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The document promotes the 2nd edition of 'Marine Mammals: Evolutionary Biology' by Annalisa Berta, aimed at both students and professionals in marine mammal science. It highlights the book's comprehensive approach to marine mammal biology, emphasizing evolutionary relationships and interdisciplinary topics. The book is available in various digital formats and can be ordered online.

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Marine Mammals:
Evolutionary Biology
2nd Edition

Annalisa Berta
Department of Biology
San Diego State University
San Diego, California

James L. Sumich
Biology Department
Grossmont College
El Cajon, California

Kit M. Kovacs
Biodiversity Programme
Norwegian Polar Institute
Tromsø, Norway

With illustrations by
Pieter Arend Folkens
A Higher Porpoise Design Group
Benecia, California

Peter J. Adam
Department of Biology
San Diego State University
San Diego, California

AMSTERDAM • BOSTON • HEIDELBERG • LONDON


NEW YORK • OXFORD • PARIS • SAN DIEGO
SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO
An imprint of Elsevier
Cover illustrations: Carl Buell

Academic Press is an imprint of Elsevier


30 Corporate Drive, Suite 400, Burlington, MA 01803, USA
525 B Street, Suite 1900, San Diego, California 92101-4495, USA
84 Theobald’s Road, London WC1X 8RR, UK

This book is printed on acid-free paper. ∞

Copyright © 2006, 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 photocopy, recording, or any information storage and retrieval system, without per-
mission in writing from the publisher.

Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford,
UK: phone: (+44) 1865 843830, fax: (+44) 1865 853333, E-mail: [email protected]. You may
also complete your request on-line via the Elsevier homepage (http://elsevier.com), by selecting “Support
& Contact” then “Copyright & Permission” and then “Obtaining Permissions.”

Library of Congress Cataloging-in-Publication Data


Application submitted.

British Library Cataloguing in Publication Data


A catalogue record for this book is available from the British Library

ISBN 13: 978-0-12-369499-7


ISBN 10: 0-12-088552-2

Printed in the United States of America


05 06 07 08 09 10 9 8 7 6 5 4 3 2 1
CONTENTS

Preface ix
Acknowledgments x

1. Introduction 1
1.1. Marine Mammals—“What Are They?” 1
1.2. Adaptations for Aquatic Life 1
1.3. Scope and Use of This Book 2
1.4. Time Scale 2
1.5. Early Observations of Marine Mammals 3
1.6. Emergence of Marine Mammal Science 7
1.7. Further Reading and Resources 9
References 9

PART I: EVOLUTIONARY HISTORY


2. Systematics and Classification 12

2.1. Introduction: Systematics—What Is It and Why Do It? 12


2.2. Some Basic Terminology and Concepts 13
2.3. How Do You Do Cladistics? 17
2.4. Testing Phylogenetic Hypotheses 19
2.5. Going Beyond the Phylogenetic Framework: Elucidating
Evolutionary and Ecological Patterns 21
2.6. Taxonomy and Classification 22
2.7. Summary and Conclusions 24
2.8. Further Reading 24
References 24

v
vi Contents

3. Pinniped Evolution and Systematics 27


3.1. Introduction 27
3.2. Origin and Evolution 27
3.3. Summary and Conclusions 46
3.4. Further Reading 47
References 47

4. Cetacean Evolution and Systematics 51


4.1. Introduction 51
4.2. Origin and Evolution 51
4.3. Summary and Conclusions 81
4.4. Further Reading 81
References 82

5. Sirenians and Other Marine Mammals: Evolution and Systematics 89


5.1. Introduction 89
5.2. Origin and Evolution of Sirenians 89
5.3. The Extinct Sirenian Relatives—Desmostylia 98
5.4. The Extinct Marine Bear-Like Carnivoran, Kolponomos 100
5.5. The Extinct Aquatic Sloth, Thalassocnus natans 102
5.6. The Sea Otter, Enhydra lutris 102
5.7. The Polar Bear, Ursus maritimus 105
5.8. Summary and Conclusions 105
5.9. Further Reading 107
References 107

6. Evolutionary Biogeography 111


6.1. Introduction—What Is Biogeography and Why Is It Important? 111
6.2. Ecological Factors Affecting Distributions of Marine Mammals 111
6.3. Present Patterns of Distribution 117
6.4. Reconstructing Biogeographic Patterns 119
6.5. Past Patterns of Distribution 121
6.6. Summary and Conclusions 127
6.7. Further Reading and Resources 128
References 129

PART II: EVOLUTIONARY BIOLOGY, ECOLOGY, AND BEHAVIOR


7. Integumentary and Sensory Systems 132
7.1. Introduction 132
7.2. Integumentary System 132
7.3. Nerves and Sense Organs 148
7.4. Summary and Conclusions 156
Contents vii

7.5. Further Reading 157


References 157

8. Musculoskeletal System and Locomotion 165


8.1. Introduction 165
8.2. Pinnipeds 165
8.3. Cetaceans 178
8.4. Sirenians 195
8.5. Sea Otter 200
8.6. Polar Bear 203
8.7. Summary and Conclusions 203
8.8. Further Reading 205
References 206

9. Energetics 213
9.1. Introduction 213
9.2. Metabolic Rates 213
9.3. Thermoregulation 217
9.4. Energetics of Locomotion 223
9.5. Osmoregulation 229
9.6. Summary and Conclusions 231
9.7. Further Reading 232
References 232

10. Respiration and Diving Physiology 237


10.1. Introduction 237
10.2. Problems of Deep and Prolonged Dives for Breath-Holders 237
10.3. Pulmonary and Circulatory Adaptations to Diving 239
10.4. Diving Response 252
10.5. Diving Behavior and Phylogenetic Patterns 254
10.6. Summary and Conclusions 262
10.7. Further Reading 262
References 262

11. Sound Production for Communication, Echolocation, and Prey Capture 270
11.1. Introduction 270
11.2. Sound Propagation in Air and Water 270
11.3. Anatomy and Physiology of Sound Production and Reception 272
11.4. Functions of Intentionally Produced Sounds 284
11.5. Acoustic Thermometry of Ocean Climate and Low-Frequency
Military Sonars 302
11.6. Summary and Conclusions 303
11.7. Further Reading 304
References 305
viii Contents

12. Diet, Foraging Structures, and Strategies 312


12.1. Introduction 312
12.2. Seasonal and Geographical Patterns of Prey Abundance 313
12.3. Adaptations for Foraging in Pinnipeds 314
12.4. Feeding Specializations of Cetaceans 324
12.5. Feeding Specializations of Sirenians 344
12.6. Feeding Specializations of Other Marine Mammals 350
12.7. Summary and Conclusions 354
12.8. Further Reading 355
References 355

13. Reproductive Structures, Strategies, and Patterns 363


13.1. Introduction 363
13.2. Anatomy and Physiology of the Reproductive System 365
13.3. Mating Systems 377
13.4. Lactation Strategies 395
13.5. Reproductive Patterns 402
13.6. Summary and Conclusions 405
13.7. Further Reading 406
References 407

14. Population Structure and Dynamics 416


14.1. Introduction 416
14.2. Abundance and Its Determination in Marine Mammals 417
14.3. Techniques for Monitoring Populations 419
14.4. Population Structure and Dynamics 432
14.5. Summary and Conclusions 444
14.6. Further Reading 445
References 445

15. Exploitation and Conservation 456


15.1. Introduction 456
15.2. Commercial Exploitation of Marine Mammals 456
15.3. Legal Framework for Marine Mammal Conservation and Protection 460
15.4. Incidental Taking of Marine Mammals 466
15.5. Environmental Contaminants 472
15.6. Single Beachings vs Mass Strandings 475
15.7. Ecotourism 478
15.8. Progress and the Future 480
15.9. Summary and Conclusions 483
15.10. Further Reading 483
References 484

Appendix: Classification of Marine Mammals 491


Glossary 513
Index 521
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PREFACE

The second edition, like the previous one, Marine Mammals: Evolutionary Biology, is
written for two audiences: as a text for an upper-level undergraduate or graduate-level
course on marine mammal biology and as a source book for marine mammal scientists
in research, education, management, and legal/policy development positions. One of
our major goals is to introduce the reader to the tremendous breadth of topics that com-
prise the rapidly expanding interdisciplinary field of marine mammal science today. Our
motivation for writing this book was the lack of a comprehensive text on marine mam-
mal biology, particularly one that employs a comparative, phylogenetic approach. We
have attempted, where possible, to demonstrate that hypotheses of the evolutionary rela-
tionships of marine mammals provide a powerful framework for tracing the evolution of
their morphology, behavior, and ecology. This approach has much to offer but is limited,
in many cases, by available comparative data. We hope that this book stimulates others
to pursue marine mammal research in this exciting new direction.

ix
ACKNOWLEDGMENTS

In preparing the second edition, we have been guided by the detailed, thoughtful, and
constructive comments of colleagues and students. The many colleagues who con-
tributed photographs and line drawings are identified in the captions. We appreciate the
copyediting of Christian Lyderson and Fred Inge Prestenge for library assistance. The
production and editorial staff at Academic Press have been very helpful in preparation
of this book; we are especially grateful to our Developmental Editor, Kirsten Funk, and
Senior Editor, Andrew Richford, as well as the Manager of Editorial Services at SPI,
Christine Brandt. Finally, we thank friends and colleagues who provided inspiration by
asking, “Why do phylogenies matter?”Although we have relied on existing published lit-
erature for information, the interpretations presented here are solely ours. In the spirit of
improving this work, we would appreciate notification of any errors, either of omission
or of fact.

Annalisa Berta
[email protected]

Jim Sumich
[email protected]

Kit Kovacs
[email protected]

x
1

Introduction

1.1. Marine Mammals—“What Are They?”

Some 100 living species of mammals (listed in the Appendix) depend on the ocean for
most or all of their life needs. Living marine mammals include a diverse assemblage of
species that have representatives in three mammalian orders. Within the order Carnivora
are the pinnipeds (i.e., seals, sea lions, walruses), the sea otter, and the polar bear. The
order Cetacea includes whales, dolphins, and porpoises, and the order Sirenia is com-
posed of sea cows (manatees and dugongs). Marine mammals were no less diverse in the
past and include extinct groups such as the hippopotamus-like desmostylians, the bizarre
bear-like carnivore Kolponomos, and the aquatic sloth Thalassocnus.

1.2. Adaptations for Aquatic Life

Marine mammals are well adapted for life in the water though they differ in the degree
to which they are adapted to this habitat. Pinnipeds, sea otters, and polar bears are
amphibious, spending some time on land or ice to give birth and to molt, whereas
cetaceans and sirenians are fully aquatic. A few major aquatic adaptations are briefly
reviewed in this chapter and are covered in greater detail in subsequent chapters.
Adaptations of the skin, specifically its increased insulation (through development of
blubber or a dense fur layer) and countercurrent heat exchange systems, help them cope
with the cold. Similarly, the eyes, nose, ears, and limbs of marine mammals have
changed in association with their ability to live in a variety of aquatic environments,
which include saltwater, brackish, and freshwater. Perhaps the most notable among
sensory adaptations are the high frequency sounds produced by some whales for use in
navigation and foraging. Other marine mammals (e.g., pinnipeds, polar bears, and sea
otters) have an acute sense of smell; these same groups also possess well-developed
whiskers with sensitive nerve fibers that serve as tactile sense organs. Pinnipeds have
front and hind limbs modified as flippers that propel them both in the water and on
land. In cetaceans and sirenians, the hind limbs are virtually absent and locomotion is
accomplished by vertical movement of the tail. Most marine mammals cope with

1
2 1. Introduction

living in salt water by conserving water in their heavily lobulated kidneys, which are
efficient at concentrating urine.
Many marine mammals are capable of prolonged and deep dives. Adaptations of the
respiratory system, such as flexible ribs that allow the lungs to collapse and thickened
tissue in the middle ear of pinnipeds and cetaceans, enable them to withstand the tremen-
dous pressures encountered at great depths. The long dives of these animals are accom-
plished by a variety of circulatory changes including a slowed heart rate, reduced oxygen
consumption, and shunting blood to only essential organs and tissues.

1.3. Scope and Use of This Book

Our goal for this second edition remains the same as for the first edition: to provide an
overview of the biology of marine mammals with emphasis on their evolution, anatomy,
behavior, and ecology. These topics are presented and discussed using, in so far as
possible, an explicit phylogenetic context. In doing so we consider different ways of
incorporating evolutionary history into comparative analyses of marine mammal bio-
logy. The phylogenetic approach advocated in this book is a young but vigorously devel-
oping research field that we believe has much to offer marine mammal science. Over the
past six years, interest in this approach has grown and we are pleased to offer a number
of new case studies that integrate a phylogenetic approach into studies of marine mam-
mal biodiversity.
The book is divided into two major sections: Part I: Evolutionary History (Chapters
2–6) is where the origin and diversity of marine mammals are revealed, and Part II:
Evolutionary Biology, Ecology, and Behavior (Chapters 7–15) is where we attempt to
explain how this diversity arose by examining patterns of morphological, behavioral,
and ecologic diversity. We have intended to explain these concepts, wherever possible, by
example and with a minimum of professional jargon. Words and phrases included in the
glossary appear in boldface type at their first appearance in the text. “Further reading”
sections have been placed at the end of each chapter and are intended to guide the reader
to more detailed information about a particular topic.

1.4. Time Scale

A historical discussion of marine mammals requires a standard time framework for


relating evolutionary events. Figure 1.1 presents the geologic time scale that is used
throughout this book (based on Harland et al., 1990). Our interest lies in the Cenozoic
Era, the last 65 million years of earth history, during which time all marine mammals
made their first appearance. Whales and sirenians were the first to appear, beginning
approximately 50 million years ago (Ma) during the early Eocene. Pinnipeds trace their
ancestry back between 29 and 23 Ma to the late Oligocene. The sea otter lineage goes
back approximately 7 Ma to the late Miocene, although the modern sea otter is known in
the fossil record only as far back as the early Pleistocene (1.6 Ma). Polar bears appear
even later, during the late Pleistocene (0.5 Ma). The desmostylians, extinct relatives of
sirenians, range from the early Oligocene through the late Miocene. The extinct carnivo-
ran Kolponomos is known from a brief time interval during the early Miocene, and the
extinct marine sloth Thalassocnus lived during the late Miocene–late Pliocene (7–3 Ma).
1.5. Early Observations of Marine Mammals 3

Cetacea
Sirenia
Desmostylia †

Pinnipedia
Kolponomos †
Carnivora
Enhydra
Ursus
Thalassocnus † Edentata

Pleisto
Early Middle Late Early Late Early Middle Late E L
Eocene Plio-
Oligocene Miocene cene

55 50 45 40 35 30 25 20 15 10 5 0
Ma
Figure 1.1. Chronologic ranges of marine mammal taxa. Solid bars show reported maximum ranges.
Ma = million years ago. (Time scale and correlations are from Harland et al., 1990, and
Berggren et al., 1995.)

1.5. Early Observations of Marine Mammals

The study of marine mammals probably began with casual observations of the appear-
ance and behavior of whales in the 4th century B.C. Still, the knowledge and history of
these animals themselves go much further back. Drawings of seals and dolphins on pieces
of reindeer antler and in caves have been found from Paleolithic times. The Greek philo-
sopher Aristotle (384–322 B.C.) in his Historia Animalium describes dolphins, killer
whales, and baleen whales, noting that “the [latter] has no teeth but does have hair that
resemble hog bristles.” Unfortunately, Aristotle’s observations were dismissed by many
later workers because of his misclassification of dolphins as fish. Following Aristotle, the
only other authority on whales in ancient times was Pliny the Elder (24–79 A.D.). In his
37-volume Naturalis Historia, he included a book on whales and dolphins in which he
provided accounts based on Aristotle’s findings and his own observations. Knowledge of
marine mammals languished for a thousand years after Aristotle and Pliny during the
Dark Ages. During the Renaissance, a rapid increase in exploration of the oceans was fol-
lowed by the publication of scientific reports from various expeditions. The earliest of
these was the Speculum Regale, an account of Iceland in the 13th century that considered
whales the only truly interesting sight the island had to offer. Its author correctly distin-
guished between northern right whales and bowhead whales, which were still confused by
many naturalists five centuries later. In the 16th century, explorers discovered the rich
feeding grounds in the high Arctic and the large whale populations that these supported.
In the mid-1500s, Konrad Gesner in his Historia Animalium presented illustrations of
whales; among them was one so large that sailors mistook it for an island (Figure 1.2).
A walrus is also illustrated in Gesner’s work (Figure 1.3a). Among the earliest draw-
ings of seals, Vitulus marinus (Figure 1.3b) in Pierre Belon’s De Aquatilibus (1553)
is most remarkable for its accuracy, particularly in the detail of the hind limbs.
In Guillaume Rondelet’s De Piscibus (1554), two seals are illustrated, one probably
4 1. Introduction

Figure 1.2. Woodcut by Conrad Gesner, from Historia Animalium, first published between 1551 and 1558,
shows a whale so large that sailors mistook it for an island.

Figure 1.3. Early illustrations of pinnipeds. (a) Walrus from Conrad Gesner’s Historia Animalium, proba-
bly taken from a drawing by Albert Dürer. (b) Seal from P. Belon, De Aquatilibus (1553). (c) Seal
from Guillaume Rondelet, De Piscibus (1554). (d) Seal from Guillaume Rondelet, De Piscibus
(1554). (e) “Sea lion” from R. Brookes, The Natural History of Quadrupeds (1763).

representing the common seal and the other the Mediterranean monk seal (Figure 1.3c,
d; King, 1983). In another book, The Natural History of Quadrupeds (1763) by
R. Brookes, it is obvious from the illustration and description of the male with a large
snout or trunk that the elephant seal is depicted as a cheerful “sea lion” with a “seaweed
tail” (Figure 1.3e; King, 1983).
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