Physiology of Elasmobranch Fishes：Structure and Interaction with Environment [A] 978-0-12-801289-5

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PHYSIOLOGY OF ELASMOBRANCH FISHES: STRUCTURE AND INTERACTION WITH ENVIRONMENT

This is Volume 34A in the FISH PHYSIOLOGY series Edited by Anthony P. Farrell and Colin J. Brauner Honorary Editors: William S. Hoar and David J. Randall A complete list of books in this series appears at the end of the volume

PHYSIOLOGY OF ELASMOBRANCH FISHES: STRUCTURE AND INTERACTION WITH ENVIRONMENT

Edited by

ROBERT E. SHADWICK Department of Zoology The University of British Columbia Vancouver, British Columbia Canada

ANTHONY P. FARRELL Department of Zoology, and Faculty of Land and Food Systems The University of British Columbia Vancouver, British Columbia Canada

COLIN J. BRAUNER Department of Zoology The University of British Columbia Vancouver, British Columbia Canada

AMSTERDAM  BOSTON  HEIDELBERG  LONDON NEW YORK  OXFORD  PARIS  SAN DIEGO SAN FRANCISCO  SINGAPORE  SYDNEY  TOKYO Academic Press is an imprint of Elsevier

Academic Press is an imprint of Elsevier 125, London Wall, EC2Y 5AS. 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 225 Wyman Street, Waltham, MA 02451, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright r 2016 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-801289-5 ISSN: 1546-5098 British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress. For Information on all Academic Press publications visit our website at http://store.elsevier.com/ Typeset by MPS Limited, Chennai, India www.adi-mps.com

Publisher: Janice Audet Senior Acquisition Editor: Kristi A.S. Gomez Senior Editorial Project Manager: Pat Gonzalez Production Project Manager: Lucı´a Pe´rez Designer: Matthew Limbert

CONTENTS CONTENTS OF PHYSIOLOGY OF ELASMOBRANCH FISHES: INTERNAL PROCESSES, VOLUME 34B CONTRIBUTORS PREFACE LIST OF ABBREVIATIONS

1.

1. 2. 3. 4.

2. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10.

3. 1. 2.

ix xiii xv xix

Elasmobranchs and Their Extinct Relatives: Diversity, Relationships, and Adaptations Through Time Philippe Janvier and Alan Pradel Introduction Systematic and Phylogenetic Framework of Chondrichthyan Diversity Environments and Adaptations Conclusion

2 4 13 14

How Elasmobranchs Sense Their Environment Shaun P. Collin, Ryan M. Kempster and Kara E. Yopak Introduction The Visual System The Non-visual System The Auditory and Vestibular Systems The Electrosensory System The Lateral Line System Cutaneous Mechanoreception The Chemosensory Systems Sensory Input to the Central Nervous System in Elasmobranchs Perspectives on Future Directions

20 22 32 33 39 44 48 49 55 72

Elasmobranch Gill Structure Nicholas C. Wegner Introduction Overview of the Elasmobranch Gill v

102 102

vi

CONTENTS

3. 4. 5. 6. 7.

4.

1. 2. 3. 4. 5. 6. 7. 8.

5.

1. 2. 3. 4. 5.

6. 1. 2. 3. 4. 5. 6. 7. 8.

7. 1. 2. 3.

Evolution of the Gill: Elasmobranch Gill Structure in Relation to Other Fishes Elasmobranch Versus Teleost Ventilation Details of the Elasmobranch Gill Diversity in Elasmobranch Gill Dimensions and Morphology Conclusions

105 108 110 125 145

Functional Anatomy and Biomechanics of Feeding in Elasmobranchs Cheryl A.D. Wilga and Lara A. Ferry General Trophic Morphology Feeding Behaviors Biomechanical Models for Prey Capture Modulation of Muscle Activity Biomechanical Models for Prey Processing and Transport Biomechanics of Filter Feeding Biomechanics of Upper Jaw Protrusion Ecophysiological Patterns

154 164 167 174 176 177 178 180

Elasmobranch Muscle Structure and Mechanical Properties Scott G. Seamone and Douglas A. Syme Introduction Fiber Types Contractile Properties Summary Future Directions

190 192 202 212 214

Swimming Mechanics and Energetics of Elasmobranch Fishes George V. Lauder and Valentina Di Santo Introduction Elasmobranch Locomotor Diversity Elasmobranch Kinematics and Body Mechanics Hydrodynamics of Elasmobranch Locomotion The Remarkable Skin of Elasmobranchs and its Locomotor Function Energetics of Elasmobranch Locomotion Climate Change: Effects on Elasmobranch Locomotor Function Conclusions

220 221 222 228 233 235 239 244

Reproduction Strategies Cynthia A. Awruch Introduction Classification of Reproductive Modes in Elasmobranchs Mating Strategies and Parthenogenesis

256 257 272

vii

CONTENTS

4. 5. 6.

8. 1. 2. 3. 4. 5.

Classification of Reproductive Cycles in Elasmobranchs Endocrine Control of Reproductive Cycles in Elasmobranchs The Future

277 282 295

Field Studies of Elasmobranch Physiology Diego Bernal and Christopher G. Lowe Introduction Thermal Physiology Swimming Kinematics and Energetics A Case Field Study: Thresher Sharks Future Directions in Field Physiology

INDEX OTHER VOLUMES

312 316 347 359 364

379 IN THE

FISH PHYSIOLOGY SERIES

391

CONTENTS OF PHYSIOLOGY OF ELASMOBRANCH FISHES: INTERNAL PROCESSES, VOLUME 34B 1. 1. 2. 3. 4. 5.

6. 7.

2. 1. 2. 3. 4. 5. 6. 7.

Elasmobranch Cardiovascular System Richard W. Brill and N. Chin Lai Introduction Cardiovascular Function and Energetics Factors Controlling and Effecting Cardiovascular Function Signaling Mechanisms Effecting Blood Vessel Diameter The Action Potential and Excitation–Contraction (EC) Coupling in Elasmobranch Hearts: The Influences of Environmental, Biochemical, and Molecular Factors Practical Applications: Physiology in the Service of Elasmobranch Conservation Summary

2 3 24 37

48 54 57

Control of Breathing in Elasmobranchs William K. Milsom and Edwin (Ted) W. Taylor Introduction Ventilation: Efferent Motor Output to the Respiratory Muscles Central Respiratory Rhythm Generation: The Source of the Motor Output The Respiratory Pattern: The Conditional Nature of the Output Relationships Between Ventilation and Heartrate Afferent Input Conclusions

ix

84 85 91 94 103 108 115

x

CONTENTS

Oxygen and Carbon Dioxide Transport in Elasmobranchs Phillip R. Morrison, Kathleen M. Gilmour and Colin J. Brauner

3.

1. 2. 3. 4.

Introduction Blood-Oxygen Transport Transport and Elimination of Carbon Dioxide Conclusions and Perspectives

128 132 184 197

Organic Osmolytes in Elasmobranchs Paul H. Yancey

4. 1. 2. 3. 4. 5. 6.

Introduction Osmoconformers Versus Osmoregulators Properties of Organic Osmolytes Metabolism and Regulation Evolutionary Considerations Knowledge Gaps and Future Directions

222 224 233 256 263 264

Regulation of Ions, Acid–Base, and Nitrogenous Wastes in Elasmobranchs Patricia A. Wright and Chris M. Wood

5.

1. 2. 3. 4. 5.

Introduction Ionoregulation Acid–Base Balance Nitrogenous Wastes Concluding Remarks

280 280 298 310 327

Feeding and Digestion in Elasmobranchs: Tying Diet and Physiology Together Carol Bucking

6.

1. 2. 3. 4. 5. 6.

Introduction Feeding Habits of Elasmobranchs Elasmobranch Gastrointestinal Tract Anatomy Digestive Enzymes and Secretions Effects of Digestion on Homeostasis Future Perspectives

348 350 365 373 379 381

Metabolism of Elasmobranchs (Jaws II) J.S. Ballantyne

7. 1. 2. 3. 4. 5. 6.

Introduction Evolutionary Context Diet and Digestion Oxidative Metabolism Carbohydrate Metabolism Nitrogen Metabolism

396 398 399 404 407 411

xi

CONTENTS

7. 8. 9. 10.

8. 1. 2. 3. 4. 5. 6. 7. 8. 9.

INDEX

Lipid and Ketone Body Metabolism Vitamin Metabolism Xenobiotic Metabolism Conclusions and Perspectives

426 435 436 437

Endocrine Systems in Elasmobranchs W. Gary Anderson Introduction Pituitary Gland Corticosteroids and Catecholamines Gastro-Entero-Pancreatic Hormones The Heart as an Endocrine Gland The Kidney as an Endocrine Gland The Pineal Calcium Regulation Conclusions and Perspectives

458 459 472 484 497 502 505 506 508

531

CONTRIBUTORS The numbers in parentheses indicate the pages on which the authors’ contributions begin.

CYNTHIA A. AWRUCH (255), School of Biological Sciences, University of Tasmania, Tasmania, Australia; Centro Nacional Patago´nico (CENPAT) – CONICET, Puerto Madryn, Chubut, Argentina DIEGO BERNAL (311), Department of Biology, University of Massachusetts Dartmouth, Dartmouth, MA, USA SHAUN P. COLLIN (19), The School of Animal Biology and the Oceans Institute, The University of Western Australia, Crawley, Western Australia, Australia; The Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia LARA A. FERRY (153), School of Mathematical and Natural Sciences, Arizona State University, Phoenix, AZ, USA PHILIPPE JANVIER (1), Muse´um National d’Histoire Naturelle, UMR7207 du CNRS (Sorbonne Universite´s, UPMC), Paris, France RYAN M. KEMPSTER (19), The School of Animal Biology and the Oceans Institute, The University of Western Australia, Crawley, Western Australia, Australia GEORGE V. LAUDER (219), Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA CHRISTOPHER G. LOWE (311), Department of Biological Sciences, California State University, Long Beach, CA, USA ALAN PRADEL (1), Muse´um National d’Histoire Naturelle, UMR7207 du CNRS (Sorbonne Universite´s, UPMC), Paris, France

xiii

xiv

CONTRIBUTORS

VALENTINA DI SANTO (219), Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA SCOTT G. SEAMONE (189), Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada DOUGLAS A. SYME (189), Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada NICHOLAS C. WEGNER (101), NOAA Fisheries, Southwest Fisheries Science Center, La Jolla, CA, USA CHERYL A.D. WILGA (153), Department of Biological Sciences, University of Rhode Island, Kingston, RI, USA KARA E. YOPAK (19), The School of Animal Biology and the Oceans Institute, The University of Western Australia, Crawley, Western Australia, Australia

PREFACE The elasmobranch group consists of sharks, skates, and rays, which, along with their sister group, holocephalans, comprises the extant cartilaginous fishes of class Chondrichthyes. Elasmobranchs hold an important position in the evolutionary history of jawed vertebrates, with fossil evidence of ancestral forms dating back close to 400 million years. There are about 1000 living species of elasmobranchs, mostly marine, which all share distinctive features: skeletal elements formed of prismatic calcified cartilage, placoid dermal scales, teeth that are shed and replaced regularly, an osmoregulatory strategy to keep body fluids nearly iso-osmotic with the surrounding water, internal fertilization with many species bearing live young, and highly developed sensory systems including electroreception. Some also elevate their core body temperatures by retaining muscle heat via vascular heat exchangers. Because of their evolutionary significance and unusual physiology, elasmobranchs are of great interest to biologists in general and fish physiologists in particular. This two-part volume, Physiology of Elasmobranch Fishes, is modeled on a previous comprehensive treatment of this field published over 25 years ago, Physiology of Elasmobranch Fishes, edited by T. J. Shuttleworth1 in 1988. In the intervening time much has changed in terms of interest and breadth of research on elasmobranchs, public awareness of their importance in oceanic ecosystems, and decimation due to commercial fishing pressures. Over the past two decades research efforts and published works on elasmobranch physiology have greatly expanded and now include more sophisticated laboratory work, increased field measurements, a notable increase in the diversity of species studied, and a particular boom in lab and field-based studies of large pelagic sharks. Interestingly, virtually all experimental physiology studies of elasmobranchs have been conducted on wild-caught animals. There are no aquaculture

1

Shuttleworth, T. J. (1988). Physiology of Elasmobranch Fishes. Berlin: Springer-Verlag. xv

xvi

PREFACE

sources for research specimens, in contrast to the situation for physiologists who work with teleosts, as many of the teleosts are supplied from aquaculture stocks that have been subjected to various degrees of genetic manipulation in their domestication. The restriction to wild-caught elasmobranchs certainly makes physiological studies of elasmobranchs more difficult, but it is also unusual in the sense that the specimens studied are not influenced by captive breeding artifacts. However, routine laboratory investigations are still impractical because many elasmobranch species, which have relatively large body size, live in remote habitats and are continuous swimmers. Here we present a broad exploration of our current knowledge of elasmobranch physiology in a two-part volume. Aspects of elasmobranch structure and interactions with their environment are covered in volume 34A, while volume 34B expands on internal physiological processes. Both parts are fully integrated by cross-referencing between the various chapters, and they share a common index. Twenty-eight authors with appropriate expertise and active research programs in the field have contributed sixteen chapters. Each synthesizes the available data into a comprehensive review of the topic, while also comparing elasmobranchs to other groups of fishes and providing a perspective on future research problems and directions. Volume 34A begins with a well-illustrated description of the evolutionary history of cartilaginous fishes, which highlights relationships between elasmobranchs, holocephalans, and their ancestors. Chapter 2 follows with a very detailed review of the battery of sensory capabilities found in elasmobranchs, which includes the more unusual electric and magnetic senses. By examining species from different habitats, this chapter investigates how elasmobranchs use their sensory systems to sample their “sensoryscape” and how this influences their behavioral responses to environmental stimuli. The structure of elasmobranch gills is described and illustrated in striking detail in Chapter 3, wherein the diversity among elasmobranchs as well as important differences from other fish groups are highlighted. Chapter 4 presents a comprehensive review of the muscular and skeletal anatomy and the mechanics that support a range of feeding behaviors, from simple ancestral biting to more derived suction and filter feeding. Skeletal muscle structure and contractile properties are reviewed in Chapter 5, with an emphasis on how elasmobranch muscle (of which we know comparatively little) compares with muscle in other fishes, and how relatively large body size in sharks confounds such comparisons. In Chapter 6, elasmobranch locomotor diversity, hydrodynamics, and energetics are discussed in comparison with teleosts, and special structures such as the heterocercal tail and the denticled skin are highlighted. Looking to the potential impact of global ocean change, new evidence on temperature effects on locomotor performance is also presented. Chapter 7 presents a comprehensive review of the diverse range of elasmobranch strategies for reproduction, from oviparity to different forms of

PREFACE

xvii

viviparity, and a survey of modes of embryonic nutrition such as oophagy and intrauterine cannibalism. Finally, Chapter 8 explores the advantages of conducting physiological studies in the field, with descriptions of current technologies and examples of new findings. These innovative approaches are opening new opportunities to study larger species in their natural environment. Volume 34B begins with two chapters on the function and control of cardio–respiratory systems. Chapter 1 compares elasmobranch and teleost cardiovascular systems, with emphasis on neural, endocrine, and paracrine control features. This chapter also considers how various species might experience cardiovascular challenges associated with increased temperature and hypoxia in future oceans. Chapter 2 then describes the physiology of respiratory systems in elasmobranchs, with emphasis on the generation of respiratory rhythm, sensory inputs, motor output patterns, and the integration of control and synchrony of the cardio–respiratory systems. The physiology of oxygen and carbon dioxide transport in elasmobranchs is reviewed in Chapter 3, focusing on functional modifications of hemoglobin and carbonic anhydrase. In addition, adaptations for respiratory gas transport in conditions of exercise, hypoxia, salinity, temperature, and, in some species, regional heterothermy are reviewed. The next two chapters deal with systems to control ion and fluid balance, and highlight the unusual reliance on urea. Chapter 4 describes how marine elasmobranchs maintain osmotic balance by the use of organic osmolytes (mainly urea and methylamines), making them hypoionic osmoconformers, while euryhaline species have reduced osmolytes and function as hyperosmotic regulators. Specific mechanisms used by elasmobranchs to balance acid and base, ions, and nitrogenous wastes by the gill, kidney, gut, and rectal gland are detailed in Chapter 5, with specific comparisons among species inhabiting marine, freshwater, and intermediate salinity habitats. Chapter 6 links feeding ecology to physiology in elasmobranchs and includes a discussion of several analytical techniques used to determine diet composition for different feeding behaviors. The anatomy of the digestive tract is covered in detail, and digestive processes specific to the demands of different ecological niches occupied are reviewed. Chapter 7 reviews metabolic processes in elasmobranchs, clearly demonstrating that their metabolic organization and regulatory mechanisms are very much driven by the need to continuously synthesize and maintain large amounts of urea. This chapter also shows how studies of elasmobranchs can provide broader insight into the evolution of metabolism in the vertebrates. Chapter 8 completes the volume with a detailed and systematic review of endocrine systems in elasmobranchs, which emphasizes the importance of hormonal control in many aspects of their physiology. One unusual feature is the production of a corticosteroid unique to elasmobranchs in the interrenal gland. Although our current

xviii

PREFACE

knowledge of elasmobranch endocrinology is extensive, it has come from studies on but a few of the hundreds of species, which suggests that there is much more to learn in future research, not just in endocrinology, but in all aspects of the physiology of these fascinating fishes. The editors would like to thank Pat Gonzalez, Kristi Gomez, Lucı´a Pe´rez, and their production staff at Elsevier for guiding this project from its inception to final publication. We thank the anonymous reviewers who provided constructive comments on the original proposal for this volume and the numerous colleagues who acted as external peer reviewers of the chapter drafts. Finally we thank the team of elasmobranch experts who authored the important written contributions and also aided efforts with their patience and collegial cooperation over the past two years. Robert E. Shadwick Anthony P. Farrell Colin J. Brauner

LIST OF ABBREVIATIONS [Ca2+]i [O2]arterial [O2]venous [TAmm] DH’ DP DPO2 DV m a b b-NHE bEND b-LPH DHO DzH+ l lmax F Q_ 11-KA 11-KT 1a-OH-B 2,3-BPG 2,3-DPG 5-HT A

intracellular (i.e., cytoplasmic) free calcium concentration arterial blood oxygen content venous blood oxygen content plasma total ammonia content apparent enthalpy of oxygenation change in venous pressure difference in the partial pressure of oxygen between water and blood (mmHg) change in venous blood volume dynamic viscosity of the water a-adrenergic receptor b-adrenergic receptor b-adrenergic Na+/H+ exchanger b endorphin b-lipotrophic hormone enthalpy of heme-oxygenation Haldane coefficient ( 4F) wavelength wavelength of maximum absorbance Bohr coefficient (Dlog P50/DpH) cardiac output 11-ketoandrostenedione 11-ketosterone 1a-hydroxycorticosterone 2,3-bisphosphoglycerate 2,3-diphosphoglycerate 5-hydroxytryptamine respiratory surface area of the gills (cm2) xix

xx AA AADC ABA ABR AC ACE Ach ACTH ADP AEP Alam ALLN AMP Ang II ANP ARG ARGase ASL ASS ATP AVP AVT BADH BHB BHBDH BK BL/s BNP CA cAMP CaO2 CBG CCK CCO CFTR cGMP CGRP CICR Cl CNP CNS CO

LIST OF ABBREVIATIONS

arachidonic acid aromatic L-amino acid decarboxylase afferent branchial artery auditory brain stem recording adenylyl cyclase angiotensin converting enzyme acetylcholine adrenocorticotrophic hormone adenosine diphosphate auditory evoked potential mean bilateral surface area of a gill lamella (mm2) anterior lateral line nerve adenosine monophosphate angiotensin II atrial natriuretic peptide arginine arginase argininosuccinate lyase argininosuccinate synthetase adenosine triphosphate arginine vasopressin arginine vasotocin betaine aldehyde dehydrogenase b-hydroxybutyrate b-hydroxybutyrate dehydrogenase bradykinin body lengths per second brain natriuretic peptide carbonic anhydrase cyclic adenosine monophosphate arterial blood oxygen content corticosteroid binding globulin cholecystokinin cytochrome c oxidase cystic fibrosis transmembrane conductance regulator cyclic guanosine monophosphate calcitonin gene related peptide calcium induced calcium release chloride ion C-type natriuretic peptide central nervous system carbon monoxide

xxi

LIST OF ABBREVIATIONS

CO2 CO2 CoA COMT COX CPS CPT CR CRF CRG CRLR CRS CS CT CvO2 CVPN DA DAG DBH DC DHA DHT DIDS DOC DON DOPA DVN E2 EC ECF ECFV eNOS EOG EROD ETA and ETB FA FABP fH FSH GC GDH

carbon dioxide content of O2 coenzyme A catechol-O-methyltransferase cyclooxygenase carbamoyl phosphate synthase carnitine palmitoyl transferase calcitonin receptor corticotrophic releasing factor central rhythm generator calcitonin receptor-like receptor cardiorespiratory synchrony citrate synthase calcitonin venous blood oxygen content cardiac vagal preganglionic neurons dorsal aorta diacylalkylglycerol=alkyldiacylglcyerol dopamine-b-hydroxylase direct current docosahexaenoic acid dihydrotestosterone: 4,4-diisothiocyanostilbene-2,2-disulphonic exchange inhibitor) dissolved organic carbon dorsal octavolateralis nucleus dihydroxyphenylalanine dorsal motor nucleus of the vagus nerve 17b-estradiol excitation-contraction extracellular fluid extracellular fluid volume endothelial NO synthase electro-olfactography ethoxyresorufin-O-deethylase endothelin receptors subtypes fatty acid fatty acid binding protein heart rate follicle stimulating hormone guanylyl cyclase glutamate dehydrogenase

acid

(anion

xxii GEP GFR GH GHRH GI GIT GLP GLUT GnRH GPC GPI linkage GPS GR GRP GS GT GTH GTP GULO H H+ H 2S Hb HCl HCO3 Hct HDL HEA HETE HIS HKA HPETE HPG HRV Hz ICFV IGF IHC IHP IMP iNOS IP3

LIST OF ABBREVIATIONS

gastro-entero-pancreatic glomerular filtration rate growth hormone growth hormone releasing hormone gastrointestinal gastrointestinal tract glucagon-like peptide glucose transporter gonadotropin releasing hormone glycerophosphorylcholine glycosylphosphatidylinositol linkage global Positioning System glucocorticoid receptor gastrin releasing peptide glutamine synthetase gonadotropins gonadotrophic hormone guanosine triphosphate gulono gamma lactone oxidase height of a lamella hydrogen ion (i.e., proton) hydrogen sulfide hemoglobin hydrochloric acid bicarbonate ion the percentage of red blood cells in blood high density lipoprotein high environmental ammonia hydroxyeicosatetraenoic acid hepatosomatic index H+, K+-ATPase hydroperoxyeicosatetraenoic acid hypothalamus–pituitary–gonadal axis heart rate variability hertz intracellular fluid volume insulin-like growth factor immunohistochemistry inositol hexaphosphate inosine monophosphate inducible nitric oxide synthase inositol triphosphate

LIST OF ABBREVIATIONS

IPP IQL IRD IRI JGA K KKS Km L-Arg LDH LDL Lfil LH LT LWS M MAO MCHC MCR MCT _ 2 MO MON MR MRC mRNA MSH MWS N N/O2 Na+ NAD+ NADH NADP NADPH NAG NANC NCX NEC NEFA nH

xxiii

inositol pentaphosphate inner quadratomandibular ligament inner ring deiodinase index of relative importance juxtaglomerular apparatus Krogh coefficient (mgO2 mm cm 2 mmHg 1 min 1) kallikrein kinin system Michaelis constant L-arginine lactate dehydrogenase low density lipoprotein total length of all the gill filaments (cm) luteinizing hormone leukotriene long wavelength sensitive molar monoamine oxidase mean corpuscular hemoglobin concentration melanocortin receptor monocarboxylate transporter O2 consumption rate medial octavolateralis nucleus mineralocorticoid receptor mitochondrion-rich cell messenger RNA melanocyte stimulating hormone medium wavelength sensitive newtons nitrogen quotient sodium ion nicotinamide adenine dinucleotide (oxidized form) nicotinamide adenine dinucleotide (reduced form) nicotinamide adenine dinucleotide phosphate (oxidized form) nicotinamide adenine dinucleotide phosphate (reduced form) N-acetyl glutamate nonadrenergic noncholinergic Na+-Ca2+ exchanger neuroepithelial cell nonesterified fatty acid Hill’s cooperativity coefficient at 50% Hb-O2 saturation

xxiv NHE NIL NKA NKCC nlam nNOS NO NOS NOX NPR NPs NPY NTP nV O2 OBs OFT OMZ ORD ORNs Osm Osm/kg OTC OUC P4 P50 PACAP PaCO2 PaO2 PC PC PCO2 Pcrit PEPCK PFK pGC PGI2 Pgs pHa pHe pHi

LIST OF ABBREVIATIONS

Na+/H+ exchanger neurointermediate lobe Na+, K+-ATPase Na/K/2Cl cotransporter number of lamellae per unit length on one side of a filament (=lamellar frequency) (mm 1) brain or neuronal NOS nitric oxide nitric oxide synthase NAD(P)H oxidases natriuretic peptide receptor natriuretic peptides neuropeptide Y nucleoside triphosphates nanovolt oxygen olfactory bulbs optimal foraging theory oxygen minimum zone outer ring deiodinase olfactory receptor neurons osmolarity osmolality ornithine transcarbamoylase ornithine urea cycle progesterone partial pressure at which Hb is 50% saturated pituitary adenylate cyclase activating peptide partial pressure of CO2 in arterial blood partial pressure of O2 in arterial blood pyruvate carboxylase proconvertase partial pressure of CO2 critical oxygen level phosphoenolpyruvate carboxykinase phosphofructokinase guanylate cyclase-linked receptors prostacyclin prostaglandin arterial blood pH extracellular pH (i.e., blood plasma pH) intracellular pH

LIST OF ABBREVIATIONS

PI PiO2 PI-PLC PK PL PL-A PLB PLLN PML PMV PNMT PO2 POMC PP PPC PPD PPi PRL PTH PTHrP pTRG PTS PUFA PvO2 PwO2 PYY Q10 QFASA R RAS RBCs RGC Rh RH Rhp2 RM ROS RPD RRG RVD RVI

xxv

pars intermedia inspired oxygen partial pressure phosphatidylinositol phospholipase-C pyruvate kinase placental lacotogen phospholipase A phospholamban posterior lateral line nerve palatoquadrate-mandibular connective tissue sheath partial molal volume phenylethanolamine-N-methyl transferase partial pressure of O2 pro-opiomelanocortin pancreatic polypeptide pericardioperitoneal proximal pars distalis pyrophosphate prolactin parathyroid hormone parathyroid hormone related protein para-trigeminal respiratory group proximal tubular segment polyunsaturated fatty acids partial pressure of O2 in venous blood partial pressure of O2 in water peptide YY relative change for a 101 C increase in temperature (temperature coefficient) quantitative fatty acid signature analysis resistance of the gills renin angiotensin system red blood cells retinal ganglion cell rhesus medium wavelength sensitive visual pigment rhesus protein 2 red muscle reactive oxygen species rostral pars distalis respiratory rhythm generation regulatory volume decrease regulatory volume increase

xxvi RVMN RYR sAC SCA SDA SERCA sGC SGLT ShUT SIA SL SNGFR SNP spl SR SR-RR SST StAR strut SV SWS T t T3 T3 T4 T4 TA TAG TBX TEP TG TH THs TMA TMAO TMAOX TR TRH TSH UBB Ucrit

LIST OF ABBREVIATIONS

respiratory vagal motor neurons ryanodine receptor soluble adenylyl cyclase stomach content analysis specific dynamic action sarco/endoplasmic reticulum Ca2+-ATPase soluble guanylyl cyclase sodium-linked glucose transporter shark urea transporter stable isotope analysis somatolactin single nephron glomerular filtration rate sodium nitroprusside splanchnic nerve sarcoplasmic reticulum sarcoplasmic reticulum ryanodine receptor somatostatin steroidogenic acute regulatory protein stingray urea transporter spiral valve short wavelength sensitive testosterone diffusion distance (mm) triiodothyronine triiodo-L-thyronine thyroxine tetraiodothyronine titratable acidity triacylglycerol thromboxane transepithelial potential thyroglobulin tyrosine hydroxylase thyroid hormones trimethylamine trimethylamine-N-oxide trimethylamine-N-oxide oxidase thyroid receptor thyroid releasing hormone thyroid stimulating hormone ultimobranchial bodies critical or maximal prolonged swimming velocity

LIST OF ABBREVIATIONS

UFR UI UII UT UV VHA VIP VLDL Vmax VNP VPD Vtg W wrc

urine flow rate urotensin I urotensin II urea transporter ultraviolet V-type H+-ATPase vasoactive intestinal (poly)peptide very low density lipoprotein maximal velocity of muscle shortening ventricular natriuretic peptide ventral pars distalis vitellogenin the width or thickness of a lamella white rami communicans

xxvii

1 ELASMOBRANCHS AND THEIR EXTINCT RELATIVES: DIVERSITY, RELATIONSHIPS, AND ADAPTATIONS THROUGH TIME PHILIPPE JANVIER ALAN PRADEL

1. Introduction 2. Systematic and Phylogenetic Framework of Chondrichthyan Diversity 2.1. Names, Taxa, and Characters 2.2. Chondrichthyan Diversity and Interrelationships 3. Environments and Adaptations 4. Conclusion

Current views about chondrichthyan phylogeny and systematics are briefly reviewed, with particular reference to the living and fossil taxa that are, or have been, once referred to as “elasmobranchs.” Recent reviews of early fossil chondrichthyans suggest that the last common ancestor of the living elasmobranchs and holocephalans probably lived by the end of the Devonian period, about 370–380 Myr ago, but a number of Paleozoic, shark-like chondrichthyans are currently regarded as stem chondrichthyans that diverged before the last common ancestor of all living taxa. Stem holocephalans display an amazing morphological diversity that reflects adaptations to very diverse benthic habitats. By contrast, both stem elasmobranchs and stem chondrichthyans are generally shark-like and were probably adapted to a pelagic mode of life. The earliest evidence for tessellated prismatic calcified cartilage, the “signature” of euchondrichthyans (i.e., all chondrichthyans which possess tessellated calcified prismatic cartilage), is about 400 Myr old, but scales and teeth tentatively assigned to chondrichthyans have been recorded from earlier periods. The “acanthodians,” a paraphyletic ensemble of Paleozoic fishes known since about 445 Myr are currently regarded as possible stem chondrichthyans that diverged before the rise of euchondrichthyans. 1 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00001-8

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1. INTRODUCTION Living elasmobranchs (in current sense) include sharks (squalomorphs and galeomorphs) and batomorphs (sawfishes, rays, skates, and torpedoes), and are the sister group of holocephalans (chimaeroids). Elasmobranchs and holocephalans are gathered into a higher group, the chondrichthyans (cartilaginous fishes). The idea that elasmobranchs and even all chondrichthyans are “primitive” jawed vertebrates (gnathostomes) stems from the conception of vertebrate systematics and evolution that progressively arose in the second half of the nineteenth century. The lack of an extensive bony skeleton in chondrichthyans was regarded as “primitive” because it is also the condition observed in living cyclostomes (hagfishes and lampreys), whose lack of jaws also suggested an earlier divergence in vertebrate history. Other arguments in favor of the “primitiveness” of elasmobranchs were based on their anatomy, notably the classical resemblance and presumed serial homology of their mandibular and hyoid arches with the series of the gill arches, already noticed by early anatomists (e.g., Owen, 1866), and later supported by the discovery of early, fossil shark-like elasmobranchs (Dean, 1909). The reputedly “primitive” anatomy of elasmobranchs has also justified extensive studies of their physiology, with the aim of reconstructing the hypothetical phenotypic condition for the last common ancestor of all gnathostomes. Ultimately, all these data were expected to help our understanding of the adaptive context of the evolutionary processes that has subsequently led to the rise of bony fishes (osteichthyans), including their limbed members, the tetrapods (terrestrial vertebrates). However, as the knowledge of living elasmobranch biology was accumulating, paleontologists provided an increasingly large assembly of anatomical data on various extinct Paleozoic jawed and jawless fishes, which revolutionized the interpretation of character distributions (Janvier 1996, 2015; Brazeau and Friedman, 2015). Notably, they showed that bone was largely present in both the dermal skeleton and endoskeleton of armored jawless fishes, or “ostracoderms,” thereby suggesting that bone preceded the rise of jaws long before the divergence of cartilaginous fishes. Whence, then, the chondrichthyans? Among early vertebrate paleontologists, Stensio¨ (1969) proposed a surprising theory about the polyphyletic origin of chondrichthyans, in which elasmobranchs, rays, and holocephalans derived independently from three groups of placoderms (an ensemble of Paleozoic, armored jawed fishes) by progressive loss of their ability to produce endoskeletal bone and breakdown of their dermal armor (suggested by the fact that the scales of the earliest chondrichthyans were not placoid, but possessed a growing bony base bearing many separate odontodes). Stensio¨’s view was

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obviously based on some striking anatomical resemblances between the shark’s braincase to that of certain placoderms (the arthrodires), and by some superficial, convergent overall morphologies shared by rays and holocephalans with other groups of placoderms (the rhenanids and ptyctodonts, respectively). This theory is now dismissed, but provided interesting insights into the possibility that the lack of bone in chondrichthyans could be a derived condition. Placoderms are currently regarded as a paraphyletic array of stem jawed vertebrates that have successively diverged before the last common ancestor of chondrichthyans and osteichthyans (Brazeau and Friedman, 2015). Chondrichthyans, in turn, are currently thought to be most closely related to some of the somewhat shark-like Paleozoic fishes, referred to as “acanthodians,” whose phylogenetic position has been long erratic (Brazeau, 2009; Brazeau and Friedman, 2015), although they were already viewed as stem chondrichthyans by Goodrich (1909). Most of what we know about fossil chondrichthyans is based on isolated teeth or fin spines, and such remains, albeit poorly informative, nevertheless document relatively well the history of the groups that still have extant relatives and possess closely similar elements of the dermal skeleton. However, the elucidation of the relationships of the major extinct chondrichthyan taxa essentially rests on a small number of specimens (generally braincases, but sometimes articulated skeletons) preserved in three dimensions thanks to the thin layer of prismatic calcified cartilage that lines their surface. Such exceptional preservations are particularly welcome for reconstructing the internal anatomy of the braincase in stem chondrichthyans; that is, chondrichthyans that are neither elasmobranchs, nor holocephalans, but already posses prismatic calcified cartilage, the “signature” of the group, and are gathered with the latter into a group called euchondrichthyans (in order to distinguish them from other, possible stem chondrichthyans that do not possess this unique type of hard tissue, such as “acanthodians”) (Pradel et al., 2014). Such material, which can now be studied by nondestructive techniques of X-ray computed microtomography, provides invaluable information about the anatomy and relationships of these early forms and may help our understanding of what the last common ancestor of chondrichthyans and osteichthyans could have looked like, notably by revealing uniquely derived characters shared by the two groups, but which have been subsequently lost or strongly modified in either of them. Skeletal characters sometimes provide information that is indirectly useful to physiologists, such as features linked to particular functions of the labyrinth (e.g., low-frequency phonoreception; Maisey and Lane, 2010). However, fossil chondrichthyans may also provide information about certain soft tissues (e.g., muscles, blood vessels, kidneys, brain, coloration patterns; Dean, 1909;

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Zangerl, 1981; Maisey, 1989; Grogan and Lund, 2000; Pradel et al., 2009) that are exceptionally preserved under certain environmental conditions and as an effect of bacterially induced mineralization. Such soft-tissue data, long regarded as trivial by paleontologists, can now be studied in great detail, thereby allowing further inferences about the biology of these fossil organisms. The goal of this introduction is to provide physiologists with a systematic framework against which functional inferences may be tested in order to enlighten the evolutionary history of the interactions of chondrichthyans with the environments throughout time (remarkable reconstructions of the early chondrichthyans and their environment can be found in a semi-popular book by Cuny and Beneteau, 2013).

2. SYSTEMATIC AND PHYLOGENETIC FRAMEWORK OF CHONDRICHTHYAN DIVERSITY 2.1. Names, Taxa, and Characters The name Elasmobranchii (elasmobranchs) was erected by Bonaparte (1838) for an ensemble of living fishes that in fact included the “Selacha” (sharks and rays) and the “Holocephala” (chimaeras). Bonaparte’s “Elasmobranchii” was thus identical in contents to Huxley’s (1880) “Chondrichthyes” (chondrichthyans), which is currently widely used because it allowed the inclusion of a number of shark-like fossil groups whose affinities to either modern “sharks” or modern chimaeras were obscure (see review in Maisey, 2012). Chondrichthyan, elasmobranch, and holocephalan monophyly is currently well corroborated by phenotypic and phylogenomic data (Maisey et al., 2004; Heinicke et al., 2009). When dealing with phylogenies and classifications that include fossil taxa, it is necessary to define clearly the contents of the taxa that are characterized by unique features (autapomorphies). Therefore, the notions of total-, stem-, and crown group are important to define the degree of generality of the characters and avoid referring a member of a stem group to a crown group because of overall resemblance, as it has often happened for some Paleozoic “sharks” (for the definition of the notion of total-, stem- and crown-groups, see Janvier, 2007). Current chondrichthyan phylogenies are relatively well corroborated, in particular for the crown groups of elasmobranchs and holocephalans (i.e., the last common ancestor of a group and all its living and fossil descendants). This concerns essentially Cenozoic and Mesozoic taxa, but a number of Paleozoic taxa regarded as stem elasmobranchs or stem holocephalans still remain of debated relationships. In addition, some Paleozoic taxa are now quite clearly identified as stem chondrichthyans

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(Pradel et al., 2011, 2014; Maisey et al., 2014), but the last common ancestor to crown chondrichthyans is regarded as late Devonian (about 370 Myr) in age, on the basis of the earliest evidence for stem holocephalans. All chondrichthyans that possess at least tessellated prismatic calcified cartilage, and possibly pelvic claspers articulated with the pelvic fins, are gathered into the euchondrichthyans, a clade within the total-group chondrichthyans, which may also include “acanthodians” (see Section 2.2.6, Fig. 1.3).

2.2. Chondrichthyan Diversity and Interrelationships 2.2.1. Elasmobranchs The elasmobranch crown group, or neoselachians, comprises squalomorphs, galeomorphs, and batomorphs. Squalomorphs have been once regarded as paraphyletic, with batomorphs being most closely related to particular squalomorph groups, the pristiophoriforms and squatiniforms, forming with them the clade Hypnosqualea. This morphology-based theory of relationships (“hypnosqualea hypothesis”; Shirai, 1996) is currently refuted by molecular data, which, in contrast, strongly suggest an early divergence of modern selachians (Fig. 1.1; Maisey et al., 2004; Heinicke et al., 2009). Squalomorphs and galeomorphs are thus currently regarded as forming a clade, although the interrelationships of its various component clades are still debated. The elasmobranch crown group contains a large number of fossil taxa that can be regarded as sister to extant ones, often on the basis of tooth morphology, but sometimes thanks to articulated skeletons (Maisey et al., 2004; Cappetta, 1997). Thanks to these generally reliable fossil data, it is possible to provide a minimum age for most living lineages back to the Jurassic or Cretaceous (66–200 Myr ago) (Maisey, 2012), although some may show important “ghost lineages,” that is, lineages whose relationships entails deeper divergences, despite the absence of fossils (Fig. 1.1). However, a number of fossil elasmobranch taxa cannot be clearly proved to belong to the crown group, despite their sometimes squalomorph, galeomorph or batomorph-like overall aspect, and are thus regarded as stem-group elasmobranchs. Such is the case of the “synechodontiforms” (a probably paraphyletic group; Fig. 1.1), and especially the hybodontiforms (Fig. 1.1), a large group of shark-like elasmobranchs that lived from the early Carboniferous (e.g., Tristychius) to the late Cretaceous (360–65 Myr ago). All these stem elasmobranchs constitute, with the crown-group, the totalgroup elasmobranchs, or euselachians (Fig. 1.1).

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Figure 1.1. Intrarelationships of the total-group elasmobranchs (Euselachii; right) and distribution of the major taxa through time. Paleozoic in white, Mesozoic in light gray, Cenozoic in dark gray. Limits between geological periods are in million years (Myr). Geological periods: Cam, Cambrian; Carb, Carboniferous; Cen, Cenozoic; Cret, Cretaceous; Dev, Devonian; Jur, Jurassic; Ord, Ordovician; Perm, Permian; Sil, Silurian; Tr, Triassic. denotes extinct taxa. Adapted from Janvier (2007). Pattern of relationships adapted from Maisey et al. (2004) and Heinicke et al. (2009). Major nodes: 1, euselachians; 2, total-group neoselachians; 3, crown-group neoselachians; 4, squalomorphs; 5, galeomorphs.

2.2.2. Holocephalans Crown-group holocephalans (Chimaeroidei) comprise only three extant clades, the callorhinchids, chimaerids, and rhinochimaerids, the latter two being sister groups (Didier, 2004; Heinicke et al., 2009; Fig. 1.2). However

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Figure 1.2. Intrarelationships of the total-group holocephalans (Euchondrocephali; right) and distribution of the major taxa through time. Same time scale as in Fig. 1.1. denotes extinct taxa. Adapted from Janvier (2007). Pattern of relationships adapted from Didier (2004) and Heinicke et al. (2009) for the chimaeroids, and from Janvier (2007) and Pradel et al. (2011) for the stem euchondrocephalans. Major nodes: 1, total-group euchondrocephalans; 2, crowngroup euchondrocephalans (chimaeroids).

they are characterized by a large number of unique soft-tissue characters that are unfortunately irrelevant to the identification of fossil members of these clades, which are essentially documented by isolated tooth plates. These nevertheless allow tracing callorhinchids back to the early Jurassic, the chimaerids to the Cretaceous, and rhinochimaerids to the Triassic (Stahl, 1999; Fig. 1.2). Articulated fossil chimaeroids are extremely rare but judging from the morphology of most Mesozoic isolated tooth plates, they were

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probably not very different from living forms. Only the early Jurassic Squaloraja and Myriacanthus, which possessed a very long frontal clasper, probably fall outside the crown group. In addition to these chimaeroid-like Mesozoic taxa, holocephalans also comprise a very diverse stem group of essentially Paleozoic clades whose relationships are still unclear, but which displays at least some characters (mostly concerning tooth histology) that are shared with chimaeroids and never occur in the euselachians. These stem holocephalans have been gathered under the name “Euchondrocephali,” an obviously paraphyletic taxon, but paleontologists still use it by including crown-group chimaeroids in it (Grogan and Lund 2004). Therefore, euchondrocephalans are in fact the total-group holocephalans. Many of these stem holocephalans have also been long referred to as “bradyodonts,” because of their supposedly slow tooth replacement, which is considered as foreshadowing the large tooth plates of chimaeroids. “Bradyodonts” have long been known mostly by isolated, crushing teeth or tooth plates made of tubular dentine, whose structure recalls that of modern chimaeroids tooth plates. The discovery of spectacular, articulated specimens in a few Carboniferous (330–300 Myrold) fossil sites has revealed the amazing morphological diversity of these forms (Fig. 1.2). Many of them were gurnard-like in shape, and probably benthic, but their heads bore a large number of spines or appendages that probably served as claspers during mating. Other stem holocephalans, such as echinochimaerids (Fig. 1.2), were more chimaeroid-like in appearance, and iniopterygians (Fig. 1.2), although showing peculiar adaptations of their paired fins, clearly possessed a rather chimaeroid-like braincase structure (Pradel et al., 2009; Pradel, 2010). Two groups are currently still regarded as stem holocephalans, the petalodontids and eugeneodontids, although their teeth do not clearly show the characteristic chimaeroid-like histology. The former are stout, possibly reef dwelling fishes (including the only known examples of deep-bodied chondrichthyans), whereas the latter are huge, shark-like fishes, whose teeth were relatively small, except for their peculiar, saw-like, symphysial tooth series. In Permian times (300–250 Myr ago), eugeneodontids could have competed in size with the largest extant sharks, but recent findings suggest that their autodiastylic jaw suspension was quite comparable to that of many other stem holocephalans, thereby foreshadowing that of modern chimaeroids (Ramsay et al., 2015). 2.2.3. Chondrichthyan Crown Group Considering the taxa currently included in these two chondrichthyan total groups (euselachians and euchondrocephalans), the last common ancestor of the chondrichthyan crown group can be dated, on the basis of fossil data from the early Carboniferous (330 Myr) by the earliest

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euselachians or the late Devonian (380 Myr), by the earliest euchondrocephalans. These dates are much younger that the molecular-clock based dates suggested by Heinicke et al. (2009); that is, middle Devonian for the neoselachians alone, but would agree with the paleontology-based dates for the chimaeroids (Triassic). However, this molecular-clock dating would put the last common ancestor to crown group chondrichthyans in the mid Ordovician, about 470 Myr ago. Paleontological data suggest an elasmobranchs-holocephalan divergence in the late Devonian (about 380 Myr ago), and some stem elasmobranchs may have been documented at that time by essentially isolated teeth (Ginter et al., 2010; Pradel et al., 2011). 2.2.4. Chondrichthyan Stem Group A number of Paleozoic chondrichthyan taxa either do not share the uniquely derived characters of the chondrichthyan crown group, or are represented by such a poorly informative material (isolated teeth, scales, or spines) that their precise affinities are difficult to decide. However, the combination of these tooth-based data with those provided by exceptional three-dimensionally preserved endoskeletal data suggests that they can reasonably be regarded as stem chondrichthyans (or stem euchondrichthyans); that is, they diverged before the last common ancestor of euselachians and euchondrocephalans (Fig. 1.3; Ginter et al., 2010; Pradel et al., 2011, 2014). These include the iconic Cladoselache (Fig. 1.3) and its close relatives, the symmoriiforms (Stethacanthus, Damocles, Ozarcus, Cobelodus, Akmonistion, Kawichthys; some of which were once regarded as stem euchondrocephalans; Fig. 1.3), and the xenacanthiforms (Xenacanthus, Orthacanthus; Fig. 1.3), and ctenacanthiforms (Cladodoides, Tamiobatis; Fig. 1.3), both classically regarded as stem elasmobranchs. Also, among the stem chondrichthyans are some lower Devonian taxa (400 Myr-old), Doliodus (Miller et al., 2003; Maisey et al., 2009; Fig. 1.3) and Pucapampella (Maisey, 2001; Janvier and Maisey, 2010; Fig. 1.3), the earliest known chondrichthyans in which some endoskeletal anatomy is preserved. Doliodus clearly displays a chondrichthyan-like cranial anatomy, despite its very short prechordal region, and it possessed pectoral fin spines, like “acanthodians” (see Section 2.2.6), and may have been closely similar to the slightly younger Antarctilamna (Young, 1982). However, Pucapampella displays a very odd cranial anatomy, with a complete ventral fissure posterior to the hypophysis and well-developed basitrabecular process that recalls osteichthyan braincase anatomy (Maisey, 2001; Janvier and Maisey, 2010). Moreover, the teeth of Pucapampella are directly attached onto the palatoquadrate and Meckelian cartilage, a character almost unknown in other chondrichthyans, except perhaps in chimaeroids. Other possible stem chondrichthyans, such as the Devonian-Carboniferous “phoebodontids,” are represented by either

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Figure 1.3. Intrarelationships of the total-group chondrichthyans (including euchondrichthyans, and assuming that acanthodians are possible stem chondrichthyans), and distribution of the major taxa through time. Same time scale as in Fig. 1.1. denotes extinct taxa. Adapted from Janvier (2007). Right: Pattern of relationships based on neurocranial characters (Pradel et al., 2011). Left: Pattern of relationships based on tooth characters (Ginter et al., 2010; Pucapampella and Doliodus added, based on Brazeau and Friedman’s (2015) topology). Major nodes: 1, total-group chondrichthyans; 2 total-group euchondrichthyans; 3, “cladodont sharks” (Cladodontomorpha); 4, crown-group euchondrichthyans.

poorly informative endoskeletal material (Thrinacoselache), or isolated teeth (Phoebodus, and possibly Leonodus, the earliest known chondrichthyan-like teeth). Among the most surprising data provided by Ozarcus, the best preserved of these stem chondrichthyans, is that the branchial apparatus was organized in a manner that was previously regarded as unique to osteichthyans (Pradel et al., 2014). An extensive character analysis based on the best preserved Paleozoic chondrichthyan braincases has yielded a tree, in which most Paleozoic taxa

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that were long regarded as either stem elasmobranchs or stem holocephalans now appear as a sister clade of the crown-group chondrichthyans (Fig. 1.3, right side; Pradel et al., 2011). Pucapampella and Doliodus, generally regarded as the most plesiomorphic total-group euchondrichthyans (Brazeau and Friedman, 2015), appear here at the base of this clade (and this might be an artifact due to the large number of plesiomorphic characters shared by these two taxa and the other Paleozoic taxa considered in the analysis), but most other taxa of this clade (i.e., ctenacanthiforms, cladoselachids, and symmoriiforms) correspond exactly to the group referred to as “cladodont sharks,” or cladodontomorphs, on the basis of tooth morphology (Ginter et al., 2010). “Cladodont sharks” are characterized by a large conical central cusp, two or more lateral cusps, and diskshaped base. However, this braincase-based tree shows xenacanthiforms as nested within the cladodontomorphs, despite their characteristic “diplodont” teeth with two large, diverging lateral cups. By contrast, the tree of Ginter et al. (2010) (Fig. 1.3, left side) resolves xenacanthiforms as the sistergroup of cladodontomorphs+crown-group chondrichthyans. Zangerl’s (1981) suggested that “diplodont” teeth were derived from the “cladodont” condition, with the tricuspid phoebodontid teeth possibly representing an intermediate condition, but Ginter et al. (2010) pointed out that the earliest known chondrichthyan teeth (e.g., Leonodus and Doliodus) rather resemble the “diplodont” type, although the cranial anatomy of Doliodus is clearly different from that of xenacanthiforms. Only Protodus, one of the earliest known chondrichthyan teeth, would agree with the “cladodont” type. Based on the relative age of the first occurrence of these different tooth types, Ginter et al. (2010) proposed that the plesiomorphic condition for chondrichthyan teeth was diplodont and that the tricuspid phoebodont tooth type arose by enlargement of the small central cusp. This tooth type may have represented a general condition, from which was derived the cladodont type by further enlargement of the central cusp, and the secondary xenacanthiform diplodonty by reduction and finally loss of the central cusp. Janvier (1996, p. 150) also suggested that the diplodont tooth type could be plesiomorphic because it strikingly resembles the often bicuspid shape of the pharyngeal denticles of many early osteichthyans. “Cladodont sharks” were thought to disappear by the end of the Permian, but the discovery of quite typical cladodont teeth in a Lower Cretaceous (120 Myr) deep-sea environment suggests that they may have survived long after the Permian–Triassic mass extinction (252 Myr ago) (Guinot et al., 2013). Stem-group and crown-group chondrichthyans are currently gathered in the total group now referred to as “euchondrichthyans” (Fig. 1.3), which is characterized by only two characteristics: the tessellated calcification of the

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endoskeleton (clearly evidenced in the 400 Myr-old Doliodus and Pucapampella), and possibly the pelvic claspers attached indirectly to the pelvic girdle (Maisey et al., 2014). 2.2.5. Putative Early Stem Chondrichthyans The earliest Paleozoic chondrichthyans that display evidence for at least tessellated prismatic calcified cartilage are about 400 Myr old and found in clearly marine, shallow water environments. However, isolated skin denticles and teeth have been described from much earlier rocks and tentatively referred to as chondrichthyans because of their resemblance to elements retrieved from younger complete fossil chondrichthyans. Some of these Early Devonian and Late Silurian (410–430 Myr-old) remains, such as Leonodus, Elegestolepis, Tuvalepis, or Polymerolepis (Karatajute-Talimaa, 1998) are indeed likely to be derived from some stem chondrichthyans, but earlier ones, dating from the Early Silurian to Middle Ordovician (440–470 Myr), display less obvious chondrichthyan characteristics. Such is the case, for example, in the mongolepids (Mongolepis, Sodolepis, Teslepis), known from minute scales with a massive bony base and a crown composed by numerous “odontodes” made of atubular dentine (see review in KaratajuteTalimaa, 1998). These isolated scales are sometimes associated with isolated fin spines (e.g., the Silurian sinacanthid fin spines; Sansom et al., 2005), whose histology recalls that of certain, younger, Devonian chondrichthyans. So far, none of these presumed chondrichthyan scales has ever been found in association with typical, tessellated prismatic calcified cartilage, and their attribution to euchondrichthyans rests essentially on their small size and remote resemblance to younger Paleozoic forms known by articulated specimens. Therefore, it is often said that the earliest evidence for chondrichthyans is in the Middle Ordovician (about 470 Myr ago), but this remains to be confirmed by articulated specimens. 2.2.6. Acanthodians as Stem Chondrichthyans? Acanthodians have been long regarded as a monophyletic group because they are the only gnathostomes that possess bony fin spines anterior to all paired and unpaired fins (e.g., Denison, 1979). In addition, most of them possess an apparently unique type of scale structure, with a bony base and a crown made of overgrowing odontodes. However, their relationships have also been long a matter of debate, essentially because their endoskeleton is poorly documented and provides little information about the key cranial characters that are classically used to reconstruct gnathostome relationships. Their shark-like external morphology has long suggested relationships to chondrichthyans (Goodrich, 1909), but some display braincase characters that also suggest relationships to osteichthyans (Davis et al., 2012). Since the

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discovery of large pectoral fin spines in the stem euchondrichthyan Doliodus, recent research on acanthodians now suggests that they form a paraphyletic array of stem chondrichthyans (Brazeau, 2009; Brazeau and Friedman, 2015). However, they all diverged before the last common ancestor of euchondrichthyans; that is, before the appearance of tessellated prismatic calcified cartilage. Actually, the endoskeleton of acanthodians only consists of either perichondral bone or globular calcified cartilage. Yet some acanthodians possess tooth whorls and scales that strikingly recall those of early euchondrichthyans (Burrow and Rudkin, 2014). The current challenge of the research on acanthodian relationships is the discovery of more, threedimensionally preserved cranial material.

3. ENVIRONMENTS AND ADAPTATIONS Fossils suggest that most of the earliest euchondrichthyans lived in relatively warm, marine shallow waters. Most of them were small, dogfishlike benthic forms, and large pelagic ones were rare until the Late Devonian, when some possible filter feeders turn up. However, there is some indication that some early chondrichthyans, notably xenacanthiforms and hybodontiforms, were already adapted to fresh waters by Late Carboniferous and Early Permian times (about 300–290 Myr). Yet this remains debated (Schultze, 2009). These presumed fresh water xenacanthiforms were among the largest fishes of their time, with elongated, sometimes eel-shaped body with a long dorsal fin and an anterior dorsal fin spine attached to the braincase in the most derived species. Later, in the Mesozoic, certain hybodontiforms also occur in reputedly fresh water lacustrine environments, sometimes confirmed by stable isotope analyses. The presence of abundant egg capsules in some of these fossil sites indicates that they could serve as nurseries, but this does not preclude a marine or brackish environment for the adults. Judging from their overall external morphology, one may infer that most stem elasmobranchs lived like modern sharks, as pelagic predators. In contrast, many of the stem euchondrichthyans and, more so, stem euchondrocephalans display peculiar anatomical features whose function remains enigmatic. Symmoriiforms possess a peculiar dorsal “spine-brush” complex (Stethacanthus, Akmonistion) or a forwardly projected dorsal spine (Falcatus, Damocles) that possibly played a role in mating. Among stem euchondrocephalans, various “bradyodonts,” such as chondrenchelyids, bore peculiar cephalic spines that also served as frontal claspers. Also, many stem euchodrocephalans display tooth morphologies that reflect

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durophagous diets, such as crushing tooth families (sometimes fused into a single plate) in chondrenchelyids, or large, parrot bill-shaped symphysial teeth in petalodontids. These stem euchondrocephalans are generally found around the large Carboniferous and Permian coral reefs. The huge symphysial tooth whorl of the Late Carboniferous and Permian eugeneodontids (e.g., Helicoprion) is a spectacular specialization that has raised fanciful interpretations, but is now best interpreted as an adaptation to feeding on ammonoid cephalopods (Ramsay et al., 2015). Among stem euchondrocephalans, iniopterygians also display a most peculiar morphology (Fig. 1.2), with large, dorsally placed pectoral fins, and possible ink pouches at the level of the pelvic girdles (Zangerl, 1981), all characters that suggest a benthic mode of life. Probably, further investigations on early euchondrocephalans will reveal other unsuspected adaptations or body shapes, some of which may parallel those known in e.g., living benthic teleosts. By contrast, the overall morphology of most stem elasmobranchs and stem neoselachians reflects adaptations to open sea, pelagic environments. So far, most fossil chondrichthyans known from articulated skeletons, including stem euchondrichthyans, provide evidence for pelvic claspers, and it is likely that internal fertilization is a general character for the total group. However, no acanthodian displays this character, whereas many “placoderms” do possess clasper-like pelvic structures, which suggests that internal fertilization was a general character for stem gnathostomes (Long et al., 2015). Assuming that acanthodians actually are stem chondrichthyans, it has been suggested that the euchondrichthyan pelvic claspers are neoformations, homoplastic with those of “placoderms” (Trinajstic et al., 2014; Long et al., 2015).

4. CONCLUSION During the last two decades, our knowledge of chondrichthyan interrelationships and relationships throughout time has been considerably increased thanks to new imaging technologies that have allowed reconstructing in detail their endoskeletal anatomy, notably the cranial structures of their earliest, Paleozoic representatives. Extensive cranial character analyses have revealed that a number of Paleozoic chondrichthyans formerly thought to be either stem elasmobranchs or stem holocephalans seem to form a large extinct ensemble of stem chondrichthyans, partly corresponding to what was referred to as “cladodont sharks” on the basis of tooth morphology, and that the last common ancestor of elasmobranchs

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and holocephalans is much younger than previously thought, probably no more than 370–380 Myr-old. Chondrichthyans thus seem to show two major evolutionary radiations, one by the end of the Silurian, which gave rise to the diversity of the stem euchondrichthyans, notably the “cladodont sharks,” and one by the end of the Devonian, which gave rise to the crown-group chondrichthyans. Elasmobranchs (euselachians when including stem elasmobranchs) retained a comparatively conserved overall morphology, despite highly specialized adaptations of the sense organs, whereas holocephalans (euchondrocephalans when including stem holocephalans) soon developed spectacular morphological specializations that reflect adaptations to very diverse, mainly benthic, marine environments. REFERENCES Bonaparte, C. L. (1838). Synopsis vertebratorum systematis. Nuovi Ann. Sci. Nat. Bologna 2, 105–133. Brazeau, M. D. (2009). The braincase and jaws of a Devonian “acanthodian” and modern gnathostomeorigins. Nature 457, 305–308. Brazeau, M. D. and Friedman, M. (2015). The origin and early phylogenetic history of jawed vertebrates. Nature 520, 491–497. Burrow, C. J. and Rudkin, D. (2014). Oldest near-complete acanthodian: the first vertebrate from the Silurian Bertie Formation Konservat-Lagersta¨tte. PLoS One 9 (8), e104171. http://dx.doi.org/10.1371/journal.pone.0104171. Cappetta, H. (1997). Chondrichthyes 2. Mesozoic and Cenozoic Elasmobranchii. In Handbook of Paleoichthyology (ed. H.-P. Schultze), vol. 3B. Stuttgart: Gustav Fischer. Cuny, G. and Beneteau, A. (2013). Requins de la pre´histoire a` nos jours. Paris: Belin. Davis, S. P., Finarelli, J. A. and Coates, M. I. (2012). Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 248–250. Dean, B. (1909). Studies on fossil fishes (sharks, chimaeroids and arthrodires). Mem. Am. Mus. Nat. Hist. 9, 209–287. Denison, R. H. (1979). Acanthodii. In Handbook of Paleoichthyology (ed. H.-P. Schultze), vol. 5. Stuttgart: Gustav Fischer. Didier, D. A. (2004). Phylogeny and classification of extant holocephali. In Biology of Sharks and Their Relatives (eds. J. C. Carrier, J. A. Musick and M. R. Heithaus), pp. 115–135. Boca Raton, FL: CRC Press. Ginter, M., Hampe, O. and Duffin, C. (2010). Chondrichthyes, Paleozoic Elasmobranchii: teeth. In Handbook of Paleoichthyology (ed. H.-P. Schultze), vol. 3D. Munich: Verlag Friedrich Pfeil. Goodrich, E. S. (1909). Cyclostomes and fishes. In A treatise on Zoology, Vertebrata Caniata (ed. E. R. Lankester), vol. 9. London: A. and C. Black. Grogan, E. D. and Lund, R. (2000). Debeerius ellefseni (fam. nov., gen.nov., spec. nov.), a autodiastylic chondrichthyan from the Mississipian Bear Gulch Limestone of Montana (USA), the relationships of the Chondrichthyes, and comments on gnathostome evolution. J. Morphol. 243, 219–245. Grogan, E. D. and Lund, R. (2004). The origin and relationships of early chondrichthyes. In The Biology of Sharks and Their Relatives (eds. J. C. Carrier, J. A. Musick and M. R. Heithaus), pp. 3–31. Boca Raton, FL: CRC Press.

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Guinot, G., Adnet, S., Cavin, L. and Cappetta, H. (2013). Cretaceous stem chondrichthyans survived the end-Permian mass extinction. Nat. Commun. http://dx.doi.org/10.1038/ ncomms3669. Heinicke, M. P., Naylor, G. J. P. and Hedges, S. B. (2009). Cartilaginous fishes (Chondrichthyes). In The Timetree of Life (eds. S. B. Hedges and S. Kumar), pp. 320–327. Oxford: Oxford University Press. Huxley, T. H. (1880). A Manual of the Anatomy of Vertebrate Animals. New York, NY: D. Appleton and Co. Janvier, P. (1996). Early Vertebrates. Oxford: Oxford University Press. Janvier, P. (2007). Primitive fishes and fishes from Deep Time. In Fish Physiology: Primitive Fishes (eds. D. J. McKenzie, A. P. Farrell and C. J. Brauner), vol. 26. pp. 1–51. San Diego, CA: Academic Press. Janvier, P. (2015). Facts and fancies about early fossil chordates and vertebrates. Nature 520, 483–489. Janvier, P. and Maisey, J. G. (2010). The Devonian vertebrates of South America and their biogeographical relationships. In Morphology, Phylogeny and Biogeography of Fossil Fishes – Honoring Meemann Chang (eds. D. K. Elliott, J. G. Maisey, X. Yu and D. Miao), pp. 431–459. Munich: Verlag Fiedrich Pfeil. Karatajute-Talimaa, V. N. (1998). Determination methods for the exoskeletal remains of early vertebrates. Mitteilungen aus dem Museum for Naturkunde in Berlin 1998, 21–52. Long, J. A., Mark-Kurik, E., Johanson, Z., Lee, M. S., Young, G. C., Zhu, M., Ahlberg, P. E., Newman, M., den Blaauwen, L., Choo, B. and Tinajstic, K. (2015). Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517, 196–199. Maisey, J. G. (1989). Visceral skeleton and musculature of a Late Devonian shark. J. Vertebr. Paleontol. 9, 174–190. Maisey, J. G. (2001). A primitive chondrichthyan braincase from the Middle Devonian of Bolivia. In Major Events in Early Vertebrate Evolution (ed. P. E. Ahlberg), pp. 263–288. London: Taylor and Francis. Maisey, J. G. (2012). What is an “elasmobranchs.” The impact of paleontology in understanding elasmobranch phylogeny and evolution. J. Fish Biol. 80, 918–951. Maisey, J. G. and Lane, J. A. (2010). Labyrinth morphology and the evolution of low-frequency phonoreception in elasmobranchs. C. R. Palevol 9, 289–309. Maisey, J. G., Miller, R. and Turner, S. (2009). The braincase of the chondrichthyan Doliodus from the Lower Devonian Campbellton Formation of New Brunswick, Canada. Acta Zool. 90 (Suppl. 1), 109–122. Maisey, J. G., Naylor, G. J. P. and Ward, D. J. (2004). Mesozoic elasmobranchs, neoselachian phylogeny and the rise of modern neoselachian diversity. In Mesozoic Fishes 3 – Systematics, Paleoenvironments and Biodiversity (eds. G. Arratia and A. Tintori), pp. 17–56. Munich: Verlag Friedrich Pfeil. Maisey, J.G., Pradel, A., Denton, J.S.S., 2014. Improving the diagnosis of crown group chondrichthyans for the Tree of Life project. In: Poster, 74th Meeting of the Society of Vertebrate Paleontology, Berlin 2004. Miller, R. F., Cloutier, R. and Turner, S. (2003). The oldest articulated chondrichthyan from the Early Devonian period. Nature 425, 501–504. Owen, R. (1866). On the Anatomy of Vertebrates. Vol.1, Fishes and Reptiles. London: Langemans, Green and Co. Pradel, A. (2010). Skull and brain anatomy of a Late Carboniferous Sibyrhynchidae (Chondrichthyes, Iniopterygia) from Kansas and Oklahoma (USA). Geodiversitas 32, 595–661.

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Pradel, A., Langer, M., Maisey, J. G., Geffard-Kuriyama, D., Cloetens, P., Janvier, P. and Tafforeau, P. (2009). Skull and brain of a 300 million-year-old chimaeroid fish revealed by synchrotron holotomography. Proc. Natl. Acad. Sci. U.S.A. 106, 5224–5228. Pradel, A., Maisey, J. G., Tafforeau, P., Mapes, R. H. and Mallatt, J. (2014). A Palaeozoic shark with osteichthyan-like branchial arches. Nature 509, 608–611. Pradel, A., Tafforeau, P., Maisey, J. G. and Janvier, P. (2011). A new Paleozoic Symmoriiformes (Chondrichthyes) from the Late Carboniferous of Kansas (USA) and cladistic analysis of early chondrichthyans. PloS One 6 (9), e24938. Ramsay, J. B., Wilga, C. D., Tapanila, L., Pruitt, J., Pradel, A., Schlader, R. and Didier, D. A. (2015). Eating with a saw for a jaw: functional morphology of the jaws and tooth-whorl in Helicoprion davisii. J. Morphol. 276, 47–64. Sansom, I. J., Wang, N.-Z. and Smith, M. M. (2005). The histology and affinities of sinacanthid fishes: primitive gnathostomes from the Silurian of China. Zool. J. Linn. Soc. London 144, 379–386. Schultze, H.-P. (2009). Interpretation of marine and freshwater paleoenvironments in PermoCarboniferous deposits. Palaeogeogr. Palaeoclimatol. 281, 126–136. Shirai, S. (1996). Phylogenetic interrelationships of neoselachians (Chondrichthyes: Euselachii). In Interrelationships of Fishes (eds. M. L.J. Stiassny, L. R. Parenti and G. D. Johnson), pp. 9–34. London: Academic Press. Stahl, B. J. (1999). Chondrichthyes III, Holocephali. In Handbook of Palaeoichthyology (ed. H.-P. Schultze), vol. 4. Pfeil, Munich: Verlag Friedrich Pfeil. Stensio¨, E.A. (1969). Elasmobranchiomorphi, Placodermata, Arthrodires. In Traite´ de Pale´ontologie (ed J. Piveteau), vol. 4(2). pp. 71–692. Paris: Masson. Trinajstic, K., Boisvert, C., Long, J. A., Maksimenko, A. and Johansson, Z. (2014). Pelvic and reproductive structures in placoderms (stem gnathostomes). Biol. Rev. Camb. Philos. Soc. 90, 467–501. Young, G. C. (1982). Devonian sharks from south-eastern Australia and Antarctica. Palaeontology 25, 87–89. Zangerl, R. (1981). Chondrichthyes 1. Palaeozoic Elasmobranchii. In Handbook of Paleoichthyology (ed. H.-P. Schultze), vol. 3A. Stuttgart: Gustav Fischer.

2 HOW ELASMOBRANCHS SENSE THEIR ENVIRONMENT SHAUN P. COLLIN RYAN M. KEMPSTER KARA E. YOPAK

1. Introduction 2. The Visual System 2.1. The Eye and Image Formation 2.2. Photoreception and Spectral Sensitivity 2.3. The Retina and the Choroidal Tapetum 2.4. Visual Sampling 2.5. Visual Abilities 3. The Non-visual System 4. The Auditory and Vestibular Systems 4.1. The Inner Ear 4.2. Vestibular Control 4.3. Auditory Abilities 5. The Electrosensory System 5.1. Structure and Spatial Sampling of the Ampullary Organs 5.2. Role in Passive Electroreception 5.3. Role in Magnetoreception 6. The Lateral Line System 6.1. Canal and Superficial Neuromasts 6.2. Sensitivity to Hydrodynamic Stimuli 7. Cutaneous Mechanoreception 8. The Chemosensory Systems 8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances 8.2. Olfactory Sensitivity 8.3. The Gustatory Apparatus 8.4. Gustatory Sampling and Sensitivity 8.5. The Common Chemical Sense 9. Sensory Input to the Central Nervous System in Elasmobranchs 9.1. Neuroanatomy 9.2. Assessing the Relative Importance of Each Sensory Modality 9.3. Encephalization 9.4. Neuroecology 10. Perspectives on Future Directions 19 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00002-X

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Elasmobranchs occupy a diversity of ecological niches with each species adapted to a complex set of environmental conditions. These conditions can be defined as a web of environmental signals, which are detected by a battery of senses, that have enabled these apex predators to survive relatively unchanged for over 400 million years. Signals such as light, odors, electric and magnetic fields, sound, and hydrodynamic disturbances all form a sensoryscape that each species can detect and process. However, the biophysical signals and their propagation within each ecological niche differ and place selection pressures on the ability of a specific sensory modality to detect and respond to prey, predator, and mate. This review investigates how elasmobranchs sense their environment by examining a diversity of species from different habitats, the ways in which they sample their sensoryscape, the sensitivity of each of their senses, and the effect this has on their behavior. The relative importance of each sensory modality is also investigated and how sensory input to the central nervous system can be assessed and used as a predictor of behavior. Although there is still a great deal we do not understand about elasmobranch sensory systems, the anatomical, physiological, molecular, and bioimaging approaches currently being used are enabling us to ask complex behavioral questions of these impressive predators.

1. INTRODUCTION Many chondrichthyan fishes are apex predators and play an important role in regulating ecosystem function. The elasmobranchs (the sharks, skates, and rays) comprise the bulk of the Chondrichthyes (B96%) and occupy a range of ecological niches in both freshwater and marine environments with some species able to migrate from one environment to the other (see Chapter 1; McEachran and Aschliman, 2004; Musick et al., 2004; Sims, 2010). These cartilaginous fishes are varied in their size, body form, swimming mode, and behavior, although many species are not yet well studied (Donley et al., 2004). Elasmobranchs possess an impressive array of highly specialized sensory systems that have been shaped by over 400 million years of evolution and have adapted to the range of environments in which they inhabit. Each sensory modality allows these fishes to detect and respond to a different set of biotic and/or abiotic stimuli over different spatial scales and over a range of sensitivities. Of the battery of senses available to a particular species, each modality does not operate in isolation but often in combination, although

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the relative importance of one or more senses differs interspecifically. Moreover, multiple, functionally distinct sensory systems provide redundancy when conditions are such that one or more senses are rendered ineffective, thereby increasing the chances that a given stimulus or object will be detected and/or correctly identified (Stein et al., 2005; Gardiner et al., 2014a,b). While a single sensory modality may suffice for some behaviors, information from multiple environmental cues can result in shorter reaction times, greater sensitivity, better spatial and temporal resolution, and improved noise rejection (Stein and Stanford, 2008; Gardiner et al., 2014a,b). A detailed knowledge of the sensory biology of elasmobranchs is essential for understanding the ways in which they interpret the biophysical world in which they are immersed and predicting their behavior. The environmental cues important to the survival of elasmobranchs include light, sound, odors, electric and magnetic fields, water movement, temperature, and pressure. This review presents an overview of studies focused on understanding the capabilities and thresholds of each sensory modality in the context of the biologically relevant signals available to elasmobranchs. The visual (image-forming and non-image-forming forms of photoreception), auditory (auditory and vestibular), chemosensory (olfactory and gustatory), electroreceptive, lateral line systems, and cutaneous mechanoreception (touch) are discussed for a diversity of species occupying a range of habitats. While gustation and touch rely on signals in the immediate vicinity of the afferent receptors, other modalities such as electroreception and lateral line operate over greater distances of approximately 30–60 cm and one to two body lengths, respectively. Depending on the water type (Jerlov, 1976) and the levels of turbidity, image-forming vision can be useful at distances of up to 100 m but non-image-forming photoreception can operate at much larger scales (hundreds of meters). Both olfaction and audition are also considered to be modalities effective over long distances with ranges of hundreds and even thousands of meters, respectively, although detection distances often exceed the distance over which accurate directional information can be determined (Atema, 2012; Gardiner et al., 2014a,b). The relative importance of each sense may differ between species and even within a single species when a different ecological niche is encountered during their lifecycle (Hueter and Gruber, 1982; Lisney et al., 2007). All sensory cues have been implicated in influencing behavior in elasmobranchs but assessing the contribution of a particular sense is difficult. While there are significant species differences in how elasmobranchs approach prey, odor is generally the first signal detected,

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leading to upstream swimming and eddy chemotaxis. Closer to the prey, as more sensory cues become available, the preferred sensory modalities vary among species, with vision, hydrodynamic imaging, electroreception, and touch being important for orienting to, striking at, and capturing prey (Gardiner et al., 2014a,b). However, studies quantitatively assessing afferent input (cranial nerve axon numbers), the volume of sensory brain lobes, and even the relative number of neurons are now beginning to provide crucial (quantitative) information of how much sensory information reaches the central nervous system and how this is processed. Anatomical, physiological, behavioral, and even new bioimaging techniques are now being employed to provide a more complete sensory profile of how these ancient predators sense their surroundings and to make predictions of the sensory drivers of natural behaviors such as feeding, the avoidance of predators, spatial orientation, activity patterns, social interactions, finding mates, and navigation. This information will ultimately enable us to understand the evolution of sensory systems, the limits of sensory perception, the neural networks involved in processing biologically relevant, environmental signals and the vulnerability of sharks to overfishing, exploitation, and environmental perturbation, including climate change (O’Brien et al., 2013; Collin and Hart, 2015).

2. THE VISUAL SYSTEM Elasmobranchs generally possess well-developed, image-forming eyes with interspecific variations in structure that reflect adaptations for vision in different photic environments, that is, from the deep-sea to the brightly lit surface waters (for recent reviews, see Hart et al., 2006; Lisney et al., 2012). Species inhabiting shallow and brightly lit waters, have large eyes capable of providing a detailed image of their surroundings (Lisney and Collin, 2007) with visual acuity (spatial resolving power) ranging from approximately 2 to 11 cycles per degree (Hueter, 1990; Lisney and Collin 2008; Theiss et al., 2010). The lateral position of the eyes in the head often affords a cyclopean visual field with varying degrees of binocular overlap in the frontal visual field (Harris, 1965; Smith, 2005; McComb et al., 2009). The extent of the visual field is species-specific and dictated by head morphology, eye mobility, eye position, pupil size and shape, the axis of accommodatory lens movement, head movement, the depth of the orbit, and the extent of eye protrusion from the body contour (Collin and Shand, 2003). It appears that lateral head movements during swimming may compensate for any paucity

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of frontally directed vision in some species and that the shape of the head influences the degree of the binocular field (McComb et al., 2009).

2.1. The Eye and Image Formation The eyes of elasmobranchs are generally hemispherical and supported by a cartilaginous, cranial orbit, which varies in size and shape and the level of eye support (Smith, 2005). At the back of the eye, six extraocular eye muscles afford some degree of eye movement in tracking moving objects or maintaining ocular fixation during swimming (Harris, 1965; Montgomery, 1983). The extent of eye movements (spontaneous eyes movements, which are conjugated and synchronized in the horizontal plane) also varies between rays (B101 in the shovelnose ray, Rhinobatos typus) and sharks (B601 in the bamboo shark, Chiloscyllium punctatum) (K. Smith, K. Fritsches and S. P. Collin, unpublished data). The extraocular eye muscles (four rectus and two oblique) surround both the optic nerve and the optic pedicel (Walls, 1942). Little is known of the function of the optic pedicel or eye stalk but the variability in its attachment to the eye and its relative hypertrophy in some species (i.e., stingrays) suggests it may play a supportive role in maintaining a fixed visual axis during lateral movements of the head (K. Smith, K. Fritsches and S. P. Collin, unpublished data). The optic nerve leaving the back of the eye conveys information of the neural image to the visual centers of the brain. For image formation to occur, quanta of light (photons) must enter the eye. Each photon is characterized by its wavelength (l) and, together with other photons of many different wavelengths, forms a visible spectrum. The color and intensity of this spectrum changes with depth, where specific wavelengths are absorbed differentially in different bodies of water according to the type and amount of organic matter suspended within the water column (Jerlov, 1976; Levine and MacNichol, 1982; McFarland, 1991a). Light reaching the eyes may be changed as it propagates within the water, where inevitably, there is a loss of intensity and often a change in the spectral composition. A number of species that live within the epipelagic zone (0–200 m in tropical and subtropical waters) also possess ocular media (cornea, lens, and vitreous humor) that absorb relatively high amounts of short wavelength light. Photo-oxidation of lens and corneal structures in elasmobranchs increases the degree of pigmentation, which subsequently reduces the relative amount of UV transmission to the retina when the animal is exposed to light with a high UV content (Nelson et al., 2003). The formation of an image in the camera-like eyes of elasmobranchs is mediated by the dioptric apparatus (cornea, lens, iris, and intraocular eye

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muscle) (Fig. 2.1). In aquatic eyes, the lens provides the only refractive power of the dioptric system, where the cornea acts simply as a protective goggle because its refractive index closely matches that of the surrounding milieu (Collin and Collin, 2001). In contrast to most teleost fishes, the elasmobranch cornea possesses a number of structural adaptations to inhibit corneal swelling in extreme temperatures and during migration between seawater and

Figure 2.1. (A–D) Lateral views of the eye of the bamboo shark, Chiloscyllium punctatum, showing the constriction of the pupil over a period of 15 min after dark adaptation for 2 h. Rostral is to the left. (E) Laser ray tracing of the lens of C. punctatus showing the convergence of the parallel red laser beams from which the focal length can be measured. (F) and (G) Transverse sections of the retina of the wobbegong shark, Orectolobus ornatus, (F) and the giant shovelnose ray, Rhinobatos typus (G). Note the pronounced tapetum cellulosum (TAP), the large horizontal cells (arrows in F) and the greater proportion of cones (asterisks) in the photoreceptor layer (PR) in R. batillum. GC, ganglion cell layer; INL, inner nuclear layer; IPL, inner plexiform layer; ONL, outer nuclear layer; OPL, outer pigment epithelium; RPE, retinal pigment epithelium. (H) Topographic map of the distribution of retinal ganglion cells (with a peak of 1919 cells/mm2) in the sandbar shark, Carcharhinus plumbeus. T, temporal; V, ventral. (I) Diagrammatic representation of the approximate extent of the visual field (represented in light gray) and the projection of retinal areas of higher cell density onto the visual surrounds (represented in dark grays) of C. plumbeus. Scale bars, 5 mm (A–D), 1 mm (E), 30 mm (F), 50 mm (G), 1 mm (H). (A–E) Adapted from S. P. Collin, K. Fritsches and D. Fern, unpublished data. (F) Reprinted from Theiss et al. (2010) with permission Copyright r 2010 Karger Publishers, Basel, Switzerland. (G) Reprinted from Hart et al. (2004) with permission from The Company of Biologists. (H and I) Reprinted from Litherland et al. (2009a,b) with permission from Cambridge University Press.

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freshwater (Menasche et al., 1988; Hart et al., 2006; Collin and Collin, 2001). The crystalline lens of elasmobranchs is spherical or near spherical (Sivak, 1978; Hueter and Gruber, 1980; Sivak, 1991; Sivak and Luer, 1991) and is supported by a suspensory ligament and a protractor lentis muscle, an ectodermal muscle located in the ventral papilla of the ciliary body, which moves the lens away from the retina (Franz, 1931; Sivak and Gilbert, 1976). Spherical aberration is negated in elasmobranchs with a central to peripheral gradient of decreasing refractive index (Sivak, 1991). The eyes of elasmobranchs are considered to be emmetropic (visually corrected) in water (Hueter et al., 2001), providing a focused image on the retina (Fig. 2.1E). A well-developed accommodatory mechanism is found in sharks (Sivak, 1976; Sivak and Gilbert, 1976), while in rays, a ramped retina provides a static form of accommodation, where both close and distant objects may be brought into focus simultaneously (Sivak, 1976; Lisney, 2004). The pupillary aperture is moveable in most species of elasmobranchs (although some deep-sea species possess fixed pupils, Kuchnow, 1971; Bozzano et al., 2001), constricting to a slit in the light-adapted state, which may adopt different orientations (Walls, 1942; Kato, 1962; Gruber and Cohen, 1978) or even form a double pupil with a small aperture at each end of the slit (Bozzano et al., 2001). Irideal control of the level of light entering the eye enables image formation and photoreception over a large range of light intensities (Schaper 1899; Gruber et al., 1975a,b; Litherland and Collin, 2008). In elasmobranchs, there is a correlation between the speed of the pupillary response and the light environment that a species inhabits, with diurnal species achieving complete constriction or dilation of the pupil up to thirty times faster than nocturnal species (Kuchnow and Gilbert, 1967; Kuchnow, 1971; Gilbert et al., 1981; Douglas et al., 1998; Fig. 2.1A–D). The irideal mechanism responsible for the pupillary response consists of a dilator muscle controlled by the third cranial nerve and an antagonistic sphincter muscle. The fastest observed response is that of the nurse shark Ginglymostoma cirratum, which takes only 5–13 s for full constriction and between 24 and 30 s for complete dilation (Gilbert et al., 1981). The main advantage of a slit pupil over a circular pupil is the ability to close it more completely under very bright illumination (Walls, 1942; Fig. 2.1A–D), which is prevalent in sharks that are active during both day and night and must cope with enormous fluctuations in light intensity (Hart et al., 2006). 2.2. Photoreception and Spectral Sensitivity The sampling of an image takes place at the level of the photoreceptors, which line the back of the transparent retina. The photoreceptor layer is comprised of two basic photoreceptor types (rods and cones).

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Rod photoreceptors have cylindrical outer segments and operate in low light (scotopic) conditions, whereas cone photoreceptors have a conical outer segment and function in bright light (photopic) conditions (Walls, 1942; Polyak, 1957). Nearly all species of elasmobranchs studied to date possess a duplex retina containing both rods and cones, although their relative proportion varies according to both habitat and behavior (Fig. 2.1F and G). Species which live in brightly lit environments and/or exhibit diurnal activity patterns tend to have a higher proportion of cones to rods, that is, 1:3 in the Atlantic stingray Dasyatis sabina, than those species living in low light habitats and/or are more active at night, that is, 1:50 in the shark Squalus acanthias (Stell, 1972; Hart et al., 2006). Phototransduction is mediated at the level of the visual pigments. The visual pigment within the outer segment is composed of a G protein-coupled receptor that consists of a protein, opsin, covalently attached to a chromophore. Activation of the visual pigment by light triggers a transduction cascade that produces electrical responses in the photoreceptors. The absorption properties of the chromophore define the spectral sensitivity of the visual pigment, which in turn is dependent on both the type of chromophore and the type of opsin with which it is conjugated. Vertebrate chromophores are aldehydes of either vitamin A1 (retinal) or vitamin A2 (3,4-didehydroretinal), and visual pigments containing these different chromophores are traditionally referred to as rhodopsins or porphyropsins, respectively (Bridges, 1972; Crescitelli, 1972). From a functional and evolutionary perspective, opsin proteins fall into five major classes (Yokoyama and Yokoyama, 1996). One of these, the mediumwavelength sensitive RH1 class (forming visual pigments with a lmax in the range B470–520 nm) is restricted to the rod photoreceptors operating in scotopic conditions. The four remaining classes are localized to cone photoreceptors used under photopic conditions, that is, medium-/longwavelength sensitive (M/LWS; lmax B500–575 nm), medium-wavelength sensitive (RH2; lmax B440–535 nm), short-wavelength sensitive (SWS2; lmax B400–488 nm), and UV/violet sensitive (SWS1; lmax 355–445 nm) (Bowmaker, 1995; Davies et al., 2012). The mechanism of phototransduction has important implications for how elasmobranchs sense their environment visually. In order to see color, the retina must contain at least two different types of photoreceptors each containing a visual pigment with a different spectral sensitivity. Hart et al. (2004) and Theiss et al. (2007) measured three spectrally distinct cone pigments in the retinas of the giant shovelnose ray Rhinobatos (=Glaucostegus) typus, the eastern shovelnose ray Aptychotrema rostrata, and the bluespotted stingray, Neotrygon kuhlii, with lmax values at 459–476 nm, 492–502 nm, and 552–561 nm, respectively, in addition to a rod pigment

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with a lmax value of 497–504 nm, thereby providing the potential for trichromatic color sampling (Fig. 2.2A and B). Although it is still uncertain how important color discrimination is in these species, recent evidence has revealed that at least one of these species (G. typus) can discriminate objects behaviorally on the basis of color rather than brightness (Van-Eyk et al., 2011). A recent study has also revealed that one other species of batoid (yellow stingrays, Urobatis jamaicensis) possesses UV sensitivity (Bedore et al., 2013). In contrast to batoids, Hart et al. (2011) found only one cone visual pigment in seven different species of sharks (lmax 532–561 nm) using microspectrophotometry suggesting that sharks are monochromats or color blind (Fig. 2.2C). Monochromacy has since been confirmed at the molecular

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Figure 2.2. (A and B) Normalized mean prebleach absorbance spectra of a single rod and three cone pigments in the giant shovelnose ray, Rhinobatos typus. lmax (wavelength of maximum absorbance) values are 504 nm (rod) and 477 nm (cone), 502 nm (cone), and 561 nm (cone). (C) Normalized mean prebleach absorbance spectra of the rod and cone visual pigments in the common blacktip shark Carcharhinus limbatus. lmax values are 506 nm (rod) and 532 nm (cone). (D) Phylogenetic analysis of the LWS and RH1 retinal opsins in the wobbegong sharks, Orectolobus ornatus and O. maculatus. Confidence values are placed at each node. The scale bar shows the number of nucleotide substitutions per site. (A and B) Adapted from Hart et al. (2004) with permission from The Company of Biologists. (C) Adapted from Hart et al. (2011) with permission from Springer Science and Business Media. (D) Reproduced from Theiss et al. (2012) with permission from the Royal Society.

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level, at least in wobbegong sharks, with only a single LWS pigment found in addition to a rod (Theiss et al., 2012; Fig. 2.2D). The inability to discriminate color has also been recently confirmed behaviorally in selachians (gray bamboo shark, Chiloscyllium griseum, Schluessel, 2014), which indicates that this group of elasmobranchs must rely on other visual cues such as contrast (Hart and Collin, 2015). Cone monochromacy is not common in vertebrates and is perhaps surprising given that many sharks frequent the same (often colorful) environments as many batoid and teleost species, all of which possess multiple spectral cone types (Marshall and Vorobyev, 2003; Hart et al., 2004; Theiss et al., 2007; Van-Eyk et al., 2011). However, most marine mammals are also color blind indicating that the loss of short wavelength-sensitive visual pigments has occurred multiple times in evolution (Peichl et al., 2001; Hart et al., 2011). It is currently unknown why color vision has been lost in sharks (and marine mammals) and whether a novel mechanism of comparing rod and cone signals in the retina exists in these evolutionarily disparate groups or that contrast is the major driver in their visual behavior. Skates (i.e., Raja erinacea and Raja ocellata) appear to possess only rods (Dowling and Ripps, 1971; Szamier and Ripps, 1983), although their retinae show light adaptive electrophysiological changes similar to other elasmobranchs and may be considered as functionally duplex (Dowling and Ripps, 1991). 2.3. The Retina and the Choroidal Tapetum Information regarding the optical image is encoded by the retinal photoreceptor responses, and this neural image is conveyed to the output cells (the ganglion cells) via interneurons (bipolar cells). While bipolar cells convey signals vertically through the retina, horizontal and amacrine cells mediate the lateral spread of visual responses. Horizontal cells, like photoreceptors, respond in a graded fashion to changes in light intensity, but unlike photoreceptors, show an increase in response amplitude with increasing stimulus area (see Hart et al., 2006 for review). Amacrine cells form extensive lateral interconnections with the processes of bipolar cells and help to shape the complex response properties of many types of ganglion cells. Cohen (1980) characterized eight different morphological subtypes of bipolar cell and three types of amacrine cell in the retina of the lemon shark Negaprion brevirostris. Typically, a large number of rods are connected to a single bipolar cell, while cones tend to show less synaptic convergence (Fig. 2.1F and G). The high degree of rod summation results in higher scotopic sensitivity but reduced spatial resolving power. Another strategy used by elasmobranchs to enhance retinal sensitivity is to increase the length of the rod outer segments

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(Gruber and Cohen, 1985; Kohbara et al., 1987; Bozzano et al., 2001) and/or to include a tapetum lucidum behind the retina. A tapetum lucidum is a mechanism to enhance visual sensitivity by reflecting or diffusing light back towards the photoreceptors and is common in animals active under low light (scotopic) conditions, either as a consequence of their nocturnal, crepuscular, or arhythmic lifestyle or because they inhabit deep or turbid waters (Rodieck, 1973). A tapetum cellulosum (a layer of cells containing organized, highly refractive crystals) is situated in the choroid of elasmobranchs and may be fixed (non-occlusible) or modifiable (occlusible) (Denton and Nicol, 1964; Kuchnow and Gilbert, 1967; Heath, 1991; Fig. 2.1F). Non-occlusible tapeta are characteristic of predominantly nocturnal species, such as the small-spotted catshark Scyliorhinus canicula (Nicol, 1961) or those inhabiting deep-water environments, such as the blackmouth catshark Galeus melastomus (Bozzano et al., 2001). In some species, the tapetum covers only part of the fundus. The reflective material of the choroidal tapeta cellulosa is crystalline guanine (Nicol and van Baalen, 1968; Somiya, 1980). The guanine crystals are packaged within membrane-bound crystal sacs stacked in order to form reflective plates 15–20 layers thick within each guanophore (Arnott et al., 1970; Braekevelt, 1994; Fig. 2.1F). During light adaptation, melanincontaining organelles (melanosomes) migrate along the interdigitating processes of the melanocytes to occlude the guanophores and prevent light from being reflected back onto the retina. Dark adaptation of the tapetum occurs by the reverse process (Bernstein, 1961; Denton and Nicol, 1964). Compared to the response of the pupil to changes in illumination, both light and dark adaptation of the tapetum occur relatively slowly. 2.4. Visual Sampling Analysis of the number and distribution of retinal neurons is a powerful indicator of how elasmobranchs sample their visual environment. Photoreceptor topography has only been examined in a limited number of species but, as found for a range of other vertebrates (Collin, 1999, 2008), areas of increased photoreceptor density or zones for acute vision (higher spatial sampling or resolving power) have been identified in all species studied to date. Acute zones typically occur across an elongated region extending horizontally from the temporal to the nasal parts of the eye, which provides a panoramic view of the visual field, potentially negating the need for compensatory eye movements (Litherland and Collin, 2008; Newman et al., 2013; Fig. 2.1H and I). The topography of the retinal ganglion cells (RGCs) or the output neurons of the retina has been examined more extensively in elasmobranchs and may represent a more accurate representation of the

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input to the CNS and ultimately a better predictor of behavior as proposed for teleost fishes by Collin and Pettigrew (1988a,b; Fig. 2.1H). Active, bentho-pelagic, pelagic, and deep-sea species tend to possess centrally positioned areae (or a concentric increase in cell density) or weakly elongated visual streaks (horizontally oriented increases in cell density), such as revealed for the gray reef shark, Carcharhinus amblyrhynchos, and the blue shark, Prionace glauca (Lisney and Collin, 2008; Fig. 2.1H). Benthic species, such as the bamboo shark C. punctatum, and the blue-spotted maskray, N. kuhlii, which feed on relatively immobile prey commonly possess a dorsal visual streak, which would facilitate downward vision and be used to panoramically scan the substrate in addition to isolating objects moving along the sand–water horizon (Theiss et al. 2007; Lisney and Collin, 2008). Direct comparisons between photoreceptor and RGC topography has only been examined in a few species (Hueter, 1990; Litherland and Collin, 2008; Garza-Gisholt et al., 2014). In the sandbar shark, Carcharhinus plumbeus, the level of summation varies between 40:1 and 80:1 (photoreceptor: ganglion cell). Deep-sea sharks also possess high convergence ratios to detect bioluminescent signals in addition to rod acute zones to detect and follow small glowing areas on the skin of conspecifics during dynamic behaviors such as cohesive swimming and hunting (Claes and Mallefet, 2011; Claes et al., 2014). Rod densities in deep-sea sharks reach densities of 82,000 rods per mm2 with over 63,000,000 rods found in each eye in the longsnout dogfish, Deania quadrispinosum, all sampling bioluminescent point sources of light (Newman et al., 2013). For the most part, the areas of highest photoreceptor cell density overlap with the areas of highest RGC density, although in some species the peak cell densities for the cones and rods are not always congruent, which suggests there might be a shift in visual function between photopic and scotopic conditions (Litherland and Collin, 2008; Garza-Gisholt et al., 2014). In some species, a strongly reflective choroidal tapetum extends across the horizontal meridian of the eye coinciding with the position of the visual streak of increased ganglion cell density (Bozzano and Collin, 2000). The heterogeneous distribution of ganglion cells across the retina is reflected in a nonlinear retinotectal projection of RGC afferents, where three times as much tectal area is devoted to ganglion cell axons emanating from the visual streak than those originating from ganglion cells in the peripheral retina in the lemon shark N. brevirostris (Hueter, 1988). 2.5. Visual Abilities The importance of vision in different behaviors has been studied for only a small proportion of elasmobranchs. As described above, variation in RGC

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topography appears to be related to the visual demands of different habitats and lifestyles, as well as the positioning of the eyes in the head. The upper limits of spatial resolving power have been calculated in 10 species and are found to be between 2.02 and 10.56 cycles per degree (Lisney and Collin, 2008). Species with a lower spatial resolving power tend to be benthic and/or coastal species that feed on benthic invertebrates and fishes. Active, benthopelagic and pelagic species from more oceanic habitats, which feed on larger, more active prey, possess higher resolving power. It has also been revealed that predicted levels of peak spatial resolving power increases with eye growth from 4.3 to 8.9 cycles per degree in the sandbar shark, C. plumbeus, and from 5.7 to 7.2 cycles per degree in the shortspine spurdog, Squalus mitsukurii, in addition to changes in the optical properties of the eyes (Litherland et al., 2009a,b). Given the lack of color vision in sharks, brightness contrast rather than color is likely to play a primary role in the detection and discrimination of ecologically relevant objects, such as predators, prey, and conspecifics. This may explain why early behavioral studies revealed discrimination between targets with contrasting vertical and horizontal black and yellow lines (in large sharks Carcharhinus spp., Cousteau and Cousteau, 1970), black and white horizontal and vertical lines (in nurse sharks, G. cirratum, Aronson et al., 1967; Graeber and Ebbesson, 1972a,b; Graeber, 1978), and a variety of shapes, dark and light objects, and striped patterns (in lemon sharks N. brevirostris, Clark, 1959, 1963) for a food reward. Myrberg (1991) suggested that distinctive fin markings may play a role in species recognition and size judging of sympatric species such as the whitetip, blacktip, and gray reef sharks. Gilbert (1963) compared the relative importance of olfaction and vision in prey detection in adult N. brevirostris by temporarily eliminating each of these senses, either by blocking the nostrils or covering the eyes. Whereas olfaction was found to be more important at long range, within 50 ft of a prey item, vision became increasingly important (depending on factors such as current strength and direction, water clarity, and light availability), and at close range (10 ft or less) Gilbert considered vision to be the principal sense used in prey detection in lemon sharks. Benthic species known to camouflage themselves against the substrate, that is, the angel shark, Squatina californica, and the wobbegong shark, Orectolobus ornatus, use a visually mediated ambush strategy to capture prey (Fouts and Nelson, 1999; Theiss et al., 2010; Egeberg, et al., 2014). The great white shark Carcharodon carcharias is thought to be a predominantly visual predator, based on a low rod-to-cone ratio (4:1), the presence of a well-developed area centralis (Gruber and Cohen, 1985; Litherland, 2001), a diurnal activity pattern, and direct observations of feeding behavior both from above and below the

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surface (Klimley and Ainley, 1996). Future studies incorporating behavioral investigations will undoubtedly test many of the predictions of visual abilities made using anatomical and physiological approaches.

3. THE NON-VISUAL SYSTEM In addition to image-forming eyes, elasmobranchs also possess photoreceptive tissue, which mediates irradiance detection and circadian photoentrainment, an endogenous time-keeping mechanism or biological clock to respond to predictable changes in environmental conditions, for example, seasons, tides, light cycles, and temperature. These aggregations of photosensitive cells possess non-visual pigments (opsins), which comprise a protein linked to a chromophore, retinal, a derivative of vitamin A1. In teleost fishes, these pigments are found in the eye (non-rod, non-cone photosensitive retinal neurons) and/or within specialized cells in the iris, CNS (pineal and parapineal, deep brain receptors), skin, and even internal organs (Drivenes et al., 2003; Bellingham et al., 2006; Davies et al., 2012). However, little is known of the non-visual system in elasmobranchs and the distribution of these pigments. Even fewer studies have revealed the localization and/or function of these photosensitive pigments in the context of a species’ preferred light environment. The pineal complex has been described for several species of elasmobranchs and has been found to comprise a pineal vesicle supported by a pineal stalk (Tilney and Warren, 1919; Ru¨deberg, 1968, 1969; Gruber et al., 1975a,b). Based on early studies, a portion of the roof of the skull of some species of selachians is shown to be unchondrified forming a “prefrontal epiphysial fontallene” or “fenestra pracerebralis” (Allis, 1923). Using light stimulation of the pineal, Hamasaki and Streck (1971) revealed that the pineal organ in S. canicula was stimulated and possessed a similar photosensitivity to the retina, where light is able to penetrate the skin and overlying cartilage to stimulate the photoreceptors lining the pineal lumen (Hamasaki and Streck, 1971; Gruber et al., 1975a,b; Meissl and Yan˜ez, 1994). The pineal organ of Scyliorhinus sp. was found to respond to changes in illumination of 4  10 6 lumens/m2, which is well below the intensity of moonlight at the water’s surface (Hamasaki and Streck, 1971). Although not overtly visible in shallow water species, a dorsal “pineal window” has been observed by Clark and Kristof (1990) in three groups of deep-sea sharks including the sixgill, gulper, and lantern shark, which make large vertical migrations between the euphotic and aphotic zones. There is apparently no parapineal gland in elasmobranchs. Little is known about the function of

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the pineal gland in elasmobranchs, but presumably it is developed in all species and provides a means of assessing diel changes in light levels and in setting circadian rhythms (Gruber et al., 1988; Bres, 1993). Ru¨deberg (1969) described the ultrastructure of the pineal organ in the small spotted catshark, S. canicula, and revealed that although the receptor cells in the pineal vesicle were cone-like in shape with irregularly developed outer segments, the receptors appear to be rod-like, and to contain a rod opsin with a peak spectral sensitivity (lmax) of 500 nm. Recent research has revealed one of the most ancient, non-visual pigment genes, melanopsin, which dates back over 400 million years, is present in a close relative of the Elasmobranchii, the Holocephali, that is, in the elephant shark, Callorhinchus milii. This species represents one of the earliest stages in the evolution of jawed vertebrates and possesses three melanopsin genes (opn4m1, opn4m2, and opn4x), all expressed in multiple tissue types including the eye and brain but also the fins, gills, liver, and testes (Davies et al., 2012). The significance of this differential pattern of expression is unclear, but may be related to the movement of the elephant shark from the deep ocean to shallow water in order to spawn, where it is exposed to a bright light environment. The opn4x (Xenopus-like) isoform of melanopsin may be the key pigment that detects light used to set its circadian rhythm in the shallow estuarine waters during the spawning season, whereas the two opn4m (mammalian-like) pigments may be more important for photoentrainment at the deeper oceanic stages of its lifecycle (Davies et al., 2012). Although unknown at present, it is assumed that sharks and rays will also be found to possess melanopsin in addition to many other non-visual pigments that will no doubt hold clues to how these elasmobranchs mediate circadian photoentrainment.

4. THE AUDITORY AND VESTIBULAR SYSTEMS Sound is a very effective channel for communication in the aquatic environment, traveling at almost 1500 m/s. Propagation of sound is affected by temperature, pressure, and salinity (McKenzie, 1960) and may be extended by reflecting from either the surface of the water and/or the interface created by a thermocline (Bretschneider et al., 2001). Ambient noise includes sounds produced by wave action, friction produced by water movement over the substrate or between currents traveling in different directions, and the varied cacophony of sounds produced by aquatic animals. Anthropogenic sound can also add to the background, over which an animal using sound to communicate would need to overcome

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(Slabbekoorn et al., 2010; Popper et al., 2014; Song et al., 2015). In animals that produce sound, there are typically three types of sonic mechanisms: stridulation (friction of teeth, fins, spines, or bones), hydrodynamic swimming movement (especially during rapid changes in direction and velocity) and swim bladder muscles (both intrinsic and extrinsic). Although the electric ray, Torpedo marmorata, has been reported to produce low frequency grunts in connection with its electrical discharges (Vincent, 1963), it is generally accepted that elasmobranchs do not typically produce sounds. Without a swim bladder, elasmobranchs receive all sounds either through direct conduction to the inner ear or by way of the lateral line system (see Section 6) both of which are able to detect frequencies up to 1000 Hz (Kritzler and Wood, 1961). Sound is an important stimulus in the aquatic environment, where natural “noise” is used to locate prey, warn of the advance of predators, attract mates, defend territories, and enable some species to navigate long distances (Sand et al., 2001). 4.1. The Inner Ear The inner ears of elasmobranchs comprise a membranous labyrinth, which derives ontogenetically from a common placode with the lateral line system, consisting of three orthogonally arranged, endolymph-filled semicircular canals and three otolithic organs or maculae: the sacculus, the utriculus, and the lagena (Retzius, 1881; Maisey, 2001; Fig. 2.3A–D). Bundles of sensory hair cells located within an ampullary swelling (crista ampullaris) at the base of each semicircular canal and within a sensory epithelium (macula) (Tester et al., 1972), respond to mechanical deflection with graded electrical potentials (Hudspeth and Corey, 1977). An additional sensory end organ (the macula neglecta) is located on the wall of the posterior semicircular canal duct (Corwin, 1977; Fig. 2.3E and F). All four maculae are sensitive to linear motion and gravity-generated acceleration. However, the sacculus and macula neglecta have been shown to be also responsive to vibratory motion, with the macula neglecta having best sensitivity to vertical movements (Popper and Fay, 1977). The hair cell bundles are embedded within a gelatinous mucopolysaccharide matrix or “cupula,” which underlies a dense matrix of endogenous calcium carbonate crystals (Carlstro¨m, 1963; Tester et al., 1972; Mulligan and Gauldie, 1989) and/or exogenous sand particles bound together with a carbon matrix (Lychakov et al., 2000; Mills et al., 2011) that form an otoconial mass. The endolymphatic pore and the “ductus endolymphaticus” are the only visible traces of the ear from the external (dorsal) surface (Lowenstein, 1971). The otolithic organs in elasmobranchs detect linear acceleration caused by self-motion and the action of gravity. The inertial lag of the otoconial

Sound pressure level (dB re 1uPa)

160 Raja erinacea (ABR)

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Raja erinacea (Behavioral)

Heterodontus francisi

130 120 110 Carcharhinus leucas

100 Negaprion brevirostris

90 80 10

100

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Figure 2.3. (A–D) Photographs of the inner ear of four species of elasmobranchs showing morphological diversity of the three semicircular canals and the otoconial masses of the utricle (u), saccular (s), and lagena (l). A. Glaucostegus typus. B. Aptychotrema rostrata. C. Urolophus paucimaculatus. D. Gymnura micrura. A, Anterior; D, Dorsal. (E and F) Scanning electron micrographs of the macula neglecta in the skate Raja ocellata showing the long kinocilia of the hair cell bundles in the peripheral region (E) and the numerous short stereocilia in the central region (F). (G) Comparison of the audiograms of a number of elasmobranch species obtained using physiological (ABR) and behavioral (classical conditioning). Open squares, Raja erinacea obtained using ABR; closed squares, R. erinacea, obtained using behavioral means; open diamonds, Negaprion brevirostris, obtained using ABR; closed diamonds, Heterodontus francisci, and closed triangles, C. leucas, all obtained using ABR. (A–D) Reproduced from Evangelista et al. (2010) with permission from John Wiley & Sons. (E and F) Reproduced from Barber et al. (1985) with permission from Springer Science and Business Media. (G) Reproduced from Casper et al. (2003) with permission from Springer Science and Business Media.

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mass(es) provides a stimulus for the macular hair cells, which are directionally polarized for more effective sound source localization (Nelson, 1967; Barber and Emerson, 1980). Connective tissue strands anchor the paste-like otolithic masses to the labyrinth wall to dampen their movement (Lowenstein, 1971). The size of the hair cells is not homogeneous within each bundle, with a kinocilium (a true cilium with nine peripheral and two central double longitudinal filaments) being larger than the stereocilia (Fig. 2.3E and F). Mechanical deflection of the cupula in one direction elicits an excitation of steady-state activity, while deflection in the other direction elicits an inhibition of neural activity. The deflection occurs because of a difference in the density of the otoconial mass compared to the rest of the body. When a sound wave reaches the animal, it will move the body because it has a similar density to the surrounding water and the animal is small relative to the wavelength of the sound wave. The denser otoconial mass will accelerate more slowly than the rest of the body, including the labyrinth (Hanson et al., 1990; Hunt, 1992; Bretschneider et al., 2001). This inertial lag will be transmitted to the macula via the otolithic membrane and cause the hair bundles to bend (Fay and Popper, 1974). Each macula is subdivided into regions occupied by hair cells with diametrically opposed orientations (Lovell et al., 2005; Fig. 2.3E and F), where excitatory and inhibitory responses will occur simultaneously or in succession under the influence of gravitational or an inertial stimulus (Lowenstein et al., 1964). It appears that the sensitivity of the elasmobranch labyrinth to gravitational stimuli is also mediated by the saccular, utricular, and lagenal otolithic organs in addition to the three semicircular canals (Lowenstein and Roberts, 1949). Another mechanotransduction mechanism has also been proposed involving the macula neglecta (Lowenstein and Roberts, 1951; Fay et al., 1974; Corwin, 1981). This mechanism relies on the conduction of particle motion into the posterior canal duct through a membrane-covered, fluid-filled opening (the fenestra ovalis) located at the base of a depression (the parietal fossa) in the dorsal chondrocranium (Daniel, 1934; Lowenstein and Roberts, 1951). Sound waves, particularly those coming from above and in front, would be transmitted to the endolymph within the posterior dorsal canal and cause local displacements of the cupula of the macula neglecta (Fay et al., 1974; Corwin, 1977). Hair cell and axon numbers within the macular neglecta of skates, R. ocellata, are significantly higher in females than males suggesting that there is a sexual dimorphism in far-field localization of prey and in mate detection (Barber et al., 1985). Corwin (1978, 1989) proposed the morphology of the elasmobranch inner ear could be characterized into two main groups according to auditory requirements and predatory ability. Werner (1930) and Thwaites (1999) also

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proposed two groups (although different to those of Corwin) based on structural differences but a recent study divides ear types into four groups based on the examination of a more extensive list of morphological criteria (Evangelista et al., 2010; Fig. 2.3A–D), placing species with a range of feeding strategies together, which suggests that both functional and phylogenetic factors may underlie the level of variation. Species in Group 1 are non-raptorial foragers, feeding on benthic marine invertebrates. Group 2 species are generally similar to those of Group 1 but this group possesses larger saccular organs. Members of Group 3 can be assigned to two different feeding strategies. The first are represented by Carcharhinus and Negaprion sharks, which are raptorial foragers, feeding on mobile active prey such as cephalapods, teleosts, and other elasmobranchs. The other is represented by species with a less active foraging mode, belonging to the “sit and wait” predators, the Orectolobus sharks. Group 4 species are all benthic demersal elasmobranchs, which are non-raptorial foragers, feeding mainly upon marine invertebrates (Evangelista et al., 2010; Fig. 2.3A–D). These studies propose that variations in the diameter and curvature of the semicircular canals may correlate with functional differences in vestibular control (Jones and Spells, 1963; Ten Kate et al., 1970; Howland and Masci, 1973). However, variations in the dimensions, shape, orientation, fluid coupling (i.e., between the anterior vertical and horizontal canal crus), temperature, endolymph chemistry of the semicircular canals, and putative differences in the cupula mechanics within the ampulla are all variables that may affect canal responses (Bernacsek and Carroll, 1981; Holstein et al., 2004; Hullar, 2006), and need to be examined in more detail. 4.2. Vestibular Control The inner ear of elasmobranchs possesses three semicircular canals, which are responsible for vestibular control, that is, detecting rotational movements of the head to maintain equilibrium and balance (Ladich and Popper, 2004). The anterior-vertical and horizontal canals are both conjoined along a common canal branch, the crus, while the circular posterior-vertical canal remains separate (Fig. 2.3A–D). Each semicircular canal ends in an ampullary swelling containing bundles of hair cells encapsulated within a jelly-like cupula containing sensory hair cells (Baird, 1974). The canals radiate from the three otoconial organs; the anterior utriculus, the central sacculus, and the posterior lagena (Fig. 2.3A–D). In the past, the canal dimensions of the inner ear (mainly the internal canal radius and the radius of curvature of the canal) have been used to predict the degree of head movement, and therefore, behavior (Jones and Spells, 1963; Fine et al., 1987). However, measurements of canal radii and

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radii of curvature are thought to be inadequate in accurately predicting animal head movements, orientation, and manoeuvrability (Hullar, 2006). As is the situation for the otoconial masses, orientational changes in the position of the head, produces an inertial lag of the endolymph filling the semicircular canals, which deflects the cupula of the crista ampullaris and, consequently, the hair bundles of the underlying sensory epithelium (Popper et al., 2003). 4.3. Auditory Abilities Hearing abilities are typically defined in terms of frequency range, threshold detection level (i.e., sensitivity) and directionality. Elasmobranchs are able to hear sounds up to about 1000 Hz and are most sensitive to frequencies below about 100 Hz (Nelson, 1967; Popper and Fay, 1977; Bullock and Corwin, 1979; Casper and Mann, 2006, 2007a,b, 2010) detected solely through the particle-motion component of an acoustic field (Popper and Fay, 1977; Corwin, 1981, 1989; Myrberg, 2001; Hueter et al., 2004; Casper and Mann, 2010; Hart and Collin, 2015). The auditory evoked potential method has been used to measure hearing thresholds in a number of species, which reveal that the inner ear of the Atlantic sharpnose shark Rhizoprionodon terraenovae, is most sensitive at 20 Hz with decreasing sensitivity at higher frequencies (Casper and Mann, 2010). Hearing thresholds measured in other species including the nurse shark G. cirratum, the yellow stingray U. jamaicensis, the lemon shark, N. brevirostris (Banner, 1967), and the horn shark, Heterodontis francisi (Kelly and Nelson, 1975) were found to be between 300 and 600 Hz (Casper and Mann, 2006, Fig. 2.3G). A more recent study has also examined hearing sensitivity using both behavioral conditioning and auditory brainstem recording (ABR) and found them to be comparable in the little skate, R. erinacea (Casper et al., 2003; Fig. 2.3G). These electrophysiological studies have confirmed earlier work by Kritzler and Wood (1961) in the bull shark, Carcharhinus leucas, by Nelson (1967) in the lemon shark, N. brevirostris, and by Dijkgraaf (1963) in the dogfish, S. canicula, which all used classical conditioning to reveal hearing thresholds at low frequencies. Nelson and Gruber (1963) and Wisby et al. (1964) were also able to attract sharks to low frequency sounds between 20 and 60 Hz, a low frequency acoustic stimulus that mimics a wounded fish after a predatory attack (Nelson and Gruber, 1963; Myrberg et al., 1969). Free-ranging sharks are also attracted to sounds possessing specific characteristics: irregularly pulsed, broad-band (most attractive frequencies below 80 Hz), and transmitted without a sudden increase in intensity (Myrberg, 2001). It appears that the qualities of “attractive” sound include

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elements from the low-frequency range and repetitive, irregular pulsing. However, the duration of individual pulses (Nelson and Johnson, 1972) and signal strength (Myrberg et al., 1972) do not appear to be critical components for attraction. Under natural conditions, owing to attenuation and the low intensity of the signal, sharks probably detect biological sounds less than 100 m from the source (Myrberg, 1978; Bres, 1993) but the direction of a sound source has been discriminated at distances of over 250 m. Unlike teleosts, elasmobranchs do not possess a swim bladder or other apparatus to convert acoustic pressure into a displacement stimulus. Therefore, elasmobranchs are only able to respond to the particle motion component of sound (acceleration, velocity, or displacement) and not the pressure component (Nelson, 1967; Gardiner et al., 2012). The sensory structures of the inner ear function as accelerometers that respond to both self-induced motion and environmental displacements. Although elasmobranchs are able to locate a sound source with considerable accuracy (Nelson, 1967) and may be considered to possess omnidirectional hearing (Casper and Mann, 2007b), the neural mechanisms by which they locate sound sources remains unknown (Gardiner et al., 2012). Future studies should be focused on a more comprehensive analysis of the frequencies each species can detect, the behavioral range over which sound is detected (behaviorally), and the central mechanisms of sound source localization.

5. THE ELECTROSENSORY SYSTEM The elasmobranch electrosensory system is a highly sensitive and multifunctional sensory modality capable of detecting minute electric field gradients produced by both biological and nonbiological sources (Kalmijn, 1974). It serves multiple functions from the detection of electric fields produced by potential prey (Kalmijn, 1966; Kajiura and Holland, 2002; Kempster et al., 2015) and approaching predators (Sisneros and Tricas, 2002b; Kempster et al., 2013b), to facilitating conspecific communication (Sisneros and Tricas, 2002a; Kempster et al., 2013a), detecting temperature gradients (Brown, 2010), and for orienting to the earth’s magnetic field to aid in navigation (Kalmijn, 1971; Klimley, 1993; Paulin, 1995). Weak electric field gradients like those produced by live prey are only detectable at short range due to the very rapid dissipation of electric fields in seawater (Kajiura and Holland, 2002; Bedore and Kajiura, 2013; Kempster et al., 2015). The exact distance at which an organism’s bioelectric field is

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Figure 2.4. (A and B) Electrosensory pore distribution maps of the dorsal and ventral surfaces of a dasyatid stingray (A) and a charcharhinid shark (B) showing the interspecific and dorsoventral differences. Pore distributions are approximate representations and for illustration purposes only. (C) Skin of a deep-sea shark illustrating the method of illuminating the positions of the pores of the ampullae of Lorenzini.

detectible is influenced by the signal strength and orientation, as well as the temperature and salinity of the surrounding water (Kalmijn, 1971). Behavioral trials to determine the sensitivity of elasmobranchs to preysimulating electric fields have, so far, revealed comparable results, with most species tested responding to electric field gradients as low as 1–5 nV/cm, within a maximum radius of approximately 50 cm from the source (Kajiura and Holland, 2002; McGowan and Kajiura, 2009; Jordan et al., 2009; Wueringer et al., 2012; Kempster et al., 2015). Nevertheless, variation in the number and distribution of electrosensory pores has highlighted that the functional capabilities of the electrorsensory syestem will likely vary by species to facilitate species-specific behaviors beyond just locating prey (Fig. 2.4A and B) (Kajiura et al., 2010; Kempster et al., 2012; Kempster et al., 2013a; Egeberg et al., 2014).

5.1. Structure and Spatial Sampling of the Ampullary Organs The superficial electrosensory pores of elasmobranchs, which are visible as small openings on the surface of the skin, may be distributed over a large surface area of the head and body (Fig. 2.4A–C). However, their associated sub-epidermal ampullary organs are bundled into distinct clusters in specific regions of the head (Chu and Wen, 1979; Camilieri-Asch et al., 2013; Kempster et al., 2013a; Egeberg et al., 2014). Ampullary organs are comprised of a number of grape-like structures called alveoli, each of which

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is lined with a sensory epithelium. The sensory epithelium consists of a series of sensory cells that detect changes in electric field gradients and transmit this information via axons of the anterior lateral line nerve (ALLN) to the brain. Each ampullary cluster is made up of hundreds of individual ampullary organs, which are themselves made up of thousands of sensory cells, which form distinct branches of the ALLN (Kempster et al., 2013a). The distinct clustering of ampullary electroreceptors results in variation in the spatial separation of individual pores on the skin’s surface and the length of their associated canals (Rivera-Vicente et al., 2011; Camilieri-Asch et al., 2013; Kempster et al., 2013a). Ampulla with the shortest canals sample electric fields over a relatively short distance, which means that the primary afferent nerve axons from these ampullary organs therefore receive proportionally less stimulation than ampulla with longer canals (RiveraVicente et al., 2011). In addition, canals that are oriented perpendicular to a uniform electric field will receive less stimulation than those that are parallel (Murray, 1962; Kajiura and Holland, 2002). The number of pores, the length of the canals, and the spatial arrangement of the electrosensory pore array over the skin are therefore important factors in each species’ ability to localize electric field sources in the three-dimensional marine environment (Rivera-Vicente et al., 2011). The abundance of electrosensory pores varies considerably at all taxonomic levels resulting in unique species-specific differences (Fig. 2.4) (Raschi, 1986; Kajiura et al., 2010; Kempster and Collin, 2011a,b; Kempster et al., 2012) that have been shown to discriminate between closely related species (Mello, 2009). Pore abundance varies between genera, families, and orders (Fig. 2.4), but has been found to be constant intraspecifically (Kempster et al., 2012). The specific distributional patterns of pores show a strong relationship at the taxonomic level of Order, and appear to be heavily influenced by morphology, with mouth position being a major contributing factor (Fig. 2.4) (Kempster et al., 2012; Kempster, 2014). Ecological factors may also have a significant impact on the structure and size of electroreceptors, the length of canals, and the size of the pore openings in the skin (Kalmijn, 1974; Chu and Wen, 1979; Whitehead, 2002; McGowan and Kajiura, 2009; Marzullo et al., 2011; Kempster et al., 2012; CamilieriAsch et al., 2013). Freshwater batoids, for example, exhibit smaller ampullary organs and shorter canals compared to their marine counterparts (Szabo et al., 1972; Chu and Wen, 1979; Szamier and Bennett, 1980; Raschi and Mackanos, 1989; Raschi et al., 1997), which is thought to be an adaptation to reduced water conductivity. Further, the bull shark, C. leucas, a species known to move regularly between freshwater and seawater, possesses ampullary organs that exhibit characteristics found in species from both fresh and salt water environments (Whitehead, 2002; Whitehead et al., 2014).

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Similarly, McGowan and Kajiura (2009) found that the electrosensitivity of rays that frequent both freshwater and saline environments did not differ, suggesting that the electrosensory systems of euryhaline species may possess specializations that are optimized to function in environments of markedly different electrical conductivity. 5.2. Role in Passive Electroreception Since it was first documented by Kalmijn (1966), a number of studies have now examined electrosensory-mediated feeding behaviors in elasmobranchs (Kajiura and Holland, 2002; Jordan et al., 2009; Kajiura and Fitzgerald, 2009; McGowan and Kajiura, 2009; Wueringer et al., 2012; Kempster, 2014; Kempster et al., 2015). By eliminating other sensory cues, these studies have confirmed the important role of the electrosensory system in facilitating feeding behaviors at close range. In addition, many studies have examined the morphology of the elasmobranch electrosensory system to provide insight into how it may be used to facilitate prey capture (Chu and Wen, 1979; Raschi, 1986; Kajiura et al., 2010; Kempster and Collin, 2011a,b; Kempster et al., 2012, 2013a; Wueringer et al., 2012; Egeberg et al., 2014). Benthic rays, for example, are thought to rely heavily on electroreception for feeding in the substrate, where prey may be concealed. This is reflected in the high abundance of electroreceptive pores that are present on the ventral side of their body, particularly around the mouth (Raschi, 1986; Kajiura et al., 2010; Kempster et al., 2012). This is thought to compensate for the restriction of visual input upon close approach to their prey. In contrast, benthic sharks typically have much lower pore abundances and a more conical head shape, which allows for a greater visual field above and below the head, where electroreception may be considered secondary to other senses such as vision and olfaction (Kempster et al., 2012; Gardiner et al., 2014a,b). In a recent study by Gardiner et al. (2014a,b), the importance of electroreception is examined in combination with other sensory systems. Gardiner et al. (2014a,b) showed that sharks are capable of detecting multiple sensory cues simultaneously, switching sensory modalities in a hierarchical fashion as they approach their prey, and substituting alternate sensory cues, when necessary, to accomplish behavioral tasks. In addition to being impressive hunters, elasmobranchs have also evolved a number of adaptations that maximize their chances of survival to avoid becoming food for other animals. The bamboo shark (C. punctatum) for example, has evolved a specific predator avoidance mechanism, mediated by the electrosensory system, to avoid predation during its early development (Kempster et al., 2013b). Shark embryos use electroreception to detect approaching predators and then to avoid being detected, they stop

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breathing and moving to prevent sending a signal that can be detected by that approaching predator (Kempster et al., 2013b). Interestingly, vertebrates that exhibit a “freeze” response to predators have also been shown to induce cardioventilatory responses, where they decrease their heart rate (bradycardia) to further reduce predation risk (Smith, 2006; Bowers and Natterson-Horowitz, 2012). As a result, the length of time that an animal is able to respond is finite, as the need to breathe and pump oxygen around the body will eventually overcome the urge to remain still and undetected. Thus, shark embryos will eventually resume, albeit much reduced, gill movements whilst still in the presence of a predator (Kempster et al., 2013b). It is likely that a similar predator avoidance strategy will also be used by small/juvenile elasmobranchs after hatching/birth to avoid detection by larger predators. As well as detecting predators and prey, the weak bioelectric fields produced by elasmobranchs can also be useful in assisting conspecifics in locating each other (Tricas et al., 1995; Kempster et al., 2013a). Although, externally, the elasmobranch electrosensory system displays no signs of sexual dimorphism that may indicate a possible function for conspecific location, sexual dimorphism has been observed in the abundance of nerve fibers that innervate the electrosensory system, which transmit information from sub-dermal ampullary clusters to the brain via discrete branches of the ALLN (Kempster et al., 2013a). In addition, Tricas et al. (1995) showed behavioral evidence that DC electric fields may assist in mate localization. They found that the modulated components of an individual’s bioelectric field (ventilatory movements of the spiracles, mouth, and gills) may be sufficient to distinguish an individual as prey or conspecific (Tricas et al., 1995). Future studies should focus on integrating the bioelectric signatures of biologically relevant organisms and sensitivity to understand the role of electroreception in communication, reproduction, and prey selectivity. 5.3. Role in Magnetoreception There is strong evidence to show that elasmobranchs are able to detect the earth’s magnetic field to assist in navigation, but the mechanisms by which this occurs remain unclear. Behavioral studies have provided evidence that elasmobranchs can detect magnetic fields (Andrianov et al., 1974; Meyer et al., 2005; Molteno and Kennedy, 2009), which are also corroborated by migration studies (Klimley, 1993; Jorgensen et al., 2010) that reveal several species can navigate over long distances in environments, where the geomagnetic field is the only plausible reference (Montgomery and Walker, 2001). Two mechanisms have been proposed for this ability to orient to the earth’s magnetic field: direct magnetoreception and induction-based electroreception (Kirschvink et al., 2001; Meyer et al., 2005; Molteno and Kennedy, 2009).

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Direct magnetoreception assumes that elasmobranchs possess magnetite-based magnetoreceptors whose primary function is to measure the geomagnetic field for the purposes of navigation. To date, the existence of a magnetoreceptor system in elasmobranchs has not been found but remains the subject of some debate (Lohmann and Johnsen, 2000; Kirschvink et al., 2001; Johnsen and Lohmann, 2005). On the other hand, inductionbased magnetoreception proposes that the orientation to the earth’s geomagnetic field is primarily achieved by magnetic induction (Kalmijn, 1984; Paulin, 1995). In this scenario, movement through the geomagnetic field induces currents in the electrosensory system that are subsequently used to achieve a compass heading. However, behavioral experiments using attached magnets have cast doubt on an induction-based mechanism (Hodson, 2000). By inserting bar magnets into the nasal cavity of the short-tailed stingray, Dasyatis brevicaudata, Hodson (2000) concluded that an induction-based mechanism was not possible because the magnets had impaired the ability of D. brevicaudata to detect magnetic field gradients. The theory dictated that a magnetic field that is stationary with respect to the electrosensory system (i.e., inserted into the nasal cavity) should have no effect on an induction-based mechanism for geomagnetic orientation. However, because elasmobranchs are cartilaginous, and thus flexible, other authors have suggested that the movement of the body with respect to the magnet might have resulted in a non-stationary magnetic field with respect to the electrosensory system, which would affect the function of an induction-based mechanism (Johnsen and Lohmann, 2005; Molteno and Kennedy, 2009). Further, Molteno and Kennedy (2009) suggested that the use of attached magnets would interfere with an induction-based mechanism because they predicted that the relative movement between the attached magnet and the electrosensory system would be more than 100 mm, a criterion not described by Hodson (2000). Clearly more work needs to be done in establishing the underlying mechanism(s) of magnetoreception.

6. THE LATERAL LINE SYSTEM The mechanosensory lateral line system is found in all fishes, and many aquatic amphibians, and functions to detect water movements to assist with navigation, and for detecting prey, predators, and conspecifics at close range (Dijkgraaf, 1963; Kalmijn, 1989; Montgomery and Skipworth, 1997; Montgomery et al., 1997; Kasumyan, 2003; Hueter et al., 2004). Specifically, mechanoreception is used to detect the presence and direction of large and

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small scale water movements caused by water currents and by the movement of other animals through the water (Dijkgraaf, 1963). The lateral line system consists of a network of receptor organs around the head and along the body to the tail (Coombs et al., 1988; Maruska and Tricas, 1998; Fig. 2.5). The specific spatial distribution of these organs will define the size of the mechanoreceptive field of the lateral line system (Denton and Gray, 1983, 1988), and thus variation in the position and orientation of individual receptor organs will result in species-specific reception capabilities (Maruska, 2001).

Tuble

Ridge Blood vessel Vesiculated epithelium Mucus Cupula Neuromast Fiber zone

“Ganglion” cells

Nerve subramulus

Figure 2.5. (A and B) Distribution of the lateral line canal system on the dorsal (upper) and ventral (lower) surface of the head of the bonnethead shark, Sphyrna tiburo. Numerous branched tubules extend from most canals and terminate in pores at the surface. Scale bar, 0.5 cm. (C and D) Distribution of the lateral line canal system on the dorsal (upper) and ventral (lower) surfaces of the butterfly ray, Gymnura micrura. The ventral system consists of both pored canals, and nonpored canals along the midline and around the mouth. Scale bars, 1 cm. HYO, hyomandibular canal; IO, infraorbital canal; SO, supraorbital canal; MAN, mandibular canal; PLL, posterior lateral line canal; SC, scapular canal; SO, supraorbital canal; SPL, subpleural loop. (E) Schematic representation of the dorsal (left) and ventral (right) lateral line canal system in the freshwater whipray, Himantura dalyensis. HYC, hyomandibular canal; IC, infraorbital canal; MC, mandibular canal; NC, nasal canal; PC, posterior canal; POC, postorbital canal; PR, prenasal canal; SCC, scapular canal; SUC, supraorbital canal; STC, supratemporal canal. (F) Diagram of a cross section of the head lateral line canal in a juvenile Carcharhinus menisorrah pup. (A–D) Reproduced from Maruska (2001) with permission from Springer Science and Business Media. (E) Reproduced from Marzullo et al. (2011) with permission from CSIRO Publishing. (F) Reproduced from Tester and Kendall (1967) with permission from University of Hawaii Press.

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6.1. Canal and Superficial Neuromasts The functional unit of all lateral line organs is the neuromast, a mechanoreceptor with directional sensitivity (Szabo, 1974). In elasmobranchs, four distinct lateral line organs have been observed, which are broadly categorized into two major types: those found in sub-epidermal canals, appropriately called canal neuromasts, and superficial neuromasts (also known as pit organs) that are not associated with a canal. As the name suggests, canal neuromasts are somewhat protected from the external environment as they are contained within a network of closed canals that are only exposed to the surrounding seawater via small pore openings. In contrast, superficial neuromasts are located on the skin surface in either open grooves (batoids) or between modified scales (sharks) exposing them directly to the surrounding water (Tester and Nelson, 1967; Peach, 2003). Canal and superficial neuromasts are comprised of sensory hair cells, supportive cells, and basal cells (Mu¨nz, 1979, 1989; Jørgensen, 1989; Maruska, 2001; Fig. 2.5F). Hair cells of the lateral line system are similar to those found in the auditory and vestibular systems (Platt and Popper, 1981; Lu and Popper, 1998). They are innervated by axons from distinct branches of the anterior (ALLN) and posterior (PLLN) lateral line nerves, which are associated with their location on the body (Norris and Hughes, 1920; Tester and Kendall, 1967; Mu¨nz, 1979). Sensory hair cells are so called because they consist of hair-like projections on their external surface, called ciliary bundles. Ciliary bundles comprise numerous stereocilia and a single large kinocilium (Flock, 1965). The tips of the cilia are embedded in a gelatinous cap known as the cupula (Fig. 2.5F); changes in pressure gradients produce water movement, which moves the cupula, subsequently bending the sensory hairs (Flock, 1967). Movements that cause the stereocilia to move towards the kinocilium result in the depolarization of the hair cell membrane, which subsequently results in an increase in the generation rate of action potentials; in contrast movement in the opposite direction causes hyperpolarization and results in a reduction in the generation rate of action potentials (Flock, 1965). Hair cell displacement of less than 1 nm is sufficient to elicit a neural response within the central nervous system, whereas saturation occurs at displacements larger than 100 nm (Kroese and Van Netten, 1989). Variation in neuromast morphology and orientation will likely have a major effect on function (Coombs et al., 1988). Compared to canal neuromasts, superficial neuromasts are typically smaller, contain fewer hair cells, and possess a smaller cupula and sensory epithelium (Mu¨nz and Claas, 1983; Coombs et al., 1988; Kalmijn, 1989). The two types of neuromasts can be further distinguished by the number of innervating afferent nerve fibers

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(Mu¨nz and Claas, 1983; Mu¨nz, 1989) and the extent of myelination of the afferent neurons (Flock and Wersa¨ll, 1962; Mu¨nz, 1979; Mu¨nz and Claas, 1983). Substantial morphological diversity is seen in the lateral line system of elasmobranchs (Garman, 1888; Tester and Kendall, 1967; Maruska, 2001), but the functional significance of these differences has received little attention. 6.2. Sensitivity to Hydrodynamic Stimuli Any movable object in water is a source of acoustic oscillations, generating both shift and pressure waves. Pressure waves spread in water faster, are extinguished more slowly, and create a far acoustic field. In contrast, shift waves have a slower speed, are extinguished more rapidly, and therefore have a much smaller distribution zone near the acoustic source (Kasumyan, 2003). Lateral line neuromasts are particularly sensitive to relatively low-frequency shift waves between 1 and 200 Hz (Sand, 1981; Bleckmann, 1993; Kasumyan, 2003). The sources of such hydrodynamic disturbances can come in many forms, from movements of the fishes themselves, other animals passing close by, the substrate, and water currents. The intensity and spectral characteristics of hydrodynamic disturbances in water depend on a number of parameters, including, but not limited to, the speed and trajectory, the acceleration of the moving object, its size and shape, and the resistance of the water (Kasumyan, 2003). Previous studies have shown that a calmly swimming fish generates oscillations with a frequency of up to 10 Hz, but sudden changes in their speed and direction can induce oscillations with frequencies up to 100 Hz (Bleckmann et al., 1991). A swimming fish is not only a source of oscillations of a certain frequency, but can also produce a hydrodynamic trace consisting of turbulent microcurrents (Kasumyan, 2003). This microturbulence can exist for a relatively long time, from several dozens of seconds to several minutes, and spread to a relatively large distance, up to several meters (Bleckmann, 1986, 1993) depending on the size of the fish and the speed and the pattern of its swimming. As a result, even a stationary fish, that is hidden out of sight, may be located by a predator simply due to the hydrodynamic trace that it leaves behind it (Montgomery and Milton, 1993; Kasumyan, 2003). The ability of an elasmobranch to detect low frequency oscillations is largely driven by the design of the sensory structures of the peripheral lateral line system. Although the morphology of canal neuromasts and superficial neuromasts are quite stable, it is the morphology of the peripheral structures

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that influence and guide the detection capabilities of individual neuromasts (Coombs and Braun, 2003). It is these morphological variations that are functionally important and can provide insights into biologically significant stimuli for a species (Coombs and Braun, 2003; Fig. 2.5). Sand (1981) found that the maximum frequency sensitivity of canal neuromasts ranges from 6.5 to 200 Hz allowing them to detect water currents at a velocity of 0.3–20 mm/s (Bleckmann, 1993; Bleckmann and Hofmann, 1998). In contrast, superficial neuromasts are found to be much more sensitive (2–15 Hz) allowing them to detect very weak water currents of just 0.03 mm/s (Sand, 1981; Bleckmann, 1993). Therefore, the relative proportion and distribution of each neuromast type will affect the overall functional capabilities of a fish’s lateral line system. As a result, based on the relative abundance and distribution of these neuromasts in a number of species (Jordan, 2008; Wueringer and Tibbetts, 2008; Marzullo et al., 2011; Gillis et al., 2012; Winther-Janson et al., 2012; Fig 2.5), we can make inferences about their function. In general, the role of superficial neuromasts is usually linked with obtaining information about the presence and direction of ocean currents and oscillations by large moveable objects. Whereas canal neuromasts are thought to assist in the detection of more localized water movements, such as those caused by passing prey (Bleckmann, 1993; Montgomery et al., 1995a,b; Engelmann et al., 2000; Kasumyan, 2003). In the future, the sensitivity of both the superficial and canal neurormast systems should be investigated in the context of each species’ environmental surroundings (water currents, surge, tidal flows, etc.) and the background “noise” with respect to body movement (i.e., swimming speed).

7. CUTANEOUS MECHANORECEPTION Cutaneous mechanoreception or touch is stimulated by skin deformation in elasmobranchs, that is, microvibrations (indentation) and changes in temperature (cold) (Bleckmann and Hofmann, 1998; Nier, 1976). Two distinct classes of mechanoreceptors (pressure and tension) have been differentiated in S. canicula, where spontaneous activity is altered once a threshold is reached. In S. canicula, the receptive fields of these neurons can be quite large (up to 60 mm2), extending across 150 placoid scales (Nier, 1976). Reactions to contact stimuli trigger protection reflexes and often locomotion but are part of the homeostatic proprioceptive system (Lissman, 1946; Lowenstein, 1956).

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8. THE CHEMOSENSORY SYSTEMS Olfaction (smell), gustation (taste), and the common chemical sense collectively comprise the chemosensory system in elasmobranchs, a modality that is generally well-developed (Hodgson and Mathewson, 1978; Kleerekoper, 1978). The propagation of chemoreceptive signals through the environment and the extent to which they are encountered by a given species depends upon swimming mode/speed, water movement, and odor concentration (Parker and Sheldon, 1913; Parker, 1914; Johnsen and Teeter, 1985). Olfaction guides many behaviors including the detection and localization of food, social communication, reproduction, and the avoidance of predators (see review by Hueter et al., 2004). Water-borne substances stimulate olfactory receptor neurons (ORNs) via paired openings in the head. Gustation is mediated by taste buds, which are primarily responsible for the evaluation and palatability of food through direct contact and the final “decision” to either ingest or reject an object. Gustation can be affected by environmental factors such as level of hunger, experience, temperature, pollutants, and pH (Atkinson and Collin, 2010). Although olfaction and gustation are separate senses, the olfactory and oral cavities are sometimes connected and irrigated by a bucopharyngeal pump (Bell, 1993).

8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances The detection of water-borne odors takes place within the paired olfactory cavities. The cavities or nares are situated ventrally in elasmobranchs and are often partially covered by skin flaps, sculptured to channel the incoming water into the vestibule lined with an olfactory epithelium (Fig. 2.6A). The flow through the nasal region can be driven solely by an external flow (e.g., generated by swimming or by a current) and therefore not only by respiratory activity (Tester, 1963; Cox et al., 2014). The major (prenarial) nasal groove along the cephalofoil in the hammerhead shark, Sphyrna tudes, has recently been shown to facilitate olfactory sampling of a large area (i.e., an extended hydrodynamic “reach”) by directing oncoming flow towards the incurrent nostril. This species also appears to utilize external (major and minor nasal grooves) and internal (apical gap) flow regulation mechanisms to limit water flow between the olfactory lamellae, thereby protecting these delicate structures from the potentially damaging high flow rates incurred by sampling a larger area (Rygg et al., 2013). In order to maximize the surface area, the olfactory epithelium is divided into a series of lamellae to form an elongated rosette (Fig. 2.6B). The parallel stacks of lamellae ensure the sensitive olfactory receptors within the

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60° 45° 30° E.Blochii

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Figure 2.6. (A) Photograph of the ventral side of the benthic shark, Chiloscyllium punctatum, showing the nares and associated flaps. (B) Illustration of the left olfactory organ of the spiny dogfish, Squalus acanthias showing the position of the olfactory lamellae and the valve flap. Ca, nasal cartilage; cp, nasal capsule; g, gallery; ic, inlet chamber; mf, membranous fold; nf, nasal flap; ob, olfactory bulb; p, protrusion of olfactory lamellae; pc, peripheral canal; r, raphe; sf, secondary fold; ve, valvular extension; vf, valve flap. (C–E) Differences in odor arrival time. (C) Differences in odor arrival time based on angle of attack. Illustration of a smooth dogfish, Mustelus canis, swimming into the leading edge of an odor patch oriented at various angles to the head. Assuming a constant swim speed, the time delay of odor arrival at the second naris (arrow) increases as the angle increases. (D) Differences in odor arrival time based on internarial spacing. Comparison of the smooth dogfish, Mustelus canis, with the sandbar shark, Carcharhinus plumbeus, and two species of hammerhead sharks, the scalloped hammerhead, Sphyrna lewini, and the winghead, Eusphyra blochii, swimming into an odor patch at a 451 angle. If the swim speed is constant across all four species, the wider spacing of the nares of the hammerheads results in an increased internarial arrival time difference (arrows). (E) Comparison of internarial arrival time differences among shark species. The expected internarial timing difference (in seconds) resulting from the encounter of the leading edge of an odor patch over a range of angles for four species of sharks: E. blochii (black solid line), S. lewini (gray solid line), C. plumbeus (gray dashed line), and M. canis (gray dotted line). The horizontal dashed lines indicate the largest and smallest timing differences tested in the study, to which M. canis demonstrated a directional response. (A) Reproduced from Schluessel et al. (2008) with permission from John Wiley & Sons. (B) Reproduced from Theisen et al. (1986) with permission from John Wiley & Sons. (C–E) Reproduced from Gardiner and Atema (2010) with permission from Elsevier.

epithelium encounter maximum exposure to the molecules in solution (Tester, 1963). There are interspecific differences in the position, size, and shape of the nares; the orientation of the rosette within the olfactory cavity; and the number and shape of the lamellae (Theisen et al., 1986; Fig. 2.6B). Although few studies have examined these differences with respect to the mode of swimming, it is expected that they will all affect the hydrodynamics

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of water flow over the olfactory epithelium and, therefore, olfactory sensitivity (Tester, 1963; Theisen et al., 1986; Zeiske et al., 1987; Schluessel et al., 2008; Rygg et al., 2013). The olfactory system is sensitive to odors of prey, conspecifics, predators, a specific habitat, reproductive partners, and anthropogenic disturbances. The propagation of these stimuli and the probability of encountering these chemosensory signals depends upon the swimming mode/speed of each species, water movement and currents in each species’ habitat, and odor concentration (Johnsen and Teeter, 1985). Since most odor plumes dissipate as a series of eddies, elasmobranchs are able to localize odor sources by simultaneous analyses of chemical (olfactory) and hydrodynamic (lateral line) dispersal fields, or eddy chemotaxis (Gardiner and Atema, 2007). The latency between encountering an odor on one side of the head versus the other has been also shown to play an important role in localizing odor sources, where the olfactory receptors within the nares on each side of the head are differentially stimulated (Gardiner and Atema, 2010; Fig. 2.6C–E). This implies that species with more widely spaced nares, that is, hammerheads, would be able to resolve smaller angles of attack at higher swimming speeds than those species with smaller intra-narial separation and explains why many larger pelagic species show klinotaxis or gradient searching (Parker, 1914; Kleerekoper, 1978; Bleckmann and Hofmann, 1998; Fig. 2.6C–E). The olfactory epithelium is populated by ORNs, which are not ciliated but possess a tuft of microvilli, which project into the nasal cavity. Different types of ORNs have been characterized based on morphological criteria; at least two in elasmobranchs (Takami et al., 1994; Schluessel et al., 2008) and at least three in teleosts (Hamdani and Døving, 2007). The surface of each olfactory lamella is divided into sensory and non-sensory regions. The sensory epithelium is easily identified by the large numbers of cilia originating from supporting cells, while the non-sensory squamous epithelium only bears microvilli. All olfactory receptors in a study of 21 species of elasmobranchs contain terminal knobs and are covered by microvilli (which also occurred over the supporting cells in the sensory and non-sensory regions), but no receptor cells possessed cilia (Schluessel et al., 2008). However, ciliated ORNs have been reported in the dogfish, S. acanthias (Bakhtin, 1977), and the zebrafish (Lipschitz and Michel, 2002). In addition to the ciliated and microvillous ORNs, a third type of chemosensory neuron has also been discovered in the olfactory epithelium of teleost fishes (Hansen and Finger, 2000; Hansen and Zeiske, 1998; Hansen and Zielinski, 2005). These crypt ORNs have an oval cell body that is almost completely surrounded by one or two supporting cells with an apical invagination (the “crypt”) thought to hold the olfactory receptor

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proteins and other elements of the transduction machinery. Crypt-like ORNs also occur in cartilaginous fishes (Ferrando et al., 2006), which suggests that they are a conserved feature in early gnathostomes. The morphologically different types of ORNs are thought to mediate responses to specific odorant classes. The olfactory system of teleost fishes is sensitive to several types of odorants, including amino acids, polyamines, bile salts, prostaglandins, steroids, and nucleotides (Hara, 1994; Rolen et al., 2003; Zielinski and Hara, 2006), and a similar situation is expected for elasmobranchs. Although elasmobranchs are thought to lack ciliated ORNs and the associated expression of specific G protein a-subunits utilizing the Gaolf transduction cascade, they are still able to detect bile salts (Eisthen, 2004; Meredith et al., 2012). 8.2. Olfactory Sensitivity Olfactory sensitivity has been assessed using both anatomical and physiological indicators. When the degree of primary (number of lamellae) and secondary folding (of each lamellae) is assessed, bentho-pelagic sharks and rays possess significantly more olfactory lamellae and larger sensory epithelial surface areas than benthic species (Schluessel et al., 2008; Theiss et al., 2009). However, there is no significant difference between lamella number or sensory surface area between groups of closely related species (Theiss et al., 2009) or species with similar diets, which indicates that differences in olfactory morphometrics are the result of functional rather than phylogenetic influences (Schluessel et al., 2008, 2010). At present, there are no data on the number or density of olfactory receptors or the level of convergence of the olfactory signals at either the level of the olfactory bulb (OB) or the telencephalon in any species of cartilaginous fish. A high convergence ratio, would predict the olfactory epithelium being stimulated at low odor concentrations (Meredith and Kajiura, 2010). Physiologically, olfactory sensitivity has typically been assessed using electro-olfactography (EOG) or single unit recording (Hodgson and Mathewson, 1978; Silver, 1979; Broun and Fasenko, 1982; Zeiske et al., 1986; Nikonov et al., 1990; Tricas et al., 2009; Meredith and Kajiura, 2010). Both techniques have revealed response thresholds to be in the subnanomolar range for serine (10 14 to 10 13 M), alanine (10 11 M), and cysteine (10 10 M) and in the micromolar range for asparagine (10 10 M) and lysine (10 8 M), although less sensitive thresholds have been documented in different species. When species with a greater lamellar surface area were analyzed using EOG, there was no correlation with olfactory threshold (Meredith and Kajiura, 2010). Future studies

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should assess the different olfactory receptor types, their distribution and convergence within specific glomeruli in the OB, as has been done for teleosts (Gemne and Døving, 1969; Doving, 1986), in addition to assessing the affinity of the amino acids to bind to the olfactory receptor sites in cartilaginous fishes (Bruch and Rulli, 1988). 8.3. The Gustatory Apparatus The gustatory receptors in elasmobranchs are situated on the apical ends of raised papillae or taste buds over the oral and pharyngeal epithelium of the mouth, basihyal (“tongue”), and gill arches. The morphology of the taste buds appears comparable to that of teleost fishes, where the sensory cells form a flask-like cluster at the apex of the papilla (Tester, 1963; Reutter et al., 1974; Finger, 1983; Atkinson, 2011). Papillae of various sizes are dispersed over the oropharyngeal cavity, gill bars, and oral valves in high concentrations although papillae appear to be absent from the oral valves of some species of batoids (Atkinson and Collin, 2010). At the apex of each papilla, the sensory cells terminate in a tuft of short, hair-like projections, which often project from a pore, for example, in the dogfish, S. canicula (Whitear and Moate, 1994). The taste buds are innervated by the facial (VII), the glossopharayngeal (IX), and the vagus (X) nerves (Norris and Hughes, 1920; Herrick, 1924; Daniel, 1934; Aronson, 1963). 8.4. Gustatory Sampling and Sensitivity Like olfaction, taste plays an important role in feeding, but our understanding of the mechanism and function of taste in elasmobranchs is still relatively poor (Atkinson and Collin, 2010). Taste-buds perched on papillae of various sizes have been observed within the oro-pharynx of the spiny dogfish, S. acanthias, where the distribution of the papillae is nonhomogeneous, which suggests that biting and manipulation of prey within the oro-pharynx may be important for taste assessment (Cook and Neal, 1921). A more recent study of gustation in sharks reveals that taste buds are more numerous in benthic species than in pelagic species (Atkinson, 2011). Topographic differences in taste bud distribution in these same groups could also reflect differences in feeding mechanism(s). Many benthic species use suction to consume soft-bodied organisms and tastebuds that are evenly distributed throughout the oral and pharyngeal cavity may imply some form of intra-oral food manipulation (Atkinson and Collin, 2010). However, some pelagic species feed predominately on larger and more active organisms and bite their prey before ingestion, where a higher density of taste buds in the regions around the jaws could indicate palatability before

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ingestion. The distribution of taste buds may also be partially controlled by the array of denticles that line the oral cavity and provide protection against abrasion during food consumption and increase friction and grip on prey items as they are manipulated within the mouth (Atkinson and Collin, 2012). Elasmobranchs appear to have relatively low densities of taste buds relative to teleost fishes but having more papillae does not necessarily equate to a greater gustatory sensitivity. There are currently no quantitative or physiological, and few behavioral, studies of gustation in elasmobranchs (Sheldon, 1909; Tester, 1963), but extracellular recording of gustatory receptors in catfishes reveals acute sensitivity to amino acids at 10 11 M (Caprio, 1975) and it is expected that there will also be a diverse palate of taste preferences revealed in future studies in elasmobranchs as has been found in teleosts (Kasumyan and Doving, 2003). There is clearly a need for more research on the sensitivity of elasmobranch taste buds, behavioral preferences to specific molecules, and the role of taste buds in the manipulation and/or ingestion of food.

8.5. The Common Chemical Sense The common chemical sense is separate from the senses of olfaction and gustation and is generally considered to be mediated by nerve fiber endings, which terminate within the epithelial cells of the oral and nasal cavities in addition to the external surface of the body (Tester, 1963). These nerve endings are part of the somatosensory system recording touch, temperature, and pain, which are innervated by spinal nerves and cranial nerves (trigeminal, facial, glossopharyngeal, and vagus), although the common chemical receptors (or irritant receptors) are thought to be primarily innervated by the trigeminal system (Sheldon, 1909; Tester, 1963). Solitary chemosensory cells also populate the taste papillae of elasmobranchs and do not appear to aggregate in a bundle or bud, but it is unclear whether this type of gustatory organ is independently innervated (Fahrenholz, 1915; Whitear and Moate, 1994). The innervation of the axonless solitary sensory cells of the taste buds in sharks is also not well understood (Finger, 1997, 2007; Reutter et al., 2000) and whether these cells are part of the common chemical sense. Future research is needed to investigate the function and innervation of this type of chemosensitivity (or chemesthesis, Bryant and Silver, 2000). Various studies to develop a chemical deterrent to sharks are thought to affect the common chemical sense (Sheldon, 1909; Springer, 1955; Sisneros and Nelson, 2001; and see review by Hart and Collin, 2015).

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9. SENSORY INPUT TO THE CENTRAL NERVOUS SYSTEM IN ELASMOBRANCHS The nervous system of cartilaginous fishes represents an early, yet remarkably complete, stage in the evolution of the vertebrate brain. There exists this startling generality in the vertebrate brain plan (Striedter, 2005), which originated at least as early as the chondrichthyans and has been carried through vertebrate evolution to modern day mammals. Early neurobiological studies were dominated by the view that sharks and their relatives possessed relatively small brains devoted primarily to olfactory processing (Aronson, 1963; Nieuwenhuys, 1967). However, it has since been shown that cartilaginous fishes are a highly encephalized group, with welldeveloped peripheral sensory systems and extreme neuro-morphological diversity. This section is focused on the input from the peripheral sense organs to the central nervous system, how this input may be quantified to predict the relative importance of different sensory modalities, central processing and how this relates to behavior, while taking into account the influences of both ecology and phylogeny. 9.1. Neuroanatomy Early chordate evolution is characterized by a number of remarkable evolutionary innovations. Of particular note is the formation of the “new head” in craniates, with its paired sense organs and basic brain plan, in addition to the co-evolution of jaws, paired fins, and the cerebellum in gnatostomes (Northcutt and Gans, 1983; Depew and Olsson, 2008). The brain of all cartilaginous fishes and indeed all jawed vertebrates is composed broadly of six major areas: the olfactory bulbs (OBs), telencephalon, diencephalon, mesencephalon, cerebellum, and medulla oblongata. Central organization and pathways within the brain have been well documented and described in a few key species (Smeets, 1983, 1998; Smeets et al., 1983; Nieuwenhuys et al., 1998; Butler and Hodos, 2005; Yopak, 2012a), and will only be broadly generalized here, with particular emphasis on sensory brain areas and structure/function relationships. 9.1.1. Olfactory Bulbs Like the peripheral olfactory sense organs, the OBs are paired structures that are positioned caudal to the olfactory epithelium. ORNs in the olfactory epithelium have short, thin axons that project directly to the OB in cartilaginous fishes, where they synapse with dendrites of second-order olfactory neurons called mitral cells (Laberge and Hara, 2001; Hamdani and Døving, 2007).

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Chimaeriformes

Myliobatiformes

Torpediniformes

Rhinopristiformes

Rajiformes

Pristiophoriformes squatiformes

Squaliformes

Hexanchiformes

Heterodontiformes

Orectolobiformes

Carcharhiniformes

Lamniformes

The ORN terminals and the mitral cell apical dendrites form specific structures called glomeruli. The axons of the mitral cells form part of the olfactory peduncles, which connect the OBs to the telencephalon. There is considerable variation in the size and shape of the OBs across species, as well as the thickness and length of the olfactory peduncles (Northcutt, 1978; Dryer and Graziadei, 1994; Smeets, 1998; Lisney and Collin, 2006; Schluessel et al., 2008) (Fig. 2.7). In hammerhead sharks (Sphyrna spp.) and batoids, the OBs take the form of elongated, sausageshaped cylinders (Dryer and Graziadei, 1993; Yopak et al., 2014b). In contrast, the OBs in most other sharks and in holocephalans consist of

Figure 2.7. Dorsal views of the brains from six representative species of cartilaginous fishes across six of the major chondrichthyan orders, which illustrate the diversity in the morphology and size of the six major brain regions found in this clade. (A) Carchariniformes: lemon shark, Negaprion brevirostris, (B) Heterodontiformes: horn shark, Heterodontus francisci, (C) Squaliformes: spiny dogfish, Squalus acanthias, (D) Rajiformes: argus skate, Dipturus polyommata, (E) Myliobatiformes: cowtail stingray Pastinachus atrus, and (F) Chimaeriformes: narrownose chimaera, Harriotta raleighana. OBs, olfactory bulbs; Tel, telencephalon; Cer, cerebellum; Cl, cerebellum-like structures; Md, medulla. Note that the mesencephalon (Mes) and diencephalon (Di) are partially obscured from a dorsal perspective. OBs absent in F. Scale bars 1 cm. Images for (D and E) adapted from Yopak et al. (2014b) and image for (F) adapted from Yopak (2012b). Phylogenetic relationships after Naylor et al. (2012).

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two ellipsoid-shaped subunits or “hemi-bulbs” (Dryer and Graziadei, 1993; Liu, 2001; Yopak et al., 2014b), termed the lateral and medial bulbs after Dryer and Graziadei (1993). Swellings have been documented along the length of the OBs of hammerhead sharks and batoids (Yopak et al., 2014b), which may also represent specific morphological subunits (see Dryer and Graziadei, 1993; Meredith and Kajiura, 2010). The olfactory peduncles vary greatly in length, and appear to be approximately circular in cross-section, whereas in batoids it is flattened and consist of distinct medial and lateral bundles (Dryer and Graziadei, 1993; Yopak et al., 2014b), which may reflect variation in the size and number of afferent fibers projecting from the OBs to the telencephalon (Schluessel et al., 2008). 9.1.2. Telencephalon Early researchers believed that the telencephalon was dominated by olfactory input (Johnston, 1911), but it has been shown to function more similarly to the telencephalon of other vertebrate groups, with only a portion of the forebrain receiving secondary and tertiary olfactory projections (Heimer, 1969; Ebbesson and Heimer, 1970; Ebbesson, 1972; Smeets, 1998; Hofmann and Northcutt, 2008, 2012). There is now extensive evidence to show that this brain area contributes greatly to the processing and moderation of other sensory modalities and complex behaviors (e.g., Schroeder and Ebbesson, 1974; Graeber, 1978; Luiten, 1981; Bodznick and Northcutt, 1984; Bleckmann et al., 1987; Smeets and Northcutt, 1987; Bodznick, 1991). The chondrichthyan telencephalon is a round, bulbous structure with two bilaterally symmetrical hemispheres (Fig. 2.7). These hemispheres are interconnected by a medial commissure in members of Elasmobranchii that is lacking in the Holocephali. This develops via a morphogenic process known as evagination, where the lateral walls of the structure expand and fold inwards, which subsequently forms the two hemispheres and associated ventricles (Holmgren, 1922), as it does in tetrapods (Butler and Hodos, 2005; Striedter, 2005). The telencephalon is divided broadly into two major areas, a dorsally positioned pallium (comprised of the lateral, dorsal, and medial pallia), and a ventral subpallium, with hypertrophy of various pallial divisions observed across this clade (Northcutt, 1989; Smeets, 1998; Hofmann and Northcutt, 2012; Yopak, 2012b). Secondary olfactory projections terminate most heavily in the lateral pallium, although they have multiple pathways to other telencephalic regions (Bleckmann et al., 1987; Smeets and Northcutt, 1987; Hofmann and Northcutt, 2008, 2012). The dorsal pallium is divided into the pars superficialis and the central nucleus (Northcutt, 1978). The central nucleus has been implicated in multimodal sensory integration, receiving input from visual and

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octavolateralis systems, as well as the control of complex behaviors (e.g., Ebbesson and Schroeder, 1971; Cohen et al., 1973; Graeber, 1978). The subpallium is divided into a septal area, an area basalis, and a striatal area, with varying numbers of subdivisions within these three areas across chondrichthyans (Smeets, 1990). A part of the area basalis, the area superficialis basalis, has been identified in all elasmobranchs studied thus far (Hofmann and Northcutt, 2008), and receives input from the lateral pallium and the OBs, although the extent to which it receives olfactory input is variable (Smeets, 1983; Smeets et al., 1983; Dryer and Graziadei, 1994; Hofmann, 1999; Hofmann and Northcutt, 2008, 2012). Higher order olfactory pathways project from the area basalis to the dorsal pallium, and, as such, it has been suggested that the dorsal pallium may also be involved in olfactory orientation (Hofmann and Northcutt, 2012). Three areas of the subpallium (area superficialis basalis, septum, and striatum) are also heavily interconnected with areas of the diencephalon (hypothalamus and ventral thalamus) and the mesencephalic tegmentum (Ebbesson and Schroeder, 1971). For additional detail on telencephalic development, cytoarchitecture, and detailed descriptions of intrinsic and extrinsic connections, please refer to previously published reviews (i.e., Smeets, 1983; Smeets et al., 1983, 1990, 1998; Smeets and Northcutt, 1987; Manso and Anadon, 1991; Dryer and Graziadei, 1994; Hofmann and Northcutt, 2008, 2012; Rodri´guez-Moldes, 2009; Demski, 2012; Quintana-Urzainqui et al., 2012, 2014). 9.1.3. Diencephalon The diencephalon is situated just caudal to the telencephalic subpallium and, although there is debate regarding the divisions between telencephalon and diencephalon (Puelles and Rubenstein, 1993; Northcutt, 1995; FerreiroGalve et al., 2008), is quadri-partitioned into the epithalamus, dorsal thalamus, ventral thalamus, and hypothalamus (Smeets, 1998; Hofmann, 1999). The epithalamus is the most dorsally located division in the diencephalon and is comprised of the habenula and the light-sensitive pineal organ (Ru¨deberg, 1968, 1969; Hamasaki and Streck, 1971; Wilson and Dodd, 1973). The dorsal thalamus, comprised of anterior, central posterior, dorsal posterior, and lateral posterior nuclei, is considered a multisensory relay station, receiving projections from a number of areas in the brain and relaying sensory information to the telencephalon (Ebbesson and Hodde, 1981; Smeets, 1981, 1982; Fiebig and Bleckmann, 1989). The anterior and dorsal portions receive input from visual/sensory brain areas, although the anterior nuclei receive input from both the retina and the optic tectum (Smeets, 1982; Northcutt, 1991), while the dorsal posterior nucleus reciprocally communicates with only the tectum (Northcutt, 1991).

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The central and lateral posterior nuclei receive electrosensory and/or mechanosensory afferents from the midbrain (Bleckmann et al., 1987) and the lateral posterior nuclei projects this information to the telencephalon (Schweitzer, 1983; Bodznick and Northcutt, 1984; Smeets and Boord, 1985), with connections to the medial (Smeets and Northcutt, 1987) and dorsal pallium (Bodznick and Northcutt, 1984; Fiebig and Bleckmann, 1989), potentially as part of an ascending electrosensory pathway (Schweitzer, 1983, 1986; Bodznick and Northcutt, 1984). The ventral thalamus, generally small in size, is divisible into three cell groups, all of which receive direct input from the retina and tectum (Smeets, 1982). The hypothalamus, however, is particularly enlarged and differentiated in cartilaginous fishes (Smeets, 1983). This brain area is engaged in homeostatic behaviors, regulation of the production of hormones, and relaying that information to the endocrine system (Northcutt, 1978; Hofmann, 1999; Demski, 2012). Main efferent pathways reach the mesencephalic tegmentum, reticular formation, and the cerebellum (Smeets and Boord, 1985; Fiebig, 1988; Pose-Mendez et al., 2013). 9.1.4. Mesencephalon The mesencephalon, or midbrain, is divided into two major areas in chondrichthyans: the dorsal tectum mesencephali (comprised of the optic tectum and the torus semicircularis) and the ventral tegmentum mesencephali, also referred to as the tegmentum (Hofmann, 1999). This brain area is similarly organized across the majority of vertebrates and is well developed across cartilaginous fishes (Smeets et al., 1983; Smeets, 1998; Lisney and Collin, 2006; Lisney et al., 2007; Yopak and Lisney, 2012; Yopak, 2012b). As in other vertebrates, the optic tectum (analogous to the superior colliculus in mammals) consists of paired lobes that form the roof of the mesencephalon (Barton et al., 1995). This region is comprised of alternating fiber and cellular layers, although debate persists concerning the number of tectal layers in cartilaginous fishes and the extent to which this characteristic varies intra- and interspecifically (Farner, 1978; Northcutt, 1979; Smeets, 1981; Ebbesson, 1984; Reperant et al., 1986; Manso and Anadon, 1991). The optic tectum is most readily associated with vision and visual processing, as it receives its major input from retinofugal fibers arising from the RGCs (Graeber and Ebbesson, 1972a,b; Northcutt, 1978, 1979; Reperant et al., 1986; Hofmann, 1999). These projections are organized topographically; that is, the optic tectum contains a map of an animal’s visual space (Bodznick, 1991). However, the visual system in cartilaginous fishes has multiple pathways; it has been shown experimentally that the tectum does not have exclusive control over visually guided behavior (Graeber, 1972; Graeber et al., 1973) and there are at least 10 other

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retinofugal targets in the brain where retinal fibers terminate (Northcutt, 1979, 1991), including the telecephalon (Graeber, 1978; Bodznick, 1991). The tectum also receives input from all other major brain areas (Boord and Northcutt, 1982; Smeets, 1982; Hofmann and Northcutt, 2008, 2012), as well as the spinal cord (Ebbesson and Hodde, 1981), and is involved in the processing of multisensory information (Smeets, 1998). Electrophysiological recordings have shown single-cell responses in the tectum to visual, electrosensory, mechanosensory, and acoustic stimuli (Bullock, 1984; Bleckmann et al., 1987; Bleckmann and Bullock, 1989; Bodznick, 1991; Hofmann and Bullock, 1995) and Smeets (1982) confirmed the existence of a direct contralateral connection between tectum and the octavolateralis areas in cartilaginous fishes. Projections from other sensory modalities, such as the somatosensory and octavolateralis systems, are also topographically organized and in register with one another (Bodznick, 1991; Hueter, 1990; Butler and Hodos, 2005). The tegmentum, located ventral to the tectum and rostral to the medulla oblongata, receives projections from most brain centers and is highly conserved across vertebrates (Striedter, 2005). Compared to the optic tectum, which has been the subject of significant study across most vertebrate classes, few comparative studies have examined the allometry and relative size of the tegmentum (Platel and Delfini, 1986; Kotrschal and Junger, 1988; Boire and Baron, 1994; Striedter, 2005; Yopak and Lisney, 2012), cytoarchitecture, and pathways (Smeets et al., 1983; Morita and Finger, 1985; Gonzalez et al., 1999; de Arriba and Pombal, 2007; Demski, 2012), although it is interconnected with the tectum and is related, in part, to visual processing. The lateral portion of the tegmentum receives input from the spinal cord (Hayle, 1973) and tectum (Boord and Northcutt, 1982; Smeets et al., 1983) and the lateral mesencephalic complex is the site for termination of secondary electrosensory, mechanosensory, and auditory fibers (Boord and Northcutt, 1982; Corwin and Northcutt, 1982). Cell groups in this area have been identified, including the midbrain reticular formation, which plays an important role in controlled locomotion in elasmobranchs (Demski, 1977; Droge and Leonard, 1983a,b), as observed in mammals (Mori et al., 1980) and teleosts (Kashin et al., 1974). 9.1.5. Cerebellum The cerebellum is considered an evolutionary innovation in gnathostomes, with many of the same cell types and organizational features conserved across all vertebrate groups. Although it has been debated whether cerebellar tissue exists in the myxinoids (Larsell, 1967; Nieuwenhuys, 1967; Ronan, 1986; Northcutt, 2002), it is generally accepted that at the onset of the jawed vertebrates (the cartilaginous fishes) there

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was a cerebellar addition to the central nervous system (reviewed by Striedter, 2005). The gross anatomy and architecture of the cerebellum has been well detailed in the literature (e.g., Eccles et al., 1967; Smeets et al., 1983; Smeets, 1998; Pose-Mendez et al., 2013) and reviewed by New (2001) and Montgomery et al. (2012). Briefly, the cerebellum is comprised of a dorsally positioned, unpaired corpus and the vestibulolateral cerebellum. In the corpus, four main histological layers can be distinguished across gnathostomes (Paul, 1982; Smeets, 1998; De Schutter et al., 2000): (i) the outer molecular layer (composed of stellate cells and an organized group of parallel fibers), (ii) the Purkinje cell layer, which varies in cellular thickness between 1 and 2 layers although are scattered throughout the cerebellum in holocephalans (Smeets et al., 1983), (iii) a fiber zone, and (iv) the innermost granular layer, including mossy fibers, Golgi cells, and granule cells (Kappers et al., 1936; Paul, 1982; Hofmann, 1999; De Schutter et al., 2000). Morphologically, the corpus cerebellum varies substantially in size, convolution, and symmetry among species (Northcutt, 1978; Puzdrowski and Leonard, 1992; Yopak et al., 2007, 2010b; Lisney et al., 2008; Yopak and Montgomery, 2008; Ari, 2011; Montgomery et al., 2012; Yopak, 2012b) (Fig. 2.7). The vestibulolateral cerebellum is further subdivided into a medial portion (often called the “lower lip”), which is associated with the vestibular system, and bilaterally paired lateral portions, often termed the “auricles” (Kappers et al., 1936; Paul, 1982; Roberts, 1988). These “auricles” join with the lower lip at one end and with the cerebellum-like structures of the medulla oblongata at the other end, which are comprised of the granule cell populations that supply parallel fibers to the medial (MON) and dorsal (DON) octavolateralis nuclei (Koester and Boord, 1978; Schmidt and Bodznick, 1987), and will be described in more detail in the next section. These cerebellum-like structures are proposed to be the evolutionary antecedent of the cerebellum (Johnston, 1902; Bell et al., 2008; Montgomery and Bodznick, 2010; Montgomery et al., 2012). The cerebellum and its function across all vertebrates has been an area of considerable debate and speculation (for comprehensive reviews, see Cordo et al., 1997; New, 2001; Highstein and Thach, 2002; Montgomery and Bodznick, 2010; Porrill et al., 2013; Baumann et al., 2014), although it is generally agreed that this structure is responsible for carrying out an effective regulation of motor control. In fishes, there is behavioral evidence for the cerebellum’s role in modulation of motor programs and body positioning (Paul and Roberts, 1977, 1979, 1981, 1990; Roberts et al., 1992; New, 2001), self-motion error correction (Montgomery et al., 2002), and dynamic state estimation for coordination of target tracking and the

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analysis of the consequences of an organisms’ own movements (Paulin, 1993, 1997, 2005). Comparative anatomical work on cartilaginous fishes has suggested the size of this area relative to the rest of the brain may be linked to habitat dimensionality, agile prey capture (Northcutt, 1978; New, 2001; Yopak et al., 2007; Lisney et al., 2008), proprioception, and sensory acquisition (Yopak and Frank, 2009). The morphological similarities between the cerebellum and the DON have led to the suggestion that there may exist a common functional algorithm between the two (Devor, 2000; Bell et al., 2008; Montgomery and Bodznick, 2010; Montgomery et al., 2012), but this has yet to be confirmed. 9.1.6. Medulla Oblongata The medulla oblongata is the most caudal component of the hindbrain, acting as a relay station between the brain and spinal cord (Northcutt, 1978; Smeets et al., 1983; Hofmann, 1999). This structure receives primary projections from the octavolateralis senses, which include the acoustic and vestibular system, electroreceptors, and mechanoreceptive lateral line (Smeets, 1998), and processes motor and sensory information from the trigeminal, facial, octaval, glossopharyngeal, and vagal nerves (Smeets et al., 1983; Striedter, 2005). The medulla oblongata is comprised of many discrete subsections and sensor-motor nuclei, including the somatic motor nuclei, visceral sensory nuclei, reticular formation, somatic sensory nuclei, and octavolateralis nuclei (reviewed by: Smeets et al., 1983; Smeets, 1998), but this structure will primarily be discussed in terms of the octavolateralis areas. Neural pathways and architecture of the cerebellar-like hindbrain in fishes have been well studied and documented (Bodznick and Boord, 1986; Schmidt and Bodznick, 1987; Bell et al., 1992; Conley and Bodznick, 1994; Hjelmstad et al., 1996), with only basic detail provided here. The cerebellum-like structures are located on the laterodorsal wall of the hindbrain in cartilaginous fishes and are comprised of electroreceptive areas, and regions receiving lateral line, acoustic. and vestibular input (Hofmann, 1999; Bell, 2002), which are analogous to the dorsal cochlear nucleus of mammals (Montgomery et al., 1995a,b). These structures include the DON and the MON, which derive their “cerebellum-like” name from the presence of a molecular layer of parallel fibers and inhibitory interneurons, which has striking organizational similarities to the molecular layer of the cerebellar cortex (Bell, 2002; Montgomery and Bodznick, 2010; Montgomery et al., 2012). The DON, found in lampreys and cartilaginous fishes (Montgomery et al., 1995a,b, 2012; Bell and Maler, 2005), is the site for central termination of primary electrosensory afferents. The receptor cells of each ampullae of Lorenzini are innervated by five afferent nerve fibers, which project to the

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DON, in addition to other octavolateral afferents (Montgomery et al., 1995a,b; Bell et al., 1997; Bell, 2002) via the dorsal branch of the ALLN (Bell and Maler, 2005), similar to the electrosensory lateral line lobe in some teleosts (e.g., Bell and Szabo, 1986a,b). In the elasmobranch brain, electrosensory afferents terminate somatotopically, forming a spatial map of the electroreceptors found sub-dermally (Bodznick and Northcutt, 1984; Bodznick and Boord, 1986; Bell, 2002), likely providing for efficient target location. Electrosensory information is aligned spatially with input from the visual field in the optic tectum (Bodznick, 1991; Hueter, 1990), while electrosensory information outside of the visual field, from the animal’s ventral surface, is mapped onto the lateral mesencephalic nucleus (Smeets, 1998). The MON is found in all aquatic vertebrates, with the exception of hagfishes (Bell, 2002) and receives the afferent nerves from the mechanosensory lateral line system as well as input from the spinal column and acoustic centers (Bodznick and Northcutt, 1980; Smeets et al., 1983; Schmidt and Bodznick, 1987; Bleckmann and Bullock, 1989; Puzdrowski and Leonard, 1993), as in teleost fishes (McCormick, 1981; Bell, 2002). Neuromasts within the lateral line on the head region are innervated by the ALLN and along the body axis and caudal fin by the posterior lateral line nerve (PLLN) (Koester, 1983; Northcutt, 1989; Puzdrowski and Leonard, 1993). Similar to the DON, primary afferents from the ALLN and PLLN terminate somatotopically in different locations in the MON (Bodznick and Northcutt, 1980; Koester, 1983; Bleckmann et al., 1987), as reported in Raja (Bodznick and Northcutt, 1984), Dasyatis (Puzdrowski and Leonard, 1993), and Platyrhinoidis (Bleckmann et al., 1987), forming a specific spatial map of primary lateral line afferents. Lateral line patterns vary between species, especially amongst members of the Batoidea (Chu and Wen, 1979; Maruska and Tricas, 1998; Maruska, 2001), although it is as yet uncertain whether this is reflected in brain morphology (see Yopak, 2012b for review). 9.2. Assessing the Relative Importance of Each Sensory Modality It is expected that major brain areas will evolve, to a degree, independently in association with major sensory systems and that neural specializations will subsequently be reflected in adapted behaviors or enhanced cognitive capabilities (Barton et al., 1995; Barton and Harvey, 2000; de Winter and Oxnard, 2001), although the central nervous system is also developmentally constrained (Harvey and Krebs, 1990; Finlay and Darlington, 1995; Yopak et al., 2010b). Masai (1969) was one of the first to find correlations between brain morphology and behavior in elasmobranchs. Since then, neurobiologists have shown that relative brain size and the

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relative development of major brain structures are correlated with primary habitat and/or specific behavior patterns in chondricthyans (Bauchot et al., 1976; Northcutt, 1977, 1978; Kruska, 1988; Myagkov, 1991; Smeets, 1998; Hofmann, 1999; Ito et al., 1999; Puzdrowski and Gruber, 2009; Ari, 2011), even in phylogenetically unrelated species that share certain life-history characteristics (Yopak et al., 2007, 2014b; Lisney et al., 2008; Yopak and Montgomery, 2008; Yopak and Frank, 2009; Mull et al., 2011; Yopak, 2012b). 9.3. Encephalization Allometric relationships between brain size and body size have now been established for most vertebrate taxa (reviewed by Striedter, 2005; Willemet, 2013), including cartilaginous fishes (Crile and Quiring, 1940; Bauchot et al., 1976; Northcutt, 1977, 1978; Demski and Northcutt, 1996; Yopak et al., 2007; Lisney et al., 2008; Ari, 2011; Mull et al., 2011; Yopak, 2012b). These studies have demonstrated that cartilaginous fishes have relative brain sizes that are comparable to most other vertebrate groups, including birds and mammals (Northcutt, 1977, 1978). A recent review by Yopak (2012b) across approximately 150 species of cartilaginous fishes found that, independent of both phylogenetic constraints and other inherent errors, brain mass increases with body mass in this group (a=0.50). This is in close concordance with other published allometric relationships between brain and body size for cartilaginous fishes (Northcutt, 1978; Demski and Northcutt, 1996; Yopak et al., 2007; Lisney et al., 2008; Yopak and Montgomery, 2008; Yopak and Frank, 2009; Mull et al., 2011) and are similar to those calculated for agnathans, birds, reptiles, and amphibians, which range from 0.5 to 0.6 (Jerison, 1973; van Dongen, 1998; Striedter, 2005; Salas et al., 2014). There is increasing evidence across vertebrates that larger brain sizes are associated with maternal investment in offspring (e.g., Iwaniuk and Nelson, 2003; Barton and Capellini, 2011; Mull et al., 2011; Tsuboi et al., 2014). Indeed, Mull et al. (2011) demonstrated that matrotrophic shark and rays have brains that are 20–70% larger than lecithotrophic species that do not provide investment beyond the yolk-sac, suggesting a strong impact of reproductive strategy on brain size evolution. Within chondrichthyans, early research demonstrated that relative brain size has increased independently among sharks and batoids and showed that galeomorphs and myliobatiforms tend to have larger brains than squalomorphs (Bauchot et al., 1976; Northcutt, 1977, 1978; Myagkov, 1991), a pattern that has been recently confirmed (Yopak, 2012b). Although it has been and continues to be highly contentious (e.g., Aboitiz, 1996; Lefebvre et al., 2004; Striedter, 2005; Deaner et al., 2007; Sol et al., 2007;

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Herculano-Houzel, 2009), it is a common assumption that encephalization (a larger than expected brain size for a given body size) reflects enhanced cognitive capabilities. Comparative studies of brain size have been greatly critiqued (for review, see Healy and Rowe, 2007) and to date there is no consensus regarding the best way to quantify life-history parameters and assess cognitive ability. Recent work has shown that large-brained guppies outperform small-brained individuals in a cognitive learning task, but produce fewer offsprings and have reduced gut size, which suggests a direct link between brain size and higher cognitive functions (e.g., Isler, 2013; Kotrschal et al., 2013), as well as the existing trade-off between cognitive benefits and energetic costs (Tsuboi et al., 2014). Although intraspecific studies are limited, links have been made between brain size variation and interpopulational differences in ecology in fishes (for review, see Gonda et al., 2013). From an ecological perspective, the cartilaginous fish species with the largest brains relative to body mass are chiefly found in reef-associated or oceanic habitats (Northcutt, 1977, 1978; Yopak et al., 2007; Lisney et al., 2008; Yopak and Montgomery, 2008; Yopak and Frank, 2009; Yopak, 2012b), as are the teleosts with the largest brains (Bauchot et al., 1977, 1989; Pollen et al., 2007; Shumway, 2008), which may reflect higher cognitive demands. In particular, the cognitive requirements for learning the complex spatial organization of a coral reef, in addition to the complex social behaviors and intra- and interspecific interactions that are often prevalent in reef habitats (Kotrschal et al., 1998; Bshary et al., 2002), might have influenced the evolution of brain size in chondrichthyans. One hypothesis asserts that highly encephalized animals engage in more strategic hunting, with behavioral innovations in the form of complex learning, tool use, and agile prey capture strategies, than do animals with small brains (e.g., Parker and Gibson, 1977; Lefebvre et al., 2004; Striedter, 2005). Although no formal investigation has yet been done in cartilaginous fishes, it has been shown that species with more passive predation strategies possess relatively small brains (Nilsson et al., 2000; Yopak and Frank, 2009), behaviors which might be less cognitively demanding in terms of sensory and/or motor requirements in comparison to more agile hunters (Kruska, 1988; Ito et al., 1999; Nilsson et al., 2000; Yopak et al., 2007). However, foraging strategies are clearly not the only factor influencing encephalization, as the planktivorous mantas and mobulids have among the largest brains across this Class (Fossi, 1984; Ari, 2011). Current research has shown that, despite their basal position, chondrichthyans are quite behaviorally complex, with learning (Clark, 1959, 1963; Aronson, 1963; Graeber, 1972; Graeber and Ebbesson, 1972a,b; Gruber and Schneiderman, 1975; McManus et al., 1984; Guttridge et al., 2009a,b; Guttridge and Brown, 2013; Schwarze et al., 2013) and adaptive

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capabilities (Montgomery, 1984; New and Bodznick, 1990; Bodznick and Montgomery, 1992), as well as complex social behaviors and dominance hierarchies (Springer, 1967; Myrberg and Gruber, 1974; Gruber and Myrberg, 1977; Klimley, 1985; Ritter and Godknecht, 2000; Guttridge et al., 2011). They not only have comparable brain/body mass ratios to birds and mammals (Bauchot et al., 1976; Northcutt, 1977), but comparable abilities when it comes to certain cognitive tasks (e.g., Schluessel and Bleckmann, 2005, 2012; Kuba et al., 2009; Kimber et al., 2014; Schluessel, 2014). Indeed, recent research has shown that cartilaginous fishes use cognitive maps to solve spatial tasks (Schluessel and Bleckmann, 2005), can use tools (Kuba et al., 2009), and can perceive subjective and illusionary contours (Fuss et al., 2014). Despite all of these advances in an understanding of elasmobranch cognition (reviewed by Schluessel, 2014), the lack of understanding of many aspects of elasmobranch cognition greatly hinders comparative analyses of brain morphology in these animals and there is clearly a need for more research on elasmobranch neuroethology. 9.4. Neuroecology In accordance with Jerison’s (1973) “principle of proper mass,” which states that the relative size of a brain region should reflect the relative importance of the neural function of that brain region, assessment of brain organization is often used as a neuroanatomical proxy for functional specialization. Current studies in chondrichthyans have used a variety of methods for assessing the size of specific brain regions in order to correlate these data with total brain size and social/ecological complexity (Yopak et al., 2010b; Yopak, 2012b). These methods include assessment of the mass of individual brain regions (Northcutt, 1977, 1978; Kruska, 1988; Yopak et al., 2007); the ellipsoid model, which assumes that each brain area approximates the volume of an idealized ellipsoid (Lisney and Collin, 2006; Yopak and Lisney, 2012); serial sectioning of brains and summing the areas and volumes of delineated brain regions (Yopak et al., 2007; Lisney et al., 2008; Yopak and Montgomery, 2008); and using advanced bioimaging to assess brain volumes (Pradel et al., 2009; Yopak and Frank, 2009; Yopak et al., 2010a). Most recently, it has been suggested that an increase in the proportion of neurons relative to non-neuronal cells, rather than mass, endows an animal with greater cognitive capacity (e.g., Herculano-Houzel et al., 2006, 2007), which has only just begun to be explored in sharks (Yopak et al., 2014a). By compiling data across these volumetric measures, laws for the scaling of various brain regions against total brain size in cartilaginous fishes have

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been determined (Yopak et al., 2010b, 2014b; Yopak, 2012b; Yopak and Lisney, 2012; Mull et al., 2011). A universal scaling law for vertebrate brains has been proposed, termed “late equals large,” wherein neural regions that cease neuronal proliferation later exhibit steeper allometric slopes than those “born” earlier (Finlay and Darlington, 1995; Reep et al., 2007; Finlay et al., 2010). Despite the great phylogenetic divergence between cartilaginous fishes and mammals, the allometric scaling of the major brain components in these two groups is startlingly similar, with the steepest slopes and strongest correlations occurring for the regions of the brain that are associated with behavioral and motor complexity (e.g., telencephalon and cerebellum), as compared to other neural regions that contain primary sensory and motor neurons (Yopak et al., 2010b). Similarly, the cerebral cortex in mammals increases at a disproportionately higher rate than other brain regions where, in general, larger brains are more and more dominated by cortex (Frahm et al., 1982). This conserved pattern of allometric scaling observed in sharks and mammals might reflect an important permissive innovation, affording the brain an “evolvable architecture.” Much like in computer architecture, principle functioning remains unchanged and it is the adding or subtracting of components that add computational power (Yopak et al., 2010b; Montgomery et al., 2012). Unlike most other major brain regions, however, the OBs do not conform to this universal scaling law that is shared from sharks through to mammals (Yopak et al., 2010b, 2014b) and, by not scaling as tightly with brain size as the other brain regions, maintain a level of statistical independence from the rest of the brain, similarly seen in bony fishes (Gonzalez-Voyer et al., 2009) and suggested for amphibians and birds (Charvet et al., 2011). There is a lack of consensus to explain this seemingly inherent variability in the size of the OBs in vertebrates, despite the structural and mechanistic similarities in the olfactory system across taxa, although it has been related to function and/ or sensitivity in cartilaginous fishes (Northcutt, 1978; Lisney et al., 2007; Schluessel et al., 2008; Yopak et al., 2010b, 2014b), decoding and map patterns of odorants for the purpose of spatial navigation (Jacobs, 2012; Yopak et al., 2014b), and/or a tighter coupling with more highly interconnected regions of the CNS (Finlay et al., 2011). 9.4.1. Commonalities in Brain Organization Irrespective of phylogenetic relationships, there is much variation in the absolute and relative size of major brain regions in cartilaginous fishes that is correlated with ecological parameters, which infers interspecific variation in functional capability and/or in the relative importance of different sensory systems. Sharks, batoids, and holocephalans occupy a wide range of ecological niches in the ocean. In the literature, these animals are often

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categorized based on primary lifestyle (benthic, benthopelagic, and pelagic) and primary habitat (bathyal, coastal, reef, coastal/oceanic, and oceanic) (Musick et al., 2004) that are then used to examine the correlatory relationships between ecology and brain organization (e.g., Yopak et al., 2007, 2014b). As these relationships have been recently reviewed (Yopak, 2012b), only general patterns of neuro-morphotypes will be described here (Fig. 2.8). For more detailed information and statistical analyses, please see original publications.

Figure 2.8. A stylized schematic, demonstrating the neuroecological trends in brain organization across sharks and batoids, grouped according to primary habitat and lifestyle. Structural enlargement (+) or recession ( ) of individual brain regions is based on generalized patterns of phylogenetically corrected residuals, which reflect interspecific variation in the relative size of these structures, collated from Yopak et al. (2007), Lisney et al. (2008), Yopak and Montgomery (2008), Yopak (2012b), Yopak and Lisney (2012), and Yopak et al. (2014b). Note that exceptions may exist. For specific values and data for individual species, see above publications. OBs, olfactory bulbs; Tel, telencephalon; TeO, optic tectum; Cer, cerebellum; Cl, cerebellum-like structures. Shark illustrations adapted from Last and Stevens (1994). Ecological illustration provided by T. Lisney. Representative brain: lemon shark, Negaprion brevirostris.

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Commonalities in the relative development of brain areas between groups of species that share certain common characteristics are termed “cerebrotypes” (Clark et al., 2001; Iwaniuk and Hurd, 2005). Although the extent to which cerebrotypes relate to phylogeny or ecology varies among taxa (Iwaniuk and Hurd, 2005), there are a number of cases where species that possess the same cerebrotype are also linked as a group by shared lifestyle similarities, such as habitat, feeding strategy, or cognitive capability. There is also some evidence for the existence of cerebrotypes in cartilaginous fishes (Yopak et al., 2007, 2012b, 2014b; Yopak and Montgomery, 2008; Yopak, 2012b), but unlike some previous studies on other vertebrate taxa (e.g., Huber et al., 1997; de Winter and Oxnard, 2001; Iwaniuk and Hurd, 2005) the relationships are not absolute (Yopak et al., 2007; Mull et al., 2011). The deep-sea represents an extreme habitat and the species that live at these depths are adapted to low temperatures, low light levels, high hydrostatic pressure, and a paucity of both prey and conspecifics (Marshall, 1979; Herring, 1987). Patterns of brain organization in chondrichthyan species found in the deep-sea reflect a habitat where vision is compromised. A deep-sea “cerebrotype” has been suggested for cartilaginous fishes (Yopak and Montgomery, 2008; Yopak, 2012b; Yopak et al., 2014b) and is characterized by a relatively small brain size; a clear relative hypertrophy of the termination sites of primary projections from the octavolateralis senses, the DON and MON (Yopak and Montgomery, 2008; Kajiura et al., 2010; Montgomery et al., 2012; Yopak, 2012b), and a reduction in the size of the optic tectum (Yopak and Lisney, 2012). Further, deep-sea species possess large OBs, irrespective of whether they have a benthic, benthopelagic, or pelagic lifestyle. This apparent increase in the importance of chemoreception and a decrease in the importance of vision in association with increased depth is also found in bony fishes (Eastman and Lannoo, 1998; Kotrschal et al., 1998; Wagner, 2001a,b). Interestingly, comparisons have been made between the environmental constraints on deep-sea sharks versus terrestrial nocturnal carnivores, where the challenges faced between these seemingly disparate groups may be quite similar (Jacobs, 2012). It is possible that the range of spatial scales, across which cartilaginous fishes in the deep-sea must localize prey, and conspecifics, with the reduced effectiveness of vision, has led to an increase in the size of the OBs, DON, and MON in this group. In contrast, reef-associated habitats are both visually and spatially complex. The species that dwell in these reef-associated habitats often have relatively large brains, with large telencephala (Yopak et al., 2007), large optic tecta (Yopak and Lisney, 2012), and relatively reduced OBs (Yopak et al., 2010b, 2014b). Correlations between telencephalon size (and indeed total brain size) and behaviors associated with cognitive abilities, such as

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social and spatial complexity, have been documented within and across the chondrichthyan clade. A relatively enlarged telencephalon, as reported in members of the Carcharhinidae, Sphyrnidae (Yopak et al., 2007), Dasyatidae, and Myliobatidae (Lisney et al., 2008; Ari, 2011), has been associated with species that live in complex habitats and interact socially (Kotrschal et al., 1998; Striedter, 2005). Many of these species, such as Carcharhinus, Neotrygon, and Himantura, and some coastal-oceanic species such as Galeocerdo and Sphyrna are also associated with reefs (Yopak, 2012b), with a high potential for multifaceted social behavior (Klimley, 1985). This provides evidence for a reef-associated cerebrotype, whereas increases in the relative size of the brain and the telencephalon are associated with complex environments in chondrichthyans, a situation found in many other vertebrates (Riddell and Corl, 1977; Huber et al., 1997; Striedter, 2005; Pollen et al., 2007; Shumway, 2008). Additional evidence for a reefassociated cerebroype includes the shared characteristics of relatively small OBs (Yopak et al., 2014b) and enlarged optic tecta, which has been linked to the visual demands of highly complex reef habitats (Yopak and Lisney, 2012). Many reef-dwelling fish species similarly have well-developed visual systems and enlarged optic tecta (Munz and McFarland, 1977; Collin and Pettigrew, 1988a,b; Bauchot et al., 1989; Ridet and Bauchot, 1990; McFarland, 1991b; Losey et al., 2003) and small OBs in comparison to other fishes (Bauchot et al., 1989; Ridet and Bauchot, 1990). Oceanic, epipelagic environments (0–200 m depth) represent one of the clearest aquatic habitats (Warrant and Locket, 2004), and pelagic predatory fishes, including sharks, have well-adapted visual systems for hunting agile prey in these habitats (Munz and McFarland, 1977; Fritsches et al., 2003a,b; Lisney et al., 2012). The largest optic tecta are documented in pelagic coastal/oceanic and oceanic sharks, such as Isurus, Carcharodon, Prionace, and Alopias (Fig. 2.8) (Yopak and Lisney, 2012). Species such as these have the absolutely and/or relatively largest eyes among the chondrichthyans and are assumed to rely heavily on vision (Lisney et al., 2007). Generally, chondrichthyan species that dwell in pelagic or coastal pelagic habitats also possess a relatively large, complex cerebellum (Yopak et al., 2007; Ari, 2011) and a relatively reduced medulla oblongata (Kajiura et al., 2010; Yopak, 2012b). Coastal pelagic species, such as the tiger shark (Galeocerdo cuvier) and the great white shark (C. carcharias) also have large OBs, a characteristic that differentiates this group from the brains of true oceanic species, where the OBs are relatively reduced (Yopak et al., 2014b). Although further work is critical, it is interesting that some of the largest OBs are found in the more migratory cartilaginous fishes that occur coastally but often cross large ocean basins, which supports the suggestion that the olfactory system is selected for decoding and mapping patterns of

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odorants, land-marking, and linking locations in olfactory space for both short and long-distance navigation (Jacobs, 2012; Yopak et al., 2014b). Recent work has shown the important of olfaction in short-distance navigation and homing in sharks (Gardiner et al., 2014a,b; Nosal and Hastings, 2014), but its direct role in long distance navigation is still in question. In addition to variation in size, the surface of the cerebellar corpus varies greatly in its degree of folding (termed foliation) (Yopak et al., 2007; Lisney et al., 2008). Foliation has been suggested to be an identifying feature of highly encephalized brains in chondrichthyans (Yopak et al., 2010b) and an increased cerebellar surface area (via an increase in cerebellar foliation) may allow for more specific representations of sensory and motor components from the body surface, as in the mammalian cortex (Carlson, 1991). Studies on foliation in chondrichyans revealed a correlation between the size and complexity of the cerebellum and ecological parameters, such as activity levels, habitat dimensionality, and behavioral specializations (Lisney and Collin, 2006; Yopak et al., 2007; Lisney et al., 2008; Yopak and Frank, 2009) and may vary ontogenetically (Yopak and Frank, 2009). There is a clear trend towards higher levels of foliation occurring in species occupying reef and oceanic habitats, such as Isurus, Sphyrna (Yopak et al., 2007), Dasyatis (Lisney et al., 2008), and Mobula (Ari, 2011) and previous studies have attributed this characteristic to highly active and/or manoeuvrable predation strategies (Yopak et al., 2007; Lisney et al., 2008). However, high levels of foliation were also reported in Rhincodon typus, and it has been suggested that foliation of the cerebellar corpus might reflect habitat dimensionality and a level of proprioception to a greater extent than previously thought (Yopak and Frank, 2009). In contrast, low levels of foliation are observed in less active benthic and bathyal benthopelagic species, such as Raja (Northcutt, 1978; Lisney et al., 2008), Cephaloscyllium (Yopak et al., 2007), and Hariotta (Yopak and Montgomery, 2008) and are potentially related to more passive predation strategies (Yopak and Montgomery, 2008) and a close association with the substrate (Northcutt, 1978; New, 2001). It has been reported that the number of cerebellar folia increases with both absolute and relative cerebellar size in chondrichthyans (Yopak et al., 2010b). Therefore, as in the bird cerebellum and the mammalian cortex (Ridgway and Brownson, 1984; Zilles et al., 1988, 1989; Striedter, 2005; Iwaniuk et al., 2006, 2007; Hall et al., 2013), the degree of folding in the shark cerebellum appears to be a morphological signature of relative brain size and is associated with greater behavioral complexity. As well as the neuroecological relationships described here, the relative size of the major brain regions are known to change ontogenetically postpartum in cartilaginous fishes, showing changes in relative size from small

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juveniles to adults (Lisney et al., 2007). These changes in brain organization with ontogeny may be correlated with shifts in diet and habitat and the sensory requirements for those developmental stages, as has been documented in a number of teleost fishes (Brandsta¨tter and Kotrschal, 1990; Montgomery and Sutherland, 1997; Wagner, 2003), although these relationships are currently poorly understood in cartilaginous fishes and require far more investigation.

10. PERSPECTIVES ON FUTURE DIRECTIONS In order to understand fully the sensory strategies used by cartilaginous fishes for survival, we must first understand the environmental signals (natural and anthropogenic) that play an important role in feeding, predator avoidance, finding mates, migration, movement patterns, communication, the formation of aggregations, and social interactions. Unfortunately, accurate measurement of environmental cues and concomitant observations of natural behaviors are rare for any one species of elasmobranch, although sensory profiles are being developed for some model species (the blacktip shark, C. limbatus; the bonnethead, Sphyrna tiburo; and the nurse shark G. cirratum, Gardiner et al., 2014a,b) with respect to the relative importance of different senses during the various phases of hunting. It is also becoming clear that there are large interspecific differences in sensitivity to environmental signals according to both ecological and phylogenetic influences. Therefore, future studies should optimally integrate field studies of natural behaviors using videography, satellite-linked archival tracking, the use of data-logging tags, and sensor array studies (Sims, 2010) in combination with in situ measurements of environmental parameters and phylogenetic statistics. These approaches, together with sensory profiling with respect to sensitivity thresholds and range, will ensure a more comprehensive understanding of the behavior or elasmobranchs. Correlating sensitivity thresholds for different sensory modalities with behavior may also aid in managing the sensory environment of cartilaginous fishes in their natural environment, in captivity (for public display and in aquaculture), alleviating fishing pressures on target species (recreational and commercial, Robbins et al., 2006; Jordan et al., 2009), and the future development of more effective attractants and repellents (Hart and Collin, 2015). Despite the important role cartilaginous fishes play in aquatic ecosystems, their numbers are declining globally due to a range of factors including non-targeted fishing pressures, the human consumption of their

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fins, the need to protect beaches and popular recreational areas for tourism, and the sale of jaws and other ornamental appendages.

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3 ELASMOBRANCH GILL STRUCTURE NICHOLAS C. WEGNER

Introduction Overview of the Elasmobranch Gill Evolution of the Gill: Elasmobranch Gill Structure in Relation to Other Fishes Elasmobranch Versus Teleost Ventilation Details of the Elasmobranch Gill 5.1. Gross Morphology – Unique Features 5.2. Gill Vasculature 5.3. The Gill Epithelium 6. Diversity in Elasmobranch Gill Dimensions and Morphology 6.1. Gill Arches 6.2. Gill Morphometrics 6.3. Theory on Elasmobranch Gill Dimensions and Limits to Gill Diffusion Capacity 6.4. Scaling 6.5. Adaptations for Fast Swimming 6.6. Adaptations for Hypoxia 6.7. Adaptations for Freshwater 6.8. Adaptations for Feeding – Gill Rakers 7. Conclusions 1. 2. 3. 4. 5.

As in other fishes, the gills of elasmobranchs are a critical interface between the internal and external environments and play vital roles in gas exchange, ion and pH balance, and the excretion of nitrogenous waste. Although the functional unit of the fish gill (the gill filament) has remained structurally and functionally intact throughout the course of fish evolution and diversification from lampreys to teleosts, the elasmobranch gill has a number of largely unique features. Perhaps most notably is the connection of the gill filaments to interbranchial septa, which affects not only the flow of water through the gills, but may provide a number of specific advantages and disadvantages to elasmobranch respiration. This chapter discusses both the structural similarities and differences of the elasmobranch gill in comparison to other fish groups and describes the breadth of structural 101 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00003-1

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branchial diversity within elasmobranchs, ranging from deep-water sharks and rays with six or seven pairs of gill arches to surface-oriented giants that use specialized gill rakers to sieve micro-sized prey out of the water.

1. INTRODUCTION Due to its multiple functions in gas exchange, ion and pH balance, and nitrogenous waste excretion, many comparative physiologists consider the fish gill as one of the most complex animal organs. This chapter focuses on the structure of the elasmobranch gill, which in a volume dedicated to the physiology of sharks, rays, and skates, provides needed insight into various life-sustaining processes that are discussed in other chapters. While the origin of the term “elasmobranch” (which is derived from their unique gill morphology) dates back to at least the 1870s, and the description of shark gills goes back much further, it was not until the second half of the twentieth century that many aspects of the elasmobranch gill were understood. Indeed, arguments persisted into the 1970s as to the basic path of ventilatory water over the respiratory surfaces, and the elasmobranch gill circulation was not well studied until the 1980s. Only in recent years have we begun to understand the functional role of the gill in the exchange of ions between the blood and the water. In comparison to the gills of teleosts, much less is still known about elasmobranch gill structure and function. This chapter synthesizes the available knowledge on elasmobranch gill structure and morphology, building off of previous reviews (Butler and Metcalfe, 1988; Butler, 1999) and highlights needs for areas of future research.

2. OVERVIEW OF THE ELASMOBRANCH GILL A series of detailed schematics of elasmobranch gill morphology, from an overview of the entire branchial apparatus down to the fine structure of the respiratory surfaces, is presented in Fig. 3.1. This figure identifies most of the structural and morphological components of the gills and ventilatorystream pathway and is thus meant to serve as a reference or guide throughout the chapter. Literally translated from its Greek roots, “elasmobranch” means “strap” or “plate gill” which refers to the unique attachment of the gill filaments to a platelike interbranchial septum that extends from each gill (=branchial) arch in the posterior-lateral direction (lateral view shown in Fig. 3.1A). In most elasmobranchs, there are five gill-bearing arches on each side of the

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Figure 3.1. Schematic overview of elasmobranch branchial morphology. (A) Enlarged lateral view of the anterior hemibranch of a single gill arch. (B) Ventral view (looking toward the roof of the orobranchial cavity) of a frontal cross-section through the branchial region showing the relationship of the oro- and parabranchial cavities and gills. (C) Lateral view of the main skeletal elements of the gill arch. (D) Dorsal view of an elasmobranch showing the relative position of the spiracles. (E) Magnified cross-section of two gill holobranchs from the dashed box in (B) showing the positioning of the interbranchial septum, gill filaments, and lamellae. (F) Enlarged view of box in (E) showing a cross-section through two gill filaments and the pathway of water past the gill lamellae and into the septal channels. (G) Cross-section through three gill lamellae from (F) showing the blood channels formed by pillar cells. (H) Magnified view of dashed box in (G) showing the details of the lamellar blood channels and gill epithelium. ABA, afferent branchial artery; AFA, afferent filament artery; EBA, efferent branchial artery; EFA, efferent filament artery; IMC, inner marginal channel; MRC, mitochondrion-rich cell; RBC, red blood cell. Drawings based largely on or modified from Daniel (1934), Kempton (1969), Mallatt (1984), Palzenberger and Pohla (1992), and Wegner (2011).

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Figure 3.1. (Continued)

orobranchial cavity (frontal plane cross-section shown in Fig. 3.1B) with an arch-like row or stack of filaments (termed a hemibranch) on each exposed side of each septum (Fig. 3.1A shows the anterior hemibranch of a single arch). For the first gill-bearing arch (hyoid arch) there is only a single posterior facing hemibranch, while on arches 2–5 there is usually both an anterior and posterior hemibranch (together termed a holobranch) on each side of the septum (Fig. 3.1B). The blade-like gill filaments of each hemibranch are attached to the interbranchial septum for the majority of their lengths with just their tips extending off the septum in order to approximate the filament tips of the

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opposing gill arch (Fig. 3.1A, B, and E). This approximation of the filament tips creates a general sieve or curtain through which the ventilatory stream must pass (Fig. 3.1B and E). Water flows from the orobranchial cavity (medial and anterior to the gill sieve) through the gill filaments and into parabranchial cavities, which are formed by the extension of the fleshy interbranchial septa past the filament tips to the lateral edge of the body (Fig. 3.1B and E). Here the septa [composed of muscular and connective tissue and supported by a number of cartilaginous rays emanating from each gill arch (Fig. 3.1C)] form the gill flaps, between which are the easily recognized gill slits characteristic of all elasmobranchs (Fig. 3.1A, B, D, and E). As in most other fishes, each side of each elasmobranch filament supports a row of lamellae, which have a flat, plate-like morphology (Fig. 3.1F) that provides a large surface area and short diffusion distance for effective gas exchange between the blood and water. Blood flow through the lamellae is generally in the opposite direction of the ventilatory water stream (Fig. 3.1F), thereby creating a counter-current loading mechanism that is effective at allowing a high proportion of dissolved environmental oxygen to diffuse into the blood stream. Pillar cells, which extend across the blood lumen and connect the respiratory epithelium on either side, direct the flow of blood through the lamellae (Fig. 3.1G and H). The lamellar water–blood barrier is typically composed of one to three layers of epithelial cells, a basement membrane, and the flanges of pillar cells that form the inner lining of the blood lumen wall (Fig. 3.1H). In many species, the lamellar epithelium may contain specialized epithelial cells such as mitochondrion-rich cells (MRCs) (involved in ion and pH balance) or goblet cells (involved in mucus production); however, these specialized cells are necessarily large and thus, in most elasmobranchs (and other fishes), are usually found in greatest density within the nonrespiratory filament epithelium (Fig. 3.1G and H).

3. EVOLUTION OF THE GILL: ELASMOBRANCH GILL STRUCTURE IN RELATION TO OTHER FISHES In order to best understand how the elasmobranch gill is both specialized and potentially limited, a basic overview of the evolutionary history of the gill and its basic structure in other fish groups is useful. There are numerous reviews on comparative aspects of gill morphology and respiration from hagfishes to teleosts (see Hughes, 1984; Wilson and Laurent, 2002; Evans et al., 2005; Graham, 2006). Fish gills are generally thought to be derived from a series of paired pouches on the lateral walls of the pharynx that open externally to slits. Based

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Figure 3.2. Stylized renderings of the branchial region for a(n) (A) lamprey, (B) elasmobranch, (C) holocephalan, and (D) teleost. (A, C, and D) are frontal cross-sections for comparison with that of an elasmobranch in Fig. 3.1B. (B) is a lateral view of the gill arch and jaw skeletal elements for an elasmobranch. Arches are labeled as mandibular (M), hyoid (H, 1) or by number. BC, branchial cavity; E, esophagus; GA, gill arch; H, hemibranch; IS, interbranchial septum; LGA, lateral gill arch; O, operculum. Drawings based on or modified from Hildebrand and Goslow (2001) and Randall et al. (2002).

on the morphology of protovertebrates (e.g., amphioxus), gill slits likely originally evolved for filter feeding with cilia moving water through the pharynx to collect particulates to be ingested. Presumably, as these basal chordates increased in size and the pharyngeal pouches became more pronounced and involved in respiration, epithelial folds developed to increase the surface area available for gas exchange. The most basal fishes, hagfishes (Order Myxiniformes), have a series of well-developed branchial pouches on either side of the pharynx (5–14 depending on the species) that are lined with extensive epithelial folds for gas transfer: the most primitive fish gill. The lampreys (Petromyzontiformes), which have seven paired branchial pouches, have a gill morphology generally similar to that of elasmobranchs and higher fishes with distinct hemibranchs on the anterior and posterior face of each gill pouch bearing filaments with lamellae that are similar in shape, structure, and orientation to other fishes (Fig. 3.2A). The fleshy tissue (=interbranchial septum) between successive gill pouches is hourglass shape in frontal cross-section (rather than “plate-like” as in elasmobranchs), and

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thus lampreys retain pouch-like chambers similar to hagfishes (Fig. 3.2A). However, unlike hagfishes, lampreys have a pronounced skeletal support system with a cartilaginous branchial arch located lateral to each hemibranch (Fig. 3.2A); this laterally-located arch is likely homologous to the extrabranchial cartilages in elasmobranchs that run along the lateral borders of the interbranchial septa (Hughes and Morgan, 1973; Mallatt, 1984) and provide rigidity to the parabranchial cavities (Fig. 3.1C and E). This rigidity is important for the expansion of the parabranchial cavities during elasmobranch ventilation (Hughes and Ballintijn, 1965). In elasmobranchs (and other jawed fishes), the septa and gills are supported by branchial arches located medial to the gills (Figs 3.1A–C, E and 3.2B–D). Each arch is typically composed of four cartilaginous segments, termed from dorsal to ventral: pharyngobranchial, epibranchial, ceratobranchial, and hypobranchial (Figs 3.1C and 3.2B) with the epiand ceratobranchial typically forming the arch that bears gill filaments and with the pharyngo- and hypobranchial anchoring the arch to the roof and floor of the orobranchial cavity. The jaws of elasmobranchs and higher fishes (the agnathans, hagfish and lampreys, lack jaws) are generally thought to be derived from branchial arches that migrated forward for use in prey capture and manipulation, with the epibranchials and ceratobranchials of the mandibular arch forming the upper and lower jaws respectively and the hyoid arch moving forward to provide added support (Fig. 3.2B). The remnant of the dorsal gill slit between the mandibular and hyoid arches forms the spiracle (Fig. 3.2B), which persists in many benthic elasmobranchs (especially rays and skates) and a few primitive bony fish lineages and allows for the inspiration of water into the orobranchial cavity through openings on the dorsal-lateral surface of the head (Fig. 3.1A, B, and D) when the mouth is buried in the substrate or engaged in prey manipulation. In many species, the remnant of the posterior hemibranch of the mandibular arch (known as the pseudobranch) still exists on the dorsal lateral surface of the orobranchial cavity. The posterior hemibranch of the hyoid arch also persists in elasmobranchs and some primitive bony fishes and in many texts (including this chapter) is referred to as the first gill arch or the first arch bearing true gills (the “pseudobranch” literally meaning “false gill”). In elasmobranchs the interbranchial septum of each gill arch extends to the lateral edge of the body to form the gill flaps and gill slits (Fig. 3.1A, B, and E). In both holocephalans (=chimaeras, Order Chimaeriformes) and bony fishes, the interbranchial septa separating the gill pouches are reduced, which results in a single large branchial (opercular) cavity on either side of the buccal cavity containing all the gill hemibranchs (Fig. 3.2C and D). With reduced septa, the gills are protected laterally by a fleshy extension of the hyoid arch (chimaera) or a bony operculum

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(bony fish) [these two types of protective coverings are not homologous (Hughes and Morgan, 1973)]. For chimaeras and a few basal bony fishes, the interbranchial septum extends out to or near the tips of the filaments (Fig. 3.2C), while in most teleosts the septum has been reduced to just near the origin of the filaments near their attachment to the gill arch (Fig. 3.2D). The filaments in teleosts are thus not bound to the septum for most of their length, and this has implications for both gill rigidity and the flow of water past the respiratory surfaces in comparison to the “strapped” gill configuration of elasmobranchs. 4. ELASMOBRANCH VERSUS TELEOST VENTILATION The major biomechanical features of gill ventilation are generally consistent within jawed fishes and have been well studied in both elasmobranchs and teleosts (see for review Brainerd and Ferry-Graham, 2006; Wegner and Graham, 2010). Water typically enters the orobranchial cavity (elasmobranchs) or buccal cavity (bony fishes) through the mouth and or spiracles and is forced through the gills using a dual pumping mechanism (Hughes, 1960a,b). This includes a “force” pump (associated with the expansion and compression of the orobranchial/buccal cavity), and a “suction” pump (created by the expansion of the parabranchial cavities/branchial cavities in bony fishes). Together, the use of these two pumps results in the flow of water over the respiratory surfaces that, although often highly pulsatile, is thought to be continuous or nearly continuous in most fishes. However, some potential for back flow, or at least the stalling of flow, has been documented in some elasmobranchs (see for review Summers and Ferry-Graham, 2003). Some fishes (particularly those that are fast or continuous swimmers) are also capable of ram ventilation in which branchial flow is established via holding the mouth and gill slits ajar during forward swimming (Hughes, 1960b; Roberts, 1975). In this case, ventilatory flow past the gas exchange surfaces is generally constant (Brown and Muir, 1970; Wegner et al., 2012). In both active (pumping) or passive (ram) ventilation, water leaving the orobranchial (buccal) cavity is forced laterally between the gill arches (sometimes referred to as gill bars) where it must turn to enter the interlamellar spaces where gas exchange occurs (Figs 3.1–3.3). In elasmobranchs, water that passes through the interlamellar channels encounters the interbranchial septum and must thus subsequently turn and follow septal channels (Fig. 3.3A and B) along the length of the filaments until it enters the parabranchial cavities and exits at the gill slits. For bony fishes, the reduction of the interbranchial septum allows water to pass through the interlamellar spaces generally unimpeded (Fig. 3.3C and D).

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Figure 3.3. Simplified drawings of the elasmobranch (A and B) and teleost (C and D) gill. (B) and (D) are enlarged views of the boxes in (A) and (C) respectively. The path of water flow through the gills is indicated by arrows. From Wegner et al. (2012).

The strapping of the gill filaments to the interbranchial septum in elasmobranchs is potentially advantageous in providing added rigidity to the gills. Specifically, this morphological configuration would suggest that high branchial flow volumes are less likely to cause deformation of the filaments resulting in the shunting of water between adjacent filaments or opposing hemibranchs and causing a decrease in oxygen extraction efficiency. This may partially explain why a high proportion of elasmobranchs, including many generally benthic-oriented genera such as Triakis are capable of ram ventilation (Hughes, 1960b; Clark and Kabasawa, 1976). However, the interbranchial septum adds a site of resistance to water flow through the elasmobranch gill. Although the total pressure gradient establishing ventilatory flow across the gills (and consequently total gill resistance) is generally similar between elasmobranchs and bony fishes during both active and ram ventilation (Hughes, 1960a,b; Brown and Muir, 1970; Wegner et al., 2012), Wegner et al. (2012) calculates that in the shortfin mako, Isurus

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oxyrinchus, up to 80% of the gill resistance results from flow through the septal channels. To compensate for this added resistance, elasmobranchs appear to have generally larger interlamellar spaces than bony fishes and consequently fewer lamellae per unit of filament length. This lower number of lamellae may impose limits to elasmobranch gill surface area and ultimately aerobic scope (Wegner et al., 2012) (see Section 6.3). 5. DETAILS OF THE ELASMOBRANCH GILL 5.1. Gross Morphology – Unique Features While a general overview is discussed above, there are several interesting and largely unique features of the elasmobranch gill that warrant additional description, many of which are poorly studied and have largely unknown, or at least unverified, functions. As the ventilatory stream passes the gill arches, it encounters the gill filaments and lamellae where gas exchange occurs. In addition to the interbranchial septum that binds and reinforces the trailing (water-exit) filament edge, thin, fleshy extensions of the gill arch on each hemibranch bind adjacent filaments on the leading (water-entry) edge. This results in a “branchial canopy” that can cover anywhere from just 6–8 lamellae (Donald, 1989) to up to 15–20% of the filament length nearest the arch (Figs 3.1A and E and 3.4) (Cooke, 1980; Benz, 1984). Some researchers have suggested that this canopy (composed of a connective tissue core covered by epithelium) creates a ventilatory dead space (Cooke, 1980) that protects developing lamellae [new lamellae are added at the base of the filament near the gill arch (Acrivo, 1935b)]. However, the canopy does not bind to the lamellae and thus there is sufficient space for water to enter and perfuse the interlamellar spaces. Therefore, while the branchial canopy likely protects the gill lamellae closest to the gill arch from bouts of high inertial water flow and mechanical damage (as indicated by a longer canopy near the ceratoepibranchial joint where inertial flow is likely strongest), these lamellae are still likely irrigated with ventilatory flow as water follows a path from high to low pressure. [Note: Unfortunately, it is not always clear whether the lamellae beneath the branchial canopy are included in estimates of elasmobranch gill surface area. These lamellae are included in gill area estimates by Wegner et al. (2010b) and Wootton et al. (2015), and, based on the similarity of gill morphometric data collected for overlapping species, likely Emery and Szczepanski (1986).] As water passes the gill arch and branchial canopy it subsequently turns to flow between the lamellae of the gill filaments, which, in most fishes, are described as being perpendicular to the long-axis of each filament (Fig. 3.1E and F). Interestingly, several studies have reported that the lamellae of various

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Figure 3.4. Detailed schematic of a cross-section through the elasmobranch gill arch and interbranchial septum showing the gill filaments and lamellae and associated features. ABA, afferent branchial artery; EBA, efferent branchial artery; L, lamella. Modified from Cooke (1980).

elasmobranch species are positioned at a slight angle to this long-axis with the leading lamellar edge angled toward the orobranchial cavity, thus slightly into the ventilatory stream (Fig. 3.4) and it has been suggested that this may help facilitate flow into the interlamellar spaces (Kempton, 1969; Wright, 1973; Cooke, 1980). However, the scope of this slight angle and its effects (if any) on water entry into the interlamellar spaces have not been quantified. Elasmobranch lamellae are generally similar in shape to those of other fishes, typically with a semicircular or rectangular profile. However, elasmobranch lamellae differ in that they often possess distinct projections on the lateral leading edges that extend toward the orobranchial cavity (Fig. 3.5) (Cooke, 1980; Olson and Kent, 1980; Benz, 1984; De Vries and De Jager, 1984). Generally, these projections appear to be more pronounced and numerous in benthic elasmobranchs and to increase in number and size along the length of the filament (Fig. 3.5A) with up to five projections being reported on lamellae near the filament tip in some species (Cooke, 1980; Olson and Kent, 1980). Because lamellae on the filament tips are the oldest, Cooke (1980) suggested they might have an unknown function during early life stages. However, Olson and Kent (1980) observed a positive correlation of projections with body size in the spiny dogfish, Squalus acanthias, and the little skate, Leucoraja erinacea, and suggested that they might help direct flow into the interlamellar spaces. It seems likely that the increased size and

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Figure 3.5. Scanning electron micrographs of elasmobranch lamellae showing their projections toward the orobranchial cavity. (A) Vascular casts of the lamellae of the smallfin gulper shark, Centrophorus moluccensis, revealing the variation in the shape and number of projections of lamellae sampled from the tip, middle, and base (top to bottom) of a representative filament. Numbers in parentheses indicate the number of projections. (B) Vascular casts of the lamellar projections of the spiny dogfish, Squalus acanthias. (C) Critical-point dried tissue showing the lamellar projections of the shortfin mako, Isurus oxyrinchus and closely associated vascular sacs. (D) Critical-point dried gill tissue of I. oxyrinchus showing the extension of lamellar projections above the leading edge of the filament tips (*). IMC, inner marginal channel; IS, interbranchial septum; LFE, leading filament edge; OMC, outer marginal channel; P, projection; SC, septal channel; VS, vascular sac. Water flow past the lamellae is from left to right in A and B, from top to bottom in C, and indicated by the dashed line in D. Modified from (A) Cooke (1980); (B) Olson and Kent (1980); (C and D) Wegner unpublished.

number of projections on lamellae near the filament tips would be useful in helping to bridge the gap between both adjacent filaments on the same arch and opposing filaments on opposing hemibranchs, thus minimizing the shunting of water flow past the filament tips without encountering the respiratory surfaces. Support for such a function is suggested by Fig. 3.5D, which shows lamellar projections at the filament tips in I. oxyrinchus extending above the rest of the filament. In addition to a function in promoting more effective flow for gas exchange, there is also some suggestion that lamellar projections may help to promote lamellar stability. Vascular casting of the gill lamellae has shown the projections are perfused by a generally well-defined outer marginal

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blood channel (Fig. 3.5A and B), which often has a constricted diameter near the apex of the projections (Olson and Kent, 1980). The added length of the outer marginal channel associated with traveling along several projections as well as the restricted diameter at key locations could serve to increase blood flow resistance, thus creating a hydrostatic skeleton to increase lamellar stiffness. In addition, a thick layer of collagen surrounding the outer marginal channel has been reported in the small-spotted catshark, Scyliorhinus canicula, and likely provides additional support to the free lamellar edge (Wright, 1973). In pelagic sharks such as I. oxyrinchus and the blue shark, Prionace glauca, these projections on the water-entry edge of the lamellae are often more subtle, but are associated with a thicker epithelium that has been suggested as a means to increase lamellar rigidity for ram ventilation (Wegner et al., 2010b). In close proximity to the projections on the leading edge of the lamellae, at least some species have button-like bulges on either side of the lamellar surface that are aligned to abut bulges of adjacent lamellae (Figs 3.5C and 3.6). For S. acanthias, these bulges are described as being epithelial outgrowths (i.e., a thickening of the lamellar epithelium) (De Vries and De Jager, 1984), but in I. oxyrinchus and P. glauca, they result primarily from an increase in the diameter of the lamellar blood lumen (Fig. 3.6) and have been thus termed “vascular sacs” (Wegner et al., 2010b). Whether primarily epithelial or vascular in composition, the location of these bulges near the water-entry edge of the lamellae (Figs 3.4, 3.5C, and 3.6A) and a positive correlation of their abundance with lamellar size (Wegner, unpublished) suggests a function in ensuring lamellar stability and spacing (De Vries and De Jager, 1984; Wegner et al., 2010b). The vascular nature of these bulges in I. oxyrinchus and P. glauca suggests that vasoactive agents and changes in blood perfusion pressure could potentially influence sac size thereby modulating both lamellar rigidity and possibly the volume and speed of water passing through the interlamellar channels (Wegner et al., 2010b). Specifically, during bouts of increased activity, an increase in cardiac output and vasodilation could potentially distend the sacs thereby further stabilizing the lamellae and slowing a potentially fast and more forceful ventilatory stream. It is generally unknown if such epithelial or vascular bulges are species specific or a common elasmobranch feature simply not recognized or reported in many past studies. In addition to the species mentioned above, vascular sacs occur in all three thresher shark species (genus Alopias) (Wegner and Wootton, unpublished data), and a vascular sac appears present in the lamellar cast from a smallfin gulper shark, Centrophorus moluccensis from Cooke (1980) shown in Fig. 3.5A. In addition, Hughes et al. (1986) reported the presence of lamellar epithelial “thickened areas” for the nursehound, Scyliorhinus stellaris.

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Figure 3.6. Micrographs of vascular sacs on the lamellae of the shortfin mako, Isurus oxyrinchus. (A) Section through four adjacent gill filaments showing one to two vascular sacs on each lamella near the leading (water-entry) edge. (B) Scanning electron micrograph of a longitudinal section through the gill filament showing the lamellar vascular sacs. (C) Light microscope image of a longitudinal filament section showing the proximity of vascular sacs from adjacent lamellae and the increased thickness of the lamellar epithelium near the outer marginal edge. (D) Magnified image of dotted box in (C) showing the details of the lamellar vascular sacs filled with red blood cells and supported by large pillar cells. Water flow is indicated by the dotted arrow in (A) and is into the page in (B–D). CC, corpus cavernosum; F, filament body; IMC, inner marginal channel; IS, interbranchial septum; L, lamella; PC, pillar cell; SC, septal channel; TE, thick epithelium; VS, vascular sac. From Wegner et al. (2010b).

5.2. Gill Vasculature As with other fishes, the elasmobranch gill circulation has two main components or pathways: the respiratory vasculature (also referred to as the arterioarterial vasculature) and the nonrespiratory vasculature (also called the arteriovenous vasculature). The former provides blood to the respiratory lamellae for gas exchange and then proceeds to the systemic circulation for oxygen delivery to the tissues. The latter is a complex network that originates from the respiratory circulation and appears to have both

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nutritive and lymphatic-like drainage functions and serves most of the filament epithelium involved in ion and pH balance (Laurent, 1984; Butler, 1999; Olson, 2002). Several studies using microvascular casting and histological techniques have allowed for a detailed understanding of both components for a variety of elasmobranchs ranging from rays (Donald, 1989; Sherman and Spieler, 1998; Basten et al., 2011) and skates (Dunel and Laurent, 1980; Olson and Kent, 1980; Laurent, 1984) to benthic (Kempton, 1969; Wright, 1973; Cooke, 1980; Dunel and Laurent, 1980; Olson and Kent, 1980; De Vries and De Jager, 1984; Laurent, 1984; Metcalfe and Butler, 1986) and pelagic sharks (Wegner et al., 2010b). Despite the use of different nomenclatures by various researchers to describe like structures (Laurent, 1984), the elasmobranch gill vasculature is largely conserved between species. A schematic overview of both the respiratory and nonrespiratory circulation of the gill filament is given in Fig. 3.7 in comparison to scanning electron microscopy images of a vascular cast filament for I. oxyrinchus (Fig. 3.8) and S. acanthias (Fig. 3.9A). 5.2.1. Respiratory Vasculature Deoxygenated blood from the ventral aorta enters each gill arch through an afferent branchial artery that provides blood to the gill filaments via afferent distributing arteries (Figs 3.7 and 3.9A–C). Each distributing artery usually runs through the interbranchial septum for approximately one-third (range one-fifth to up to two-thirds) the length of the filaments to supply blood to one to four afferent filament arteries. Each afferent filament artery has two sections, a recurrent branch distributing blood to the basal section of each filament (closest to the arch), while a distal branch supplies the blood toward the filament tip. The recurrent and distal sections of each filament artery open at regular intervals to an extensive cavernous body (Figs 3.7, 3.8B and C, and 3.9A), with numerous collagen and elastic fiberbased trabeculae extending across its lumen, called the corpus cavernosum. The corpus cavernosum extends medially from the afferent filament artery into the filament body (Figs 3.7–3.9) where it generally occupies the position of the cartilaginous filament rod in the filaments of most bony fishes (Figs 3.1F, 3.4, and 3.6A); filament rods are not found in elasmobranchs. While some have suggested the corpus cavernosum plays a role in the hemolysis of aging erythrocytes (Acrivo, 1935a) and may also function as a pulse-smoothing capacitance vessel prior to blood entry into the thin-walled lamellae (Wright, 1973; De Vries and De Jager, 1984), these views have not been substantiated (Metcalfe and Butler, 1986; Butler, 1999), and it is now generally accepted that its main function is as a hydrostatic skeleton that provides rigidity to the gill filaments. Direct evidence for this was provided by De Vries and De Jager (1984) who artificially applied

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Figure 3.7. Schematic of the filament respiratory (white) and nonrespiratory (gray) circulation for a generalized elasmobranch. Dotted arrows indicate the direction of blood flow. ABA, afferent branchial artery; ACV, afferent companion vessel; ADA, afferent distributing artery; AFA, afferent filament artery; ALA, afferent lamellar arteriole; AS, arch sinus; AvA, arteriovenous anastomose; BCS, branchial canopy sinus; CC, corpus cavernosum; EBA, efferent branchial artery; ECV, efferent companion vessel; EFA, efferent filament artery; ELA, efferent lamellar arteriole; IL, interlamellar vessels; L, lamella. Modified from Donald (1989).

physiological blood pressures to the corpus cavernosum in situ and observed the erection of the filament tips away from the interbranchial septum to contact filament tips of the opposing hemibranch (the position normally observed in live animals). In many species the corpus cavernosum also extends laterally into the septal tissues on either side of the afferent filament artery (Figs 3.8B and 3.9A and C). These lateral extensions, which may serve as anchor points for the filament bound portion of the corpus cavernosum, are relatively short near the base of the filaments, but become much more pronounced near the filament tips where septal cavernosa from adjacent filaments often

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Figure 3.8. Scanning electron micrographs of vascular casts of the filament circulation from a shortfin mako, Isurus oxyrinchus. (A) Synoptic view of the gill filament circulation in the same orientation as that depicted graphically in Fig. 3.7. (B) Enlarged view of dotted box in (A) (upper right) with the interlamellar circulation removed to show the corpus cavernosum and its connections to the afferent filament artery (delineated by arrows). Also note the presence of the septal corpus cavernosum extending out of the page. (C) Magnified image of box in (B) showing both large and small connections of the afferent filament artery with the corpus cavernosum. (D) Enlarged image of dotted box in (A) (upper right) with the interlamellar circulation still intact. (E) Magnified image of dotted box in (D) showing the afferent lamellar arterioles leaving the corpus cavernosum and the interlamellar circulation running between the arterioles and underneath the lamellae. (F) Enlarged view of box in (A) (long dashes, upper left) showing the connection of the efferent lamellar arterioles to the efferent filament artery and the cast of a vascular sac on the efferent edge of a lamella. (G) Magnified image of box in (A) (short dashes, bottom middle) showing a nutrient vessel intertwined with the interlamellar circulation. (H) Enlarged view of (G). Water flow is from left to right in all images. ACV, afferent companion vessel; AFA, afferent filament artery; ALA, afferent lamellar arteriole; CC, corpus cavernosum; ECV, efferent companion vessel; EFA, efferent filament artery; ELA, efferent lamellar arteriole; L, lamella; IL, interlamellar vessel; OMC, outer marginal channel; SCC, septal corpus cavernosum; N, nutrient vessel; VS, vascular sac. Modified from Wegner et al. (2010b).

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Figure 3.9. Vasculature of the elasmobranch gill. (A) Scanning electron micrograph of a vascular cast gill filament from the spiny dogfish, Squalus acanthias. (B) Scanning electron micrograph of a cast of the first gill arch of the western shovelnose stingaree, Trygonoptera mucosa, showing the afferent circulation providing blood to the gill filaments. Note the presence of the vascular cascade connecting adjacent afferent filament arteries near the filament tips. (C) Light micrograph of an Indian ink injected gill arch of the small-spotted catshark, Scyliorhinus canicula, with the top hemibranch removed to show the afferent circulation of the underlying hemibranch. Note the interconnections of the septal corpus cavernosum (SCC) of adjacent afferent filament arteries near the filament tips. Other abbreviations: ABA; afferent branchial artery; ACV, afferent companion vessel; ADA, afferent distributing artery; AFA, afferent filament artery; CC, corpus cavernosum; EFA, efferent filament artery; FT, filament tip; GA, gill arch; IL, interlamellar vessels; IS; interbranchial septum; L, lamella; SS, septal sinus; VA, vascular arcade. Modified from (A) Olson and Kent (1980); (B) Donald (1989); (C) Wright (1973).

anastomose together (Fig. 3.9C). During exercise, increased blood pressure may thus not only increase the rigidity of the gill filaments, but may also increase the stiffness of the interbranchial septum. Interestingly, urolophid stingrays lack the septal portion of the corpus cavernosum, which appears to be replaced by or perhaps reduced to a single vessel-like “vascular arcade,” which connects the afferent filament arteries near the filament tips (Fig. 3.9B) (Donald, 1989; Sherman and Spieler, 1998; Basten et al., 2011). The lack of septal cavernosa in urolophids may correlate with their

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general inactivity, and hence a reduced need for a stiff interbranchial septum or septal-anchored filament cavernosa. Arising from the filament portion of the corpus cavernosum are short lamellar arterioles that provide blood to the respiratory lamellae (Figs 3.7 and 3.8E). Like most other fishes, blood flow through elasmobranch lamellae is thought to be sheet-like (Farrell et al., 1980), although the placement of the pillar cells running across the lumen often appears to delineate rough channels or preferred routes (Figs 3.5A and 3.8E). The outer marginal channel is particularly well defined, and, as mentioned previously, may have a hydrostatic functional capacity. In addition, one or more inner marginal channels are typically embedded within the body of the filament (Figs 3.1G and H, and 3.6D). Following gas exchange, oxygenated blood exits the lamellae via efferent lamellar arterioles that empty into an efferent filament artery (Figs 3.7, 3.8F, and 3.9A) that runs along the length of each filament and brings blood back to the gill arch (Fig. 3.7). Blood from the efferent filament arteries of each hemibranch is collected by a separate efferent branchial artery (thus with the exception of the first gill arch, which only has a posterior-facing hemibranch, there are two efferent branchial arteries per arch), from which it proceeds to the systemic circulation. 5.2.2. Nonrespiratory Vasculature Stemming from the respiratory circulation is the nonrespiratory or arteriovenous vasculature. The nonrespiratory vasculature is often subdivided into two parts: the interlamellar circulation (also referred to as the lymphatic-venous circulation) and the nutrient circulation, although this division is still equivocal (Laurent, 1984; Olson, 2002). The complex network of interlamellar vessels within the filament body (often termed the central venous sinus) comprise a low-pressure system that generally runs parallel to the inner margins of the lamellae (Figs 3.7, 3.8A, D–H, and 3.9A) and is thought to be closely associated with the filament epithelium where MRCs are present in high abundance (Olson and Kent, 1980; Laurent, 1984; Olson, 2002; Wilson and Laurent, 2002; Evans et al., 2005). Depending on the species, these vessels appear to receive blood from a combination of small anastomoses with the efferent filament artery (Fig. 3.7), efferent lamellar arterioles, and or corpus cavernosum. Intermingled with, but largely separate from the interlamellar or central venous sinus vessels are nutrient vessels that course through the filaments and interbranchial septa (Fig. 3.8G and H). The nutrient vessels appear to originate from the efferent filament and branchial arteries and drain into the interlamellar circulation. Within the filament, the interlamellar and some nutrient vessels drain into afferent and efferent companion vessels that run parallel to the afferent and efferent filament arteries (Figs 3.7, 3.8D and F, and 3.9A) (Note: afferent

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and efferent used here refer solely to their location in proximity to the afferent and efferent filament arteries and not to a function associated with gas exchange). Along their course toward the gill arch the afferent companion vessels often connect and drain into large sinuses within the interbranchial septum (Fig. 3.9A), while the efferent companion vessels may connect with sinuses within the branchial canopy (Fig. 3.7). Ultimately this low-pressure system empties into septal and gill arch sinuses that drain dorsally into the anterior cardinal sinus and ventrally into the inferior jugular sinus (De Vries and De Jager, 1984; Butler, 1999). 5.2.3. Gill Vasculature and Blood Shunting Early physiological studies on elasmobranch respiratory function showed highly variable gill O2 utilization and correlating variable dorsal aortic PO2 levels (e.g., Lenfant and Johansen, 1966; Piiper and Schumann, 1967; Grigg and Read, 1970), and Piiper and Schumann (1967) and others suggested this might be associated with the shunting of blood around the respiratory surfaces of the gills through the nonrespiratory circulation. Such shunting would indicate the ability of elasmobranchs to modulate blood flow through the gills to meet aerobic demands under different physiological conditions (e.g., exercise vs. rest), the benefit of which would allow for a decreased perfusion of the thin respiratory surfaces, and hence a decrease in passive ion movement between the blood and water (=reduced ionic regulatory costs) during bouts of relative inactivity. As a result, most of the early studies on elasmobranch gill vasculature examined the potential for nonrespiratory shunts of blood to bypass the respiratory exchange surfaces. Although the nonrespiratory interlamellar circulation in several species anastomoses with both the afferent and efferent respiratory vasculature, it is generally considered a distensible venolymphatic system, which is generally free of red blood cells and operates at pressures well below that of both the afferent and efferent filament arteries and is thus unable to serve as a physiological bypass. Rather than vascular shunts, it is now generally thought that ionic regulatory costs can be minimized during rest by regional changes in the distribution or perfusion of blood through the respiratory surfaces with large regions of the gills being essentially shutdown during rest and recruited during exercise. Regional changes in gill blood flow has been shown for several elasmobranchs (e.g., Satchell et al., 1970; Cameron et al., 1971) and is likely achieved through regional differences in vascular resistance, the use of sphincters (which are present at numerous locations throughout the gill vasculature), and changes in blood perfusion pressures induced by varying levels of cardiac output with activity (e.g., at reduced cardiac outputs, fewer lamellae would be perfused with blood). Variable oxygen extraction

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efficiencies and dorsal aortic PO2 values could also result from changes in ventilation – perfusion matching (Piiper and Scheid, 1984; Butler and Metcalfe, 1988; Bhargava et al., 1992) with the coordination in timing of the pulsatile blood and ventilatory flow increasing O2 uptake, and a mismatch decreasing utilization. However, such mismatches are unlikely to mitigate ionic regulatory costs and models suggest that in sedentary species such as S. stellaris, a mismatch in ventilation-perfusion timing has little effect on gas exchange (Malte, 1992). An interesting exception to the lack of true vascular shunts may be present in urolophid rays, in which some afferent filament arteries appear to be directly connected to their corresponding efferent filament artery at the filament tip (Donald, 1989; Sherman and Spieler, 1998). The extent to which blood flows through the filament tip and bypasses the respiratory exchange surfaces (and the extent to which this can be controlled) remains unknown and deserves additional study. For rays, such a bypass would be particularly useful as they are often at rest on the substrate and thus would only occasionally require additional capacity for increased O2 uptake. 5.3. The Gill Epithelium The gill epithelium is heavily involved in several life-sustaining processes. It provides both a barrier and a means of transport for molecules between the internal and external environments and is thus vital for homeostasis. Elasmobranch lamellar and filament epithelia are similar to those of other fishes and detailed comparative accounts can be found in reviews by Laurent (1984), Wilson and Laurent (2002), and Evans et al. (2005). The lamellar epithelium is typically composed of one to three layers of epithelial cells, with polygonal squamous pavement cells lining most of the apical (outer) surface (Figs 3.10 and 3.11). The surface of these cells typically have fingerlike microvilli or microridges that are thought to help anchor a mucous layer that provides protection from bacteria and other foreign materials, reduces gill drag (Daniel, 1981), and likely decreases the permeability of the epithelium to certain ions and other molecules (Hill et al., 2004). Subsurface to the pavement cells typically lie undifferentiated epithelial cells distributed over a basement membrane (=basal lamina) that separates the epithelium from the lamellar vasculature. Epithelial cell nuclei are often positioned above the columns of pillar cells (Figs 3.6D and 3.10) which allows for decreased epithelial thickness over the blood channels where most gas exchange occurs. However, in benthic elasmobranchs (which typically have relatively low metabolic demands), specialized cells, namely MRCs (also called chloride cells due to their role in chloride excretion from the gills of marine teleosts) and goblet cells (=mucous cells) can also be found in the

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Figure 3.10. Cross-section through a lamella of the shortfin mako, Isurus oxyrinchus, showing the lamellar blood channels (BCs) formed by pillar cells (PCs) and the overlaying lamellar epithelium composed primarily of thin pavement cells (PVCs). Note the location of a pavement cell epithelial nucleus (N) above the pillar cell column so as to limit the diffusion distance immediately above the BCs. Below the cross-sectioned lamella is the epithelial surface of the adjacent lamella showing the microvilli and microridges characteristic of fish gill epithelia. RBC, red blood cell.

lamellar epithelium (Hughes and Wright, 1970; Wright, 1973; Sala et al., 1987; Duncan et al., 2010). Because their large size increases diffusion distances, these specialized cells are usually more abundant in the filament epithelium, especially in more active species that require short diffusion distances (Wegner et al., 2010b). The filament epithelium is generally similar to that of the lamellae although it is typically much thicker (three or more layers of cells) and contains regionally higher concentrations of MRCs and goblet cells (Fig. 3.11). As in teleosts, MRCs appear to be most abundant in the interlamellar filament epithelium where they overlay and likely interact with the interlamellar circulation (Wright, 1973; Olson and Kent, 1980; Laurent, 1984; Wilson and Laurent, 2002) and are also in close approximation to the inner marginal channels of the lamellae. Goblet cells can be found throughout the filament epithelium and are often highly concentrated on both the leading and trailing edges of the filament, as well as the interlamellar spaces. MRCs in elasmobranchs are thought to be used primarily in salt uptake and acid-base balance (similar in function to those of freshwater teleosts), rather than the primary marine teleost function in Na+ and Cl excretion

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Figure 3.11. Scanning electron micrograph of the filament epithelial surface along the septal channel of the common thresher shark, Alopias vulpinus, showing pavement cells (PVCs), mucus (M) emerging from goblet cell pores, and the apical surface of mitochondrion-rich cells (MRCs) emerging between some pavement cells. Note the difference in the microvillar pattern of pavement and MRCs.

(Wilson et al., 1997; Piermarini and Evans, 2001; Evans et al., 2004; Tresguerres et al., 2006; Roa et al., 2014; Wright and Wood, 2015). Thus, unlike marine teleosts, elasmobranch MRCs are usually found singly with nonleaky, tight junctions between neighboring pavement cells (Wilson et al., 1997, 2002), which differs from the configuration observed for marine bony fishes in which MRCs are usually accompanied by accessory cells with leaky tight junctions that create a paracellular route for Na+ efflux (Laurent, 1984; Wilson and Laurent, 2002; Evans et al., 2005). Superficially, elasmobranch MRCs are generally similar to those of teleosts with high mitochondrial densities, a basally located nucleus, and a densely packed sub-apical tubulovesicular system (Fig. 3.12). The apical surface of MRCs can be highly variable, ranging from deep invaginations to convex crests (Laurent, 1984; Wilson and Laurent, 2002; Wilson et al., 2002), but appears to always be covered with microvilli that are typically longer or have a different pattern than those of the surrounding pavement cells (Hughes and Wright, 1970; Wilson et al., 2002; Evans et al., 2005) (Fig. 3.11). While the function of these microvilli is still largely unclear, there does appear to be a positive correlation between microvillar size with MRC activity, as the microvilli tend to become

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Figure 3.12. (A) Transmission electron micrograph (TEM) section of a mitochondrion-rich cell (MRC) from the interlamellar filament epithelium of the spiny dogfish, Squalus acanthias, showing the basally located nucleus (N), supranuclear tubulovesicular system (TVS), numerous mitochondria (M), and the basolateral plasma membrane (BLM) with extensive infoldings. The MRC is in close proximity to both the interlamellar water channel (IC) and gill vasculature (bottom right) containing red blood cells (RBCs). (B) TEM section of an MRC showing the apical surface and the nonleaky tight junctions (arrowheads) between the MRC and adjacent pavement cells (PVCs). Modified from Wilson et al. (1997).

larger and or thicker with exposure to divalent ions (e.g., Zn2+) or freshwater (Crespo, 1982). Elasmobranch MRCs lack the tortuous basolateral tubular system of marine teleosts (Laurent, 1984; Sala et al., 1987; Wilson et al., 1997), but have extensive infoldings of the basolateral membrane (Fig. 3.12) that are the sites of Na+-K+-ATPase expression in some MRCs, while other MRCs express vacuolar-proton ATPase (V-H+-ATPase) in the cytoplasm that inserts into the basolateral membrane upon blood alkalosis (Fig. 3.13). Cells

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Figure 3.13. Immunofluorescent-stained longitudinal section through a gill filament of the leopard shark, Triakis semifasciata, showing the presence of two mitochondrion-rich cell (MRC) subtypes in the interlamellar filament epithelium: MRCs with Na+-K+-ATPase (red) and MRCs with V-H+-ATPase (green). Cell nuclei are stained blue. L, lamellae; F, filament body. Image courtesy of J. Roa and M. Tresguerres.

with Na+-K+-ATPase expression are specialized for H+ excretion (in exchange for Na+ uptake), while those with V-H+-ATPase excrete HCO3 (in exchange for Cl ) (Piermarini and Evans, 2001; Evans et al., 2004, 2005; Tresguerres et al., 2006; Roa et al., 2014). In addition to MR and goblet cells, the elasmobranch filament epithelium also contains neuroepithelial cells (Laurent, 1984), which are found deep within the epithelium and are thought to play a role in oxygen sensing and the regulation of blood flow (Sundin and Nilsson, 2002). Finally, large flask-shaped cells with a narrow apical region, abundant mitochondria, and numerous vesicles have been documented in the filament epithelium of some elasmobranchs, but their function is unknown (Wright, 1973; Wilson et al., 2002). 6. DIVERSITY IN ELASMOBRANCH GILL DIMENSIONS AND MORPHOLOGY The first several sections of this chapter have focused primarily on common structural features of the elasmobranch gill. However, as in bony fishes, elasmobranch gill morphology varies in relation to habitat and life history. While elasmobranchs are not nearly as diverse as teleosts, they have

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nonetheless filled a number of different niches resulting in varied body plans or ecomorphotypes (Compagno, 1990), ranging from freshwater stingrays to the highly streamlined and regionally endothermic sharks of the open ocean. This section focuses on functional differences within the elasmobranch gill and its specialization for increased oxygen uptake, enhanced osmoregulatory function, and adaptations associated with feeding. 6.1. Gill Arches Perhaps one of the most obvious examples of diversity in elasmobranch gill morphology is variation in the number of gill bearing arches. Most elasmobranchs have five gill arches containing nine hemibranchs (one hemibranch on the hyoid arch followed by four holobranchs) on either side of the orobranchial cavity (Fig. 3.1B). However, well known are the Hexanchiformes, which include the frill shark, Chlamydoselachus anguineus, and the sixgill sharks (Hexanchus spp.) which have six branchial arches (one hemibranch and five holobranchs) on either side of the orobranchial chamber, as well as the sevengill sharks (Heptranchias, Notorynchus) which have seven (one hemibranch and six holobranchs) (Fig. 3.14). While it has been tempting for some evolutionary biologists to draw the parallel between the seven paired gill pouches of lampreys and the seven arch pairs of some Hexanchiformes (which in some previous phylogenies were positioned near the base of the elasmobranch tree), there is little evidence to support that seven (or six) gill arches is the basal elasmobranch character state (especially considering the first two arches in gnathostomes have moved forward to form and support the jaws). Examination of the “extra” gill arches points to their independent evolution in Chlamydoselachus and Hexanchus (thus challenging the monophyly of the hexanchoids) with the additional independent evolution of an extra arch pair in the sevengill sharks (Shirai, 1992). In addition to the Hexanchiformes, a single species of saw shark, the sixgill sawshark, Pliotrema warren (Order Pristiophoriformes), and at least one ray species, the sixgill stingray Hexatrygon bickelii (Order Myliobatiformes) have six gill arch pairs. Thus it appears that the evolution of additional gill arches has occurred multiple times within elasmobranchs, and it seems reasonable that this characteristic may be related to the deep, and presumably low-oxygen habitats that these species tend to inhabit (with the notable exception of Notorynchus, which is a generally shallow water, coastal species). However, measurements of gill surface area are needed to support this hypothesis. Another interesting deviation from the normal elasmobranch branchial arch configuration occurs in the collared carpet sharks (Family Parascylliidae, Order Orectolobiformes). These sharks have five gill arch pairs

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Figure 3.14. Simplified schematic showing the diversity in elasmobranch gill arch number and hemibranch configuration (also shown are the closely related holocephalans). H, hyoid arch (also referred to in this text as gill arch 1).

like most elasmobranch species, but lack filaments on the posterior side of the fifth arch (Goto et al., 2013). The fifth parabranchial cavity thus lacks any respiratory gill tissue (Fig. 3.14) and has a strikingly large gill slit [most gill slits tend to remain constant or decrease in height along the length of the shark (Dolce and Wilga, 2013)] that appears to be used to create extra force during suction feeding (Goto et al., 2013). As parascylliid sharks are coastal benthic species that inhabit well oxygenated waters and likely have low oxygen demands, the forfeit of this hemibranch appears to be an acceptable loss in order to enhance their ability for prey capture through suction feeding.

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6.2. Gill Morphometrics Even without gill specialization that includes the addition or loss of gill arches or hemibranchs, the size of the gills can vary widely among species, and while the gill is involved in multiple functions, such differences in gill morphometrics appear to correlate most directly with its function in gas _ 2 in mgO2 min 1) at the gill is exchange. The rate of oxygen uptake (MO directly related to both gill dimensions and dissolved oxygen levels within the environment as described by the Fick equation: _ 2 ¼ ðK .A.DPO2 Þ=t MO

(3.1)

where K is the diffusion or Krogh coefficient through a specific material (e.g., the gill epithelium, mgO2 mm cm 2 mmHg 1 min 1), A is the respiratory surface area of the gills (usually reported as the total bilateral surface area of all the lamellae in the gills in cm2), DPO2 is the mean difference in the partial pressure of oxygen between the water and the blood (mmHg), and t is the diffusion distance (mm). According to Eq. (3.1), increases in gill surface area (A) or a decrease in diffusion distance (t) will augment oxygen uptake. If DPO2 is low due to low levels of environmental oxygen, an increase in A or decrease in t are needed to maintain the same level of oxygen uptake. As a result, gill surface area and gill diffusion distances correlate with both oxygen demands and the dissolved oxygen levels of the environment. Fig. 3.15 shows the gill surface areas for all elasmobranchs determined to date, with highly-active species having larger gill surface areas than those of less-active, benthic species. Particularly large are the gill surface areas of the lamnid sharks (Family Lamnidae) and the thresher sharks (Family Alopiidae), which are highly active predators, many of which are able to increase aerobic performance through regional endothermy (Bernal et al., 2012). The relationship between resting metabolic rate and gill surface area for the few elasmobranchs for which accurate data are available for both variables is shown in Table 3.1. While some caution should be used when extrapolating regression equations for gill surface area and metabolic rate to a common mass for interspecific comparisons (in this case 1 kg, which is not a realistic size for some species), the metabolic rate to gill surface area ratio is strikingly similar between species of varying activity levels, indicating their close correlation. However, considering that functional gill area can be reduced during rest (e.g., through changes in blood perfusion, see Section 5.2.3), it seems likely that gill area may correlate even more tightly with maximum sustainable metabolic rate, and this may help explain some of the variation in Table 3.1. Hence the relatively small gill surface area relative to resting metabolic rate in the marbled electric ray,

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Figure 3.15. Relationship of gill surface area to body mass for all known elasmobranchs studied to date. Note: Gill areas estimated for the megamouth shark, Megachasma pelagios, and shortfin mako, Isurus oxyrinchus, by Oikawa and Kanda (1997) are not included in the present figure as they were shown to be inaccurate (Wegner et al., 2010b). *Regression line for Torpedo marmorata includes five specimens of the electric ray, T. nobiliana. The single data point for the scalloped hammerhead, Sphyrna lewini, is the mean of three individuals estimated from a gillarea-to-body-mass graph from Emery and Szczepanski (1986). Sources: Wootton et al. (2015)a, Emery and Szczepanski (1986)b, Wegner et al. (2010b)c, Grim et al. (2012)d, Boylan and Lockwood (1962)e, Hughes and Morgan (1973)f, Hughes (1977)g, Hughes (1972)h, Hughes et al. (1986)i, Hughes (1978)j, Dabruzzi and Bennett (2013)k, Duncan et al. (2011)l.

Torpedo marmorata (=high ratio of resting metabolic rate to gill area compared to other species in Table 3.1) may indicate that this species is not able to increase its oxygen uptake much above that at rest. For a species such a T. marmorata with low activity levels this may not be problematic and should reduce costs associated with osmoregulation. Unfortunately, comparing maximum metabolic rate to gill surface area is difficult due to the challenge of conditioning sharks and rays to swim steadily in swim tunnel respirometers at maximum sustainable speeds.

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Table 3.1 Relationship between resting metabolic rate (RMR) and gill surface area for five elasmobranchs Common name Sandbar shark Spiny dogfish Shortfin mako Shortfin mako Small-spotted catshark Marbled electric ray

Species names Carcharhinus plumbeus Squalus acanthias Isurus oxyrinchus Isurus oxyrinchus Scyliorhinus canicula Torpedo marmorata

RMR (mgO2 kg 1 h 1)

Gill area for 1 kg RMR/area fish (cm2) (mgO2 h 1 m 2)

47.23a 52.64c 141.57e 141.57e 38.20g

4074b 3700d 9550b 8038f 2004h

115.93 142.27 148.24 176.13 190.62

20.72i

759i

272.99

RMRs were adjusted to 151C using a Q10 of 2 and to a body mass (M) of 1.0 kg using M0.80 (unless species-specific scaling coefficients were known). Metabolic studies lacking experimental temperature or body mass data or using data from animals that were surgically stressed (e.g., Piiper and Schumann, 1967) are not included. Sources: a Dowd et al. (2006). b Emery and Szczepanski (1986). c Brett and Blackburn (1978). d Boylan and Lockwood (1962). e Sepulveda et al. (2007). f Wegner et al. (2010b). g Sims (1996). h Hughes (1972). i Hughes (1978).

Missing from Table 3.1 is the incorporation of diffusion distance data, which according to Eq. (3.1) equally affects the rate of oxygen uptake. Diffusion distance data are difficult to incorporate into models of oxygen uptake as oxygen must travel through the interlamellar water, the lamellar epithelium, the blood, and into erythrocytes where it binds to hemoglobin. Thus, diffusion distances are tied to multiple measurements, as well as the hydrodynamics of the ventilatory stream and blood flow. Still, insight can be gained by examining the thickness of the water–blood barrier and thickness of the lamellae themselves (Table 3.2). These tend to be thin in active, pelagic sharks. For example, I. oxyrinchus has a water–blood barrier approximately an order of magnitude thinner than some benthic shark species. 6.3. Theory on Elasmobranch Gill Dimensions and Limits to Gill Diffusion Capacity Gill surface area (A) is the product of a number of constituent dimensions: A ¼ Lfil .2nlam .Alam

(3.2)

Table 3.2 Thickness of the water–blood barrier and lamellae reported for elasmobranchs of varying activity level and habitat Common name

Species name

Shortfin mako Bigeye thresher Pelagic thresher Blue shark Common thresher Spotted skate Thornback skate Nursehound Nursehound Tope Spiny dogfish Small-spotted catshark

Isurus oxyrinchus Alopias superciliosus Alopias pelagicus Prionace glauca Alopias vulpinus Raja montagui Raja clavata Scyliorhinus stellaris Scyliorhinus stellaris Galeorhinus galeus Squalus acanthias Scyliorhinus canicula

Water–blood barrier thickness (mm) Lamellar thickness (mm) Reference 1.1570.22 1.6070.08 1.6170.19 1.6570.59 2.5570.27 4.85 5.99 9.4371.72 9.62 9.87 10.14 11.27

11.3871.61 12.5072.59 12.5170.53 15.2473.41 14.2970.94

34.1

Wegner et al. (2010b) Wootton et al. (2015) Wootton et al. (2015) Wegner et al. (2010b) Wootton et al. (2015) Hughes and Wright (1970) Hughes and Wright (1970) Hughes et al. (1986) Hughes and Wright (1970) Hughes and Wright (1970) Hughes and Wright (1970) Hughes and Wright (1970)

Note: The diffusion distance data compiled in this table clearly show a correlation with elasmobranch activity level. However, techniques for measuring and preparing samples can vary between studies, which can affect results and should thus be considered when making comparisons. For example, Hughes (1984) notes that the electromicrograph sections used for measurements in Hughes and Wright (1970) were not always cut and mounted exactly perpendicular to the lamellar surface, thus likely resulting in some overestimation of thickness. However, reexamined measurements for S. stellaris (Hughes et al., 1986) in which harmonic means of the water–blood barrier were calculated and values were corrected for the Holmes effect, slant, and shrinkage, were only about 2% different than the original estimates. Still additional and repeat studies of diffusion distances in the gills are warranted, especially in species for which a surprisingly thick water–blood barrier is reported. For example, micrographs in several studies (including those in Hughes and Wright, 1970) show water–blood barrier distances much shorter than the means reported in this table by Hughes and Wright (1970).

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where Lfil is the total length of all the gill filaments, nlam is the number of lamellae per unit length on one side of a filament (i.e., lamellar frequency, which is multiplied by two to account for lamellae on each side of the filament), and Alam is the mean bilateral surface area of a lamella. Consequently, an increase in any of these dimensions results in a larger gill surface area. While gill surface area correlates with metabolic demand, these componential dimensions (Lfil, nlam, Alam) are sculpted by various factors. Particularly important are hydrodynamic considerations that must be balanced to create optimal ventilatory-flow conditions in the interlamellar channels for gas exchange (Strother, 2013; Park et al., 2014). The velocity (and consequently residence time) of water in contact with the lamellae in the interlamellar channels is largely dependent on the resistance imposed by the gills. Resistance (R) through the interlamellar channels is described by the Hagen-Poiseuille equation for water flow between parallel plates. For a single interlamellar channel: R ¼ 12ml=d 3 h

(3.3)

and for all interlamellar channels in the gills: R ¼ 12mlðd þ wÞ=d 3 hLfil

(3.4)

where m is the dynamic viscosity of the water, l is the length of the interlamellar channel, d is the diameter or width of the channel, w is the width or thickness of a lamella, and h is the lamellar height (dimensions shown in Fig. 3.16). According to this equation, an increase in lamellar

Figure 3.16. Schematic from Fig. 3.1 showing lamellar dimensions associated with Eqs (3.3) and (3.4). Variable abbreviations: d, diameter of interlamellar channel; h, lamellar height; l, lamellar length (=length of interlamellar channel); w, lamellar thickness.

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length (l) or lamellar frequency (thus decreasing d) amplifies gill resistance (and consequently the energy required to ventilate the gills), while an increase to lamellar height (h) or the length of the gill filaments (Lfil), decreases gill resistance. Thus, from an energetic standpoint (i.e., minimizing increases to gill resistance), gill surface area is optimally increased through large (tall) lamellae and high total filament lengths (Hughes, 1966; Wegner, 2011). In reality, certain fish groups appear to adhere to this optimal configuration to augment gill area, while others do not. For high-energy demand and ram-ventilating teleosts such as tunas (family Scombridae), gill surface area is increased through long gill filaments, but also through high lamellar frequencies, which decreases d and greatly amplifies gill resistance (Muir and Hughes, 1969; Wegner et al., 2010a). Wegner et al., (2010a) suggested the increase in resistance imposed by high lamellar frequencies might help slow the fast and forceful branchial stream produced by ramventilation to create more optimal conditions for efficient gas exchange. In contrast to high-performance teleosts, fast-swimming elasmobranchs (e.g., the lamnid sharks) do not have increased lamellar frequencies, but rather adhere to the theorized optimal configuration by increasing gill area through long filaments and large lamellae (Emery and Szczepanski, 1986; Wegner et al., 2010b). Because the septal channels contribute substantially to gill resistance (Wegner et al., 2012), high lamellar frequencies, which would further increase resistance, are likely precluded as a metric in elasmobranchs to increase gill surface area. Consequently and because increased filament length and large lamellae require additional space within the branchial chambers (high lamellar frequencies do not), total gill surface area is quickly constrained in fast swimming elasmobranchs by the dimensions of the branchial chambers and cranial streamlining. Thus in comparison to tunas (the zenith of teleost aerobic performance), lamnid sharks (the peak of elasmobranch performance) have one-half the lamellar frequency, which results in approximately one-half the total gill surface area, and likely limits elasmobranch aerobic capacity in comparison to teleosts (Wegner et al., 2010b, 2012). In addition to apparent limits in gill surface area, gill diffusion distances in elasmobranchs are generally longer than those of teleost species that are similar in activity level and habitat. First, elasmobranch interlamellar channels are generally wider in order to compensate for the added resistance of the septal channels. Second, the water–blood barrier in elasmobranchs is generally thicker (Hughes and Wright, 1970; Wegner et al., 2010b). This may be related to the generally large lamellae of elasmobranchs (a thicker lamellar epithelium would provide additional support) or other functions associated with individual epithelial components. For example, Hughes and Wright (1970) showed that benthic elasmobranchs have a thicker lamellar

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basement membrane and generally longer microvilli (which would anchor a thicker mucosal layer on the gills) than those of teleosts. Both could be related to reducing the loss of important ions and other molecules to the external environment that are used by marine elasmobranchs to maintain an osmolarity close to that of seawater (Smith, 1936). This is in part supported by the findings of Fines et al. (2001) that showed that the basolateral membranes of the gill epithelial cells of S. acanthias have a very high cholesterol content that likely lowers gill permeability to urea without inhibiting oxygen diffusion, and findings by Hill et al. (2004) showing the low permeability of urea and other molecules through the gill apical membrane and mucous layer. Third, in addition to a thicker water–blood barrier, the blood channels of elasmobranch lamellae are generally wider (thus increasing lamellar thickness and diffusion distances within the blood), likely to accommodate the intrinsically large red blood cells of elasmobranchs (Fa¨nge, 1992; Wilhelm Filho et al., 1992). 6.4. Scaling Important insight into gill function and whole organismal physiology can be gained by examining how gill dimensions change with fish growth. This relationship is typically described by the power-law scaling equation: Y ¼ aM b

(3.5)

or log form, log Y ¼ log a þ b log M

(3.6)

where, Y is a particular gill morphometric (e.g., A, Lfil, nlam, or Alam), a is the intercept value for a 1 g specimen, M is fish mass, and b is the species-specific slope or scaling exponent. Assuming the gills grow isometrically (i.e., gill mass increases at the same rate as body mass, b=1.0), isometric geometry of the gills (the length/area/volume relationship) predicts that Lfil should scale to the one-third (i.e., length/volume, b=0.33), nlam to the negative one-third (length 1/volume, b= 0.33), and Alam to the two-thirds (area/volume, b=0.67), which when added together, sum to the expected scaling exponent for total gill surface area (area/volume, b=0.67). In teleost fishes, the scaling exponent for gill surface area to body mass can range from under 0.50 to over 1.00, with a mean of 0.80. This mean is significantly greater than that predicted by isometric scaling and appears to correlate with the mean scaling exponent for fish standard metabolic rate with body mass (0.81) (Palzenberger and Pohla, 1992; Wegner, 2011). For the much more limited pool of elasmobranchs studied to date (Table 3.3) the gill area scaling exponent ranges from 0.74 to 1.03 with a mean of 0.85,

Table 3.3 Regression equation intercepts (a) and scaling exponents (b) for elasmobranch gill surface areas (A) shown in Fig. 3.15 and associated componential dimensions (Lfil, nlam, and Alam) in comparison to body mass (M, in g) according to the power-law scaling equation Y=aMb A (cm2)

Lfil (cm)

nlam (mm 1)

a

a

Common name

Species names

Common thresher shark Small-spotted catshark Marbled electric ray+ Pelagic thresher shark Blue shark Dusky shark Shortfin mako Nursehound Bigeye thresher shark White shark Shortfin mako Sandbar shark Common thresher sharka Atlantic stingraya Cownose raya

Alopias vulpinus 2.46 1.0299 499.16 0.3216 56.71 Scyliorhinus canicula 2.62 0.9610 72.28 0.3510 17.15 Torpedo marmorata 1.17 0.9368 51.36 0.3966 34.17 Alopias pelagicus 12.51 0.8928 774.31 0.2901 78.61 Prionace glauca 5.50 0.8800 162.18 0.3800 25.70 Carcharhinus obscurus 6.17 0.8800 186.21 0.4000 67.61 Isurus oxyrinchus 35.89 0.7834 612.31 0.2904 39.19 Scyliorhinus stellaris 6.21 0.7790 81.40 0.3650 30.27 Alopias superciliosus 52.17 0.7753 2036.74 0.2221 107.87 Carcharodon carcharias 42.66 0.7700 954.99 0.2900 56.23 Isurus oxyrinchus 57.54 0.7400 676.08 0.2800 100.00 Carcharhinus plumbeus 24.55 0.7400 134.90 0.4000 46.77 Alopias vulpinus 2511.89 0.4100 263.03 0.3700 457.09 Dasyatis sabina 421.46 0.2000 Rhinoptera bonasus 2987.61 0.2000 Mean 0.8474 0.3322

a

a

b

b

b 0.1628 0.0710 0.1665 0.1871 0.0900 0.1600 0.1113 0.1670 0.2154 0.1500 0.2000 0.1300 0.3400

0.1509

Alam (mm2) a

b

0.00048 0.01030 0.00336 0.00105 0.00661 0.00245 0.00748 0.01270 0.00092 0.00407 0.00427 0.01905 0.10233

0.8609 0.6840 0.7060 0.7881 0.5900 0.6500 0.6043 0.5800 0.7921 0.6300 0.6600 0.4800 0.3800

Mass range (kg) 7.9–91.5 0.115–0.800 0.1–20.0 11.8–78.2 12–120 20–200 4.6–71.0 0.585–2.615 48.8–127.3 12–1300 12–125 20–75 60–180 0.40–0.65 4.5–7.2

Reference Wootton et al. (2015) Hughes (1972) Hughes (1978) Wootton et al. (2015) Emery and Szczepanski Emery and Szczepanski Wegner et al. (2010b) Hughes et al. (1986) Wootton et al. (2015) Emery and Szczepanski Emery and Szczepanski Emery and Szczepanski Emery and Szczepanski Grim et al. (2012) Grim et al. (2012)

(1985) (1985)

(1985) (1985) (1985) (1985)

0.6688

Indicates species not included in scaling exponent means due to low sample size or a limited body-mass size range in comparison to other species. +Five of the 22 specimens included in the regression equations for Torpedo marmorata are the electric ray, T. nobiliana. Lfil, total filament length; nlam, lamellar frequency (=number of lamellar per mm filament); Alam, mean bilateral surface area of a lamella.

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which closely matches the mean scaling exponent for standard/resting metabolic rate (0.84) in six elasmobranch species for which mass dependent metabolic data are available (Hughes, 1978; Du Preez et al., 1988; Sims, 1996; Ezcurra, 2001; Dowd et al., 2006). Species-specific deviation from the mean gill-area-to-body-mass scaling exponent may provide insight into changes in fish metabolism or other physiological processes with growth. For example, the high scaling exponent for the gill surface area of the common thresher shark, Alopias vulpinus (1.03), may reflect an increased ability for regional endothermy (and hence disproportionate increase in oxygen demands) with body size (Wootton et al., 2015). This disproportionate increase in gill surface area results from a disproportionate increase in the size of gill lamellae (the scaling exponent for Alam is 0.86 in comparison to the predicted 0.67) (Table 3.3), which is consistent with theoretical predictions for augmenting gill area while minimizing increases to gill resistance. 6.5. Adaptations for Fast Swimming Within the apparent constraints imposed on elasmobranch gill dimensions (see Section 6.3), fast swimming pelagic sharks have much larger gill surface areas and shorter diffusion distances than those of benthic species (Fig. 3.15, Table 3.2). In the lamnids and some other oceanic groups, the pectoral fins are positioned more posteriorly than in many less-active benthic species (Thompson and Simanek, 1977; Compagno, 1990; Dolce and Wilga, 2013). While this positioning likely has hydrodynamic considerations for continuous swimming, it may also allow for the longitudinal expansion of the branchial chambers and generally longer gill filaments. Fast-swimming pelagic sharks also tend to have relatively large gill slits of similar length (Dolce and Wilga, 2013), which likely minimizes slit effects on branchial resistance and swimming drag. While fast-swimming sharks lack the gill fusions of ramventilating teleosts [used to stabilize the gill filaments and lamellae against a forceful ram-ventilatory stream (Muir and Kendall, 1968; Wegner et al., 2013)], their filaments are strengthened by the interbranchial septum and their lamellae appear to be stiffened by lamellar vascular sacs (see Section 5.1). The largest gill areas in all elasmobranchs are found in the lamnid and alopiid sharks and can be more than twice those of other oceanic shark species (Emery and Szczepanski, 1986; Wegner et al., 2010b; Wootton et al., 2015). For lamnids and A. vulpinus, large gill areas are likely required to meet high oxygen demands associated with regional endothermy and increased aerobic performance. However, the gill surface area of the pelagic thresher shark, A. pelagicus, which is not known to elevate its body temperature above ambient (Patterson et al., 2011), rivals that of the

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regionally endothermic lamnids and A. vulpinus (Fig. 3.15). Wootton et al. (2015) suggested that the large gill area in A. pelagicus may, in part, reflect its tropical warm-water environment, which contains less oxygen than temperate seas (warm water has a reduced oxygen solubility coefficient) and would keep the body temperature of A. pelagicus above that of most regionally endothermic sharks. As most studies have focused on temperate and subtropical species, there is little known about the gill dimensions of warmer water elasmobranchs and how gill morphometrics and structure may vary with temperature.

6.6. Adaptations for Hypoxia Large gill surface areas also allow for enhanced oxygen uptake in hypoxic environments. The largest elasmobranch gill surface area documented to date belongs to the bigeye thresher shark, Alopias superciliosus (Wootton et al., 2015), which undertakes diel vertical migrations to depths of 300–500 m where, in many locations within its range, it forages within the hypoxic waters of the subsurface oxygen minimum zone (OMZ) (Nakano et al., 2003; Weng and Block, 2004). The gill area of the bigeye thresher is increased by its extremely long gill filaments, which occur within laterally expanded branchial chambers (Fig. 3.17A). The large size of these brachial chambers emphasizes the nuchal grooves along the sides of the head and produces its distinct “helmeted” contour. Wootton et al. (2015) suggested that as A. superciliosus feeds heavily on slow-moving prey within the OMZ, the selective pressure of cranial streamlining may have been relaxed, thus allowing for larger branchial chambers capable of housing a gill surface area larger than those of other, more streamlined elasmobranchs. Other deep-water sharks that occupy the OMZ appear to have a similar approach to augment gill surface area through long filaments, although gill morphometric data are needed to confirm this. Some species of the deepwater catshark genus Parmaturus and the triakid genus Iago are reported to have enlarged branchial chambers and elongated gill filaments (Compagno, 1990). The lollipop catshark, Cephalurus cephalus, found at depths of 250– 850 m gets its name from its unique body shape and large head which likely houses expanded branchial chambers and gills (Fig. 3.17B). In addition to having an extra gill arch, the deep-dwelling frill shark (240–1500 m) possesses gill filaments that appear to fill the branchial cavities and are long enough to extend out their large gill slits. The extension of filament tips out of the gill slits has also been suggested for the deep-dwelling Apristurus catsharks (Graham, 2006). However, this seems unlikely due to the small gill slits of this genus, which if filled with filaments, would likely obstruct

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Figure 3.17. Expanded branchial chambers of the (A) bigeye thresher, Alopias superciliosus, and (B) lollipop catshark, Cephalurus cephalus which house large gills for increased gas exchange within the oxygen minimum zone. The branchial chambers are expanded laterally in A. superciliosus and both laterally and longitudinally in C. cephalus. Images modified from or based on Compagno (1990, 2001) and Wootton et al. (2015).

ventilatory flow. Furthermore, specimens examined by the current author in the preparation of this chapter did not possess this particular anatomy. Recent research has shown that at least some elasmobranchs are capable of relatively rapid increases in gill surface area in response to decreases in environmental dissolved oxygen. Shallow marine and estuarine species such as the Atlantic stingray, Dasyatis sabina, can become trapped in shallow isolated pools during low tide that, at night, can become severely hypoxic due to biological respiration. Dabruzzi and Bennett (2013) showed

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that stingrays in the laboratory exposed to daily hypoxic intervals (30% O2 saturation for 7 h), increased gill surface by up to 70% after just 20 days. Like many freshwater teleosts (see for review Nilsson, 2013), this appears to occur primarily via apoptosis of the filament epithelium which exposes additional lamellar area that is embedded within the filament body (Bennett, Personal Communication). However, detailed morphometric analyses are still needed and the wide range of gill surface areas reported for this species (see Fig. 3.15) (Grim et al., 2012; Dabruzzi and Bennett, 2013) suggests that even larger changes or population-specific differences in gill surface area are likely. Additional studies on changes in gill morphology in this and other species such as the epaulette shark, Hemiscyllium ocellatum (which is often exposed to anoxic pools in tropical reefs) would provide further valuable insight into elasmobranch respiratory plasticity and responses to hypoxia. 6.7. Adaptations for Freshwater Although the vast majority of elasmobranchs occur solely in the marine environment, approximately 5% of extant species can regularly be found in freshwater, and a few groups (comprising about 3–4% of elasmobranch species) such as the potamotrygonid stingrays, are specialized for freshwater and cannot tolerate higher salinities (Ballantyne and Robinson, 2010). Most of the physiological research on freshwater elasmobranchs has focused on their ability to osmoregulate, which, with the typical marine elasmobranch osmolarity close to that of seawater, requires a number of adaptations. Studies on the gills of freshwater elasmobranchs have focused primarily on the function, prevalence, and distribution of MRCs. For euryhaline species such as D. sabina and the bull shark, Carcharhinus leucas, MRC abundance increases in freshwater to meet augmented demands for NaCl uptake and acid-base balance (Piermarini and Evans, 2000; Piermarini and Evans, 2001; Reilly et al., 2011). Fig. 3.18 shows the stepwise change in the proliferation and distribution of two MRC subtypes (Na+/K+-ATPase-rich and V-H+ATPase rich cells) in D. sabina that are found primarily in the interlamellar filament epithelium in seawater acclimated individuals, but become increasingly more abundant on the lamellar epithelium with lower salinities (Piermarini and Evans, 2001). The increase in MRC abundance in the lamellar epithelium for freshwater elasmobranchs likely increases the thickness of the water–blood barrier, thus decreasing the diffusion capacity of the gills (although this and other gill morphometric data are largely lacking from the literature). As air-saturated freshwater typically contains 15–20% more oxygen than seawater (depending on temperature) a thick water–blood barrier may not

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Figure 3.18. Longitudinal sections through the gill filament and lamellae of the Atlantic stingray, Dasyatis sabina, showing the relative distribution of mitochondrion-rich cells (brown=V-H+ATPase-rich; blue=Na+/K+-ATPase-rich) for rays from (A) freshwater, (B) freshwater acclimated to seawater for two weeks, and (C) seawater. Modified from Piermarini and Evans (2001).

be detrimental to oxygen uptake and should be advantageous in decreasing the diffusive loss of ions to the environment. Palzenberger and Pohla (1992) showed that freshwater teleosts have generally smaller gill surface areas than comparable marine teleosts, and this likely correlates to the higher oxygen

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concentration in freshwater. Future studies on freshwater elasmobranch morphometrics would provide interesting insight into the osmo-respiratory compromise. 6.8. Adaptations for Feeding – Gill Rakers One highly variable structural element of the gills not directly associated with gas exchange is the gill raker. In most elasmobranchs, gill rakers are either absent or are small and knob-like and likely serve to protect the gills during feeding. However, four elasmobranch lineages (Cetorhinidae, Megachasmidae, Mobulidae, and Rhincodontidae) have independently evolved elaborate raker-based filtering apparatuses for suspension feeding. Perhaps the most intricate filtration system is found in the whale shark, Rhincodon typus, in which nearly the entire pharyngeal surface is lined by 20 giant interconnected filter pads composed of a denticle-covered reticulated mesh with small irregularly shaped pores (Fig. 3.19) (Motta et al., 2010). Each pad, formed by rakers on each gill arch epi- or ceratobranchial, is joined to the neighboring pad by a connective tissuebased raphe (Fig. 3.19B), thus ensuring that all water entering the mouth passes through the filtering apparatus. The reticulated mesh (Fig. 3.19C, D, and F) appears composed of tertiary and quaternary folds of the gill rakers that have fused together to form an irregular pattern. The primary and secondary rakers [termed secondary and primary vanes, respectively, by Motta et al. (2010)] that support the reticulated mesh, appear positioned to help direct post-filter flow toward the gill filaments (Fig. 3.19E and F). Functionally similar to the filter pads of R. typus are the gill rakers of the mobulids (mantas and devil rays), in which individual rakers (also termed filter lobes) contain leaf-like secondary rakers or lobes that are in such close proximity they form a reticulating mesh and assume a plate-like appearance (Fig. 3.20) (Paig-Tran et al., 2013; Paig-Tran and Summers, 2014). Although each row of rakers on either side of each epi- and ceratobranchial is called a filter pad or plate, mobulid pads differ from those of R. typus in that they are composed of individual rakers that, with the exception of Mobula tarapacana, do not appear to be fused and in no cases connect to the rakers of the opposing arch. However, like R. typus, the trailing (water-exit) edge of the primary and secondary rakers form vanes that direct post-filtered water toward the gill filaments for gas exchange (Fig. 3.20B). The orientation and reticulating mesh morphology of the filter pads of both mobulids and R. typus, coupled with the finding of prey smaller than mesh size in the stomachs, suggests that both groups may use cross-flow filtration, in which the tangential shearing of water flow parallel to the filter surface pushes particulate food items toward the back of the pharynx to be swallowed

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Figure 3.19. The branchial filtering apparatus of the whale shark, Rhincodon typus. (A) Schematic rendering of an anterior-lateral view of a whale shark showing the position of the filter pads and direction of water flow as indicated by solid black lines. The enlarged view of a single gill arch shows primarily the trailing (water-exit) edge of the filter pad revealing the primary gill rakers that provide structural support and direct flow toward the gill filaments. (B) Water-entry side of the upper (left) and lower (right) filter pads from the left side of the orobranchial chamber removed from the gill arches and laid flat. Note the connective tissue-

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without direct contact with the sieve (Motta et al., 2010; Paig-Tran et al., 2013; Paig-Tran and Summers, 2014). The gill rakers of the basking shark, Cetorhinus maximus, and megamouth shark, Megachasma pelagios, are much simpler in structure and are likely associated with a more traditional filtering mechanism in which the food items become physically caught in the rakers for collection and later swallowing. For C. maximus, the rakers are long and largely rigid keratinous bristle-like structures (Fig. 3.21A) that emanate from the distal end on both sides of each gill arch (Daniel, 1934; Matthews and Parker, 1950; Sims, 2008). When the mouth is closed, the rakers lay flat against the arch. As the mouth opens for feeding, the rakers extend off the gill arch and approach those of the adjacent arch, forming a series of “V” shaped filters that point toward the oral cavity and fill the pharyngeal slits (Daniel, 1934; Sims, 1996). A thick mucosal epithelium lines much of the gill arches and orobranchial cavity and likely produces mucus that in theory coats the rakers to aid in prey adhesion and capture (Matthews and Parker, 1950; Paig-Tran and Summers, 2014). In M. pelagios, closely spaced, repeating, and largely flexible papillae-like rakers (Fig. 3.21B and C) are composed of a hyaline cartilage core covered by dense connective tissue, a thin epithelial layer, and placoid denticles (Yano et al., 1997; Paig-Tran and Summers, 2014). The functional significance of the numerous denticles (Fig. 3.21C) is not known, but like C. maximus, it is hypothesized that they may be largely covered by mucus for prey adhesion. While M. pelagios feeding has never been observed, the large mouth and small gill slits suggest an engulfment mechanism (in which engulfed prey are filtered as water is pushed out the gill slits) rather than the steady swimming, ram filtration that is used heavily by R. typus and likely exclusively by mobulids and C. maximus.

based raphae connecting adjacent gill pads to ensure all water passes through the filtering apparatus. Gill pads are numbered from 1–5 anterior to posterior. The white ruler is 15 cm. (C) Enlarged view of the water-entry side of a gill pad showing the reticulated mesh. (D) Enlarged view of the reticulated mesh. (E) Water-exit side of the gill pad revealing the primary and secondary rakers [secondary and primary vanes respectively of Motta et al. (2010)] that support the gill pads and direct water toward the gill filaments. (F) Magnified view of a cross-section though the gill pad showing the reticulated mesh which appears to be composed of tertiary and quaternary folds of the gill rakers that have fused together. The white square in (E and F) is 1.0 cm2. Water flow through the filter in (B–D) is into the page and is from top to bottom in (E and F). BC, branchial canopy; CTR, connective tissue raphe; F, filaments; GA, gill arch; P, filter pad; R, primary raker; RM, reticulated mesh; SR, secondary raker. (A–C, E, and F) Modified from Motta et al. (2010) and (D) Courtesy of P. Motta (Unpublished). (A) Based on an illustration by Emily S. Damstra.

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Figure 3.20. Gill filtering apparatus of the mobulid rays. (A) Anterior view into the orobranchial cavity of the spinetail mobula, Mobula japonica, showing the leading (water-entry) side of the gill rakers emanating from both sides of each gill arch. Gill arches 2–5 are numbered. (B) Extracted gill arch from the Chilean devil ray, M. tarapacana, showing the leading surface of the primary and secondary rakers from the ceratobranchial (lower left) and the outflow channels of the rakers from the epibranchial (upper right). BC, branchial canopy; C, ceratobranchial; E, epibranchial; F, filaments; GA, gill arch; IS, interbranchial septum; R, raker. (A) Reprinted with permission of Gisela Kaufmann, Manta Trust. (B) Modified from Paig-Tran et al. (2013).

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Figure 3.21. Gill rakers of the (A) basking shark, Cetorhinus maximus and (B and C) megamouth shark, Megachasma pelagios. The long bristle-like gill rakers of C. maximus (A), which interconnect at their base, are shown removed from the gill arch. The papillae-like gill rakers for M. pelagios (B) are shown emanating from both sides of each arch (numbered 1–5). (C) is a magnified scanning electron micrograph of the white box in (B) showing the denticles that cover the surface of M. pelagios rakers. F, filaments; RB, raker base.

7. CONCLUSIONS As in other fishes, the gills of elasmobranchs are essential in gas exchange, ion and pH balance, and nitrogen excretion, and, in some cases, feeding. Despite the importance of the gill to basic physiological function, most of our knowledge on elasmobranch gill structure and function has historically been based on the study of just a few representative species such as S. acanthias, S. canicula, and S. stellaris, which are relatively common, sedentary, and temperate sharks that are easily held in captivity. It has only been more recently that morphological assessments have been expanded to include a wider diversity of elasmobranch species to those that push the limits of physiological function in terms of rapid swimming and regional

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endothermy (Wegner et al., 2010b, 2012), life in hypoxia (Dabruzzi and Bennett, 2013; Wootton et al., 2015), or adaptations for freshwater (Piermarini and Evans, 2000, 2001; Duncan et al., 2010; Reilly et al., 2011). Such research is yielding exciting results and insights into the capabilities and limitations of the elasmobranch gill for gas exchange and consequently aerobic function, gill plasticity and possible remodeling, and adaptations for extreme osmotic stress. Still these studies have likely just begun to scratch the surface. The gill morphology of many groups such as deep-sea and obligate freshwater elasmobranchs has gone largely unstudied. Unfortunately, due to their large body size, extreme or remote habitats, and active swimming requirements, many elasmobranch groups cannot be brought into the laboratory for direct physiological study. For such species, examination of branchial morphology can provide insight into metabolic requirements and other important physiological processes. ACKNOWLEDGMENTS I would like to thank G. Kaufman, P. J. Motta, K. R. Olson, E. W. M. Paig-Tran, P. M. Piermarini, J. Roa, M. Tresguerres, and J. M. Wilson for providing images used in figures for this chapter. I also thank H. Dewar, H. J. Walker, and the Scripps Institution of Oceanography Vertebrate Collection for specimens and samples examined, and E. York and S. Faulhaber for technical assistance with SEM use. Finally, I thank H. Aryafar, H. Dewar, and an external reviewer for their helpful comments on the manuscript.

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4 FUNCTIONAL ANATOMY AND BIOMECHANICS OF FEEDING IN ELASMOBRANCHS CHERYL A.D. WILGA LARA A. FERRY

1. General Trophic Morphology 1.1. Skeletal Apparatus 1.2. Feeding Musculature 1.3. Jaw Suspension Mechanisms 1.4. Dentition 2. Feeding Behaviors 3. Biomechanical Models for Prey Capture 3.1. Feeding Sequence Phases 3.2. Suction Feeding Characteristics 3.3. Bite Feeding Characteristics 4. Modulation of Muscle Activity 5. Biomechanical Models for Prey Processing and Transport 6. Biomechanics of Filter Feeding 7. Biomechanics of Upper Jaw Protrusion 8. Ecophysiological Patterns

The morphology of the feeding apparatus in elasmobranchs has evolved a surprisingly wide range of modifications in a system with so few skeletal elements. As feeding mechanisms evolved from an ancestral biting mechanism in Paleozoic taxa, to incorporate suction, ram, and filter feeding mechanisms in modern taxa, the associated musculoskeletal system also diversified. Whereas the mechanical pattern for opening and closing the mouth clearly remains conserved, several different mechanisms have evolved for protruding and adducting the jaws that are related to feeding style, prey type, and ecological habitat. Modifications of the musculoskeletal architecture are commonly associated with those changes, although changes in motor activity pattern are few. Here we discuss these changes in the context of biomechanical, physiological, and ecological evolution. 153 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00004-3

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1. GENERAL TROPHIC MORPHOLOGY 1.1. Skeletal Apparatus The feeding apparatus of chondrichthyans is deceptively simple for a taxon that includes formidable predators that so spectacularly expose their teeth and jaws when feeding. Only ten articulating cartilages comprise the jaws and jaw support in sharks, seven in skates and rays, and three in chimeras. A rich and long history of anatomical research details the broad range of variation in the head and jaws of these captivating cartilaginous fishes (Gegenbaur, 1872; Gadow, 1888; Fu¨rbringer, 1903; Gregory, 1904; Marion, 1905; Allis, 1914; Daniel, 1934; Denison, 1937; Lightoller, 1939; Holmgren, 1941; Marinelli and Strenger, 1959; Nobiling, 1977; Compagno, 1988, 1999). These studies have provided a wealth of information for functional and biomechanical investigations of chondrichthyan feeding (see reviews by Motta and Wilga, 2001; Motta and Huber, 2012). The jaws and their supporting cartilages are thought to have evolved from anterior branchial arches that first functioned to enhance water flow during breathing and then became secondarily adapted for biting as they became bigger (Reif, 1982; Mallat, 1996; but see Smith, 1999; Wilga, 2010; Gillis et al., 2013). Branchial arches are composed of five articulating parts (Daniel, 1934). The two longest rod-like cartilages support gills and form a sideways V with their articulation at the apex pointed caudally and laterally, and their anterior ends pointed medially: these are the dorsal epibranchial and ventral ceratobranchial cartilages (Daniel, 1934). A short hypohyal cartilage connects the anterior end of each ceratobranchial to the single medial basibranchial, while the short pharyngobranchial cartilage at the anterior end of the epibranchial cartilage points caudally (Daniel, 1934). As the anteriormost branchial arch became more robust over time, it was able to pump more water over the gills to improve ventilatory performance, and then fortuitously became suitable for grabbing prey (Reif, 1982; Mallat, 1996). The second branchial arch evolved to support the jaws while the remaining branchial arches retained their ventilatory function. This first arch is now called the mandibular arch because of its additional function for feeding and consists of the dorsal palatoquadrate cartilage (now an epimandibular) and the ventral Meckel’s cartilage (now a ceratomandibular). The palatoquadrate and Meckel’s cartilages articulate with each other at the jaw joint and with their contralateral halves at an anterior symphysis (Daniel, 1934). The jaw joint has two quadratomandibular joints, which is characteristic of cladodont level taxa and above (Schaeffer, 1967). These dual jaw joints are oriented perpendicular to each other, in the horizontal and dorsoventral planes, preventing lateral motion and restricting jaw opening and closing to the dorsoventral plane (Motta and Wilga, 1995, 1999; Fig. 4.1). Some species have interconnecting labial cartilages

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Figure 4.1. Musculoskeletal morphology of the head of representative elasmobranchs. (A) Squaliformes, spiny dogfish, Squalus acanthias. (B) Orectolobiformes, nurse shark, Ginglymostoma cirratum. (C) Carcharhiniformes, lemon shark, Negaprion brevirostris. (D) Lamniformes, goblin

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Figure 4.1. (Continued)

shark, Mitsukurina owstoni. (E) Lamniformes, shortfin mako shark, Isurus oxyrinchus, on left; Lamniformes, white shark Carcharodon carcharius on right. (F) Carcharhiniformes, lemon shark, N. brevirostris, inset photo: right jaw joint separated to show the two articulations of the jaw joint. (G) Rhinobatiformes, Atlantic guitarfish, Rhinobatos lentiginous, dorsal (left), superficial ventral (middle), and deep ventral (right) views. Asterisk, position of the jaw joint; dashed gray line indicates occlusal plane, which extends to jaw joint in in-line jaw joints (scissor model); solid gray line connects occlusal plane to jaw joint in offset jaw joints (nutcracker model); BC, branchial constrictors; BY, basihyal; CA, coracoarcualis; CH, coracohyoideus; CHM, coracohyomandibularis; CM, coracomandibularis; CR, cranium; CU, cucullaris; CY, ceratohyal; DHM, depressor hyomandibularis; DM, depressor mandibularis; DR, depressor rostri; EPL, ethmopalatine ligament; EX, epaxialis; EY, eye; HC, hyoid constrictors; HX, hypaxialis; HY, hyomandibula; IM, intermandibularis; LH, levator hyomandibularis; LP, levator palatoquadrati; LR, levator rostri; MC, Meckel’s cartilage; NC, nasal capsule; EP, ethmoid process; OP, orbital process; OPL, orbital-palatine ligament; PNL, palatonasal ligament; PO, preorbitalis; POL, lateral preorbitalis; POM, medial preorbitalis; PQ, palatoquadrate; RO, rostrum; PQP, ascending process of palatoquadrate; RO, rostrum; RP, raphe overlying pericardium; SP, spiracularis; QJL, lateral quadratomandibular joint; QJM, medial quadratomandibular joint; QMA, anterior quadratomandibularis; QMD, dorsal quadratomandibularis; QME, deep quadratomandibularis; QMM, medial quadratomandibularis; QMP, posterior quadratomandibularis; QMV, ventral quadratomandibularis. Modified from Motta and Wilga (1995, 1999), Wilga and Motta (1998a,b), Wilga (2005).

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that lie along the edges of the jaws that pull a fold of skin across the sides of the gape as the mouth opens (see Fig. 4.1A muscle figure, and Fig. 4.1B skeletal and muscle figures). The pharyngo-, hypo-, and basi-mandibular elements have been lost in the mandibular arch. The second arch is now called the hyoid arch due to its new function as the jaw supporting mechanism. The dorsal hyomandibular cartilage (now an epihyal) articulates with the otic region of the chondrocranium at the proximal end and with the ventral ceratohyal cartilage at the distal end (Daniel, 1934; De Beer, 1937; Fig. 4.1). The single medial basihyal has been retained in the hyoid arch and interconnects the ceratohyal cartilages. The ceratohyal–basihyal cartilages are dissociated from the hyomandibular cartilage in skates and rays (Gregory, 1904). The mandibular arch articulates with the distal end of the hyomandibular cartilage near the jaw joint. The hyoid arch, under muscular control, greatly expands the buccal region to generate suction for ventilation and feeding and creates a large buccal area in bite feeders (Motta and Wilga, 2001; Motta and Huber, 2012). 1.2. Feeding Musculature The ventilatory muscles associated with the anterior branchial arches became modified as the jaws and hyoid took on an increasing role in feeding behavior (Fig. 4.1). The main groups of muscles that were retained in the mandibular and hyoid arches are the hypobranchials that depress the arch, adductors that compress the arch, and constrictors that elevate or compress the arch (Marian, 1905; Edgeworth, 1935; Miyake et al., 1992). Hypobranchial muscles associated with depressing the jaws (coracomandibularis) and hyoid (coracohyoideus–coracoarcualis complex) became hypertrophied relative to branchial arches, but otherwise are relatively conserved throughout modern lineages (Edgeworth, 1935; Miyake et al., 1992; Wilga et al., 2000; Summers and Ferry-Graham, 2003; Brainerd and FerryGraham, 2006; Dean et al., 2012; Fig. 4.1F and G). The coracomandibularis originates from the coracoid bar (scapulocoracoid cartilage) directly by muscular insertion in most taxa (i.e., Squalus, Negaprion, Ginglymostoma, Sphyrna, and Alopias) with some fibers emanating from the pericardium (Ginglymostoma) and from the deep hypobranchial raphe (tendinous sheath), which originates from the coracoid bar that overlies the coracoarcualis muscle in some taxa (Mustelus, Isurus; Daniel, 1934; Motta and Wilga, 1995, 1999; Wilga and Motta, 1998a,b, 2000; Wilga, 2005). In all taxa, the coracomandibularis is unpaired and inserts on Meckel’s cartilage adjacent to each side of the symphysis (Daniel, 1934; Motta and Wilga, 1995, 1999; Wilga and Motta, 1998a,b, 2000; Wilga, 2005). The common coracoarcualis originates from the pectoral girdle and inserts onto the coracohyoideus, and

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the coracohyoideus originates in turn from the coracoarcualis and inserts on the basihyal (Daniel, 1934; Wilga et al., 2000). The jaw and hyoid depressor muscles in actinopterygians differ from those of chondrichthyans. Lower jaw depression by the coracomandibularis muscles is the basal condition in gnathostomes (placoderms, coelacanths, and chondrichthyans; Wilga et al., 2001). The coracomandibularis was lost in Osteichthyes and was replaced by the protractor hyoideus muscle (Wilga et al., 2001). Fusion and modification of the intermandibularis and interhyoideus muscles produced the protractor hyoideus muscle (often referred to as the geniohyoideus) in actinopterygians (Edgeworth, 1935; Winterbottom, 1974). The coracohyoideus muscle, called the sternohyoideus in actinopterygians, became modified to depress the lower jaw in actinopterygians (Edgeworth, 1935; Winterbottom, 1974). The relatively simple adductor muscle that closes the branchial arches was lost in the hyoid arch and has been extensively modified as the jaws evolved. The adductor mandibulae complex of the mandibular arch is composed of the quadratomandibularis and preorbitalis muscles, which function to adduct and protract the jaws (Edgeworth, 1935; Lightoller, 1939; Vetter, 1874; Miyake et al., 1992; Motta and Wilga, 1995, 1999; Fig. 4.1A–E). The ventral quadratomandibularis muscle has remained relatively conserved, whereas the dorsal quadratomandibularis muscle has become subdivided in most lineages, with as many as five distinguishable parts (Marion, 1905; Daniel, 1934; Moss, 1972; Compagno, 1988; Shirai, 1996; Wilga et al., 2001; Wilga, 2005). The muscles involved with jaw protrusion and retraction have undergone more subdivision and altered attachment sites independently throughout phylogenetic history more so than any other muscle group. In the basal condition, a single preorbitalis muscle extends from the quadratomandibularis musculature at the jaw joint to the ventral region of the nasal capsule and functions to protract the upper jaw (Wilga et al., 2001). This condition is retained in Hexanchiformes, Squaliformes, and basal Lamniformes (Wilga et al., 2001; Fig. 4.1A, D, and E). The preorbitalis muscle is subdivided in several taxa, with some of the new divisions inserting onto the palatoquadrate cartilage (Fig. 4.1C and E; Carcharhiniformes and Lamnidae) or chondrocranium (Fig. 4.1B and G; Heterodontiformes, Orectolobiformes, Carcharhiniformes, Batoidea), but still functions to protract the upper jaw. In contrast, other new divisions extend between the chondrocranium and Meckel’s cartilage and function as jaw adductors (Fig. 4.1B and G; Heterodontiformes, Orectolobiformes, Batoidea; Marion, 1905; Daniel, 1934; Moss, 1972; Compagno, 1988; Shirai, 1996; Wilga and Motta, 1998b; Wilga et al., 2001; Wilga, 2005; Motta et al., 2008). The arch levator muscles evolved as a subdivision of the constrictor muscle sheet that compresses the arches (Marion, 1905; Miyake et al., 1992). The basal condition for the levator palatoquadrati is to have a

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single division that originates from the chondrocranium and inserts on the palatoquadrate cartilage to retract the upper jaw (Daniel, 1934; Wilga et al., 2001; Fig. 4.1A, D, E, and G). This muscle has subdivided once in heterodontiform and orectolobiform sharks but still functions to retract the upper jaw (Daniel, 1934; Nobiling, 1977; Motta and Wilga, 1999). As the cranium and jaws evolved and lengthened in carcharhinid sharks, the origin and orientation of the levator palatoquadrati changed its function to protraction of the upper jaw rather than retraction (Compagno, 1988; Motta et al., 1997; Wilga and Motta, 2000; Fig. 4.1C). In contrast, the levator hyomandibulae has remained largely conserved morphologically (undivided and extending from the chondrocranium and epaxialis musculature to the hyomandibular cartilage) and functionally (elevating the hyoid arch) in most taxa, but has modified insertion sites in a few groups; that is, the Carcharhinidae, Lamnidae, and Alopidae (Wilga et al., 2001; Wilga, 2005; Fig. 4.1A, B, D, E, and G). The constrictor muscles of the mandibular and hyoid arches, intermandibularis and interhyoideus, also remain relatively conserved (Lightoller, 1939; Miyake et al., 1992). The intermandibularis and interhyoideus muscles originate on the medial edges of Meckel’s and ceratohyal cartilages respectively and extend medially to merge with the contralateral fibers or to insert on the central aponeurosis overlying the coracomandibularis (Daniel, 1934; Motta and Wilga, 1995, 1999; Wilga and Motta, 1998a,b, 2000; Wilga, 2005). The interhyoideus is just deep to the intermandibularis, which completely covers it (Fig. 4.1F). Batoids have several additional muscles that have subdivided from the constrictor and hypobranchial muscles. Levator and depressor rostri muscles subdivided from the constrictor hyoideus to elevate and depress the rostrum (Marion, 1905; Miyake et al., 1992; Fig. 4.1G). A depressor mandibulae also subdivided from the constrictor hyoideus muscle sheet and depresses Meckel’s cartilage (Marion, 1905; Miyake et al., 1992; Wilga and Motta, 1998b). Batoids also have two unique muscles that depress the hyomandibular cartilage, a depressor hyomandibularis and coracohyomandibularis muscle (Marion, 1905; Miyake et al., 1992; Wilga and Motta, 1998b). Substantial variation exists in the jaw and hyoid arch muscles of skates and rays, particularly between durophagous and nondurophagous stingrays (Kolmann et al., 2014). 1.3. Jaw Suspension Mechanisms The upper jaw is noticeably exposed as it protracts during feeding in many elasmobranch species. The extent of that movement away from the cranium is determined by the size and shape of the jaw suspension. There are more morphological and functional varieties of jaw suspension types in the Chondrichthyes than in any other vertebrate group: holostyly, euhyostyly, amphistyly (Paleozoic and Modern types), orbitostyly, hyostyly (at least

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Figure 4.2. Evolution of jaw suspension modes in chondrichthyans. Biting with an autodiastylic or amphistylic jaw suspension appears to be the basal feeding mode. Suction and filter feeding modes also evolved with hyostyly and euhyostyly, but only suction in orbitostyly. Ceratohyal in green; EP, ethmoid articulation (rope-like); Hyomandibula in red; PN, palatobasal articulation (rope-like); Meckel’s cartilage in blue; OP, orbital articulation (sleeve-like); Palatoquadrate in yellow when not fused with cranium, gray when fused with cranium (Holocephali); Cranium in gray; PT, postorbital articulation (sleeve-like). B, bite; F, filter; and S, suction, feeding types. Modified from Wilga (2002) and Wilga et al. (2007).

four Modern types; Gregory, 1904; Wilga, 2002, 2005; Maisey, 1980; Fig. 4.2). An autodiastylic ancestor was presumed to have given rise to holostyly, amphistyly, and euhyostyly, with amphistyly then giving rise to orbitostyly and hyostyly (De Beer and Moy-Thomas, 1935). Chimeras are holostylic, with the palatoquadrate fused to the chondrocranium and the hyoid arch being functionally a branchial arch that supports the fleshy operculum with no connection to the jaws (Patterson, 1965; Grogan and Lund, 2000; Gillis et al., 2011). In all elasmobranchs, the jaws are suspended from the chondrocranium by a ligamentous articulation of the hyomandibular cartilage with Meckel’s cartilage near the jaw joint; this is broadly defined as being hyostylic (Maisey, 1980). Therefore, the jaw suspension types in modern elasmobranchs are all functionally “hyostylic” (Maisey, 1980). In sharks, the palatoquadrate also articulates with the chondrocranium by way of one or two additional joints that differ in morphology by

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suspension type, not only among extant taxonomic groups, but also between extinct and extant taxa (Wilga, 2002, 2005; Maisey, 2008). These additional palatoquadrate-cranial articulations may take the form of shallow gliding joints (postorbital in amphistyly), well-defined sockets with processes (orbital in orbitostyly; ethmoidal in orectolobiform and heterodontiform hyostyly), or ligaments emanating from a simple bump-like process without a well-defined cranial socket (ethmoidal in carcharhiniform and lamniform hyostyly; palatonasal in lamniform hyostyly). These may have connecting ligaments that are solid and rope-like (ethmoidal, palatonasal) or hollow and sleeve-like (orbital, postorbital; Wilga, 2002, 2005). Longer ligaments allow the upper jaw to be protracted further from the cranium as in the white shark (Carcharodon carcharias; lamnid hyostylic articulation) and spiny dogfish (orbitostylic). Whereas those with two palatoquadrate-cranial articulations may be capable of undergoing little protrusion, as exemplified in sevengill sharks (amphistylic with orbital and postorbital articulations and short ligaments), or may be able to undergo extensive protrusion, as observed in the goblin shark (Mitsukurina owstoni; hyostylic with ethmoidal and palatonasal articulations with long ligaments; Wilga, 2002, 2005). Skates and rays lack the palatoquadrate-cranial articulations, therefore the hyomandibular cartilage is the sole supporting element of the jaws and this configuration is euhyostylic (truly only suspended by the hyomandibulae; Gregory, 1904). 1.4. Dentition Chondrichthyan tooth types vary from the well-known cutting and tearing morphologies to those that are used in clutching or grinding food (Cappetta, 1987). Clutching teeth are used for grasping and holding smaller soft-bodied fish and invertebrates, and are characterized by one large central cusp with one or more smaller lateral cusps. Examples of this tooth type are found in orectolobiform species like the nurse shark (Ginglymostoma cirratum), and the bamboo shark (Chiloscyllium plagiosum; Fig. 4.3A). Tearing teeth are used for piercing and tearing larger slippery prey, like most fish, and may have small lateral cusps, as in the sandtiger shark (Carcharias taurus; Fig. 4.3B). Sharp teeth direct forces into soft flesh to increase the effectiveness of a bite (Whitenack and Motta, 2010). Cutting teeth may take the form of one large triangular cusp with serrations along the edges for gouging chunks from oversized prey, as in the white shark C. carcharias. Cutting teeth also may take the form of backward pointed blades, that may or may not be serrated, for sawing through large prey, as does the tiger shark (Galeocerdo cuvier) when feeding on sea turtles, and the spiny dogfish when feeding on large fish (Fig. 4.3C). Notches or indentations in the teeth are thought to enhance and direct tearing forces into soft flesh

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Figure 4.3. Representative tooth types in elasmobranchs. (A) Clutching teeth in bamboo sharks (Chiloscyllium plagiosum) (normal position). (B) Tearing teeth in sandtiger sharks (Carcharias taurus). (C) Cutting teeth in spiny dogfish (Squalus acanthias). (D) Crushing teeth in skates (Raja sp.). (E) Grinding teeth in rays (Myliobatis sp.). (F) Clutching–grinding teeth in horn sharks (Heterodontus sp.). (G) Depressed crushing position of C. plagiosum teeth. From Ramsay and Wilga (2007).

(Whitenack et al., 2011). Some sharks use small, molar-like teeth to crush small crustaceans, such as shrimp, like many skates and the smoothhound shark (Mustelus sp.; Fig. 4.3D), while myliobatid rays have pavement teeth that are used to grind the shells of mollusks (Summers, 2000; Summers et al., 2004; Fig. 4.3E). Some sharks have a heterodont dentition, with different tooth types in the upper and lower jaws, or different tooth types in the anterior and posterior regions of the jaws. For example, the sandbar shark (Carcharhinus plumbeus) has piercing teeth on the lower jaw for holding and cutting teeth in the upper jaw, whereas the bonnethead (Sphyrna tiburo) and horn sharks (Heterodontus sp.) have clutching teeth in the anterior region of the jaws for grasping prey and molars in the posterior region to which they move prey, such as crabs or echinoderms, for crushing (Fig. 4.3F). The teeth are embedded in the oral epithelium overlying the jaws in most elasmobranchs, but may form a flattened interconnected pavementlike surface in some species that crush hard prey. The teeth are held upright by elastic ligaments in most orectolobid species, however, and when a tooth encounters prey harder than can be pierced, it is pushed inward and the outer surface of the tooth is then used as an uneven crushing surface (Ramsay and Wilga, 2007; Fig. 4.3G).

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Figure 4.4. Jaw and tooth position. (A) Left lateral schematic of the jaws and teeth of Helicoprion davisii (left) and a modern shark (right). (B) Left lateral (left), left medial (right), and ventral (bottom) views of the jaws and tooth whorl of H. davisii. BP, basal process (articulation with cranium); EC, encasing cartilage; EP, ethmoid process (articulation with cranium); FT, functional teeth; MC, Meckel’s cartilage; LB, labial cartilage; NT, new teeth; OE, oral epithelium; PQ, palatoquadrate cartilage; QF, quadrate fossa (for AM muscles); RT, tooth root. After Tapanila et al. (2013) and Ramsay et al. (2015).

Most chondrichthyans continuously replace their teeth by generating new rows of teeth along the medial surface of the jaws (Fig. 4.4, NT). These move upward toward the margin of the jaws in an escalator-like fashion. However, one row of symphysial teeth in an extinct chondrichthyan (Helicoprion) formed a single long tooth root base that curled around in volutions as new teeth developed, producing a saw-blade like tooth whorl (Tapanila et al., 2013; Fig. 4.4). Older teeth were encased in cartilage that along with other supporting labial cartilages stabilized the tooth whorl between the lower and upper jaws preventing the teeth from sawing through the cranium (Tapanila et al., 2013; Ramsay et al., 2015). The tooth whorl of Helicoprion was likely used to cut and push soft prey, such as the arms of the

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ammonoids and nautilods that were abundant at the same time, into the mouth (Ramsay et al., 2015). The occlusal plane of the jaws may be inline or offset from the jaw joint in sharks. Species where the jaw joint is offset from the occlusal plane, such as bamboo sharks, typically use the jaws as crushing or grinding tools, like mammalian herbivores (Ramsay and Wilga, 2007; Fig. 4.1B). An offset jaw joint allows the upper and lower jaws to close in parallel and the teeth to contact simultaneously like an old-fashioned nutcracker (Maynard and Savage, 1959). Spiny dogfish (Squalus acanthias) also have offset jaw joints, and use their cutting teeth and jaws to grasp fish and then shake their heads vigorously from side to side for an effective cutting tool (Wilga and Motta, 1998a; Fig. 4.1A). In contrast, species where the occlusal plane of the jaws is inline with the jaw joint use their jaws as shearing or cutting tools, much like mammalian carnivores (Ramsay and Wilga, 2007). Those species with an inline jaw joint, like lemon, goblin, and white sharks, close the jaws sequentially from the joint end first then out to the tips like scissors (Maynard and Savage, 1959; Fig. 4.1C–E). Filter-feeding evolved relatively recently independently in four elasmobranch lineages: twice in Lamniformes, once in Orectolobiformes, and once in Myliobatiformes (Paig-Tran and Summers, 2014). Filter feeding species largely lack true teeth and instead use branchial filters (modified gill rakers) to extract zooplankton from the water column. There are two known types of branchial filters (Fig. 4.5). One consists of a robust, flattened filter pad of highly branching filaments to create a mesh-like structure (e.g., whale sharks, Rhincodon typus, Orectolobiformes; and mantas and devil rays, Manta spp., Myliobatiformes; Motta et al., 2010; Paig-Tran and Summers, 2014). The other consists of elongated filaments arranged side by side and more closely resembles the comb-like gill raker structure found in bony fishes (e.g., the lamniform basking, Cetorhinus maximus, and megamouth, Megachasma pelagios, sharks). With the exception of basking sharks, the branchial filter is composed of a hyaline cartilage skeleton surrounded by a layer of highly organized connective tissue that may function for support. Basking sharks have branchial filters composed entirely of smooth keratin. Megamouth sharks and most of the myliobatiform rays also have tooth-like dermal denticles along the surface of the filter pad, possibly to prevent being damaged by large particles (Paig-Tran and Summers, 2014). 2. FEEDING BEHAVIORS All chondrichthyans are carnivorous predators, and use suction, bite, ram feeding, or a combination of these behaviors, to capture prey. Most elasmobranchs use ram feeding (swimming toward prey) to some degree in

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Figure 4.5. Branchial filters and filtering mechanisms (modified from Paig-Tran et al., 2011, 2013). The filter pores, or openings, can be exactly the same in each of the three models. Yet, the direction of the water flow relative to the openings creates differences in the sizes of particles that are retained. (A) Dead-end sieving is much like a strainer. Particles are retained passively, based upon their ability to pass through the pores in the filter. (B) With cross-flow filtration, fewer particles escape through the pores. Water motion retains even small particles and keeps many of them from contacting, and therefore passing through, the pores. Some small particles will be carried through the pores by the effluent that passes through the pores. This perpendicular flow, however, also helps to prevent pore clogging. (C) In cross-flow with tangential shearing, the vortices formed at the edges of the pores (caused by the way in which flow impacts those edges), resuspend even the smallest of particles. Almost no flow passes through the pores, as the vortices redirect water, and particles, back out of the pore openings.

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Figure 4.6. Feeding sequence and specialized feeding morphology in sharks. (A) Bite feeding in the lemon shark (Negaprion brevirostris) and (B) suction feeding in spiny dogfish (Squalus acanthias). Arrows indicate relative prey and predator movement from the right to the left (modified from Wilga et al., 2007). (C) Head and cranial skeleton of a bite feeder, bonnethead shark (Sphyrna tiburo), and a suction feeder, white-spotted bamboo (Chiloscyllium plagiosum) at peak gape. In C. plagiosum, the large labial cartilages pull a curtain of skin forward to laterally occlude the gape. Note the slightly protractile upper jaw of S. tiburo that moves away from the cranium, whereas the upper jaw of C. plagiosum slides forward against the chondrocranium. BY, basihyal; CR, cranium; CY, ceratohyal; HY, hyomandibula; LB, labial cartilages; MC, Meckel’s cartilage; NC, nasal capsule; PQ, palatoquadrate cartilage. After Wilga et al. (2007).

capturing prey. Bite feeders use ram feeding to approach potential prey and then seize the prey with the jaws. Although suction feeders may use ram feeding to approach potential prey, they also use suction to draw the prey into the mouth, where it may then be seized by the jaws or drawn completely into the buccal cavity, bypassing the jaws. Biting by grasping and tearing prey is probably the basal mode of feeding in chondrichthyans, at least at the cladodont level (Schaeffer, 1967; Schaeffer and Williams, 1977). Bite feeders typically have relatively long jaws with a wide lateral gape, which permits a wide degree of mouth opening and thus enabling a larger bite area (Schaeffer, 1967; Moss, 1977; Fig. 4.6). In contrast, the evolution of shorter jaws and more mobile jaw suspension in many recent and extant taxa enabled jaw protrusion and suction feeding (Schaeffer, 1967; Moss, 1977). Species strongly reliant on suction feeding often possess distinctive characteristics, which include: (i) large labial cartilages that form “cheeks” to occlude the sides of the mouth; (ii) a relatively small mouth opening (compared with the aforementioned species); (iii) the capacity for rapid expansion of the buccal

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cavity, which is often facilitated by (iv) hypertrophied hypobranchial muscles. This serves to focus suction inflow to directly in front of the mouth opening (Moss, 1977; Motta and Wilga, 2001; Wilga et al., 2007; Nauwelaerts et al., 2008; Fig. 4.6). Filter feeding elasmobranchs use suction (whale and megamouth) or ram (whale, basking, cownose, manta) feeding to engulf clouds of zooplankton and fish (Sanderson and Wassersug, 1993; Nakaya et al., 2008). Suction filter feeders possess many of the same characteristics as the more generalized suction feeding predators described above, as the generation of an inward current of water is still required. Ram filter feeders utilize a large mouth opening to surround and engulf the zooplankton. Both suction and ram filter feeders rely on an enlarged buccal cavity to contain massive volumes of water, and a large branchial surface area for filtering prey from that water (Paig-Tran et al., 2011).

3. BIOMECHANICAL MODELS FOR PREY CAPTURE 3.1. Feeding Sequence Phases Musculoskeletal mechanisms for prey capture in phylogenetically diverse species reveal several variations on a common theme, associated with evolutionary changes in jaw kinesis. Feeding events have expansive mouth opening, compressive mouth closing, and recovery to resting state phases, with each characterized by distinct muscle activity patterns and associated skeletal movements (Ferry-Graham, 1997a,b, 1998a,b; Motta et al., 1997, 2002, 2008; Wilga and Motta, 1998a,b, 2000; Figs 4.7–4.9). Unlike teleost fishes, which have a preparatory phase that precedes the expansive phase (Liem, 1978; Lauder, 1983; Lauder and Shaffer, 1993; Ferry-Graham and Lauder, 2001; Westneat, 2006), elasmobranchs only occasionally have a preparatory phase (Motta et al., 1997; Wilga and Motta, 1998a,b; Wilga and Sanford, 2008). A preparatory phase is closely linked with the production of an explosive suction feeding event and is characterized by a short compressive phase prior to mouth opening that enhances the volumetric change during the suction phase. In the expansive phase of mouth opening, the lower jaw and hyoid are depressed, and the head may be raised. Head elevation varies by the position of the prey relative to the predator and whether the strike is on the substrate or in the water column. The hypobranchial and epaxial muscles are simultaneously active to depress the lower jaw and hyoid arch and raise the head posterodorsally (Motta et al., 1997; Wilga and Motta, 1998a,b, 2000). Depression of the lower jaw pulls the distal end of the hyomandibular

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Figure 4.7. Representative biomechanical models of shark feeding in a squalean shark (left, spiny dogfish Squalus acanthias), a galean shark (center, lemon Negaprion brevirostris), and a batoid (right, Atlantic guitarfish Rhinobatos lentiginosus). (A) Expansive phase. (B) Compressive phase. Squalus represents cutting of prey where the jaws occlude near the middle of lower jaw elevation. Negaprion represents gouging where the lower jaw is held at maximum depression by large prey while the upper jaw is protracted to perform the gouging cut. Rhinobatos represents grasping of prey from the substrate by skates and rays. (C) Recovery phase. Black lines indicate muscles; black arrows indicate the direction of muscle contraction; and gray arrows indicate the direction of skeletal movement. BY, basihyal; CA, coracoarcualis; CH, coracohyoideus; CHM, coracohyomandibularis; CM, coracomandibularis; CR, cranium; CY, ceratohyal; DHM, depressor hyomandibularis; DM, depressor mandibularis; EX, epaxialis; EPL, ethmopalatine ligament (curly lines); HY, hyomandibula; LH, levator hyomandibularis; LP, levator palatoquadrati; MC, Meckel’s cartilage; PO, preorbitalis; POD, dorsal preorbitalis; POV, ventral preorbitalis; PQ, palatoquadrate; QM, quadratomandibularis. Modified from Motta et al. (1997) and Wilga and Motta (1998a,b).

cartilage ventrally, which in turn rotates the jaw apparatus away from the cranium. This may be why the levator palatoquadrati muscle is sometimes active shortly after mouth opening in squalean and batoid taxa; that is, to maintain connection of the upper jaw with the cranium as the lower jaw is protruded. Without this bracing, the upper jaw is at risk of deflecting prey

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Figure 4.8. Representative motor activity pattern of six muscles during capture, processing, and transport events in a galean shark, bonnethead (Sphyrna tiburo). 1, onset of lower jaw depression; 2, maximum lower jaw depression; 3, maximum upper jaw protrusion; 4, jaw closure; 5, jaw closure after crushing prey. EX, epaxialis; CM, coracomandibularis; LH, levator hyomandibularis; LP, levator palatoquadrati; PO, preorbitalis; QM, quadratomandibularis. Scale bar=200 ms. From Wilga and Motta (2000).

Figure 4.9. Composite diagram of synchronized means of kinematic (top) and motor (bottom) patterns during prey capture events in a squalean shark (left, spiny dogfish Squalus acanthias) and a galean shark (right, lemon Negaprion brevirostris). Kinematic bars: black, onset of event to maximum; gray, maximum event to end; cross, maximum event. Motor bars: black, onset and duration of muscle burst; white, onset and duration of second muscle burst. %, proportion of events in which the muscle burst was active if less than 100%. Error bars indicate 1 SEM. EX, epaxialis; CA, coracoarcualis; CB, coracobranchialis; CH, coracohyoideus; CM, coracomandibularis; HL, head lift; HY, hyoid depression; LB, labial extension; LH, levator hyomandibularis; LJ, lower jaw depression; LP, levator palatoquadrati; PG, maximum gape; PM, prey movement; PO, preorbitalis; POD, dorsal preorbitalis; POV, ventral preorbitalis; QMD, dorsal quadratomandibularis; QMV, ventral quadratomandibularis; UJ, upper jaw protrusion. After Motta et al. (1997) and Wilga and Motta (1998a,b).

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drawn toward the mouth. The motor activity pattern for the muscles involved in lower jaw depression and cranial elevation is conserved across elasmobranch taxa (Wilga et al., 2000). The posterior end of the upper jaw at the jaw joint can be partially protracted, rotated downward as the lower jaw and hyoid are depressed. While the jaws appear to be rotated outward at the symphysis in sharks during this mouth opening phase, the jaws are rotated medially in many batoids, except in those with crushing pads overlying a fused symphyses (Wilga and Motta, 1998b; Dean and Motta, 2004; Dean et al., 2006). In the compressive phase, the upper jaw is protracted as the lower jaw is elevated, thus both jaws contribute to closing the mouth. At this time, the jaws and teeth are revealed in bite feeders, while in suction feeders the labial cartilages are pulled forward to draw a curtain of skin across the sides of the mouth (to form “cheeks”), obscuring the teeth and jaws. However, upper jaw protraction occurs during the expansive phase in torpedo (Narcine brasiliensis) and cownose rays due to anatomical coupling of the jaws in an extreme jaw protraction mechanism (Dean and Motta, 2004; Sasko et al., 2006). The quadratomandibularis muscle divisions are simultaneously activated to adduct the jaws toward each other and in doing so protract the upper jaw away from the cranium particularly when large prey hinders lower jaw elevation (Motta et al., 1997, 2008; Wilga and Motta, 1998a,b, 2000). The preorbitalis muscle (original single or dorsal preorbitalis) activates shortly thereafter and, by pulling the jaw joint region anteriorly, forces the upper jaw to move down the cranial grooves or notches into the protracted position (Motta et al., 1997, 2008; Wilga and Motta, 1998a). The ventral preorbitalis muscle functions like the quadratomandibularis muscles, from which it arose from, in adducting the upper jaw toward the lower jaw (Motta et al., 1997, 2008; Wilga and Motta, 2000). The mouth is closed during the compressive phase, with protraction of the upper jaw decreasing the time to jaw closure (Wilga, 2002). This too is different from teleosts, in which the upper jaw is protracted during the expansive phase and typically retracts prior to the jaws closing on or around the food item (Lauder and Shaffer, 1993; Westneat, 2006). In the recovery phase, the jaws are elevated back under the cranium. Activity of the levator palatoquadrati and levator hyomandibularis muscles may begin at the end of the compressive phase in squalean sharks and batoids (Wilga and Motta, 1998a,b). This acts to elevate or retract the jaws by pulling the upper jaw and hyomandibula back under the cranium. The levator hyomandibulae has additional insertions onto the lower jaw in alopid and lamnid sharks and provides a more direct means of elevating the jaws (Wilga, 2005). This theme is remarkably conserved among species that rely to any degree on suction.

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3.2. Suction Feeding Characteristics Compared to teleosts, few elasmobranchs are truly specialized for suction feeding. Orectolobiform sharks (except wobbegongs), and perhaps heterodontiforms, are the only shark species that are specialized for capturing prey by extreme suction. Hyoid arch movement is a key component in the suction feeding mechanism and differs fundamentally between teleosts and elasmobranchs. In suction feeding teleosts, buccal expansion is accomplished by simultaneous ventral depression of the ceratohyal-basihyal complex and lateral expansion of the hyomandibulae (Ferry-Graham and Lauder, 2001; Westneat, 2006). However, ceratohyal–basihyal complex depression alone drives fluid flow into the mouth during suction feeding, as well as ventilation, in sharks and batoids (Wilga, 2008, 2010). The sides or “cheeks” of the buccal region are compressed medially due to the laterally (sharks) or anteriorly (batoids) directed hyomandibular tips that are constrained to move medially to open the mouth (Wilga, 2008, 2010; Fig. 4.10).

Figure 4.10. Fundamental difference in the suction feeding mechanism between elasmobranchs and teleosts. Hyoid area width decreases with increased gape size in sharks with laterally directed hyomandibular cartilages and skates and rays, which have anterior directed hyomandibular cartilages. In contrast, hyoid area width increases in sharks with posterior directed hyomandibular cartilages and teleosts with ventrally directly hyomandibular bones. Arrows show direction of hyoid area changes and hyomandibular movement from onset to peak gape. Dotted lines show the resting position of the hyomandibular and Meckel’s cartilages. BY, basihyal; CR, cranium; CY, ceratohyal; HY, hyomandibula; I, interhyal; S, suspensorium. After Wilga (2008).

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Despite this apparent handicap compared to teleosts, elasmobranchs can generate substantial suction pressure during feeding. Nurse (G. cirratum), bamboo (C. plagiosum), and leopard (Triakis semifasciata) sharks, and lesser electric rays (N. brasiliensis) generate subambient buccal pressures as low as 110 kPa (mean 21), 99 kPa (mean 21), 12 kPa (mean 5.5), and 31 kPa (mean 21.7) respectively during suction feeding (Dean and Motta, 2004; Wilga et al., 2007; Lowry and Motta, 2008). Suction pressure for the much smaller bluegill sunfish (Lepomis macrochirus; 60 kPa), banded cichlid (Heros severus; 20 kPa), and largemouth bass (Micropterus salmoides; 20 kPa) remain impressive (Lauder, 1980; Norton and Brainerd, 1993; Sanford and Wainwright, 2002; Svanback et al., 2002). Like bluegill sunfish, bamboo sharks foraging in the water column capture prey caught within a parcel of fluid up to one-mouth diameter away from the mouth (Day et al., 2005; Nauwelaerts et al., 2008; Fig. 4.11). Foraging close to a substrate

Figure 4.11. Fluid field generated during feeding in elasmobranchs. (Top) White-spotted bamboo sharks, Chiloscyllium plagiosum. Prey capture on the substrate extends effective suction distance compared to that in the water column. (Middle) Fluid velocity area is 1.6 fold larger in successful strikes and prey transports compared to missed strikes. (Bottom) Urolophus halleri generates strong suction flow using the flexible rostrum against the substrate to draw prey toward the mouth. In contrast, Leucoraja erinacea generates strong compressive flow using the rostrum as a paddle and relatively weak suction flow. Red colors indicate faster water velocity than blue colors. After Nauwelaerts et al. (2007, 2008) and Wilga et al. (2012).

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amplifies the effective suction distance up to 2.5 times (mouth diameter) in bamboo sharks due to ground effects (Nauwelaerts et al., 2007; Fig. 4.11).

3.3. Bite Feeding Characteristics Bite feeding elasmobranchs have relatively long backwardly directed hyomandibulae that move outward as the ceratohyal–basihyal complex is depressed, as in bite and suction feeding teleosts, but function instead to increase gape size (Wilga, 2008; Fig. 4.10). Accordingly, bite feeders generate little negative pressure during feeding: 2.1 kPa in spiny dogfish (S. acanthias), 1.4 kPa in little skate (Leucoraja erinacea), and 10 kPa in peacock cichlids (Aulonocara hansbaenschi; Wilga et al., 2007). This fundamental difference in the suction feeding mechanism between teleosts and elasmobranchs is a result of morphological divergence in hyoid arch morphology (Wilga, 2008). In bite and ram-feeding predators, the expansive and recovery phases are less important because generating a current of water through the head is not essential for prey capture. The relative timings and durations of skeletal movements during these two phases may vary markedly from species to species. The compressive phase, however, is of major importance for the creation of a strong or forceful bite to tear, break, or otherwise gain access to a small enough piece of the food item for transporting and swallowing. Here we see changes in the teeth and jaws, relative to those of suction feeders, which enhance the biomechanical production of force. Muscles may be hypertrophied, and tooth shape may vary to increase the effectiveness of the bite (see Fig. 4.3). Bite force has been measured using bite force transducers or calculated using physiological cross-sectional area for several chondrichthyan species with some surprising results. The horn shark (Heterodontus francisci) has the greatest measured bite force (159 N), with the blacktip shark (Carcharhinus limbatus) close behind (107 N). This is followed by the bamboo shark (C. plagiosum; 62 N), the bonnethead (S. tiburo; 26 N), and the spiny dogfish (S. acanthias; 15 N) (Huber and Motta, 2004; Huber et al., 2008; Mara et al., 2010). Theoretical bite force for the white shark (C. carcharias) is an astonishing 17,652 N, with Helicoprion davisii being estimated to generate about half that at 8,246 N, and the bull shark (Carcharhinus leucas) well behind at 2,128 N (Huber et al., 2008; Habegger et al., 2012; Ramsay et al., 2015). The primary determinant of greater bite force is greater body size (isometric relationship), although jaw length, modification of muscle insertion, and muscle cross-sectional area are also implicated in achieving high mass-specific bite force (Habegger et al., 2012).

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Clearly, the bite mechanism of various shark species are well suited to cutting through relatively tough prey like fish, to slicing through harder prey like sea turtle shells and seal limb bones, and even to crush mollusk and crab shells. Such high bite forces are even more impressive when one realizes that, although the teeth are composed of bone, the jaws are cartilaginous. Nonvertebral cartilaginous elements in elasmobranchs are comprised of an inner core of hyaline-like uncalcified cartilage surrounded by an outer covering of tessellated cartilage (Dean and Summers, 2006; Fig. 4.12). Thicker tessellated layers in the jaws and hyoid arch functions to stiffen the cartilage (Dingerkus et al., 1991; Summers, 2000; Dean and Summers, 2006; Balaban et al., 2015). The second moment of area (increases when more material is further from the center) of the ceratohyal cartilage is higher in suction feeding sharks than bite feeding sharks (Tomita et al., 2011). This indicates that they have increased resistance to the large bending stresses generated during suction feeding (Tomita et al., 2011). The hyomandibular cartilage of bamboo sharks (C. plagiosum), a specialized suction feeder, is more heavily calcified and is stiffer (has a higher Young’s modulus) under compression than spiny dogfish (S. acanthias), dusky smoothhounds (Mustelus canis), and sandbar sharks (C. plumbeus), which rely more on biting to capture their prey (Balaban et al., 2015). Indeed, in a theoretical computer simulation of biting in white sharks (C. carcharias) jaws made of cartilage had greater deformation compared to the same jaws made of bone (Wroe et al., 2008). This arrangement of tessellated blocks interconnected by fibrous joints allows the outer cartilage to be stronger, compared to the inner core of unmineralized cartilage, while also remaining flexible. Accordingly, Poisson’s ratio (width to length changes under compression) is highly variable among species ranging from 2.3  10 5 to 4.3  10 1, indicating that interspecific differences likely exist in cartilage performance depending on prey type and load experienced by the jaws (Balaban et al., 2015).

4. MODULATION OF MUSCLE ACTIVITY Some elasmobranch species are capable of modulating jaw muscle activity based on prey type. Complex prey types, such as crab, shrimp, whole fish or squid typically elicit greater asynchronous bilateral activity of the quadratomandibularis and preorbitalis muscles than do simple prey types (pieces of the same or small fish; Gerry et al., 2008). The trophic generalists, such as the spiny dogfish and little skate (L. erinacea) modulate bilateral jaw adductor muscle activity depending on prey type, whereas the

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Figure 4.12. Morphology and mechanics of tessellated elasmobranch cartilage. (A) Schematic of a cross-section of Meckel’s cartilage of a round stingray Urobatis halleri. UC, uncalcified to calcified cartilage interface; Blue square delimits one tesseral block (after Dean and Summers, 2006). Photos of hyomandibular surface showing blocks of tesserae (brownish) and interconnecting ligaments (whitish) in the (B) spiny dogfish Squalus acanthias and (C) little skate Leucoraja erinacea. (D) Plot of Young’s modulus versus percent mineralization in four shark species with associated cross-sections: B white-spotted bamboo Chiloscyllium plagiosum; D, spiny dogfish Squalus acanthias; M, dusky smoothhound Mustelus canis; and S, sandbar Carcharhinus plumbeus. After Balaban et al. (2015).

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trophic specialists, such as the bamboo and smoothhound sharks, activate the jaw muscles synchronously for all prey types (Gerry et al., 2008, 2010). Synchronous activation of the jaw adductors increases bite force, which is particularly beneficial for durophagous (hard prey feeding) species like the bamboo and smoothhound sharks. Little skates have the greatest range of variability and are capable of activating the jaw muscles bilaterally synchronously (at the same time), bilaterally asynchronously (alternating activation), or unilaterally only (activation of one side only; Gerry et al., 2008, 2010). Processing of prey elicits greater asynchronous muscle activity than does prey capture with head-shaking evincing alternating bilateral activation as the head is moved from side to side, while biting of prey in one side of the jaws reveals completely unilateral activation (Wilga and Motta, 1998a; Gerry et al., 2008, 2010). 5. BIOMECHANICAL MODELS FOR PREY PROCESSING AND TRANSPORT Prey processing and transport mechanisms are similar to those of prey capture, but are of shorter duration, and are accompanied by limited skeletal excursions (Gillis and Lauder, 1995; Ferry-Graham, 1997b; Motta et al., 1997; Wilga and Motta, 1998a,b, 2000). Similarly, mouth opening in processing and transport events is shorter in duration than capture events to lessen the chance of prey escaping from the buccal cavity. Hyoid depression is of similar duration to capture events, enabling the generation of suction needed to reposition the prey for processing or swallowing (Gillis and Lauder, 1995; Ferry-Graham, 1997b; Motta et al., 1997; Wilga and Motta, 1998a,b, 2000; Wilga et al., 2012). Accordingly, the fluid field generated during successful captures is similar to that in the transporting of prey in the bamboo shark (Nauwelaerts et al., 2008; Fig. 4.11). This phenomenon appears to be a plesiomorphic trait among aquatic feeding fish and amphibians (Gillis and Lauder, 1995). Not surprising, the fluid field generated in missed strikes is smaller than that during successful captures, which indicates less effort or lack of motivation by the predator, bamboo sharks in this case (Nauwelaerts et al., 2008; Fig. 4.11). A preparatory phase, which includes activation of the jaw and hyoid levator muscles, and occasionally the jaw adductor muscles during the expansive phase, often occurs after a missed strike prior to a subsequent successful strike, and also during consecutive processing events (suction or bite) in the lemon shark (Negaprion brevirostris), spiny dogfish (S. acanthias), and guitarfish (Rhinobatos lentiginosus; Motta et al., 1997; Wilga and Motta, 1998a,b; Wilga and Sanford, 2008).

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Batoids use the body to direct fluid flow when handling prey. Morphological differences between skates and rays drive behavioral differences in prey handling, which results in divergent fluid flow patterns. The round stingray (Urolophus halleri) will press its flexible rostrum and pectoral fins against the substrate and form a tent with the body to generate suction inflow under the body to uncover buried prey (Wilga et al., 2012; Fig. 4.11). Atlantic cownose rays fluidize sand by blowing at it and then enclose uncovered prey items between the cephalic lobs (Sasko et al., 2006). In contrast, the relatively stiff rostrum of the little skate generates little suction when elevated, instead the rostrum is used as a paddle to strike prey or to push a considerable parcel of fluid to uncover buried prey (Wilga et al., 2012; Fig. 4.11). In hard prey specialists, acquiring the prey item is not a particularly challenging task, but processing the prey item and breaking it apart to gain access to the nutritive portions may be. The jaws of such durophagous species may be reinforced. This often takes the form of multiple layers of calcification, or tesserae (Summers et al., 2004; Fig. 4.12), with or without the addition of struts within the cartilage meshwork to resist deformation (Dean et al., 2006; Summers, 2000; Ferry-Graham et al., 2010). Importantly, the jaws can act as a lever system to amplify the force produced by the jaw adductor muscles (Summers, 2000). The upper and lower jaws are, in the mechanical sense, rigid bars with inextensible ligaments that limit gape expansion and link the lateral margins of the jaw together. The jaws act as a second order lever system, with the adductor on one side providing an input force, the ligaments on the other side forming the fulcrum, and the prey item between them receiving the output force. This lever system multiplies the forces imparted onto the prey item by the biting or crushing plates (Summers, 2000). Positive allometry in this system of jaw levers and jaw muscles over ontogeny in horn sharks (H. francisci) and spotted ratfish (Hyodrolagus colliei) allows them to feed on hard prey earlier in their life history than if they underwent isometric growth (Huber et al., 2008; Kolmann and Huber, 2009). Similarly, size dependent changes in feeding performance can restrict behavior, obligate prey capture by suction in bamboo sharks (C. plagiosum), or facilitate flexibility, in the generalist jack of all trades capture leopard sharks (T. semifasciata; Lowry and Motta, 2008).

6. BIOMECHANICS OF FILTER FEEDING In filter-feeding elasmobranchs, the expansive phase is the predominant phase in feeding. The bolus of water containing prey may be ingested using ram or suction mechanisms. Ram filter feeding typically involves continuous

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swimming for an extended period of time, during which water flows into the large open mouth and out through the elongated gill slits as in the basking shark, C. maximus (Sanderson and Wassersug, 1993). Another type of ram filter feeding presumably occurs in the megamouth shark (M. pelagios). This species has short gill slits and finely ridged elastic skin on the lateral and ventral sides of its head, which are likely to expand as they are forcibly filled with water (as the mouth opens to engulf a bolus of water, as seen in rorqual whales; Nakaya et al., 2008). Suction filter feeding (as used by the whale shark R. typus; see Sanderson and Wassersug, 1993) is grossly similar to the suction mechanism described above, where a bolus of water is rapidly engulfed. The biomechanical mechanisms of particle retention and transport appear to be positively affected by the flow-speed or foraging speed of the shark, which in turn influences the speed of water flow over the filtering apparatus (Paig-Tran et al., 2011). The permeability of the filtering apparatus is also important; however, while increases in permeability negatively influence the efficiency of the filtering apparatus, they do not markedly affect the efficiency of the movement of food particles toward and into the esophagus. Thus, the basking shark is likely the only elasmobranch species to employ dead-end sieving. It has a filtering apparatus that projects well into the buccal cavity, perpendicular to the direction of flow, and it likely must generate an internal flow to clear the apparatus periodically (Paig-Tran et al., 2011; see also Fig. 4.5). Some mobulid rays rely on a sticky surface to trap and ingest planktonic particles (Paig-Tran and Summers, 2014); but this is not universal among mobulids or other filter feeding elasmobranchs. The remaining species likely use some form of cross-flow filtration, in which shear stresses across the surface of the gill arches cause food particles to be laterally transported toward the esophagus (Motta et al., 2010; Paig-Tran et al., 2013), with or without tangential shearing to generate cyclonic flow (Peterson et al., 2014).

7. BIOMECHANICS OF UPPER JAW PROTRUSION The mechanism for protracting the upper jaw away from the cranium varies among elasmobranch taxa, with four mechanisms having been described to date. These mechanisms function to rapidly close predator-prey distance, close the jaws faster than one jaw moving alone, gouge pieces from large prey, and grasp with more precision. Those species with greater jaw protraction have longer ligamentous connections between the cranium and upper jaw or lack the ligaments completely (Wilga et al., 2001; Wilga,

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2002, 2005). Evolutionary changes in the mechanism for upper jaw protrusion involved several anatomical modifications that may be accompanied by alteration in muscle activation patterns (Wilga et al., 2001). The basal condition is an undivided preorbitalis muscle (PO) that is active in concert with its parent quadratomandibularis muscle during the compressive phase, as in squalean taxa (Wilga et al., 2001). Activation of the preorbitalis muscle pulls the jaws anteriorly, which in turn pushes the orbital process of the upper jaw into sliding ventrally along a vertical groove in the cranium; essentially pushing the upper jaw into protracting at the anterior end of the gape (Motta et al., 1997; Wilga and Motta, 1998a,b) (Fig. 4.7 Squalus). This precise mechanism for protracting the upper jaw toward the lower jaw enables effective cutting of prey between the upper and lower jaws (Moss, 1977; Wilga and Motta, 1998a). The most frequently encountered modification involved subdivision of the preorbitalis muscle in the carcharhiniform and lamniform sharks to form a dorsal and ventral subdivision (Wilga et al., 2001). Both of the new subdivisions still function concurrently with the quadratomandibularis in carcharhiniform species (Motta et al., 1997; Wilga and Motta, 2000; Gerry et al., 2008), and thus presumably in lamniform species as well (Figs 4.8 and 4.9). Increased muscle force, coupled with short orbital processes and the lack of a restrictive cranial groove, allows the upper jaw to move anteriorly as well as ventrally to enhance the ability to gouge pieces from overlarge prey (Moss, 1977; Motta et al., 1997; Wilga and Motta, 2000; Fig. 4.7, Negaprion). The preorbitalis muscle is further subdivided in the orectolobiform, heterodontiform, and batoid clades (Marion, 1905; Nobiling, 1977; Motta and Wilga, 1999). These preorbitalis subdivisions have origins that extend from the cranium and modified insertions onto the lower jaw, resulting in vertical trajectories that resemble that of the quadratomandibularis from which they arose (Edgeworth, 1935; Lightoller, 1939; Fig. 4.1). Activation of these vertical preorbitalis muscles still occurs simultaneously with the quadratomandibularis, but they now function to close the mouth by elevating the lower jaw. This adds considerably more muscle mass to generate higher bite forces for crushing hard prey (Wilga and Motta, 1998b; Motta et al., 2008). Structural modification of the levator palatoquadrati muscle is accompanied by an alteration in the motor pattern leading to a change in feeding kinematics in carcharhinid and sphyrnid sharks (Motta et al., 1997; Wilga and Motta, 2000; Wilga et al., 2001). The shifting of the levator palatoquadrati to a more anterior position on the cranium results in it assuming a more horizontal orientation (Compagno, 1988). The levator palatoquadrati muscle is now active during the compressive phase rather than the recovery phase and assumes a new function of protracting the upper jaw (Motta et al., 1997; Wilga and Motta, 2000; Wilga et al., 2001;

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Figs 4.8 and 4.9). As above, additional muscular support for protracting the upper jaw provides more force for gouging the upper jaw through prey. 8. ECOPHYSIOLOGICAL PATTERNS Elasmobranchs, like most fishes, are often described as being opportunistic foragers, implying that they will take advantage of whatever is around them. The tiger shark is renowned for having items such as car license plates and other, obviously, nonnutritive items in their stomachs. This does not mean, however, that all species are indiscriminate eating machines, as has often been portrayed in the popular literature. Many species, in fact, have diets that are quite specialized and consume a much narrower range of food items than what is available in the environment. Species may also be selective, meaning that they show a preference for certain food items, and consume those items more frequently than would be predicted based on availability. Dietary breadth is a reflection of factors both internal and external to the organism. The factors described above, including feeding morphology, behavior, and biomechanical constraints, are key factors that determine what ultimately contributes to elasmobranch diets (FerryGraham and Lauder, 2001; Wilga et al., 2007, 2012; Dolce and Wilga, 2013). Additional physiological parameters related to the locomotor, sensory, and digestive systems, also play a role in determining what the predator encounters and perceives as prey, what will attempt to ingest, and what can successfully consume. External factors, such as temperature, currents, and other physical parameters affect what is available in the environment. Ecological interactions within and among species can further restrict the resources available to the predator. Because they are all carnivorous, elasmobranchs tend to be at or near the top of most trophic schemes. They, like all top predators, tend to attain large body sizes, but relatively smaller population sizes. Some of the more interesting examples of dietary specializations in sharks include those of cookie cutter sharks (Isistius brasiliensis), which cut small, cookie-sized holes in the sides of larger organisms such as whales and consume the plugs so removed. Even species like the white shark are relatively specialized, with large individuals foraging almost exclusively on marine mammals, using a suite of predatory behaviors uniquely suited to such prey – a technique of biting, retreating, and waiting for the prey item to succumb through exsanguination. For filter feeders such as the whale shark, zooplankton and small fish are the targeted prey as opposed to phytoplankton or other smaller, less energetically rewarding food items. Species may be highly selective in their adjustment of gross behaviors (i.e., foraging location,

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swimming speed), and fine behaviors (i.e., adjusting of sieve plates), to ensure that they are able to target energy rich zooplankton prey (Paig-Tran et al., 2011). Among elasmobranchs there are some examples of specialized tool use associated with prey capture. Tool use is considered to be highly behaviorally advanced in an evolutionarily sense. The use of the hammerlike head, or cephalofoil, by hammerheads (Sphyrnidae), to pin and restrain stingrays prior to ingestion arguably fits the definition of tool use (Brown, 2011). Although this is probably not the reason for the origin of the cephalofoil (the hammer has profound effects on sensory systems; Kajiura et al., 2005; Mara et al., 2015), its co-option for this use represents a level of sophistication typically attributed only to birds and mammals. Other uses of tools for prey capture include the electroshock of torpedo rays (Torpediniformes) for stunning prey and employment of the snout of the cownose ray (Rhinoptera bonasus) in digging up clams and other food items that are otherwise hidden from predators. Such “tool use” is likely widespread within elasmobranchs and tightly correlated with dietary specialization. Although chondrichthyan fishes lack the pharyngeal jaws of teleosts and the muscular tongue of tetrapods, they have evolved other mechanisms to process complex prey (Dean et al., 2005). As explained above, sharks have several different mechanisms for controlling upper jaw movements that are useful in gouging pieces from prey too large to fit into the mouth (i.e., white sharks on marine mammals; cookie cutter sharks on large fish or marine mammals), or cutting prey too long to be swallowed (i.e., spiny dogfish on herring and cods; Dean et al., 2005). In contrast, skates and rays have increased musculature controlling lower jaw motions, that coupled with an upper jaw free from the cranium, allows them to effectively separate the edible portions of prey from the inedible (skates on shrimp, rays on shellfish; Dean et al., 2005, 2007). The hyoid arch is a key component in generating the water flow that moves prey around within the mouth, which is decoupled from the branchial arches in rays for even more complex processing (Wilga and Sanford, 2008; Dean et al., 2007). Most of these ecophysiological and ecomorphological insights rely on advancing technology to provide us with access to the organisms at a level previously unheard of. Quantifying the complex feeding kinematics of a large, toothy predator is daunting enough. Following these organisms into their habitats, which can be as vast as the entire ocean, so that we can learn how these morphologies are deployed in a functional sense requires technological advances possible only in recent decades. Understanding where the organisms go, and what they do there, connects the morphology to the ecology, and allows us to understand the real consequences of evolutionary change.

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5 ELASMOBRANCH MUSCLE STRUCTURE AND MECHANICAL PROPERTIES SCOTT G. SEAMONE DOUGLAS A. SYME

1. Introduction 2. Fiber Types 2.1. Metabolic Profiles 2.2. Distribution and Contributions to Swimming 2.3. Ultrastructure 2.4. Innervation 2.5. Membrane Potential and Activation 3. Contractile Properties 3.1. Mechanics and Energetics of Contraction 3.2. Axial Variation 3.3. Thermal Sensitivity 3.4. Scaling 4. Summary 5. Future Directions

The skeletal muscles of elasmobranchs share most of the fundamental ultrastructural, physiological, and contractile properties with muscles in teleost fishes, but also appear to differ in a number of ways. There are relatively slow and highly oxidative red muscles, which tend to be superficial on the body and comprise a small proportion of the total muscle mass, and relatively fast white muscles located medially forming the bulk of the swimming musculature. Red muscles are used only during slow, cruise swimming, and fast muscles during burst movements, but unlike in telesosts there appears to be no mixing of recruitment of the two fiber types between these activities. Pink muscles, and perhaps other fiber types, are also commonly observed but are relatively sparse. A few shark species exhibit regional red muscle endothermy and associated internalization of the red muscle mass, a condition convergent with designs in tunas. In sharks studied to date, which are mostly large in size, there is no apparent axial variation in red muscle contractile physiology, which 189 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00005-5

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might be interpreted to mean that muscles along the body length perform a similar task during swimming, but much more information regarding muscle activation, muscle strain, and distribution patterns is needed to illuminate these observations. Muscles of relatively large sharks have very slow contraction kinetics, regardless of temperature, perhaps belying the slow movements of these animals, while muscles of smaller sharks are faster and tend to show more pronounced temperature sensitivity, particularly in endothermic animals. Many insights into the contractile physiology of skeletal muscle in general have been gained through the study of shark muscle, but otherwise we know very little about muscle and locomotor physiology across the diversity of sharks, skates, and rays.

1. INTRODUCTION As with their teleost relatives, there exists a tremendous diversity within the approximately 1000 species of elasmobranch fishes in body form, body size, locomotion, thermal biology, and environment. This includes skates, rays, and sharks, from Dwarf lantern to massive Whale sharks, benthic and pelagic species, ectothermic species and regionally endothermic lamniformes sharks, species that occupy polar through equatorial waters, marine and fresh-water species, and swimming behaviors that encompass lateral undulation, rajiform undulation, and mobuliform oscillation. Accompanying this diversity and in the face of near 400 million years of evolution independent from the teleosts, the elasmobranchs will surely provide great opportunity to learn about functional anatomy, locomotion, and the physiology of the muscles that power swimming. Yet our knowledge about elasmobranch muscle and how it is used in swimming, in the context of fishes overall, pales woefully, to the point the reader is cautioned that in this chapter most generalizations about elasmobranchs as a clade refer to studies based on a few species of sharks; we know even less about skates and rays. It is not that there is little left to learn, rather, the challenges of obtaining, housing, and working with elasmobranchs are not trivial, and the economic significance and convenience of working with teleosts, particularly the salmonids, sees them dominate the study of fish muscle. Fortunately, these circumstances have not tempered our enthusiasm for studying how the muscles of elasmobranchs are built and work, and the field remains a productive fascination for those who pursue it. Through this interest, a good deal of what we know about skeletal muscle

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in general, muscle in fishes, and fish locomotion and anatomy, stems from the study of elasmobranchs. For sharks, lateral undulations of the body serve as the primary form of locomotion, where contractions of myotomal skeletal muscles power waves of body bending that travel from anterior to posterior along the length of the body in a coordinated manner. The dorsoventrally flattened skates and rays have adopted very different locomotor strategies, where vertical oscillations or undulatory waves of the highly expanded pectoral fins power swimming and the tail appears reduced and incapable of contributing to significant propulsion in most species. The functional anatomy and physiology of the trunk musculature of sharks remains only sparsely described, and we know almost nothing about the pectoral fin muscles used by skates and rays, less still than in the relatively few species of teleosts that employ paired fin swimming. Yet, what we do know has been revealing. Shadwick and Goldbogen (2012) provide a comprehensive summary of functional muscle anatomy and contributions to swimming biomechanics in sharks, which we will mostly not touch upon here but rather focus on the physiology of the muscle itself. The reader is also directed to Chapter 6 of this current volume, by Lauder and Di Santo, for discussions of swimming biomechanics. Of some claim to fame, it was the elasmobranch torpedo ray, Torpedo sp., for which Lorenzini (1678) (referenced in Bone, 1966) first described the slow and fast skeletal muscle types in vertebrates, labeled red and white, respectively, based on their coloration and their anatomical separation. Then, about 300 years later, Bone (1966) used measures of muscle electromyographic activity during swimming in the lesser spotted dogfish (Scyliorhinus canicula) to demonstrate that these muscles appear to operate as independent motor systems: Red muscles power slow, sustained swimming and white muscles power burst and fast-start swimming. While Bone graciously acknowledges the 1962 PhD dissertation of Colin Pennycuick as perhaps the original factual demonstration that red fibers power slow swimming and white fast, it was again in dogfish sharks that Pennycuick made his discovery. These findings alone, though largely through serendipity in involving elasmobranch fish, but perhaps not entirely (see Section 2), stand as some of the most transformative advances in our understanding of locomotion, not just in fish but in all animals – two thumbs up for the study of elasmobranch muscle physiology. This chapter will summarize our relatively sparse, but disproportionately intriguing knowledge regarding elasmobranch muscle physiology, and will include how they are built, function, and respond to their environment.

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2. FIBER TYPES The different types of skeletal muscle fibers, their distribution, and contractile and metabolic characteristics are modestly well-described in elasmobranchs, and information from studies to date suggest they are quite similar, although not identical, to what is noted in teleosts. Readers are directed to the extensive review on fish fiber types by Sa¨nger and Stoiber (2001), and further description of their general patterns of distribution and function by Syme (2006) and references therein. Following, we will discuss observations specific to elasmobranchs. As in most teleosts, three different fiber types are commonly described in elasmobranchs, red fibers, pink fibers, and white fibers, with a thin layer of superficial tonic fibers observed in some species (Fig. 5.1 left panel) (Bone, 1966; Kryvi and Totland, 1977; Kryvi et al., 1981). The red, pink, and white fiber types would correlate, functionally, with slow, intermediate, and fast twitch fibers of other vertebrates. The superficial tonic fibers are relatively sparse in number (Bone, 1966; Kryvi and Totland, 1977; Kryvi et al., 1981). The relationship of the superficial tonic fibers to other vertebrate fiber types is not well understood. Additional fiber types can be defined based on staining for ATPase and oxidative or glycolytic enzyme activity (e.g., Bone and Chubb, 1978; Sa¨nger and Stoiber, 2001), but still exhibit the typical gradient of slow Regional endotherm

Ectotherm Superficial

Red

Pink

White

Lateral

Medial

White

White

Red

Red

Gut

Figure 5.1. Left panel: Location and relative size of the superficial, red, pink, and white muscle fibers on the body of a shark. Superficial fibers, if present, lie at the lateral surface just under the skin, while white fibers lie deep in a medial position. Right panel: Cross section showing fiber distribution within a typical ectothermic shark (left half), where red fibers are located peripheral to the white, just under the skin. Cross section of a shark that exhibits regional red muscle endothermy (right half), where red fibers are located more medial and away from the body surface. Note, superficial and pink fibers are omitted from this panel for clarity. Adapted from Bone (1966), with kind permission from Cambridge University Press (left panel).

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in superficial layers toward fast in the deep layers. It is unlikely that it is helpful to define many additional fiber types as being functionally unique, but rather that across the spectrum there exists operative diversity. 2.1. Metabolic Profiles Red fibers in elasmobranchs have a rich vascular supply, higher in the regionally endothermic shortfin mako (Isurus oxyrinchus) than in ectothermic species studied (Kryvi and Eide, 1977; Totland et al., 1981; Bernal et al., 2003a), a relatively high mitochondrial volume density (18–34% measured in several species of shark, including both ectothermic and regionally endothermic species) (Kryvi, 1977; Totland et al., 1981; Bone et al., 1986, 2003a), and relatively high levels of myoglobin, being higher than in most teleosts and 3- to 10-fold higher still in the endothermic lamnid sharks than in ectothermic species, with the lamnids rivaling the remarkable myoglobin levels noted in tunas (Kryvi et al., 1981; Bernal et al., 2003a). They have a relatively (compared with fast fibers) low calcium-activated myosin ATPase activity (Bone et al., 1986); high calcium ATPase sensitivity (Altringham and Johnston, 1982); small diameter (18–75 mm measured across several species of shark); many peripheral nuclei in some species (Kryvi, 1977; Kryvi and Totland, 1977; Bone et al., 1986) but not all (Bone, 1978); and contain high levels of fat and moderate amounts of glycogen (Bone, 1966; Kryvi, 1977; Bernal et al., 2003a). White fibers of elasmobranchs are less well studied. They make up the vast majority of the myotomal muscle mass; mostly all that is not red is white. White fibers have a large diameter (80–205 mm in S. canicula), nuclei are scattered through the cytoplasm, and they contain minimal fat and glycogen (Bone, 1966; Kryvi, 1977; Bone et al., 1986). They have a relatively high calcium-activated myosin ATPase activity and low calcium ATPase sensitivity (Altringham and Johnston, 1982), possess a poor vascular supply, although there is considerable variability across species (Totland et al., 1981), have relatively little myoglobin, even less than the white fibers of most teleosts, and from almost no to relatively few mitochondria (o1–5% volume density) (Bone, 1966; Bone et al., 1986; Kryvi, 1977; Kryvi and Eide, 1977; Kryvi and Totland, 1977; Kryvi et al., 1981; Totland et al., 1981). They are thus expected to fatigue very rapidly and recover very slowly, as they generally do in teleosts (Kryvi, 1977). However, while they are clearly not well designed for aerobic activity, nor do they appear to have a particularly high capacity for anaerobic metabolism. Curtin et al. (1997) demonstrated using both NMR and heat measurements from white muscle of S. canicula that only 1 min of activity reduced phosphocreatine levels to 50% of resting, but this required well

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over 60 min to recover, almost an order of magnitude longer than observed for muscle in several species of frogs, which are themselves considered relatively anaerobic and appear to use anaerobic metabolism to recover energy charge in muscles after exercise. Curtin et al. (1997) suggest this very slow recovery after exercise in shark white fibers reflects not only the very low mitochondrial content, but also an apparent complete reliance on this limited oxidative metabolism to resynthesize phosphocreatine. Perhaps related to the poor anaerobic capacity, white fibers of the blackmouth catshark (Galeus melastomus) and the velvet belly lanternshark (Etmopterus spinax) possess only one of the three isoenzymes of lactate dehydrogenase expressed in their red, intermediate, and white fibers, and this isoenzyme appears correlated with anaerobic (low oxidative capacity) muscle types in other animals (Totland et al., 1978). Pink fibers possess characteristics that tend to fall intermediate to red and white fibers, providing them with the alternative name of intermediate fibers (Sa¨nger and Stoiber, 2001). They have a moderate vascular supply, myoglobin content, and mitochondrial content (volume density of 3–15% measured in three species of shark) (Kryvi, 1977; Kryvi et al., 1981; Totland et al., 1981). They have a diameter intermediate to red and white fibers (75–135 mm in S. canicula), and often lie as a thin sheet between the red and white muscle layers (Bone, 1966; Kryvi, 1977). Pink fibers contain faint traces of glycogen and appear to contain no fat (Kryvi, 1977). The superficial tonic fibers lie in a thin layer that surrounds the red muscle and have been described in only two species, S. canicula and the related nursehound shark S. stellaris, where they comprise less than 0.6% of the myotomal cross-sectional area, but have not been observed in other shark genera including Galeus, Mustekus, Squalus, Prionance, and Cetorhinus (Bone, 1966; Bone et al., 1986). These fibers appear more closely associated with red than white fibers, and share the same innervation pattern and peripheral nuclei, but lack fat (Bone, 1966). They are about 80–90 mm in diameter with a mitochondria volume density of about 9.5% (Bone, 1966), which is more than white and similar to red in individuals of the same species. 2.2. Distribution and Contributions to Swimming The muscle fiber types in most fishes, including sharks (but perhaps not rays), are spatially separated such that there is very little if any intermingling of the different fiber types, with red muscles typically being located under the skin, pink fibers (if present) being just deep to the red, and white fibers lying deep (Fig. 5.1 left panel; reviewed in Sa¨nger and Stoiber, 2001). Of note, this separation of fiber types, spatially and perhaps also neurally and

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functionally, appears to be particularly distinct in most elasmobranchs, where there is not only a very clear demarcation between the muscle layers, but where studies of muscle and motorneuron activity during swimming suggest there is no overlap in recruitment of red versus white fibers during slow versus fast swimming, respectively; whereas there appears to be at least some mixing of recruitment while swimming in teleosts (Bone, 1966, 1978; Bone et al., 1978; Johnston, 1981; Mos et al., 1990). Glycogen levels in white fibers do not change during sustained locomotion, but drop during vigorous swimming, while in red fibers levels of glycogen decrease during sustained swimming yet remain constant during vigorous movements (Bone, 1966). While studies of muscle recruitment in swimming elasmobranchs that would support this functional separation are extremely limited, additional support is noted in the innervation patterns of red and white muscle in elasmobranchs (see Section 2.4), in the relatively extreme differences in myoglobin expression between red versus white fibers in elasmobranchs relative to teleosts (Kryvi et al., 1981), and in the almost complete lack of mitochondria noted in shark white fibers (Kryvi, 1977). The evolutionary basis of the emphasis on this separation of fiber recruitment in elasmobranchs is not understood. It may simply reflect a particular developmental pattern, or it may reflect a difference in ecophysiology. For example, Bone (1966) comments on the tendency for elasmobranchs to sustain swimming (powered by red fibers only) for long periods, including extensive migrations. He quotes an earlier observation in highlighting the incredible indefatigability of elasmobranch red muscle, wherein a grey nurse shark (Carcharias arenarius) swam for 6 years around an aquarium without interruption, equivalent to traveling 8 times around the world. However, sustained swimming and long migrations are likewise common in pelagic teleosts, and so the functional basis of the extreme separation of red and white muscle in at least some elasmobranchs remains uncertain. In contrast to the clear separation of red and white muscle reported in sharks, the red and white fibers of stingrays may not be so clearly separated (Hagiwara and Takahashi, 1967; Singer and Ballantyne, 1989). Skates and rays generally do not swim using lateral undulations of the axial skeleton, but rather by rajiform or mobuliform oscillations of the pectoral fins (Rosenberger, 2001). Whether there is a functional relationship between these modes of swimming and fiber types being mixed within the pectoral fin muscles, versus being separated in the axial muscles that power lateral undulations of the body of sharks, is unknown. Red fibers comprise a notably constant 2–2.6% of the total body mass in sharks studied to date, which is relatively small compared with other fish species, and this appears to be conserved across body size (although an exception is reported in a very large specimen of white shark, Carey et al.,

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1985), and conserved whether ectothermic or regionally endothermic species are examined (Carey et al., 1985; Bernal et al., 2003a). Shadwick and Goldbogen (2012) suggest the low red muscle content may reflect sharks being only slightly negatively buoyant and very streamlined, so the minimum speed required to maintain hydrodynamic equilibrium and hence the power required for swimming is relatively low. Likewise, Bone (1966) postulates that the relatively small proportion of red muscle in fish in general (and conversely the very large proportion of white muscle) may be attributed to the near neutral buoyancy of fishes, allowing them the luxury of using only a small amount of slow, energetically economical red fibers to power swimming most of their lives, but with little energetic penalty for also carrying a large mass of fast and powerful white muscles that are used only occasionally, but to a great effect when called upon. Despite a relatively constant amount of red muscle, the distribution of red muscle within the body varies markedly across species and appears related to the biomechanics of swimming (see also Chapter 6 in this volume by Lauder and Di Santo for further discussion, particularly the section dealing with kinetics and body mechanics). In most sharks, myotomal red muscle takes a subcutaneous position with white muscle deep to the red (Fig. 5.1 right panel), and red muscle becomes more abundant towards the posterior of the trunk (Bone, 1966; Kryvi, 1977; Kryvi and Eide, 1977; Bernal et al., 2003a). Sharks with this myotomal arrangement (superficial red) contain a musculotendinous system that is similar to most teleost fishes (Gemballa et al., 2006; Shadwick and Gemballa, 2006; Shadwick and Goldbogen, 2012), which links the muscle to adjacent skeletal and cutaneous elements that result in local body bending, and sharks with this anatomy appear to be ectothermic animals that swim with pronounced lateral undulations of the body (Bernal et al., 2003a). The other myotomal arrangement is found amongst the regionally endothermic lamnid sharks, including members of the family Lamnidae and the common thresher shark (Alopias vulpinus) of the family Alopiidae, where the red muscle has migrated to a medial and much more anterior position (Fig. 5.1 right panel) (Carey et al., 1985; Bernal et al., 2003a; Donley et al., 2004). In this position red muscle is thought to shorten and lengthen more independently of the surrounding skin and white muscle, and rather than causing local body bending it transfers work to the caudal fin via connective myocomata resulting in a stiffer mode of swimming (Bernal et al., 2003a; Donley et al., 2004; Gemballa et al., 2006; Shadwick and Gemballa, 2006; Shadwick and Goldbogen, 2012). Although the common thresher shark, which also possesses this particular anatomy, still swims with a higher degree of lateral undulation; this behavior is likely due to the red muscle extending into the caudal peduncle in this species (Bernal

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et al., 2003a, 2010; Syme and Shadwick, 2011). This medial and anterior location of red muscle that connects to the axial skeleton by a derived musculotendinous system (compared to other sharks) (Gemballa et al., 2006; Shadwick and Goldbogen, 2012), along with regional endothermy and patterns of increased capacity for oxygen delivery and oxidative metabolism, appears convergent with tunas (Bernal et al., 2003a). The functional role of pink fibers in elasmobranchs is uncertain, although we might anticipate it is similar to that proposed in teleosts, which is supplementing the red muscle at higher speeds of swimming (see reviews by Sa¨nger and Stoiber, 2001; and Syme, 2006 for discussions). Bone (1966) proposes that pink fibers, situated just deep to the red and adjacent to the white, appear closely associated with white fibers in histology, innervation, perhaps development, fat content (lack of), resting membrane potential, and presence of propagating action potentials. They appear wellsuited to contribute to faster swimming. In contrast, Totland et al. (1978) propose these intermediate fibers appear more similar to red than white based on lactate dehydrogenase (LDH) isoenzyme expression. The function of the superficial fibers remains unclear. Bone et al. (1986) have suggested they may play a postural role, rather than locomotion. S. canicula, which possess superficial fibers, are commonly observed in aquaria resting with their tails and heads raised off of the bottom, but lay limp on the bottom when anesthetized, while shark species that appear to lack tonic fibers are demersal or pelagic and thus may not need tonic, postural fibers. Bone (1966) saw fit to dismiss the superficial fibers as likely unimportant in swimming and thus from further discussion in that context; we agree that the superficial fibers do not appear well suited to contribute much power to swimming, and so will follow suit for the most part. However, subdermal pressure has been suggested to contribute to skin stiffness and energy transfer in swimming sharks and scombrids (Wainwright et al., 1978; Westneat and Wainwright, 2001), and these superficial fibers seem ideally situated to perhaps contribute to generating such pressures and influencing skin stiffness. Thus, we should not entirely rule out a role for the superficial fibers in swimming, although the apparent lack of such fibers in many sharks leaves questions about even this role. 2.3. Ultrastructure The limited information we have regarding ultrastructure of elasmobranch skeletal muscle comes from the study of a few species of sharks: E. spinax, G. melastomus, and S. canicula (Kryvi, 1977; Bone et al., 1986). In the sharks studied, contractile filaments comprise over 90% of the cell volume in white fibers and less than 60% in red fibers (Kryvi, 1977);

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Figure 5.2. Schematic reconstruction of the general structure of the sarcoplasmic reticulum and T-tubule system in skeletal muscle of sharks. Longitudinal section of three myofibrils (MF). The sarcoplasmic reticulum forms a fenestrated collar (SRFC) around the myofibrils in the H-zone region of the A-band, extends to the Z-line (Z) via tubules that then expand into terminal cisternae in the region of the I-band. The terminal cisternae come into close proximity with the cell membrane T-tubules (T), where either a terminal cisternae from only one sarcomere lies adjacent to the T-tubule forming a dyad (TC-d), or terminal cisternae from both sarcomeres that straddle the T-tubule form a triad (TC-t). Adapted from Kryvi (1977), with kind permission from Springer Science and Business Media.

however, this is almost certainly species specific and so these numbers should not be considered universal. The sarcomeric structure is typical of vertebrate skeletal muscle. Sarcomeres of red, intermediate, and white fibers show clear Z-lines, A- and I-bands, H-zone, and M-lines (Kryvi, 1977). Six thin filaments surround each thick filament in a hexagonal lattice, forming a 2:1 thin:thick filament ratio, with thick filaments also arranged in hexagonal patterns and connected to the Z-disc (Kryvi, 1977). Interestingly, in S. canicula, M-lines are absent in superficial fibers and the myofilaments are not as clearly aligned as in the sarcomeres of red and white fibers (Bone et al., 1986), an arrangement consistent with a tonic fiber type where the sarcomeric structure is less well-defined or absent. The volume density of the sarcoplasmic reticulum, a key structure regulating calcium storage, release, and uptake in skeletal muscle, is about double in white and intermediate fibers than in red (Kryvi, 1977; Bone et al., 1986), likely conferring more rapid rates of activation and inactivation in the former. Patterns of structure of the sarcoplasmic reticulum are also similar to those described for typical vertebrate skeletal muscle (Fig. 5.2). The

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Figure 5.3. Upper panel: Shark red muscle fibers, top fiber shown cut in cross section to illustrate the grooves or clefts in which synaptic terminals lie. Fibers are innervated by a pair of neurons, one entering from each end of the fiber. Synaptic terminals are distributed along the length of the fiber and contain round and tubular vesicles. Lower panel: Shark white muscle fibers are innervated via a cluster of synaptic terminals located focally at the fiber tips only. Each fiber is innervated by a pair of neurons that enter from the same end of the fiber, often with one fiber being larger in width than the other. Synaptic terminals contain large and small vesicles, perhaps suggesting different neurotransmitters. Based on data from Bone (1972).

sarcoplasmic reticulum forms a fenestrated collar that surrounds the H-zone region of the A-band and connects to terminal cisternae via irregular tubules in the I-band (Kryvi, 1977). The terminal cisternae form triads or dyads (frequently two dyads in Galeus) with the flattened transverse tubules of the cell membrane and are generally located at the edges of the Z-line or in the I-band offset from the Z-line (Kryvi, 1977). Unlike in teleosts, the interface between the transverse tubules and terminal cisternae is not always located at the Z-line, and there appear to be clefts in the terminal cisternae that are also present in Chimaera and Squalus (Kryvi, 1977), which led Kryvi to propose that the clefts may be a chondrichthyan phenotype. The clefts may enhance the area for sarcolemmal calcium release, but their function has not been explored as yet. 2.4. Innervation Patterns of muscle fiber innervation have been described in S. canicula (Bone, 1966, 1972; Bone et al., 1986). Red muscles are innervated by a distributed en grappe (grape-like) pattern of synaptic terminals (Fig. 5.3).

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The muscle fibers appear to receive synaptic input from two separate motor axons, where axons enter the myotome from the myosepta at both ends of the fibers, with multiple terminations from individual axons distributed along the length of the fiber resting in grooves or channels on the muscle fiber surface, and a single axon can innervate multiple muscle fibers, as is observed in teleost red fibers (Bone, 1966, 1972; Bone et al., 1986; reviewed by Altringham and Johnston, 1981). Variation in the structure of the subjunctional folds in the muscle fiber membrane below the nerve terminals has been noted (Bone, 1972), and two different vesicle profiles have been observed in the nerve terminals of red fibers, circular and tubular, both relatively small, ranging in diameter from 30 to 50 nm (Bone, 1972). The functional implications of these differences are unclear. It appears that superficial muscle fibers are innervated in a similar manner as the red fibers (Bone, 1966; Bone et al., 1986). White fibers are focally innervated at one end only by a basket-like collection of terminals that appear to grasp the end of the fiber (Fig. 5.3; Bone, 1966, 1972; Bone et al., 1986). As with red fibers, two axons appear to contribute to the neuromuscular junctions of a single muscle fiber. While nerve axons arise from the myosepta at both ends of the fiber bundles within a myotome, the axons that innervate any given fiber arise from the same end of the fiber, they are sometimes of unequal width, and there are relatively small and large vesicles within the terminals, perhaps suggestive of different neurotransmitters (Bone, 1972). This arrangement is similar to that observed in chondrosteans, dipnoans, and some primitive teleosts, but differs from that in white fibers of modern teleosts, which have terminals distributed along the length of the fibers similar to the pattern in red fibers and which may have implications for the ability of white fibers to contribute to slower swimming in many teleosts (reviewed in Altringham and Johnston, 1981). This basket-like formation is also found in pink fibers (Bone, 1966). However, Bone (1964) comments on a pattern of innervation noted in intermediate (pink?) fibers of the Torpedo ray that is seemingly unique from the patterns in both red and white fibers. These intermediate ray fibers are innervated by basket-like synaptic clusters near but not at their ends and appear somewhat intermediate between the pattern in red and white fibers. In some cases in white fibers, single nerve terminals lie in small depressions scattered along the end of the muscle fiber, or several nerve terminals lie close together in the same depression (Bone, 1972). For the latter, two types of nerve terminals are described, one containing vesicles similar to those in the single terminals noted above, and the second being a more diverse and much larger (80–100 nm in diameter) group of vesicles (Bone, 1972). The junctions with smaller vesicles appear cholinergic, but it is not confirmed that the larger junctions are also cholinergic (Bone, 1972).

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2.5. Membrane Potential and Activation Membrane electrical properties of muscle fibers have been measured in a few elasmobranch species. Resting membrane potential measured in pelvic fin muscles of mixed fiber type from three stingray species was from 70 to 75 mV (Hagiwara and Takahashi, 1967). In S. canicula white fibers, resting membrane potential and membrane resistance were 85 mV and 1588 Ocm2, respectively, while in red fibers they were 71 mV and 5410 Ocm2, respectively (Stanfield, 1972); Stanfield suggests some of the difference in resting membrane potential between red and white fibers may reflect the difficulty of electrode penetration into red fibers. White fibers of S. canicula (Stanfield, 1972) and mixed fibers of stingrays (Hagiwara and Takahashi, 1967) are much more permeable to chloride than to potassium at rest, showing much larger changes in resting potential in response to changes in extracellular chloride than to potassium concentration, although red fibers appear less permeable to chloride than do white fibers (Stanfield, 1972). Hagiwara and Takahashi (1967) thus conclude that resting membrane potential of elasmobranchs is determined largely by chloride concentration, as opposed to potassium as in teleost muscle. However, the Donnan equilibrium is a function of both conductance and concentration, so we might more safely conclude that changes in membrane potential are highly sensitive to chloride concentration, but membrane potential itself may still be heavily influenced by potassium distribution, as it appears to be in most vertebrate skeletal muscles. Regardless, this is an intriguing observation worthy of further investigation. Stanfield (1972) studied membrane potentials and the ionic basis of depolarization in muscle of S. canicula. Following exposure to a pulse of point depolarizing current, red fibers displayed a delayed increase in potassium conductance but only some showed substantial changes in sodium conductance, and none of the fibers studied generated action potentials. Conversely, white fibers showed an increase in sodium conductance followed by a delayed increase in potassium conductance and then inactivation of this current, and all generated action potentials, similar to what is observed in other vertebrate twitch muscle fibers. While no action potentials were elicited through point stimulation of red fibers, Stanfield (1972) proposes that red fibers may still be capable of firing action potentials via nervous activation across the en grappe synaptic field. Likewise, Bone (1966) did not find convincing evidence of action potentials in red fibers in swimming dogfish, although this is based on indirect evidence from extracellular EMG recordings. In contrast, Curtin and Woledge (1993b) and Lou et al. (2002) observed twitch contractions in response to single electrical shocks in all of the red fibers they studied from S. canicula, providing compelling evidence that

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red fibers in these sharks are twitch fibers and not tonic, as has also been noted in the red muscle of many teleosts (Syme, 2006). Of interest, during action potentials, membrane potential shows a significant overshoot in elasmobranch fibers, but not in teleosts (Hagiwara and Takahashi, 1967), suggesting differences in either ion concentrations or conductance changes between these clades. Action potentials in elasmobranch muscle can be induced by an increase in extracellular sodium ion concentration and are suppressed by tetrodotoxin (Hagiwara and Takahashi, 1967; Stanfield, 1972), indicating a similar mechanism of sodium excitability as observed in most teleost and vertebrate twitch fibers in general. Hagiwara and Takahashi (1967) propose that focal innervation only at the fiber ends in elasmobranch white muscle may be associated with the larger action potential, where a larger action potential would be more prone to propagate along the entire fiber and result in contraction of the entire fiber, a circumstance also observed in cyclostomes. White fibers in modern teleosts, in contrast, show local depolarization, but the distributed synaptic pattern results in contraction of the entire muscle without the need for propagating action potentials. In this sense, elasmobranchs may have a lesser degree of fine control over white muscle activation than do teleosts, where individual fibers are either fully on or off, which may in turn contribute to a design where the separation of the roles of red and white muscle to slow and fast swimming is more pronounced in elasmobranchs.

3. CONTRACTILE PROPERTIES 3.1. Mechanics and Energetics of Contraction Swimming requires power; swimming faster requires more power. The force and shortening exerted by myotomal muscle during contraction generates the power to undulate the body and/or fins that cause swimming. As is observed for skeletal muscle in other vertebrates, the slower, red fibers of sharks produce less force and have slower maximal rates of shortening than the faster white fibers, and so produce less power. Following are some examples. In muscle where the cell membrane is either removed or perforated using chemical detergents (i.e., “skinned”), which allows direct activation via extracellular calcium, red fibers of S. canicula produce about 80 kNm 2 of force, white fibers about 180 kNm 2, and superficial fibers about 50 kNm 2 (Bone et al., 1986; Altringham and Johnston, 1982). Isometric force produced by living (not skinned) fibers appears higher than for skinned. Living red fibers of the same species produce 140 kNm 2 (Lou et al., 2002); a lower value of 70 kNm 2 has also been reported (Curtin and

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Woledge, 1993b), but likely reflects the presence of damaged muscle within the preparation (Lou et al., 2002). Living white fibers produce 240–290 kNm 2 of force (Curtin and Woledge, 1988; Lou et al., 2002). These values of force are well within the ranges reported for skeletal muscle from other fishes (reviewed by Syme, 2006), although it would be comforting to have data from more than a single shark species to corroborate. The lower area-specific force of red muscle compared with white is attributed, although not entirely, to the lower myofibrillar volume in red fibers compared to white (Altringham and Johnston, 1982; Lou et al., 2002). Shark muscle, again like other vertebrate skeletal muscle, shows an inverse relationship between force production and speed of shortening. From this relationship we can determine the maximum speed at which the muscles can shorten as an index of inherent muscle speed, and also the power output of the muscle (the product of force and shortening velocity) as an informative measure of the ability of the muscle to contribute to locomotion. In S. canicula, the maximum velocity of shortening in white muscle is greater than for red by about two- to threefold (Altringham and Johnston, 1982; Bone et al., 1986; Curtin and Woledge, 1988; Lou et al., 2002), and maximum power of white muscle is greater than for red by fourto sixfold (Bone et al., 1986; Lou et al., 2002). Maximum power output, calculated from the force–velocity relationship of living red and white muscle of S. canicula, is about 28 Wkg 1 and 90–120 Wkg 1, respectively (Curtin and Woledge, 1988; Lou et al., 2002), and these values are at least double those reported using skinned muscle fibers of the same species (Bone et al., 1986). Maximal power measured during cyclic contractions from living muscle (i.e., the work-loop method, see Syme, 2006 for a review of the application of this method using fish muscle) is 47 Wkg 1 in white muscle of S. canicula (Curtin and Woledge, 1993a). Despite a number of studies using the work-loop method on shark red muscle, equivalent, mass-specific values of power are not available for red muscle due to the difficulty of accurately quantifying viable muscle mass in isolated bundles of red muscle. Again, the above results of power for shark muscle are not unlike those observed in other fishes in general, although there exists great variability in this regard. Of interest, the above referenced studies on shark muscle have provided some of the first evidence that living and skinned muscle fibers appear different in the forces that they produce, in power output, and the curvature of the force– velocity relationship; those authors provide some suggestions for the basis of the differences, but are beyond the scope of our discussion here. To produce force and power, chemical energy must be transduced into mechanical energy. The rate that energy is consumed by muscle, as well as the rate that mechanical work is done (i.e., power output), generally rises, peaks, and then falls with increased speed of muscle shortening, and this is

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also noted in shark muscle (Curtin and Woledge, 1991). These relationships suggest that there is an optimal swim speed for maximal power output, and perhaps also for energy use: Swimming faster or slower will reduce power available from muscle and energy used, which has implications for the economy of swimming. The energy used by muscle during a contraction can be partitioned into that used by the cross bridges to do work (i.e., to generate force and cause shortening), and that associated with accessory processes, including calcium homeostasis to regulate muscle activation and production of heat. Calcium homeostasis has been measured to constitute about 35% of the energy used by white muscles in S. canicula during isometric contractions, within the range (18–41%) reported for muscle from other vertebrates (Lou et al., 1997). Hence, a considerable amount of metabolic energy consumed by muscle is not realized as work output. This leads to the concept of muscle efficiency, a measure of the relative amount of energy that is used to produce useful work and power versus that which contributes to accessory processes or is lost as heat. Efficiency and the effects of power output and conditions of muscle activation on efficiency are of great importance to understanding how fish use muscles to swim. Much of the research in this field has been conducted using shark muscle, and the conclusions likely have broad application to muscles and movement in other animals as well. In these studies efficiency is measured as the ratio: (muscle work)/(heat + muscle work). The heat produced by muscle as it is activated and contracted is measured using a thermopile, a stack of exquisitely sensitive thermocouples placed against the muscle. During contractions of S. canicula white muscle, when the muscle is fully activated and shortened at a constant velocity, maximal efficiency is about 33% and remains relatively constant over a twofold range of shortening velocities (Curtin and Woledge, 1991). When shortening velocity is adjusted to maximize power output, average efficiency is slightly less, about 31%. However, when the muscles stretch and shorten and are activated in a cyclic fashion, as occurs during swimming, efficiency is even greater, maximally 41% in white muscle (Curtin and Woledge, 1993a) and 51% in red muscle (Curtin and Woledge, 1993b). There is thus merit to the argument that fish power sustained swimming with red muscle, and not white, as a mechanism to conserve energy. Of relevance to how muscles are used during locomotion, the frequency that muscle length must oscillate (analogous to the tailbeat frequency in a swimming fish) in order to maximize muscle power output is faster than the frequency that maximizes efficiency (Fig. 5.4; Curtin and Woledge, 1993a,b). This suggests a tradeoff between the conditions required to maximize muscle power versus efficiency, where higher speeds maximize power and lower speeds maximize efficiency, which would undoubtedly be of consequence to swimming fish and animal locomotion in general. However, this effect of

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Efficiency

Power Power Efficiency

Increasing cycle frequency

Increasing duration of activation

Figure 5.4. Relationships between (left) the cycle frequency of muscle lengthening/shortening (analogous to tailbeat frequency in a swimming fish) and (right) the duration that muscle is active during each cycle of contraction, and muscle efficiency and power output. Power is maximized at a higher cycle frequency than efficiency, but each remains near maximal when the other is maximized (left). Power is maximized at a higher stimulus duration than efficiency, and each is reduced substantially when the other is maximized. Based on measurements from red and white shark muscle in Curtin and Woledge (1993a,b, 1996).

cycle frequency on power and efficiency, at least over the range that they are each near maximal, is relatively small (Fig. 5.4). In white muscle, efficiency or power are within about 10% of being maximal when the other is maximized, in red muscle they are each within about 5% of maximal when the other is maximized, and efficiency is near maximal over a relatively broad range of cycling frequencies, particularly in white muscle (Curtin and Woledge, 1996). Thus, while a tradeoff exists, its impact may not be large. Like cycle frequency, the duration of muscle activation during each cycle of stretch/shortening also impacts power and efficiency, where longer periods of muscle activation are required to maximize power versus efficiency in S. canicula white muscle (Fig. 5.4; Curtin and Woledge, 1996). However, power and efficiency are maximized at notably different durations of muscle activation, such that maximizing one entails a significant tradeoff in the other (e.g., efficiency is reduced by about 33% below maximal at the point that power is maximized, and power is reduced by about 50% and sometimes more at the point that efficiency is maximal; Fig. 5.4). Lou et al. (1999) propose the reduced efficiency with longer durations of muscle activation is due to energy that is stored in internal elastic structures within the muscle being lost as heat during muscle relaxation, rather than contributing to muscle work as it can with shorter periods of activation. These findings, based on studies of elasmobranch muscle, again suggest fish must compromise between high power output (swim speed) and economical contractions (low cost of transport), and have carried considerable weight in our interpretation of how fast and slow muscles are used by animals to move.

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There are a handful of other studies using shark muscle to better understand and describe various aspects of contractile physiology of skeletal muscle in a broad context; we have not considered them here as their relationship to understanding elasmobranch muscle per se is less direct. We alert the reader that they exist. 3.2. Axial Variation Axial (head to tail) variation in muscle contractile physiology infers variation in muscle function along the length of the fish. Axial variation in speed of muscle contraction is commonly, although not universally, noted in teleosts (Altringham and Ellerby, 1999; Coughlin, 2002; Syme, 2006), where anterior red muscles tend to be faster than posterior muscles, perhaps to account for the reduced muscle strain near the head (Rome et al., 1993) or to enhance maneuverability (Syme et al., 2008). However, axial variation in contractile physiology of shark muscle appears notably absent, at least amongst the limited number of species studied to date, and this lack of variation appears to extend across both ecothermic and regionally endothermic species. There are no, or only minor, axial differences reported in measures of twitch kinetics; muscle work and power; and the activation conditions that maximize work in sharks (Bernal et al., 2005; Donley et al., 2007, 2012). The lack of axial variation in muscle contractile physiology, and in the specific patterns of the timing of muscle activation observed in swimming sharks (Donley and Shadwick, 2003; Donley et al., 2005) suggests a lack of axial variation in muscle function (i.e., the muscles along the length of the body are doing the same thing). This could be due to a relatively limited repertoire of swimming behaviors in sharks compared with teleosts (Donley et al., 2007), or perhaps to there being a greater emphasis placed on a single function of axial red muscle in sharks (e.g., power production) that would not necessitate axial variation in contractile physiology (Donley et al., 2012). The lack of axial variability in shark muscle may simply be a synapomorphy with no or as yet not understood functional basis (Donley et al., 2012). Perhaps it is due to a lessened functional significance of axial variation in muscle speed in larger fishes; all of the sharks investigated to date are considerably larger than the teleost species studied (Donley et al., 2012), and so the lack of axial variation in sharks may simply be an artifact of not having studied enough smaller species. It would be surprising that there is in fact no axial variation in muscle function in sharks, making this a fruitful area for further study. There are reports of axial variation in measures of muscle strain during swimming in some sharks, strain being the relative amount of stretch and shortening that the muscles experience as the body bends during swimming,

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where more anterior muscles generally experience smaller strain than posterior muscles (Donley and Shadwick, 2003). These patterns are noted specifically in sharks with superficial red muscle, where muscle strain is proportional to the extent of body bending and to the distance from the red muscle to the spine. Hence, the axial variation in muscle strain in these fish is largely a result of increased amplitude of body bending toward the tail versus the head. In sharks that exhibit regional red muscle endothermy, however, red muscle is located closer to the spine and red muscle shortening is uncoupled from local body bending (Bernal et al., 2001; Shadwick and Goldbogen, 2012; Donley et al., 2012). Given this uncoupling, we would not expect a direct relationship between the amplitude of body bending and red muscle strain, and in the lamind sharks there is little body bending except at the tail itself. In support of this expectation, in these fish there is either no evidence of axial variation in red muscle strain (Bernal et al., 2010, A. vulpinus), or variability in patterns ranging from no axial variation to increased strain toward the tail (Donley et al., 2005, I. oxyrinchus). These patterns, albeit based on measures from only a few shark species, appear to match patterns observed in teleost fish (Shadwick and Goldbogen, 2012), likely with the same functional basis and consequences.

3.3. Thermal Sensitivity Temperature has a large impact on the contractile physiology of fish muscle, notably in measures associated with rates, such as muscle power output and enzyme activity. Most sharks are ectothermic poikilotherms and so we expect the function of their muscles will be influenced heavily by the ambient water temperature. See Section 2 of Chapter 8, Vol 34A, by Bernal and Lowe for discussions of the extent of changes in muscle temperature in ectothermic poikilothermic sharks versus those that exhibit regional red muscle endothermy. However, peculiarly, much of what we know about the thermal biology of shark muscle comes from studies on the relatively few species of sharks specialized for regional red muscle endothermy, including the Lamnidae and one member of the Alopiidae family of sharks (Carey et al., 1985; Bernal et al., 2001; Bernal and Sepulveda, 2005). This bias stems from our curiosity about fish that are large and warm. Unfortunately, the bias introduces the complication that most of our knowledge is based on relatively homeothermic muscles, which form a small minority of elasmobranch muscle. It further introduces the complication that because endothermic fish tend to be very large, and because size also greatly impacts measures associated with muscle speed (see Section 3.4), it becomes very difficult to separate inferences about the effects of temperature from those of

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animal size. We must be mindful of this when making comparisons and drawing conclusions. As with teleosts (Syme, 2006), twitch kinetics of shark muscle become slower with decreasing temperature (Bernal et al., 2005; Donley et al., 2007, 2012). The Q10, the relative change in rate for a 101C increase in temperature, for various measures of twitch duration in sharks appears to range widely, from about 2 to 5, across white and red muscles, small to large species, and ectothermic and regionally endothermic muscle (Bernal et al., 2005; Donley et al., 2007, 2012). Yet patterns are seen, particularly when comparisons are made between small and large specimens, between red and white muscle within species, or comparing regionally endothermic versus ectothermic species of similar size. For example, maximal power output of red muscle from the ectothermic leopard shark (Triakis semifasciata) has a Q10 of about 0.8 (is slightly lower at 251C than at 151C) , while power of red muscle from a regionally endothermic lamind shark, the shortfin mako I. oxyrinchus, of similar size has a Q10 of about 3 over the same temperature range (Donley et al., 2007). Similarly, endothermic red muscle of the lamnid salmon shark, Lamna ditropis, is much more temperature sensitive than its ectothermic white muscle, with a Q10 for power of about 6 versus 2.5, respectively, to the extent that red muscle could likely not power swimming in these fish if allowed to cool only a few degrees (Bernal et al., 2005). However, while power of red muscle in endothermic thresher sharks A. vulpinus also appears to have a relatively high temperature sensitivity (Q10=6), similar to that in salmon sharks, it does not appear much different than in the white muscle (Q10=5) (Donley et al., 2012). Thus, regionally endothermic red muscles may seem to have a higher temperature sensitivity than ectothermic muscles (red or white), yet only one species of ectothermic shark has been studied in this context, and comparisons of red to white muscle are problematic in interpretation; therefore, we need more information. If assessing the effects of temperature on muscle by using the tailbeat frequency at which muscle power is maximized, red muscle from small specimens of endothermic I. oxyrinchus is also much more temperature sensitive than red muscle from similarly sized, ectothermic T. semifasciata (Donley et al., 2007) (Fig. 5.5). These observations support the notion the endothermic muscles are more temperature sensitive than ectothermic. However, it appears that thermal sensitivity of the tailbeat frequency for maximal power is considerably less in large sharks, regardless of regional endothermy. In large salmon and common threshers shark specimens (both exhibiting regional red muscle endothermy), there is little impact of temperature on the frequency at which power is maximized in both white and red muscle (Bernal et al., 2005; Donley et al., 2012). It has been suggested that the relatively slow red muscle phenotype observed in large

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Figure 5.5. Relationship between temperature and the cycle frequency at which muscle power is maximized in red muscle from the ectothermic leopard shark (Triakis semifasciata) and the endothermic shortfin mako shark (Isurus oxyrinchus). Note the increased thermal sensitivity of muscle from the mako shark. From Donley et al. (2007), with kind permission from the Company of Biologists.

sharks, and perhaps the hydrodynamics of swimming in large fish, result in a slow tailbeat regardless of temperature; big individuals simply beat their tails relatively slowly whether warm or cold (Donley et al., 2012). Thus, we might conclude that endothermic red muscles exhibit a relatively high thermal sensitivity, doing very well when warm but producing substantially less power and at slower tailbeat frequencies when cool, while ectothermic muscles perform similarly well across a spectrum of temperatures, appearing relatively insensitive to the effects of temperature. These relationships may confer ectothermic species with adequate swimming abilities across a wide range of water (and muscle) temperatures, as they might experience in their environments, while the red muscles of regionally endothermic species work very well at the relatively warm and stable conditions within the fish, but poorly if allowed to cool. However, in larger fish the red muscles tend to be slow at all temperatures (although this has only been studied in endothermic species) and thus the effect of temperature on tailbeat frequency appears less. The relatively high thermal sensitivity of regionally endothermic red muscle may at first appear to perhaps both limit (when cold) and enhance (when warm) the performance of the muscle and thus swimming abilities in fish that possess it. However, the physiological relevance of thermal sensitivity in a regionally endothermic muscle may be mute if these muscles remain warm regardless of water temperature. We need more information about muscle temperature in swimming sharks, particularly its stability over time and environmental

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temperature, to pursue these hypotheses further. There is some recent progress in this regard (see Chapter 8, Vol 34A, Bernal and Lowe). Relatively little is known about how temperature may impact metabolism of elasmobranch muscle, although we might safely assume it would be similar to that described for other poikilothermic species, in general. There do not appear to be notable differences in levels of key oxidative and anaerobic enzymes in red and white muscles between ectothermic (relatively cool) and regionally endothermic (relatively warm) species, nor between elasmobranchs and teleosts in general (Dickson et al., 1993), suggesting there aren’t large differences between clades or compensation for differences in muscle temperature. However, the warmer temperatures at which red muscles operate in the endothermic lamnid and alopiid sharks would elevate the activity of these enzymes by 50–100% above what would occur at ambient water temperatures, perhaps conveying a metabolic and performance advantage (Bernal et al., 2003b). 3.4. Scaling There are few studies on elasmobranchs that note the effect of fish size on muscle anatomy or physiology, whether across or within species, although there is some information. Bernal et al. (2003a) report a scaling coefficient of one (i.e., isometric) for red muscle mass versus body size in Prionace glauca (blue shark), T. semifasciata, A. vulpinus, L. ditropis, and I. oxyrinchus, whether analyzed within or across species, suggesting the relative mass of red muscle is independent of fish size in sharks in general. Although Carey et al. (1985) noted that a very large white shark (Carcharodon carcharias) specimen had proportionally more red muscle than smaller conspecifics. The scaling coefficient for the concentration of myoglobin per gram of red muscle for both I. oxyrinchus and A. vulpinus is zero (Bernal et al., 2003a), again indicating no scaling with body size. Larger animals tend to have slower muscles, and fishes (Syme, 2006), including sharks, appear to be no exception. In the relatively large shark specimens, A. vulpinus and L. ditropis (155 190 and 216 222 cm, respectively) (Bernal et al., 2005; Donley et al., 2012), the twitch durations are longer than in smaller shark specimens, I. oxyrinchus and T. semifasciata (75 120 and 70 115 cm, respectively) (Donley et al., 2007) (Fig. 5.6), as would be anticipated. Unfortunately, measures of twitch speeds from living muscle of other animals of similarly large size are not available for comparison. Yet, the twitches in red muscle of these large sharks do seem noteworthy in being so slow. Isometric twitches in the red muscle of A. vulpinus are about fivefold slower than in white muscle, with individual red muscle twitches lasting about 4 s at 161C (Donley et al., 2012), and

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Figure 5.6. Isometric twitches of red muscle at 15 161C from four shark species, including relatively small specimens of leopard and shortfin mako sharks (about 1 m length), and relatively large specimens of common thresher and salmon sharks (about 2 m length). Solid lines are anterior red muscle, broken lines are posterior red muscle. Vertical bar indicates the onset of stimulation, and arrows indicate the point at which force has fallen to approximately 50% of maximal as a measure of twitch duration. Data from Donley et al. (2007), with kind permission from the Company of Biologists; Donley et al. (2012), with kind permission from Springer Science and Business Media; and Bernal et al. (2005), with kind permission from AAAS.

about 30-fold slower than those of white muscle in L. ditropis, lasting about 4.5 s at 151C (Bernal et al., 2005). In contrast, the twitch duration of red muscle in the smaller T. semifasciata is much briefer, about 2 s at 151C, and in relatively small specimens of I. oxyrinchus about 2.5 s at 151C (Donley et al., 2007). While the slower twitch durations in the larger specimens is likely a size effect, and not species, we do not have information from within a single shark species about the effects of size on twitch speed to confirm this. For example, relatively fast twitches were measured from relatively small specimens of I. oxyrinchus, but these sharks can grow to lengths that far surpass those of the larger specimens of A. vulpinus and L. ditropis studied. Some sharks, with their incredible range of size across the lifespan, would make an excellent model organism in which to address hypotheses about size versus speed relations in muscle. With a tailbeat frequency that is limited, in part, by the rate that muscle can turn on and off (i.e., slow twitch speed), and likely by the hydrodynamics of swimming and the mass of red muscle available to power oscillations of the tail, large sharks appear to have no choice but to swim with very slow tailbeat frequencies, particularly when their red muscle is cool. The tendency for contraction kinetics to slow with increased animal

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size in all animals suggests sharks are not unusual in this regard, although hydrodynamics of swimming in large fish likely plays a major role in dictating tailbeat frequency as well. Perhaps surprisingly, the maximum velocity of muscle shortening (Vmax) and maximal power output of shark muscle, two other measures of inherent muscle speed, do not appear to scale with size; power and Vmax in white muscles from S. canicula are independent of fish length across the full range of sizes the species attains (Curtin and Woledge, 1988). This is consistent with observations in teleosts as well, where rates of muscle shortening and power output appear relatively independent of body size, but is completely at odds with observations in terrestrial and flying vertebrates where they scale inversely with body mass (reviewed in Syme, 2006). Perhaps this belies developmental differences across fishes, or fundamental differences in locomotor demands of swimming animals.

4. SUMMARY Sharks, like teleosts, appear to use primarily slow (red) and fast (white) muscle fibers to power slow and sustained versus fast and intermittent swimming, respectively. Pink fibers, observed in most species, likely make a minor contribution to swimming, perhaps supplementing the red and white, although this is not well understood, even in teleosts. Red fibers are relatively slow with low power output, and are highly oxidative, with some measures of oxidative capacity exceeding those in most teleosts, particularly in sharks exhibiting regional red muscle endothermy. Red fibers are innervated by more than one neuron, with multiple terminals distributed in an en grappe pattern over the fiber. This pattern may be associated with a tonic contractile response, although red fibers of at least some sharks are a twitch type and fire action potentials; there remains uncertainty regarding details about the electrophysiology of red muscle in elasmobranchs. Studies on S. canicula reveal that red fibers are more efficient at producing mechanical power than white fibers, which likely contributes to their role in prolonged swimming. White fibers are fast and, based on limited information, may also be largely oxidative but with extremely limited capacities in this regard. They also receive innervation from more than one axon, but are focally innervated with basket-like terminals along the end of the fiber only, a condition unlike that noted in modern teleost white fibers which show a distributed pattern of nerve terminals much like red fibers, and which is suggestive of a twitch fiber type in sharks that does not show graded contractions and thus may not be well-suited to contribute to slow speed

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and low power activities. There are at least two types of nerve terminals on white fibers; the pharmacology and functional basis of their differences are not well understood. White fibers fire action potentials via a voltage-gated sodium conductance, similar to that reported for other vertebrate twitch fibers. They produce high force and power and are used during burst and fast-start swimming for brief periods from which they recover very slowly. This dichotomy in anatomy and function between red and white muscle seems particularly distinct in sharks, where measures of muscle activity in swimming fish and patterns of innervation suggest there is little to no overlap in recruitment and contributions to each type of swimming. This requires further investigation to confirm and to understand the functional basis and implications. The pattern of red muscle distribution within the body of sharks appears to be indicative of whether the shark is ecto- versus endothermic, although we still know very little about such patterns in most sharks. In ectothermic sharks, red muscle is superficial, located just under the skin, and tends to be more abundant towards the posterior of the animal, although it extends most of the length of the body. In contrast, regionally endothermic sharks contain red muscle that is more medial and anterior, a condition convergent with the design in endothermic tunas, although red muscle extends the full length of the body and even into the caudal fin in endothermic A. vulpinus. Despite the ecto- or endothermic configurations, red muscles in sharks studied to date (which are very few) do not show any axial variation in contractile physiology or recruitment patterns; the functional implications of this are as yet unclear. Red and white muscles appear to intermingle in stingrays, have not been investigated in skates, and in general are very poorly described in these clades of elasmobranch species. Temperature has a notable impact on muscle contractile performance, with measures of muscle speed, power, and the tailbeat frequency at which power is maximized decreasing with decreased temperature. However, these relationships appear dependent on species size and red muscle endothermy (or not). Red muscle from sharks that exhibit regional red muscle endothermy tend to be relatively more sensitive to temperature than red muscle from sharks that are ectothermic. This may endow ectothermic species with the ability to sustain power and swimming across a broad range of environmental temperatures, and while it may suggest red muscles of endothermic species are not well suited to function in the cold, the high thermal sensitivity of endothermic red muscles may be physiologically inconsequential if these muscles remain warm always; further studies are needed in this regard. Red muscle from larger sharks tend to be slower than from smaller sharks, and impressively slower in very large sharks. Further, red muscles from large sharks have relatively slow contractile kinetics

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regardless of temperature or endo/ectothermy, where large sharks may beat their tails slowly, in part, as an inherent property of their slow muscles at all temperatures of the water or body.

5. FUTURE DIRECTIONS Where to go from here can be guided to a large extent by the reminder that most of the little that what we know about elasmobranch muscle, particularly in an ecophysiological context, comes from studies on a relatively few species of shark and is biased toward sharks that are relatively large and which possess warm red muscle. The preponderance of sharks are small and ectothermic, but only a few have been studied, and most of these have been described either primarily for comparison with larger species or as a means to advance our understanding of muscle itself rather than to understand the shark for their own sake. As such, the diversity of elasmobranch muscle, its ultrastructure, morphology, physiology and function during swimming, is particularly under explored. There thus remains great potential to learn about the structure and function of the muscles of more species of shark, and of any species of skate or ray. This could include further exploring the effects of fish size on muscle contractile physiology, which, based on current data, appears to have a very large impact on twitch speed but no impact on shortening velocity or power. The tremendous range in body size of sharks makes this a wonderful opportunity that is difficult to achieve in teleosts or mammals. Much of the groundwork has already been laid for the more challenging measures from large sharks, although the largest sharks studied thus far have been about 2 m in length (L. ditropis and A. vulpinus) while there are numerous shark species swimming the waters at double this length, and some that are over 12 m long. There is more to learn about ecto- versus endothermic red muscles, if they differ in efficiency given the notable oxidative capacity of endothermic red muscle in sharks, and the long standing question of their evolutionary origins and the functional advantages they might provide. We lack information about the temperature sensitivity of muscle from both small and large ectothermic sharks, and likewise from large teleosts in general, which would add considerably to our interpretation of the effects of temperature and body size on muscle function in sharks and other fishes. Some ectothermic sharks, such as large sleeper sharks (Family Somniosidae), reside in waters at temperatures colder than as yet studied in any shark muscle. Perhaps the association between large size and slow muscle contractions affords them the ability to survive in such cold environments.

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We know nothing about thermal adaptation or acclimation in shark muscle, and little about differences in design and function in species that are eury- or stenothermic. Red muscle distribution within the body, body shape, and the patterns of body bending during swimming all appear interrelated, and while we have made intriguing discoveries in understanding these designs in a few cases in sharks, there remains a wealth of diversity yet to be described and perhaps information to be applied. We know almost nothing about skates and rays in this regard, arguably some of the most unusual and maneuverable animals on earth. Even the ultrastructure, innervation, and electrophysiology of elasmobranch muscle are only scantily described. What we do know is that when we study elasmobranchs we tend to learn something new, interesting, and insightful, testament to the immense diversity of physical and physiological designs within the clade. The remarkable and enduring success of these fish in aquatic ecosystems, and our curiosity about animals that yet remain so poorly- and misunderstood, should compel us to learn more about how they are built and work, despite the challenges of doing so.

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Donley, J. M., Sepulveda, C. A., Aalbers, S. A., McGillivray, D. G., Syme, D. A. and Bernal, D. (2012). Effects of temperature on power output and contraction kinetics in the locomotor muscle of the regionally endothermic common thresher shark (Alopias vulpinus). Fish Physiol. Biochem. 38, 1507–1519. Gemballa, S., Konstantinidis, P., Donley, J. M., Sepulveda, C. and Shadwick, R. E. (2006). Evolution of high-performance swimming in sharks: transformations of the musculotendinous system from subcarangiform to thunniform swimmers. J. Morph. 267, 477–493. Hagiwara, S. and Takahashi, K. (1967). Resting and spike potentials of skeletal muscle fibres of salt-water elasmobranch and teleost fish. J. Physiol. 190, 499–518. Johnston, I. A. (1981). Structure and function of fish muscles. Symp. Zool. Soc. Lond. 48, 71–113. Kryvi, H. (1977). Ultrastructure of the different fibre types in axial muscles of the sharks Etmopterus spinax and Galeus melastomus. Cell Tiss. Res. 184, 287–300. Kryvi, H. and Eide, A. (1977). Morphometric and autoradiographic studies on the growth of red and white axial muscle fibres in the shark Etmopterus spinax. Anat. Embryol. 151, 17–28. Kryvi, H. and Totland, G. K. (1977). Histochemical studies with microphotometric determinations of the lateral muscles in the sharks Etmopterus spinax and Galeus melastomus. J. Mar. Biol. Ass. U.K 51, 261–271. Kryvi, H., Flatmark, T. and Totland, G. K. (1981). The myoglobin content in red, intermediate and white fibres of the swimming muscles in three species of shark – a comparative study using high-performance liquid chromatography. J. Fish Biol. 18 (3), 331–338. Lorenzini, S. (1678). Osservazioni Intorno Alle Torpedini. Firenze: Onofri. Lou, F., Curtin, N. A. and Woledge, R. C. (1997). The energetic cost of activation of white muscle fibres from the dogfish Scyliorhinus canicula. J. Exp. Biol. 200, 495–501. Lou, F., Curtin, N. A. and Woledge, R. C. (1999). Elastic energy storage and release in white muscle from dogfish Scyliorhinus canicula. J. Exp. Biol. 202, 135–142. Lou, F., Curtin, N. A. and Woledge, R. C. (2002). Isometric and isovelocity contractile performance of red musle fibres from the dogfish Scyliorhinus canicula. J. Exp. Biol. 205, 1585–1595. Mos, W., Roberts, B. L. and Williamson, R. (1990). Activity patterns of motoneurons in the spinal dogfish in relation to changing fictive locomotion. Phil. Trans. R. Soc. Lond. B 330, 329–339. Rome, L. C., Swank, D. and Corda, D. (1993). How fish power swimming. Science 261, 340–343. Rosenberger, L. J. (2001). Pectoral fin locomotion in batoid fishes: undulation versus oscillation. J. Exp. Biol. 204, 379–394. Sa¨nger, A. M. and Stoiber, W. (2001). Muscle fiber diversity and plasticity. In Fish Physiology: Muscle Development and Growth, vol. 18 (ed. I. A. Johnston), pp. 187–250. New York, London: Academic Press. Shadwick, R. E. and Goldbogen, J. A. (2012). Muscle function and swimming in sharks. J. Fish Biol. 80, 1904–1939. Shadwick, R. S. and Gemballa, S. (2006). Structure, kinematics, and muscle dynamics in undulatory swimming. In Fish Physiology: Fish Biomechanics, vol. 23 (eds. R. E. Shadwick and G. V. Lauder), pp. 241–280. San Diego, CA: Academic Press. Singer, T. D. and Ballantyne, J. S. (1989). Absence of extrahepatic lipid oxidation in a freshwater elasmobranch, the dwarf stingray Potamotrygon magdalenae: evidence from enzyme activities. J. Exp. Zool. 251, 355–360. Stanfield, P. R. (1972). Electrical properties of white and red muscle fibres of the elasmobranch fish Scyliorhinus canicula. J. Physiol. Lond. 222, 161–186.

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Syme, D. A. (2006). Functional properties of skeletal muscle. In Fish Physiology: Fish Biomechanics, vol. 23 (eds. R. E. Shadwick and G. V. Lauder), pp. 179–240. San Diego, CA: Academic Press. Syme, D. A. and Shadwick, R. E. (2011). Red muscle function in stiff-bodied swimmers: there and almost back again. Phil. Trans. Roy. Soc. B 366, 1507–1515. Syme, D. A., Gollock, M., Freeman, M. J. and Gamperl, A. K. (2008). Power isn’t everything: muscle function and energetic costs during steady swimming in Atlantic cod (Gadus morhua). Physiol. Biochem. Zool. 81 (3), 320–335. Totland, G. K., Kryvi, H. and Slinde, E. (1978). LDH isoenzyme pattern in the three fibre types in axial muscle of the sharks Galeus melastomus and Etmopterus spinax. J. Fish Biol. 12, 45–50. Totland, G. K., Kryvi, H., Bone, Q. and Flood, P. R. (1981). Vascularization of the lateral muscle of some elasmobranchiomorph fishes. J. Fish Biol. 18, 223–234. Wainwright, S. A., Vosburgh, F. and Hebrank, J. H. (1978). Shark skin: function in locomotion. Science 202, 747–749. Westneat, M. W. and Wainwright, S. A. (2001). Mechanical design of tunas: muscle, tendon, and bone. In Tuna: Physiology, Ecology and Evolution (eds. B. Block and D. Stevens), pp. 271–311. San Diego, CA: Academic Press.

6 SWIMMING MECHANICS AND ENERGETICS OF ELASMOBRANCH FISHES GEORGE V. LAUDER VALENTINA DI SANTO

1. 2. 3. 4. 5. 6. 7. 8.

Introduction Elasmobranch Locomotor Diversity Elasmobranch Kinematics and Body Mechanics Hydrodynamics of Elasmobranch Locomotion The Remarkable Skin of Elasmobranchs and Its Locomotor Function Energetics of Elasmobranch Locomotion Climate Change: Effects on Elasmobranch Locomotor Function Conclusions

The remarkable locomotor capabilities of elasmobranch fishes are evident in the long migrations undertaken by many species, in their maneuverability, and in specialized structures such as the skin and shape of the pectoral and caudal fins that confer unique locomotor abilities. Elasmobranch locomotor diversity ranges from species that are primarily benthic to fast open-ocean swimmers, and kinematics and hydrodynamics are equally diverse. Many elongate-bodied shark species exhibit classical undulatory patterns of deformation, while skates and rays use their expanded wing-like locomotor structures in oscillatory and undulatory modes. Experimental hydrodynamic analysis of pectoral and caudal fin function in leopard sharks shows that pectoral fins, when held in the typical cruising position, do not generate lift forces, but are active in generating torques during unsteady swimming. The heterocercal (asymmetrical) tail shape generates torques that would rotate the body around the center of mass except for counteracting torques generated by the ventral body surface and head. The skin of sharks, with its hard surface denticles embedded in a flexible skin, alters flow dynamics over the surface and recent experimental data suggest that shark skin both reduces drag and enhances thrust on oscillating propulsive surfaces such as the tail. Analyses of elasmobranch 219 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00006-7

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locomotor energetics are limited in comparison to data from teleost fishes, and data from batoids are particularly scarce. We present an overview of comparative data on elasmobranch energetics, with comparisons to selected teleost fishes: generally, teleost fishes exhibit low costs of transport compared to elasmobranchs. Many elasmobranch species are particularly susceptible to changing oceanic conditions in response to climate change as a result of benthic habitat, reproductive mode, or reproductive site fidelity. Experimental studies on skates demonstrate that even small changes in water temperature can negatively impact locomotor performance, and locally adapted populations can differ in how they respond to abiotic stressors.

1. INTRODUCTION Elasmobranch fishes exhibit remarkable locomotor diversity, sometimes forming large aggregations of individuals (Clark, 1963) for feeding and reproduction, exhibiting long distance oceanic migrations, and inhabiting ecological zones that vary from benthic to coral reefs to the open ocean. Associated with this behavioral and ecological diversity is an array of morphological and physiological adaptations that range from specialized skin structure, to the arrangement of muscle fibers in the segmental body musculature, to the structure and shape of the body wall and fins. Recent studies of elasmobranch locomotion have involved analysis of patterns of body and fin bending, how body muscles function to generate thrust, hydrodynamic effects of tail and fin movement, and analysis of the effects of the shark skin surface on swimming function. Furthermore, energetic analyses of elasmobranch swimming, while still few in number, are beginning to allow broader comparisons to teleost fishes for which a large database on the energetics of locomotion exists. Although the topic of elasmobranch locomotion has been addressed in a number of overviews recently (Lauder, 2006, 2015; Maia et al., 2012; Shadwick and Goldbogen, 2012; Shadwick and Lauder, 2006; Wilga and Lauder, 2004a) our goal in this chapter is to focus on selected recent results, place these new data in the context of previous work, and provide some original data on locomotor hydrodynamics and batoid energetics. We conclude with a discussion of the possible effects of climate change on ocean chemistry and how this will affect locomotor function and energetics in key elasmobranch species, an area of considerable topical importance but one that has not received much previous attention.

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2. ELASMOBRANCH LOCOMOTOR DIVERSITY Elasmobranchs display a remarkable diversity of locomotor designs and use a variety of anatomical systems to execute some amazing feats of movement. Chimeras use pectoral fin flapping motions in addition to undulatory body undulations in a manner very similar to pectoral fin swimming in teleost fishes (Daniel, 1988). Rays swim using complex motions of their pectoral fins, which can be undulated in a wave-like motion as in stingrays (Blevins and Lauder, 2012; Rosenberger and Westneat, 1999), oscillated primarily in the vertical plane as illustrated by swimming manta rays (Moored et al., 2011a,b), or a combination of both (Rosenberger, 2001). A series of recent papers has shown how some species of skates can use their modified pelvic fins as “limbs” to push against the substrate during benthic locomotion, a behavior termed “punting” (Koester and Spirito, 2003; Macesic and Kajiura, 2010; Macesic et al., 2013; Macesic and Summers, 2012). Most shark species possess an elongated body with one or more dorsal, pectoral, and anal fins that can be actively moved even as the body undergoes undulatory motion during swimming. The body shapes of sharks are themselves quite diverse and the classic paper by Thomson and Simanek (1977) provided the first general overview of the diversity of body shapes, and the Thomson–Simanck framework has been used by a number of subsequent authors (e.g., Shadwick and Goldbogen, 2012; Wilga and Lauder, 2004a). Dorsoventrally flattened angel sharks use expanded pectoral fins in addition to body undulation to power locomotion, while the diversity of shark body shapes includes species with classic heterocercal (asymmetrical) tail fins and fast pelagic swimmers such as lamnid sharks with a wing-like tail fin that is externally almost symmetrical in shape, with the upper and lower lobes of nearly equal area. Body shape is relevant to locomotion not only for discussions of streamlining and drag reduction in pelagic species, but also because sharks use their body and head shapes to generate lift and to regulate body torques as we discuss below. Parameters such as head shape (which can range from conical to flattened or blunt), and flattening of the ventral body surface to create lift when the body is inclined, are key to understanding the process of undulatory locomotion in sharks, which differs from that of the more completely studied teleost fishes due to differences in body density and tail shape (Maia et al., 2012). Morphological diversity in elasmobranch body and fin shapes is associated with a great diversity of ecological locomotor behaviors which include migration across vast oceanic distances as well as diel migrations probably associated with feeding (see Chapter 8) (Graham et al., 2012; Weng and Block, 2004; Weng et al., 2007). And yet the study of

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elasmobranch body form in relation to ecology and migratory patterns has just begun and is a rich area for future research (e.g., Irschick and Hammerschlag, 2014a,b). In addition, we wish to draw attention to the relative lack of information on the routine swimming speeds of elasmobranchs (see Chapter 8) (Lowe, 1996; Parsons and Carlson, 1998). There is a natural focus both in the literature and in the popular press on the high speeds and on the maximal swimming performance of fishes in general and sharks in particular. But the most ecologically relevant locomotor factor that may dictate locomotor efficiency during long migrations to reproductive sites, diel migrations, or the day-to-day search for food is the average, routine swimming speed that can be aerobically maintained at relatively low energetic cost. Such activity might take place at swimming speeds near the minimum cost of transport, but this has yet to be documented. Routine swimming speeds in many elasmobranch species are reported to be around 1 body length per second (e.g., Parsons, 1990; Parsons and Carlson, 1998), and routine slow swimming in Greenland sharks (Somniosus microcephalus) involves tail beat frequencies below 1 Hz (Shadwick, personal communication). This may be in part due to a scaling effect of the larger body size in most elasmobranchs compared to teleost fishes, where routine swimming speeds tend to be greater than a body length per second but absolute body lengths are smaller. There is a notable lack of data on routine swimming speeds in chimaeras, skates, rays, and indeed in most shark species also. Elasmobranch species can be challenging to study ecologically under field conditions, and are not amenable to direct visual tracking to obtain routine swimming speed estimates. Tagging studies with high temporal resolution capable of recording tail beat frequencies and water flow speed past the body probably represent the main means of obtaining this information, and we hope that future work will provide a much clearer picture of the frequency distribution of swimming speeds with high temporal fidelity in a variety of elasmobranch species.

3. ELASMOBRANCH KINEMATICS AND BODY MECHANICS The general descriptive terminology that is associated with elasmobranch locomotion mirrors that used to describe swimming in bony fishes (Maia et al., 2012; Shadwick, 2005). Most sharks swim using body undulations in a generally “anguilliform” or eel-like mode with waves of body bending passing down the body (Fig. 6.1), although measurement of specific parameters such as body wavelength and amplitude place many shark species in the “subcarangiform” classification with the body length containing less than a half wavelength

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Figure 6.1. Undulatory locomotion using waves of body bending in swimming sharks. (A and B) Bonnethead shark (Sphyrna tiburo) showing body conformation at two times when the tail is approximately 1801 out of phase during a single tail beat cycle. (C and D) Spiny dogfish shark (Squalus acanthias) at similar times in the tail beat cycle. Note the undulatory wave on the body and the change in shape of the heterocercal tail (yellow arrows) during swimming. From Lauder (2015).

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(Webb and Keyes, 1982). While this classificatory terminology dates back to the classic papers of Breder (1926) and Lindsey (1978) and has been expanded in recent years to differentiate between BCF (body and caudal fin) and MPF (median and paired fin) locomotion, we believe that much of the diversity of locomotor function in fishes is obscured by this descriptive terminology. Specifically, even during undulatory locomotion using waves of body bending, the median and paired fins of sharks play an important role in balancing pitch, roll, and yaw torques, and the dorsal fins in particular are also capable of generating thrust by accelerating water posteriorly (Maia and Wilga, 2013a,b; Wilga and Lauder, 2000). Median and paired fins in elasmobranchs are under active control by intrinsic musculature and their function during undulatory locomotion is integral to understanding how destabilizing forces are managed by swimming elasmobranchs. However, compared to the fins of teleost fishes, which possess highly flexible fin rays with a bilaminar structure that allows active bending (Lauder, 2006), elasmobranch fins with their rod-like fin rays appear to be less flexible and capable of lower curvatures and range of motion. An additional function of median fins during swimming in sharks is the interaction between flows generated by the dorsal fins and the caudal fin (Maia and Wilga, 2013a; Webb and Keyes, 1982), a phenomenon that has also been studied extensively in teleost fishes (Drucker and Lauder, 2001; Standen and Lauder, 2007). Depending on the relative timing of active dorsal and caudal fin movements, fluid vortices shed from the dorsal fins can interact with caudal fin flows to substantially alter free-stream fluid motion incident to the tail. The roles of fins can change considerably during unsteady locomotor movements compared to their function during steady swimming. Studies of the function of shark pectoral fins, for example, have shown that fin conformations maintained during steady horizontal swimming are adjusted during vertical maneuvering in order to generate torques that pitch the body up or down (Fish and Shannahan, 2000; Wilga and Lauder, 2000, 2001), which facilitates vertical movement in the water column. Control of pitching body motions may be especially important in elasmobranchs, which tend to be negatively buoyant and lack the gas-filled swimbladder common to most teleost fishes. Batoid fishes are known for their use of pectoral fins during locomotion (Blevins and Lauder, 2012; Fontanella et al., 2013; Klausewitz, 1964; Parson et al., 2011; Rosenberger, 2001), and skates and rays also show changes in fin and body position during transitions from steady horizontal swimming to vertical maneuvering. Study of locomotion in skates illustrates the changing role that fins can take when maneuvers are initiated and during vertical movement. In the little skate, Leucoraja erinacea, steady horizontal locomotion occurs via wave-like motions of the expanded pectoral fins (Fig. 6.2). Although pectoral fin motion is generally wave-like, the shape of the pectoral fin changes considerably between downstroke and upstroke

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Figure 6.2. Swimming kinematics in the little skate, Leucoraja erinacea. (A and B) Frames from high-speed video recordings of body and pectoral conformations during steady horizontal locomotion at a swimming speed of 1.2 BL/s. (C and D) Body and pectoral fin conformation at a time 0.24 s after the images shown in (A) and (B). Note the change in pectoral wave shape. (E and F) Body and pectoral conformation during vertical (ascending) locomotion (E), and during downward (ventral) descent (F). Ascending is active and often accompanied by high amplitude and rapid pectoral fin motions, while descending can be passive following body reorientation at a negative angle of attack to oncoming flow.

(compare Fig. 6.2, panels A and C). Lateral views show that during the downstroke, a relatively sharp transition point can occur in the middle of the fin margin as the wave is propagated posteriorly (Fig. 6.2A). During the upstroke, the fin margin takes on a more rounded shape (Fig. 6.2C); the effect of these downstroke–upstroke shape changes on patterns of fluid flow and force production are as yet unknown. Fin kinematics in the little skate show some interesting changes while executing vertical maneuvers. Ascending in the water column is actively powered by higher amplitude fin wave-like motions than those used during steady forward swimming (Fig. 6.2E). However, descending occurs by reorienting the body at a negative angle of attack and is largely passive with only low amplitude movements of the pectoral fins (Fig. 6.2F). Very few kinematic studies of locomotion in freely swimming skates or rays are available, so it is not currently possible to say how general these observations are. An additional noteworthy aspect of pectoral fin locomotion in batoids was described by Blevins and Lauder (2012) in their study of three-dimensional

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pectoral fin kinematics in the freshwater stingray Potamotrygon orbignyi. They observed that the outer margin of pectoral fin, during the downstroke, can be rather substantially cupped downward, and hence curved into the flow. If pectoral fin kinematics were dominated by the fluid loading occurring as the fin is moved down against the fluid, then the fin margin would be expected to be curved upward as is seen on the pectoral fin in the oscillatory motion of manta rays. But the opposite conformation often occurred in the freshwater stingray, and suggests that active control of the fin margin allows detailed shape changes during swimming, which perhaps function to control how water flows over the fin edge and to increase thrust by directing more water posteriorly. Batoids are also noted for benthic locomotion where fin movements occur near the substrate and are subject to “ground effect” hydrodynamic influences. Ground effects are well known for flying animals and man-made aircraft where both rigid and flapping wings alter flows near surfaces (see review in Rayner, 1991), but the dynamics of aquatic animals interacting with the substrate are very different given the flexible undulating propulsive modes observed in fishes. The ground effect has proven challenging to study in live elasmobranchs, but several recent papers have addressed some of the kinematic and hydrodynamic factors involved with rays swimming in ground effect using simple physical models. Studies using flexible membranes as models of ray wings, either with dual actuators driving a rubber membrane (Blevins and Lauder, 2013) or a single leading edge actuator controlling a flexible panel (Quinn et al., 2014a,b), have shown that swimming near the bottom can greatly alter flow patterns over the undulating membrane. Remarkably, even though kinematics of the membranes can remain relatively unchanged, substantial improvements in swimming efficiency can be achieved. In sharks the function of the asymmetrical (heterocercal) shape of the tail received renewed attention beginning with the paper by Thomson (1976) who first suggested that the asymmetrical shape acts to direct locomotor force through the center of body mass and thus avoids inducing rotational torques tending to pitch the head down. This contrasts with the classical view that the heterocercal tail generates lift forces (Affleck, 1950). The heterocercal tail moves in a complex manner (Fig. 6.1C and D: yellow arrows) and requires a full three-dimensional study to determine the orientation of different regions of the tail during swimming. Experimental analysis of three-dimensional motion of the heterocercal tail in leopard sharks (Ferry and Lauder, 1996) suggested that the classical model was correct, and that orientation of the tail surface during side-to-side movement indicates that lift forces are produced, which pitch the head ventrally around the center of mass (COM). However, confirmation of this suggestion based

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on kinematics required subsequent experimental studies of fluid flows generated by the tail and calculation of the direction of reaction forces on the body. We consider those results in the next section along with implications for body dynamics in swimming sharks. One aspect of elasmobranch locomotion that has received little attention is the analysis of unsteady locomotor behaviors such as accelerations and escape responses. Domenici et al. (2004) analyzed escape responses in spiny dogfish and Seamone et al. (2014) have recently used a predator model to induce escape responses in the same species. Spiny dogfish show generally similar c-start escape patterns to those of teleost fishes, although variability among responses is relatively high and the speed of the response was slower than values typical for teleost fishes. Escape and turning performance has been analyzed quantitatively in rays by Parson et al. (2011) and in sharks by Maia and Wilga (2013b), Porter et al. (2009, 2011), Shadwick and Goldbogen (2012), and Kajiura et al. (2003). Further analysis of unsteady swimming behaviors, which may in fact be among the most common locomotor events in the daily repertoire, is very much needed to round out the picture of elasmobranch swimming diversity. The study of elasmobranch body mechanics from the perspective of material design and function has progressed greatly in recent years. Elasmobranch skeletal mechanics in particular has received attention, and the functional design of the batoid wing (Dean et al., 2009; Dean and Summers, 2006) and shark vertebral elements (Porter and Long, 2010; Porter et al., 2006, 2007, 2014) have been used as inspiration for the design of vertebral columns that serve as models for flexible mechanical devices and for evolutionary analyses of alternative undulatory designs (Liu et al., 2010; Long et al., 2006, 2011). Understanding the mechanics of how undulatory body motions are achieved in elasmobranchs has come a long way since the classic paper by Bone (1966) used electromyography in dogfish, Scyliorhinus canicula, to show the division of labor between red and white myotomal fibers as swimming speed increases. His paper demonstrated convincingly that red, aerobic, muscle fibers were used for slow-speed swimming, while the larger glycogen-containing and deeper white fibers that make up the majority of myotomal volume were used for high-speed swimming and unsteady movements (also see subsequent papers that elaborate on this original result; Bone, 1978, 1988, 1999; Bone et al., 1978). Donley and Shadwick (2003) followed up the work of Bone with a comprehensive analysis of red muscle function that included measurement of fiber strain with sonomicrometry and quantification of body bending kinematics to show that the pattern of red muscle activation was consistent along the body for slow to moderate speed swimming and contributed to positive power along the

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length, unlike previous results obtained for many teleost fishes. Recent overviews of shark muscle function can be found in Shadwick and Gemballa (2006), Shadwick and Goldbogen (2012) and Syme (2006) (see also Chapter 5). Analysis of the mechanics of shark musculature changes considerably when fast-swimming pelagic species such as lamnid sharks are considered because the red muscle is internalized and located medially (Bernal et al., 2003a,b; Graham et al., 1994; Sepulveda et al., 2005), and these red fibers possess an elevated temperature with respect to ambient water (Bernal et al., 2005, 2009; see also Chapter 8). The remarkable evolutionary similarity between pelagic lamnid sharks and tuna (Bernal et al., 2001; Donley et al., 2004; Shadwick, 2005) in the location of the red musculature and in the attachment of body muscle fibers to collagenous myosepts is one of the most outstanding known examples of convergent biomechanical evolution.

4. HYDRODYNAMICS OF ELASMOBRANCH LOCOMOTION Experimental analyses of water flow over the bodies and fins of swimming elasmobranchs have enabled a number of hypotheses about body and fin function to be addressed. Quantitative flow visualization borrows approaches from engineering to visualize and analyze patterns of water movement over the surface and in the wake of the body and fins (Drucker and Lauder, 1999). In swimming leopard sharks, Wilga and Lauder (2002, 2004b) showed that the heterocercal tail generated a momentum jet that is directed posteriorly and ventrally, and thus produces a reaction force aimed above the center of mass (COM) (Fig. 6.3). This confirmed the canonical model of heterocercal tail function and indicates that the classic heterocercal tail shape generates lift forces and body torques. Flammang et al. (2011) applied a recently developed volumetric flow imaging approach to heterocercal tail function and showed a more complex vortex wake signature than previously suspected (Fig. 6.3D), while confirming earlier work on the direction of forces and the momentum jet produced by heterocercal tails (Fig. 6.3E). Borazjani and Daghooghi (2013) have shown an important additional feature of fish tails that applies to both heterocercal and homocercal tail hydrodynamics: the tail appears to generate an attached leading edge vortex that enhances thrust in a manner similar to proposed previously for insect and bird wings. The significance of differences in shape between the upper and lower lobes in the heterocercal tail for leading edge vortex structure is as yet unknown, but the computational fluid dynamic approach promises new insights into the function of elasmobranch caudal fins.

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Figure 6.3. Dynamics of locomotion in sharks studied with three-dimensional (3D) kinematics and particle image velocimetry. (A) 3D analysis of pectoral fin conformation in swimming leopard sharks (Triakis semifasciata, 21–26 cm total length) shows that the pectoral fins are held in a position that generates minimal vorticity during steady swimming. (B) Summary of forces acting on the body of a steadily swimming shark (see text for discussion). (C) Plot of the angle of the fluid dynamic jet formed by the tail vortex ring versus body angle. Jets are negative (below the horizontal) no matter what the body angle in leopard sharks, which indicates that the tail generates torques around the center of mass. These torques are counteracted by lift forces on the body. (D) Vortex ring conformation generated by one tail beat in a swimming spiny dogfish (Squalus acanthias). (E) Vertical slice through the vortex wake of a swimming leopard shark showing two centers of vorticity and the central fluid jet inclined below the horizontal. Modified from Flammang et al. (2011) and Wilga and Lauder (2000, 2002).

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Data on flow visualization over the body and pectoral fins (Wilga and Lauder, 2000) combined with analysis of flows generated by the tail provide an overall picture of the balance of forces on the body of freely swimming sharks (Fig. 6.3). During steady horizontal locomotion, pectoral fins are held in a conformation that results in near zero net lift forces (Fig. 6.3A). However, this changes dramatically during maneuvering when pectoral fins change their angle of attack to initiate pitch moments about the COM. During horizontal steady swimming, the body is inclined to the horizontal and generates lift forces and also counter-rotating torques around the COM (Fig. 6.3B). Both net lift and torques must balance and this is achieved dynamically during each tail beat as the head, body, and tail lift forces match gravitational forces, and oppositely-signed torques balance to prevent net rotation (Fig. 6.3B). In leopard sharks, the angle of the fluid dynamic tail jet is independent of the angle of the body during swimming, while in bamboo sharks, Chiloscyllium punctatum, Wilga and Lauder (2002) observed changes in jet angle, which became more horizontal as body angle increased during slow speed swimming. Sharks adjust their body angle as swimming speed changes, and during slow horizontal swimming at 0.5 L/s the body may be inclined at an angle of approximately 101 or more, while at a speed of 2.0 L/s the body is nearly horizontal. However, a cautionary note is in order here. Studies that generate accurate kinematic data on the body and fins of elasmobranchs necessarily involve using smaller animals that are suitable for laboratory flumes and camera arrangements, and it is still unclear if these conclusions apply to larger freely-swimming sharks in unrestricted open-ocean conditions. The heterocercal tail of sharks has also inspired the construction of simple physical models that have been used to understand some of the basic kinematic and hydrodynamic properties of propulsive surfaces with angled trailing edges as compared to homocercal (externally symmetrical) shapes (Lauder et al., 2011, 2012). Interestingly, analysis of the self-propelled speeds of simple flexible plastic panels with different trailing edge shapes showed that the heterocercal shape had increased swimming speeds (approximately 7% faster on average) compared to panels with the same area but a vertical trailing edge. However, this occurs with a slightly increased cost of transport (Lauder et al., 2011), and the vortex wake shed by the heterocercal panel differed in several ways from that of freely swimming leopard sharks. This difference could be due to obvious differences in structure between the simple plastic panel models and the tail of live sharks, and also to active stiffening via muscle fibers intrinsic to the tail and changes in stiffness through pressure changes in the tail as sharks swim (Flammang, 2010).

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Figure 6.4. Hydrodynamics of locomotion in the little skate, Leucoraja erinacea, swimming at 2.0 BL/s. This individual has a disk length of 8.5 cm. (A–C) Position of the body and pectoral fin in the laser light sheet with particles illuminating the flow to allow particle image velocimetry analyses (A), velocity vector field at this time with free-stream flow subtracted (B), and vorticity generated by pectoral fin motion (C). (D–F) Comparable images at a time 0.56 s later in time.

Experimental hydrodynamic data on batoid locomotion are not currently available for live animals swimming steadily, and most hydrodynamic data relevant to skate and ray swimming come from panel models or robotic systems (Moored et al., 2011a,b). Here we present experimental hydrodynamic measurements of flow around the body and in the wake of the little skate, L. erinacea, during steady locomotion at a moderate swimming speed of 2.0 L/s (Fig. 6.4). Particle image velocimetry of flows around the body and wake of the undulating pectoral fins shows clear momentum jets that alternate from posterodorsal to posteroventral (compare Fig. 6.4, panels B and E). These momentum jets are not symmetrical and jet velocities resulting from the upstroke appear to be of higher speed and carry greater momentum than downstroke flows. In addition to the associated vortex wake, flow slowed by interaction with the body and wing is evident as ribbon-like strips of vorticity over the upper

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Figure 6.5. Structure and function of the denticles (scales) on the skin of a bonnethead shark (Sphyrna tiburo) and manufactured biomimetic model shark skin. (A) Left panel, environmental scanning electron microscope image of skin denticles near the anal fin (green scale bar¼200 m) of a bonnethead shark (Sphyrna tiburo); right panel, scanning electronic microscope image of fabricated biomimetic synthetic shark skin used for hydrodynamic testing. Artificial shark skin is produced using additive manufacturing (3D printing); green scale bar¼1 mm. (B) Dynamic testing of the hydrodynamic function of shark skin denticles using pieces of shark skin that are

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body and lateral pectoral edge (Fig. 6.4C). These preliminary data suggest that further studies including a diversity of batoid species would be useful for understanding how different patterns of pectoral fin motion and body positions alter flows produced by the pectoral fins, and the relative balance of upstroke and downstroke momentum production.

5. THE REMARKABLE SKIN OF ELASMOBRANCHS AND ITS LOCOMOTOR FUNCTION As the fin and body surfaces of elasmobranchs undulate and are moved through the water, the skin encounters a time-dependent flow pattern. Friction between skin and the water is likely to be an important (although still of unknown magnitude) source of drag, and there is now a large literature on how the skin of elasmobranchs might have special dragreducing properties. Much of this literature is based on engineered models (Bechert et al., 1986; Bechert and Hage, 2007; Dean and Bhushan, 2010) and shows that surface texture, of an appropriate size and spacing, can result in drag reduction as fluid is moved steadily past a textured surface. Shark skin has inspired much of this research on the function of surface texture due to its remarkably complex structure (Kemp, 1999; Liem et al., 2001; Motta et al., 2012; Reif, 1982, 1985). Small (100 um to 1 mm) bony dermal denticles (Fig. 6.5A) cover the skin. Denticles are embedded into the dermis (Kemp, 1999; Motta, 1977) with a small expanded bases, and have stalk-like structures that extend through the skin to support ridged flanges exposed to water flow at the surface (Fig. 6.5A). Although studies of shark skin models under static conditions where the textured surface does not move have provided a solid baseline of data on attached to a flat support (shown on the left) which in turn is attached to a mechanical flapping foil device that allows controlled side-to-side and rotational motions of the shark skin membrane. Graph shows the self-propelled swimming speed of the shark skin membrane with intact denticles and after the denticles have been sanded off (to produce a relatively smooth surface) under three different motion programs. Note that in each case the swimming speed of the shark skin with denticles intact is significantly greater (*) than after the denticles have been removed by sanding. (C) Assembly of the tested flexible biomimetic shark skin foil (on left) and hydrodynamic analysis. A flat support attaches to the yellow area with holes on the left side of the foil, and this support is moved by a mechanical flapping device. Graph of the results from measuring the self-propelled swimming speed of the biomimetic shark skin foil (blue bars) compared to the smooth control (red bars) at different pitch angles. Heave motion was 71.5 cm at 1 Hz for all trials. At pitch angles of 51, 101, and 151 the biomimetic shark skin foils swim significantly faster (*) than the smooth controls. At the other four pitch angles, the swimming speeds are similar. Modified from Oeffner and Lauder (2012), Wen et al. (2014), and Lauder (2015).

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drag reduction, the lack of dynamic testing is of special concern. Shark skin, during free-swimming, is exposed to time-dependent flows with changing angles of attack and also flow separation over leading edges of the fins and tail, and also possibly along the body (Anderson et al., 2001). This suggests that dynamic testing is needed where skin and biomimetic versions of shark skin can be moved under a controlled motion program that mimics that of freely-swimming sharks, and forces, fluid flow patterns, and swimming performance measured. Wen et al. (2014) manufactured a biomimetic shark skin, and tested its function in comparison to a smooth control (Fig. 6.5A, right panel). Manufactured shark skin mimics have the advantage of allowing good experimental control, as smooth surfaces with the same mass as the artificial skin can also be studied and swimming performance compared. Oeffner and Lauder (2012) used pieces of real shark skin to make flexible membranes attached to a supporting rod (Fig. 6.5B). By attaching this rod to a computer controlled mechanical flapping apparatus (Lauder et al., 2007, 2011) that allows dynamic testing, they were able to move the pieces of shark skin in an undulatory motion program with realistic angles of attack and to achieve curvatures of the shark skin that match that of freelyswimming sharks. They found that the textured denticle surface increased swimming speed by an average of 12.3% compared to a smoothly sanded control in which the denticles have been removed, moving with the same motion program of heave and pitch (Fig. 6.5B). An additional key result was that the increased swimming speeds did not occur in shark skin membranes that were attached to rigid surfaces, indicating that flexibility and bending of the shark skin membrane is critical to the increased performance with the roughened denticle surface. Analysis of the flow field around swimming shark skin membranes and the sanded controls revealed a possible new role for the denticle-covered shark skin surface. Oeffner and Lauder (2012) found changes in the intensity and location of the leading edge vortex attached to the swimming shark skin membrane suggesting that the roughened surface might enhance thrust by promoting leading edge suction compared to a smooth control. They hypothesize that this effect may have been at least partially responsible for the observed increased swimming speeds, and may apply to regions of the shark body where flow separation occurs, such as the tail. One limitation of studying real shark skin is that it is difficult to modify the denticle pattern and make experimental alterations to determine which specific features of shark denticles most affect swimming mechanics. To address this issue, Wen et al. (2014) manufactured a biomimetic shark skin and smooth controls and compared their performance under dynamic swimming conditions. Fig. 6.5C shows how the self-propelled swimming

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speed of the biomimetic shark skin and smooth controls compares when moved at a constant heave of 71.5 cm at 1 Hz under a variety of different pitch angles. Manufactured shark skin swam significantly faster at pitch angles of 51, 101, and 151, but at the same speed as the smooth control at low (01) and high (20–301) pitch angles. The effect of the shark skin surface on locomotor performance thus depends critically on the motion program and how the surface interacts dynamically with oncoming flow as it moves through water. These results suggest that the function of the roughened denticle-covered skin of sharks is complex and motion-dependent, and it is clear that much more remains to be discovered about the diversity of denticle patterns over the body and among species, the effect of possible movement of individual denticles during swimming (Lang et al., 2008, 2014), and the functional significance of the ornamentation on the denticle surface. 6. ENERGETICS OF ELASMOBRANCH LOCOMOTION Studies that estimate the energetic costs incurred by elasmobranchs during swimming are scarce. In a few cases, costs of locomotion have been measured using a Brett-type swim tunnel (Brett, 1971), although recent technological advances have allowed researchers to approximate energetic costs in freeswimming sharks using speed and tail-beat sensors that have been calibrated to oxygen consumption rates (e.g., Graham et al., 1990; Scharold and Gruber, 1991; Sepulveda et al., 2004; Bernal et al., 2012; see also Chapter 8). Most studies on the metabolism of elasmobranchs have focused on a few benthic and inactive species, resting on the bottom of a respirometer (resting metabolic rate; Brett and Blackburn, 1978; Ferry-Graham and Gibb, 2001; Di Santo and Bennett, 2011b). However, some studies also measured resting metabolic rates of more active sharks, such as the mako shark, which exhibit oxygen consumption rates at rest similar to comparably sized yellowfin tuna Thunnus albacares (240 vs. 253 mg O2  kg 1 h 1, respectively; Graham et al., 1990; Dewar and Graham, 1994). A few other researchers have used swim tunnels to measure swimming metabolic rates in sharks. The metabolic rates of elasmobranchs during steady swimming have been reported for mako (Graham et al., 1990; Sepulveda et al., 2007), leopard (Scharold et al., 1988a), lemon (Scharold and Gruber, 1991), blacknose sharks (Carlson et al., 1999), and for one batoid, the little skate (Di Santo and Kenaley, in preparation), and these comparative data are summarized in Fig. 6.6 and Table 6.1. The little skate exhibits lower energetic costs during steady swimming when compared to more active ectothermic and lamnid sharks. Oxygen consumption decreases somewhat in the little skate as a function of

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Figure 6.6. Oxygen consumption rates (VO2 7 SE) of five species of elasmobranchs at different swimming speeds (in Body Lengths per second, BL/s): open triangle: Isurus oxyrinchus (Graham et al., 1990); closed triangle: Negaprion brevirostris (Scharold and Gruber, 1991); open circle: Triakis semifasciata (Scharold et al., 1988); closed circle: Carcharhinus acronotus (Carlson et al., 1999); closed square: Leucoraja erinacea (Di Santo and Kenaley, unpublished data).

speed within the range tested (0.75–1.25 BL/s). It is possible that the slightly higher metabolic rates of skates swimming at the lowest speed (Fig. 6.6) may be due to the fact that they were swimming below the velocity necessary to maintain hydrostatic equilibrium (Bernal et al., 2012), and thus incurred additional costs to maintain body stability. Even though there are only a few studies on elasmobranch energetics during activity, it is apparent that there is a positive association between fast-swimming fishes and swimming metabolic rates (Table 6.1). For instance, even after adjusting for temperature and body size, scalloped hammerhead sharks Sphyrna lewini consume nearly double the amount of oxygen that leopard sharks use when both are swimming about 1 body length per second (Scharold et al., 1988; Lowe, 1996, 2002). Basic measures of oxygen consumption such as the resting metabolic rate and active metabolic rate are useful for a gross determination of the costs of activity in a species. However, calculating the aerobic scope (i.e., the difference between the maximum and the resting metabolic rates) can be used to estimate the capacity for activity in fishes (Fry, 1947; Farrell et al., 2008, 2009; Roche et al., 2013). Not surprisingly, lamnid sharks exhibit high

Table 6.1 Summary of resting metabolic rates (RMRs), swimming or active metabolic rates (AMRs), and cost of transport (COT) for elasmobranchs and selected teleosts Species

Temperature (1C) Mass (kg)

RMR (mgO2  h

1

AMR  kg 1) (mgO2  h

1

COT  kg 1) (kJ  kg

Anguilla anguilla Oncorhynchus mykiss Negaprion brevirostris Triakis semifasciata Isurus oxyrinchus Squalus

19

0.155

42.21

62.71

0.62

19

0.161

–

130.4

2.73

25

1.39

152.6

240.2

3.84

–

–

105

229

–

16.5–19.5

4.4–9.5

344

541

3.79

10

2

32.4

88.4

–

Scyliorhinus stellaris Scarus schlegeli Rhinecanthus aculeatus Sphyrna lewini

17.8–19.3

2.5

92

162

–

26–27

0.243

127

–

2.39

26–27

0.106

74.7

–

1.74

22–28

5.90–12.21

–

273.9

1.45

Leucoraja erinacea

15

0.009

35.54

69.5

3.8

1

Behavior  km 1) and speed

Reference

van Ginneken et al. (2005) van Ginneken et al. (2005) Scharold and Gruber (1991) Scharold et al. (1988) Sepulveda et al. (2007) Brett and Blackburn (1978) Steady swimming Piiper et al. (1977) 0.27 BL/s Ucrit 2.3 BL/s Korsmeyer et al. (2002) Ucrit 1.5 BL/s Korsmeyer et al. (2002) Free-swimming Lowe (2002) 0.81 BL/s Steady swimming Di Santo and 1.25 BL/s Kenaley (in Preparation) Steady swimming 0.5 BL/s Steady swimming 0.7 BL/s Swimming 0.4 BL/s Swimming 0.84 BL/s Swimming 0.65 BL/s Swimming speed not controlled

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active metabolic rates (Fig. 6.6) which correlate with long-distance migrations and the ability to catch fast-moving prey (Bonfil et al., 2005; Sepulveda et al., 2007; Jorgensen et al., 2010). Lamnid sharks also exhibit relatively high resting metabolic rates to accommodate morphological and physiological adaptations for high swimming performance. In fact, it has been estimated that white sharks use about 46% of their total energy intake just to sustain basal metabolic demands (Ezcurra et al., 2012). The deployment of small activity loggers has enabled measurement of the costs of locomotion in free swimming fishes (Scharold et al., 1988; Scharold and Gruber, 1991; Farrell et al., 2008; Gleiss et al., 2010). Although precise speed sensors, accelerometers, and heart-rate monitors are now available and can be calibrated with standard swimming tests in the laboratory, there are many abiotic and biotic factors that can alter metabolic and heart rates in fishes beside swimming speed. It is unlikely that an elasmobranch would swim constantly at the same depth and in the same area, and it is therefore likely to encounter a variety of thermal environments, salinities, pH, and dissolved oxygen levels. All these abiotic factors are known to affect physiological processes in fishes (Fry, 1971; Carlson and Parsons, 2001; Meloni et al., 2002; Farrell et al., 2008; Di Santo and Bennett, 2011a; Di Santo, 2015). In addition, the presence or absence of predators, prey, and conspecifics can alter cost of activity (Wurtsbaugh and Li, 1985; Trudel et al., 2001; Allan et al., 2013; Binning et al., 2013). These factors make interpreting the data obtained from loggers challenging, but for pelagic elasmobranchs there is often little alternative. The energetics of steady free swimming in elasmobranchs can be quite difficult to measure, especially in benthic species that are ordinarily mostly sedentary, and an alternative measure of locomotor capacity can be obtained by measuring excess post-exhaustion oxygen consumption in fishes that have been manually chased (Cutts et al., 2002; Svendsen et al., 2011; Roche et al., 2013). In this protocol, researchers gently and repeatedly tap the fish thus eliciting “burst-and-glide” swimming until the fish is unresponsive to handling, that is, fatigue is achieved, and the fish is immediately transferred to a respirometer to measure the “oxygen debt” accumulated as a result of intense short exercise (Svendsen et al., 2011; Clark et al., 2013; Di Santo, in review). For many benthic species, this method represents, to date, the only effective way to measure maximum metabolic rates, and it also may result in higher oxygen consumption rates than those measured during swimming, allowing a better estimation of maximal aerobic capacity (Clark et al., 2013; Roche et al., 2013). In the section ‘Climate Change: Effects on Elasmobranch Locomotor Function’ we describe results from this method applied to the little skate in an effort to understand the effects of changing oceanic conditions on locomotor energetics.

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Finally, we emphasize that there is a near total lack of studies on the cost of locomotion in batoids, and the data shown in Fig. 6.6 for the little skate represent the only measurements that we are aware of. Without broader taxonomic representation of elasmobranch energetic data, we will not be able to make general conclusions as to energetic underpinnings associated with different modes of locomotion, and this is an especially fruitful area for future research.

7. CLIMATE CHANGE: EFFECTS ON ELASMOBRANCH LOCOMOTOR FUNCTION Since the industrial revolution, global atmospheric carbon dioxide (CO2) concentrations have increased from 280 to about 400 ppm (in 2015), thus reaching levels that have not been experienced in the past 65 million years (IPCC, 2013). The two major consequences of the accelerating increase in atmospheric CO2 concentration are a rise in ocean temperature and acidification (i.e., lower pH). Temperature alone is considered to be the “abiotic master factor” as it is known to affect nearly every metabolic process in fishes (Fry, 1971; Brett, 1971). In fact, fishes are known to select different temperatures in order to enhance physiological processes (Sims et al., 2006; Wallman and Bennett, 2006; Di Santo and Bennett, 2011a). As ocean temperature increases as a consequence of climate change, we might expect fish to adjust to the new thermal environment through physiological acclimatization (Somero, 2010; Donelson et al., 2012), adaptation (Angilletta et al., 2004; Baumann and Conover, 2011; Di Santo, 2015), or behavioral thermoregulation (Perry et al., 2005; Greenstein and Pandolfi, 2008). Similarly to other metabolic processes, swimming performance in fishes is known to be affected by abiotic climate-related factors such as temperature and pH (Chin and Kyne, 2007; Ishimatsu et al., 2008; Pang et al., 2011; Chen et al., 2011). Swimming performance increases with temperature up to a thermal optimum, beyond which performance declines rapidly. As organisms often live close to their thermal optimum, even a slight increase in ambient temperature may drastically reduce the energy available for highly demanding aerobic activities, such as locomotion (Rummer et al., 2014; Di Santo, in review; Brill and Lai, 2015). Locomotor efficiency is key to survival and reproduction in fishes, as swimming is used to migrate daily and seasonally to forage, spawn, and avoid predators. In addition, in light of environmental change, efficient locomotion may also ensure that elasmobranch fishes are able to find suitable refugia. Relocation to more favorable areas assumes that populations

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of elasmobranchs will be able to find and move to the new locations, and this assumption should be treated with caution (Chin and Kyne, 2007). The ability (or lack of thereof) to undertake large-scale migrations raises serious concerns especially for less mobile, or philopatric species that tend to remain close to their home areas. When comparing the costs of transport and metabolic rates of a range of elasmobranch and teleost fishes, it becomes apparent that metabolic rates per se are not a good indicator to predict the ability of a fish to migrate (Table 6.1). In fact, even though the European eel, Anguilla Anguilla, has comparable swimming metabolic rates to the little skate (62.7 vs. 69.5 mgO2  kg 1  h 1), it uses over five times less energy than the little skate to cover the same distance (Table 6.1). These results correspond to observations of activity of these two species in nature. The European eel has a very low cost of transport as a result of the combination of undulatory locomotor mode, a long body length and low oxygen consumption, and can therefore undertake a migration of 6000 km from Europe to the Sargasso Sea in 180 days (van Ginneken et al., 2005). In contrast, the little skate shows high site fidelity (philopatry) and short migratory distances (Di Santo, 2015), despite the fact that the lowest active metabolic rate measured in this species is comparable to that of the European eel. Even though, generally, teleosts seem to exhibit lower costs of transport when compared to elasmobranchs based on the available comparative data in Table 6.1, it seems that the small body size of the little skate may reduce efficiency of locomotion over long distances and increase overall energy expenditure. In fact, the little skate has some of the highest costs of transport within elasmobranch species tested to date, and it is only surpassed by more active and larger sharks, such as the mako (Table 6.1). In light of these data, it is important to consider cost of transport along with resting and active metabolic rates to improve predictions of whether or not fish species may be able to significantly shift their geographic range. Ocean warming is already affecting demography, geographic range, and predator timing of populations and species (Murawski, 1993; Walther et al., 2002; Perry et al., 2005; Parmesan, 2006; Dulvy et al., 2008; Chen et al., 2011). Demographic changes include shifts in recruitment, body size, and survival (Po¨rtner and Farrell, 2008; Genner et al., 2010; Gardner et al., 2011). Geographic shifts include those toward the poles (Walther et al., 2002; Perry et al., 2005; Beaugrand et al., 2008; Chen et al., 2011), and phenological changes include anticipating the timing of spawning and migrations (Farrell et al., 2008; Martins et al., 2011; Eliason et al., 2011), causing a mismatch between prey and predator timing (Raubenheimer et al., 2012). In particular, warming is thought to expand species ranges toward higher latitudes or deeper waters (Walther et al., 2002; Parmesan, 2006; Burrows et al., 2011). Perry et al. (2005) documented a shift in mean depth of the cuckoo ray, Leucoraja naevus, with

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species moving to deeper water as a response to warming, while Stebbing et al. (2002) showed a correlation between warming of the North Atlantic and migration of warmer water elasmobranch species, such as the sharpnose sevengill Heptranchias perlo and big-eye thresher Alopias superciliosus, to the Cornish coasts of Great Britain. Some species are highly migratory and may travel across oceans to exploit seasonal productivity events (see Camhi et al., 2008, for review). It is clear that, in order to undertake such large-scale migration toward suitable refugia, elasmobranch fishes should be able to sustain prolonged swimming, and more data are needed to determine migratory capacities. Compared to viviparous elasmobranchs, oviparous species such as skates have a reduced geographic distribution (Goodwin et al., 2005). This is thought to occur because skates are typically smaller in size than livebearing elasmobranchs, and size correlates with the ability to maintain wider geographic ranges (Musick et al., 2004). Additionally, skates have to restrict their ranges to suitable spawning habitats, because embryos are spatially and temporally constrained in the egg case for a prolonged period of time (one or more seasons; Palm et al., 2011; Di Santo, 2015). As a consequence, although some batoids undertake seasonal latitudinal migrations, some species, like the little skate in the Northwestern Atlantic, only show weak seasonal distribution patterns that consist of short distance movements from coastal and shallow waters to offshore and deeper waters during colder months (McEachran, 2002). Perhaps because of these spawning and spatial constraints, growth rates and maturation times are different in adjacent populations of little skates from the Gulf of Maine and Georges Bank (Di Santo, 2015). In addition, when the effects of increasing temperature and acidification on the costs of the escape response were tested in the little skate by employing a chasing protocol, performance showed a decline even with a modest increase in temperature (31C) beyond the thermal optimum (Fig. 6.7). This effect is particularly pronounced in skates from the Gulf of Maine, thus underscoring the importance of comparative studies of locally adapted populations within a species. An additional factor that can affect locomotor performance is acidification, which is known to exacerbate the effect of warming on elasmobranch swimming performance. In fact, increased water acidification reduced the escape performance (intensity of response and aerobic scope) in juvenile little skates from the Gulf of Maine, while a much less pronounced effect was observed in the Georges Bank population (Fig. 6.7). Even though the increase in temperature and acidification was not lethal in this species, it decreased endurance during the escape response, and prolonged recovery time after exhaustive exercise (Fig. 6.8), thus reducing the likelihood that the fish will be resilient in changing environment. While low pH increased recovery time in both populations, skates from the Gulf of Maine exhibited elevated metabolic

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Figure 6.7. (A) Time to fatigue, (B) turns to fatigue, (C) intensity of exercise measured in turns per minute (mean 7SE) for Leucoraja erinacea from the Gulf of Maine (n¼24) and the Georges Bank (n¼24) at three temperatures and two pH conditions (high¼8.1 and low¼7.7). Different pH levels were controlled as suggested by Riebesell et al. (2010) according to high emission scenarios by year 2100 model RCP 8.5 (IPCC, 2013). Different lower and upper case letters represent significant differences within high and low pH conditions, respectively; double daggers represent significant differences between pH treatment at each temperature; asterisks represent significant differences between populations (Tukey-Kramer MCT; a¼0.05) (Di Santo, in review).

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Figure 6.8. Post-exhaustion oxygen consumption responses (mean 7SE) in two populations (Georges Bank, A and B, and Gulf of Maine, C and D) of juvenile little skate Leucoraja erinacea (n ¼ 24 per population) raised in common garden conditions to mimic current and future levels of warming and acidification (high pH ¼ 8.1, low pH ¼ 7.7). Colors indicate different temperatures. The symbol * indicates significant difference in mean oxygen consumption between resting metabolic rates (controls) and post-exhaustion metabolic rates (repeated measures ANOVA followed by Dunnett’s test, p o 0.05) (Di Santo, in review).

rates for as much as double the time as individuals from Georges Bank (Fig. 6.8), making them potentially more vulnerable to ocean acidification. Whenever migration or dispersal capacities are restricted because of a limited locomotor capacity, or surrounding habitats are unsuitable, climate change is expected to cause widespread extinctions (Dulvy et al., 2008). Because the response to temperature and acidification increase is likely to be species- and age-specific, it is plausible to expect demographic and functional shifts in marine ecosystems (Perry et al., 2005). Local extirpation of ecologically important species, like elasmobranchs, have the potential to destabilize ecosystem functioning. It has been suggested that species with faster generation times will be able to respond more rapidly to environmental changes either through adaptation or by shifting geographic ranges toward more suitable habitats (Somero, 2010). However, elasmobranchs are typically large and even smaller species may grow and mature at a slow rate, making them particularly susceptible to rapid changes in the environment. Until recently, plastic responses were not considered a possible long-term solution to directional change in the environment, but recent studies have proposed that transgenerational acclimation to warming and acidification may increase performance of offspring of fishes exposed to increased

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temperature (Ho and Burggren, 2009; Donelson et al., 2011; Grossniklaus et al., 2013). Although a number of studies have examined the effect of ocean warming and acidification on teleost fishes over the past five years (e.g., Checkley et al., 2009; Baumann and Conover, 2011; Baumann et al., 2012; Nilsson et al., 2012), our understanding of the impacts on elasmobranch species is still surprisingly limited. To improve management practices for elasmobranch populations, there is an urgent need for implementation of multistressor studies on different life stages and on individuals sampled at different locations. This will allow us to identify critical life stages for survival, as well as the potential for acclimation and/or adaptation in swimming performance when directional environmental change occurs (Melzner et al., 2009; Checkley et al., 2009; Baumann and Conover, 2011; Baumann et al., 2012; Nilsson et al., 2012). Multistressor studies on different life stages and locally adapted populations may also allow us to understand the mechanisms underlying resilience to warming and acidification and ultimately can aid in determining “winning and losing” elasmobranch physiotypes under a changing climate.

8. CONCLUSIONS Despite considerable progress toward understanding elasmobranch locomotion in recent years, there is still much to be done with some surprising gaps remaining. In particular, there are relatively few data on elasmobranch locomotor energetics and batoid swimming energetics in particular, for which data are only available for one small skate species (Table 6.1). Active metabolic rates of pelagic sharks are certainly extremely challenging to measure directly, and controlled studies in a laboratory flume setting will be difficult to achieve given the complications of swimming large sharks in the confined space of a flume working section. Surrogate and indirect metrics such as heart rate do not provide a complete picture of the cost of transport, and it is likely that values of active metabolic rates for many shark species will remain largely inferential for some time to come. But even fundamental kinematic analyses of body and tail deformation during swimming are limited to a few species, and three-dimensional data are available for even fewer and mostly smaller species. A much broader quantitative study of locomotor kinematics in three-dimensions is key to understanding the diversity of locomotor modes and the relation between body shape and bending patterns of the body and tail during swimming and maneuvering. The remarkable diversity of elasmobranch shape and internal structure is not reflected in functional studies, which to date have focused on

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a very limited subset of diversity. A key challenge for the future is to extend current work on locomotor biomechanics to encompass a variety of species of different habits and forms. ACKNOWLEDGMENTS This work was supported by ONR-MURI Grant N000141410533 monitored by Dr. Bob Brizzolara, ONR grant N00014-09-1-0352 monitored by Dr. Tom McKenna, and by National Science Foundation grants EFRI-0938043 and CDI 0941674. Many thanks to all our collaborators for their assistance and efforts to better understand elasmobranch locomotion over the years.

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7 REPRODUCTION STRATEGIES CYNTHIA A. AWRUCH

1. Introduction 2. Classification of Reproductive Modes in Elasmobranchs 2.1. Females 2.2. Males 3. Mating Strategies and Parthenogenesis 3.1. Sperm Storage, Polyandry, and Multiple Paternity 3.2. Parthenogenesis 4. Classification of Reproductive Cycles in Elasmobranchs 4.1. Females 4.2. Males 4.3. Female-Male Reproductive Cycles 5. Endocrine Control of Reproductive Cycles in Elasmobranchs 5.1. Females 5.2. Males 5.3. Serotonin, Corticosteroids, Thyroid Hormone, and Calcitonin 6. The Future

Elasmobranchs are an evolutionarily conserved group that has successfully survived for over 400 million years. The permanence of elasmobranch populations has largely depended on the reproductive strategies of the population, as the primary requirement for successful propagation of any species and their individuals is the ability to reproduce. In vertebrates, reproductive strategies are regulated by the brain-gonadal axis, which controls the synthesis of reproductive hormones triggering all aspects related to reproduction. This chapter details the different reproductive strategies employed by elasmobranchs, from the wider range of reproductive modes including oviparity (egg-laying) and different forms of viviparity (livebearing); followed by a description of the different reproductive cycles, from seasonal to continuous, displayed by both sexes. Finally, the role of

255 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00007-9

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reproductive hormones in both females and males regulating gametogenesis and the different reproductive cycles are discussed. The endocrine control of the elasmobranch reproductive strategies are preserved throughout vertebrate evolution, however they are distinct within this group.

1. INTRODUCTION The primary requirement for successful propagation of any species and their individuals is the potential to reproduce, as such this is one of the most important life history events for any organism. Understanding the process of reproduction requires knowledge of the species’ reproductive strategies, which include a complex mixture of adapted characteristics designed by natural selection to solve ecological problems, how the species adapt their life history strategies in a giving environment (Stearns, 1976). The most effective reproductive strategy is one that produces as many fit progeny as necessary to ensure species survival. A number of diverse reproductive strategies have been developed by elasmobranchs during their long evolutionary history (400 million years). In males, the modification of the pelvic fins into claspers (copulatory organs) allows for internal fertilization (Grogan et al., 2012); while females have evolved a range of reproductive strategies characterized by two distinct parity modes: oviparity (egg-laying) and viviparity (live-bearing). Furthermore, there is substantial diversity of maternal-embryonic trophic relationships based on the method of nutrient input ranging from lecithotrophy where embryonic development is supported solely by the yolk sac with no additional maternal input, to matrotrophy where at least part of the embryonic development is supported by additional maternal input of nutrients (Carrier et al., 2004; Wourms, 1977, 1981). These series of reproductive strategies are expressed through reproductive cycles, which are regulated by a combination of physical and biological variables to ensure that young fish are produced in the most favorable environment for survival (Bromage et al., 2001; Pankhurst and Porter, 2003). Sperm or follicle production can be either seasonal or occur continuously throughout the year in males and females, respectively (Hamlett and Koob, 1999; Koob and Callard, 1999; Parsons and Grier, 1992; Wourms, 1977). Finally, the brain-pituitary-gonadal axis is a cascade system that regulates the entire reproductive process, promoting gametogenesis and subsequent gamete maturation (Awruch, 2013; Sherwood and Lovejoy, 1993).

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2. CLASSIFICATION OF REPRODUCTIVE MODES IN ELASMOBRANCHS 2.1. Females Traditionally, researchers have proposed a progressive general evolutionary transition for the Elasmobranchii and Holocephali, from a primitive condition of oviparity to a derived condition of viviparity (Compagno, 1990; Dulvy and Reynolds, 1997; Wourms and Lombardi, 1992) although there are rare cases of reversal from live-bearing to egg-laying at lower taxonomic levels (Dulvy and Reynolds, 1997). However, recent evidence suggest that viviparity was present in a Palaeozoic Elasmobranch and Holocephalan (Grogan et al., 2012), including the finding of two pregnant 318 Myr holocephalans, Harpagofututor volsellorhinus, supporting the hypothesis that multiple modes of viviparity were developed early in the chondrichthyan lineage (Grogan and Lund, 2011). A likely consequence of being predisposed to viviparity was the development of a chondrichthyan capacity for internal fertilization (Wourms et al., 1988). Similarly, when the reproductive modes are categorized on the basis of the maternal-embryonic trophic relationships, lecithotrophy has been commonly considered the more primitive form (Wourms, 1981; Wourms et al., 1988). However, new evidence showed that matrotrophic reproductive strategies were utilized by early Chondrichthyan lineages (Grogan and Lund, 2011; Musick and Ellis, 2005). Accordingly, in the last few years, recent fossil data have refined the proposed trend (from oviparity to viviparity) to a more recent theory postulating that multiple forms of viviparity are the ancestors in both the Elasmobranchii and Holocephali (Grogan and Lund, 2011; Long et al., 2009; Musick and Ellis, 2005). Based on parity and the maternal-embryonic relationship nine reproductive strategies have been identified in elasmobranchs (Fig. 7.1). 2.1.1. Oviparous Approximately 42% of elasmobranch species are oviparous (Compagno, 1990; Dulvy and Reynolds, 1997). All oviparous species are lecithotrophic, wherein embryos derive their sole source of nutrition throughout development from yolk reserves produced by the maternal liver that are sequestered in the yolk sac. Embryos possess two yolk sacs, the external and the internal yolk sac. During development yolk is mobilized from the external yolk sac and transported via the yolk stalk to the internal yolk sac and onward to the developing embryo by a rudimentary intestinal tract (Fig. 7.2). As

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Figure 7.1. Classification of reproductive modes in elasmobranch females according to parity and embryo nutrition.

development progresses, the internal yolk sac increases in size while the external yolk sac is digested until ultimately both are consumed and all that remains is a yolk-sac scar when yolk absorption is almost complete at hatching (Hamlett and Koob, 1999; Hamlett et al., 2005b). Oviparous species produce eggs that are enclosed in leathery, structurally complex, and durable egg cases before deposition on the seabed (Hamlett and Koob, 1999). Embryonic development occurs inside these egg cases (Blackburn, 2005; Wourms, 1977). The cases also contain the egg “jelly,” a gelatinous material that serves as hydrodynamic support for the egg/embryo during early development (Fig. 7.3) (Wyffels, 2009). The egg cases are tertiary egg envelopes as are produced by the oviducal glands, the specialized regions of the anterior portion of the oviduct secreting the structural proteins and enzymes that form the rigid cases (see Hamlett et al., 2005b for a complete review on the oviducal gland properties and functions). The sequence of egg case formation is a rapid process (12–24 h) that follows a similar but not identical pattern in all elasmobranch species (Koob et al., 1986). In the draughtboard shark, Cephaloscyllium laticeps, four stages have been distinguished (Fig. 7.3): (i) the posterior coiled tendrils of the egg case develop and protrude from the posterior part of the oviducal gland; (ii) the posterior half of the egg capsule develops extending from the oviducal gland;

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Figure 7.2. Embryo development in oviparous sharks. (A and B) External yolk sac (EYS) during early stages of embryo development. (C) EYS diminishes just before hatching. (D) Representation of the body cavity during embryo development. Internal yolk sac (IYS) and its connection to stomach (S) and spiral intestine containing spiral valve (SV) for digestion and absorption. External gill filaments (G) aid in respiration prior to development of gill lamellae. From Hamlett et al. (1993), with permission.

Figure 7.3. Egg case development in oviparous sharks. (A) Classification of the different egg case developmental stages in the draughtboard shark C. laticeps. (B) Egg case containing a recently ovulated egg showing the external yolk sac (EYS), the embryo (E) and the jelly (J) supporting the egg. From Awruch et al. (2009), with permission.

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(iii) the entire egg capsule is completed but the anterior coiled tendrils remain within the oviducal gland, and an egg can be distinguished inside the egg case; (iv) the egg case is fully formed, with no tendril attachments to the oviducal gland and is ready to be deposited (Awruch et al., 2008b). However, in the clearnose skate, Raja eglanteria, the development proceeds according to the following sequence: (i) formation of the anterior horns of the egg case; (ii) formation of the anterior two-thirds of the egg case; (ii) the fertilized egg flows into case; (iv) the posterior third of the egg case forms; and (v) the posterior horns of the egg case develop (Fitz and Daiber, 1963). While egg case formation is similar for all elasmobranch species, its final morphology varies widely and is likely related the ecological/biological role that each case plays during embryonic development (Flammang et al., 2007). For example, skates produce a concave “horn” type egg case that anchors the case to the sea floor (Mabragan˜a et al., 2011), however, the Port Jackson shark, Heterodontus portusjacksoni, forms a screw-shaped egg case that is lodged within rock crevices (Powter and Gladstone, 2008b); and many, but not all, elasmobranchs of the family Scyliorhinidae produce egg cases with extremely elongated tendrils for attachment to objects protruding from the substratum (Awruch et al., 2009; Ebert et al., 2006; Flammang et al., 2007). Parental care in the form of nest or egg guarding is not evident in oviparous elasmobranch fish (Compagno, 1990; Jacoby et al., 2012); therefore embryo survival is heavily reliant on selection of the appropriate substrate for egg case deposition. Consequently, egg cases are often deposited on complex habitat, containing rocky crevices and other hiding places, where neonates are expected to hatch in close proximity to one another (Jacoby et al., 2012; Powter and Gladstone, 2008a). In elasmobranch fish oviparity can be divided into two different modes (Compagno, 1990; Nakaya, 1975). Single (or extended) oviparity: in this case one egg is laid at a time from each uterus (posterior oviduct), usually in pairs (Castro et al., 1988; Luer and Gilbert, 1985). There is no embryonic development until the egg is laid, meaning all embryonic development occurs outside the mother. The number of egg cases deposited over the course of the spawning season (interval between depositions) and egg incubation times (interval from fertilization until hatching) varies significantly between species (Awruch et al., 2009; Heupel et al., 1999; Luer and Gilbert, 1985). Some oviparous species are polyovular, that is, multiple fertilized ova are enclosed in each egg case. For example, the big skate, Raja binoculata, produces large egg cases that contain two to seven embryos (Hitz, 1964). Approximately 39% of living elasmobranchs show extended oviparity, including all Heterodontiformes, some Orectolobiformes, some Carcharhiniformes, and all skates (Rajidae) (Compagno, 1990; Musick and Ellis, 2005).

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Multiple (or retained) oviparity: one or several egg cases are retained in each uterus where embryos develop to an advanced stage prior to oviposition. Egg cases are deposited on the seabed where embryonic development is completed in a relatively short time outside of the mother’s body. In the graceful catshark, Proscyllium habereri, each uterus contains only a single egg case at any one time prior to oviposition, while in the blackspotted catshark, Halaelurus buergeri, gravid females carry several egg cases in each uterus (Dodd and Dodd, 1986; Francis, 2006). In this last species ovulation is serial, thus, each case contains an embryo at a stage of development corresponding to the time at which the egg was ovulated. When embryos in the posterior region of the uterus are almost fully developed these cases are deposited on the seabed. To date, multiple oviparity has been reported only in nine species of Carchariniformes: five Halaelurus (Francis, 2006; Nakaya, 1975), two Galeus (Compagno et al., 2005; Costa et al., 2005; Wyffels, 2009), a single Proscyllid, P. haberari (Dodd and Dodd, 1986), and it may occur in a single species of Orectolobiform, Stegostoma fasciatum (Goto, 2001; Musick and Ellis, 2005; Wyffels, 2009). 2.1.2. Viviparous Viviparity is a highly successful reproductive mode and is the dominant form of reproduction found in approximately 58% of elasmobranchs (Compagno, 1990; Wourms, 1981). All viviparous elasmobranch species follow the same sequence in the reproductive development process: (i) ovulation; (i) fertilization; (iii) embryonic development to near-term inside the maternal body where the initial incubation phase occurs inside a thin capsule secreted by the oviducal gland (afterward the capsule may play a different role depending on the reproductive mode); and (iv) parturition of autonomous free living offspring. The existence of different modes of viviparity in elasmobranchs raises interesting questions regarding the evolution of these reproductive patterns. Numerous authors report that viviparity in elasmobranchs has evolved independently on multiple occasions in a number of divergent lineages (Compagno, 1990; Dulvy and Reynolds, 1997; Musick and Ellis, 2005; Wourms, 1981), with several factors being postulated to have contributed to the evolution of the different modes of viviparity such as; habitat selection, feeding ecology, predation (embryonic conspecific predation as well as other predatory species), maternal size, egg/embryo size, and maternal-fetal relationship (Compagno, 1990; Wourms, 1977, 1981). As with oviparous species there is no evidence suggesting parental care of any sort in viviparous elasmobranchs following parturition. Viviparity can be divided into two main categories according to embryonic nutrition (Musick and Ellis, 2005; Wourms et al., 1988) (Fig. 7.1).

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2.1.2.1. Lecithotrophic Viviparous. Nutrients are supplied solely by the yolk sac with no additional maternal input throughout embryonic development. This strategy includes only one form of viviparity, yolk-sac viviparity. In the last few years some confusion has occurred over the terminology used to classify yolk-sac viviparity (Musick and Ellis, 2005; Wyffels, 2009). Yolk-sac viviparity is an aplacental reproductive mode (no placental connection develops between the mother and the embryo) that has been historically called “ovoviviparity,” however since the 1970s the term “ovoviviparity” was replaced by “aplacental viviparity” (Compagno et al., 2005; Hamlett and Koob, 1999; Wourms, 1977). The reason behind this change is because early studies on several “ovoviviparous” species showed important differences in the source of nutrients during gestation (Amoroso, 1960). In yolk-sac viviparity near-term embryos show a dry weight loss in the order of 20–25% of the initial organic egg mass, because during gestation the egg is the only reservoir of organic material used in forming embryonic structures as well as serving as energy source (Amoroso, 1960; Hamlett et al., 2005b). In contrast, matrotrophic species generally show dry weight loss of less than 20% or weight gain during embryonic development, an indication that maternal input is providing supplemental nutrition beyond those accounted for in the yolk sac (Hamlett et al., 2005b). However, in some elasmobranch fish where the maternal input is minimal (see section 2.1.2.2 Incipient histotrophy) the differences between nonmaternal yolk sac and maternal inputs are difficult to distinguish, unless data on the organic content of the egg and near-term embryo are available (Braccini et al., 2007; Capape´ et al., 1990; Guallart and Vicent, 2001; Hamlett et al., 2005b). As a consequence, the term “ovoviviparity” was abandoned and replaced by “aplacental viviparity,” which now includes three major modes of elasmobranch reproduction; yolksac viviparity and two matrotrophic forms; histotrophy and oophagy (see section 2.1.2.2 Oophagy). However, in accordance with Musick and Ellis (2005) and Wyffels (2009), this term is only descriptive and by no means defines the diversity of viviparous modes found in elasmobranchs; thus, cautious should be taken when using the term. Yolk-sac viviparity occurs in about 18% of living elasmobranch species although it is entirely absent in Heterodontiformes and Lamniformes (Compagno, 1990). The embryo development occurs in two stages, the preand post-eclosion phases. During the pre-eclosion phase several species were found to encapsulate the ovulated eggs in an elongated, thin, translucent, and dense jelly-like substance for hydrodynamic support as the tertiary egg envelope or capsule, commonly called the candle (Graham and Daley, 2011; Jones and Geen, 1977; Jones and Ugland, 2001) (Fig. 7.4). The number of embryos the candle (in each uterus) may hold varies between species: for example in the dogfish, Squalus acanthias, and the hidden angel shark,

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Figure 7.4. Early stages (pre-eclosion) of embryo development in viviparous elasmobranchs. (A) Elongate, thin, translucent “candles” enclosing in utero eggs of Squalus megalops. (B) Encapsulated embryos (E) within later “candle” stages. (C) Uterus of Rhizoprionodon taylori containing eggs, each egg is enclosed by a “candle.” (A and B) From Braccini et al. (2007), with permission; (C) photo Daniela Waltrick.

Squatina occulta, an average of two to six eggs/embryos are enclosed in each candle (Kormanik, 1993; Sunye and Vooren, 1997), while only one egg/ embryo is contained in each candle in the little gulper shark, Centrophorus cf. uyato (McLaughlin and Morrissey, 2005). In addition, a pregnant whale shark, Rhinocodon typus, was found to carry about 300 embryos many of which were still attached to the external yolk sac and were enclosed in individual cases (Joung et al., 1996). Because the egg cases were not as fragile as the “candles” but not as tough as the typical oviparous egg cases, it has been postulated that whale sharks follow a yolk-sac viviparous reproductive mode (Joung et al., 1996). A similar reproductive mode was postulated for the nurse shark, Ginglymostoma cirratum, where embryos were enclosed in more durable capsules for the first 12–14 weeks of the 5- to 6-month gestation period with no evidence of any supplemental mode of embryonic nourishment (Castro, 2000). The initial pre-eclosion stage of the embryonic development occurs within the capsule, thereafter the capsule breaks open releasing the embryos freely into the uterus to complete the post-eclosion gestation to near-term (Kormanik, 1992; Sunye and Vooren, 1997). The timing of each phase varies between species. In some species such as S. acanthias eclosion occurs during early gestation (4–6 months in a 20- to 23-month gestational cycle) (Jones and Geen, 1977; Jones and Ugland, 2001), while in others such as the angel sharks S. occulta and S. guggenheim eclosion occurs at a more advanced stage of development (within 4 months of an 11-month gestational cycle) (Sunye and Vooren, 1997).

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Nourishment of the developing embryo and the process of yolk absorption and utilization is similar to those of oviparous species (Hamlett and Koob, 1999; Hamlett et al., 2005b; Jollie and Jollie, 1967). Nutrients are provided by yolk from an external yolk sac; whereas the internal yolk sac increases in size, external yolk-sac absorption is almost complete at parturition (Fig. 7.2) (Jollie and Jollie, 1967; Jones and Geen, 1977). In many species the internal yolk sac is not fully utilized at parturition as the newborns use this yolk as an energy reservoir while they are beginning to forage on their own (Jones and Geen, 1977). During gestation the embryo develops within the mother’s uterus. The uterus specializes in regulating the intrauterine environment, but not nutrient provision, providing respiratory exchange (supplying oxygen), osmoregulation (water and inorganic ions), and waste removal (Hamlett and Koob, 1999; Kormanik, 1992). The uterine wall in yolk-sac viviparous species is vascularized and folded to increase the respiratory membrane, but these folds do not possess secretory activity as in matrotrophic viviparous species (Kormanik, 1993; Otake, 1990). 2.1.2.2. Matrotrophic Viviparous. In this strategy, embryonic nutrients are initially supplied by the external yolk sac, and once these are exhausted, maternal nutrients will supplement the yolk through a variety of mechanisms (Hamlett and Koob, 1999; Wourms et al., 1988). Similar to yolk-sac species, there is a pre-eclosion phase wherein embryos are enclosed in a thin liable transient egg candle envelope. This strategy occurs in around 40% of viviparous elasmobranchs where maternal nutrients are supplied in the form of uterine secretions (histotrophy); by the ingestion of unfertilized eggs (oophagy) or sibling embryos (adelphotrophy); or placental transfer (placentatrophy) (Hamlett et al., 2005b; Musick and Ellis, 2005). Thus, six matrotrophic viviparity modes can be distinguished in elasmobranchs according to the trophic maternal-embryo relationship (Hamlett et al., 2005b) (Fig. 7.1). Histotrophy: embryos receive nutrients derived directly from maternal tissues. The uterus develops intrauterine vascularized folds (=villi) or compartments to transfer nutrients and regulate the intrauterine environment. The maternal uterus is specialized to secrete into the intrauterine lumen nutritive organic fluid known as “uterine milk” or histotroph, which is consumed by the embryo either by ingestion or absorption across the external gill filaments. The histotroph is rich in lipids, proteins, and carbohydrates, which allows the embryos to increase greatly in size during gestation. Species that display histotrophy show considerable variation in the quality and quantity of uterine secretions, and accordingly three types of histotrophic

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strategies have been distinguished in elasmobranchs: incipient, minimal, and lipid histotrophy. To date these strategies have been reported in species from the orders Squaliformes and Rajiformes suborder Myliobatoidei (stingrays), and among the Carcharhiniformes in the families Triakidae and Pristiophoridae (Hamlett et al., 2005b; Musick and Ellis, 2005). (i) Incipient histotrophy: although yolk is the primary nutrient throughout embryonic development, the uterine epithelial cells produce modest mucoid histotroph secretions, low in organic content, which supplement yolk supplies. There is a dry weight loss during embryonic development but not as extensive as in yolk-sac viviparity (Hamlett et al., 2005b; Storrie et al., 2009). For example, in the saw shark Pristiophorus sp., the eclosion from the initial capsule occurs well before the external yolk sac is absorbed and by approximately mid-term into the development, the internal yolk sac reaches a similar size as the external sac. During early gestation, the uterine epithelium forms robust villi with minor histotroph secretions, while in nearterm embryos the histotroph secretions diminish and there is an increase of intercellular spaces transferring water and minerals from the maternal to the uterine environment (Hamlett et al., 2005b). (ii) Minimal histotrophy: during early-mid gestation there is an abundant mucoid histotroph secretion to supplement yolk. The uterine epithelium does not form villi but does undergo secretory changes during gestation (Otake, 1990; Storrie et al., 2009). Later in gestation the uterine mucosa reduces histotroph secretion and forms individual uterine compartments, which isolate each embryo from its siblings, and each compartment increases the surface area for water and mineral transfer from the mother to the embryo. There is a substantial dry weight gain during embryonic development. This type of reproductive strategy has been extensively described in the gummy shark Mustelus antarticus (Storrie et al., 2009). Each embryo is enclosed in a tertiary egg envelope for the 11- to 12-month gestation period. Early-term M. antarticus embryos (2–3 months) possess large external yolk sacs and small internal yolk sacs, and the uterus has an increased number of mucosa cells, which indicates histotroph secretion of supplementary nutrients. Mid to late-term embryos (6–8 months) show no internal yolk sacs and small regressed external yolk sacs, thus yolk supplies are diminished by this stage. At this time, uterine compartments display expanded lumens, wider blood vessels, and a reduction of mucous cells. External yolk sacs are absent in full-term embryos. During embryonic development, there is an approximate 800% gain in dry mass as a result of the extensive histotroph secretion supplementing yolk stores in early to midgestation with water and mineral transfer being significantly enhanced later in gestation (Hamlett et al., 2005b; Storrie et al., 2009).

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(iii) Lipid histotrophy: fertilized eggs are enclosed in tertiary egg candle envelopes during very early stages of development that is yolk dependent. After eclosion, as the embryos grow in size the external yolk-sac reserves are depleted and the uterus increases in size to accommodate the embryos. The uterine epithelium forms elongated villi termed “trophonemata,” which significantly increase the surface area for histotroph secretion and respiratory exchange (Hamlett et al., 2005b; Smith and Merriner, 1986). The histotrophs are formed in secretory crypts contained in the trophonemata. Histotroph secretions are rich in lipids, with proteins and fatty acids also present albeit in lower concentrations (Hamlett et al., 2005b). In early gestation these secretions are modest, trophonemata display secretory crypts alternating with small vessels. In later gestation there is an increase in histotroph secretions and, as respiratory demands of the larger embryos are greater, morphological modifications (length and vascularization) of the trophonemata become evident to effectively reduce the diffusion distance for gas exchange from the mother to the embryo (Hamlett et al., 1985, 1996). This type of lipid histotroph reproductive strategy is typical of stingray species, where the rich histotroph secretion nourishing the developing embryo results in a massive weight gain of as much as 1680–4900% organic content during gestation (Needham, 1942). How trophonemata reach the embryo varies between stingrays; for example, in the lobed stingaree Urolophus lobatus, there was modest trophonemata production to supplement yolk supplies during early developmental stages (3–4 months), when embryos possessed a large external yolk sac. However, by the time embryos were 5 months old the external yolk sac was small, and the internal yolk was present in the abdominal cavity. By 6 months, no external yolk sac was present and the trophonemata become more elongated and enter the gill spiracles and mouth of the developing embryo (White et al., 2001). In contrast, in the southern stingray, Dasyatis americana, although similar gestational phases have been observed, there is no direct vascular maternal– fetal connection. The muscular uterus closely envelops the young and thus, trophonemata are brought into physical contact with the embryo (Hamlett et al., 2005b, 1996). Oophagy: embryos develop initially from yolk-sac nutrition. Thereafter, developing embryos ingest a continuous supply of yolk material from unfertilized eggs present in the uterus (Gilmore, 1993; Musick and Ellis, 2005). This type of reproductive strategy has been reported in all members of the order Lamniformes studied to date (Gilmore et al., 2005), and has evolved in the Pseudotriakidae family (order Carcharhiniformes) (Yano, 1992, 1993). Both groups produce large neonates requiring considerable maternal investment; however, the mechanisms of oophagy differ between species in terms of unfertilized egg production and storage of supplement

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yolk material. Within the Carcharhiniformes this reproductive strategy has been reported in the slender smoothhound, Gollum attenuates (Yano, 1993) and false catshark, Pseudotriakis microdon (Yano, 1992). Basically, the uterus of the gravid female contains egg envelopes that enclose the developing embryo in addition to a number of unfertilized ova. These undeveloped ova mostly disintegrate and provide exogenous yolk for the developing embryo, which ingests this exogenous yolk source and accumulates it in its external yolk sac. Following capsule eclosion, the embryo develops by using yolk nutrients from its own external yolk sac (endogenous) and by the yolk accumulated exogenously. In lamniformes, the yolk provided by multiple eggs is accumulated in the stomach of the developing embryo. Throughout most of the gestation period the mother continuously produces unfertilized eggs that the developing embryos actively feed on by storing the yolk in the cardiac stomach. Two different oophagous strategies are distinguished in lamnoid sharks (Gilmore, 1993; Gilmore et al., 2005). The most common strategy allows the development of multiple embryos (two to nine) per uterus wherein unfertilized eggs supplement the external yolk-sac nutrients; while the second strategy incorporates embryophagy as another source of nutrients (supplementing yolk sac and unfertilized eggs), which limits the progeny to one large embryo per uterus. This strategy, commonly called adelphophagy (or embryophagy or embryonic cannibalism), has only been documented in the sand tiger (or gray nurse) shark, Carcharias taurus (Gilmore, 1993; Hamlett and Koob, 1999), and although all lamnoids are oophagous not all are embryophagous. Although few lamnid sharks displaying a common oophagy strategy have been examined to date, such as the shortfin mako shark, Isurus oxyrinchus; porbeagle shark, Lamna nasus; great white shark, Carcharodon carcharias; and the thresher shark, Alopias superciliosus, capsule formation and variation in capsule morphology appears similar in all species (Francis, 1996; Francis and Stevens, 2000; Gilmore, 1993; Gilmore et al., 2005; Gruber and Compagno, 1981). Females produce different egg capsules throughout gestation relative to embryo nutritional needs, ranging from those produced early following ovulation containing no eggs and only a gelatinous ovalbumin/mucoid material to those containing numerous fertilized or unfertilized eggs. It is believed that only one embryo will develop to term in each capsule containing fertilized eggs, while capsules produced during the major oophagous interval during embryonic development contain the largest number of unfertilized eggs (Gilmore et al., 2005). Embryos develop functional teeth early, that are different from adult dentition and adapted for tearing open other egg capsules and during eclosion (Francis and Stevens, 2000; Shimada, 2002). Embryos in all species

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will typically metabolize all available yolk supplies in the last 2 months of a 10- to 15-month gestational period. During this period maternal production of large masses of yolk, which lasted for several months, ceases. At parturition, neonates are born with large body lengths, and need to function as active predators soon after birth. The number of neonates at birth varies between species. Most lamnid sharks produce fewer than 10 embryos, with a minimum fecundity of one to two embryos per uterus found in A. superciliosus, A. vulpinus, and A. pelagicus and maximum fecundity recorded in I. oxyrinchus (18 neonates) and C. carcharias (14 neonates) (Bruce, 1992; Gilmore, 1993; Gilmore et al., 2005; Moreno and Moron, 1992). The species in this reproductive strategy typically produce young with large body lengths up to 150 cm total length (TL) such as C. carcharias and Alopias vulpinus (Gilmore, 1993). Adelphophagy (embryophagy or intrauterine cannibalism): This is a form of oophagy in which the largest embryo in each uterus will consume all the smaller siblings, thereafter the developing embryo relies on unfertilized eggs for the duration of the gestation period. This reproductive mode has been identified in only a single species, C. taurus (Gilmore et al., 1983, 2005; Hamlett and Koob, 1999). Carcharias taurus females produce capsules containing fertilized embryos during the first 70 days of the 12-month gestation period. Most likely only one embryo (although up to three embryos have been found to develop within a single capsule) will reach finalterm. Once the largest embryo in the capsule reaches the size of about 100 mm at about 5–6 months, functional teeth have developed (Shimada, 2002). The dentition allows the embryo to breaks out of its own capsule into an intrauterine environment filled with egg capsules and to cut through these capsules to capture and consume the embryos within. Cannibalism assures rapid growth for 50 days producing a large embryo going from a relatively small size (about 60 mm TL) to the relatively large size (about 340 mm TL). With the completion of cannibalism, unfertilized yolk capsules are used as a food source, the oophagous stage. About 1 month prior to birth, ovulation ceases and the embryonic stomach decreases in size. The embryos are born at approximately 1000 mm TL (Gilmore et al., 2005; Hamlett and Koob, 1999). Placentatrophy: nutritional demands during early embryonic development are supported by the yolk sac with a progressive shift to histotroph, then the distal section of the yolk sac becomes modified to form a yolk-sac placenta physically connecting the mother and the embryo (Hamlett et al., 2005a; Otake, 1990). This type of reproductive strategy occurs in 9% of living elasmobranchs and only in sharks; five families within the Carcharhiniformes: Pseudotriakidae, Leptochariidae, Triakidae, Hemigaleidae, and Carcharinidae (Compagno, 1990; Musick and Ellis, 2005). Similar to other

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matrotrophic reproductive strategies, in early pre-implantation gestation stages, individual fertilized eggs/embryos are enclosed in a thin, translucent and dense jelly-like tertiary envelope. The egg is situated at the posterior end of the envelope and any excess envelope is folded anterior to the egg (Fig. 7.5). Initially, egg envelopes are free in the uterus and the embryos are nourished by yolk sac during this stage. Histotrophy is limited to a mucouslike substance that serves primarily as a lubricant. Thereafter, in the first few months of likely a 12-month gestation period, dorsal and ventral uterine flaps approach each other to form a separate uterine compartment for each embryo (Hamlett et al., 2005b; Pratt, 1979). The formation of uterine compartments, which increase surface area for metabolic exchange, is in concert with depletion of yolk-sac contents and a shift toward abundant histotroph secretions by the uterine epithelium into the uterine compartment. During later gestational stages the depleted yolk sac undergoes development modifications (placentatrophy) to form the embryo component of the placenta, while complimentary sites on the maternal uterus constitute the maternal component of the placenta. All placental transfers between the mother and the embryo originate from the uterine epithelium at the placental sites. In addition, supplement nutrients in the form of uterine histotroph are also provided by adjacent placental areas termed paraplacental sites (Hamlett, 1989; Hamlett and Hysell, 1998). Despite the common origin of yolk sac and uterus to form the placenta, there is morphological diversity between species. In the majority of the species the tertiary egg envelope is enclosed within each uterine compartment and this persists throughout gestation and becomes a component of the maternal-embryo interface. In the spadenose shark, Scoliodon laticaudus (Otake, 1990); the blue shark, Prionace glauca (Otake, 1990); and the bigeye houndshark, Iago omanensis (Fishelson and Baranes, 1998) the egg envelope degenerates and is not a component of the interface. In P. glauca the fetal epithelium is closely associated to the uterine mucosa (Otake, 1990), while a “trophonematous complex” connects the mother and the embryo (Hamlett et al., 2005a; Otake, 1990). In I. omanensis the embryo yolk sac forms “trophic villi” that will in turn interact with the maternal uterus (Fishelson and Baranes, 1998); however, the placentrophy process still remains very unclear in this species (Hamlett et al., 2005a). Independent of the type of morphological placentation displayed in the different species, this type of reproductive strategy could be included as special and a highly modified form of histotrophy as suggested by Hamlett et al. (2005a) “y. the placental transfers involve maternal secretion at the placental site rather than blood to blood transfer and calls into doubt whether any shark placenta is actually hemotrophic.” Further studies are necessary to clarify and understand placental mechanisms in sharks.

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Figure 7.5. Ontogenic development of uterine compartments in placental sharks. (A–E) Immature placental sharks possess an ovary (o) with developing follicles and small oviduct (ov), not differentiated into a uterus. A sexual maturity, yolked eggs (y) are shed from the ovary and enter the oviducal gland, where an egg envelope is formed around each egg. Fertilized eggs (e) reside in the uterine compartments (uc) and the excess egg envelope is sequestered in an egg envelope reservoir (asterisk). The yolk stalk differentiates into an umbilical cord (uc) and the yolk sac becomes a part of functional placenta (p). From Hamlett et al. (1993), with permission.

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2.2. Males Male elasmobranch fish have evolved complex and distinctive anatomical and physiological specializations as part of their reproductive strategy. The development of unique erectile copulatory organs, termed claspers, which are elongated modifications of the pelvic fins, allows for facilitation of sperm transfer into the female genital tract and internal fertilization (Callard et al., 1988; Long et al., 2009). Claspers play a critical role influencing reproductive success because with the acquisition of internal fertilization egg retention in females becomes a prerequisite and therefore all viviparous reproductive strategies become possible (Blackburn, 1992, 2005). The evolution of claspers in male elasmobranch fish required development of specific muscles necessary to transfer sperm through the claspers and maneuver the clasper into the correct position (Callard et al., 1988). Structural modifications, the degree of calcification, and size of the claspers, are necessary in all elasmobranch males during sexual development (Clark and Von Schmidt, 1965). Claspers need to be heavily calcified for successful maneuvering during copulation, thus changes in clasper calcification during puberty are required (Callard et al., 1988; Clark and Von Schmidt, 1965). In the majority of the species studied to date a rapid and abrupt increase in clasper length during puberty was observed (Ainsley et al., 2011; Awruch et al., 2008a; Francis and Duffy, 2005). However, in the bonnethead shark, Sphyrna tiburo, claspers grew in length continuously during puberty and did not reach functional maturity until a short period before mating activity commences in the mature population (Gelsleichter et al., 2002). The authors suggested that clasper growth appeared to be strictly regulated in S. tiburo to ensure growth of these organs to sizes critical for reproductive success. However, little is known about the relationship between clasper length and successful reproduction in elasmobranchs, and to what extent clasper size influences sperm competition and/or female choices. Sperm competition will influence the reproductive success of males, therefore clasper size is likely critical and maybe advantageous to the male particularly if semen deposition is proximal to the site of fertilization (Birkhead, 1998, 2000). Comparison with other vertebrates showing intromittent copulatory organs, the evolution of clasper size could be related to mate selection of a secondary sexual characteristics by females (Eberhard, 1985), although such behaviors have yet to be demonstrated in elasmobranch fish (Parsons et al., 2008). As the degree of calcification and size of claspers are external features that can be easily measured, clasper length and calcification are routinely used as an external diagnostic to assess sexual development in male elasmobranch fish. The calcification (or rigidity) of the clasper is assessed by hand, as either “uncalcified” when the organ is soft and easily bent; “partially calcified” when

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the organ is flexible but showing some degree of rigidity; or “calcified” when the organ is completely firm and resistant to deformation. Thus, three different reproductive developmental stages are usually distinguished in elasmobranch males: juveniles have uncalcified claspers, subadults with partially calcified claspers, and adults with fully calcified claspers (Awruch et al., 2008b; Francis and Duffy, 2005). Once male elasmobranch fish have reached sexual maturity there is no evidence of seasonal or life history variation in clasper calcification; however, cyclical variations in clasper size such as swollen claspers are correlated with mating season in the spotted catshark, Scyliorhinus canicula, and the Epaulette shark, Hemiscyllium ocellatum (Garnier et al., 1999; Heupel et al., 1999). Variations within the internal reproductive system and the capacity of males to produce sperm, have been observed in several species (Garnier et al., 1999; Heupel et al., 1999; Sumpter and Dodd, 1979) with sperm production and male reproductive strategies falling into two categories. Continuous sperm production: this reproductive strategy is characterized by little or no seasonal changes in testicular development and sperm production after males reach first sexual maturity. Continuous production of mature spermatocysts (a functional testicular unit where spermatogenesis occurs ultimately ensuing the production of mature sperm) has been observed in several elasmobranch species such as: the winter skate, Leucoraja ocellata (Sulikowski et al., 2004); the thorny skate, Amblyraja radiata (Sulikowski et al., 2005b); P. glauca (Pratt, 1979); and C. laticeps (Awruch et al., 2009). Seasonal sperm production: this strategy is characterized by marked seasonal changes in sperm production once males reach first sexual maturity. In the majority of male elasmobranch fish studied to date the relative abundance of the different stages of spermatogenesis varies seasonally. For example, in the starspotted smooth-hound, Mustelus manazo; the spotless smooth-hound, Mustelus griseus; H. ocellatum; S. canicula; and S. acanthias advance spermatogenesis stages were found to be highly correlated with the mating season (Garnier et al., 1999; Heupel et al., 1999; Simpson and Wardle, 1967; Teshima, 1981). However in S. tiburo, testis undergo an annual testicular cycle of complete regression and recrudescence where not all spermatogenic stages were present throughout the year (Parsons and Grier, 1992).

3. MATING STRATEGIES AND PARTHENOGENESIS The whole point of mating in elasmobranch species is the successful deposition of semen inside the female’s reproductive tract (Birkhead, 2000). Individual male elasmobranch fish will have greater fertilization success if

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their sperm are deposited closer to the female oocytes, however, a more distant deposition of sperm may provide the female fish with greater control over fertilization. This conflict provides potential rationale for the observed differences in mating strategies displayed by elasmobranch species in addition to explaining much of the variation in the reproductive anatomy of females and males. While males have evolved large claspers to place the sperm in the optimal position within the female’s reproductive tract, females have evolved long reproductive tracts to retain some control over fertilization (Pratt and Carrier, 2005). Logistical problems associated with studying elasmobranch fish in their natural habitat have resulted in a paucity of studies examining mating behavior of elasmobranch fish in the wild. Thus knowledge of their mating processes (courtship, copulation, and post copulation) is very limited and mostly the result of captive observations. Copulation is typically accomplished by the male holding the female, by biting her and inserting the clasper into the female’s cloaca. However, there is a substantial variety of mating positions in elasmobranchs, even in the small proportion of species where such behaviors have been observed; that is probably related to the differences in body form and swimming behavior (Demski, 1990). In sharks, the male tends to coil himself around the female, grabbing a pectoral fin in his mouth and inserting into the cloaca. In skates and rays, males make either a dorsal or ventral approach and copulation occurs in a “ventral to ventral” position with the female upright, above or below the male (Chapman et al., 2003; Pratt and Carrier, 2001; Tricas, 1980; Uchida et al., 1990). Commonly only one clasper is inserted into the female’s cloaca with males alternating the use of the right and left clasper in successive copulation events (Carrier et al., 1994; Tricas and Le Feuvre, 1985); however, the insertion of both claspers has also been observed in the Javanese cownose ray, Rhinoptera javanica (Uchida et al., 1990). Furthermore, the duration of copulation varies between species, from 10 to 30 s in the chain dogfish Scyliorhinus rotifer (Castro et al., 1988) and the southern stingray, Dasyatis americana (Chapman et al., 2003); 1–2 min in C. Taurus (Gordon, 1993); and up to 35 min in H. ocellatum (West and Carter, 1990). Females remain passive during copulation, often displaying bite wounds on their fins, body, gills, and cloaca during the mating season (Gilmore et al., 1983; Gordon, 1993; Pratt, 1979). Interestingly, sexual dimorphism is evident in the skin and dentition of several elasmobranch species. Differences in skin thickness between the sexes were observed in P. glauca and D. sabina wherein dermal layers of the body surface are significantly thicker in maturing and adult females than in a corresponding region of same size males (Kajiura et al., 2000; Pratt, 1979). Differences in dental morphology between sexes in addition to seasonal

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changes in adult dentition may reflect changes in behavior related to mating. In the stingray, Dasyatis akajei; the Atlantic stingray, Dasyatis sabina; the Bullseye round stingray, Urobatis concentricus; and S. canicula (Crooks et al., 2013; Kajiura and Tricas, 1996; Kajiura et al., 2000; McCourt and Kerstitch, 1980; Taniuchi and Shimizu, 1993) the teeth of adult males are more pointed than those of females. The authors suggested that these differences cannot be attributed to food preference but rather dentition changes in males at sexual maturity were an adaptive mechanism to assist with establishing adequate grip during mating. 3.1. Sperm Storage, Polyandry, and Multiple Paternity Sperm storage has been commonly reported in elasmobranchs (Pratt, 1993) and may have co-evolved with elasmobranch mating strategies. The principal site for fertilization and sperm storage occurs in the oviducal gland of adult females; however, in species that do not store sperm fertilization is believed to occur in the upper oviduct region (Gilmore et al., 1983; Hamlett et al., 1998, 2005b). Sperm storage is an advantage to fertilize all oocytes, yet may not be required if mating within a population is synchronous, while storage is essential for nomadic species that at time mate opportunistically. The time of sperm storage varies between species and can be a short as 5–6 weeks in the blonde skate Raja brachyura (Clark, 1922); to at least 3 months in R. eglanteria (Luer and Gilbert, 1985); 15 months in C. laticeps (Awruch et al., 2009); and more than 2 years in S. canicula (Dodd et al., 1983). Multiple mating is the act of a female mating more than once in a single breeding season either with the same male or different males. When multiple mating includes several males contributing to a female’s litter, the mating system is called polyandry (DiBattista et al., 2008a). This mating strategy is likely to trigger pre-copulation male–male competition and/or postcopulation sperm competition. The ability of the majority of elasmobranch females to store sperm in the oviducal glands may allow sperm competition to occur among males mated over an extended period raising the possibility of post-copulation mate choice by the female (Carrier et al., 1994; Pratt and Carrier, 2005). Since mating and courtship practices of elasmobranchs are poorly characterized, the degree of pre- and post-copulation choices that females are able to exercise is still unknown (Pratt and Carrier, 2005). Many elasmobranch species were reported to congregate at particular mating grounds (Carrier et al., 1994; Pratt and Carrier, 2001), likely providing an arena for female choice and male–male competition. When polyandry is common, males will compete for access to females, while females may

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develop counter-strategies such as seeking refuge and exhibiting avoidance behavior, to limit male access (Sims, 2005; Sims et al., 2001, 2005). For example, in G. cirratum multiple males were observed pushing and grasping the same female during mating activities, although only a small percentage of mating attempts ended in copulation because of avoidance behavior displayed by the female (Carrier et al., 1994). Females may benefit directly or indirectly from polyandry (Birkhead, 2000; Tregenza et al., 2006; Zeh and Zeh, 2001). Direct benefits are those that increase reproductive success, provide direct material to females or their offspring (e.g., shared parental care or nuptial gifts for females), while indirect genetic benefits may not affect reproductive success of the females, but may increase reproductive success or survivorship of the offspring (e.g., increasing genetic variance in progeny, precopulatory or postcopulatory trading-up of “good genes,” and post copulatory defense against genetic incompatibility) (Tregenza et al., 2006; Zeh and Zeh, 1997). The occurrence of polyandry in many elasmobranch species alongside the high cost of mating (as mating injuries have the potential to cause extensive blood loss and infection) suggest that polyandry provides benefits to elasmobranch females. However, these are not direct benefits as females and their offspring do not receive any material benefit from males (DiBattista et al., 2008a; Fitzpatrick et al., 2012). It is likely that strong indirect genetic benefits are related to an opportunity for pre-fertilization selection paternity and/or post-fertilization sperm selection (Chapman et al., 2004; Fitzpatrick et al., 2012). By increasing the number of sperm donors, females may ensure additive effects of paternal genes in offspring and/or may minimize the possibility of unsuccessful mating with infertile males, which enables females to exploit post-copulatory mechanisms that minimize the risk and cost of fertilization by genetically incompatible sperm (DiBattista et al., 2008a; Fitzpatrick et al., 2012; Zeh and Zeh, 1997). The most straightforward method for biasing fertilization success available to females is to exert precopulatory mate choice for preferred males (Barbosa and Magurran, 2006; Birkhead and Moller, 1993). However females can also exercise cryptic choice for preferred males through a variety of post-copulatory processes (Fitzpatrick et al., 2012) by either accepting fewer sperm from undesirable males or by ejecting sperm from undesirable males after copulation. In addition, the storage of sperm in the oviducal glands for many months may allow sperm competition to occur over a protracted period, which allows females to weed out incompatible sperm and to differentially utilize sperm from preferred males (Birkhead, 1998; Feldheim et al., 2002). Multiple paternity, the siring of a single brood of offspring by multiple males, is direct evidence of polyandry and has been highlighted in a number of

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species of elasmobranchs using genetic tools and has been observed in the lemon shark, Negaprion brevirostris (Feldheim et al., 2001); G. cirratum (Saville et al., 2002); S. tiburo (Chapman et al., 2004); S. canicula (Lage et al., 2008); the sandbar shark, Carcharhinus plumbeus, the bignose shark, Carcharhinus altimus, the Galapagos shark, C. galapagensis (Daly-Engel et al., 2006, 2007); and the leopard shark, Triakis semifasciata (Nosal et al., 2013). However, the frequency of multiple paternities varies widely. For example, a predominance of genetic monogamy has been reported in the shortspine spurdog, Squalus mitsukurii (Daly-Engel et al., 2010) and S. tiburo (Chapman et al., 2004), while a predominance of genetic polyandry has been reported in N. brevirostris (DiBattista et al., 2008b; Feldheim et al., 2001) and S. canicula (Griffiths et al., 2012). Moreover, rates of multiple paternity can also vary among populations of a single species, for example, in C. plumbeus multiple paternity ranges from 40% in the central Pacific Ocean to 85% in the North-West Atlantic Ocean (Daly-Engel et al., 2007; Portnoy et al., 2007). Daly-Engel et al. (2010) and Nosal et al. (2013) suggested that the frequency of multiple paternity is correlated with female aggregation behavior reflecting the probability of encountering mates during each mating period, which varies among and within species depending on the extent of sexual segregation (Sims, 2005; Wearmouth and Sims, 2008). For example, prolonged sexual segregation might account for the low multiple paternity frequencies in S. mitsukurii and T. semifasciata (Daly-Engel et al., 2010; Nosal et al., 2013), while the comparatively high frequency in N. brevirostris might be due to the formation of dense mixed-sex mating aggregations (Feldheim et al., 2002). 3.2. Parthenogenesis True parthenogenesis (Greek for “virgin birth”) is a form of asexual reproduction in which the production of offspring occurs in the absence of any male genetic contribution. Females produce unfertilized eggs that will develop into viable embryos (Neaves and Baumann, 2011). Parthenogenesis has been documented in bony fishes, reptiles, amphibians, birds (Neaves and Baumann, 2011), and most recently in elasmobranchs (Chapman et al., 2007; Feldheim et al., 2010; Portnoy et al., 2014). There are two forms of parthenogenesis: in apomictic parthenogenesis the germ line cells (gametocytes) bypass meiosis to undergo only regular cell divisions (mitosis) to produce an egg that is genetically identical to its mother (i.e., the maternal genome is transmitted to the embryo intact), while in automictic parthenogenesis (automixis) there is a fusion of post-meiotic cells in the mother producing offspring with elevated homozygosity compared to its mother (i.e., genetic diversity is lost in transmission) (Lampert et al., 2007;

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Watts et al., 2006). Parthenogenesis is defined as “obligate” when organisms exclusively reproduce through asexual means, while it is “facultative” when species that ordinarily rely on sexual reproduction can resort to facultative parthenogenesis under extenuating circumstances that isolate females from males (Booth et al., 2012; Neaves and Baumann, 2011). Parthenogenesis has been confirmed, using genetic data, in five species of captive elasmobranchs: S. tiburo (Chapman et al., 2007); C. limbatus (Chapman et al., 2008); the whitespotted bamboo shark, Chiloscyllium plagiosum (Feldheim et al., 2010; Voss et al., 2001); S. fasciatum (Robinson et al., 2011); and the whitetip reef shark, Triaenodon obesus (Portnoy et al., 2014). The studies provided evidence that all these species utilized an automixis form of parthenogenesis as a reproductive strategy and viable offspring were produced. In some of these cases females have produced several healthy offspring over multiple reproductive cycles, and although in many cases the mortality rate across the litters was very high (more than 80%), some other pups were able to live for at least 5 years (Feldheim et al., 2010; Robinson et al., 2011; Voss et al., 2001). Increasing cases of parthenogenesis have been reported in elasmobranchs; however, if this reproductive strategy benefits and how it may benefit elasmobranch populations remains unknown. Although the ability for females to reproduce through facultative parthenogenesis would be selectively advantageous in situations where males are sparse (e.g., a possibility in the wild due to low population densities caused by overexploitation), very little is known about the long-term viability of automictic parthenogenesis in elasmobranchs and the occurrence of parthenogenesis in wild populations. The reduction in genomic diversity in automictic parthenogenesis could reduce female fitness by increasing expression of recessive genetic disorders (Neaves and Baumann, 2011; Watts et al., 2006). Thus, the genetic costs of parthenogenesis may offset the benefit of having a mechanism to avoid occasional reproductive failure in elasmobranch populations. However, if females have no other options available for passing on genes, then this strategy would require that at least some portion of the offspring produce viable gametes (Portnoy et al., 2014).

4. CLASSIFICATION OF REPRODUCTIVE CYCLES IN ELASMOBRANCHS A reproductive cycle is defined as a series of events that an organism must undergo in order to reproduce. In female elasmobranch fish, these events are the ovarian cycle (follicle development for ovulation); mating;

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pregnancy (egg case formation and retention in oviparous); and parturition (oviposition in oviparous). Males are less complex and just require the testicular cycle (the production of sperm) and mating. In elasmobranchs as in many other vertebrate species, these series of events are coupled and regulated by environmental factors (e.g., photoperiod, water temperature), and each event occurs consistently at certain times of the year with the ultimate aim to ensure that young are born when environmental conditions are the most favorable for survival (Luer and Gilbert, 1985; Mull et al., 2008; Waltrick et al., 2014; Wourms and Demski, 1993). 4.1. Females Four categories of reproductive cycles can be defined for elasmobranch females: (i) species that are reproductively active throughout the year, (ii) species that are reproductively active throughout the year, but exhibit seasonal periods where a greater proportion of reproductive activity occurs, (iii) species with a well-defined seasonal cycle, where animals are reproductively active for only a portion of the annual cycle, and (iv) species that are pregnant for approximately a full year, after which they spend a year or two in dormancy (Hamlett and Koob, 1999; Koob and Callard, 1999; Wourms, 1977). 4.1.1. Continuous Breeders Continuous breeders include both oviparous and viviparous species in categories (i) and (ii). Among oviparous elasmobranchs, species such as the smalleyed catshark, Apristurus microps (Ebert et al., 2006) and A. radiata are reproductively active year-round (Sulikowski et al., 2005a), while species such as, L. ocellata (Sulikowski et al., 2004); C. laticeps (Awruch et al., 2009); and S. canicula (Henderson and Casey, 2001; Sumpter and Dodd, 1979) display a partially defined reproductive cycle with females capable of continuously laying eggs but showing a seasonal peak in activity. For example, C. laticeps females lay eggs in pairs at monthly intervals throughout the year, but with a peak in egg deposition between January and June (Awruch et al., 2009), while L. ocellata egg case production peaks in September through November (Sulikowski et al., 2004). In continuous oviparous breeders the ovarian cycle is incessant throughout the reproductive cycle because these oviparous species are intermittent ovulators, the follicular development continues throughout the protracted ovulatory period (Koob and Callard, 1999) (Fig. 7.6). In viviparous continuous breeders pregnancy lasts nearly a full year, with mating and the subsequent pregnancy ensuing soon after parturition (Koob and Callard, 1999). For example, the Pacific angel shark, Squatina californica,

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Figure 7.6. Continuous reproductive cycle in elasmobranchs. In viviparous elasmobranchs follicle development is either restricted to the later gestational stages (A) or continuous throughout pregnancy (B). In oviparous elasmobranchs follicle development runs parallel with encapsulation and egg retention (C). Adapted from Hamlett and Koob (1999), with permission.

and several Mustelus species (family Triakidae) were reported to display an annual reproductive cycle with a 9- to 12-month gestation period (Conrath and Musick, 2002; Natanson and Cailliet, 1986). Similarly, R. taylori is an annual reproducer with a gestation period of 11.5 months during which time embryonic development is diapaused at the blastodisc stage for a 7-month period (Waltrick et al., 2014). In contrast, S. acanthias does not have an annual cycle, but a biannual cycle with a 22-month gestation period and mating occurring every 2 years (Chatzispyrou and Megalofonou, 2005; Jones and Ugland, 2001; Tsang and Callard, 1987b). The ovarian cycle in viviparous continuous breeders is superimposed on pregnancy; however, in some species follicle development continues throughout pregnancy or is restricted to the later gestational phase (Koob and Callard, 1999). In M. canis follicle size parallels embryo size with follicles reaching ovulation size at the time of parturition, indicating tight parallel control of the ovarian and gestational cycle (Conrath and Musick, 2002). In contrast, in S. acanthias follicular development is restricted during the initial half of pregnancy but then proceeds rapidly through the remainder of gestation, and follicles reach ovulation size at the time of parturition just prior to mating (Koob and Callard, 1999; Tsang and Callard, 1987b) (Fig. 7.6).

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4.1.2. Seasonal Breeders Seasonal breeders include oviparous and viviparous elasmobranch species in categories 3 and 4. A well-defined seasonal reproductive period has been reported in several oviparous species. In H. ocellatum (Heupel et al., 1999) and R. eglanteria (Rasmussen et al., 1999) egg laying occurs during a 6-month period of the year, while in the Port Jackson shark, Heterodontus portusjacksoni, and the filetail shark, Parmaturus xaniurus, oviposition is restricted to 1–2 months (Flammang et al., 2008; Powter and ´ vila et al., 2007). A large reserve of developing Gladstone, 2008b; Tovar-A follicles are present in the ovaries throughout the reproductive cycle; however, mature follicles ready to be ovulated are observed only during the egg laying season (Heupel et al., 1999; Koob et al., 1986) (Fig. 7.7). Pregnancy in viviparous seasonal elasmobranchs either persists for several months while the remainder of the year is dormant or lasts 1 year followed by a year or two dormant (Koob and Callard, 1999; Wourms and Demski, 1993). For example, D. sabina and S. tiburo display 5- to 6-month gestation periods within the annual cycle (Manire et al., 1995; Snelson et al., 1997), while C. plumbeus has a 2-year reproductive cycle with parturition occurring every 2 years and pregnancy lasting 1 year and during the intervening year females are not pregnant (McAuley et al., 2007). Similarly, the broadnose sevengill shark, Notorynchus cepedianus, appears to have at least a bi-annual reproductive cycle, being pregnant for approximately 1 year and spending

Figure 7.7. Seasonal reproductive cycle in elasmobranchs. In viviparous elasmobranchs follicle development occurs between pregnancies; after parturition a resting period might follow before follicle developed restarts (A). In oviparous elasmobranchs complete follicle development occurs between the laying periods; however, as these cycles could last weeks or months, later stages of follicle development and maturation occurs in parallel with capsule formation and egg retention during the laying period (B). Adapted from Hamlett and Koob (1999), with permission.

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at least 1 year nonpregnant (Awruch et al., 2014). Then again, the reproductive cycle in the Portuguese dogfish, Centroscymnus coelolepis, and the lantern shark, Etmopterus spinax, likely encompasses a 1-year pregnancy separated by 2 years of nonpregnancy (Coelho and Erzini, 2008; Figueiredo et al., 2008). Ovarian cycles in seasonal breeders occur exclusively between pregnancies, and during the nonpregnant months immediately preceding ovulation, follicular development rapidly increases (Coelho and Erzini, 2008; Koob and Callard, 1999; McAuley et al., 2007) (Fig. 7.7). 4.2. Males In male elasmobranch fish sperm production can be either seasonal or occur throughout the year and can be coupled or not with the mating period (Parsons and Grier, 1992). For example, in species such as C. laticeps, L. ocellata, A. radiata, and P. glauca males are able to produce spermatozoa all year round (Awruch et al., 2009; Pratt, 1979; Sulikowski et al., 2004, 2005a). In contrast, H. ocellatum, S. canicula, S. tiburo, M. manazo, and M. griseus show clear seasonality in their reproductive cycles as a pronounced seasonal change in testicular development is observed (Garnier et al., 1999; Heupel et al., 1999; Manire and Rasmussen, 1997; Teshima, 1981). However, Crews (1984) and Parsons and Grier (1992) suggest that a seasonal peak in testicular development may not necessarily coincide with the peak in the mating season, thus gonadal activity and mating behavior are not necessarily functionally associated. In many seasonally breeding vertebrates, sperm production immediately precedes or coincides with mating behavior. This pattern of gonadal activity in relation to mating is defined as an associated reproductive tactic observed in several species of elasmobranchs wherein seasonal sperm production coincides with a defined mating season (Heupel et al., 1999; Tricas et al., 2000). However, a dissociated reproductive tactic occurs when sperm production is decoupled from mating. This reproductive strategy has been reported in M. griseus, M. manazo, and the round stingray, Urobatis halleri, wherein approximately 5–6 months intervene between peak testicular development and the mating season (Mull et al., 2008; Teshima, 1981) and about 2 months in S. tiburo (Manire and Rasmussen, 1997). In several elasmobranch male species, sperm have been reported to be stored in the male reproductive tract (weeks to months) before transfer to the female (Pratt and Tanaka, 1994). The reasons underlying this apparent decoupling between testicular development and mating behavior remain unknown. One possible explanation is that the physiological mechanisms leading to sperm production and possible sperm storage do not always correspond with the mating season, which is mainly regulated by female reproductive strategies. Studies on sperm production showed that there is an inverse relationship between

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sperm production and its accumulation with temperature (Garnier et al., 1999; Heupel et al., 1999; Mull et al., 2008). Moreover, in oviparous females inhabiting warmer waters, the period of sperm storage by the oviducal gland is usually coincident with the winter months (Ellis and Shackely, 1995; Luer and Gilbert, 1985; Rasmussen et al., 1999). It could be hypothesized that the short periods of sperm storage reported for elasmobranch females in lower latitudes may reflect the inability of sperm to survive for long periods at elevated temperatures (Kime and Hews, 1982). It is likely that the production and storage of sperm decoupled from the mating season may allow males to produce sperm when the physiological conditions are more favorable and mate as soon as environmental conditions are conducive and females are present. 4.3. Female–Male Reproductive Cycles The relationship between female and male reproductive cycles can vary. The male and female of the same species may differ fundamentally in their reproductive tactics (Ellis and Shackley, 1997; Henderson and Casey, 2001) or both sexes may have a synchronized reproductive cycle (Heupel et al., 1999; Kyne and Bennett, 2002; Sulikowski et al., 2004). For example, a clear seasonal reproductive period for both females and males has been reported in H. ocellatum wherein females lay eggs from August to January and males have the highest volume of sperm in the epididymis during August to November (Heupel et al., 1999), while in A. radiata both sexes are reproductively active all year round (Sulikowski et al., 2005a). In contrast, although C. laticeps females were able to reproduce all year round, a peak in egg deposition was found between January to June. However, males did not show a peak in sperm production at any time of the year. Similarly, S. canicula females and males presented unsynchronized cycles, wherein females have a higher follicle production, which reaches ovulation size in May and males have higher sperm production in November through December (Henderson and Casey, 2001). For species that are able to store sperm, both for males (Pratt and Tanaka, 1994) and more commonly for females (Pratt, 1993), there is no necessity to have a synchronous reproductive cycle between both sexes. 5. ENDOCRINE CONTROL OF REPRODUCTIVE CYCLES IN ELASMOBRANCHS Data on elasmobranch reproductive endocrinology is available for a limited number of species. As a consequence, understanding of the endocrine mechanisms that control the diversity of reproductive strategies

7.

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that have evolved in elasmobranchs is limited in comparison with other vertebrate groups (Awruch, 2013; Gelsleichter and Evans, 2012). There is a considerable structural and functional similarity with other vertebrates, however, many hypotheses of the endocrine pathways regulating elasmobranch reproduction have not yet been proven. As in other vertebrates, the hypothalamus–pituitary–gonadal (HPG) axis regulates all aspects of reproduction in elasmobranchs (Callard et al., 1989b; Forlano et al., 2000). The release of gonadotropin-releasing hormone (GnRH) produced mainly in the hypothalamus stimulates the production of the gonadotropins (GT) from the pituitary gland (Sherwood and Lovejoy, 1993; Wright and Demski, 1993), which in turn will regulate the synthesis of steroid hormones by the target cells (Fig. 7.8). To date, two genes for GnRH-I and GnRH-II have been identified in elasmobranchs with the potential for a third – GnRH-III (D’Antonio et al., 1995; Lovejoy et al., 1993; Tostivint, 2011). GnRH acts by binding

GnRH

VL

GTH

L

Vtg

E2 Gonadal steroids Figure 7.8. General scheme of the hypothalamus–pituitary–gonadal (HPG) axis regulation. The hypothalamus produces and releases gonadotropin-releasing hormone (GnRH) to the pituitary ventral lobe (VL), which will synthetize gonadotropic hormones (GTH) to regulate steroid production by the gonads. These steroids have a paracrine regulation over the gonads, and will regulate further production of GTH and GnRH. In females, estradiol (E2) will activate and regulate vitellogenin (Vtg) production by the liver, which in term will control vitellogenin intake during follicle development.

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to a G-protein coupled-receptor GnRHR (Zohar et al., 2010) and while multiple forms of GnRHR have been identified in vertebrates (Kim et al., 2011), it has yet to be identified in elasmobranch fish. Elasmobranchs lack a direct neural or vascular connection between the hypothalamus and the ventral lobe of the pituitary where the gonadotropic hormones (GTH) are known to be present. Thus, all forms of GnRH are likely released into bloodstream and transported to the ventral lobe where they will regulate GTH synthesis (D’Antonio et al., 1995; Pierantoni et al., 1993; Sherwood and Lovejoy, 1993). Two forms of GTH, sharing similar structural characteristics to follicle stimulating hormone (FSH) and luteinizing hormone (LH), have been identified in elasmobranchs (Que´rat et al., 2001). It has been suggested that these two forms play a similar role as described for FSH and LH in regulating gametogenesis and steroidogenesis in vertebrates (Dobson and Dodd, 1977; Dodd et al., 1983; Levavi-Sivan et al., 2010; Maruska and Gelsleichter, 2011). However, FSH and LH actions at the level of the gonads through the cell specific expression of the FSH and LH receptors remains unclear as these receptors have yet to be identified in elasmobranch fish. Based on evidence in other vertebrate groups it is likely that the gonadotropin–receptor complex triggers the adenylate cyclase signaling cascade leading to the activation or de novo synthesis of steroid synthesizing enzymes resulting in production of steroid hormones (Eckert, 1988). The gonads in both females and males are the primary producers and source of steroid hormones (Fasano et al., 1989; Pankhurst, 2008), and as in other vertebrates the primary gonadal steroids involved in the elasmobranch reproductive events are the C21 steroids (progestins), the C19 steroids (androgens), and the C18 steroids (estrogens) (Fig. 7.8). 5.1. Females The gonadal steroids that have been more extensively studied are progesterone (P4), 17b-estradiol (E2), and testosterone (T) (Awruch, 2013; Maruska and Gelsleichter, 2011). In females, E2 and T are mainly produced by the granulosa and theca cells of ovarian follicles, and while granulosa cells are also capable of producing P4, the corpora lutea is the primary source of this gonadal steroid (Lutton et al., 2005). There is considerable diversity in the follicular cycle of female elasmobranch fish regardless of the viviparous or oviparous strategy used (Koob and Callard, 1999). In both viviparous and oviparous species follicle development either overlaps or is temporarily separated from the period of egg laying, egg retention, or pregnancy. This diversity in reproductive cycles confirms that the endocrine structures developed a pivotal system for regulating pre- and post-ovulation reproductive events (Callard et al., 2005b; Koob and Callard, 1999).

7.

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5.1.1. Oviparous In oviparous elasmobranchs, studies on endocrine and morphological correlates of reproductive events and in situ experiments investigating the role reproductive steroids have been reported for only a few species (Awruch, 2013). It is well recognized that the principle role of E2 during the ovarian cycle is preparing the female reproductive tract for ovulation; however, the role of E2 during egg encapsulation and oviposition remains unclear (Fig. 7.9). The main role of E2 in fish displaying oviparous reproductive cycles is to regulate the organs responsible for nutrient provision to the developing embryo. Synthesis of vitellogenin by the liver is one example, and high levels of E2 during follicular development are indicative of E2 stimulation of vitellogenin synthesis in oviparous fish. Furthermore, estrogen receptors have been identified in the liver of the little skate, Leucoraja erinacea (=Raja erinacea) (Koob and Callard, 1999); and increasing levels of circulating vitellogenin were observed during the preovulatory rise of E2 in both L. erinacea (Perez and Callard, 1993) and S. canicula (Craik, 1978, 1979). Reduction in circulating levels of E2 just prior to ovulation have been reported in oviparous species and are likely associated with the antagonist effects of E2 with changes in plasma levels of T and P4 (Awruch et al., 2008b; Koob et al., 1986). Although in some oviparous species an increase in E2 levels were observed prior to ovulation, these increases are probably the result of continual recruitment of follicles Follicle development

Ovulation and encapsulation P4 Egg retention and oviposition E2 T

Follicular phase

Laying phase

Figure 7.9. Schematic representation of circulating plasma levels of 17b-estradiol (E2), testosterone (T), and progesterone (P4) in oviparous elasmobranchs during reproductive cycles. 17b-estradiol and T are higher during the follicular phase, while P4 concentrations rapidly and briefly peak just before ovulation. All hormone levels decrease, but not to basal titters, during the laying phase.

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that occurs in species that exhibit asynchronous gamete development, whereas there is often no change in plasma steroids following ovulation (Heupel et al., 1999; Rasmussen et al., 1999; Sumpter and Dodd, 1979). A decrease in circulating levels of E2, but maintenance of measurable levels during encapsulation and oviposition, is likely and indicates that estrogens could play a role during these stages. The physiological factors triggering the process of encapsulation remain poorly studied; however, hormones are likely involved in the induction of capsule formation (Gilmore et al., 1983; Koob and Callard, 1991). Oviducal gland development coincides with follicle development in many oviparous species (Awruch et al., 2008b; Heupel et al., 1999; Koob et al., 1986; Sulikowski et al., 2005a), together with the identification of an E2 receptor in the oviduct of L. erinacea (Reese and Callard, 1991) and E2 treatment causing oviducal gland enlargement and capsule protein synthesis in S. canicula (Dodd and Goddard, 1961), it is likely that E2 plays a role in oviducal development and subsequent egg encapsulation. Relaxin is a hormone responsible for regulating several reproductive events in vertebrates. Initially, relaxin appeared to assist maintenance of pregnancy by increasing uterine flexibility to accommodate the embryos and by inhibiting myometrial contractions to prevent premature parturition (Koob and Callard, 1982). However, relaxin is best known for its role in facilitating parturition later in development by increasing the extensibility of the cervix and pubis (Koob and Callard, 1982; Sorbera and Callard, 1995). In oviparous elasmobranchs relaxin has been detected in the ovary of L. erinacea (Bullesbach et al., 1987). Furthermore, treatment with porcine relaxin resulted in an increase of the extensibility of the cervix, increasing cross sectional area of the cervical lumen in the same species, and the response was potentiated by E2 (Callard et al., 1993). Thus, it is believed that relaxin and E2 may regulate cervical compliance to conform with the shape of the rigid egg case during egg retention and to prepare the cervix for oviposition (Callard and Koob, 1993; Koob and Callard, 1982). The role of circulating T in oviparous elasmobranch females remains unknown, and as no androgen receptors have been reported in the reproductive tract of any female, the suggested function remains speculative (Fig. 7.9). In general, changes in plasma concentration of T correlate with those of E2 in a precursor/product relationship (Callard et al., 2005a). However, plasma levels of T have been shown to increase during the latter stages of follicle maturation in several species of elasmobranch, remaining high after ovulation (Awruch et al., 2008b; Koob et al., 1986; Rasmussen et al., 1999; Sulikowski et al., 2004). This may suggest a down regulation of aromatase activity (regulating conversion of T to E2) leading to accumulation of T rather than its onward conversion to E2. It is possible that

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androgens may play a role in encapsulation and oviposition, but how and which specific function androgens may regulate is unknown. Alternatively, the maintenance of high androgen concentrations following ovulation may be the result of continual recruitment of maturing follicles in these species. Finally, maintenance of high levels of circulating androgens may be associated with the regulation of sperm storage by the oviducal gland in oviparous species. As E2 was correlated with oviducal gland function in oviparous species (Koob et al., 1986; Heupel et al., 1999; Sulikowski et al., 2004), and androgens play an important role in sperm maturation (Callard, 1991; Gelsleichter et al., 2002), it is possible that the oviducal gland’s ability to store sperm is regulated by a balance between E2 and T. Progesterone is a maturational steroid that regulates the later stages of follicular development by stimulating the resumption of meiosis in ovarian follicles that have completed vitellogenesis and suppressing the hepatic production of vitellogenin (Pankhurst, 2008) (Fig. 7.9). In oviparous species, plasma levels of P4 remained low during the follicular phase but showed a marked spike just prior to ovulation followed by a significant reduction at ovulation (Awruch et al., 2008b; Heupel et al., 1999; Koob et al., 1986; Rasmussen et al., 1999). The role of P4 as a maturational steroid in oviparous species is supported by the presence of P4 receptors in the liver of L. erinacea as well as the ability of P4 to block follicular development in this species (Paolucci and Callard, 1998; Perez and Callard, 1992, 1993). Progesterone also likely regulates egg retention and oviposition in oviparous species; however, the mechanisms of this action are unknown. The role of P4 in regulating egg retention and ovipositon is supported by studies that show P4 administration inducing early oviposition in L. erinacea (Koob and Callard, 1985). Furthermore, female smooth skates, Malacoraja senta, without carrying egg cases showed increased circulating levels of P4 compared to those with egg cases at any developmental stage (Kneebone et al., 2007). 5.1.2. Viviparous Similar to oviparous species, the major role of E2 in viviparous elasmobranchs is the regulation of organs and tissues that will provide nutrients to developing embryos (Callard et al., 2005a) (Fig. 7.10). Circulating E2 levels are higher during follicular development in all viviparous species studied to date (Awruch, 2013; Gelsleichter and Evans, 2012). Although hepatic E2 receptors have not yet been identified in any viviparous species, the stimulatory effect that E2 exerts on vitellogenin production has been demonstrated by in vitro studies in S. acanthias and the spotted ray, Torpedo marmorata (Ho et al., 1980; Prisco et al., 2008) supporting the role of E2 in controlling hepatic yolk synthesis. High levels of circulating E2 observed during ovulation have been linked with the role of

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Squalus acanthias Ovulation

CL

Follicle development

E2 P4

Ovulation

Parturition

Pregnancy 2 years

Sphyrna tiburo and dasyatis sabina Follicle development

Ovulation

CL

P4 E2

Ovulation

Pregnancy

Parturition

1 year Figure 7.10. Schematic representation of circulating plasma levels of 17b-estradiol (E2) and progesterone (P4) in viviparous elasmobranchs during reproductive cycles. In S. acanthias plasma E2 levels are higher during follicle development while P4 levels rise during ovulation and remain elevated during the first half of the 2-year pregnancy. In Sphyrna tiburo and Dasyatis sabina E2 is high during follicle development dropping during the first half of the pregnancy to rise again when both species shift from yolk-sac nourishment to maternal inputs. Circulating P4 concentrations are elevated at the time of ovulation remaining high during early pregnancy to decrease in late pregnancy. CL, corpora lutea. Adapted from Koob and Callard (1999), with permission.

this steroid in regulating protein secretion by the oviducal gland during encapsulation and/or controlling the passage of a fertilized egg into the uterus (Callard et al., 2005a; Snelson et al., 1997; Tricas et al., 2000; Tsang and Callard, 1987b). Further, a negative correlation between plasma E2 levels and fertility in female S. tiburo suggests a possible role for E2 in the preservation of stored sperm within the oviducal gland (Gelsleichter

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and Evans, 2012). After ovulation E2 levels decrease and remain low during the initial stages of pregnancy then increase at the end of the pregnancy remaining high during parturition in several viviparous species such as D. sabina, S. tiburo and S. acanthias (Koob and Callard, 1999; Manire et al., 1995; Snelson et al., 1997; Tricas et al., 2000). Coincidental with the increase in plasma E2 levels, there is a shift in embryonic nutrient supply from the yolk reserves to the maternal source, for example, in concordance with an increase in circulating E2 a shift to trophonemata secretions and placental formation were reported in D. sabina (Snelson et al., 1997) and S. tiburo (Manire et al., 1995, 2004). In addition, plasma increases in E2 during late pregnancy have been related to its association with relaxin and preparation of the cervix for parturition. Relaxin has been identified in the ovary of S. acanthias (Tsang and Callard, 1983), where it was found to increase the cross-sectional cervical lumen at late pregnancy and to prevent abortion of near-term embryos (Koob et al., 1984; Sorbera and Callard, 1995). Similar to oviparous species, the roles that androgens play in viviparous females modulating different reproductive events are basically unresolved. Androgen receptors have yet to be reported in female elasmobranch fish and circulating levels of androgen do not show a consistent trends between species where data are available. Although T appears to be the primary androgen, measurable levels of 11-ketosterone (11-KT), dihydrotestosterone (DHT), and 11-ketoandrostenedione (11-KA) have been provided in some species (Henningsen et al., 2008; Manire et al., 1995, 1999; Rasmussen and Gruber, 1990; Tricas et al., 2000). Similar to oviparous species, androgens likely serve as precursors for E2 synthesis as in several females endogenous concentrations of T, DHT, or 11-KT rise during follicular development and closely follow circulating levels of E2 (Callard et al., 2005a; Koob and Callard, 1999; Manire et al., 1995) (Fig. 7.10). In those species that exhibit embryonic diapause, androgens may play a role in the modulation of the diapause either by the maintenance and/or termination of the arrested development stages. In R. taylori T was elevated during most of the diapause, which suggests a role of this hormone in the maintenance and eventual termination of embryonic diapause in this species (Waltrick et al., 2014). Circulating T levels were reported to be elevated during the courting period in N. brevirostris, D. sabina, S. tiburo, and U. halleri (Manire et al., 1995; Mull et al., 2010; Rasmussen and Gruber, 1990, 1993; Tricas et al., 2000) suggesting a likely role for androgens in mediating courting and copulatory behavior. Furthermore, androgens have been associated with the maintenance of stored sperm by the oviducal gland, as S. tiburo showed an increase in 11-KA during mating and sperm storage (Manire et al., 1995).

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Although no P4 receptors have been isolated in any viviparous elasmobranch females to date, the role of P4 as a maturational steroid is supported by the antagonist effects between P4 and E2 displayed in several elasmobranch species (Manire et al., 1995; Mull et al., 2010; Tsang and Callard, 1987a) (Fig. 7.10). Progesterone was reported to inhibit vitellogenin synthesis when elevated circulating levels of P4 were coincident with low circulating levels of E2 and a lack of vitellogenin expression in the liver of T. marmorata (Prisco et al., 2008). Circulating P4 levels increase prior to ovulation and remain elevated during the initial pregnancy stages (Mull et al., 2010; Prisco et al., 2008; Tricas et al., 2000) suggesting a classic role for this hormone in the maintenance of pregnancy. The maintenance of P4 plasma concentrations at moderate levels just prior to ovulation during diapause in R. taylori (Waltrick et al., 2014), combined with a reduction in uterine contractions in the presence of P4 in S. acanthias (Sorbera and Callard, 1995), suggest a role for P4 in maintaining an appropriate uterine environment in gravid females. 5.2. Males In males, the testis is the primary site of steroid synthesis with a major production with most being produced by the Sertoli cells alongside contributions by the Leydig cell and possibly germ cells (Engel and Callard, 2005; Marina et al., 2002). Steroid secretions from the testis regulate spermatogenesis; development of the reproductive tract; development of secondary sex characteristics; and sexual behavior in vertebrates, but exactly how these steroids operate in elasmobranchs remain unclear. It is recognized that androgens have a distinct role in regulating the development of spermatozoa and the final stages of sperm maturation (the transformation of immotile round cells to free swimming sperm). Plasma T concentrations were reported to increase during the middle to late stages of spermatogenesis in several elasmobranch species (Awruch, 2013; Gelsleichter and Evans, 2012) and in vitro studies of different stages of spermatogenesis found higher T levels correlated with advanced spermatogenic stages (Sourdaine and Garnier, 1993; Sourdaine et al., 1990); however, the presence of androgen receptors localized within the testes of S. acanthias during the early stages of spermatogenesis suggests a regulatory role for androgens in the development of spermatogonia (earlier pre meiotic spermatogenesis stages) (Cuevas and Callard, 1992). Although T appears to be the primary androgen in male elasmobranch fish, other androgens such as DHT, 11-KT, and 11-KA have also been reported to play a role in spermatogenesis (Callard et al., 1989a; Engel and Callard, 2005; Garnier et al., 1999; Manire et al., 1999). However, lack of evidence and consistency in reported data has hampered our understanding

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of the potential role these androgens may play. For example, despite the reported presence of 11-KT in S. tiburo (Manire et al., 1999) and S. canicula (Garnier et al., 1999), this hormone does not appear to have a functional role in sexual maturation C. laticeps (Awruch et al., 2008b) and N. cepedianus (Awruch et al., 2014). In elasmobranch species with a seasonal sperm production a clear seasonality in androgen levels associated with spermatogenesis has been observed. For example, throughout the reproductive cycle of H. ocellatum, the Atlantic sharpnose shark, Rhizoprionodon terraenovae, and S. canicula, androgen concentrations were at the lowest levels when testes were predominantly at the very early stages of spermatogenesis. Circulating levels of androgens typically correlate positively with maturation of sperm (Garnier et al., 1999; Heupel et al., 1999; Hoffmayer et al., 2010); however, continuous sperm producers such as C. laticeps and A. radiata, do not have such a correlation as sperm matures (Awruch et al., 2009; Sulikowski et al., 2005a). Although to date no androgen receptors been identified outside of testicular tissue (Callard, 1991; Conrath and Musick, 2002) androgens likely play a role in the development of the claspers for copulation (Awruch et al., 2008b; Rasmussen and Murru, 1992; Sulikowski et al., 2005b) and sperm storage (Garnier et al., 1999; Gelsleichter et al., 2002; Heupel et al., 1999; Manire and Rasmussen, 1997). Estrogen concentrations are not normally quantified in elasmobranch males; however, several studies have confirmed that elasmobranch males do produce substantial quantities of E2 (Awruch, 2013; Hoffmayer et al., 2010; Tricas et al., 2000) and E2 receptors have been identified in elasmobranch testes (Callard et al., 1985; Cuevas and Callard, 1992). Estradiol has been associated with the regulation of the early phases of sperm development as elevated E2 levels were found during early to mid-stages of spermatogenesis, and estrogen receptors (similar to androgen receptors) were found to be highest in the testicular regions of premeiotic stages of spermatogenesis (Callard, 1991; Cuevas and Callard, 1992; Manire and Rasmussen, 1997; Sulikowski et al., 2004; Tricas et al., 2000). Thus, variations of E2 throughout the reproductive cycle of male elasmobranch fish have been associated with testicular development. However, it remains unclear whether E2 plays a role in modulating spermatogenesis in elasmobranch males, and if any function is representative in plasma levels. Plasma E2 levels have also been reported to be very low with no clear variation within the male reproductive events in several species (Awruch et al., 2008b; Garnier et al., 1999). However, Gelsleichter and Evans (2012) suggested that plasma levels of E2 might not reflect its function in the testes if the effect of this hormone was mainly paracrine (cell to cell communication). Indeed in male S. canicula maximum circulating levels of E2 were reported to be 10-fold lower than maximum testicular levels (Garnier et al., 1999).

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Similar to estrogens, P4 levels are not normally quantified in elasmobranch males, nonetheless, several species are known to have measureable circulating levels of this reproductive hormone (Awruch et al., 2008b; Garnier et al., 1999; Manire and Rasmussen, 1997; Tricas et al., 2000). However, patterns of P4 production throughout the reproductive cycle are very unclear. While in some species such as C. laticeps and S. canicula there were no changes associated with the different stages of spermatogenesis (Awruch et al., 2008b; Garnier et al., 1999), in others such as S. tiburo and N. brevirostris, plasma P4 levels increased with testicular development (Manire and Rasmussen, 1997; Rasmussen and Gruber, 1993). Progesterone was also associated with the final stages of postmeiotic spermatogenesis (spermiogenesis and spermiation) as the presence of P4 receptors was highest during these stages (Cuevas and Callard, 1992). Additionally, several authors have suggested that the observed patterns in circulating levels of P4 is a function of the steroid acting as a precursor for the synthesis of downstream androgens and possibly estrogens (Callard, 1991; Manire and Rasmussen, 1997; Simpson et al., 1963, 1964). However, circulating levels of P4 were reported to peak independently of T in S. canicula and D. sabina (Garnier et al., 1999; Gelsleichter and Evans, 2012; Snelson et al., 1997). As in females, relaxin has also been identified in male elasmobranch fish (Bu¨llesbach et al., 1997), and was isolated from the testes in S. acanthias (Steinetz et al., 1998). However, relaxin has always been considered a “female” hormone, and as a result the function and the mechanisms of relaxin in males are poorly investigated. Elevated levels of relaxin were reported during copulation and late spermatogenesis in S. tiburo, which may indicate a role for relaxin in regulating sperm quality and the ability of males to effectively store semen prior to the mating period and/or transfer semen during copulation (Gelsleichter et al., 2002). However, a relaxin-like compound (Raylaxin) identified in D. sabina did not increase sperm activity and quality in this species and relaxin concentrations were reported to be 1000 times higher in the semen of S. tiburo than in the circulation (Gelsleichter and Evans, 2012), which suggests that the hormone may play a more important role in the female reproductive tract following copulation and successful implantation of sperm (Bu¨llesbach et al., 1997; Gelsleichter and Evans, 2012).

5.3. Serotonin, Corticosteroids, Thyroid Hormones, and Calcitonin There are several hormones that have been linked with reproduction in both female and male elasmobranchs, and although few studies have been conducted and conclusions remain speculative, potential roles in reproduction are worth mentioning.

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5.3.1. Serotonin Serotonin or 5-hydroxytryptamine (5-HT) is a neurotransmitter that is involved in the regulation of a wide variety of physiological functions, such as sensory and motor functions and secretion of hormones including reproductive hormones (Carrera et al., 2008; Ayala, 2009). The presence of serotonin-like binding has been reported in the siphon sacs of sharks (Mann, 1960). These are paired ventral organs associated with the claspers, whose function is to eject sperm into the female’s reproductive tract (Hamlett, 1999). Circulating concentrations of 5-HT were reported to be 200 times higher in mature compared to immature S. acanthias males (Mann, 1960). Furthermore, in vitro administration of siphon sac secretions of serotonin (0.2–04 mg) in S. acanthias caused uterine contractions (Mann and Prosser, 1963). The authors suggested that the presence of such a high concentration of serotonin in the semen of S. acanthias could indicate a functional role for serotonin in reproduction, either influencing ejaculation or uterine contractions to stimulate transfer of sperm in the reproductive tract and thus aid fertilization (Mann, 1960; Mann and Prosser, 1963). 5.3.2. Corticosteroids The detection and quantification of corticosterone has been mainly used to assess stress in elasmobranchs; yet, this hormone may also play a role in the reproductive biology of this group of fish. Sex differences in corticosterone concentrations have been reported in T. obesus (Rasmussen and Crow, 1993), S. tiburo (Manire et al., 2007), and D. sabina (Manire et al., 2007; Snelson et al., 1997). Differences in plasma concentrations of corticosterone associated with maturity were also reported for D. sabina and S. tiburo males, where corticosterone levels increased significantly during the later stages of spermatogenesis and mating (Manire et al., 2007). Seasonal variations of corticosterone levels were also found in elasmobranch females but are inconsistent. Higher corticosterone concentrations were associated with late pregnancy and post-partum stages in D. sabina, but with follicle development, mating, and early pregnancy in S. tiburo (Manire et al., 2007). Similar to other vertebrates (Michael et al., 2003; Romero, 2002), it is likely that seasonal corticosterone patterns are related to reproductive activity in elasmobranchs; however, additional studies are necessary for a complete understanding of the role that corticosterone may play in regulating reproduction. 5.3.3. Thyroid Hormones Thyroid hormones (THs) triiodothyronine (T3), and thyroxine (T4) are well-known regulators of development and metabolism in vertebrates.

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There is increasing evidence that THs are also involved in gonadal differentiation and reproductive function through the HPG axis in vertebrates. THs and sex steroid hormone axes interact in vertebrates to regulate developmental and adult endocrine systems (Duarte-Guterman et al., 2014). In elasmobranchs THs have been associated with reproductive events in several species (Crow et al., 1999; McComb et al., 2005; Volkoff et al., 1999), although TH did not show differences associated with sexual stages in male D. sabina, TH was found to be significantly higher during the ovulation and early gestation in female D. sabina and S. tiburo (McComb et al., 2005; Volkoff et al., 1999). Furthermore, TH measured in maternal yolk steadily increased from pre-ovulation to post-ovulation and peaked during the pregnancy stage (McComb et al., 2005). Although TH function in elasmobranch males remains completely unknown, it is likely that TH plays a crucial embryonic developmental role in elasmobranchs as described in other vertebrates (Duarte-Guterman et al., 2014; Hulbert, 2000). Interestingly, levels of TH in the maternal yolk of S. tiburo were lower in gravid females from populations inhabiting lower water temperatures and exhibiting comparatively lower metabolic rates, compared to individuals of the same species occupying high temperature waters and displaying higher development metabolic rates (McComb et al., 2005). 5.3.4. Calcitonin A relationship between calcitonin and gonadal steroid production has been observed in the majority of vertebrate groups (Yamauchi et al., 1978; Krzysik-Walker et al., 2007) and an association has been made between calcitonin and pregnancy, follicle development and embryonic development (Bjornsson et al., 1986; Krzysik-Walker et al., 2007). In elasmobranchs calcitonin is produced by the ultimobranchial gland, a paired organ situated in the musculature between the pharynx and pericardial cavity (Suzuki et al., 1995). Estradiol regulates the synthesis of calcitonin in D. sabina (Suzuki et al., 1995), which together with the presence of E2 receptors in the ultimobranchial gland of the same species may support the hypothesis that calcitonin is involved in regulation of reproduction (Yamamoto et al., 1996). Calcitonin may also regulate aspects of embryo yolk nutrition during early gestation, as a peak in maternal serum calcitonin levels were found throughout the yolk-dependent stage during pregnancy in the placentatrophic S. tiburo (Nichols et al., 2003). Furthermore, calcitonin concentrations were also found in the gastrointestinal system of developing embryos during the yolk-dependent stages but not during the late placental stages of embryo development (Nichols et al., 2003).

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6. THE FUTURE Elasmobranchs have remained virtually unchanged since their divergence from jawless fishes over 400 million years ago to evolve diverse, highly complex mechanisms for assuring reproductive success. In the past 20 years significant advances have been made to understand elasmobranch life history strategies, particularly their reproductive tactics. However, while a greater knowledge on their reproductive modes has been gained, substantial gaps in understanding their reproductive cycles and the role of the reproductive steroids remain. In recent years studies have increasingly adopted a multifaceted research strategy, integrating reproductive morphology and endocrinology. Results from these studies show high correlation between changes in reproductive tracts and gonadal steroids highlighting the role of hormones in addressing reproductive parameters (Awruch et al., 2008a; Awruch et al., 2014; Mull et al., 2010; Williams et al., 2013). Nonetheless, important differences remain, and in many cases contradictory patterns of plasma steroids in both female and male elasmobranchs are reported. Future studies need to combine in vitro and in vivo experiments correlating morphological changes of the reproductive tract with gonadal steroids and gametogenesis to understand gonadal synthesis. Furthermore, analyses of whole genomes have become a powerful tool for understanding the function of physiological mechanism (Gwee et al., 2009; Nelson and Habibi, 2013; Nock et al., 2011). It is likely that in the future, genomic studies will also become a powerful tool to better comprehend the reproductive mechanisms in elasmobranchs. Finally, increasing studies are using reproductive endocrinology toward the conservation of threatened and endangered species – conservation endocrinology (Awruch et al., 2014; Kersey and Dehnhard, 2014; Tubbs et al., 2014). Fundamental to the conservation and management of any species is an understanding of their reproduction, thus, knowledge of reproductive status among individuals has been used to assist in the management of target species. In this regard noninvasive reproductive hormone monitoring has become a preferred approach to obtain reproductive information in a multitude of species, including mammals, birds, and amphibians (Kersey and Dehnhard, 2014; Tubbs et al., 2014), and is also becoming a popular approach for elasmobranchs (Awruch et al., 2008a, 2014; Prohaska et al., 2013).

ACKNOWLEDGMENT The author thank the two anonymous reviewers for invaluable comments. The Winnifred Violet Scott Foundation and Save our Seas Foundation provided the funding through several grants to Awruch, C. A.

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8 FIELD STUDIES OF ELASMOBRANCH PHYSIOLOGY DIEGO BERNAL CHRISTOPHER G. LOWE

1. Introduction 1.1. Early Field Physiology 1.2. Importance of Linking Laboratory and Field Work 1.3. Biotelemetry and Biologging 2. Thermal Physiology 2.1. Thermal Biology in the Lab 2.2. Thermal Biology in the Field 2.3. Behavioral Thermoregulation 2.4. Thermal Refuging 2.5. Physiological Thermoregulation 2.6. Thermal Effect on Metabolic Rate 3. Swimming Kinematics and Energetics 3.1. Swimming 3.2. Heart Rate 3.3. Feeding and Digestion 4. A Case Field Study: Thresher Sharks 4.1. The Role of the Caudal Fin 4.2. RM Morphology 4.3. RM Uncoupling and Swimming Mode 4.4. RM Endothermy and Thermal Distributions 5. Future Directions in Field Physiology

This chapter reviews how field work with elasmobranchs offers an important complement to laboratory studies, and highlights examples of when going to the field is the only, and most often the best, option to work with species that are large, elusive, or cannot be held in captivity. We begin by offering a brief summary of the pioneering work in shark field physiology (ca. 1960), the technologies used to track and log physiological data in the field, and how field work can expand and enhance the knowledge gained in the laboratory. The chapter then proceeds to offer a more detailed account of how field and laboratory work have offered a better understanding of the 311 Physiology of Elasmobranch Fishes: Structure and Interaction with Environment: Volume 34A FISH PHYSIOLOGY

Copyright r 2016 Elsevier Inc. All rights reserved DOI: http://dx.doi.org/10.1016/B978-0-12-801289-5.00008-0

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thermal biology of sharks and rays, and provides examples of work showing the use of behavior and some of the physiological mechanisms that elasmobranchs can utilize to alter the rates of key physiological parameters. Because most sharks and rays are highly mobile, we then address how field work has been used to study their swimming kinematics, bioenergetics, and their feeding ecology. This is followed by a case study on how field work has given an unprecedented glimpse into the biology, ecology, and physiology of the thresher sharks, a unique group of sharks for which most prior information was obtained from dead specimens that were captured incidentally by fishermen. While the logistical difficulties surrounding field work with sharks and rays has often lead to scenarios where only a few specimens were studied, the development of new and lower cost technologies and the use of better techniques for handling sharks in the wild will allow the recording of more physiological and environmental variables and allow access to a higher number of species, even in places thought to be inaccessible in the past.

1. INTRODUCTION Most fish physiologists work under conditions that force them to become perpetual on-the-site troubleshooters, as the vast majority of the technology used to collect in vivo data has been borrowed from a more terrestrial setting (usually modified to not only withstand exposure to water but be semiportable too). These logistical difficulties are exacerbated when working with marine fishes and grow exponentially when attempting to study large, hard-to-handle species, particularly those that have large jaws filled with sharp teeth. This chapter presents an overview of the importance of working in the field, gives examples of how field work complements laboratory work, and reiterates how recent technological advances are beginning to elucidate the unique physiology of sharks in the wild. While these studies may lack controls and significant replication, they provide a more holistic view of how elasmobranchs respond physiologically and behaviorally to changing abiotic and biotic factors within their environment. The development of new fieldapplied technologies and techniques are allowing for a better understanding of the integrated roles of physiology and behavior in groups of animals not amenable to controlled captive experimentation. Growing knowledge of how individuals respond to changing environmental conditions offer extensive modeling opportunities that will prove useful in the study of the physiological adaptations of sharks.

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1.1. Early Field Physiology Historically, studying the physiology of marine fishes has posed numerous technical and logistical challenges, particularly when attempting to work on large and highly mobile species (e.g., sharks) that cannot be kept in captivity or a laboratory setting. Early attempts to study sharks in the field were limited by the ability to secure the funding needed for ship time; the availability and durability of the research vessels; the ability of scientists to find and collect specimens; and the perpetual battle with corrosion acting on the rudimentary electronic equipment used out at sea. The early pioneers of shark field physiology, like Frank Carey and John Kanwisher, designed and built their own multichannel acoustic transmitters to record physiological data from free-swimming wild sharks as they moved through thermally dynamic open ocean conditions (Carey et al., 1982; Carey and Scharold, 1990). In parallel, field work was being conducted by Don Nelson and colleagues on physiological links between sensory biology of sharks and how, for example, sound perception may affect heart function (e.g., Nelson, 1967). During the next several decades, work on captive sharks began to elucidate their bioenergetics and describe their swimming performance (e.g., Brett and Blackburn, 1978; Weihs et al., 1981) with numerous high-risk attempts to start taking the laboratory out to sea in order to access sharks that could not be held in captivity (e.g., Graham et al., 1990). While during the last 50 years, working with sharks in the field may appear to have become routine, we can reiterate to the reader that this remains anything but routine. All of the logistical and technical challenges faced by the early field pioneers still exist today, and while the advancements in electronics have only decreased the footprint needed to take the physiology laboratory to the field and the development of new technologies, or the adapting (often jerry-rigging) of existing ones, now allow for the collection or transmission of key physiological data collected from specimens in the wild, field physiologist still live with the reality of going to sea, face the challenge of finding their specimens, and hope to delay the inevitable loss of their field equipment. Nonetheless, the ability to capture large sharks in the field, even when working from a small boat, and the opportunity to follow them and quantify important physiological parameters in situ (e.g., blood gases, electrolytes, metabolites), or to rapidly transport live tissues to the laboratory, have provided new insights into the physiology of elasmobranchs (e.g., Bernal et al., 2005; Donley et al., 2012; Marshall et al., 2012). However, these types of studies provide but a short-term “snap-shot” of the physiological status and capacities of sharks, and the evolution of new sensor technology (e.g., electrocardiograms, gastric pH, inertial measurement units, dissolved oxygen, temperature, depth), coupled with

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miniaturized dataloggers and telemetry transmitters and innovative ideas for taking the laboratory to the field will provide new insights into the physiology of free-swimming elasmobranchs. 1.2. Importance of Linking Laboratory and Field Work The study of free-swimming sharks and rays in their natural environment is plagued with logistical difficulties (Bushnell et al., 1989; Parsons and Carlson, 1998). For this reason, the majority of work on sharks and rays has relied on the use of individuals under captive conditions in either public or research aquaria. During the last decade several public aquaria have succeeded remarkably in keeping new species, including several large pelagics (e.g., manta rays, Mobula sp.; whale sharks, Rhincodon typus; white sharks, Carcharodon carcharias) for extended periods of time (months to years) in large display tanks allowing the opportunity to study them for more than the brief periods (minutes), typical of underwater observations in the field. While the benefits of studying the biology and physiology of sharks in captive settings can allow for control and manipulation of certain environmental conditions, more commonly, larger animals are held in large tanks or semi-natural systems (ponds) that prohibit experimental manipulations, and the principal objective (i.e., public observation) and associated high cost of their captivity precludes their availability for invasive physiological experiments. In some cases, sharks and rays have been placed in experimental chambers (e.g., small circular tanks, shuttle boxes, swimtunnel respirometers) where key environmental (e.g., ambient temperature, dissolved oxygen, light levels) and biological (e.g., swimming speed) parameters can be controlled and manipulated (see Chapters 3 and 6, and Ballantyne, 2015). Unfortunately, the use of experimental chambers is limited by their location, their size, and their capacity to control environmental parameters. For these reasons, not surprisingly, there has been marked progress in the understanding of the physiology and swimming kinematics of relatively small species or juvenile stages of larger species (generally individuals o1 m in length) that do well in captivity (e.g., sandbar shark, Carcharhinus plumbeus; leopard shark, Triakis semifasciata; lemon shark, Negaprion brevirostris; spiny dogfish, Squalus acanthias) with opportunistic work being done in the short-term (days to weeks) on more elusive (e.g., juvenile scalloped hammerhead, Sphyrna lewini) or larger pelagic species (e.g., juvenile mako, Isurus oxyrinchus; white shark, C. carcharias) (Carlson et al., 2004; Dowd et al., 2006; Bernal et al., 2012; Ezcurra et al., 2012). This lack of proper acclimation may lead to a biased and inaccurate assessment of their physiological capacities (e.g., Steffensen, 1989), as, for example, studies on the metabolic rates of other hard-to-study

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fishes (e.g., tuna) show that the energetics demands decrease with the duration of acclimation (Dewar and Graham, 1994; Blank et al., 2007). Thus, there remains a meager understanding of how longer term acclimatization may affect the physiological capacities of sharks, in particular large, ram-ventilating, actively swimming species. Nonetheless, several studies have attempted to use laboratory-based measurements as a mechanism to extrapolate the energetic and kinematic performance of freeswimming individuals that, to date, are not routinely or cannot be kept in captivity (Graham et al., 1990; Lowe et al., 1998; Lowe and Goldman, 2001; Sepulveda et al., 2007b). Thus, while controlled laboratory-based studies have increased our understanding of shark physiology, it remains unknown if these estimates are representative of their free-swimming performance in the field. Our ability to study large and highly mobile elasmobranchs under controlled laboratory conditions remains limited; therefore, making field work the only practical approach, requiring that either the laboratory goes to the field or the implementation or development of new technologies that allow the collection of physiological data for free-swimming individuals. 1.3. Biotelemetry and Biologging While the last several decades have witnessed the rapid evolution and the wide-spread use of archival tagging, satellite tagging, and both active (actively following the tagged shark) and passive (using an array of stationary acoustic receivers) acoustic telemetry on captive and freeswimming sharks (Nelson, 1990; Lowe and Goldman, 2001; Lowe and Bray, 2006), there remains a need for new studies that bridge the gap between laboratory and field estimates of physiological performance. The use of biotelemetry to assess how key physiological parameters (e.g., swimming speed, tailbeat frequency (TBF), body temperature, heart rate) affect swimming energetics (i.e., metabolic rate) has relied mostly on using laboratory-based respirometry to determine the degree to which particular physiological parameters can be used to estimate metabolic rate for freeswimming individuals in the field (Carey et al., 1982; Scharold et al., 1988; Scharold and Gruber, 1991; Lowe et al., 1998; Parsons and Carlson, 1998; Sundstro¨m and Gruber, 1998; Lowe, 2002). For example, the field metabolic rates of free-swimming juvenile lemon sharks, scalloped hammerhead sharks, and bonnethead sharks (Sphyrna tiburo) have been estimated by coupling of laboratory-based measurements of oxygen consumption with data from either speed-sensing transmitters (Parsons and Carlson, 1998; Sundstro¨m and Gruber, 1998) or custom made tailbeat transmitters (Lowe et al., 1998; Lowe, 2002). However, it must be stressed that the use of biotelemetry data as the foundation for the estimation of the

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field-performance in free-swimming sharks comes with inherent limitations. For example, Lowe (2002) argued that using TBF alone as a measure of swimming activity may be too simplistic, as it does not represent acceleration or deceleration, and cannot account for any alteration of tailbeat amplitude, which when taken together, are needed to increase the accuracy of estimated field metabolic rates. Recent work has begun to combine the benefits of biotelemetry with biologging, by, for example, using archival dataloggers to record high resolution three dimensional body accelerations, ambient temperature, depth, and even video cameras, that are coupled with acoustic transmitters to provide a geo-referenced, three-dimensional, oceanographic snapshot of the animal and the environment (Table 8.1). More recently, there has been a push to develop and deploy new autonomous underwater vehicles (AUVs) that can actively track tagged sharks without any shipboard commands and simultaneously document numerous environmental conditions in the waters surrounding the tagged animal (Forney et al., 2012; Clark et al., 2013; Lowe, unpublished data; Xydes et al., 2013). While these approaches are still in their infancies, they will most certainly yield a more comprehensive measure of how sharks and other elasmobranch fishes respond physiologically and behaviorally to their surroundings.

2. THERMAL PHYSIOLOGY Ambient water temperature is a key abiotic variable that significantly affects the physiology of sharks (Carlson et al., 2004; Wallman and Bennett, 2006; Bernal et al., 2012; Brill and Lai, 2015; Morrison et al., 2015; Ballantyne, 2015). In general, sharks do not maintain a body temperature that is independent from that of the surrounding environment, resulting in body temperature that mirrors that of ambient conditions (i.e., poikilothermy). Therefore, ambient water temperature markedly affects the metabolic demands of sharks, where higher temperatures result in higher energetic expenditures and faster rates of important physiological processes (e.g., enzyme kinetics, protein function, metabolism) (Reynolds and Casterlin, 1980; Clarke and Fraser, 2004). However, a large range of body sizes, their diverse habitat use patterns, and a high mobility have made quantifying the effects of environmental conditions on the physiological state of sharks extremely challenging. During the last several decades, the development of new fish tracking and environmental monitoring technologies (e.g., telemetry and dataloggers) have resulted in a steady surge of field studies that attempt to quantify how

Table 8.1 Types of sensor equipped acoustic and satellite transmitters and biologgers used to study shark behavior and physiology Type

Sensors available

Manufacturers

Study species examples

Study examples

Acoustic telemetry Active tracking – continuous pulse transmitters

D T TBF U Tm Ts GpH HR

Vemco-Amirix Sonotronics Custom-made

Blue sharks (T, D) Lemon sharks (T, U, HR) Mako sharks (T, D, Ts) Blacktip reef sharks (T, D, GpH) Hammerhead sharks (TBF) White sharks (T, D, Tm, Ts)

Carey and Scharold (1990) DiGirolamo et al. (2012), Scharold and Gruber (1991) Holts and Bedford (1993), Sepulveda et al. (2004) Papastamatiou et al. (2007b) Lowe (2001) Goldman (1997), Carey et al. (1982)

Acoustic telemetry Passive tracking – psuedo-random pulse interval transmitters

ID code D T

Vemco-Amirix

Gray reef sharks (ID) Whitetip reef sharks (ID) Sicklefin lemon sharks (ID) Blacktip reef sharks (ID, T)

Speed et al. (2012)

Acoustic telemetry Archiving –transponder transmitters

ID code D T Other tag IDs

Vemco-Amirix

Leopard sharks (ID, T, D)

Hight and Lowe (2007)

(Continued )

Table 8.1 (Continued ) Type

Sensors available

Manufacturers

Study species examples

Study examples

Satellite telemetry Pop-off archival transmitters

D T L

Wildlife Computers Microwave Telemetry

Blue sharks Salmon sharks Bigeye thresher sharks White sharks Whale sharks Basking sharks

Campana et al. (2011), Steven et al. (2010) Weng et al. (2005) Weng and Block (2004) Del Raye et al. (2013) Thums et al. (2013) Skomal et al. (2009)

Biologgers Required retrieval

A D T V

Little Leonardo Daily-dairy Vemco-Amirix Lotek, Onset

Tiger sharks (A, D, T, V) Whale sharks (A, D, T) Nurse sharks (A) Common thresher shark (D, T)

Nakamura et al. (2011) Gleiss et al. (2011) Whitney et al. (2010) Cartamil et al. (2011)

Abbreviations: ID, ID code; D, Depth; T, Temperature; TBF, Tailbeat frequency; U, Swimming speed; Tm, Muscle temperature (thermistor probe); Ts, Stomach temperature; GpH, Gastric pH; HR, Heart rate; L, Light; A, 3D acceleration; V, Video.

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some elasmobranchs move in relation to various environmental conditions (e.g., temperature, salinity, dissolved oxygen, and pH) (Schlaff et al., 2014). Not unlike many teleost fishes, actively swimming sharks are known to occupy and utilize a wide range of habitats over the short term (daily use of the water column) and long term (seasonal migrations), which ultimately subjects them to large, and sometimes rapid and repeated, changes in environmental conditions. Out of the numerous environmental variables that can affect the physiology of fish (sharks in particular), water temperature has always been considered to be the most important as it most likely influences their horizontal and vertical distributions, behaviors, short-term habitat use, dispersal, and metabolism (Carey et al., 1971; Magnuson et al., 1979; Neill, 1979). However, the lack of controlled experimental laboratory-based studies have made it difficult to disentangle the effects of temperature from that of other biotic and abiotic factors that influence physiology and behavior. 2.1. Thermal Biology in the Lab Most thermal energetic studies on sharks have been conducted in ectothermic species in captivity and hence have been limited to either a narrow range of ambient temperatures or changes that do not mirror the complex thermal environments (vertical and horizontal thermal fronts) and the rapid and repeated changes in temperature that sharks encounter in the field. However, laboratory work does show that the energetic demands of sharks are directly correlated with temperature as, for example, metabolic rates increase two or three times for every 101C elevation in ambient temperature (temperature coefficient, Q10, of 2 or 3; Schmidt-Nielsen, 1997) (e.g., Ballantyne, 2015), but vary in magnitude based on the duration of acclimation. For example, sharks that have been seasonally acclimated (months) have a lower Q10 (1.3 in scalloped hammerhead from 21–291C; 2.3 in bonnetheads from 19–281C; Carlson and Parsons, 1999; Lowe, 2001) when compared to those exposed to more rapid temperature changes (hours to days) (Q10 values of 2.5 in leopard sharks from 10–261C; 2.9 in sandbar sharks from 18–281C; Miklos et al., 2003; Dowd et al., 2006) (Table 8.2). While the physiological mechanisms leading to such a wide degree of metabolic temperature sensitivity remain poorly understood, the capacity to seasonally migrate and occupy differing thermal environments (e.g., vertical movements, coastal vs. offshore) may greatly influence their ecophysiology. Thus, ambient temperature will play a major role in the energetic demands of sharks that undergo diurnal or seasonal changes in thermal habitat as a result of their horizontal (i.e., geographic) or vertical (i.e., depth) movement patterns. There are, however, several shark species that are capable of

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Table 8.2 The effects of temperature (Q10) on metabolic rate or muscle contraction in sharks and rays Species

Temperature range (1C)

Method Mean Q10

Study

Atlantic stingray (Daysatis sabina) Cownose ray (Rhinoptera bonasus) Bat ray (Myliobatis californica) Bull ray (Myliobatis aquila) Leopard sharks (Triakis semifasciata) Spiny dogfish (Squalus acanthias) White spotted bamboo shark (Chiloscyllium plagiosum) Bonnethead shark (Sphyrna tiburo) Lesser guitarfish (Rhinobatos annulatus) Small-spotted catshark (Scyliorhinus canicula) Sandbar shark (Carcharhinus plumbeus) Scalloped hammerhead shark (Sphryna lewini) Gray carpet shark (Chiloscyllium punctatum) Epaulette shark (Hemiscyllium ocellatum) Common thresher shark (Alopias vulpinus) Salmon shark (Lamna ditropis) Mako shark (Isurus oxyrinchus)

21–31

OC

2.10

19–28

OC

2.33

DiSanto and Bennett (2011a,b) Neer et al. (2006)

14–20

OC

6.81

Hopkins and Cech (1994)

10–25 10–26 15–25 7–18

OC OC MC OC

1.87 2.51 3.1 2.2

DuPreez et al. (1988) Miklos et al. (2003) Donley et al. (2007) Brett and Blackburn (1978)?

20–28

OC

2.08

DiSanto and Bennett (2011a,b)

20–30

OC

2.34

Carlson and Parsons (1999)

10–25

OC

2.27

DuPreez et al. (1988)

7–17

OC

2.61

Butler and Taylor (1975)

18–28

OC

3.24

Dowd et al. (2006)

21–29

OC

1.34

Lowe (2001)

23–25

OC

1.5

Chapman et al. (2011)

23–25

OC

1.3

Chapman et al. (2011)

8–24

MC

1.9–2.5

Donley et al. (2012)

10–26

MC

2.0–3.7

Bernal et al. (2005)

15–28

MC

2.9

Donley et al. (2007)

Abbreviations: OC, oxygen consumption; MC, muscle contraction.

maintaining their body temperature significantly above ambient (regional endothermy), which may result in a different thermal effect on their energetics (see Section 2.5). Therefore, the use of inter-species corrections when addressing the thermal effects on energetic metabolism between sharks that have widely different temperature preferences or physiological

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adaptations for regional endothermy should be used with caution if attempting to determine species-specific temperature tolerances, thermal limits, and the behavioral and physiological capacity for thermoregulation (Clarke, 1991). 2.2. Thermal Biology in the Field Studies on the movement patterns of free-swimming sharks are both labor intensive and very costly. During the last several decades the technological advancements of passive and active acoustic, archival, and satellite tags have led to a dramatic increase in the understanding of the spatio-temporal movements of sharks (Nelson, 1978, 1990; Weng et al., 2005; Schlaff et al., 2014). These works have offered new supporting evidence on the thermal distributions of sharks that were originally derived from fishery-dependent methods (e.g., commercial catches, tag, and recapture) but have also disclosed movement patterns that were, until recently, unknown (Nakano et al., 2003; Weng and Block, 2004; Bonfil et al., 2005; Weng et al., 2005; Skomal et al., 2009). While the species-specific movement patterns of sharks can be documented by examining their latitudinal and vertical distributions, it is important to note that there are marked diurnal differences in the thermal (vertical) distribution of many species. In general, during the nighttime hours sharks, particularly pelagic species, remain within the upper wellmixed layer of the ocean, and thus the vertical distribution of many species may overlap as they most likely associate with the distribution of their prey species comprising the deep-sound scattering layer (e.g., Carey and Robison, 1981; Holland et al., 1990; Schaefer and Fuller, 2002; Musyl et al., 2003). By contrast, during the daylight hours some sharks show significant vertical movements reaching depths that are at or below the thermocline. It is at this time that some pelagic sharks reveal their physiological specializations or tolerance to reduced temperatures accompanying increases in depth (Bernal et al., 2009). Measuring the thermal conditions that a shark may experience has been achieved by actively following an individual that has been tagged with an external temperature-sensing acoustic transmitter. Simultaneous sampling of the water depth and temperature during these tracks can provide a characterization of the environmental thermal stratification and where the individual spends time relative to those conditions (Carey et al., 1982). Alternatively, deploying and recovering archival tags that have been attached either externally or in the coelomic cavity can provide a detailed log of the thermal environments spanned by the individual over longer durations of time (e.g., weeks, months, years); however, because the

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individual is not being actively tracked no information is available on relevant oceanographic features (e.g., thermal water stratification) in the areas close to the shark and there are no geo-location estimates that can be used to determine any larger-scale encounters with different water masses or significant bathymetric features. By contrast, the simultaneous use of both external and internal temperature transmitters can not only provide valuable physiological data that will allow the quantification of whole body thermal rate coefficients (i.e., how quickly the individual warms up or cools down as it moves, vertically or horizontally, through thermally stratified environments) and give insight into the potential role that thermal inertia may play in larger sharks (Carey et al., 1981, 1982; Goldman, 1997), but will offer a larger scale view of the thermal preferences and tolerances of free swimming sharks and how these may be affected by the surrounding environment.

2.3. Behavioral Thermoregulation There have been a growing number of studies on ectothermic sharks and rays that document the spatial and temporal changes in distribution patterns across a population or use predictable changes in the behaviors of individuals in response to water temperature to suggest these elasmobranchs are using behavioral thermoregulation. Field data show that both sharks and rays can seasonally aggregate in particular locations, typically shallow areas, where water is known to be warmer than the normal habitat used. For example, adult female gray reef sharks (Carcharhinus amblyrhynchos) were observed aggregating in shallow, warm lagoon habitats in a tropical atoll between March and May, when they would otherwise be sighted along cooler reef edges and channels (Economakis and Lobel, 1998). Similarly, adult female leopard sharks in southern California have been observed to also aggregate in shallow coastal habitats during summer months, presumably because those habitats were warmer than adjacent waters (Manley, 1995). Although male and female round stingrays (Urobatis halleri) have been found to seasonally aggregate in shallow coastal or estuarine habitats during spring months for mating (Babel, 1966), only mature females remain in the warm and shallow estuarine habitats throughout the summer months (Mull et al., 2010; Jirik and Lowe, 2012). While possible that these female aggregations form to serve some social function, it has been postulated that this behavior (maternal thermophily) may provide some reproductive benefit as the aggregations were specifically associated with warmer habitats and generally only mature females were observed within the aggregations (Economakis and Lobel, 1998; Hight and Lowe, 2007; Jirik and Lowe, 2012).

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Characterization and confirmation of behavioral thermoregulation for individual sharks in the field has come from studying their behavior in relation to changing ambient temperatures. Most frequently, these sharks are tracked using acoustic telemetry while simultaneously monitoring environmental parameters and quantifying changes in behavior (e.g., movement to or away from changing thermal conditions) and changes in body core temperature in relation to ambient conditions. For example, acoustic tracking of several coastal sharks (gray reef, whitetip reef (Triaenodon obesus), sicklefin lemon (Negaprion acutidens), and blacktip reef sharks (Carcharhinus melanopterus)) in Coral Bay, Western Australia, showed that while all species had a strong seasonal correlation between water temperature and the likelihood of detection at certain locations, for some species (i.e., blacktip reef sharks) there was a distinct diel pattern of habitat use with females aggregating in shallow beach habitats during daytime hours followed by departures from that area after dark (Speed et al., 2012). The simultaneous deployment of numerous ambient temperature dataloggers at different habitats within the bay showed that the daytime habitats for aggregating blacktip sharks had the greatest diel thermal fluctuations and were the warmest. Additional passive telemetry tracking of female blacktip sharks internally fitted with temperature transmitters showed that during the day there was a small but elevated body core temperature (approximately 11C above ambient), with most sharks dispersing from the site after dark when water temperatures began to fall. While Speed et al. (2012) contend that these data support behavioral thermoregulation as sharks moved between thermally heterogeneous habitats and maintained a body core slightly above ambient temperature during the day, both the thermal benefit to reproduction from this behavior and the physiological mechanism used to elevate body temperature remain unknown. It may be possible that (i) these sharks are found in warmer shallower regions relative to the location of the ambient temperature dataloggers, (ii) the shallow, clear water enhances the absorption of solar heat by the shark’s skin, or (iii) that swimming activity may produce sufficient metabolic heat production to offset convective and conductive heat losses to the cooler surrounding water. Whereas studies of this nature are beginning to explore the potential physiological benefits of behavioral thermoregulation, there remains a lack of sufficient experimental data that quantifies the physiological effects associated with these behaviors. In a similar manner, the presence of behavioral thermoregulation in aggregating species has come from studying the behavior of individuals within the aggregations in relation to changing environmental conditions. Tracking studies of female leopard sharks aggregating in shallow coastal embayments showed diurnal movement patterns, with nightly (presumably

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(A)

Used Available

(C)

Relative abundance

0.8

0.6

0.4

0.2

(B) 20

21

22 Celsius

23

0

24

22.0

22.2

22.4

22.6

22.8

23.0

Temperature (°C)

(D)

0

30

60

Meters

Figure 8.1. Example of a (A) leopard shark (B) 4 h active track (black lines) overlaid on a seafloor temperature map to illustrate movements relative to a thermally stratified habitat. (C) Frequency distribution from Kernel utilization distribution of tracking positions of a tagged leopard shark relative to seafloor temperatures at those locations compared to the frequency distribution of seafloor temperatures available in the area of the black box in (B). While this shark occupied warm waters, the warmest waters available in the area were too shallow (o30 cm deep) for the sharks to access. (D) Autonomous tracking vehicle (Iver 2, Ocean Server equipped with Lotek MAP600 stereo hydrophones and integrated receivers) used to collect movement data (B) and programmed to not get into within 15 m of the tagged shark and circle the periphery of the field site (Big Fisherman’s Cove, Santa Catalina Island). Sea floor temperature was calculated using an inverse distance weighting interpolation.

foraging) excursions away from the aggregation site followed by reimmigration of many individuals to the aggregating site the following morning (Manley, 1995). Subsequent work attempting to document behavioral thermoregulation in this species used temperature dataloggers on the seafloor throughout one of the smaller aggregation sites to characterize diurnal water temperature changes (Hight and Lowe, 2007) (Fig. 8.1). Leopard sharks move into the aggregation site during the day, as conditions warmed (~20–241C), and dispersed from the site after dark when the water cooled (~19–201C). A more recent study documented the body

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core temperature and depth of aggregating female leopard sharks that were surgically fitted with temperature/depth-sensing acoustic transponders (Vemco Chat tags) capable of downloading stored data to a stationary acoustic receiver located at the aggregation site (Hight and Lowe, 2007). That work showed that for all individuals a daily pattern was present: the body core temperature rose over the course of the day (peaking in the early evening) and began to decrease later at night as sharks either moved into either cooler deeper water or as the shallow water temperature declined. Unfortunately, the ambient water temperatures during the off-site movements were not documented. Taken together, these experiments suggest that the adult female leopard sharks were altering their behavior in relation to changing environmental temperatures. Behavioral thermoregulation has been hypothesized to result when adult female elasmobranchs are in a gravid state (Economakis and Lobel, 1998). Although a conclusive determination of pregnancy in the field (e.g., via hormone screening or in situ ultrasonography) remains difficult to ascertain, there may be a potential benefit of seeking warmer waters during gestation (Jirik and Lowe, 2012). In the case of leopard sharks their diurnal movements into warmer waters enabled individuals to raise their body core temperature during the day by more than 31C over ambient; this was hypothesized to result in a 17% increase in their metabolic rate (Hight and Lowe, 2007). While temporarily costly, this behavior may decrease their gestation time by several months due to an increased rate of embryo development. Leopard sharks are thought to have a gestation period ranging from 10 to 12 months (Cailliet, 1992; Kusher et al., 1992), and at higher latitudes have not been found to aggregate, possibly because ambient water temperatures are too cold and there is no thermal advantage (Carlisle and Starr, 2009). Therefore, it is possible that individuals that aggregate in warmer habitats have shorter gestation (10 months) while northern, nonaggregating individuals have longer gestation (12 months), but there are no empirical data to support this hypothesis. However, evidence supporting the potential role of maternal thermophily has been documented in aggregating female round stingrays that were confirmed to be pregnant via field ultrasonography (Mull et al., 2010; Jirik and Lowe, 2012). Pregnant female rays were found to selectively move to, and remain in a shallow saltwater pond (~3.51C warmer than neighboring habitat) during the summer months potentially resulting in one of the shortest gestation periods (3–4 months) known for elasmobranchs (Babel, 1966; Mull et al., 2010; Jirik and Lowe, 2012). A shorter gestation period is thought to be beneficial for females by allowing partruded individuals to begin feeding at higher rates in habitats with higher prey abundance as a means to reprovision before their winter migrations (Jirik and Lowe, 2012).

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While insufficient evidence from field-based studies precludes the quantification of how this aggregative thermoregulatory behavior may actually benefit female reproduction (e.g., shorter gestation periods, large birth sizes of offspring, or higher offspring survival), laboratory studies have quantified thermal preferences and metabolic costs for some elasmobranch species, which offer support to some of the observed behaviors in the field. Laboratory work on Atlantic stingrays (Daysatis sabina) housed in a shuttlebox tank that created a thermal gradient typical of their normal summer habitats (24–301C) and allowed individuals to select preferred thermal conditions showed that pregnant females had a greater preference for warmer water (Wallman and Bennett, 2006). When the temperature preference between pregnant and nonpregnant females is taken into account (i.e., using a Q10 of 2.1; derived from laboratory-based metabolic rates; Di Santo and Bennett, 2011b; Table 8.2), selection of warmer conditions by pregnant females may reduce their gestation periods by up to 10 days. Assuming the benefits of increased metabolism resulting from seasonal or daily forays into warmer water can increase rate of embryo growth and shorten gestation periods, then elasmobranchs with greater temperature sensitivities (higher Q10s) may be expected to adopt these aggregative thermoregulatory behaviors more often than those with lower metabolic Q10s (Table 8.2). 2.4. Thermal Refuging Because in sharks and rays behavioral thermoregulation has been observed in both aggregating and nonaggregating individuals and populations, it is likely that there are multiple physiological benefits for the temporo–spatial selection of specific thermal habitats. Numerous sharks and rays have been observed to move between areas of different water temperatures at different times of day, and in most cases both male and females exhibit this behavior, which suggests that it does not necessarily confer a reproductive benefit. For example, laboratory-based thermal choice experiments and field-based tracking of adult male small-spotted catsharks (Scyliorhinus canicula) showed that this demersal species selects warmer (shallower) waters during the day or when feeding, and then returns to colder (deeper) waters at night or to rest and digest (Sims et al., 2006). This type of behavioral thermoregulation was termed as a “hunt warm – rest cool” strategy, whereby the animals could lower their daily energetic costs by up to 4%. A similar behavior has been documented in bat rays (Myliobatis californica), which moved into shallow, warmer (~211C) mud flats to forage, and then return to deeper, colder (161C) water to rest (Matern et al., 2000). For bat rays, their unusually high thermally sensitive

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metabolic rate (Q10=6.8, 14–201C; Table 8.2) makes shuttling behavior an energy-saving strategy (Hopkins and Cech, 2003). Although the thermal effect on gastric evacuation rate for bat rays is not known, work on Atlantic stingrays across typical summer water temperatures (24–271C) found that both the rate of evacuation (Q10=3) and absorption (Q10=2.2) were less thermally sensitive (Di Santo and Bennett, 2011a), suggesting that there may be marked energetic benefits for individuals to “hunt warm and rest cool.” In most cases, where behavioral thermoregulation has been proposed for elasmobranchs in the field, these animals appear to neither exhibit eccritic behavior nor attempt to maintain a constant elevated ambient temperature. For example, juvenile lemon sharks acoustically tracked in the Bahamas showed that relatively larger individuals selected water temperatures averaging 301C while smaller ones potentially avoided predation by remaining in the shallower, warmer mangrove habitats (Morrissey and Gruber, 1993). While it remains difficult to determine whether predation pressure or ontogeny may affect the thermal regimes of lemon sharks, the mapping of changing seafloor temperatures (using temperature dataloggers) has allowed for the documentation of the spatial heterogeneity of their home ranges (DiGirolamo et al., 2012). Tracking data for small juvenile lemon sharks (1.2–2.7 kg) fitted with external temperature dataloggers and acoustic transmitters showed their daytime movements into increasingly warmer habitats (28–361C) in their home range and the return to cooler areas (21– 271C) later in the night and early in the morning (DiGirolamo et al., 2012). Surprisingly, this pattern was maintained seasonally, despite overall changes in diel temperature extremes. Thus, in a manner similar to rays, this pattern of behavioral thermoregulation may enable these young lemon sharks to increase their foraging activity and elevate the absorption rate of meals by “hunting warm during the day and resting cool at night.” Although there are clearly other biological constraints (e.g., prey abundance, storm events, predation pressure) that influence habitat selection in small, more vulnerable sharks, the diel patterns of behavior suggests the presence of likely physiological benefits by moving between thermal extremes. The number of field-based studies providing evidence of thermally driven movements and site fidelity in sharks and rays has grown considerably during the last two decades; however, significant gaps remain in our understanding of their behavioral physiology. Much of this disparity arises from the inherent problem of scale between laboratory and field-based studies. Laboratory work on sharks documenting the effects of temperature on their physiology has been limited to either smaller species or juveniles due to the limitations of captive facilities; the size and complexity of the experimental chambers; and the large footprint (drag) of the telemetry and archival tags. For these reasons, only larger

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individuals have been tagged and tracked in the field using biotelemetry and biologging technologies. For example, relatively short-term acoustic active tracking data (10–136 h) from the pelagic adult blue shark (Prionace glauca) (198–300 cm FL) (e.g., an ectothermic carcharhinid) show that they have the capacity to undergo dives well below the thermocline (~400 m, 71C) (Carey and Scharold, 1990). A more recent satellite telemetry tracking study by Campana et al. (2011) showed that the vertical movement of juvenile blue sharks (129–201 cm FL) in the Gulf Stream off the Northwest Atlantic reached depths of up to 800–1000 m. It is likely that sojourns into deep water during the day may allow blue sharks to exploit additional food resources found in the cooler waters at greater depth that are out of range for other warm water limited species (Bernal et al., 2001b, 2009). However, unlike the colder waters in the west of the Gulf Stream where the adult blue sharks were previously tracked (Carey and Scharold, 1990), the water temperature in the Gulf Stream, where the juvenile blue sharks were tracked, did not fall below 151C (8.51C below that of the surface water temperature) (Campana et al., 2011). This suggest that depth per se may not be a key limiting variable for blue sharks, but rather that time spent at or below the thermocline may limit the extent of their vertical movements (see Section 2.5.1) (Bernal et al., 2009). The higher temperature of this deeper Gulf Stream water allows smaller blue sharks with a lower thermal inertia to remain in deep waters for extended periods of time in search for prey without compromising their body core temperature. For many large pelagic ectothermic sharks, the ability to penetrate colder, deeper water in search of prey or navigation cues may require sufficient body mass (thermal inertia) to mitigate the effects of the prolonged exposure times to deeper depths. These dives are often followed by extended periods of time swimming in warmer surface waters, presumably to rewarm. Evidence of this possible behavioral thermoregulation has been documented in the diving patterns of whale sharks that were fitted with both pop-off archiving satellite transmitters (PATs) and Splash transmitters (recording water temperature, depth, and light) (Thums et al., 2013). In one pattern of diving, sharks were observed making dives to over 300 m and remaining at these depths for periods as long as 169 min, after which the animals returned to surface waters and remained there for several hours before resuming normal diving behavior. While temperature, depth, and light sensing archiving PATs have provided a much more detailed characterization of how pelagic sharks move through a potentially highly stratified thermal environment, there is still, however, a need to understand how core body temperature changes relative to these condition, and how the behavior is influenced by

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resulting physiological processes affected by temperature, pressure, and exposure to hypoxia.

2.5. Physiological Thermoregulation The body temperature of most sharks closely matches that of ambient water temperature because all metabolically produced heat is rapidly lost to the water either across the body surface (thermal conduction) or via the blood at the gills (convective transfer) (Brill et al., 1994). However, sharks in the family Lamnidae and the common thresher shark (Alopias vulpinus; family Alopiiadae) have evolved a suite of morphological adaptations that allow their body core (i.e., red myotomal swimming muscles, RM) and other regions of the body (i.e., eyes, brain, viscera) to be maintained at a warmer temperature relative to ambient temperature (regional endothermy) (Carey and Teal, 1966, 1969a,b; Carey et al., 1971, 1985; Block and Carey, 1985). These sharks appear to retain the metabolic heat generated during continuous swimming by the contraction of the aerobic RM and by the viscera during digestion and assimilation (Carey and Teal, 1969a; Carey et al., 1981, 1985; Block and Carey, 1985; Wolf et al., 1988). Exposure to rapid and repeated movements across thermal fronts (both vertical and horizontal) are a common trait of these pelagic sharks and regional endothermy may allow for the maintenance of a more thermally stable internal operating environment for the locomotor, digestive, and sensory systems. Thus, the selective advantages of regional endothermy may have allowed these sharks to expand their thermal niche and make accessible the additional food resources of the cooler, more productive waters at both a greater depth and at higher latitudes (Block and Carey, 1985; Carey et al., 1985; Bernal et al., 2001a; Dickson and Graham, 2004). Although for several lamnid sharks RM endothermy appears to have resulted in a broader latitudinal distribution and thermal tolerance, there are other examples that do not neatly fit this explanation. For example, the three species of thresher sharks have markedly different thermal distributions (Smith et al., 2008; Stevens et al., 2010) (see Section 4.4.) and several other pelagic sharks (e.g., blue shark, basking sharks, Cetorhinus maximus) have the capacity to dive into deep water well below thermocline and venture into high latitudes for extended periods of time (Carey and Scharold, 1990; Skomal et al., 2009). One potentially important shared trait that may allow these sharks to be exposed to cold water for prolonged periods of time may be a large body size, as an increased mass holds greater thermal inertia; however, no field data are available to support this view.

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2.5.1. Muscle Endothermy The swimming muscles in sharks are comprised of red and white (WM) myotomal muscle fiber types (Johnston, 1981; Bone, 1988; Rome et al., 1988). The RM in sharks comprises about 2% of body mass and is characterized by being a myoglobin rich aerobic fiber that power continuous swimming. By contrast, the myoglobin-poor WM comprise more than 50% of the body mass and is recruited during short duration, burst swimming (e.g., catching prey or predator avoidance) (see Chapter 5; Johnston, 1981; Bone, 1988). Unlike ectothermic sharks in which the RM is located subcutaneously (i.e., laterally) along the length of the body (mostly posteriorly), the RM position of regionally endothermic sharks is markedly different in that it is located in close proximity to the vertebral column (i.e., medially) and is predominantly distributed more anteriorly along the body (Carey and Teal, 1969a; Carey et al., 1971, 1985; Bernal et al., 2001a; Sepulveda et al., 2005) (Fig. 8.2). This medial RM position has led to a unique vascular layout where large arteries branch from either the efferent branchials or from the dorsal aorta to form lateral vessels (one on each side of the body) that run directly beneath the skin along the length of the body (i.e., lateral circulation), from which smaller, thin-walled arteries branch inwards to perfuse the RM. Venous return from the RM is through small thin-walled veins that run outward to join the lateral veins that run subcutaneously (very close to the lateral arteries) back to the heart. This unique vascular layout allows blood flowing to and from the medial RM to form a network of juxtaposed vessels (retia) that, while not allowing for the diffusion of dissolved gases, readily permit the transfer of heat (Carey and Lawson, 1973; Carey and Gibson, 1983) (Fig. 8.3), effectively acting as a countercurrent heat exchanging system and resulting in thermal transfer (the basis for RM endothermy) between the cool arterial blood entering the RM and the warm venous blood leaving it (Carey and Teal, 1969a,b; Carey et al., 1971; Carey and Lawson, 1973; Graham et al., 1983; Brill et al., 1994; Bernal et al., 2001a; Morrison et al., 2015). The capacity for RM endothermy in sharks has been typically measured by inserting a temperature probe deep into the axial muscle (targeting the RM) in a specimen immediately after capture. The temperature of the RM is then compared to the sea surface temperature (SST) in order to determine the degree to which RM temperature exceeds SST (i.e., thermal excess) (Carey and Teal, 1969a; Carey et al., 1971, 1985; Anderson and Goldman, 2001; Bernal et al., 2001a; Goldman et al., 2004; Bernal and Sepulveda, 2005; Patterson et al., 2011). In contrast to ectothermic sharks where RM thermal excess is small or may even be negative (i.e., RM temperature below SST), sharks capable of RM endothermy have a RM temperature that can

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sa

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Figure 8.2. Representative cross-sectional slice showing the position of the red muscle (RM) and the major blood vessels in ectothermic (bigeye thresher, A) and endothermic (common thresher, B) sharks. Also shown are simplistic vascular diagrams of the anterior region of both sharks and a representative cross-sectional slice showing the RM position and the major blood vessels. hv, heart ventricle; da, dorsal aorta; pcv, post cardinal vein; lv, lateral vein; la, lateral artery; rete, heat exchanging rete; ecl, efferent collecting loop; eba, efferent branchial arteries; sa, subclavian arteries; ca, celiac artery. Recreated from Patterson et al. (2011) and Bernal et al. (2012).

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(C) time (hrs) 0

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5 silky shark 6 tiger shark 7 scalloped hammerhead 8 manta ray

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Figure 8.3. Red muscle (RM) temperature in sharks. (A) Muscle temperature elevation in sharks as a function of sea surface temperature (SST). (B) Representative cross section of a salmon shark taken at approximately 50% FL, which shows the thermal profile between the skin and the internal RM with probe measurements following the path of the arrow. (C) An example of movement patterns of a salmon shark in the Gulf of Alaska showing ambient water

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be up to 17.51C above SST, with species inhabiting colder waters (i.e., higher latitudes or deeper depth distributions) showing the largest thermal excess when compared to those found in warmer waters (Carey et al., 1971, 1985; Bernal et al., 2001a, 2009) (Fig. 8.3). Because the measurement of RM thermal excess, through intramuscular puncture, relies on the retention of metabolically produced heat during sustained, aerobic swimming, the degree of swimming activity prior to probe insertion can influence RM temperature elevation. For this reason, any reduction in swimming activity during capture or as a result of exhaustion can translate into an abnormally lower RM temperature upon reaching the boat (Carey et al., 1985; Goldman et al., 2004; Bernal and Sepulveda, 2005). Indeed, the thermal excess of stressed or moribund sharks is generally lower or may even be negligible, and thermal studies on sharks routinely select for specimens that were actively swimming when landed (Carey and Teal, 1969a; Smith and Rhodes, 1983; Block and Carey, 1985; Carey et al., 1985; Anderson and Goldman, 2001; Bernal and Goldman, personal observation). In some cases, at-vessel measurements of RM temperature in sharks are difficult to interpret. For example, boat-side measurements of RM temperature in bigeye thresher sharks (Alopias superciliosus) reported above ambient temperature values (Carey et al., 1971). This finding, however, may have resulted from local oceanographic anomalies as these specimens were captured in waters where a marked thermal inversion (water at 30 m was approximately 101C warmer relative to SST) was present and it was not possible to determine the precise depth at which the sharks were swimming prior to capture. For this reason, if the bigeye thresher sharks used by Carey et al. (1971) were swimming within the warm (deep) inversion layer prior to capture, their muscle temperatures would be warmer than the colder SST, resulting in RM thermal excess due to behavioral and not physiological mechanisms. These results demonstrate the intrinsic problem of using both boat-side temperature measurements and SST to determine the presence and degree of RM endothermy, and make it clear that the thermal stratification of the water column and knowledge of the depth at which the sharks were

temperature and internal muscle temperature recorded during an acoustic telemetry track. (A) Dashed line indicates the line of equality (i.e., where RM temperature ¼ SST). Data are shown as mean7SE for common thresher (Alopias vulpinus, n ¼ 24), pelagic thresher (A. pelagicus, n ¼ 7), and salmon shark (Lamna ditropis, n ¼ 31). Individual data shown for all others. Linear regressions (i.e., RM temperature vs. SST) are shown for shortfin mako shark (Isurus oxyrinchus, n ¼ 38, TRM ¼ 13.8+0.51 SST), and porbeagle shark (Lamna nasus, n ¼ 13, TRM ¼ 10.8+0.72 SST). Figure recreated from data in Bernal et al. (2012), Anderson and Goldman (2001), Bernal et al. (2001a), Smith and Rhodes (1983), Carey et al. (1971), Bernal and Sepulveda (2005), Patterson et al. (2011), Carey and Teal (1969a).

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swimming prior to capture is critically important. For these reasons a better assessment of the capacity for RM endothermy in sharks comes from fieldbased acoustic telemetry determinations of tissue temperatures in freeswimming sharks and from laboratory-based work on sharks swimming under controlled conditions. Documenting the internal body and ambient temperature of freeswimming fish in the field has been achieved by inserting a thermistor, attached to an acoustic tag, deep into the axial muscle and simultaneously measuring axial muscle temperature and external water temperature in real time (Carey and Lawson, 1973; Carey and Robinson, 1981) or by storing muscle temperature data in an external archival tag (Fig. 8.3). While the latter method requires the archival tag to be recovered for data download, the former can telemeter shark body temperatures only when in acoustic detection range of the animal. Carey et al. (1982) designed a multitransmitter package consisting of an epaxial muscle thermistor, an ambient water thermistor, and depth-sensing transmitters that could be harpooned into the dorsal musculature of a large shark. Each transmitter operated at a different frequency to allow for data to be telemetered simultaneously, thus providing a mechanism to document ambient water and body temperature as the freeswimming shark traversed different depths. Although the development of these innovative methods to measure the body and ambient temperature in free-swimming sharks marked a significant milestone for field physiologists, the logistical complexity of both methods has resulted in relatively few studies on sharks that document their fine-scale use of the water column while simultaneously recording their internal body core temperature. Tricas and McCosker (1984) acoustically tracked a white shark off South Australia that exhibited a 3–41C elevation in deep muscle temperature over ambient temperature during two hours, while swimming in water with a temperature of approximately 211C. In a similar manner, Carey et al. (1982) found that the deep muscle (presumably RM) of a large white shark acoustically tracked in the northwest Atlantic exhibited a similar thermal excess (3–51C) when swimming in ambient water ranging from 61C to 181C. This white shark showed a distinct preference for swimming in the thermocline, a behavior that has since been commonly observed in other endothermic fishes (Carey et al., 1971, 1982; Carey and Robinson, 1981; Holland et al., 1992; Holts and Bedford, 1993; Block et al., 1998; Brill et al., 1999). The documentation of both internal body and ambient temperature and the thermal changes of the deep muscle temperature allowed, for the first time, a field-derived estimation of metabolic rate (60 mg O2 kg 1 h 1) in these large (W900 kg), pelagic, endothermic sharks (Carey et al., 1982). When placed in a comparative context, the metabolic rate of a large white shark was estimated to be about three times higher than that of a spiny

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dogfish, after being adjusted to a similar body mass (~1000 kg) and temperature (201C). Further discussion of metabolic rates in elasmobranchs can be found in Chapter 6 of this volume and in Ballantyne (2015). For ectothermic sharks, acoustic telemetry of free-swimming blue sharks that had been affixed with an internal thermistor (deep WM) showed that during descents from the warm surface (261C) to depths below the thermocline (91C), the body core temperature was directly affected by ambient temperature (Carey and Scharold, 1990). During those dives (from ~100 to 200 min in duration) the body core temperature decreased from about 211C to approximately 141C resulting in a low thermal rate coefficient for cooling (k=–0.0051 k min 1) and providing an apparent thermal benefit that may enhance sensory and locomotory performance at depth. This thermal advantage would disappear, however, if the blue shark remained at this depth (temperature) for an additional 4–5 h at which time its body core temperature would ultimately decrease until reaching thermal equilibrium with ambient (Bernal et al., 2009). Surprisingly, those blue sharks did not remain at depth for that long, but rather when the body core temperature reached approximately 141C they returned to the warm surface for up to 50 min until their body core rewarmed to approximately 211C before undergoing their next dive. However, there has been no work on the thermal effects on muscle function (see Section 2.5.1.1.) in blue sharks and it remains unknown if, regardless of depth, there is a potential lower thermal limit (e.g., ~141C) that triggers these sharks to leave the deeper, colder depths and return to warmer waters to thermally recharge their swimming muscles and safeguard contractile function (see Chapter 5). Laboratory studies on shortfin mako sharks swimming in a thermally controlled water tunnel were able to determine their capacity for controlling heat-balance during steady, continuous swimming by subjecting them to repeated stepwise rapid changes in ambient temperature that mimicked the range of temperatures encountered during normal vertical excursions (Holts and Bedford, 1993). The results showed that mako sharks swimming at a constant speed, and exposed to rapid changes in ambient temperatures, can modulate rates of heat gain and heat loss, offering evidence of physiological thermoregulation (Carey and Lawson, 1973; Bernal et al., 2001b). The exact mechanism for this, however, remains unresolved but is presumably associated with an altering of blood flow rate and retial heat-transfer efficiency (Carey and Teal, 1969a,b; Carey et al., 1982; Graham et al., 1983; Block and Carey, 1985; Brill et al., 1994; Dewar and Graham, 1994). Although laboratory studies of thermoregulation in swim tunnels are not feasible for large sharks it is the only method currently available in which both ambient temperature and swimming speed (metabolic heat production) can be controlled.

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To date, field data are not available to allow the comparison of the thermal balance of two sympatric pelagic sharks (regional endotherm vs. ectotherm) undergoing identical vertical (temperature) movements. However, this comparison may be possible by utilizing simple thermodynamic models that rely on laboratory and tracking studies to describe the physiological ability to alter rates of heat gain and heat loss (Carey and Scharold, 1990; Bernal et al., 2001b; see Section 2.5.1.2.). These models predict that an endothermic shark (e.g., mako shark) undergoing dives from the surface (e.g., 201C) to, or below, the thermocline (e.g., 10–121C) would sustain an overall warmer RM operating temperature (thermal excess of 51C or more) during the times of cold water exposure relative to an ectothermic counterpart (e.g., blue shark) (Bernal et al., 2009). Moreover, if the ectothermic shark were to mimic the recorded vertical movements of a tracked endothermic shark (e.g., 30 min descents below the thermocline and 8 min periods of basking at the warm surface (Holts and Bedford, 1993; Sepulveda et al., 2004), the body temperature of the former would theoretically decline with each dive, while the latter would maintain a warmer temperature of the RM (Bernal et al., 2009). For this reason, field work that documents heat balance in freeswimming sharks using physiological telemetry or archival tags is needed to determine the extent of physiological thermoregulation in larger regionally endothermic sharks and ectothermic sharks across a range of body sizes. As a way of decoupling the physiological control of body temperature regulation, future work is needed on free-swimming sharks where RM temperatures can be monitored in the field during times when retial efficiency can be influenced (i.e., pharmacologically) by altering blood flow rates (heat exchange efficiency), where it is expected that individuals should start to exhibit more behavioral thermoregulatory movements which may be comparable to those of ectothermic sharks. While RM endothermy in sharks may not provide them with a greater tolerance to colder waters (e.g., blue and mako sharks have similar thermal distributions) it may allow them to make rapid and repeated excursions into cooler, more productive waters while safeguarding muscle function (Neill et al., 1976). In addition, other sharks with RM endothermy are able to seasonally inhabit very cold, highly productive, subpolar waters (e.g., 2– 101C) while maintaining an almost constant RM temperature (~201C or more above ambient; Goldman et al., 2004) (Fig. 8.3), potentially providing them seasonal access to the ample food resources of subpolar waters without compromising their physiological function under perpetual cold conditions. However, the full extent to which the sharks are capable of RM endothermy still remains unresolved, as it requires simultaneous measurements of (i) RM temperature, (ii) ambient temperature, (iii) the duration of time spent at depth, and (iv) an accurate measure of swimming activity.

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2.5.1.1. Temperature Effect on Muscle Function. Work on muscle performance in both endothermic and ectothermic sharks has shown that there are numerous similarities in the contractile properties of the swimming muscles as, for example, the stimulus duration, stimulus phase, net work, and power output of the locomotor muscles are relatively consistent along the body of sharks (Donley et al., 2007) even when comparing ectothermic (e.g., leopard shark) and endothermic (e.g., mako shark) species. However, there appears to be a very different thermal effect on RM function between regionally endothermic and ectothermic sharks (see Chapter 5). When compared at the same temperature endothermic sharks appear to achieve maximal power output at higher cycle (tailbeat) frequencies relative to ectothermic species. In addition, the range of operating temperatures at which peak muscle performance is produced appears to be very narrow in the endothermic species (Donley et al., 2007). For example, the endothermic salmon shark (Lamna ditropis), which commonly inhabit waters cooler than 101C and can even frequent water as cold as 21C (Weng et al., 2005; Goldman, personal observation), maintain a RM thermal excess of at least 141C (Goldman et al., 2004; Bernal et al., 2005). If the operating temperature of the RM falls below 201C, there appears to be a significant deterioration of muscle function as it stops producing positive work during a contractile cycle (i.e., tailbeat) (Bernal et al., 2005). This thermal sensitivity has also been documented in other sharks with RM endothermy, although it is less pronounced and muscle performance can be sustained when cooled to 151C (Donley et al., 2007, 2012). By contrast, these thermal effects are not as prominent for other sharks that are not capable of RM endothermy (e.g., leopard shark, bigeye threshers – see Section 4.4) in which muscle function is still possible, although at much slower cycle frequencies, at cooler temperatures below 151C and even at 81C (Donley et al., 2007; Bernal and Sepulveda, personal observation). 2.5.1.2. Thermal Modeling. Although using laboratory- and field-derived tissue (i.e., RM) temperature data collected by either telemetry or archival tags in swimming sharks allows for a more accurate assessment of the degree of muscle endothermy, there is a need to consider how key variables affecting both heat production (e.g., swimming activity) and retention (e.g., heart rate, blood flow through retia) may alter their capacity for physiological thermoregulation. Laboratory studies on small mako sharks steadily swimming in a thermally controlled water tunnel indicate their capacity to modulate rates of heat gain and heat loss during large and rapid changes in ambient temperature offering evidence of physiological thermoregulation (Bernal et al., 2001b). While that work demonstrated the thermoregulatory ability of a small lamnid, it did so under forced

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thermal regimes in specimens that had not undergone any significant acclimation to a laboratory setting. For this reason it remains unknown how behavior (e.g., choosing a water temperature) and physiology (e.g., modulating swimming activity and retial efficiency) may influence thermoregulation. Recent work on salmon sharks fitted with two telemetry tags (one with an internal thermistor to measure RM temperature, the other measuring depth and ambient water temperature) allowed an unprecedented, albeit brief, glimpse of the in vivo operating temperature of a free swimming endothermic shark in subpolar waters (Bernal et al., 2012; Goldman, personal communication) (Fig. 8.3). Remarkably, the RM temperature of these salmon sharks appeared to be held within a narrow thermal range (16–191C) even when the shark underwent large and rapid changes in ambient temperature (from 171C to 51C) during a dive. Unfortunately, the degree of swimming activity (heat production) during the tracks was not able to be documented. Surprisingly, the in vivo RM temperatures recorded using telemetry were below those at which positive work is achievable using isolated muscle preparations (see Section 2.5.1.1.). It is likely that the logistical difficulties of this field study (dealing boatside with a large, unhappy shark on a stretcher) precluded the precise placement of the thermistor in the center of the RM and hence temperature traces reflect the area surrounding the RM (i.e., deep WM), which are known to have a lower thermal excess (Carey and Teal, 1969a,b; Bernal et al., 2005). Alternatively, the inherent error in the precision of the temperature sensors in the telemetry tags used may have led to the lower-than expected values of in situ RM temperatures. Nonetheless, the emerging capacity to go to the field and obtain these types of free-swimming data on large sharks allows for a closer inspection of the physiological and behavioral capacities for thermoregulation. Thus, there is a need for mathematical models that can make predictions from field data and better assess the thermal biology of large sharks that can only be studied at sea. Recent efforts have produced mathematical models that describe the thermoregulatory capacities of free-swimming endothermic fish. To date, Newtonian-based heat transfer models have been used to calculate the thermal rate coefficient (k 1C min 11C gradient 1; a lumped parameter encompassing conduction, forced convection, and passive convection at the body core, body surface, and environment) in some endothermic fish (Graham and Dickson, 1981; Brill et al., 1994; Holland and Sibert, 1994; Bernal et al., 2001b, 2009; Malte et al., 2007; Boye et al., 2009). These models, however, cannot separate the effects of physiological, behavioral, and passive thermodynamics without substantial changes in k. Therefore, there is a continuing need to develop new models (e.g., using Fourier-based

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heat conduction), that can incorporate potential changes in thermal conduction and convection which are influenced by changes in key variables, such as ambient water temperature, previous body temperature, muscular heat production, mass blood flow, and heat exchanger efficiency (Boye et al., 2009). Thermal balance models have been developed for tunas due to the relatively more abundant physiological and ecological data collected during previous laboratory and field studies (Holland et al., 1992; Brill and Jones, 1994; Dewar et al., 1994; Korsmeyer et al., 1996; Block and Stevens, 2001; Korsmeyer and Dewar, 2001; Shiels et al., 2010). However, work on other large pelagic sharks that cannot be held in captivity will continue to rely solely on field studies. Sophistication of heat balance models will require more fine-scale information about the animal as it moves through different thermal conditions and focus should be placed on scenarios that employ technologies that can, for example, simultaneously measure (at much higher rates) ambient temperature, internal body temperature, swimming velocity, heart rate, and swimming activity. 2.5.2. Cranial Endothermy In general, sharks occupy an environment where, during the daylight hours, light is abundant and penetrates the upper, photic layer of the water column. This has led sharks to rely heavily on vision and most all have evolved both well-developed eyes and visual cortex of the brain (see Chapter 2) (Lisney and Collin, 2006; Lisney et al., 2007). In addition, species that are more nocturnal or spend the daylight hours at depth (below the photic zone) have eyes that function well under low-light levels and are considered to be dark-adapted (Lisney et al., 2012). The eyes of sharks are relatively large and receive a large blood supply from the efferent hyoidean and pseudobranchial arteries to meet their high metabolic demands (Block, 1987). Because the oxygenated blood arising from the gills is at thermal equilibrium with ambient, the temperature of the eye and brain reflects the temperature of the surrounding water. Work on other fishes has shown that a warming of the brain and eye region significantly enhances physiological processes (e.g., synaptic transmission, postsynaptic integration, conduction, and, in the eye, temporal resolution) that result in improved neuro-visual function (Konishi and Hickman, 1964; Friedlander et al., 1976; Montgomery and Macdonald, 1990; Fritsches et al., 2005; Van Den Burg et al., 2005). For example, recent work on swordfish (Xiphias gladius) shows that warming the retina significantly improves temporal resolution by increasing (Q10 of 5.1) the flicker fusion frequency rate of the eye (Fritsches et al., 2005). Therefore, the capacity to warm and maintain an elevated eye and brain temperature may enhance the ability to

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detect prey in low-light levels and at low temperatures and avoid predators (Block, 1986; Fritsches et al., 2005). Exposure to colder temperatures will significantly affect eyesight and impair neural integration. Therefore, the prey of ectothermic elasmobranchs may be more restricted to slower moving, easy to capture invertebrates and fishes at deeper (darker), colder depths due to decreased visual and neural function, but little work has been focused on this aspect of their foraging ecology. While most sharks have evolved to function under a condition where the eyes are in thermal balance with ambient, lamnid sharks have evolved the capacity for cranial endothermy, which allows for the elevation of brain and eye temperatures (Block and Carey, 1985; Wolf et al., 1988; Anderson and Goldman, 2001; Bernal et al., 2001a). However, unlike billfish, swordfish, tuna, and opah (Carey, 1982; Block, 1986, 1987; Sepulveda et al., 2007a; Runcie et al., 2009), where a combination of modified ocular muscles appears to be the principal eye–brain heat producing mechanism and vascular specializations act as local heat exchangers work in order to maintain an above ambient cranial temperature, lamnid sharks are unique in having a specialized vein that transports warm blood from the RM to the cranial region. This unique large vein is deeply embedded in the RM, proceeding anteriorly and joining the myelonal vein prior to forming a meningeal vascular plexus that envelopes the brain. This allows blood that has been warmed by the contracting RM to reach the brain, bathing it in warm blood, and allowing conductive heat transfer before flowing via the posterior cerebral vein into a large orbital sinus (i.e., orbital rete; Wolf et al., 1988) in close proximity to the eye. Taken together these physiological and morphological adaptations effectively elevate the temperature of the brain (up to 9.51C above SST; Block and Carey, 1985; Bernal et al., unpublished data; Anderson and Goldman, 2001) and eyes (up to 12.91C above SST; Block and Carey, 1985; Bernal and Graham, Unpublished Data; Alexander, 1998; Anderson and Goldman, 2001). It has been suggested that the large extra-ocular eye muscles of lamnid sharks may aid, as an additional source of metabolic heat, in cranial endothermy (Wolf et al., 1988; Alexander, 1998). Indeed, the relative mass of the extra-ocular muscles in lamnids (~50 to 60% of the total eye weight) is more than twice that of other species, and its deep-red color (i.e., myoglobin rich) may indicate elevated levels of aerobic metabolism (Block and Carey, 1985; Wolf et al., 1988; Alexander, 1998). While new evidence shows that, when compared to ectothermic blue sharks, the medial rectus ocular muscle of makos has a high activity of citrate synthase (a key enzyme for oxidative metabolism; Kehrier, 2012), lamnid eye muscles do not appear to have the structural specializations for thermogenesis found in the eye muscles of other fishes with cranial

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endothermy (i.e., billfish) (Carey, 1982; Block, 1986, 1987; Sepulveda et al., 2007a; Runcie et al., 2009). Another shark, the bigeye thresher, has abnormally large eyes and possesses a large orbital plexus (putative rete) and has been suspected of having cranial endothermy (Carey, 1982; Block and Finnerty, 1994; Weng and Block, 2004). Unfortunately, there are no published temperature data available for this species; however, opportunistic work on captured bigeye, common, and pelagic threshers show that the temperature of the eye (via acute probe penetration) does not appear to be warmer than SST (Bernal and Sepulveda, personal observation). There are two species of myliobatoid rays that appear to have cranial retia (Alexander, 1996) but, to date, there have been no temperature measurements and their in vivo cranial temperatures remain unknown. For all sharks, the presence of cranial endothermy has relied on temperature measurements (taken boatside) via acute thermistor or thermocouple probe insertions. The inherent limitations of such an invasive technique has not allowed the true extent for cranial endothermy to be determined and it is not understood how cranial endothermy may ultimately impact their capacity to penetrate colder (deeper, higher latitude) or dimly lit waters without compromising neuro-visual function. To date, there has been no field or laboratory work on sharks to determine the in vivo thermal effects on intact eye function and we know of no field-based attempts to telemeter or archive the cranial temperatures or the light-levels encountered by free-swimming sharks. 2.5.3. Visceral Endothermy Understanding the feeding behavior and foraging ecology of elasmobranchs requires knowledge of the physiological processes affecting digestion and absorption of nutrients, many of which are directly affected by temperature (see Section 3.3; Bucking, 2015). In general, the rate of digestion is directly affected by intrinsic activity and thermal sensitivity of key digestive enzymes (e.g., pepsin, trypsin) (Schmidt-Nielsen, 1997). Therefore, the presence of an elevated visceral temperature has been considered to be a potential mechanism to enhance the rate of digestion and assimilation (Carey et al., 1981, 1984; Stevens and McLeese, 1984a; Goldman, 1997) and may also be a significant contributor to the warming of the body core, which may allow these fishes to penetrate and inhabit cool waters (reviewed by Dickson and Graham, 2004). Recent work on the in vitro activities of key digestive enzymes (i.e., pepsin, trypsin, lipase) in endothermic and ectothermic sharks shows that at in vivo temperatures, the former had significantly higher activities (from 6 to 27 times) relative to the latter, suggesting that regional endothermy increases the physiological

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performance of the warmed visceral organs (Newton et al., 2015). Thus, for sharks not capable of maintaining elevated visceral temperatures the potential effect of temperature on digestive processes may likely drive diel thermoregulatory behavior in many species that have access to highly structured thermal conditions (see Section 3.3). In sharks, the capacity to maintain visceral temperatures above ambient has been documented in lamnid sharks and there remains speculation that the common thresher sharks can do this as well (Carey et al., 1985; Fudge and Stevens, 1996; Goldman, 1997; Goldman et al., 2004; Sepulveda et al., 2004) (Fig. 8.4). However, the morphological specializations present in these

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two groups differ significantly. While the blood delivery to the viscera of most sharks is through the large celiac artery, the principal arterial visceral circulation in lamnids is through the greatly enlarged pericardial vessels arising from the efferent branchials (Burne, 1923; Carey et al., 1981). Upon reaching the anterior viscera, these arteries penetrate a large venous sinus, filled with warm blood returning from the viscera, and branch repeatedly to form the suprahepatic rete. Prior to exiting the sinus the arterial vessels of the rete coalesce and re-form a large vessel that is the main blood supply to the viscera. This vascular layout in lamnids results in all blood flow to and from the viscera (e.g., stomach, liver, spiral valve) being through the suprahepatic rete, which effectively acts as a heat exchanger between the warm (venous) and cool (arterial) blood. By contrast, blood delivery to the viscera in the common thresher appears to be as in other non-lamnid sharks; however, in the common thresher there are a number of small retia, including a single retia along the portal vein and several other retia associated with the stomach wall and spiral valve (Eschricht and Mu¨ller, 1835 in Fudge and Stevens, 1996). Although these retia appear to be different from those observed in lamnids (Burne, 1923) there has been no detailed morphological description of these structures, beyond a cursory anatomical survey, which precludes a comparison between the morphological specializations of threshers and other fishes with analogous structures (i.e., retia in viscera of tuna). Aside from the different anatomy (i.e., location and complexity) of the visceral retia between lamnids and the common thresher, the principal source of heat used to maintain a gut temperature markedly above ambient appears to arise from digestion (catabolism). For example, the visceral temperatures of a salmon shark taken by acute probe penetration range from 4–141C above SST, with the warmest temperature found in the spiral valve, a large organ with a high surface area that is the main site for digestion and assimilation of food arriving from the stomach (Anderson and Goldman, 2001; Bernal, unpublished data). Unfortunately, there are no published data for the visceral temperatures of any thresher shark species, and opportunistic field data collected via acute thermal probe penetration on all three thresher species has not documented any thermal excess in the viscera (Bernal and Sepulveda, personal observation), suggesting this group’s inability to potentially elevate body core temperature via digestion. It has been suggested that visceral endothermy in lamnids may be affected by altering blood flow to the suprahepatic rete by either diverting the delivery of arterial blood from the suprahepatic rete to the dorsal aorta (i.e., into the celiac, spermatic, and lineo-gastric arteries) or by rerouting venous return from the suprahepatic rete into a large central channel that leads directly into the sinus venosus (Burne, 1923; Goldman and Bernal,

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personal observation; Carey et al., 1981). Evidence of smooth and circular muscle within the walls of the rete-associated vessels suggest that dilation or constriction could be used to alter up to 20% of returning blood flow through or around the rete (Carey et al., 1981). In addition, salmon and porbeagle (Lamna nasus) sharks have an additional rete present in close proximity to the kidney (renal rete; Burne, 1923; Goldman and Bernal, personal observation) with temperatures that are as much as 11.41C above SST (Anderson and Goldman, 2001; Bernal and Graham, unpublished data). Although this suggests that an additional highly effective heatconserving structure is present in the viscera of lamnids, its role, and the potential role that other large, metabolically active organs (e.g., the liver) play in visceral endothermy remains unresolved. The use of acoustic telemetry allows for a noninvasive method to document the visceral temperatures of free-swimming sharks in the field. The ability to feed a temperature sensing acoustic transmitter (hidden in a piece of food) to a shark, and have it remain within the stomach for up to several days allows for a relatively simple way to quantify visceral endothermy (Fig. 8.4). Because the stomach is in a central location in the viscera and, in lamnids, is in close proximity to the suprahepatic, renal, and lateral cutaneous retia, its temperature can be used as a good indicator and proxy for body core temperature (Goldman, 1997; Goldman et al., 2004). Field-work on mako, white, and salmon sharks shows that the temperature of the stomach is not only warm (from 8–211C above ambient) but remains within a very narrow range and appears to be independent of changes in ambient temperature (Carey et al., 1981; McCosker, 1987; Goldman, 1997; Goldman et al., 2004; Sepulveda et al., 2004) (Fig. 8.4A). This is unlike the stomach temperature of free-swimming tuna, the only other group known to have visceral endothermy, which experience a rapid (within hours) and large (up to 201C) temperature increase after prey ingestion followed by a steady decrease back to the pre-feeding temperature (Carey and Lawson, 1973; Carey et al., 1984; Stevens and McLeese, 1984b; Gunn et al., 2001; Bestley et al., 2008). For tuna, the repeated correlation between a feeding event and the corresponding increase and decrease of stomach temperature suggests that heat production results from digestion and assimilation (Carey et al., 1984; Stevens and McLeese, 1984b). By contrast, for lamnid sharks, the stomach temperatures remain continuously elevated even during times of large changes in ambient temperature (Carey et al., 1981; McCosker, 1987; Goldman, 1997; Goldman et al., 2004; Sepulveda et al., 2004). It is possible that all the field-derived stomach temperatures collected from lamnids reflect sharks that always have food items in their digestive system (i.e., active heat production from digestion) or, alternatively, indicate a very slow stomach clearance rate (food items remain in the digestive track for long periods of

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time: see Section 3.3.). Telemetry data on free-swimming mako and white sharks show that during the tracking period there are abrupt, short-lived changes in stomach temperature (i.e., ingestion of cool prey items) suggesting frequent feeding events (Fig. 8.4A). In addition, recent field work on free swimming shortfin mako sharks that were fed telemetry tags hidden in a bait of known mass, tracked for up to 12 h and recaptured to document the state of digestion of the bait, showed very fast rates of prey digestion (less than 6 h) (Sepulveda and Bernal, personal observation) (Fig. 8.4D). Thus, free-swimming lamnids sharks appear to not only feed frequently but some (e.g., makos) may experience very fast rates of stomach clearance, which may allow the shark to quickly make room for the next meal. It may also be possible that the anatomical layout for blood delivery to and from the viscera in lamnids (a large, single rete) may act as a continuous heat exchanger (always “on”), thus retaining most of the heat derived from digestion and assimilation in all the visceral organs. By contrast, blood delivery to the multiple organ-specific retia in tunas and the common thresher may be “on” only when that organ is metabolically active. For example, the stomach temperature will increase when prey is being digested in that organ but as the food stuffs move to the remainder of the digestive tract (e.g., pyloric caeca, spiral valve) then stomach temperatures diminish and heat production and retention shift to the next organ and its associated retia. Clearly, future work is needed to resolve if there are organspecific temperature changes associated with different stages of digestion and how these may be affected by ambient temperature in both sharks capable of visceral endothermy and those that may exhibit behavioral thermoregulation. The deployment in the field of new miniature temperature-sensing acoustic transmitters (e.g., Vemco V9TP, Lotek MM-8-TP) which are small enough to be hidden in bait and fed to free-swimming sharks (Fig. 8.4B and C) while simultaneously attaching an external temperature transmitter (darted to the dorsal musculature) will allow for the comparison of internal (visceral) and environmental temperatures under natural conditions. 2.6. Thermal Effect on Metabolic Rate During the last several decades there has been a significant increase in the understanding of the relationship between body size, temperature, and metabolism across numerous teleost taxa (Clarke and Johnston, 1999; Gillooly et al., 2001; Brown et al., 2004; Clarke and Fraser, 2004). For sharks, however, very little is known about their energetic metabolism and less is understood on the mass- and thermal-scaling effects and how these may influence their thermoregulatory behavior. Again, the general view on

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shark metabolism comes from a limited number of studies on small, relatively sedentary, species that are easily kept in captivity. For elasmobranchs and most other fishes, metabolic rates have been estimated using respirometry methods to measure the rate of oxygen consumption. Metabolic rates are approximated based on the assumption that most fishes rely on a largely protein-rich diet, and that there should be less variability in the oxycalorific coefficient of food. Laboratory measurements of metabolic rates in sharks and rays show that individuals having undergone some acclimation have metabolic Q10s that vary widely (1.3–6.8), with species that exhibit typical (~2) and high (6.8) Q10s showing some degree of behavioral thermoregulation. This scenario has also been documented in some pelagic species. For example, free-swimming juvenile blue sharks tracked in the Gulf Stream spent the majority of their time diving to a significant depth (400 m), albeit still above the thermocline, experiencing a 91C temperature differential between surface waters and those at depth (Campana et al., 2011). It was hypothesized that by following these dive patterns these blue sharks may gain a metabolic advantage. Campana et al. (2011) estimated that the metabolic rate of the juvenile blue sharks exhibiting these dive patterns would decrease by 2.5 times (assuming a Q10 of 2.9) when compared to that of the same individual if it remained at the warmer surface. Moreover, that study argued that food resources in the surface waters would also be more limited than at depth, an additional benefit of spending more daytime hours at depth. Although no data exist on how temperature affects swimming oxygen consumption rate in regionally endothermic sharks, any prediction of the thermal effects on their energetics will be inherently complicated by their ability for physiological thermoregulation (see Section 2.5.). Lamnids are known to undergo seasonal migrations to higher latitudes and exhibit rapid and repeated diurnal sojourns to deeper (i.e., colder) waters (Weng et al., 2005; Domeier and Nasby-Lucas, 2008; Jorgensen et al., 2009; Del Raye et al., 2013). Despite the fact that lamnids frequent colder waters, their ability to warm swimming muscles will alter contractile function and, to a certain degree, may lead to a decreased thermal effect on swimming metabolism, as has been shown for some tunas (Carey and Teal, 1966; Dizon and Brill, 1979; Dewar and Graham, 1994). Taken together, laboratory studies on the metabolic rate in sharks and rays suggest that their thermal sensitivities are species-specific. Thus, the energetic benefits afforded by behavioral thermoregulation and thermal refuging (see Sections 2.3 and 2.4.) will be vastly different among species. For these reasons, there is a need to study the metabolic rates across ecotypes (e.g., active, sedentary, large, cold, endothermic) to elucidate how different species balance behavioral tradeoffs with physiological capabilities and adaptation limits.

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3. SWIMMING KINEMATICS AND ENERGETICS 3.1. Swimming In sharks, whole body undulatory swimming is powered by the myotomal muscles (see Chapters 5 and 6). The myoglobin-rich RM comprise approximately 2% of body mass and are recruited during continuous swimming relying on aerobic metabolic pathways to sustain contractions for prolonged periods of time (days–months–years). By contrast the myoglobin-poor WM, which comprise between 50% and 60% of body mass, are recruited during burst swimming and rely on anaerobic metabolic pathways to sustain contraction for brief periods of time (seconds). Because both continuous and burst swimming are powered by these myotomal muscles, any increase in the swimming speed will be correlated with elevated metabolic demands by the active muscles. There are several studies that show how the aerobic cost of locomotion (i.e., oxygen consumption rate) in sharks increases exponentially with swimming speed, a scenario commonly attributed to hydrodynamics were the drag forces increase with the square of velocity (Videler and Wardle, 1991; Videler, 1993). For this reason there is much interest in understanding what the relationship is between swim speed and the species-specific aerobic metabolism and what the optimal free-swimming speeds are for sharks of varying sizes in the field. To this end, new work using stationary underwater stereo-video cameras could be used to document, in a relatively simple manner, the free-swimming speeds of shark in the wild as they pass in front of the cameras field of view (Letessier et al., 2015). The quantification of swimming speed in captivity and the use of speedsensing transmitters attached to small sharks (e.g., lemon sharks) swimming in a water-tunnel respirometer have been used to extrapolate their laboratory-based swimming energetics to the field (Gruber et al., 1988; Bushnell et al., 1989; Carey and Scharold, 1990; Parsons and Carlson, 1998; Sundstro¨m and Gruber, 1998). There have been several other attempts to use speed-sensing acoustic transmitters on larger, mature sharks (e.g., +150 cm lemon sharks) to estimate the metabolic rates and derive fieldbased energy budgets (Gruber et al., 1988; Sundstro¨m and Gruber, 1998). Work on bonnethead sharks quantified their swimming speeds in an artificial lagoon using speed-sensing acoustic transmitters and documented their swimming energetics in a circular respirometer when subjected to different oxygen regimes (Parsons and Carlson, 1998). Under hypoxic conditions, bonnethead sharks in the laboratory swam significantly faster and increased their mouth gape (i.e., the capacity for ram ventilation) with an overall increased aerobic demand as a function of the increased

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swimming speeds. Thus, relative to the free-swimming speeds documented in the field, animals in captivity may not show representative swimming speeds due to the potential stress associated with confinement and the restrictive size of the experimental enclosures (Lowe, 1996; Parsons and Carlson, 1998; Sundstro¨m and Gruber, 1998). There are, however, significant limitations to this approach as (i) small or juvenile sharks cannot be tracked in the field using the speed-sensing transmitters due to the large size of the tags and (ii) large and mature sharks, that can be tracked in the field, are too large to be studied in a laboratory setting (Graham et al., 1990). Moreover, extrapolating metabolic rate data across a wide size range requires both mass-specific and temperature corrections, both of which are not well understood in sharks. Much like using heart rate (see Section 3.2.), the use of swimming speed to estimate the metabolism of free-swimming elasmobranchs in the field requires laboratory calibration and thereby limits the use of this technique in many of the larger or elusive species. 3.1.1. Tailbeat Frequency For sharks an increase in swimming speed is achieved by either an increase in tailbeat amplitude, TBF, and/or body wavelength (Webb and Keyes, 1982; Graham et al., 1990; Lowe, 1996). These changes in swimming kinematics positively correlate with the cost of locomotion when measured in captive individuals and may provide a reliable indicator of swimming activity (i.e., energetics) in the field (Stasko and Horrall, 1976; Briggs and Post, 1997; Lowe et al., 1998). To date, TBF can be recorded or transmitted using measurements of myotomal muscle electromyograms, using sonomicrometry to document body undulations, or by deploying an externally attached acoustic tag fitted with a reed switch on the caudal peduncle to detect lateral movement of the tail (Lowe et al., 1998; Donley et al., 2005; Bernal et al., 2010). By understanding the relationship between these kinematic variables, swimming speed and oxygen consumption rate under different thermal conditions, it is possible to estimate the costs of transport of animals in the field. Lowe (1996, 2001) found a positive relationship between TBF and oxygen consumption rates for juvenile scalloped hammerhead sharks exercised at different speeds and water temperatures in a large flume respirometer. However, comparisons in swimming kinematics between similar sized individuals exercised in the flume and in a semi-natural pond, indicated that sharks swim differently in the flume and had higher TBF and modulated TBA differently than free-swimming sharks in the field during slower straight-line swimming. At more elevated swimming speeds, kinematic parameters were more in congruence. Based on these performance measures, Lowe et al. (1998) developed a tailbeat

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acoustic transmitter that could be mounted on the caudal fin of the shark to transmit during each successive tailbeat. Juvenile hammerhead sharks were then tracked in the field over 24 h periods and their daily costs of transport was estimated using the relationship between TBF and water temperature (Lowe, 2002). While that work provided a detailed and comprehensive estimate of daily locomotory costs for juvenile scalloped hammerhead sharks, TBF alone is probably not the best metric for predicting metabolic rates as all laboratory derived kinematic parameters were measured during straight line swimming and free-swimming shark in the field rarely swim in straight line or at constant speeds and depths for prolonged periods of time. Therefore, using TBF alone will surely underestimate the actual locomotory costs, where fast-start and turning would not be well represented using only a tailbeat transmitter. Newer techniques such as accelerometry provide a much more comprehensive estimate of swimming exertion over varying swimming behaviors and speeds (Table 8.1). 3.1.2. Accelerometry Recently, more detailed information on swimming activity has been documented by attaching high frequency sampling (W30 Hz) three-axis acceleration dataloggers (ADLs) or acoustic accelerometers (e.g., Vemco V9AP transmitters) to aquatic animals (Tanaka et al., 2001; Yoda et al., 2001; Wilson and McMahon, 2006). Accelerometers, oriented in different axes, measure gravitational and dynamic (inertial) changes in tag position (i.e., body position) and can correlate cyclical changes in three-dimensional position with different levels of swimming activity (i.e., TBF) and swimming behavior (e.g., continuous vs. burst swimming). Recent work on sharks has also begun to provide new insights into how overall dynamic body acceleration (ODBA), a sum of all axes forces (yaw, pitch, and surge), may be closely correlated with oxygen consumption (swimming energetics) (Wilson and McMahon, 2006; Gleiss et al., 2009a,b; Halsey et al., 2009; Whitney et al., 2012). This approach is opening the door to integrate laboratory-based respirometry and accelerometry to more accurate estimates of field-based energetic costs (Whitney et al., 2012). There have been a growing number of studies using ADLs affixed to larger sharks to characterize dynamic forces associated with swimming and other behaviors. Whitney et al. (2007) attached ADLs to the non-obligate ram-ventilating reef white tip to quantify the frequency and duration of activity of individuals in semi-natural enclosures. The ADLs enabled them to clearly identify periods of activity and inactivity and showed that sharks were still nocturnally active despite being regularly fed during the day in captivity. Gleiss et al. (2009a) used ADLs attached to lemon sharks to

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characterize four different swimming behaviors (resting, initiation of swimming, steady swimming, and fast-start swimming) in a semi-natural lagoon. Mating behavior in nurse sharks (Ginglymostoma cirratum) has been identified using ADLs by measuring changes in angle and orientation associated with mating and copulation (Whitney et al., 2010). While ADLs have been useful in quantifying periods of activity, changes in swimming behavior, and other behaviors, establishing a link between accelerometry and energetic costs has proved to be more difficult. Because sharks are negatively buoyant, forward swimming is required to maintain hydrostatic equilibrium. In fish, ADLs incorporating pressure (depth) sensors have been used to estimate potential energy saving changes in swimming behavior – referred to as “swim-and-glide” patterns of movement. Unlike “yo-yo” diving behavior in fish, which consists of repeated and steep movements, powered by swimming, between shallow and deep water, the swim-and-glide swimming pattern is characterized when a negatively buoyant fish swims upwards (at a steep angle) in the water column and then ceases to swimming (body undulation stop) and glides downward through the water column at a lesser angle (Weihs, 1973; Whitney et al., 2012). Gleiss et al. (2011) attached an ADL and pressure sensor to whale sharks in the field and found a greater ODBA during the ascents. This higher ODBA coupled with the steeper angle of swimming suggests that upwards trajectory requires greater force exertion relative to the gliding (lower ODBA) phase, which was sustained for longer distances and had a shallower angle of the swimming trajectory. Even though for most fishes there has been no direct measure of the relationship between ODBA and metabolic rate (i.e., oxygen consumption), it is highly likely that this swimming behavior translated into considerable energy savings. Work on tiger sharks (Galeocerdo cuvier) using ADLs with depth sensors and forward-facing videologgers shows that individuals rarely glided during descents and were actively swimming up and down through the water column (Nakamura et al., 2011). Unlike the potential cost savings of swimand-glide, the more energetically expensive yo-yo diving behavior in the tiger shark may be important for navigation or the location of prey in areas where the shark interacts with a complex bathymetry or encounters steep vertical thermal gradients. Despite the growing utility and more comprehensive measure of swimming related forces (e.g., ODBA), the use of ADLs to quantify the energetic costs of locomotion in the field remains limited due to the challenges of measuring oxygen consumption rates (metabolic rate) of sharks. Thus, little has been learned about the relationship between ODBA and a measure of energy expenditure. This has been largely due to the inherent limitation of the ADLs (their size and placement) and the inability

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to deploy these tags on smaller animals that can then be studied under controlled conditions (e.g., metabolic rates measured across a wide range of swim speeds). Moreover, because ADLs must be externally attached to the animal to allow for logger recovery, these packages can add drag and thereby increase the cost of locomotion. For this reason, the smaller the ADL package relative to the overall size of the shark the lesser the potential energetic impact, and additional comparisons across size ranges on individuals should consider the relative effects of drag. Work by Gleiss et al. (2010) attempted to directly measure the costs of ODBA using a small ADL on juvenile scalloped hammerhead sharks swimming in a flume respirometer (both the flume and experimental design used were the same as those used previously on juvenile hammerheads; Lowe, 1996, 2001). Since only yaw and pitch vectors were used in the dynamic body acceleration analysis, Gleiss et al. (2010) only measured partial dynamic body acceleration (PDBA). Although a positive linear relationship was documented between oxygen consumption and PDBA, the swimming speeds of these sharks were limited and not sufficient to allow for an accurate back calculation of standard metabolic rate (metabolic rate at zero velocity). In addition, free-swimming sharks fitted with ADLs in both large tanks and shallow ponds had a mean lower PDBA when compared to similarly sized sharks swimming at minimal cruising speeds in the flume. These findings suggest that it is likely that the flow dynamics of the flume and the hydrodynamics of the cephalofoil of the hammerheads may affect their swimming performance in the flume resulting in higher observed energetic costs than would occur when swimming at comparable speeds in the field (Lowe, 1996, 2001, 2002; Gleiss et al., 2010). Although these results are not unexpected, the use of ADLs clearly provides a more accurate proxy for the cost of swimming than previous metrics such as TBF, as swimming speed can vary by modulating TBF and tailbeat amplitude. Thus, the use of ODBA can provide a more comprehensive measure of swimming related forces over changes in velocity and can better represent the costs incurred during acceleration/deceleration, turning, and burst swimming. However, new approaches are needed that will allow for the field-based measurement of oxygen consumption rates without the use of flumes or annular respirometers. Improvements in fiberoptic oxygen probes and miniaturization of circuits may eventually allow for incurrent (buccal)/outcurrent (gill slit) measurements of oxygen differential, that in combination with ADLs, will provide a platform to directly link the oxygen consumption rates with ODBA under normal and varied swimming behaviors. As the cost of ADLs continues to decrease their deployment in the field will continue to increase. However, the inherent logistical challenges of using this technology still remain, for example, the ADLs need to be physically

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recovered (must detach from the shark) to allow for the data to be downloaded. Therefore, the packages must be attached externally, which likely affects the swimming behavior of the shark due to increased drag and skin irritation. In addition, it remains important to account for the costs of carrying the tags, particularly on smaller animals, as instrumented sharks show an increased cost of transport (25–35% higher) relative to those without transmitters (Scharold et al., 1988; Lowe, 2002). 3.2. Heart Rate During the last several decades there has been a growing understanding of cardiac function in fish, with most work being conducted on teleosts (Farrell, 1991; Farrell and Jones, 1992). Unfortunately, work on sharks has lagged far behind and what is known can be mostly attributed to work on small or juvenile species that are easily held in captivity. There have been several attempts to study heart function in larger sharks, but in those cases the laboratory has either gone out to sea or small individuals have been brought back to the laboratory for relatively short (hours) periods of time. Thus, most of what is known on the hearts of sharks comes from morphological and biochemical analyses of frozen or preserved samples (Tota et al., 1983; Emery, 1985; Emery et al., 1985; Farrell and Jones, 1992; Bernal et al., 2003) with opportunistic laboratory work using electrophysiological techniques and a limited number of work on live fibers or in situ hearts (Brill and Lai, 2015; Brill and Bushnell, personal communication). Unfortunately, it remains difficult to study heart function in free-swimming sharks, and even more logistically challenging in the larger species. Nonetheless, there have been several attempts to work on the in vivo heart function in the field by using acoustic telemetry, echocardiography, or by instrumenting freshly captured sharks aboard a ship or when they are immediately transported back to the laboratory (Lai et al., 1989, 1990a,b). Field work on sharks has measured their heart rate by implanting electrocardiogram leads into freshly captured specimens that are either restrained on deck (not swimming) or forced to swim in portable flumes (e.g., Lai et al., 1997). While these techniques offer a direct readout of the waves of myocardial depolarization and repolarization (changes in electrical potential: PQRS) and can be used to determine changes in beat frequency they do not provide stroke volume and thus cannot be used as a measure of cardiac output (Farrell and Jones, 1992). Work on sharks shows that heart rate is in the mid-range for fishes (Farrell and Jones, 1992) and appears to be both species-specific and linked to the levels of swimming activity. For example, echocardiograms in live restrained sharks at a similar temperature

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(18–201C) showed that the resting heart rate (beats per minute, bpm) of the sedentary swell shark (Cephaloscyllium ventriosum) (~21 bpm) is markedly lower than that of the shortfin mako shark (~34 bpm) (Lai et al., 2004). Data for sharks swimming in a flume while instrumented with ECG leads show that swimming speed significantly affects heart rate (i.e., leopard sharks resting approximately 36 and 47 bpm when swimming at 0.8 lengths/s; Scharold et al., 1988) with mako sharks having among the highest heart rates documented, so far, for sharks (78 bpm when swimming at 0.45 lengths/s; Lai et al., 1997). Temperature also has a direct effect on heart beat frequency. In spiny dogfish resting heart rate doubles between approximately 81C (19 bpm) and 151C (40 bpm) and in sandbar sharks the heart rate of immobilized individuals has a Q10 of ~2.2 (18–281C) (Dowd et al., 2006). The use of ECG acoustic transmitters, which integrate the electrical signal of cardiac contraction and consequently emit an acoustic signal with every heart beat have also been used in both laboratory and field experiments in an attempt to find the relationship between heart rate and metabolic rate. The first laboratory-based attempts to use this technology were on instrumented leopard and lemon sharks swimming in a flume at a range of aerobic swimming speeds (Scharold et al., 1988; Scharold and Gruber, 1991). Those findings show that heart rate significantly increased with swimming speed but that there was high variability between heart rate and oxygen consumption, with heart rate accounting for only 32% of the rise in oxygen consumption. Similarly, work on juvenile lemon sharks swimming at voluntarily speeds in an annular respirometer show that heart rates also significantly increased with swimming speed, but that heart rate only accounted for 18% of the rise in oxygen consumption (Scharold and Gruber, 1991). Taken together, for leopard and lemon sharks changes in heart rate appear to make a relatively small contribution to the degree of oxygen consumption, suggesting that increases in stroke volume and/or arteriovenus oxygen differences are the major components of changing oxygen consumption with increased swimming activity (Scharold et al., 1988; Scharold and Gruber, 1991). Indeed, work on resting and swimming leopard sharks in a flume also found that changes in stroke volume appeared to govern cardiac output in this species (Lai et al., 1989). For these reasons, heart rate could not be considered to be an adequate indictor of metabolic rate in these two species, and no field experiments were conducted. Based on morphological similarities in the hearts of most all ectothermic sharks, it has been suggested that ectothermic species exhibit this type of cardiac response (i.e., changes in stroke volume dominate cardiac output) (Emery, 1985; Farrell, 1991; Tota and Gattuso, 1996). However, a different scenario may be present for sharks that are capable of regional endothermy.

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Specifically, work on the cardiac function of mako sharks indicates that the morphology of their hearts (e.g., thick ventricular walls with high proportion of compact myocardium, well developed coronary circulation) resembles more that of tuna, and even mammals, than that of other sharks (reviewed by Bernal et al., 2001a). In addition, work on restrained makos shows that changes in cardiac output are governed by changes in heart rate and that stroke volume appears to be nearly fixed (Lai et al., 1997). Thus, unlike ectothermic sharks, documenting the heart rate of shortfin makos (i.e., lamnid sharks) may provide an adequate field indicator of metabolic rate. However, the relationships between heart rate and swimming speed and between heart rate and oxygen consumption for these sharks remain unknown. The feasibility of measuring heart rates (via biotelemety or biologging) in a laboratory setting and in the field makes this variable of particular interest for future work. However, there is a need to fill the gap in the understanding of the role that heart rate plays in cardiac output and how heart rate may correlate with oxygen consumption (i.e., metabolic rate) in sharks that vary (intra- and inter-specifically) in size, swimming activity, ambient temperature, and the capacity for regional endothermy. The development and deployment of the latest technologies, such as acoustic transponders, underwater listening stations, and satellite telemetry, along with improvements in captive animal husbandry will eventually allow the study of the bioenergetics in more active and pelagic species. 3.3. Feeding and Digestion Although the use of tracking technologies have allowed for a better understanding of the movement and activity patterns of sharks in the field it remains challenging to document how they respond to changes in environmental conditions and to quantify key feeding behaviors (e.g., foraging, prey chase, capture, ingestion) and the associated physiological processes (i.e., digestion and assimilation) (Bucking, 2015). Historically, characterization of feeding frequency, chronology, and diet of sharks requires the capture, sacrifice, and the analysis of stomach content for hundreds or thousands of individuals that are caught in different locations, during different seasons, and at different times of day coupled with knowledge of prey abundance and availability (Corte´s et al., 1996; Corte´s, 1997). More recently, the use nonlethal gastric lavage techniques have been used to collect the stomach contents of sharks (e.g., Bush, 2003). While both of these methods can be used to estimate the state of digestion (a proxy for the time of ingestion) and calculate feeding frequency by documenting the varying stomach fullness relative to the time of day (Corte´s, 1997;

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Wetherbee and Corte´s, 2004; Corte´s et al., 2008), they do have important limitations, as individuals can only be sampled once and the invasive nature of the procedure may affect their behavior. Moreover, appropriate interpretation of these methods requires an understanding of the physiological processes involved in digestion and assimilation, information that has generally been lacking in sharks (Papastamatiou, 2007). Field movement data for many species of sharks have shown crepuscular or nocturnal peaks in activity, which have been hypothesized to be associated with foraging behavior. Stomach content analyses of sharks, however, have not shown these times of high activity to correspond to periods of feeding success. In fact, most diet studies suggest that sharks are feeding opportunistically, and therefore lack any distinct diel periodicity (Corte´s, 1997; Wetherbee and Corte´s, 2004; Corte´s et al., 2008). While it has been possible to estimate the feeding frequency for some juvenile sharks (e.g., 11 h for scalloped hammerhead sharks, Bush, 2003; 33–47 h for lemon sharks, Corte´s and Gruber, 1990; and 95 h for sandbar sharks, Medved et al., 1985), little is known about feeding frequencies of adult sharks as field work is particularly difficult. For this reason, there is a need to use remote sensing techniques that document actual feeding events that extend beyond sole estimates of activity or movements. Studies on captive sharks show that their digestive processes vary interspecifically and are most likely associated with their activity levels and ecology (Papastamatiou and Lowe, 2005). To date there is laboratory-based evidence that both temperature and diet composition affect the rate of food passage in many species (Medved, 1985; Corte´s and Gruber, 1990; Corte´s, 1997; Wetherbee and Corte´s, 2004; Wallman and Bennett, 2006; Di Santo and Bennett, 2011a), but there are few studies that have been able to document this in wild free-swimming sharks. The digestion, in the muscular stomach, of an ingested meal undergoes both chemical and a mechanical breakdown resulting in a chyme slurry before passing into the spiral valve intestine. Hydrochloric acid secreted by the oxynticopeptic cells of the gastric lining upon gastric distention of food entering the stomach lowers pH, which enhances the chemical breakdown of hard structures and activation of proteolytic enzymes (Papastamatiou, 2007; Corte´s et al., 2008). This change in pH associated with food entering the stomach has been proposed as a traceable signal that could be remotely monitored in freeswimming sharks to determine the periodicity of feeding events (Fig. 8.5). Serial sampling of gastric fluid pH values from captive leopard sharks after they were fed a meal of squid showed that pre-prandial gastric pH was initially low (~1.7), but rapidly increased (~3.5) following meal ingestion (~1 h) and then decrease back to pre-prandial levels within 12–24 h and remained low even after stomach clearance (up to 96 h) (Papastamatiou and

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Time (days) Figure 8.5. Gastric pH (black line) and gastric temperature (gray line) profiles for sharks fed a pH/temperature sensing datalogger in captive setting. (A) Nurse shark (28 kg, male) and (B) blacktip reef shark (21 kg, female). Feeding events shown by arrows detailing the meal size (% of body mass) and the meal type (S: squid; M: mackerel; RF: reef fish). Unknown natural feeding event observed in the blacktip shark (?). Plots are redrawn from Papastamatiou and Lowe (2005) and Papastamatiou et al. (2007b).

Lowe, 2004). A comparison of these gastric pH trends to those continuously measured for up to 10 days in captive adult sharks that were fed an autonomous in situ gastric pH/temperature datalogger (earth & Ocean Technologies) showed a similar pH pattern following ingestion of meals (Fig. 8.5). However, comparable tests on captive nurse sharks showed a different pattern of pH change following meal ingestion. Unlike leopard sharks, nurse sharks gastric pH returned to more neutral pH upon gastric clearance or oscillated between neutral and low pH (Papastamatiou and Lowe, 2005) (Fig. 8.5A). These different patterns of fasting gastric pH can be potentially attributed to differences in natural feeding periodicities between these species. Active foraging species such as leopard sharks are thought to feed daily (Kao, 2000) and likely maintain a low gastric pH in order to ready the gut for regular feeding events. By contrast, less active species such as nurse sharks, which may only feed weekly, could potentially not need to maintain a low gastric pH, but periodically lower it to eliminate

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harmful bacterial growth in the stomach between more widely spaced feeding events (Papastamatiou and Lowe, 2005; Papastamatiou, 2007). While the use of pH sensing dataloggers allow for the measurement of feeding events and also provide new data on the magnitude of the pH change over time, which appear to be related to meal size, the use of this technology is limited as the pH dataloggers need to be recovered from sharks following natural regurgitation or by gastric lavage. However, integration of pH sensors into acoustic transmitters can provide real-time information on timing of feeding events, size of meals, and other associated behaviors such post-prandial thermoregulation. To date, captive experiments using gastric pH dataloggers have increased our understanding of the digestive processes and feeding periodicities of several species of sharks, but little is known on the feeding frequency in the wild under natural conditions. A new generation of gastric pH acoustic transmitter (e.g., Vemco Ltd.) that can telemeter real-time changes in gastric pH for up to 14 days has been deployed in adult reef blacktip sharks held in a semi-natural pond (Papastamatiou et al., 2007a). Sharks were fed the gastric pH-sensing transmitter and then different meal sizes of squid, reef fish, or mackerel, in addition, some sharks were also fed a stomach motility/ temperature-sensing datalogger (earth & Ocean Technologies) that uses a piezo-electric film to measure changes in gastric muscle contraction associated with mechanical digestion and movement of chyme from the stomach into the spiral value intestine. Motility/temperature datalogger retentions of 4–13 days provided continuous measures of gastric motility over multiple feeding periods and, similar to leopard sharks, changes in gastric pH following meal ingestion were proportional to meal size (regardless of meal type), and showed an increase in pH with meal ingestion, followed by a more gradual decline to a fasting (pre-meal) level pH (Fig. 8.5B). Gastric motility peaked approximately 7–12 h following meal ingestion and meal type appeared to only influence motility during the first 24 h. Meals of softer more collagenous prey (squid) resulted in lower overall stomach motility than that of harder, boney prey (mackerel and reef fish). Stomach temperature also had a significant effect on motility during the first 7 h of digestion, although stomach temperature changes were relatively small (o21C) and corresponded to diel changes in water temperature. The positive effects of temperature on gastric motility further emphasizes how individuals that behaviorally thermoregulate may move to warmer water temperatures following a meal to either increase the rate of passage, which could potentially reduce assimilation efficiency but increase resumption of appetite, or move to cooler water (see Section 2.4) to slow down rate of passage, which could increase assimilation efficiency (Sims et al., 1996; Hume, 2005; Papastamatiou, 2007; Corte´s et al., 2008). Unfortunately, all feeding and

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digestion experiments to date have been on captive individuals in relatively small lagoons which have likely not allowed sharks to select specific thermally structured habitats that may influence rates of digestive processes. Although using gastric pH sensors as a remote indictor of feeding in freeranging sharks holds some promise, there are distinct challenges and limitations with using electrolytic pH probes in dataloggers or transmitters that has likely prevented their use in field studies. Unfortunately, glass pH probes are both fragile and susceptible to erosion by extremely low stomach pH values (e.g., pH~ 0.1 in sharks), reducing the capacity to reuse the datalogger or transmitters. Like most electrolytic pH probes, sensor drift is a technical reality and because underwater pH probes require a pressure compensated electrolyte chamber, their accuracy is unreliable after approximately 14 days of use (Papastamatiou and Lowe, 2004, 2005; Papastamatiou et al., 2007a,b). Meyer and Holland (2012), however, developed and tested a conductivity/temperature-sensing gastric datalogger that could also be fed to free-swimming sharks to characterize feeding and digestion (Fig. 8.6). This device uses two stainless steel electrodes on the surface of the datalogger to measure changes in bulk electrical impedance associated with HCl secretion and ingestion of seawater with a meal. This datalogger was fed to a captive tiger (217 cm TL) and a sandbar shark (191 cm TL) held in a semi-enclosed lagoon and were retained in the stomachs for periods between 8 and 22 days, allowing for the recording of multiple feeding events of different ration sizes. Ingestion of food and seawater resulted in a rapid drop in electrical impedance of gastric fluid in Feeding event (3.8 kg)

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both species, which was maintained for approximately 7–13 h (Fig. 8.6). This period of time was similar to the lag time in gastric motility observed in blacktip reef sharks (Papastamatiou et al., 2007b) and is believed to be attributed to a phase of digestion where the meal is being steeped in gastric acid, seawater, and proteolytic enzymes. Following this lag period was a gradual, but significant rise and highly variable impedance lasting up to 24 h, before rapidly dropping. This pattern was suggested to be associated with a chyme phase of digestion whereby there is a peak in stomach motility increasing mechanical breakdown of the meal to a fully mixed acidic slurry. The rapid decline in impedance following this stage is believed to be associated with the movement of the chyme from the stomach and into the duodenum where impedance measurements are comparable to a fasting state (Fig. 8.6). While there were no simultaneous measurements of gastric pH, motility, or physical indication of digestive stage of food in these animals, the patterns of gastric fluid impedance seem to closely match patterns observed in better calibrated gastric pH and motility experiments (Papastamatiou and Lowe, 2004, 2005; Papastamatiou, 2007). Unlike the problems associated with glass pH probes, this sensor technology holds great promise for field use on free-ranging sharks because of the stability of the sensor. Although more controlled captive trials are needed to adequately calibrate this technology, this sensor type could readily be incorporated into an acoustic transmitter for real-time acquisition of feeding behavior or incorporated into a satellite transmitter for in situ storage and the data retrieval after regurgitation. Coupling this technology with ADLs and videologgers would provide far more detailed information on feeding behavior of free-ranging sharks, but because of the size of the technology, would probably be limited to larger animals.

4. A CASE FIELD STUDY: THRESHER SHARKS The three species of thresher shark (family Alopiidae) are a unique group of pelagic sharks that are easily recognized by the extremely elongated upper lobe of their caudal fin, which approaches the length of the trunk of the body. Most of what is known about threshers has resulted from opportunistic catches by scientists and fishery-dependent catches by commercial fishermen. Although this has led to a growing knowledge of their geographical distributions and numerous aspect of their biology (e.g., morphometrics, reproduction) and ecology (e.g., diet composition) little is known about their physiology, as threshers cannot be kept in captivity and their large size, need for continuous swimming, and elusive nature make

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them extraordinarily difficult to study in the laboratory. Thus, up until the late 1990s, what was known about threshers came from the study of dead specimens, from tissues samples, and from catch (or bycatch) data. 4.1. The Role of the Caudal Fin Despite distinct morphological and ecological differences among the three species (see below), the functional role of the unifying thresher trait, the long caudal fin, was until recently, unknown. It was assumed, based on the prey items collected in the stomach and fisheries-related data showing individuals being frequently hooked in the tail, that the caudal fin was used during prey capture (Allen, 1923; Gubanov, 1972; Stillwell and Casey, 1976; Preti et al., 2001; Nakano et al., 2003; NOAA, 2009; Heberer et al., 2010; Sepulveda et al., 2015). The earliest description of a feeding event in a freeswimming thresher was poetically documented by Allen (1923) “the thresher shark passed partly ahead of the victim (probably half its own length) when it turned quickly and gave the coach-whip lash with the tail y the victim was much confused.” This feeding behavior was not confirmed until field work using videologging documenting free-swimming feeding events showed that the caudal fin of the common and pelagic thresher is used in the pursuit and capture of prey with caudal fin slaps that can whip the tail at speeds of up to 35 m s 1 (Aalbers et al., 2010; Oliver et al., 2013). Although the elongated caudal fin appears to play a key role during feeding, acting as an appendage to stun prey before being consumed, there has been no work on the effects such a long tail may have on swimming kinematics and energetics.

4.2. RM Morphology The superficial similarities in the overall body morphology among threshers are striking; however, recent laboratory work has shown that the internal architecture of the swimming muscles and the vascular layout perfusing the RM are markedly different. While the RM position of both pelagic and bigeye thresher sharks is similar to that of most all other sharks (superficial RM; located directly under the skin) the RM of the common thresher is in a medial position and forms a piston-like structure that is distributed predominantly toward the anterior of the body (Sepulveda et al., 2005) (Fig. 8.2). Moreover, the vascular supply to the RM in the common threshers relies on large lateral vessels that give rise to putative countercurrent heat exchangers (Bone and Chubb, 1983; Patterson et al., 2011). Both of these anatomical specializations were only known previously to exist in lamnid sharks and tunas.

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4.3. RM Uncoupling and Swimming Mode The understanding of the functional role of RM position (medial vs. superficial) during swimming in sharks has relied on short-term laboratory work in a flume to document the swimming biomechanics in small or juvenile specimens (Donley and Shadwick, 2003; Donley et al., 2004). For sharks (and other fishes) with a superficial RM position, contraction of their RM is in phase with local body bending, such that RM contractions result in bending of the body at that position (Katz and Shadwick, 1998; Katz et al., 2001; Donley and Shadwick, 2003). In contrast, the medial RM of lamnid sharks appears to be mechanically uncoupled from the surrounding WM, which results in shearing between these two muscle groups during sustained swimming and allows large tendons to transmit forces from the anteriorly located RM toward the tail (Shadwick et al., 1999; Bernal et al., 2001a; Donley et al., 2004; Syme and Shadwick, 2011). This morphological adaptation effectively uncouples the RM from local body bending and thus separates the area of the body which produces force from that which undergoes lateral, thrust-producing movements and minimizes the degree of lateral undulation by the anterior body, thereby reducing drag and providing a potential biomechanical advantage for performance at sustained, aerobic cruise swimming speeds (reviewed by Syme and Shadwick, 2011). As opposed to sharks with a superficial RM position, which undergo pronounced whole-body undulations during sustained swimming, the unique RM-tendinous complex in lamnids allows thrust production to be primarily concentrated in the caudal area and to be driven mainly by caudal oscillations, the hallmark of “thunniform swimming mode” (Magnuson, 1978; Donley et al., 2004). All lamnid sharks are highly mobile and share a suite of morphological and physiological adaptions (e.g., fusiform body, caudal keels, lunate caudal fin, medial RM position) that allow for high performance swimming (Bernal et al., 2001a). Thus, the presence of lamnid-like medial RM in the common threshers could potentially allow RM/WM decoupling and translate to a decrease in whole-body undulations during sustained swimming. However, the body design of the common thresher is not only unlike that of lamnids (e.g., not fusiform, lacking caudal keels), but their caudal fin morphology is a radical departure from a lunate caudal anatomy exemplified by the thunniform swimmers. Past work has classified the swimming mode of thresher sharks as subcarangiform, wherein the degree of body bending increases rapidly toward the posterior half of the body during cruise swimming (Webb and Keyes, 1982; Webb and Blake, 1998). This designation of swimming mode has solely been based on their body shape, as experimental work on their swimming biomechanics in the laboratory

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were, at that time, not possible. Nevertheless, the radically different RM position among the thresher species (i.e., superficial in pelagic and bigeye vs. medial in the common thresher) may result in different swimming biomechanics even with the remarkable similarities with their external body and fin morphologies. For these reasons any attempt to document the presence of lamnid-like RM mechanics and to assess the swimming mode of the common thresher had to take the laboratory to the sea and work on live specimens. Recent field work on common threshers that were quickly captured and brought alongside the boat to allow the study of RM function using sonomicrometry to document RM strain and changes in the phase of RM contraction offered evidence of RM uncoupling (Bernal et al., 2010). Thus, the medial RM of the common thresher appears to be mechanically similar to that of lamnids; however, a cursory video analysis of the threshers swimming alongside the boat did not reveal a thunniform type of swimming mode (high body undulations were present during sustained swimming). It is thus possible that relative to thunniform swimmers, the extremely elongate caudal fin of threshers alters both the hydrodynamics of swimming and results in significant differences in swimming kinematics between these groups, despite the shared RM anatomy (see Syme and Shadwick, 2011). 4.4. RM Endothermy and Thermal Distributions Although RM uncoupling in lamnids and the common thresher may ultimately offer a potential biomechanical advantage, the medial position of the RM in both of these groups is also associated with a specialized vascular arrangement. Field and laboratory work on lamnids has shown their capacity for RM endothermy (see Section 2.5.); however, only morphological evidence on the presence of putative RM heat exchangers existed for common thresher sharks (Bone and Chubb, 1983). Recent field work using acute thermal probe penetrations documented the presence of RM thermal excess in the common threshers (Bernal and Sepulveda, 2005) but not in the other two thresher species (Patterson et al., 2011). Thus, in addition to the mechanical benefit of a medial RM position in the threshers, which may offer a biomechanical advantage despite the threshers not adopting a stiff-bodied, thunniform swimming, an added benefit of this morphological uniqueness is an increased RM temperature that will potentially safeguard muscle performance when exposed to cold water (see Section 2.5.1.1.) and ultimately affect their capacity for sustained swimming. Fishery catch data and recent field work using acoustic telemetry and satellite tracking show that threshers are distributed circumglobally, with the pelagic thresher (Alopias pelagicus) being the most tropical and the

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common and bigeye thresher geographically overlapping in more temperate waters (reviewed by Bernal et al., 2009). More detailed acoustic tracking data show that relative to the common and pelagic threshers, the bigeye thresher routinely dives to greater depths and enters higher latitudes and has the greatest thermal tolerance, being able to penetrate cold (6–101C), and often hypoxic, waters for extended periods of time (6–8 h) (Nakano et al., 2003; Weng and Block, 2004; Cartamil et al., 2010, 2011; Bernal et al., unpublished data). For bigeye threshers, exposure to cold temperatures for prolonged periods of time will inevitably lead to a low RM temperature that may ultimately impact RM function. However, ongoing work on freshly excised RM fiber bundles from bigeye threshers show that even while the cycle frequency (i.e., potential TBF) that results in the most power decreases markedly between 241C (~0.51 Hz) and 81C (~0.27 Hz) the ability to maintain positive power during shortening is maintained even at cold temperatures (Bernal and Sepulveda, personal observation). By contrast, the RM of the common thresher (and lamnids) shows that a decrease in temperature has a dramatic detrimental effect on the RM if it cools slightly below its in vivo operating temperature (see Chapter 5) (Bernal et al., 2005; Donley et al., 2007, 2012). Therefore, the thermal effects on bigeye thresher RM contraction are not as significant as those in the regionally endothermic common thresher. Moreover, relative to other ectothermic sharks (e.g., leopard shark) where muscle function is still possible below 151C, albeit at low cycle frequencies, but not likely below 81C, bigeye threshers RM continue to function at much colder temperatures (Donley et al., 2007). While regional RM endothermy enables the common thresher (and lamnids) to maintain a warm RM temperature when exposed to cool ambient conditions (Fig. 8.3A) and may ultimately safeguard muscle function during dives or when migrating to higher latitudes, the physiological specializations present in bigeye thresher that allow them to penetrate very cold waters, which are often well within the midwater oxygen minimum zone (below 1.5 mL O2 L 1), for extended periods of time and still maintain RM and cardiovascular function remain unknown. Recent morphological work on the gills of the three thresher species shows that bigeye threshers have the largest gill surface area and that the pelagic and common thresher sharks have similar gill areas, despite the expected higher aerobic demands associated with regional RM endothermy in the common thresher (see Chapter 3) (Wootton et al., 2015). While the unusually large gill area in bigeye threshers is likely associated with its ability to tolerate prolonged exposure to hypoxia there are no data on other important physiological adaptations (e.g., blood–oxygen binding affinity and thermal effects, muscle vascularization, and ultrastructure) that may shed insight

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into how bigeye threshers are capable of sustaining their aerobic demands under these potentially limiting environmental conditions. Taken together, the study of this uniquely specialized group of sharks shows the importance of field work and how field work is the platform on which to increase our understanding of their eco-physiology. Development of new laboratory tools and field telemetry/biologging techniques will allow a more thorough understanding of the evolution and performance abilities of these sharks as they experience a changing ocean climate.

5. FUTURE DIRECTIONS IN FIELD PHYSIOLOGY The development of new technologies to collect environmental and physiological data in the field and captivity has clearly opened up new opportunities to examine the eco-physiology of sharks. However, due to the large costs associated with all aspects of captivity (e.g., specimen collection and husbandry, building large facilities) it remains unlikely that, in the near future, aquaria (research or public) will actively seek to collect large, often elusive, elasmobranchs and allow scientists unimpeded access to conduct experimental work. Remarkably, some aquaria around the world have succeeded in keeping unique specimens in captivity (e.g., white sharks, whale sharks) but even the least invasive experimentation on these unique, or hard to find, elasmobranchs seems out of reach. Moreover, if the opportunity should arise and sharks are available for physiological work in captivity, there are key limitations imposed by the inherent experimental tools used (e.g., chambers, electronics) as they need to be in the correct location, be the right size, have adequate power requirements, and have the capability to control environmental parameters. For these reasons, taking the laboratory to the field (however difficult that may be) remains the best approach. Physiologist should not be timid about attempting to work with elasmobranchs in the wild, but rather rise to the challenge of setting up field-based laboratories and developing or adapting new data collection tools, and not be afraid to fail. While there is still a need to engineer smaller, more precise sensors that can simultaneously measure and transmit or log important physiological (e.g., blood gases and pH, locomotor muscle activity, heart rate, and tissue temperatures) and environmental (e.g., depth, temperature, pH, dissolved oxygen) variables from wild, free-swimming sharks, there is still a need to, first, go to the field and find the sharks. In addition, the recent development of autonomous underwater and surface vehicles will not only change how data will be collected from instrumented animals but also improve our ability to resolve how animals move through

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highly dynamic environmental conditions. Coupling these tools with fieldbased laboratories will provide a better understanding on how some of these species adapt and cope with changing oceanographic regimes. In addition, large aquaria and large captive holding facilities will potentially offer opportunities to calibrate techniques under controlled conditions for large, historically unstudied species.

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INDEX Note: Page numbers followed by “f ” and “t” refer to figures and tables, respectively. A ABR, see Auditory brainstem recording Acanthodians, 2–3, 9–10, 12–13 Acceleration dataloggers (ADLs), 349 Accelerometry, 349–352 Acoustic telemetry, 315 Actinopterygians, 158 Active metabolic rates (AMRs), 237t Adelphophagy, 267, 268 ADLs, see Acceleration dataloggers ALLN, see Anterior lateral line nerve Alopias pelagicus, see Pelagic thresher Alopias superciliosus, see Bigeye thresher sharks Alopias vulpinus, see Thresher sharks Alopiidae, see Thresher sharks Amacrine cells, 28–29 Ambient water temperature, 316 Ampullary organs, structure and spatial sampling of, 40–42 AMRs, see Active metabolic rates Anaerobic metabolism, 193–194 Anterior lateral line nerve (ALLN), 40–41 Aplacental viviparity, 262 Arch levator muscles, 158–159 Arterioarterial vasculature, 114–115 Atlantic stingray (Dasyatis sabina), 138–139, 140f Auditory abilities, 38–39

Auditory and vestibular systems of elasmobranchs, 33–34 auditory abilities, 38–39 inner ear, 34, 35f auditory requirements and predatory ability, 36–37 macula, 36 otolithic organs in elasmobranchs, 34–36 vestibular control, 37–38 Auditory brainstem recording (ABR), 38 Autonomous underwater vehicles (AUVs), 316 Axial variation, 206–207

B Bamboo sharks (C. plagiosum), 174 Basket-like formation, 200 Basking shark (Cetorhinus maximus), 143 gill rakers, 145f Batoids, 159, 177 fishes, 224–225 BCs, see Blood channels Behavioral thermoregulation, 322 adult female elasmobranchs, 325 in aggregating species, 323–325 characterization and confirmation, 323 field-based studies, 326 leopard shark, 324f

379

380

INDEX

Bigeye thresher sharks (Alopias superciliosus), 333–334 Biologging, 315–316 Biomechanics filter feeding, 177–178 prey capture, 168f bite feeding elasmobranchs, 173–174 feeding sequence phases, 167–170 motor activity pattern of muscles, 169f suction feeding elasmobranchs, 171–173 synchronized means of kinematic and motor patterns, 169f prey processing and transport, 176–177 upper jaw protrusion, 178–180 Biotelemetry, 315–316 Bite feeders, 166–167 Bite feeding elasmobranchs, 173–174, see also Suction feeding elasmobranchs Bite forces, 173, 174 Blood channels (BCs), 122f Bony fishes (Grade Teleostomi), 107–108 Bradyodonts, 8 Branchial arches, 154 Broadnose sevengill shark (Notorynchus cepedianus), 138–139 C C. griseum, see Chiloscyllium griseum C. plagiosum, see Bamboo sharks C. taurus, see Carcharias taurus Calcitonin, 294 Calcium homeostasis, 203–204 Canal neuromasts, 46–47 Candle, 262–263 Carbon dioxide (CO2), 239 Carcharhinus amblyrhynchos, see Gray reef sharks Carcharias taurus (C. taurus), 268 Caudal fin, 360 Center of mass (COM), 226–227 Central nucleus, 57–58 Cephalurus cephalus, see Lollipop catshark Ceratohyal–basihyal complex depression, 171 Cerebellum, 60–62 Cerebrotype, 69 Cetorhinus maximus, see Basking shark

Chemosensory systems of elasmobranchs, 49, see also Electrosensory system of elasmobranchs common chemical sense, 54 gustatory apparatus, 53 gustatory sampling and sensitivity, 53–54 olfactory apparatus, 49–52 olfactory sensitivity, 52–53 water-borne substances sampling, 49–52 Chiloscyllium griseum (C. griseum), 27–28 Chimaeroidei, see Crown-group holocephalans Chlamydoselachus anguineus, see Frill shark Chloride cells, see Mitochondrion-rich cells (MRCs) Chondrichthyan diversity, see also Elasmobranchs environments and adaptations, 13 iniopterygians, 14 internal fertilization, 14 symmoriiforms, 13–14 tand interrelationships, 6f, 7f, 10f acanthodians, 12–13 chondrichthyan crown group, 8–9 chondrichthyan stem group, 9–12 elasmobranch, 5 holocephalans, 6–8 putative early stem chondrichthyans, 12 names, taxa, and characters, 4–5 Chondrichthyan(s), 3 crown group, 8–9 feeding apparatus of, 154 fishes, 20 stem group, 9–12 teeth replacement, 163–164 telencephalon, 57 tooth, 161–162 Choroidal tapetum, 28–29 Chromophores, 26 Cladodont sharks, 10–11 Claspers, 271, 271 Climate change, 239 dispersal capacities, 243–244 metabolic processes, 239–240 ocean warming, 240–241 post-exhaustion oxygen consumption responses, 243f time to fatigue, turns to fatigue, 242f

381

INDEX

Clutching teeth, 161–162 Collared carpet sharks, 126–127 COM, see Center of mass Common chemical sense, 54 Complex prey types, 174–176 Cone photoreceptors, 25–26 Continuous sperm production, 272 Contractile properties axial variation, 206–207 isometric twitches of red muscle, 211f mechanics and energetics of contraction, 202–206 scaling, 210–212 temperature and cycle frequency relationship, 209f thermal sensitivity, 207–210 Cookie cutter sharks (Isistius brasiliensis), 180–181 Copulation, 273 Coracohyoideus–coracoarcualis complex, 157–158 Coracomandibularis, 157–158 Corpus cavernosum, 115–116, 116–119 Corticosteroids, 293 Cost of transport (COT), 237t COT, see Cost of transport Cranial endothermy, 339, see also Muscle endothermy; Visceral endothermy eyes of sharks, 339–340 on temperature measurements, 341 Crown-group holocephalans (Chimaeroidei), 6–8 Cupula, 46 Cutaneous mechanoreception, 48 Cutting teeth, 161–162 D D. brevicaudata, see Dasyatis brevicaudata Dasyatis brevicaudata (D. brevicaudata), 44 Dasyatis sabina, see Atlantic stingray Deep-sea, 69 Dentition, 161–164 DHT, see Dihydrotestosterone Diencephalon, 58–59 Dietary breadth, 180 Dihydrotestosterone (DHT), 289 Direct magnetoreception, 44 Donnan equilibrium, 201

Dorsal pallium, 57–58 Dorsal quadratomandibularis muscle, 158 Dorsal thalamus, 58–59 E Ecophysiological patterns, 180–181 Elasmobranch gill structure, 102 diversity in dimensions and morphology, 125–126, 127f adaptations for fast swimming, 136–137 adaptations for feeding, 141–144 adaptations for freshwater, 139–141 adaptations for hypoxia, 137–139 gill arches, 126–127 gill filtering apparatus of the mobulid rays, 144f gill morphometrics, 128–130 gill surface area relationship, 129f regression equation, 135t RMR and gill surface area relationship, 130t scaling, 134–136 theory on elasmobranch gill dimensions and limits, 130–134 water–blood barrier and lamellae, 131t elasmobranch vs. teleost ventilation, 108–110 gill epithelium, 121–125 gill evolution, 105–108 gill vasculature, 114–121, 118f and blood shunting, 120–121 nonrespiratory vasculature, 119–120 respiratory vasculature, 115–119 vascular casts of the filament circulation, 117f gross morphology, 110–113 immunoflorescent-stained longitudinal section, 125f overview, 102–105, 104f stylized renderings of branchial region, 106f Elasmobranch muscle structure, 190–191 contractile properties axial variation, 206–207 isometric twitches of red muscle, 211f mechanics and energetics of contraction, 202–206 scaling, 210–212

382 Elasmobranch muscle structure (Continued) temperature and the cycle frequency relationship, 209f thermal sensitivity, 207–210 fiber types, 192–193 distribution and contributions to swimming, 194–197 innervation, 199–200 location and size, 192f membrane potential and activation, 201–202 metabolic profiles, 193–194 ultrastructure, 197–199 future directions, 214–215 Elasmobranch physiology field studies biotelemetry and biologging, 315–316 early field physiology, 313–314 fish physiologists, 312 linking laboratory and field work, 314–315 swimming kinematics and energetics, 347–359 thermal physiology, 316 behavioral thermoregulation, 322–326 effects of temperature, 320t physiological thermoregulation, 329–345 sensor types, 317t thermal biology in field, 321–322 thermal biology in lab, 319–321 thermal effect on metabolic rate, 345–346 thermal refuging, 326–329 thresher sharks, 359–364 Elasmobranchii, 57 Elasmobranchs, 2–3, 20, 106f, 180 chondrichthyans, 3 fishes, 190–191, 220 kinematics and body mechanics, 222–224 batoid fishes, 224–225 batoids, 226 dynamics of locomotion in sharks, 229f elasmobranch locomotion, 227 fast-swimming pelagic species, 228 locomotor movements, 224 undulatory locomotion, 223f lamellae, 105, 110, 111–112 vascular sacs on, 114f locomotion energetics, 235–236 oxygen consumption, 236–238

INDEX

RMRs, AMRs, COT, 237t taxonomic representation, 239 locomotor diversity, 221–222 sensory input to central nervous system in, 55 assessing importance of sensory modality, 63–64 encephalization, 64–66 neuroanatomy, 55–63 neuroecology, 66–72 septa and gills, 107 skeletal characters, 3–4 suction feeding, 171 teleost ventilation vs., 108–110 Electro-olfactography (EOG), 52–53 Electrosensory system of elasmobranchs, 39–40, see also Chemosensory systems of elasmobranchs behavioral trials, 40 magnetoreception, role in, 43–44 role in passive electroreception, 42–43 structure and spatial sampling of ampullary organs, 40–42 Ellipsoid model, 66 Embryonic cannibalism, see Adelphophagy Embryophagy, see Adelphophagy Encephalization, 64–66 Endocrine control of reproductive cycles in elasmobranchs, 282–283 calcitonin, 294 corticosteroids, 293 females, 284 oviparous, 285–287 viviparous, 287–290 HPG axis regulation, 283f males, 290 elasmobranch species, 291 estrogen concentrations, 291 relaxin, 292 serotonin, 293 THs, 293–294 EOG, see Electro-olfactography Epaulette shark (Hemiscyllium ocellatum), 138–139 Epithalamus, 58 Euchondrichthyans, 11–12 Evagination, 57 Extended oviparity, see Single oviparity

383

INDEX

F Fast swimming, adaptations for, 136–137 Feeding adaptations for, 141–144 biomechanical models for prey capture, 168f bite feeding elasmobranchs, 173–174 feeding sequence phases, 167–170 motor activity pattern of muscles, 169f suction feeding elasmobranchs, 171–173 synchronized means of kinematic and motor patterns, 169f ecophysiological patterns, 180–181 feeding behaviors, 164–167 filter feeding biomechanics, 177–178 muscle activity modulation, 174–176 prey processing and transport mechanisms, 176–177 sequence phases, 167–170 trophic morphology branchial filters and filtering mechanisms, 165f dentition, 161–164 feeding musculature, 157–159 jaw and tooth position, 163f jaw suspension mechanisms, 159–161, 160f musculoskeletal morphology, 156f skeletal apparatus, 154–157 of tessellated elasmobranch cartilage, 175f tooth types, 162f upper jaw protrusion biomechanics, 178–180 Feeding and digestion, 354–355 captive sharks, 355 gastric pH acoustic transmitter, 357–358 and gastric temperature, 356f sensors, 358–359 serial sampling of gastric fluid pH values, 355–357 in situ gastric electric impedance of freeswimming tiger shark, 358f Female–male reproductive cycles, 282 Female elasmobranchs, see also Male elasmobranchs endocrine control of reproductive cycles, 284

oviparous, 285–287 viviparous, 287–290 fish, 257 oviparous, 257–261 parity and embryo nutrition, 258f viviparous, 261–270 reproductive cycles, 278 continuous breeders, 278–279 seasonal breeders, 280–281 Filter-feeding, 164 biomechanics, 177–178 elasmobranchs, 167 First arch bearing true gills, see Fish gill, arch Fish gills, 105–106 arch, 107 Fish metabolism, 134–136 Foliation, 71 Follicle stimulating hormone (FSH), 284 Free-swimming sharks, 314–315 Freshwater, adaptations for, 139–141 Frill shark (Chlamydoselachus anguineus), 126 FSH, see Follicle stimulating hormone

G G. cirratum, see Ginglymostoma cirratum Galeocerdo cuvier, see Tiger sharks Geniohyoideus, 158 Gill arches, 126–127 Gill epithelium, 121–125 Gill evolution, 105–108 Gill morphology, 110–113 Gill morphometrics, 128–130 Gill rakers, 141–144, 145f Gill surface area, 126, 128, 129f Gill vasculature, 114–121, 118f and blood shunting, 120–121 nonrespiratory vasculature, 119–120 respiratory vasculature, 115–119 vascular casts of filament circulation, 117f Ginglymostoma cirratum (G. cirratum), 25 Ginglymostoma cirratum, see Nurse sharks GnRH, see Gonadotropin-releasing hormone Gonadotropin-releasing hormone (GnRH), 283–284 Gonadotropins (GT), 283–284 Grade Teleostomi, see Bony fishes Gray reef sharks (Carcharhinus amblyrhynchos), 322

384

INDEX

Ground effect, 226 Gustatory apparatus, 53 Gustatory sampling and sensitivity, 53–54 H Hearing abilities, 38 Heart rate, 352–354 Hemiscyllium ocellatum, see Epaulette shark Hexanchiformes, 126 Hexanchus spp, see Sixgill sharks Histotrophy, 264–265 incipient, 265 lipid, 266 minimal, 265 Holocephalans, 6–8, 106f, 107–108 Holocephali, 57 Horizontal cells, 28–29 HPG axis, see Hypothalamus–pituitary– gonadal axis Hydrodynamic stimuli, sensitivity to, 47–48 Hydrodynamics of elasmobranch locomotion, 228–233 5-Hydroxytryptamine (5-HT), see Serotonin Hyoid arch, 157, 181 movement, 171 Hypothalamus–pituitary–gonadal axis (HPG axis), 282–283, 283f Hypoxia, adaptations for, 137–139 I Immunoflorescent-stained longitudinal section, 125f Incipient histotrophy, 265 Iniopterygians, 14 Inner ear, 34, 35f auditory requirements and predatory ability, 36–37 macula, 36 otolithic organs in elasmobranchs, 34–36 Innervation, 199–200 Intrauterine cannibalism, see Adelphophagy Isistius brasiliensis, see Cookie cutter sharks Isometric twitches of red muscle, 210–211, 211f

J Jaw suspension mechanisms, 159–161, 160f

K 11-ketoandrostenedione (11-KA), 289 11-ketosterone (11-KT), 289

L Lactate dehydrogenase (LDH), 197 Lamellar epithelium, 121–122 Lamnid sharks, 128 Lampreys (Petromyzontiformes), 106–107, 106f Lateral line system of elasmobranchs, 44–45, 45f canal and superficial neuromasts, 46–47 hydrodynamic stimuli, sensitivity to, 47–48 network of receptor organs, 45 LDH, see Lactate dehydrogenase Lecithotrophic viviparous, 262–264, see also Matrotrophic viviparous Leopard shark, 324f, 325, 352–353 Lipid histotrophy, 266 Locomotor function, 233 roughened denticle-covered skin of sharks, 235 shark skin models, 233–234 structure and function of denticles, 232f swimming shark skin membranes, 234 Lollipop catshark (Cephalurus cephalus), 137–138 Lymphatic-venous circulation, 119–120

M M. antarticus, see Mustelus antarticus Magnetoreception, role in, 43–44 Male elasmobranch fish, 271 claspers, 271, 272 seasonal sperm production, 272

385

INDEX

Male elasmobranchs, see also Females elasmobranchs endocrine control of reproductive cycles, 290 elasmobranch species, 291 estrogen concentrations, 291 relaxin, 292 reproductive cycles, 281–282 Mandibular arch, 154–157 Mating strategies, 272–273 multiple paternity, 274–276 polyandry, 274–276 sperm storage, 274–276 Matrotrophic viviparous, 264 histotrophy, 264–265 lamnid sharks, 268 in lamniformes, 267 ontogenic development of uterine compartments, 270f oophagy, 266–267 placentatrophy, 268 Meckel’s cartilage, 154–157, 159, 159–161 Medulla oblongata, 62–63 Megachasma pelagios, see Megamouth shark Megamouth shark (Megachasma pelagios), 143 gill rakers, 145f Melanopsin, 33 Membrane potential and activation, 201–202 Mesencephalon, 59–60 Metabolic rate, 315–316 thermal effect on, 345–346 Midbrain, see Mesencephalon Minimal histotrophy, 265 Mitochondrion-rich cells (MRCs), 105, 122–125, 123f increase in lamellar epithelium, 139–141 TEM section, 124f MRCs, see Mitochondrion-rich cells Multiple mating, 274 Multiple oviparity, 261 Multiple paternity, 274–276 Muscle activity modulation, 174–176 Muscle endothermy, 330, see also Cranial endothermy; Visceral endothermy free-swimming sharks, 334 laboratory studies, 335 RM endothermy in sharks, 330–333 temperature in sharks, 332f

temperature effect on muscle function, 337 thermal advantage, 334–335 thermal modeling, 337–339 Muscle fiber, 194–195 Muscle function, temperature effect on, 337 Musculoskeletal morphology, 156f Mustelus antarticus (M. antarticus), 265 N Neuroecology, 66–72 commonalities in brain organization, 67–68, 68f cerebrotypes, 69 deep-sea, 69 epipelagic environments, 70–71 foliation, 71 neuroecological relationships, 71–72 reef-associated habitats, 69–70 Non-occlusible tapeta, 29 Nonvisual system of elasmobranchs, 32, see also Visual system of elasmobranchs melanopsin, 33 pineal complex, 32–33 Notorynchus cepedianus, see Broadnose sevengill shark Nurse sharks (Ginglymostoma cirratum), 349–350 Nutrients, 262 O OB, see Olfactory bulb ODBA, see Overall dynamic body acceleration Odontodes, 12 Olfactory apparatus, 49–52 Olfactory bulb (OB), 52, 55–57 Olfactory receptor neurons (ORNs), 49 Olfactory sensitivity, 52–53 OMZ, see Oxygen minimum zone Oophagy, 266–267 Optic tectum, 59–60 ORNs, see Olfactory receptor neurons Osmoregulation, 128–129 Overall dynamic body acceleration (ODBA), 349

386

INDEX

Oviparous, 257–258, 285–287 egg case development in, 259f embryo development in, 259f embryonic development, 258–260 multiple oviparity, 261 single oviparity, 260 Ovoviviparity, 262 Oxygen minimum zone (OMZ), 137 P Palatoquadrate, 154–157, 159–161 Pars superficialis, 57–58 Parthenogenesis, 276–277 Passive electroreception, role in, 42–43 PATs, see Pop-off archiving satellite transmitters Pavement cells (PVCs), 122f, 123f Pavement teeth, 161–162 PC, see Pillar cells Pelagic sharks, 112–113 Pelagic thresher (Alopias pelagicus), 362–363 Petromyzontiformes, see Lampreys Photoreception, 25–28 Photoreceptors, 25–26 Phototransduction, 26 Physiological thermoregulation, 329 cranial endothermy, 339–341 muscle endothermy, 330–339 visceral endothermy, 341–345 Pillar cells (PC), 122f Pineal complex, 32–33 Pink fibers, 194 Pit organs, see Superficial neuromasts Placentatrophy, 268 Placoderms, 14 PLLN, see Posterior lateral line nerve PO muscle, see Preorbitalis muscle Poikilothermy, 316 Polyandry, 274–276 Pop-off archiving satellite transmitters (PATs), 328 Porphyropsins, 26 Posterior lateral line nerve (PLLN), 46 Preorbitalis muscle (PO muscle), 158, 178–179 Prey capture biomechanical models, 168f bite feeding elasmobranchs, 173–174 feeding sequence phases, 167–170 motor activity pattern of muscles, 169f

suction feeding elasmobranchs, 171–173 synchronized means of kinematic and motor patterns, 169f Prey processing and transport mechanisms, 176–177 Progesterone, 287 Protractor lentis muscle, 23–25 Pseudobranch, 107 Purkinje cell layer, 61 Putative early stem chondrichthyans, 12 PVCs, see Pavement cells Q Quadratomandibularis, 158 R R. terraenovae, see Rhizoprionodon terraenovae Ram filter feeders, 167 RBCs, see Red blood cells Red blood cells (RBCs), 124f Red fibers, 193, 195–196, 199f Red muscle (RM), 330, 331f, see also White muscle (WM) endothermy and thermal distribution, 362–364 morphology, 360 temperature in sharks, 332f uncoupling and swimming mode, 361–362 Reef-associated habitats, 69–70 Regional endothermy, 319–321, 329 Relaxin, 286, 292 Reproduction strategies brain-pituitary-gonadal axis, 256 by elasmobranchs, 256 endocrine control of reproductive cycles in elasmobranchs, 282–294 mating strategies and parthenogenesis, 272–277 reproductive mode classification in elasmobranchs females elasmobranch fish, 257–270 male elasmobranch fish, 271–272

387

INDEX

Reproductive cycles, 277–278 female–male reproductive cycles, 282 females elasmobranchs, 278 continuous breeders, 278–279 seasonal breeders, 280–281 male elasmobranchs, 281–282 Resting metabolic rates (RMRs), 237t Retained oviparity, see Multiple oviparity Retina, 28–29 Retinal ganglion cells (RGCs), 29–30 RGCs, see Retinal ganglion cells Rhincodon typus, see Whale shark Rhizoprionodon terraenovae (R. terraenovae), 38 Rhodopsins, 26 RM, see Red muscle RMRs, see Resting metabolic rates Rod photoreceptors, 25–26 S S. tudes, see Sphyrna tudes Scaling of gills, 134–136, 210–212 Sea surface temperature (SST), 330–333 Seasonal sperm production, 272 Sensory epithelium, 40–41 Serotonin, 293 Sevengill sharks, 126 Sexual dimorphism, 273–274 Sharks elasmobranch skeletal muscle ultrastructure, 197–198 lateral undulations, 191 muscle, 203 skin models, 233–234 Sharp teeth, 161–162 Single oviparity, 260 Sixgill sharks (Hexanchus spp.), 126 Skates, 28, 221, 224–225, 241 Skeletal apparatus, 154–157 Skin of elasmobranchs and locomotor function, 233 roughened denticle-covered skin of sharks, 235 shark skin models, 233–234 structure and function of denticles, 232f swimming shark skin membranes, 234

Sound, 33–34 Spectral sensitivity, 25–28 Sperm storage, 274–276 Sphyrna tudes (S. tudes), 49 Spiny dogfish (Squalus acanthias), 164 Squalus acanthias, see Spiny dogfish SST, see Sea surface temperature Suction feeding elasmobranchs, 171–173, see also Bite feeding elasmobranchs difference in suction feeding mechanism, 171f fluid field generation, 172f Suction filter feeders, 167 Superficial neuromasts, 46–47 Superficial tonic fibers, 194 “Swim-and-glide” patterns of movement, 350 Swimming kinematics and energetics feeding and digestion, 354–355 captive sharks, 355 gastric pH acoustic transmitter, 357–358 gastric pH and gastric temperature, 356f gastric pH sensors, 358–359 serial sampling of gastric fluid pH values, 355–357 in situ gastric electric impedance of freeswimming tiger shark, 358f heart rate, 352–354 swimming, 347 accelerometry, 349–352 tailbeat frequency, 348–349 Swimming mechanics and energetics climate change, 239 dispersal capacities, 243–244 metabolic processes, 239–240 ocean warming, 240–241 post-exhaustion oxygen consumption responses, 243f time to fatigue, turns to fatigue, 242f elasmobranch kinematics and body mechanics, 222–224 batoid fishes, 224–225 batoids, 226 dynamics of locomotion in sharks, 229f elasmobranch locomotion, 227 fast-swimming pelagic species, 228 locomotor movements, 224 undulatory locomotion, 223f elasmobranch locomotion energetics, 235–236 oxygen consumption, 236–238

388

INDEX

Swimming mechanics and energetics (Continued) RMRs, AMRs, COT, 237t taxonomic representation, 239 elasmobranch locomotor diversity, 221–222 elasmobranch swimming, 220 hydrodynamics of elasmobranch locomotion, 228–233 in little skate, 225f skin of elasmobranchs and locomotor function, 233 roughened denticle-covered skin of sharks, 235 shark skin models, 233–234 structure and function of denticles, 232f swimming shark skin membranes, 234 Swordfish (Xiphias gladius), 339–340 Symmoriiforms, 13–14 T T. marmorata, see Torpedo marmorata T3, see Triiodothyronine T4, see Thyroxine Tailbeat frequency (TBF), 315–316 Tailbeat frequency, 348–349 Tapetum cellulosum, 29 Tapetum lucidum, 29 TBF, see Tailbeat frequency Tegmentum, see Ventral tegmentum mesencephali Telemetry, 316–319 Telencephalon, 57–58 Teleost, 106f, 109f elasmobranch ventilation vs., 108–110 Thermal modeling, 337–339 Thermal refuging, 326–329 Thermal sensitivity, 207–210 Thomson–Simanck framework, 221 Thresher sharks (Alopias vulpinus), 128, 134–136, 359–360 caudal fin, 360 RM endothermy and thermal distribution, 362–364 RM morphology, 360 RM uncoupling and swimming mode, 361–362 THs, see Thyroid hormones Thyroid hormones (THs), 293–294

Thyroxine (T4), 293–294 Tiger sharks (Galeocerdo cuvier), 350 Torpedo marmorata (T. marmorata), 33–34, 128–129 Triakis, 109–110 Triiodothyronine (T3), 293–294 U Ultrastructure, 197–199 Upper jaw protrusion biomechanics, 178–180 V V-Hþ-ATPase, see Vacuolar-proton ATPase Vacuolar-proton ATPase (V-Hþ-ATPase), 122–125 Venolymphatic system, 120 Ventral quadratomandibularis muscle, 158 Ventral tegmentum mesencephali, 59 Ventral thalamus, 59 Vestibular control, 37–38 Vestibulolateral cerebellum, 61 Visceral endothermy, 341–342, see also Cranial endothermy; Muscle endothermy acoustic telemetry, 344–345 in lamnids, 343–344 stomach and ambient temperatures, 342f Visual abilities, 30–32 Visual sampling, 29–30 Visual system of elasmobranchs, 22–23, see also Nonvisual system of elasmobranchs eye and image formation, 23 camera-like eyes of elasmobranchs, 23–25 pupillary aperture, 25 quanta of light, 23 photoreception and spectral sensitivity, 25–26 photoreceptors, 26–27 phototransduction, 26 Skates, 28 visual pigment in species of sharks, 27–28 retina and choroidal tapetum, 28–29 visual abilities, 30–32 visual sampling, 29–30

389

INDEX

Viviparity, 261 Viviparous, 261, 287–290 lecithotrophic, 262–264 matrotrophic, 264–270

White muscle (WM), 330, see also Red muscle (RM) WM, see White muscle X

W Xiphias gladius, see Swordfish Water-borne substances sampling, 49–52 Whale shark (Rhincodon typus), 141, 142f White fibers, 200

Y Yolk-sac viviparity, 262, 262–263

OTHER VOLUMES IN THE FISH PHYSIOLOGY SERIES VOLUME 1

Excretion, Ionic Regulation, and Metabolism Edited by W. S. Hoar and D. J. Randall

VOLUME 2

The Endocrine System

VOLUME 3

Edited by W. S. Hoar and D. J. Randall Reproduction and Growth: Bioluminescence, Pigments, and Poisons

VOLUME 4

Edited by W. S. Hoar and D. J. Randall The Nervous System, Circulation, and Respiration Edited by W. S. Hoar and D. J. Randall

VOLUME 5

Sensory Systems and Electric Organs Edited by W. S. Hoar and D. J. Randall

VOLUME 6

Environmental Relations and Behavior Edited by W. S. Hoar and D. J. Randall

VOLUME 7

Locomotion Edited by W. S. Hoar and D. J. Randall

VOLUME 8

Bioenergetics and Growth

VOLUME 9A

Edited by W. S. Hoar, D. J. Randall, and J. R. Brett Reproduction: Endocrine Tissues and Hormones

VOLUME 9B

Edited by W. S. Hoar, D. J. Randall, and E. M. Donaldson Reproduction: Behavior and Fertility Control Edited by W. S. Hoar, D. J. Randall, and E. M. Donaldson

391

392

OTHER VOLUMES IN THE FISH PHYSIOLOGY SERIES

VOLUME 10A

Gills: Anatomy, Gas Transfer, and Acid-Base Regulation Edited by W. S. Hoar and D. J. Randall

VOLUME 10B

Gills: Ion and Water Transfer Edited by W. S. Hoar and D. J. Randall

VOLUME 11A

The Physiology of Developing Fish: Eggs and Larvae

VOLUME 11B

Edited by W. S. Hoar and D. J. Randall The Physiology of Developing Fish: Viviparity and Posthatching Juveniles

VOLUME 12A

Edited by W. S. Hoar and D. J. Randall The Cardiovascular System

VOLUME 12B

Edited by W. S. Hoar, D. J. Randall, and A. P. Farrell The Cardiovascular System Edited by W. S. Hoar, D. J. Randall, and A. P. Farrell

VOLUME 13

Molecular Endocrinology of Fish Edited by N. M. Sherwood and C. L. Hew

VOLUME 14

Cellular and Molecular Approaches to Fish Ionic Regulation Edited by Chris M. Wood and Trevor J. Shuttleworth

VOLUME 15

The Fish Immune System: Organism, Pathogen, and Environment Edited by George Iwama and Teruyuki Nakanishi

VOLUME 16

Deep Sea Fishes

VOLUME 17

Edited by D. J. Randall and A. P. Farrell Fish Respiration

VOLUME 18

Edited by Steve F. Perry and Bruce L. Tufts Muscle Development and Growth Edited by Ian A. Johnston

VOLUME 19

Tuna: Physiology, Ecology, and Evolution Edited by Barbara A. Block and E. Donald Stevens

VOLUME 20

Nitrogen Excretion Edited by Patricia A. Wright and Paul M. Anderson

VOLUME 21

The Physiology of Tropical Fishes Edited by Adalberto L. Val, Vera Maria F. De Almeida-Val, and David J. Randall

OTHER VOLUMES IN THE FISH PHYSIOLOGY SERIES

VOLUME 22

The Physiology of Polar Fishes Edited by Anthony P. Farrell and John F. Steffensen

VOLUME 23

Fish Biomechanics Edited by Robert E. Shadwick and George V. Lauder

VOLUME 24

Behavior and Physiology of Fish

393

Edited by Katharine A. Sloman, Rod W. Wilson, and Sigal Balshine VOLUME 25

Sensory Systems Neuroscience

VOLUME 26

Edited by Toshiaki J. Hara and Barbara S. Zielinski Primitive Fishes

VOLUME 27

Edited by David J. McKenzie, Anthony P. Farrell, and Collin J Brauner Hypoxia

VOLUME 28

Edited by Jeffrey G. Richards, Anthony P. Farrell, and Colin J. Brauner Fish Neuroendocrinology

VOLUME 29

Edited by Nicholas J. Bernier, Glen Van Der Kraak, Anthony P. Farrell, and Colin J. Brauner Zebrafish Edited by Steve F. Perry, Marc Ekker, Anthony P. Farrell, and Colin J Brauner

VOLUME 30

The Multifunctional Gut of Fish Edited by Martin Grosell, Anthony P. Farrell, and Colin J. Brauner

VOLUME 31A

Homeostasis and Toxicology of Essential Metals Edited by Chris M. Wood, Anthony P. Farrell, and Colin J. Brauner

VOLUME 31B

Homeostasis and Toxicology of Non-Essential Metals Edited by Chris M. Wood, Anthony P. Farrell, and Colin J. Brauner

VOLUME 32

Euryhaline Fishes Edited by Stephen C McCormick, Anthony P. Farrell, and Colin J. Brauner

VOLUME 33

Organic Chemical Toxicology of Fishes Edited by Keith B. Tierney, Anthony P. Farrell, and Colin J. Brauner