Deep-Sea Fishes Imants G

Cambridge University Press 978-1-107-08382-0 — Deep-Sea Fishes Imants G. Priede Frontmatter More Information

Deep-Sea Fishes Biology, Diversity, Ecology and Fisheries

The technological advances of the last twenty years have brought huge advances in our understanding of the deep sea and of the species inhabiting this elusive and fascinating environment. Synthesising the very latest research and discoveries, this is a comprehensive and much-needed account of deep-sea fishes. Priede examines all aspects of this incredibly diverse group of animals, reviewing almost 3,500 species and covering deep-sea fish evolution, physiology and ecology as well as charting the history of their discovery from the eighteenth century to the present day. Providing a global account of both pelagic and demersal species, the book ultimately considers the effect of the growing deep-sea fishing industry on sustainability.

Copiously illustrated with explanations of the deep-sea environment, drawings of ﬁshes and information on how they adapt to the deep, this is an essential resource for biologists, conservationists, ﬁshery managers and anyone interested in marine evolution and natural history.

Imants G. Priede is Professor Emeritus at Oceanlab, a field research station of the Institute of Biological and Environmental Sciences, University of Aberdeen. He has over 40 years of experience studying deep-sea fish, from longlining and trawling on the Royal Research Ship Challenger in the 1970s to participating in and leading expeditions to the Pacific Ocean, Atlantic Ocean, Mediterranean Sea and the Mid-Atlantic Ridge. The founder of Oceanlab, he also pioneered satellite tracking of sharks in the 1980s and is the recipient of the 2011 Beverton Medal of the Fish Society of the British Isles.

Deep-Sea Fishes Biology, Diversity, Ecology and Fisheries

IMANTS G. PRIEDE Professor Emeritus, Oceanlab, University of Aberdeen, Scotland, UK

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www.cambridge.org Information on this title: www.cambridge.org/9781107083820 DOI: 10.1017/9781316018330 © Imants G. Priede 2017 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2017 Printed in the United Kingdom by TJ International Ltd. Padstow Cornwall A catalogue record for this publication is available from the British Library. Library of Congress Cataloging-in-Publication Data Names: Priede, I. G., author. Title: Deep-sea fishes : biology, diversity, ecology and fisheries / Imants G. Priede, professor emeritus, Oceanlab, University of Aberdeen, Scotland, UK. Description: Cambridge, United Kingdom ; New York, NY : Cambridge University Press, 2017. | Includes bibliographical references and index. Identifiers: LCCN 2017006037 | ISBN 9781107083820 (Hardback : alk. paper) Subjects: LCSH: Deep-sea fishes. | Deep-sea biology. | Deep-sea ecology. Classification: LCC QL620 .P75 2017 | DDC 597/.63–dc23 LC record available at https://lccn.loc.gov/2017006037 ISBN 978-1-107-08382-0 Hardback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication and does not guarantee that any content on such websites is, or will remain, accurate or appropriate.

To my wife, Maria.

CONTENTS

Preface page ix 1.7.2 Methods of Fish Capture 51 1.7.3 Imaging Systems 61 1 Introduction 1 1.7.4 Tagging and Tracking of Fishes 65 1.1 Definition of Deep-Sea Fishes 1 1.2 The Structure of the World’s Ocean 2 Colonisation of the Deep Sea by Fishes 68 Basins 2 2.1 Introduction 68 1.2.1 Ocean Depth Zones 2 2.2 Present-Day Depth Distribution of Fishes 68 1.2.2 Ocean Basin Formation, Slopes, 2.3 The History of Deep-Sea Fishes 72 Plains, Ridges, Islands and 2.4 Origins of the Modern Deep-Sea Fish Fauna 76 Seamounts 6 2.4.1 Agnatha 76 1.2.3 The Bathyal Slopes 2.4.2 Chondrichthyes 76 (200–3000 m Depth) 11 2.4.3 Actinopterygii 79 1.2.4 Hydrothermal Vents and 2.4.4 Sarcopterygii 85 Cold Seeps 12 2.5 Ancient and Secondary Deep-Sea Fishes 85 1.2.5 The Abyss (3000–6000 m Depth) 13 1.2.6 The Hadal Zone (>6000 m Depth) 15 3 Adaptations to the Deep Sea 87 1.3 History of the Ocean Basins 16 3.1 Introduction 87 1.4 The Deep-Sea Environment 21 3.2 Energy Metabolism 87 1.4.1 Deep Water Formation, Circulation 3.3 Effects of Pressure 90 and Oxygenation of the Deep 21 3.4 Size and Shape 91 1.4.2 Surface Ocean Circulation and Gyres 27 3.5 Buoyancy 93 1.4.3 Ocean Biomes 27 3.5.1 The Swim Bladder and Gas Gland 93 1.5 Food Supply to the Deep and the 3.5.2 Lipid Buoyancy 100 Distribution of Biomass 30 3.5.3 Weight Reduction 101 1.5.1 Export of Particulate Organic 3.6 Muscle Adaptations 102 Matter from the Surface 30 3.7 Gill Area 103 1.5.2 Food Falls 31 3.8 Heart and Circulatory System 104 1.5.3 Distribution of Biomass in 3.9 The Art of Slow Swimming and the the Deep Sea 31 Optimum Speed Fallacy 105 1.6 History of Discovery of Deep-Sea Fishes 35 3.10 Feeding and Growth 108 1.6.1 From the Beginnings of Ichthyology 3.11 Life History Strategies 114 to the First Deep-Sea Discoveries, 3.12 Excretion 118 1554–1860 35 3.13 Sensory and Communication Systems 119 1.6.2 Great Voyages of Discovery, 3.13.1 Diversity of Brain Morphology 119 1860–1914 38 3.13.2 Vision 122 1.6.3 To the First Manned Descents into 3.13.3 Camouflage in the Deep 125 the Deep, 1914–1945 41 3.13.4 Bioluminescence 127 1.6.4 The Great Twentieth-Century 3.13.5 The Olfactory and Gustatory Scientific Expansion from 1945 42 Systems 133 1.7 Collection and Methods 49 3.13.6 Underwater Sound and the 1.7.1 Accessing the Deep Sea 49 Octavo Lateral System 133

viii Contents

3.14 Time in the Deep Sea 135 4.3.25 Order Tetraodontiformes 299 3.15 Diseases and the Immune System 136 4.3.26 Order Lophiiformes 301 3.16 The Maximum Depth Limit for Fishes 138 4.4 Class Sarcopterygii 314 4.4.1 Order Coelacanthiformes 314 4 Systematic Description of Deep-Sea Fishes 139 5 The Deep-Sea Fish Faunas 317 4.1 Class Myxine 139 5.1 Mesopelagic and Bathypelagic Fish 4.1.1 Order Myxiniformes 139 Fauna 317 4.1.2 Order Petromyzontiformes 141 5.1.1 Arctic Ocean 319 4.2 Class Chondrichthyes 142 5.1.2 Paciﬁc Ocean 319 4.2.1 Order Chimaeriformes 142 5.1.3 Indian Ocean 333 4.2.2 Order Hexanchiformes 144 5.1.4 Atlantic Ocean 334 4.2.3 Order Pristiophoriformes 144 5.1.5 The Antarctic Ocean 335 4.2.4 Order Squatiniformes 145 5.2 Bathyal Demersal Fishes 4.2.5 Order Squaliformes 145 (200–3000 m Depth) 335 4.2.6 Order Lamniformes 149 5.3 Abyssal Demersal Species 4.2.7 Order Carcharhiniformes 150 (3000–6000 m Depth) 347 4.2.8 Order Torpediformes 152 5.4 Fishes of the Hadal Zone 4.2.9 Order Pristiformes 152 (>6000 m Depth) 356 4.2.10 Order Myliobatiformes 152 5.5 Fishes of Hydrothermal Vents and 4.2.11 Order Rajiformes 153 Cold Seeps 358 4.3 Class Actinopterygii 155 5.6 The Circumglobal Deep-Sea Fish Fauna 362 4.3.1 Order Albuliformes 155 4.3.2 Order Notacanthiformes 156 6 Deep-Sea Fisheries and Conservation 363 4.3.3 Order Anguilliformes 158 6.1 Global Trends in Deep Fishing 363 4.3.4 Order Alepocephaliformes 166 6.2 Types of Fishing 364 4.3.5 Order Argentiniformes 171 6.2.1 Baited Traps and Lines 364 4.3.6 Order Stomiiformes 175 6.2.2 Static Nets 364 4.3.7 Order Ateleopodiformes 186 6.2.3 Pelagic Trawling 364 4.3.8 Order Aulopiformes 187 6.2.4 Bottom Trawling 365 4.3.9 Order Myctophiformes 196 6.3 Global Trends in Fish Catch 365 4.3.10 Order Lampriformes 203 6.4 Composition of the World Deep-Sea 4.3.11 Order Polymixiiformes 207 Fish Catch 367 4.3.12 Order Zeiformes 208 6.4.1 The Top Twenty Deep-Sea Species 384 4.3.13 Order Stylephoriformes 210 6.4.2 Other Species 391 4.3.14 Order Gadiformes 210 6.5 Overview of the Fishing Trends 400 4.3.15 Order Ophidiiformes 228 6.6 The Impacts of Deep-Sea Fishing 400 4.3.16 Order Batrachoidiformes 238 6.7 Conclusions 403 4.3.17 Order Gobiesociformes 238 4.3.18 Order Stephanoberyciformes 239 Epilogue 404 4.3.19 Order Beryciformes 241 4.3.20 Order Cetomimiformes 245 Appendix 406 4.3.21 Order Syngnathiformes 248 References 415 4.3.22 Order Scorpaeniformes 249 Index 470 4.3.23 Order Perciformes 264 Colour plates can be found between pages 252 and 4.3.24 Order Pleuronectiformes 294 253.

PREFACE

My first direct experience of deep-sea fishes was during November 1974 when I joined the Royal Research Ship Challenger for an expedition in the NE Atlantic under the leadership of Malcolm Clarke (Marine Biological Association Laboratory Plymouth, MBA) and John Blaxter (Scottish Marine Biological Association, Oban, SMBA). Also on board were Bob Foster (MBA) and John Gordon (SMBA), and the aim was to test the fishing capabilities of the new ship using long lines, midwater trawls and bottom trawls. It was a great privilege to sail with this eminent team, and I was immediately enthralled by the extraordinary diversity of deep-sea fishes as I encountered my first morids, grenadiers, deep-sea sharks, lantern fishes, hatchet fishes, smooth-heads, dragonfishes and many other species. Having previously specialised in research on salmon and trout, this was all new to me. This volume is to some extent addressed to my younger self, providing information I wish I had known then. However much has changed since that expedition, almost 1,000 additional deep-sea species have been described since then. We were fishing in a pristine environment not yet touched by commercial fishing activity, and there was no GPS for navigation or 3-D sonar, so bottom fishing was relatively blind with nets often damaged or lost. Years later when I returned on the same ship as the cruise leader, it became clear that the abundance of many dominant demersal species had been significantly reduced by commercial fishing, and by the 1990s we were working in an environment that had become modified by human activity, possibly motivated by reports of the earlier exploratory fishing activity. Science has advanced greatly in the intervening years, and in addition to those named earlier, I am grateful to key persons who have increased my knowledge of the deep sea and enabled me to develop my own research. George Somero first invited me to the Scripps Institution of Oceanography, where I learned of his work on biochemical adaptations of fishes to high pressure and others doing interesting work at the time. Amongst these was Ken Smith Jr., with whom I started a most fruitful collaboration studying the behaviour of living fish in their natural environment at abyssal depths in the Pacific Ocean. In the Atlantic Ocean Tony Rice (National Oceanography Centre, NOC) and Peter Herring (NOC) invited me on their cruises aboard the RRS Discovery off Madeira and West Africa and working with Julian Partridge (University of Bristol), Ron Douglas (City University, London) and Hans-Joachim Wagner (University of Tübingen) taught me much about adaptations of visual and neural systems of fishes. With Anastasios Tselepidis (Hellenic Centre for Marine Research, HCMR) I worked on RV Philia in the Eastern Mediterranean and found out about fishes in the warm deep sea. Meetings with Katsumi Tsukamoto (University of Tokyo) gave me insights into the biology of eels and links with Japan that enabled my team to begin work in hadal trenches of the Pacific Ocean. Nigel Merrett (Natural History Museum, London) has been most influential, acting as a fount of knowledge on deep-sea fishes and as the scientific trawl skipper on several of my cruises, training his successors in arts of fishing at great depths in the years before he retired from active field work. The Census of Marine Life programme (2000–2010) was most important for many marine biologists, and I am particularly grateful to Odd Aksel Bergstad (Institute of Marine Research, Norway) for our collaboration on the Mid-Atlantic Ridge and colleagues I worked with during this time, including

x Preface

Tracey Sutton for his knowledge of pelagic species (Nova Southeastern University, Fort Lauderdale, Florida) and David Shale whose photographs feature in this volume. The aim of this book is an account of the deep sea and the fish that live there. Chapter 1 defines deep-sea fish, outlines the structure of the ocean basins and their history over geological time, the oceanography necessary to understand the environment and food supply to the deep. The history of the discovery of deep-sea fishes is described from before Linneaus, through great expeditions of the nineteenth century to the present day. The methods for capture and investigation of deep-sea fishes are explained. Chapter 2 describes the colonisation of the deep sea in relation to the history of evolution of fishes, survival through major extinction events and recent evidence from molecular genetics. Chapter 3 considers the physiological and other adaptations necessary to survive in the deep and concludes with a discussion of the maximum depth limits of fishes. Chapter 4 gives a description of all deep-sea fishes arranged systematically. Two hundred and twenty two families are identified as contributing to the global deep-sea fish fauna. The aim has been to create a reference work in which a fish caught in the deep sea anywhere in the world can be looked up. The reader should find some information at least down to genus level with an account of the most important or interesting species. To achieve this aim, a rather broad definition of deep-sea fishes has been adopted, but nevertheless species such as some lamnid sharks and tunas that are capable of diving deep here are not considered as true deep-sea species. Line drawings are provided of at least one representative from every significant family. The drawings are diagrammatic, inspired by the thumbnail diagrams in the excellent Fishes of the World by Nelson (2006) but with slightly different conventions. As in Nelson, details of the texture of the skin or scales are not shown, but here the fin rays are drawn. The details of branches in soft fin rays are not shown; caudal and other soft fin rays are depicted by a single bold line. Spiny fin rays are represented accurately within the limitations of image size. All the drawings are the same length, but a scale bar indicates the true size of a typical large adult specimen. Neither the illustrations nor the text are intended as a means of species identification; there are excellent guides published by FAO and regional keys that fulfil that role. Chapter 5 cuts across taxonomy to describe the assemblages or communities of fishes, often comprising species distantly related to one another that live together in the main deep-sea environments from just beneath the surface layers to deep-ocean trenches and their regional differences. Chapter 6 is concerned with exploitation of deep-sea fishes from global trends in commercial fishing through to consideration of over 250 species recorded as exploited and the environmental impacts of such fisheries. The analysis in this chapter is derived from official statistics compiled by the Food and Agriculture Organisation of the United Nations (FAO) and does not take account of illegal, unreported and unregulated landings (IUU), except where specifically mentioned. Chapter 7 makes some concluding remarks. This book has depended greatly on data from FishBase. I am grateful to Rainer Froese, Nicolas Bailly and the staff at FishBase for their help in accessing the necessary information. I have also drawn on the work and help of my own research team, foremost in which were engineers, Phil Bagley, with whom I set up the Oceanlab facility in the University of Aberdeen, and Alan Jamieson, who is now leader of research at hadal depths. The following former postdoctoral fellows and research students have all made their distinctive contributions: John Armstrong, David Bailey, Luke Bullough, Martin Collins, Nicola Cousins (Neé, King), Jessica Craig, Simon Creasey, Toyo Fujii, Jasmin Godbold, Amy Heger, Camila Henriques,

Preface xi

Emma Jones, Kirsty Kemp, Thom Linley, Kirsty Morris, Tomasz Niedzielski, Mark Shields, Martin Solan, Alastair Smith, Ben Wigham and Cynthia Yau. I also thank Rupert Baker (Royal Society of London) for granting access to the Francis Willughby’s Historia Piscium (1686), Gilbert T. Rowe (Texas A& M University) and Chih-Lin Wei (University of Taiwan) for access to their biomass data, Bruce Robison (Monterey Bay Research Institute) for advice on underwater vehicles and other issues, Poly Hadziabdic (British Oceanographic Data Centre) for access to CTD data, Julien Claes (University of Louvain) and Dave Ebert (Moss Landing Marine Laboratory) for advice on bioluminescent sharks and Jeff Drazen (University of Hawaii) for helpful discussions by email. Georges Cuvier wrote in 1828 that positive natural history requires work and expense that cannot be afforded without patronage. He points out that in the fourth century BC, Alexander the Great gave Aristotle eight hundred talents, sufﬁcient to employ several thousand assistants to work on his Historia Animalium; possibly the largest research grant in the history of zoology expressed as a percentage of the total economy. Cuvier argued that progress in ichthyology requires more Alexanders. The Alexanders that provided most of the funding for my research have been the UK Natural Environment Research Council (NERC) and the Framework Programme of the European Union. It was a privilege to be appointed by NERC as the scientist on the project board for construction of the RRS James Cook, which in 2007 replaced the RRS Challenger on which I had started my deep-sea career. The RRS James Cook can deploy sophisticated equipment with an accuracy of a few metres in mid-ocean, something we could only dream of 30 years previously. I have written this book during tenure of an Emeritus Professorship at the University of Aberdeen, Scotland. I thank the Heads of the School of Biological Sciences, Professor Elizabeth Baggs and Professor Graeme Paton for granting me access to necessary facilities. Much of the work has been done at the Hellenic Centre for Marine Research (HCMR) in Crete, Greece, and I thank the Director of the Institute of Oceanography of HCMR, Vassilis Lykousis, for supporting this work and George Petihakis for accommodating me in his team. The entire work has been read by Margaret Eleftheriou, whom I thank for her hard work and support throughout. I thank Dominic Lewis and Jenny van der Meijden of Cambridge University Press for nursing this text through commission and production. Finally, I thank my family for their support through my long absences at sea and preoccupation with work and writing while at home: my late wife Lindsay, wife Maria, daughters Susannah, Camilla and Nanouyia and sons-in-law Nikolas and Tim. Although in some respects this book reﬂects my life’s work, it has been mostly produced during 30 months of intense reading and writing aided by Maria’s motivation and sustenance, without which it would not have been completed. Granddaughters Zoelia and Rosalind have provided welcome distractions from the task, greatly easing the burden of work.