knowledge of feeding in these tetrapods are needed at all the levels, from evolutionary ecology to sensory functional biology. The chapter attempts to show the generalities vs specialities of the trophic system in relationship with ecological demands through the diversity of lizards although a large number of questions remain to be investigated. Kinematic studies in various species with various types of food/prey provide the opportunity to discuss the combined effect of historical and ecological constraints on the feeding behavior in lizards. Our knowledge on feeding provides one of the best models of morpholigcal, functional, and behavioral evolution as demonstrated by Schwenk (2000), Bels (2003), Reilly and McBrayer (2007) and Bels et al. (2019). The question of evolution of the adhesive model permitting to successful catch food must now be added to the suggested evolutionary hypothesis. This mechanism remains to be deeply studied because it is a key point to explain the success of the feeding behavior in lizards using the tongue to capture their food. Also clearly chemoreception and feeding plays a functional trade-off on tongue morphology and use that still must be investigated. Neuro-ethological studies

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of feeding are very scarce and probably are now needed to understand the actions of the nervous system that give rise to prey selection and capture behaviors. Further attentions to both behavioral and neurobiological issues are needed to provide deep insight into our understanding of the evolution of the functioning of the sensory and nervous systems in generating and controlling behavior in lizards, from capture to swallowing. Finally, the studies of skull and hyo-lingual morphology related to ecological constraints including food/prey properties are now well studied in some species to extract micro- and macro-evolutionary trends in a changing ecological word. Acknowledgements We thank very much K. Tanalgo (Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, P. R. China) for permission to use photographies of gekkos exploiting nectar (Fig. 13.2). We also thank Kiisa Nishikawa and one anonymous reviewer for their help to improve our chapter.

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Vitt LJ, Pianka ER (2014) Lizard ecology: historical and experimental perspectives. Princeton University Press, Princeton Vitt LJ, Pianka ER, Cooper WE Jr, Schwenk K (2003) History and the global ecology of squamate reptiles. Am Nat 162(1):44–60 von Geldern CE (1919) The mechanism in the production of the throat-fan in the Florida chameleon, Anolis carolinensis. Proc Calif Acad Sci 9:313–329 Wagemans F, Chardon M, Gasc JP, Renous S, Bels VL (1999) Drinking behaviour in Anolis carolinensis (voigt, 1837) and Oplurus cuvieri (gray, 1831)(reptilia: Iguania: Iguanidae). Can J Zool 77(7):1136–1146 Wagner GP, Schwenk K (2000) Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. Evolutionary biology. Springer, Boston, MA pp 155–217 Wainwright PC, Bennet AF (1992a) The mechanism of tongue projection in chameleons: I. Electromyographic tests of functional hypotheses. J Exp Biol 168:1–21 Wainwright PC, Bennet (1992b) The mechanism of tongue projection in chameleons: II. Role of shape change in a muscular hydrostat. J Exp Biol 168:23–40 Wainwright PC, Kraklau DM, Bennett AF (1991) Kinematics of tongue projection in Chamaeleo oustaleti. J Exp Biol 159(1):109–133 Wassif ET (2001) The fine structure of the dorsal lingual epithelium of the scincine lizard Chalcides ocellatus Forscal (Scncidea Sauria Reptilia). I. Histogenesis of the lingual epithelium. Egypt J Biol 3:12–19 Wassif ET (2002) Ultrastructure of the lingual epithelium of adult scincine lizard Chalcides ocellatus. Egypt J Biol 4:76–86 Webber MM, Jezkova T, Rodríguez-Robles JA (2016) Feeding ecology of sidewinder rattlesnakes crotalus cerastes (Viperidae). Herpetologica 72:324–330 Whitaker AH (1987) The roles of lizards in New Zealand plant reproductive strategies. NZ J Bot 25:315–328 Wikelski M, Gall B, Trillmich F (1993) Ontogenetic changes in food intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus Bell). Oecologia 94:373–379 Wikelski M, Thom C (2000) Marine iguanas shrink to survive El Niiio. Science 403:37–38 Wikelski M, Wrege PH (2000) Niche expansion body size and survival in Galápagos marine iguanas. Oecologia 124:107–115 Wikelski M, Romero LM (2003) Body size, performance and fitness in Galapagos marine iguanas. Int Comp Biol 43:37686 Wilken AT, Middleton KM, Sellers KC, Cost Davis JL, Holliday CM (2017) Modeling Complex Cranial Joints in Varanus exanthematicus. FASEB J 31:577–5 Willson MF, Sabag C, Figueroa J, Armesto JJ, Caviedes M (1996) Seed dispersal by lizards in Chilean rainforest. Rev Chil Hist Nat 69:339–342 Wittorski A, Losos JB, Herrel A (2016) Proximate determinants of bite force in Anolis lizards. J Anat 228:85–95 Wotherspoon D, Burgin S (2016) Sex and ontogenetic dietary shift in Pogona barbata, the Australian eastern bearded dragon. Aust J Zool 64(1):14–20 Wotton DM (2002) Effectiveness of the common gecko (Hoplodactylus maculatus) as a seed disperser on Mana Island New Zealand. N Z J Bot 40:639–647 Wotton DM, Drake DR, Powlesland RG, Ladley JJ (2016) The role of lizards as seed dispersers in New Zealand. J R Soc N Z 46:40–65 Yang C, Wang L (2016) Histological and morphological observations on tongue of Scincella tsinlingensis (Reptilia Squamata Scincidae). Micron 80:24–33 Yenmi¸s M, Ayaz D, Sherbrooke WC, Veselý M (2016) A comparative behavioural and structural study of rain-harvesting and non-rain-harvesting agamid lizards of Anatolia (Turkey). Zoomorphology 135(1):137–148 Zghikh LN, Vangysel E, Nonclercq D, Legrand A, Blairon B, Berri C, Bordeau T, Rémy C, Burtéa C, Montuelle SJ (2014) Morphology and fibre-type distribution in the tongue of the Pogona vitticeps lizard (Iguania Agamidae) J Anat 225:377–389

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Zhang W, Li N, Tang X, Liu N, Zhao W (2018) Changes in intestinal microbiota across an altitudinal gradient in the lizard Phrynocephalus vlangalii. Ecol Evol 8:4695–4703 Zood A (1933) The mechanism of projection of the chameleon’s tongue. J Exp Biol 10:174–185 Zuffi MA, Giannelli C (2013) Trophic niche and feeding biology of the Italian wall lizard Podarcis siculus campestris (De Betta 1857) along western Mediterranean coast Acta. Herpetol 8:35–39

Chapter 14

Feeding in Snakes: Form, Function, and Evolution of the Feeding System Brad R. Moon, David A. Penning, Marion Segall and Anthony Herrel

Abstract Snakes are a diverse group of squamate reptiles characterized by a unique feeding system and other traits associated with elongation and limblessness. Despite the description of transitional fossil forms, the evolution of the snake feeding system remains poorly understood, partly because only a few snakes have been studied thus far. The idea that the feeding system in most snakes is adapted for consuming relatively large prey is supported by studies on anatomy and functional morphology. Moreover, because snakes are considered to be gape-limited predators, studies of head size and shape have shed light on feeding adaptations. Studies using traditional metrics have shown differences in head size and shape between males and females in many species that are linked to differences in diet. Research that has coupled robust phylogenies with detailed morphology and morphometrics has further demonstrated the adaptive nature of head shape in snakes and revealed striking evolutionary convergences in some clades. Recent studies of snake strikes have begun to reveal surprising capacities that warrant further research. Venoms, venom glands, and venom delivery systems are proving to be more widespread and complex than previously recognized. Some venomous and many nonvenomous snakes constrict prey. Recent studies of constriction have shown previously unexpected responsiveness, strength, and the complex and diverse mechanisms that incapacitate or kill prey. Mechanisms of drinking have proven difficult to resolve, although a new mechanism was proposed recently. Finally, although considerable research has focused on the B. R. Moon (B) Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA e-mail: [email protected] D. A. Penning Department of Biology & Environmental Health, Missouri Southern State University, Joplin, MO 64801, USA M. Segall Département d’Ecologie et de Gestion de la Biodiversité, UMR 7179 C.N.R.S/M.N.H.N., 57 rue Cuvier, Case postale 55, 75231 Paris Cedex 5, France A. Herrel Département Adaptations du Vivant, Muséum national d’Histoire naturelle, UMR 7179 C.N.R.S/M.N.H.N, 55 rue Buffon, 75005, Paris Cedex 05, France e-mail: [email protected] © Springer Nature Switzerland AG 2019 V. Bels and I. Q. Whishaw (eds.), Feeding in Vertebrates, Fascinating Life Sciences, https://doi.org/10.1007/978-3-030-13739-7_14

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energetics of digestion, much less is known about the energetics of striking and handling prey. A wide range of research on these and other topics has shown that snakes are a rich group for studying form, function, behavior, ecology, and evolution.

14.1 Snake Origins and Evolution Recent advances, including the description of new fossils and the redescription of known fossils (Scanlon 2012; Longrich et al. 2012), have enhanced our understanding of the origin of snakes. A recent phylogenetic analysis based on genetic as well anatomical data (Hsiang et al. 2015) showed that snakes likely originated in the early Cretaceous (~128.5 Ma), as suggested by the fossil Coniophis, which is considered to be the earliest known true snake. Coniophis is important because it shows features of the skull that are intermediate between those of lizards and other snakes. The animal had hooked teeth and an intramandibular joint, which suggests that it fed on relatively large, soft-bodied prey (Longrich et al. 2012). Yet the maxilla was still firmly attached to the rest of the skull (Longrich et al. 2012). Mosasaurs have also been thought to possess a flexible lower jaw with a well-developed intramandibular joint, suggesting that this feature may have evolved in the ancestor of both mosasaurs and snakes (Lee et al. 1999). The crown group of snakes probably evolved 20 million years later, with the diversification of caenophidian snakes taking place after the Cretaceous–Paleogene mass extinction (Hsiang et al. 2015). One of the ongoing debates concerning the origin of snakes has been whether they derive from a burrowing (Conrad 2008; Gauthier et al. 2012; Martill et al. 2015; Hsiang et al. 2015) or marine (Lee et al. 1999) ancestor. Recent studies on the morphology and evolution of the visual system and inner ear of lizards and snakes suggest that snakes most likely had a terrestrial and fossorial origin (Simoes et al. 2015; Yi and Norell 2015). Indeed, not only does an analysis of visual opsins suggest that the visual system in stem snakes was reduced, but also the vestibule of the inner ear in the stem snake Dinilysia was strikingly similar to that of burrowing lizards, suggesting that Dinilysia was specialized for detecting ground-borne vibrations. In a recent integrative study of skull evolution in snakes, Da Silva et al. (2018) concluded that all snakes and their sister group evolved from a surface-dwelling terrestrial ancestor with non-fossorial behavior. Yet the most recent common ancestor of crown snakes had a skull shape adapted for fossoriality. Although the debate on the origin of snakes is far from resolved, a consensus is now emerging that the earliest snakes, or at least the stem snakes leading to the crown group of snakes, were fossorial or semi-fossorial animals that had a functional intramandibular joint and ate relatively large prey (Hsiang et al. 2015; Martill et al. 2015; Simoes et al. 2015; Yi and Norell 2015). The unusual jaws and feeding mechanics observed in the earliest branching lineages of snakes (Scolecophidia; Haas 1973; Kley 2001, 2006; Kley and Brainerd 1999; Rieppel et al. 2009) must thus be considered derived secondary specializations associated with an obligate underground lifestyle that went hand in hand with the loss of additional visual pigments (Simoes et al. 2015). The jaw elements became elongated and more highly kinetic in some

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later lineages of snakes, and these snakes have been called macrostomate snakes in reference to their enlarged gapes and abilities to ingest relatively large prey. In phylogenies based on morphological data or combined morphological and molecular data, macrostomate snakes form a monophyletic group. The macrostomate condition likely did not evolve before the late Cretaceous (Hsiang et al. 2015). Although the position of the Tropidophiidae remains debated, recent molecular phylogenies place this taxon as the sister group to Anilius (Pyron et al. 2013; Figueroa et al. 2016), suggesting that the macrostomate condition evolved or was lost more than once within snakes. As data sets and phylogenetic analyses become more comprehensive, the evolution of macrostomate morphology may be resolved with more confidence. For this review, we refer to the macrostomate condition and its consequences for feeding, without implying the monophyly of macrostomate snakes. Most lizards have relatively akinetic skulls and eat small prey, although some can eat prey as large as 35% of their own body mass (Shine and Thomas 2005). Lizards typically rely on high bite forces to reduce prey into smaller parts, a strategy rarely observed in snakes (but see Jayne et al. 2002). In contrast, snakes typically rely on cranial kinesis to ingest prey whole. Although the early branching lineages of alethinophidian snakes (all extant snakes except for blind snakes) retained relatively akinetic skulls, the macrostomate morphology of later lineages is characterized by a greater degree of cranial kinesis than in lizards, allowing them to swallow relatively large prey. The maximum size of prey that a snake can ingest is limited by the maximum size of its open mouth, which is often referred to as gape limitation (Greene 1983). Macrostomate snakes have lengthened several cranial elements including the palatomaxillary arch, the suspensorium (quadrate and supratemporal), and the mandible, which allow the mouth to open to a greater extent than in earlier lineages of snakes. The evolution of increased gapes was associated with diverse changes in the morphology, mechanics, physiology, behavior, and ecology of feeding. In this review, we highlight recent research on many of these aspects of snakes, particularly research published after the last major review of feeding in snakes by Cundall and Greene (2000).

14.2 Morphology Understanding mechanisms of movement, including those associated with feeding, requires a strong foundation in morphology. The static and dynamic properties of bones, ligaments, muscles, tendons, and other morphological structures are crucial to the diverse functions that the structures support and produce. Excellent reviews on the cranial anatomy of snakes exist (Cundall and Greene 2000; Cundall and Irish 2008; McDowell 2008), and here we briefly review studies that appeared after these reviews or that were not discussed in detail in them. Recent years have seen the publication of anatomical descriptions of the cranial skeleton in some early branching lineages of snakes that were relatively poorly known, including anatomical descriptions of several blind snakes (Kley 2006; Rieppel et al. 2009), uropeltid snakes (Olori and Bell 2012), and Xenopeltis (Frazzetta

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1999), as well as some descriptions of ontogenetic changes in skull morphology (Palci et al. 2016; Scanferla 2016). The homology of the jaw muscles in lizards and snakes was also discussed in a recent paper (Johnston 2014), revising the homology hypothesis proposed by McDowell (1986). Johnston pointed out that the jaw muscles in macrostomate snakes appear adapted for mouth opening rather than powerful closing, and that this change appears to have involved increasing muscle fiber length by the loss of aponeuroses and a modification of the M. levator anguli oris (LAO) that allowed it to act both on the venom gland and as a jaw adductor. The original function of the LAO would then have been taken over by the apomorphic M. neurocostomandibularis. Two recent papers describing dental specializations in relation to diet were also published (Jackson and Fritts 2004; Britt et al. 2009). Jackson and Fritts (2004) described dental specializations in wolf snakes, including enlarged maxillary teeth, an arched maxilla with a large diastema, and ungrooved posterior maxillary fangs that allow them to hold on to and slice through hard or protected prey such as skinks. Britt et al. (2009) examined differences in the teeth of thamnophiine snakes that eat slugs and those that eat fish or are more generalist feeders. Interestingly, slug eaters showed pronounced posterior ridges on the posterior maxillary teeth. In some snail-eating snakes, directional asymmetries in tooth number and lower jaw shape have been documented that are related to the predominance of dextrality (clockwise turning) in snails (Hoso et al. 2007; dos Santos et al. 2017). The snakes can extract snails from their shells faster when feeding on dextral than sinistral snails, suggesting that these asymmetries are adaptive (Hoso et al. 2007). These papers, along with many discussed below, nicely demonstrate how understanding morphology is crucial to understanding function.

14.2.1 Head Size and Shape Head shape is remarkably variable in snakes and has been suggested to be adaptive, with relative head width, in particular, being related to the maximal prey size that can be consumed in a wide sample of snakes (Vincent et al. 2006a). In some cases, such as egg-eating snakes in the genus Dasypeltis, adaptations for consuming extremely large food items may limit the ability to eat some kinds of prey (Gans 1952, 1974; Gartner and Greene 2008). Indeed, the specializations for egg eating have resulted in the loss of most teeth, effectively restricting these animals to eating only eggs. Although head shape in snakes is typically investigated because of its expected importance to feeding, snake heads serve many functions in addition to prey capture and transport. For example, head size and shape may be important in anti-predator mechanisms. Specifically, head triangulation, the ability of a snake to flatten its head and make it more triangular, has been suggested to reduce predator attacks based on studies with clay models (Valkonen et al. 2011; Dell’Aglio et al. 2012). In addition, measurements of head shape may be informative in phylogenetic and systematic analyses (Mangiacotti et al. 2014; Ruane 2015).

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Head size and shape are not static, however, and significant plasticity in head shape has been documented (Forsman 1996; Queral-Regil and King 1998; Bonnet et al. 2001; Aubret et al. 2004; Smith 2014). Pioneering work by Forsman (1996) first demonstrated that adders that were fed more frequently developed relatively larger heads than those subject to food restriction. Moreover, Bonnet et al. (2001) showed that feeding frequency also impacted relative head and fang proportions, with snakes that were fed more frequently having relatively wider heads and relatively longer fangs. Subsequent studies manipulated feeding frequency and prey size (QueralRegil and King 1998; Aubret et al. 2004; Smith 2014). These studies showed that feeding larger prey to snakes resulted in relatively longer jaws (Queral-Regil and King 1998; Aubret et al. 2004) or broader heads (Smith 2014). Interestingly, Aubret and Shine (2009) demonstrated that the plasticity in head shape diminished with the time after colonization of a new island. The ability to respond plastically may consequently depend on the environmental variability encountered by a species. Most of these studies quantified head shape externally using either linear measures or geometric morphometric approaches. In contrast, one study that used radiographs to quantify the effects of prey size on the sizes of cranial skeletal elements did not find a treatment effect (Schuett et al. 2005), suggesting that the observed effects on head shape in other studies may reflect differences in musculature rather than differences in the skeletal elements. Given the importance of these features to feeding mechanisms and diet, many studies have investigated the growth of the head in snakes (see review in Cundall and Greene 2000; Vincent et al. 2007; Borczyk 2015; Andjelkovic et al. 2016a; Palci et al. 2016). Generally, studies have found a negative allometry of head size, with the possible exception of head width, which in some species grows with positive allometry (Borczyk 2015). Furthermore, allometry generally explains a significant proportion of the shape differences observed during growth (Andjelkovic et al. 2016a; Murta-Fonseca and Fernandes 2016). Adult snakes typically have more strongly developed muscle attachment sites (Palci et al. 2016), greater physiological crosssectional areas of the cranial muscles (Vincent et al. 2007), and relatively longer quadrates (Palci et al. 2016; Scanferla 2016). Given that juvenile snakes have relatively large heads for their body sizes, some studies have investigated whether juveniles show increased levels of performance despite their smaller absolute sizes (Vincent et al. 2006b; Hampton 2014; Hampton and Kalmus 2014). These studies have shown that although gape size increases with negative allometry, juveniles do not have a relatively better performance than adults in terms of transport time or the number of jaw movements needed to ingest prey. The skeletal elements that best predict gape size also appear to differ between species (Hampton 2014; Hampton and Kalmus 2014). In some species, the observed differences in head shape have been linked to variation in diet (Vincent et al. 2004; Meik et al. 2012; Natusch and Lyons 2014; see Vincent and Herrel 2007 for a review). Furthermore, the morphological differences between juveniles and adults may also explain the observed ontogenetic changes in diet in many species (Vincent et al. 2004; Natusch and Lyons 2012; Lopez et al. 2013; Scanferla 2016). Prey size typically increases with head size in most snakes (Arnold 1993). However, in some cases, changes in head size and shape

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have been suggested to be linked to a shift from ectothermic to endothermic prey (Natusch and Lyons 2012; Scanferla 2016). In addition to differing between juveniles and adults, head shape often also differs between males and females of the same species, often in response to the sexual differences in diet (Vincent et al. 2004; Krause and Burghardt 2007; Meik et al. 2012; Henao-Duque and Ceballos 2013; Andjelkovic et al. 2016a, b). However, beyond the variation between adults and juveniles or between the sexes, different species or populations of snakes also often vary considerably in head shape (Voris and Voris 1983; Grudzien et al. 1992; Dwyer and Kaiser 1997; Forsman and Shine 1997; Mori and Vincent 2008; Brecko et al. 2011; Hampton 2011; Henderson et al. 2013; Natusch and Lyons 2014; Fabre et al. 2016; Segall et al. 2016; Fig. 14.1). This variation has been suggested to be adaptive, as it allows the consumption of different types and sizes of prey (Dwyer and Kaiser 1997), the occupation of different microhabitats (Fabre et al. 2016), the capture of elusive prey underwater (Herrel et al. 2008; Segall et al. 2016), or a combination of these. Among populations of garter snakes and adders, for example, nonadaptive hypotheses for the observed inter-population divergence in relative head size were rejected, suggesting that geographically heterogeneous selection optimizes prey-handling ability (Grudzien et al. 1992; Forsman and Shine 1997). However, in some cases, no differences in diet were observed despite considerable variation in head size and shape among populations (Natusch and Lyons 2014). Across species, head shape is often associated with variation in diet, especially when it involves specialization for handling food items such as hard-shelled prey that impose specific functional demands (Dwyer and Kaiser 1997; Fabre et al. 2016). In many cases, subtle differences have also been observed between snakes that eat bulky prey such as frogs and those that eat more streamlined prey such as fish or lizards (Mori and Vincent 2008; Hampton 2011). These differences become more pronounced for snakes that capture prey under water, where the wide heads of snakes that eat bulky prey could interfere with the ability to capture streamlined, elusive aquatic prey (Hibbitts and Fitzgerald 2005; Herrel et al. 2008; Segall et al. 2016). This trade-off is especially likely to occur in frontally striking species, as wide heads tend to generate bow waves that alert prey sooner to the presence of the predator, and may even push prey away from the line of attack of the predator (Hibbitts and Fitzgerald 2005; Van Wassenbergh et al. 2010). Because of these strong constraints, strongly convergent head shapes are generally observed in aquatic snakes (Hibbitts and Fitzgerald 2005; Herrel et al. 2008; Vincent et al. 2009; Segall et al. 2016). The advent of comprehensive phylogenies for many snake lineages has permitted analyses of these radiations and the roles that head size and shape have played in them. A recent study of Indo-Australian sea snakes demonstrated the presence of two distinct ecomorphs that differ in head shape (Sanders et al. 2013). The microcephalic ecomorph is smaller, has a narrow head and body, and specializes on eels that are captured in burrows. The macrocephalic ecomorph, on the other hand, has a large head and feeds on crevice dwelling eels and gobies. Interestingly, both ecomorphs have evolved independently at least twice, suggesting that differences in head shape may be the basis of the rapid divergence of species within the clade (Sanders et al. 2013). That head size can rapidly respond to strong selective pressures is nicely shown by the decrease in relative head size in Australian snakes that eat toads (Phillips and

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Epicrates cenchria Cylindrophis ruffus Acrochordus granulatus Achalinus rufescens Agkistrodon contortrix Enhydris chinensis Bitia hydroides Cantoria violacea Fordonia leucobalia Prosymna meleagris Micrurus lemniscatus Naja annulata Pseudonaja textilis Aipysurus laevis Ephalophis greyae Hydrophis platurus Hydrophis schistosus Grayia ornata Helicops carinicaudus Tachymenis peruviana

Fig. 14.1 Figure illustrating the diversity of head shapes observed in snakes. Illustrated are dorsal and lateral head views of a variety of snakes derived from 3D scans and plotted next to a phylogeny illustrating the relationships among these taxa

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Shine 2004). Yet, a recent study using a geometric morphometric approach showed strong convergence in head shape in boas and pythons occupying similar habitats, suggesting that habitat use, in addition to diet, may drive the evolution of head shape (Esquerré and Keogh 2016; but see Henderson et al. 2013 for an example of dietdriven convergence in tree boas of the genus Corallus). A study on the convergence between oxyuranine elapids from Australia and a distantly related assemblage of snakes from North America even suggested that diet did not drive the phenotypic convergence between these groups, despite the fact that head measurements were analyzed in the data set. Thus, recent analyses have not always supported the idea that the head should reflect the type and size of prey eaten in gape-limited predators such as snakes (Gans 1961), although in many case, this is likely to be so (e.g., Fabre et al. 2016; Klaczko et al. 2016). Rather than solely reflecting adaptations to diet, head size and shape clearly respond to multiple selective factors, including both diet and habitat use. When physical constraints on head shape are strong (as with underwater prey capture; see Herrel et al. 2008; Segall et al. 2016), convergence is to be expected regardless of the selective drivers (diet or locomotion).

14.3 Function 14.3.1 Prey Detection Searching for prey typically involves at least some locomotion, which is integral to feeding biology but usually studied separately from feeding (Higham 2007). Foraging involves morphological, physiological, mechanical, and behavioral traits, and has immediate consequences for feeding success as well as longer term consequences for life history, reproduction, and fitness (McLaughlin 1989; Beaupre and Montgomery 2007). Although different foraging modes are broadly associated with distinct sets of traits, variation, and flexibility among snakes defy simple characterization of foraging modes into active and ambush foragers (Greene 1997; Beaupre and Montgomery 2007). During foraging, snakes may detect prey chemically, visually, or mechanically. Tongue flicking is a particularly important sensory behavior in snakes that involves the transport of stimuli from the external environment to the vomeronasal organ (also known as the Jacobson’s organ) in the roof of the mouth. Tongue flicking is brought about by a hydrostatic mechanism involving elongation of the posterior part of the tongue (de Groot et al. 2004). Recent studies have shown that oscillatory tongue flicks are most likely used to collect odorants (Daghfous et al. 2012), such as during foraging. In contrast, simple downward extension when the tongue touches an object or the substrate likely serves to sample nonvolatile chemical stimuli (Daghfous et al. 2012). After tongue extension, the tongue is retracted into the oral cavity and chemicals are transferred to the Jacobson’s organ. However, the exact mechanism of transfer remains poorly understood. For lizards with unforked tongues, the transfer from the tongue to the vomeronasal organ may take place through a hydraulic mechanism, with the anterior tongue acting as a piston (Filoramo and Schwenk 2009). Whether a

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similar mechanism operates in snakes remains unknown. Although it had been suggested that a forked tongue may allow snakes to compare paired stimuli (Schwenk 1994), recent studies that employed unilateral transections of the vomeronasal nerve indicated that this may not be the case, as rattlesnakes were able to trail prey even after unilateral nerve transection (Parker et al. 2008). Thus, the deeply forked tongue may serve only to increase the odor sampling area (Parker et al. 2008). In some aquatic species, the tongue may also be used to lure fish by keeping it rigidly extended with only the very tips touching the water (Welsh and Lind 2000). In addition to using chemical and visual cues, sand vipers (Cerastes; Young and Morain 2002) and probably other snakes can use ground-borne vibrations to localize prey (Randall and Matocq 1997; Friedel et al. 2008). Aquatic snakes also possess specialized mechanoreceptors (scale sensillae) that may detect water motion (Povel and van de Kooij 1997; Westhoff et al. 2005; Catania et al. 2010; Crowe-Riddell et al. 2016), especially in snakes that forage in low-visibility environments (e.g., Hart et al. 2012; Crowe-Riddell et al. 2016). Yellow anacondas (Eunectes notaeus) can detect water-borne vibrations in laboratory experiments, although the extent to which they do so in the wild or for predation remains unknown (Young 2007). Snakes can also detect airborne sounds and respond with consistent predatory or defensive behaviors, which suggests that auditory stimuli may be more important to snakes than is currently recognized (Young and Aguiar 2002; Young 2003). Pit vipers and some boas and pythons can detect infrared light (heat) using pit organs on the face. Pit organs may be used for predation, defense, thermoregulation, or other functions. To date, pit organs have been studied more thoroughly in pit vipers than in boas and pythons. Recent work has shown that infrared detection involves heat-sensitive ion channels in the pit organs (Gracheva et al. 2010). Eye and pit sizes are negatively correlated in crotaline snakes, suggesting a trade-off in functions and perhaps selective pressures between eyes and pits (Liu et al. 2016). However, the results of heat-transfer analyses suggesting that images formed by pit organs are poorly focused and of low contrast (Bakken and Krochmal 2007) seem to imply a limit to how much the trade-off between eyes and pits could favor the pits. Nevertheless, pit organs are highly sensitive and can be used in prey acquisition. For example, rattlesnakes (Crotalus atrox) can detect infrared stimuli that simulate a rodent at distances up to 100 cm (Ebert and Westhoff 2006). Ball pythons (Python regius) can detect moving infrared stimuli at distances up to 30 cm, and assess their direction and distance independently of visual cues (Ebert et al. 2007). Respiratory evaporative cooling of the snout in rattlesnakes can enhance the temperature difference between the pit organs and endothermic prey, thus enhancing pit organ function in predation (Cadena et al. 2013). Pit organs may also be important to other functions besides predation. Krochmal and Bakken (2003) found that rattlesnakes can use their pit organs in thermoregulation; they further suggested use in thermoregulation as a possible alternative hypothesis to prey acquisition for the evolution of pit organs. In a broader comparative study, Krochmal et al. (2004) showed that diverse pit vipers can rely on facial pits for thermoregulatory movements, suggesting that the use of pit organs for thermoregulatory behaviors may represent an ancestral trait among pit vipers. It seems plausible that the evolution of pit organs involved simultaneous benefits to predation, defense, and thermoregulation; however, it may be difficult to test these hypotheses separately from one another.

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14.3.2 Prey Capture Snakes capture prey using movements of the head, jaws, and some length of the anterior trunk; the same or similar movements are often used in defensive contexts. These movements are usually called “strikes,” although other terms have been used (lunge, lateral sweeping, slow-capture techniques, and fast-capture techniques) based on the use and speed of the body and head (Cundall and Greene 2000; Alfaro 2003; LaDuc 2002). Of any behavior displayed by snakes, striking is one of the most widely known, yet least studied and understood behaviors. Confounding the dearth of knowledge is inconsistency in the variables used to characterize strikes and ambiguity in the literature about differences between predatory and defensive strikes. It is difficult to draw generalizations when comparing results from different methods, variables, species, and types of strikes. Nevertheless, here we review some key themes from research on snake strikes and note directions of future research that are likely to be productive. Cundall and Greene (2000) equated prey capture with ingestion. However, prey capture often involves distinct movements from ingestion. Below we discuss the distinct movements involved in prey-capture mechanisms such as striking and biting, prey-handling mechanisms such as constriction and pinioning, and ingestion mechanisms such as mandibular or maxillary raking, snout shifting, and pterygoid walking movements. Once a prey animal has been detected, it must be captured. Capture can involve simple biting or seizing of prey, lateral sweeping movements with open jaws to capture prey (particularly in aquatic feeding), or lunging or striking to make contact with prey from some distance.

14.3.2.1

Biting and Simple Seizing

Small prey, regardless of type, are often simply grasped with the jaws and quickly swallowed alive (Cundall and Greene 2000). This simple-seizing method of prey capture appears to be the only prey-capture mechanism used by scolecophidian snakes, although scolecophidians also use unique intraoral transport mechanisms (Kley and Brainerd 1999; Kley 2001; discussed further below) and sometimes further processing (i.e., decapitating termites; Mizuno and Kojima 2015). Many alethinophidian snakes also employ simple biting or seizing behaviors, although they have not yet been well studied (Cundall and Greene 2000). Some alethinophidians appear to use biting or simple seizing exclusively, whereas others modulate their prey-handling behaviors in response to cues from the prey (de Queiroz 1984; Cundall and Greene 2000; Bealor and Saviola 2007; Fig. 14.2). Even some larger prey that are neonatal or harmless will be ingested without further use of more complex prey-handling behaviors (de Queiroz 1984). In a separate section below, we discuss ingestion mechanisms employed once a prey item has been captured. Upon prey capture, many nonvenomous snakes must remain in contact with the prey, regardless of its type or size, until it is consumed or subdued. Snakes may use

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Fig. 14.2 a Pinion method of prey handling used by the bullsnake, Pituophis melanoleucus, b pinion plus nonoverlapping loop, c fully encircling coils (reproduced from de Queiroz 1984)

their jaws or portions of their body to hold onto prey, and in some cases will release the prey from the jaws after initial contact. The high degree of cranial kinesis in snakes is thought to reduce bite forces (Jayne et al. 2002). Some theoretical models have predicted bite capacity in snakes based on skull morphology (Mori and Vincent 2008), but unfortunately bite forces in snakes are largely unexplored. The strong bites required to hold onto and sometimes directly subdue large and strong prey indicates that quantifying the jaw forces used in biting and ingestion in snakes could provide interesting and surprising results. However, to our knowledge, bite force has been quantified in only one species of snake thus far (Lampropeltis getula; Penning 2017a).

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Penning (2017a) found that bite forces in kingsnakes (Lampropeltis getula) were within the range of bite forces in lizards, but lower for a given head size than in lizards. Interestingly, when kingsnakes experienced simulated prey struggling (via manual movement of the bite-force sensor), they responded by momentarily increasing their bite forces, although the forces never reached the initial peak performance. Bite force and constriction pressure were positively correlated with one another, which is expected because snakes often use their jaws to capture and hold onto prey while they constrict it (Penning 2017a). Given the great diversity of diets among snakes, it seems likely that bite forces also vary widely among species and may be surprisingly high in large snakes and those that subdue vigorous prey using only their jaws. For example, snakes in the genera Drymarchon and Masticophis are noted for having powerful jaws (Werler and Dixon 2000; Ernst and Ernst 2003; Gibbons and Dorcas 2015) and have been documented to subdue large prey such as rats, cats, rabbits, and opossums using only their jaws (reviewed in Ernst and Ernst 2003; Stevenson et al. 2010). These snakes appear to deliver strong bites and may forcefully thrash prey. Thrashing appears to quickly incapacitate prey but is well tolerated by the snakes (Cundall and Greene 2000). These snakes are also noted for swallowing live vertebrates that are still mobile and can be seen moving within the esophagus (Lillywhite 2014). Potential differences between feeding and defensive bites in all snakes remain to be determined.

14.3.2.2

Open-Mouthed Sweeping

Many aquatic and semiaquatic snakes capture prey by sweeping the head and anterior trunk from side to side with an open mouth (e.g., reviewed by Cundall and Greene 2000, and later quantified by Alfaro 2003). Nerodia rhombifer and Thamnophis elegans both sometimes forage using relatively slow lateral sweeping movements of the anterior trunk and head with the mouth open (Alfaro 2003). These sweeping movements may occur from a stationary position, during forward swimming, or after an unsuccessful forward strike. However, the faster lateral and forward strikes also differed kinematically among N. rhombifer, T. elegans, and T. couchii. Hence, the term “sideways sweeping” is inadequate for characterizing the diversity of foraging movements both within and among species (Alfaro 2003). The similarities in lateral sweeping movements among distantly related species suggested convergent evolution of this prey-capture mechanism (Cundall and Greene 2000). However, upon testing for convergence in European and North American natricine snakes, Bilcke et al. (2006) found that aquatic prey-capture strategy and strike velocity were significantly correlated with prey density, not with diet. Additional research on the mechanisms and evolution of aquatic feeding in snakes is likely to reveal yet more diversity.

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Striking

Snakes that feed on wary, highly mobile, or large prey often capture it using lunges or strikes from some distance. Both classic (Klauber 1972; Parker and Grandison 1977) and recent work (LaDuc 2002) have described a strike as a lunge. Cundall and Greene (2000) noted the distinction between short and slow lunges and long and fast strikes. This dichotomy is qualitative and probably represents an oversimplification of a performance continuum (Cundall et al. 2007), although the dichotomy seems to apply at least broadly to the thamnophiine snake studied by Alfaro (2002, 2003). Given our limited data and the variable nature of striking in snakes (Smith et al. 2002; Alfaro 2002, 2003; Cundall et al. 2007; Penning et al. 2016), as well as the likelihood of future advances in our understanding of snake strikes, we feel that it is premature to try to classify and apply standardized terms to the types of strikes. Similarly, Higham et al. (2017) felt that strikes must be quantified in nature before we can fully assess strike performance. In this review, we define a strike broadly as a distinct movement of the head toward a target that may be a threat or prey; such a strike may be forward or lateral, and may be slow, intermediate, or fast. Whether scolecophidian snakes can even strike remains to be seen. Given their burrowing lifestyle and slow-moving prey, it is unlikely that predatory striking behavior is needed or could even be employed in their subterranean environments (Cundall et al. 2007). To date, what we know about striking derives from alethinophidians, and particularly from booid (Frazzetta 1966; Cundall and Deufel 1999; Deufel and Cundall 1999; Cundall et al. 2007) and colubroid snakes (Van Riper 1954; Greenwald 1974, 1978; Janoo and Gasc 1992; Kardong and Bels 1998; LaDuc 2002; Herrel et al. 2011; Penning et al. 2016). Most studies have addressed forward strikes in a terrestrial environment over a relatively narrow range of temperatures (ca. 25–30 °C). A few studies have addressed strikes that involve lateral or undulatory movements (e.g., Kardong and Bels 1998; Smith et al. 2002; Alfaro 2003; Catania 2009, 2010), and even fewer studies have addressed terrestrial-to-aquatic strikes (e.g., Vincent et al. 2005), or arboreal strikes (Herrel et al. 2011). There is no typical pattern that represents these diverse strikes. Future studies are likely to discover considerable variation in strikes related to size, temperature, behavioral context, environment, species, lineages, and other variables. Both prestrike behaviors and strikes differ in feeding and defensive contexts (see Young et al. 2001b; LaDuc 2002), and the outcomes of strikes can have major fitness consequences. The roles of feeding strikes are clear: to make contact with prey so that the next stages of feeding can occur (such as constriction, envenomation, ingestion, etc.). The overall role of defensive strikes is also fairly clear: to deter a potential threat from a predator. However, the specific goals of defensive strikes are not well known, and may include maintaining or enlarging the gap between the snake and the threat (i.e., no contact), making contact to deter the threat directly by bluffing, startling it, causing pain, or perhaps other functions. It is important to be careful when making inferences about one kind of strike from another because predatory strike performance may not be a reliable predictor of defensive strike performance and vice versa. Offensive and defensive strike metrics are often used interchangeably because the behaviors appear qualita-

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tively similar; however, they can be quantitatively distinct and should be treated as separate performance metrics. Much of the previous work on strike performance has focused on the kinematics of the head and jaws during strikes (Cundall and Deufel 1999; Deufel and Cundall 1999; Cundall and Greene 2000; Cundall et al. 2007). Fewer studies have quantified axial kinematics during striking. The limited evidence available, which is mainly from heavy-bodied vipers, indicates that prestrike posture does not appear to affect strike kinematics (Kardong and Bels 1998; Young 2010). Whether this applies to nonviperid snakes warrants testing. Different patterns of axial movement can be used to push the head forward. In feeding strikes, Kardong and Bels (1998) described a “gate model” of straightening in which accordion-like axial bends in the anterior trunk straighten out, and a “tractor-tread” model in which the body flows through a postural curve, with limited straightening. Alfaro (2003) also noted feeding strikes matching both the open-gate model and the tractor-tread model in thamnophiine snakes. For his study species with the fastest strikes, Thamnophis couchii, the opengate mechanism produced the highest speeds by enabling the snake to recruit a larger proportion of the body. Indeed, more axial bends should sum to a greater resultant velocity. Alfaro (2003) also noted that the tractor-tread model applied more clearly to the posterior parts of the trunk than anterior ones in T. elegans, and that by exerting forces posteriorly against the water, the posterior part of the body probably contributes to sideways sweeping and may contribute to the motion of forward strikes as well. The similarity of the tractor-tread model to undulatory locomotion was clear (Kardong and Bels 1998), and makes us wonder whether the patterns of axial muscle activation are similar to those of locomotion, and whether tractor-tread strikes are slower than open-gate strikes and involve more continuous motor control rather than ballistic control that cannot be adjusted via feedback once initiated. Such questions remain to be addressed in future research. As with axial movements during striking, little work has addressed the mechanisms that produce and control strikes. Young (2010) showed that several muscles are electrically active in Bitis arietans before defensive strike movements begin, suggesting that the strikes are ballistic and powered by an elastic recoil mechanism. However, both the ballistic nature and possible elastic mechanisms of strikes remain uncertain. Some snake strikes may be ballistic, with the rapid movements involved and functional limitations of sensory processing precluding mid-strike adjustments (Cundall et al. 2007). Kardong and Bels implied ballistic motion in feeding strikes by stating that adjustments to strike trajectory or in response to prey evasion are made after contact, not during forward movement. However, Frazzetta (1966) discussed a snake changing course during a strike. Some indirect evidence suggests that strikes may not be ballistic. Many ballistic movements powered by elastic recoil mechanisms are independent of temperature across diverse organisms (Anderson and Deban 2010; Deban and Lappin 2011; Deban and Richardson 2011; Deban and Scales 2016), whereas the few relevant studies thus far have shown significant temperature dependence in strike performance in snakes (Greenwald 1974, 1978; Shine et al. 2002). Young (2010) suggested that some snakes may use elastic mechanisms

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to power striking, whereas others may use different mechanisms. Additional research on strike mechanisms is clearly needed to resolve these issues, and may have broader implications for our understanding of vertebrate muscle function and its evolution. Three other important aspects of snake strike performance are beginning to be studied: How body size, environment, and predator–prey interactions affect strike performance. In general, larger snakes can strike over longer absolute distances than smaller snakes if they use the same proportion of their body. Due to correlations among variables in strikes (duration, distance, velocity, and acceleration) and the fact that some snakes continue to accelerate through both feeding and defensive strikes (Young et al. 2001a; LaDuc 2002; Vincent et al. 2005; Herrel et al. 2011), longer strikes typically produce higher velocities before prey contact. Herrel et al. (2011) showed that adult Trimeresurus albolabris striking defensively from arboreal perches cover the same absolute strike distance as juveniles, leading to similar strike velocities across a range of body sizes. This result also means that the strike distances of juveniles are longer relative to their body size than in adults, suggesting selective pressures on juvenile strike performance. However, LaDuc (2002) showed that Crotalus atrox, a terrestrial pit viper, will strike over twice as far at a potential threat than at prey. Whether or not arboreal feeding strikes differ from the defensive strikes studied by Herrel et al. (2011) remains to be tested in future research. Many snakes are aquatic or semiaquatic, and experience stronger environmental constraints on fast movements such as striking due to the higher drag experienced when moving in water than in air. The fully aquatic tentacled snake, Erpeton tentaculatus, reaches one of the highest strike accelerations and shortest durations yet determined in any snake (Smith et al. 2002). Tentacled snakes also exploit the stereotyped C-start maneuver of fish to capture them effectively (Catania 2009, 2010). They do so by feinting with their body to elicit a C-start in a nearby fish, which then moves toward the snake’s advancing jaws or toward a position the snake anticipates and strikes toward (Catania 2009, 2010). The prey-capture mechanism of tentacled snakes appears unique. However, some snakes can use rapid forward strikes to capture aquatic prey, in addition to the lateral sweeps described above, despite apparent hydrodynamic constraints. Alfaro (2002, 2003) found that Thamnophis couchii, T. elegans, and Nerodia rhombifer all can use rapid forward strikes in addition to the slower lateral sweeps. Thamnophis couchii achieves the highest forward strike performance by recruiting and straightening nearly its entire body (Alfaro 2003). Researchers have hypothesized that underwater strikes may be hindered by drag and may generate bow waves that displace prey and make capturing it more difficult (Young 1991; Vincent et al. 2005). However, recent hydrodynamic modeling has shown that the effects of drag and displacement of prey during aquatic strikes is probably less important than previously thought (Van Wassenbergh et al. 2010). The effects of gape appear to be particularly important in aquatic strikes (Van Wassenbergh et al. 2010), yet largely remain to be studied experimentally. Studies of strike kinematics have begun to illustrate differences in strike performance as well. However, which aspects of strikes are good indicators of performance is not yet clear and may differ with circumstances. Variables that may be good indicators of performance include strike acceleration, velocity, duration, success rate,

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and perhaps other variables. In predatory strikes, which often involve only short distances (LaDuc 2002; Clark et al. 2012; Higham et al. 2017), acceleration may be more important than velocity because strikes typically do not involve a chase, and rapid acceleration is necessary to help a snake close the gap between itself and the prey before the prey can evade the strike (Penning et al. 2016). In defensive strikes, acceleration may be the crucial variable if contact is important, because high acceleration is required to make contact before the target evades. However, if contact is not a goal of defensive strikes, then neither acceleration nor velocity may be important, except perhaps to the extent that they contribute to an effective bluff or startle effect. Vipers have often been assumed to have the highest strike performance (e.g., Van Riper 1954; Klauber 1972; Janoo and Gasc 1992; Whitaker et al. 2000). However, Penning et al. (2016) showed that at least one nonvenomous colubrid snake (Pantherophis obsoletus) can strike defensively with similar levels of performance to vipers (Agkistrodon piscivorus and Crotalus atrox; Fig. 14.3). Although the performance of feeding strikes in these snakes is still under study, we predict that feeding strikes will also involve similar and high levels of performance. These snakes often feed on the same or similar prey (e.g., small rodents), which presumably imposes similar demands on strike performance, regardless of which snake is involved. To

Fig. 14.3 Video images of defensive strikes by Pantherophis obsoletus (top) and Crotalus atrox (bottom) recorded at 250 frames s−1 with a Keyence camera (Itasca, IL, USA) (reproduced from Penning et al. 2016)

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catch a rodent, any snake needs to strike fast enough to make contact before the rodent escapes. What happens next, whether simple biting, constriction, or injection of venom, is a separate stage of the feeding process that could not happen if the snake did not make contact with the prey. More generally, we suspect that snake strike performance is driven largely by the response times of predators and prey, largely independent of phylogeny. Historically, field observations of snake strike performance were rare. We know so little about strikes in natural environments that lab tests may not reflect the actual conditions in which snakes use this behavior, although a few studies have observed that wild rattlesnakes may strike with similar kinematics to captive snakes (Cundall and Beaupre 2001; Clark et al. 2012; Higham et al. 2017; Fig. 14.4). These studies have begun to offer important insights into strike performance in nature. During feeding strikes in the wild, rattlesnakes (Crotalus spp.) took averages of 0.07–0.2 s to reach their targets (Cundall and Beaupre 2001; Clark et al. 2012; Higham et al. 2017); the fastest strikes overlapped with the 0.05–0.08 s average strike durations measured under laboratory conditions, but strikes in the wild often took much longer than those in the lab (LaDuc 2002; Penning et al. 2016). Strike durations in both the lab and the wild can be so short that snakes may avoid sensory detection by their prey, reaching them before the prey are even aware of the threat (Penning et al. 2016). However, field recordings of rattlesnake strikes show that some prey can detect imminent strikes and rapidly evade them or retaliate if evasion is unsuccessful (Cundall and Beaupre 2001; Clark et al. 2012; Higham et al. 2017). Clark et al. (2012) found that strike success (prey capture) in the field was significantly related to strike distance (Fig. 14.5), which supports laboratory results of snakes striking only when prey move close enough (LaDuc 2002). In 49% of field strikes, prey initiated evasive maneuvers, significantly increasing their chances of avoiding predation (Clark et al. 2012); similarly, Higham et al. (2017) recorded four successful and four unsuccessful strikes by C. scutulatus in the wild. Selection for high strike performance may be influenced by the prey’s sensory and response capacities (Penning et al. 2016; Higham et al. 2017). Recent field recordings have shown that both rattlesnakes and their prey are capable of high accelerations (ca. 500–600 m s−2 ) during striking and evasion over very short durations (Higham et al. 2017). More analyses of strikes in nature and of prey response times and behaviors are needed to better understand the dynamics and evolution of this crucial component of snake predation. As a snake makes contact with prey, it must quickly accomplish the next stage, such as anchoring the jaws onto the prey, injecting venom and retracting, or forming a constriction coil or equivalent posture, before the prey can escape or defend itself. Whatever the subsequent predation mechanism, the snake’s jaws become the interface between the two organisms. Small or harmless prey is often ingested alive, with the snake remaining in contact with the prey from the moment of capture onward. Larger and more dangerous prey is usually handled differently. Upon contact with prey, jaw closing marks the end of a strike (Cundall and Greene 2000). The mechanism of tooth engagement with prey is not well known and may involve snaring (Deufel and Cundall 1999), downward or rearward stabbing (Frazzetta 1966; LaDuc 2002; but see Deufel and Cundall 1999), or other movements by both snake and prey. For many

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Fig. 14.4 The predictive framework for escape maneuvers of kangaroo rats in response to strikes from rattlesnakes. This sequence of events is expected during natural interactions, and was observed in multiple interactions. Amy Cheu provided these illustrations (reproduced from Higham et al. 2017)

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Fig. 14.5 Trajectory of prey movement was categorized depending on the relative angle between the anteroposterior axis of the snake (ap) and the movement vector of the prey (pv). PV was calculated by connecting the position of the prey 1 s before strike initiation (P1) with the position of the prey when the strike was initiated (P2). If angle θ was greater than 45°, prey was categorized as moving laterally; if θ < 45°, prey was categorized as moving anteroposteriorly. The case shown would be categorized as lateral retreat, because θ > 45° and the prey item had crossed the AP axis before the strike was initiated (reproduced from Clark et al. 2012)

venomous snakes, venom is quickly delivered and the head is retracted away from the prey after brief contact for venom delivery (reviewed in Cundall and Greene 2000; Lillywhite 2014), although some snakes will remain in contact with prey based on prey size and habitat complexity (Lillywhite 2014). Strikes likely produce enough kinetic energy to drive fangs through tissue without the need for additional contractile forces from the jaws themselves (Anderson et al. 2016). Although strong bite forces are probably not required for fang penetration, pressure at the point of fang penetration may be extremely high because the force of impact of the snake’s head is applied to extremely small areas of the fang tips.

14.3.2.4

Venom Delivery

Venom delivery systems in snakes typically consist of a pair of venom glands, their associated muscles and enlarged teeth (Jackson 2003; Fig. 14.6). Recent years have seen significant advances in our understanding of the regulation of venom expulsion in rattlesnakes. In a series of studies, Young and collaborators describe how the

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Fig. 14.6 Head muscles of a Python regius, showing an unspecialized pattern of external adductor muscles; b the viperid, Vipera aspis; c the elapid, Elapsoidea sundevalli, and d the atractaspidid, Atractaspis dahomeyensis. The adductor externus muscles are shown in color: red, adductor externus superficialis and derived fibers; yellow, adductor externus medialis and derived fibers; blue, adductor externus profundus and derived fibers. Snakes not drawn to the same scale (reproduced from Jackson 2003)

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gland musculature in rattlesnakes is functionally subdivided, allowing the regulation of venom flow (Young et al. 2000). Furthermore, the fang sheath is important in allowing venom expulsion by displacing the inner fang membrane from the entrance orifice of the fang, thus allowing venom flow (Young et al. 2001a; Young and Kardong 2007). The duration of venom flow, flow rate, and total volume of venom delivered were lower in predatory than defensive strikes (Young and Zahn 2001). Surprisingly, although it is difficult to observe without high-speed video recordings, vipers rapidly reposition fangs after contact with prey in more than one-third of their strikes (Cundall 2009). In a comparative study by Cundall and Deufel (2006), there were no significant differences in ingestion performance between colubrids and viperids despite major differences in cranial morphology, perhaps because the venom delivery system of viperids has been subject to little selection pressure for intraoral prey transport or because there are trade-offs between intraoral prey transport and strike performance in vipers. In many vipers and some elapids, venom has complex proteolytic and necrotizing effects, which may enhance the digestion of large prey (Thomas and Pough 1979; Nicholson et al. 2006), although such effects were not found in several recent studies (McCue 2007; Chu et al. 2009; LaBonte et al. 2011). The relationship between snake venoms and diets, and whether or not venom composition is subject to selection, has been difficult to resolve and may vary among species (e.g., Daltry et al. 1996; Sasa 1999a, b; Wüster et al. 1999; Barlow et al. 2009). The wide variation in venom composition, prey types and sizes, and temperature effects on enzyme and digestive function, all indicate the need for more research on the relationship between venom composition and diet, and the functional significance of venom (Mackessy 2010). Significant advances in our understanding of the evolution of the venom itself have come from several recent papers and books (e.g., Chippaux and Huchzermeyer 2006; Mackessy 2009; Fry et al. 2013; Fry 2015; Mackessy and Saviola 2016). Unexpectedly, it is also the venom (specifically the venom disintegrins) that provides the cues used by viperid snakes to relocate their prey after prey release (Saviola et al. 2013). Whereas the anatomy and function of the venom delivery system in viperid and elapid snakes have been relatively well described in the past (Kochva 1978; Underwood 1997; Jackson 2003), recent studies have shed additional light on the morphology of the venom gland (Duvernoy’s gland) in rear-fanged colubrids (de Oliveira et al. 2016). The role of Duvernoy’s gland in piscivorous species appears to be associated with incapacitating prey to facilitate prey handling and transport (Mori 1998; de Oliveira et al. 2016). Other gland types, including labial glands (de Oliveira et al. 2014, 2017) in goo-eating snakes (i.e., species eating earthworms, snails, and slugs) have also been described recently. In addition, a novel protein-secreting delivery system has been described in goo eaters (Zaher et al. 2014). The unusual part of this system is that it opens into the oral epithelium rather than being associated with the teeth (Zaher et al. 2014). Toxin glands in snakes are not restricted to oral glands, however, as some Asian snakes of the genus Rhabdophis have nuchal defensive glands that sequester the toxins from toad prey (Hutchinson et al. 2007, 2013). Moreover, these toxins can be passed on to the offspring from mothers containing high levels of

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toxins (Hutchinson et al. 2007). Our increased understanding of venoms and venom delivery systems now allows for integrative studies linking venom composition with anatomical traits such as head shape and fang length (Margres et al. 2015), showing that there is covariation between anatomical traits (fang length) and venom-related traits (i.e., myotoxin concentration; see Margres et al. 2015).

14.3.2.5

Prey Restraint and Subjugation

As noted above, many snakes remain in contact with the prey after striking and biting. Many nonvenomous and some venomous snakes use portions of the body to subjugate or kill prey prior to ingestion. Critical functions of prey handling after a strike or bite are to prevent the prey animal from escaping and to subdue it so that it can be ingested. Prey-restraint mechanisms include using jaws and teeth to damage prey mechanically, injecting venoms to incapacitate prey, and constricting to incapacitate prey (Cundall and Greene 2000). Five general methods of prey handling have been described in the literature: simple seizing, pinioning, applying a hairpin loop, constriction, and envenomation. Here, we briefly discuss several of these mechanisms, and particularly highlight recent work on venom delivery and constriction. For many venomous snakes, envenomation is the exclusive prey-handling behavior and precludes the need for other behaviors. Other venomous snakes will remain anchored to the prey during envenomation, but may release it if they experience potentially dangerous struggling or defensive movements from the prey. The control and mechanics of venom injection are not well known. Some evidence indicates that vipers can control or meter the amount of venom injected, which has been referred to as the venom-metering hypothesis (reviewed by Hayes et al. 2002) and may be advantageous because venom production appears to be energetically expensive (McCue 2006a). However, the amount of venom injected could also be affected by the pressures in both the snake’s venom-injecting system and prey tissues, which has been called the pressure-balance hypothesis (Young et al. 2001a). Venom-metering and pressure-balance mechanisms are not entirely mutually exclusive, and both can be affected by the highly dynamic movements involved in predator–prey interactions during striking and biting. The extent to which metering and pressure-balance mechanisms determine the amount of venom injected in vipers and other venomous snakes remains poorly understood and in need of further study. We know much less about feeding mechanisms and essentially nothing about factors that control venom in elapids and venomous colubrids, although the basic physics of the pressure-balance mechanism would certainly apply. Elapid snakes, such as the coral snake Micrurus nigrocinctus, appear to hold onto prey after biting until paralysis occurs (Urdaneta et al. 2004), as do several other elapids (Radcliffe and Chiszar 1980; Kardong 1982; Greene 1984). If paralysis does not occur, such as after venom removal by manual milking, then the snakes change prey-handling behavior by moving their initial bites to the head of the prey and then holding onto the head to immobilize the prey by mechanical means (Urdaneta et al. 2004).

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As we noted above, prey that are small or harmless are often captured with simple seizing and then quickly swallowed alive (Cundall and Greene 2000). Many alethinophidian snakes can also modulate their prey-handling behaviors in response to cues from prey (de Queiroz 1984; Cundall and Greene 2000; Bealor and Saviola 2007), using more complex prey-handling behaviors for more active and potentially more dangerous prey (de Queiroz 1984; Cundall and Greene 2000; Bealor and Saviola 2007). If prey struggle or are large, they may be thrashed from side to side while held in the jaws, which appears to subdue them effectively (Cundall and Greene 2000). Alternatively, prey may be further subjugated by pinioning, in which the snake presses the prey against the substrate or the wall of a tunnel (Hisaw and Gloyd 1926; Willard 1977; Greenwald 1978; de Queiroz 1984; Rudolph et al. 2002). Often, pinioning is used to restrain a prey item while it is being consumed (de Queiroz 1984). Pinioning behaviors are not well known, particularly as used in confined spaces that are difficult to observe and record, and need further study. At least two alethinophidian snakes are capable of biting pieces off or out of prey by using a combination of body and jaw movements (Jayne et al. 2002). Many snakes apply loops of the body to prey and squeeze it in a constriction coil (e.g., Greene and Burghardt 1978). Constriction is a behavioral pattern that immobilizes prey with pressure exerted from two or more points along the body (Greene and Burghardt 1978). However, this definition includes both constriction and hairpin loops, which are considered to be distinct in complexity (Bealor and Saviola 2007; Mehta 2009; Penning and Cairns 2016). Constriction behavior evolved early in snakes and represents an ancient behavioral homology across many families of snakes (Greene 1994), although constriction behaviors vary among taxa in ways that we have only begun to characterize (e.g., Mehta and Burghardt 2008). Constriction behavior has been lost in several lineages of snakes, yet was retained or possibly evolved independently in diverse lineages of venomous snakes (Shine and Schwaner 1985). Constriction behavior serves both to restrain and kill prey (Cundall and Greene 2000). Constriction pressure is a good measure of prey-handling performance in constrictors because pressure is one of the key mechanisms that kills prey (Hardy 1994; Moon 2000a; Boback et al. 2015). Constriction pressure is generated by contractions of the axial muscles (Moon 2000a), which have variable scaling relationships among species (Jayne and Riley 2007; Herrel et al. 2011; Penning and Moon 2017). Constriction performance increases with body size both among and within species (Moon and Mehta 2007; Penning et al. 2015; Penning and Dartez 2016; Penning 2017a), although these studies found different maximum pressures and scaling exponents that warrant further study (Figs. 14.7 and 14.8). Constriction performance is reduced due to lower muscle cross-sectional areas after fasting during pregnancy (Lourdais et al. 2004), but can be restored within weeks after feeding resumes (Lourdais et al. 2005). Much of the previous work on constriction performance focused on how snake morphology and body condition affect constriction performance. Recent work has also shown differences in constriction performance related to differences in prey characteristics and diet. Prey size does not affect the constriction performance of kingsnakes (Lampropeltis getula) feeding on prey of 5–15% relative prey mass, but prey size plays an important role during sequential encounters with prey

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Fig. 14.7 Peak constriction pressures measured for snakes of different sizes (N  12 species and 30 individuals). The line indicates a bivariate least-squares linear regression (y  7.72xl.39 , R2  0.88). Hollow circles indicate species of Acrantophis, Boa, Charina, Lichanura, and Sanzinia; diamonds indicate species of Morelia; solid circles indicate species of python; squares indicate species of Lampropeltis, Pantherophis, and Pituophis; the star indicates Tropidophis haetianus; and the triangle indicates the predicted pressure for a giant (30 cm in diameter) constrictor (reproduced from Moon and Mehta 2007)

(Penning 2017b). Multiple feeding events on large prey led to a reduction in constriction performance not seen in snakes feeding on multiple small prey. Kingsnakes also generate higher constriction pressures than their intraguild competitors (rat snakes, Pantherophis spp.; Penning and Moon 2017) and are capable of killing these other constrictors with constriction (Jackson et al. 2004). Currently, the only distinguishable difference between these snakes is their coil posture during constriction, which suggests that coil posture affects the pressure exertion (Penning and Moon 2017). Kingsnakes reliably use spring-like coils, whereas rat snakes use less regular and highly variable coil postures. Additional research on possible differences in muscle anatomy and function between kingsnakes and rat snakes is currently underway and may help explain the mechanisms of successful intraguild predation by kingsnakes on other constrictors. Historically, constriction was thought to kill prey by suffocation, and although an alternative mechanism was proposed almost a century ago (McLees 1928), ventilatory disruption and suffocation remained the most invoked cause of death by constriction in the literature (e.g., Parker and Grandison 1977; Zug 1993; Cundall

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Fig. 14.8 Constricting pythons coil around and squeeze prey animals, which exerts pressure on the prey that scales positively with snake diameter. a A 1081 g juvenile Burmese python (Python molurus bivittatus) constricting a lab rat (Rattus norvegicus) weighing 99 g. b The scaling relationship between peak constriction pressure and snake diameter (reproduced from Penning et al. 2015)

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and Greene 2000). Hardy (1994) reassessed the observations of McLees (1928) that constriction can kill small mammals faster than suffocation alone, and supported McLees’s hypothesis of circulatory arrest as the primary mechanism of death by constriction. Moon (2000a) was the first to measure constriction pressures and showed that Pituophis melanoleucus and Lampropeltis getula could exert pressures well above the systolic blood pressures of mice, which meant that they were high enough to induce circulatory arrest in mice. Furthermore, Moon (2000a) determined that the snakes could detect prey movements as subtle as heartbeats and would respond with increased constriction pressures. Both of these findings were later corroborated by Boback et al. (2012, 2015). Constriction is usually used to kill endothermic prey, whereas restraining constriction may be more common with ectothermic prey, which is then eaten while still alive (Greene and Burghardt 1978; Cundall 1987; Hardy 1994; Cundall and Greene 2000; Boback et al. 2015). However, constriction involves a highly dynamic interaction between predator and prey, and several aspects of this interaction may affect the outcome. Snake and prey sizes are obvious variables that probably affect the mechanism and outcome of constriction (Mehta 2003; Moon and Mehta 2007). Constriction by very small snakes involves low pressures that may kill prey by suffocation (Moon and Mehta 2007). However, the constriction pressures exerted by diverse snakes are often high enough to make circulatory arrest the proximate mechanism of death in mammalian prey (Moon 2000a; Moon and Mehta 2007; Boback et al. 2015; Penning et al. 2015; Penning and Dartez 2016). Constriction may cause internal bleeding and high tissue pressures (Greene 1983; Penning and Dartez 2016), interfere with or damage neural tissue (Penning et al. 2015; Penning and Dartez 2016), and in large snakes perhaps damage the spine of a prey animal (Rivas 2004). The dynamic and variable movements of constrictors and their prey may affect the mechanism and outcome of constriction more than the predator–prey size relationship (Moon and Mehta 2007). The assumption that constriction restrains rather than kills ectothermic prey appears to be based largely on inferences about ectotherm physiology. Ectothermic prey is thought to be more resistant to constriction than are endotherms (Hardy 1994; Boback et al. 2012, 2015) due to their lower oxygen demands and higher tolerance of hypoxia than endotherms (Pough 1980). Ectotherms are thought to fatigue quickly, but are otherwise eaten alive (Hardy 1994; Cundall and Greene 2000; Boback et al. 2015). When constriction kills ectothermic prey, it is assumed to take much longer than for endotherms (Zug 1993; Boback et al. 2015). However, the hypothesized effects of constriction on ectothermic prey have not been tested and remain speculative. Many questions remain about how constriction affects ectothermic prey. For example, how does the constrictor, an ectotherm, endure the pressures exerted by constriction longer than the prey animal, another ectotherm, if both have similar physiology and similar susceptibility to fatigue? Kingsnake constriction of other snakes has been observed to last over 7 h (Jackson et al. 2004), although we have observed constriction to kill lizards in minutes. Hence, we recommend both caution in perpetuating assumptions about how constriction affects ectothermic prey and more careful research on this issue in the future. The diverse factors that determine constriction performance and how it affects prey clearly need to be studied further.

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14.3.3 Prey Transport 14.3.3.1

Intraoral Transport

Once a snake has captured a prey item (and subdued it in the species that do so), the snake begins ingestion movements that are collectively called prey-handling, prey-transport, or intraoral transport. Prey-transport mechanisms have been studied in diverse snake lineages, although in relatively few species. Most studies have addressed the morphology and kinematics of jaw function and cranial kinesis, whereas much less research has addressed the forces involved in prey transport and postcranial transport. However, recent studies have advanced our understanding of snake feeding structures and mechanisms in several important ways. The first detailed functional studies of feeding in scolecophidian snakes (blind snakes or thread snakes) were those of Kley and Brainerd (1999) and Kley (2001). Within the scolecophidians, leptotyphlopids are characterized by having teeth only on the lower jaw and by having toothless upper jaw elements that are firmly attached to the rest of the head. Leptotyphlops dulcis uses bilateral mandibular raking of the highly kinetic lower jaw to ingest very small prey items such as the larvae and pupae of ants and termites (Kley and Brainerd 1999; Kley 2001). These raking movements appear to be powered directly by muscles and are relatively fast, occurring 2–3 times per second, and allow the snakes to ingest many small prey items quickly. As prey is ingested, the anterior part of the trunk is flexed slightly vertically and then straightened in movements that appear to augment ingestion, although axial bending appears not to be involved in postcranial swallowing (Kley and Brainerd 1999). In contrast to the leptotyphlopids, typhlopid snakes are characterized by having teeth only on the upper jaws, which are mobile, and toothless lower jaws that are relatively rigid and akinetic. Typhlops lineolatus and Rhinotyphlops schlegelii have similar cranial morphology and feeding mechanisms that involve rapid (3–5 Hz) bilateral maxillary raking movements to ingest the larvae and pupae of ants and termites (Kley 2001). The fast raking movements appear to be produced indirectly through movements of the pterygoid and palatine bones (Kley 2001); as in the leptotyphlopids, these fast movements allow the snakes to ingest many small prey items quickly. Both mandibular and maxillary raking function as both prey capture and ingestion mechanisms. In contrast to the distinctive raking mechanisms in blind snakes, alethinophidian snakes all use alternating left and right ratcheting movements of jaws (Kley 2001). Most alethinophidian snakes have long, toothed medial upper jaws (palatopterygoid arches) and toothed mandibles. The tips of the mandibles are connected by a stretchable ligament that allows the left and right mandibles to separate widely during ingestion and to move fore and aft largely independently of one another. The posterior ends are connected by ligaments to the upper jaws, which tends to couple the movements of upper and lower jaws on the same side. Given the unique feeding mechanisms in scolecophidian snakes, Kley (2001) noted that unilateral feeding may have been ancestral for snakes and was subsequently lost in the scolecophidians, or that it may have evolved within the Alethinophidia, which

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he felt was the more parsimonious hypothesis. In Cylindrophis ruffus, which may represent an early branch of alethinophidian snakes, the palatomaxillary arches are attached fairly firmly to other bones in the snout (Cundall 1995). During intraoral transport, Cylindrophis ruffus uses first lateral movements of the posterior braincase and unilateral movements of the toothed jaws to move its head over prey in a mechanism called “snout-shifting,” and then bilateral movements of the jaws coupled with anterior vertebral bending. The mandibular tips separate only moderately (up to two times their resting separation), which limits their gape, but a mobile intramandibular joint allows the mandibles to conform to variable prey. Upper jaw mobility in Cylindrophis involves the ventral snout and does not result from reduced attachments to the braincase and snout. Cundall (1995) concluded that palatomaxillary kinesis in Cylindrophis is intermediate between the limited degree in lizards and the greater kinesis of advanced snakes, and that evolutionary changes in the snout were critical to diversification of the feeding apparatus in alethinophidian snakes. In some snakes, such as snail-eating snakes, the lower jaws have become more important to feeding than the upper jaws (Hoso et al. 2007; dos Santos et al. 2017). In most alethinophidian snakes, particularly those with large gapes and substantial cranial kinesis, the upper jaws are more loosely connected to the snout and can protract and retract somewhat independently of the rest of the head. During ingestion, the upper and lower jaws protract together on one side and retract on the other side, with lesser movements of the snout and braincase; the protraction and retraction movements alternate on the left and right sides to ingest prey in a mechanism called the pterygoid walk (Boltt and Ewer 1964). The pterygoid walk appears to involve the snake’s head advancing forward over the prey, which often remains stationary relative to the ground (Dullemeijer 1956; Albright and Nelson 1959; Gans 1961; Frazzetta 1966). However, at least a few alethinophidian snakes, such as African mole vipers (Atractaspis spp.), have modified fangs and cranial morphology that make them unable to use pterygoid walking movements (Deufel and Cundall 2003); instead, these snakes ingest prey using cycles of mandibular adduction, anterior trunk compression, ventral flexion of the head, and ultimately extension of the head and anterior trunk over the prey. Few studies have recorded the cranial muscleactivation patterns associated with feeding (e.g., Cundall and Gans 1979; Cundall 1983), and most species remain to be studied. However, recent research has begun to quantify and compare ingestion performance based on the number of pterygoid walking movements (jaw protractions) or time required to ingest prey (e.g., Vincent and Mori 2008; Vincent et al. 2006b, 2009; Hampton 2011, 2014; Pereira et al. 2016). With large prey items that are a substantial fraction of the snake’s weight, pulling the prey into the mouth probably requires forces higher than the relatively small jaw muscles can exert, whereas advancing the head over the prey may reduce the jaw forces needed and allow some of the axial muscles to contribute to ingestion. However, snakes sometimes lift the prey off the ground at some point before ingestion is complete; we have observed such movements in some boids and colubrids ingesting rodent prey, although how many kinds of snakes use such movements and with what sizes of prey are not yet well known. If the head and prey are tilted upward enough, then snakes may be using gravity to aid in ingestion; alternatively, these movements

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may indicate that the jaw muscles and bones (and anterior axial muscles associated with the head) exert forces high enough to pull prey into the mouth. As noted above, an increased gape was important to the evolution of diverse snakes (Cundall and Greene 2000; Rieppel 1988). Surprisingly, despite its importance to the function and evolution of snakes, gape has usually been addressed qualitatively or with indirect quantitative indices. The term “gape” may refer to different aspects of the mouth opening, such as the maximum angle achieved at the jaw joint during mouth opening or maximum cross-sectional area that can be achieved at the posterior end of the oral cavity (Hampton and Moon 2013). Cross-sectional area of the posterior oral cavity and anterior esophagus appear to be critical to gape (Cundall et al. 2014; Fig. 14.9). Among the various skeletal elements that may contribute to gape area, the lengths of the lower jaw and suspensory elements, and the width of the head, have been hypothesized to be particularly important because they could affect the maximum size of the mouth opening (Cundall 1987; Cundall and Greene 2000; Hampton and Moon 2013; King 2002; Miller and Mushinsky 1990). Recently, Hampton and Moon (2013) quantified the maximum gape in western diamond-backed rattlesnakes (Crotalus atrox) as the largest cross-sectional area that could be achieved during forced swallowing in thawed specimens that had been frozen previously but not chemically preserved. They then tested which were the best predictors of gape area

Fig. 14.9 Lateral diagrammatic view of the head and anterior trunk of a macrostomate snake to show how the floor of the mouth is arranged during ingestion of large prey. The net effect is that the mandibles surround the entry to the esophagus, not the oral cavity, while the palatomaxillary arches rachet the snake’s head over the prey. The tongue is normally not visible during transport, possibly because the tongue sheath is compressed beneath the prey (reproduced from Cundall et al. 2014)

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among several external and cranial skeletal measurements and two published gape indices from King (2002) and Miller and Mushinsky (1990). They found that body length was the best predictor of maximum gape and when body length was excluded from the analysis, quadrate and mandible lengths were the best predictors of maximum gape. Quadrate length probably contributes to gape area directly; however, the importance of mandible length to gape area was less clear and may relate to its covariation with head width (Vincent et al. 2006a). Two published gape indices did not prove to be better indicators of actual gape than the jaw and quadrate lengths, and the gape values they produced differed significantly from the empirically determined gapes. It would be beneficial to test these results against those from fresh specimens because the properties of soft tissues may be critical in determining maximum gape areas or angles (e.g., Close and Cundall 2014; Close et al. 2014; Cundall et al. 2014). Furthermore, additional research has indicated that the morphological predictors and scaling of gape differ among species and perhaps lineages (Hampton 2014; Hampton and Kalmus 2014). Several aspects of prey items may also limit a snake’s ability to ingest them. For example, prey shape and type may affect ingestion performance (Pough and Groves 1983; Vincent et al. 2006a, b; Wilson and Hopkins 2011; Close and Cundall 2012) in addition to prey mass (Forsman and Lindell 1993). Moreover, prey shape can also affect locomotor performance once the prey has been ingested (Wilson and Hopkins 2011), suggesting that this aspect of diet can have significant fitness consequences. Comparative studies of gape and the effects of prey dimensions and properties on feeding performance could help clarify key functional shifts in the evolution and diversification of snakes. Two species of snakes are known to circumvent gape limitation by biting pieces out of prey. The homalopsine snakes Gerarda prevostiana and Fordonia leucobalia bite pieces out of freshly molted crabs (Shine and Schwaner 1985; Jayne et al. 2002). This feeding mechanism appears to be unique among snakes, and allows these snakes to feed on prey that would be too large to consume whole. Jayne et al. (2002) argued that the highly kinetic jaws and needle-like teeth of snakes are poorly suited to generating large bite forces, which makes this feeding mechanism particularly surprising. However, as we noted above, it seems likely that some snakes can generate higher bite forces than we currently recognize. In alethinophidian snakes, several elements associated with the oral cavity—particularly the jaw joint, tongue, hyoid elements, and glottis—are organized differently from those in other vertebrates (Cundall et al. 2014; Fig. 14.10). In particular, the tongue and hyoid elements have shifted ventrally and posteriorly relative to those of other vertebrates. The glottis demarcates the functional beginning of the esophagus in snakes (Cundall et al. 2014). Therefore, Cundall et al. (2014) concluded that mandibular depression shortens the effective length of the oral cavity when snakes swallow large prey, and the upper jaws ratchet prey “almost directly into the esophagus.” During ingestion, a snake’s oral cavity changes shape dynamically, though slowly, as parts of the prey with different shapes move through the oral cavity and anterior esophagus (Cundall et al. 2014). Early studies noted that these changes in shape involve movement of musculoskeletal elements as well as extension and recoil

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Fig. 14.10 Organization of the floor of the anterior gut in a representative amniote tetrapod (a) and in a snake (b). Although considerable liberty has been taken with anatomy, in almost all tetrapods except snakes, the trunk-cervical boundary is marked by pectoral elements and skeletal connections (ribs and costal cartilages) between the dorsal and ventral axial components (vertebrae [not shown but in line with the braincase] and sternum). The cranial-cervical boundary is typically marked by the jaw joint, base of the tongue and hyoid, and the glottis. Yellow indicates presumed distribution of epithelial cells of endodermal origin lining the floor of the gut. Abbreviations: jj, jaw joint, and hence location of posterior end of mandible; md, anterior end of mandible; pg, pectoral girdle (reproduced from Cundall et al. 2014)

of soft tissues (e.g., Gans 1952, 1961, 1974; Gans and Oshima 1952). The esophagus and stomach must stretch laterally and in some cases longitudinally (e.g., Jackson et al. 2004). However, the functional properties of the soft tissues were quantified only recently. Among the most visible aspects of soft-tissue extension during feeding in snakes are stretching of tissues associated with the lower jaws. Close and Cundall (2014) recently found that in water snakes (Nerodia sipedon), intermandibular separation during ingestion reached over seven times its resting length, which is highly unusual among vertebrate tissues, and involved mainly stretching of the fibrous connective tissues between the scales of the lower jaw. In the epidermis, stretching flattened folds in the skin between the scales, and in the dermis stretching involved collagen realignment and extension of elastin deep in the dermis. Close and Cundall (2014) inferred from histological structure that dermal elastin contributed to passive recovery after stretching. As oral tissues stretch during ingestion of prey, several cranial muscles must not only accommodate the stretch, but maintain contractile function to complete the ingestion. Close et al. (2014) studied the changes in length and function of intermandibular muscles during feeding in snakes, and found that they become highly stretched, with sarcomere lengths more than doubling relative to their resting lengths, yet recover normal function. Such long extension pulls actin and myosin filaments apart beyond overlap, misaligns striations, and distorts the

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sarcoplasmic reticulum and triad positions (Close et al. 2014). Initial recovery must be passive, because sarcomeres get stretched beyond filament overlap, and probably involves the elastic protein titin; subsequent recovery involves active or passive shortening beyond resting lengths, to a point involving overlap of opposing actin filaments within a sarcomere, eventually followed by a return to resting length (Close et al. 2014). Close et al. (2014) found no apparent damage to sarcomeres during such stretching. The whole muscle stretched even more than the sarcomeres because of stretching in associated connective tissues and slippage of muscle fibers (Close et al. 2014). These recent studies of soft-tissue properties provide a foundation for additional research that could resolve structural and functional changes associated with the evolution and diversification of snakes, particularly the changes associated with the evolution of enlarged gapes. They have also shown that snakes are excellent model organisms for studying mechanisms of extreme tissue deformation without injury.

14.3.3.2

Postcranial Transport

Once ingested, a meal needs to be swallowed, i.e., transported from the anterior esophagus to the stomach. Swallowing has not yet been studied well in any snakes (Cundall and Greene 2000). Small prey may be transported exclusively by esophageal peristalsis, although peristalsis in snakes remains poorly known. However, postcranial axial bending movements produced by skeletal muscles appear to be important in helping push larger food items from the anterior esophagus along a substantial length of the body to the stomach (Kley and Brainerd 2002; Moon 2000b; Fig. 14.11). Thus, swallowing looks somewhat like a kind of inside-out locomotion, with some of the same epaxial muscles involved in locomotion contributing to internal force exertion for swallowing (Moon 2000b). In the colubrid snakes, Pituophis melanoleucus and Lampropeltis getula, axial bending patterns used during swallowing appear to vary from undulatory to accordion-like concertina bends, and the associated epaxial muscle activity appears more variable than during steady locomotion (Moon 2000b). Kley and Brainerd (2002) used X-ray videography to study axial bending movements in detail during postcranial swallowing in P. melanoleucus, and found that three out of four distinct phases of postcranial prey transport involved undulatory or concertina-like movements of the an