Marine Mammals: Evolutionary Biology

Marine Mammals

Evolutionary Biology

Third Edition

Annalisa Berta

Department of Biology, San Diego State University, San Diego, CA, USA

James L. Sumich

Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA

Kit M. Kovacs

Norwegian Polar Institute, FRAM Center, Tromsø, Norway; University Centre on Svalbard (UNIS), Svalbard, Norway

Table of Contents

Cover image

Title page

Copyright

Preface

Acknowledgments

Chapter 1. Introduction

1.1. Marine Mammals—What Are They?

1.2. Adaptations for Aquatic Life

1.3. Scope and Use of this Book

1.4. Time Scale

1.5. Early Observations of Marine Mammals

1.6. Emergence of Marine Mammal Science

1.7. Further Reading and Resources

Part 1. Evolutionary History

Chapter 2. Phylogeny, Taxonomy, and Classification

2.1. Introduction: Investigating Evolutionary Histories

2.2. Some Basic Terminology and Concepts

2.3. How Do You Build a Phylogenetic Tree?

2.4. Testing Phylogenetic Hypotheses

2.5. Applying Phylogenies: Elucidating Evolutionary and Ecological Patterns

2.6. Taxonomy and Classification

2.7. Summary and Conclusions

2.8. Further Reading and Resources

Chapter 3. Pinniped Evolution and Systematics

3.1. Introduction

3.2. Origin and Evolution

3.3. Summary and Conclusions

3.4. Further Reading and Resources

Chapter 4. Cetacean Evolution and Systematics

4.1. Introduction

4.2. Origin and Evolution

4.3. Summary and Conclusions

4.4. Further Reading and Resources

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

5.1. Introduction

5.2. Origin and Evolution of Sirenians

5.3. The Extinct Sirenian Relatives—Desmostylia

5.4. The Extinct Marine Bear-Like Carnivoran, Kolponomos

5.5. The Extinct Aquatic Sloth, Thalassocnus natans

5.6. Marine Otters

5.7. The Polar Bear, Ursus maritimus

5.8. Summary and Conclusions

5.9. Further Reading and Resources

Chapter 6. Evolution and Geography

6.1. Introduction

6.2. Species Identity

6.3. Speciation

6.4. Ecological Factors Affecting Distributions of Marine Mammals

6.5. Present Patterns of Distribution

6.6. Reconstructing Biogeographic Patterns

6.7. Past Patterns of Distribution

6.8. Summary and Conclusions

6.9. Further Reading and Resources

Part 2. Evolutionary Biology, Ecology, and Behavior

Chapter 7. Integumentary and Sensory Systems

7.1. Introduction

7.2. Integumentary System

7.3. Nerves and Sense Organs

7.4. Summary and Conclusions

7.5. Further Reading and Resources

Chapter 8. Musculoskeletal System and Locomotion

8.1. Introduction

8.2. Pinnipeds

8.3. Cetaceans

8.4. Sirenians

8.5. Sea Otter

8.6. Polar Bear

8.7. Summary and Conclusions

8.8. Further Reading and Resources

Chapter 9. Energetics

9.1. Introduction

9.2. Metabolic Rates

9.3. Thermoregulation

9.4. Energetics of Locomotion

9.5. Osmoregulation

9.6. Summary and Conclusions

9.7. Further Reading and Resources

Chapter 10. Respiration and Diving Physiology

10.1. Introduction

10.2. Challenges of Deep and Prolonged Dives for Breath-Holders

10.3. Pulmonary and Circulatory Adaptations to Diving

10.4. Diving Response

10.5. Diving Behavior and Phylogenetic Patterns

10.6. Summary and Conclusions

10.7. Further Reading and Resources

Chapter 11. Sound Production for Communication, Echolocation, and Prey Capture

11.1. Introduction

11.2. Sound Propagation in Air and Water

11.3. Anatomy and Physiology of Sound Production and Reception

11.4. Functions of Intentionally Produced Sounds

11.5. Acoustic Thermometry of Ocean Climate and Low-Frequency Military Sonars

11.6. Summary and Conclusions

11.7. Further Reading and Resources

Chapter 12. Diet, Foraging Structures, and Strategies

12.1. Introduction

12.2. Seasonal and Geographical Patterns of Prey Abundance

12.3. Adaptations for Foraging in Pinnipeds

12.4. Feeding Specializations of Cetaceans

12.5. Feeding Specializations of Sirenians

12.6. Feeding Specializations of Other Marine Mammals

12.7. Summary and Conclusions

12.8. Further Reading and Resources

Chapter 13. Reproductive Structures, Strategies, and Patterns

13.1. Introduction

13.2. Anatomy and Physiology of the Reproductive System

13.3. Mating Systems

13.4. Lactation Strategies

13.5. Reproductive Patterns

13.6. Summary and Conclusions

13.7. Further Reading and Resources

Chapter 14. Population Structure and Dynamics

14.1. Introduction

14.2. Abundance and Its Determination in Marine Mammals

14.3. Techniques for Monitoring Populations

14.4. Population Structure and Dynamics

14.5. Summary and Conclusions

14.6. Further Reading and Resources

Part 3. Exploitation, Conservation, and Management

Chapter 15. Exploitation and Conservation

15.1. Introduction

15.2. Exploitation of Marine Mammals

15.3. Marine Mammal Conservation and Protection

15.4. Progress and the Future

15.5. Summary and Conclusions

15.6. Further Reading and Resources

Appendix

Color Plates

Glossary

Index

Copyright

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Preface

The third edition of Marine Mammals: Evolutionary Biology, like the previous two, is written for two different 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 comprise 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 mammal biology, particularly one that employs a comparative, phylogenetic approach. We have attempted, where possible, to demonstrate that hypotheses of the evolutionary relationships 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 join us in the pursuit of marine mammal research in this exciting new dirsection.

Acknowledgments

In preparing the third edition, we have been guided by the detailed, thoughtful and constructive comments of colleagues and students to the previous editions. We thank many colleagues who contributed photographs and line drawings; they are identified in the captions. We appreciate the reference copyediting and library assistance of Heidi Ahonen. The production and editorial staff at Elsevier have been very helpful in preparation of this book: we are especially grateful to Senior Acquisitions Editor, Kristi A.S. Gomez, Senior Project Manager, Caroline Johnson, and Production Project Manager, Lucía Pérez, as well as Senior Editorial Project Manager, Pat Gonzalez. Finally, we thank friends and colleagues who provided inspiration by asking Why do phylogenies matter?

Although we have relied on existing published literature for information, the interpretations presented herein are solely ours. In the spirit of improving this work, we will be appreciative of notification of any errors, either of omission or of fact.

Annalisa Berta email address: aberta@mail.sdsu.edu

Jim Sumich email address: jlsumich1@gmail.com

Kit M. Kovacs email address: kit.kovacs@npolar.no

Chapter 1

Introduction

Abstract

Marine mammals are defined and their adaptations reviewed in this introductory chapter. Extant marine mammals include more than 125 species with representatives in three mammalian orders: Carnivora: pinnipeds, marine otters, and polar bears; Cetacea: whales, dolphins, and porpoises; and Sirenia: manatees and dugongs. Objectives are identified and the organization of the book is presented. A standardized time scale for relating evolutionary events pertaining to marine mammals is provided. Historical review of marine mammals follows beginning with early casual observations in ancient times to the present-day emergence of marine mammal science as a clearly defined discipline characterized by technological advances in microelectronics (e.g., satellite telemetry and time–depth recorders) as well as molecular biology (e.g., genome studies that combine DNA analysis and bioinformatics).

Keywords

Book scope and organization; History; Marine mammal science; Time scale

1.1. Marine Mammals—What Are They?

Some 130 species of mammals (listed in the Appendix) currently depend on the ocean for most or all of their life needs. Extant marine mammals include a diverse assemblage of species that have representatives in three mammalian orders. Within the order Carnivora the pinnipeds (i.e., true seals, fur seals, sea lions, and walruses), marine otters (including the sea otter), and the polar bear all spend considerable amounts of time in marine environments. Cetacea, which include the whales, dolphins, and porpoises, fall within the artiodactyls (even-toed ungulates) and are included in the superorder Cetartiodactyla. Finally, the order Sirenia is composed of the sea cows, including both the 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 carnivoran Kolponomos, and the aquatic sloth Thalassocnus. Figure 1.1 shows the various groups of living and some extinct marine mammals and their species-level diversity.

1.2. Adaptations for Aquatic Life

Marine mammals are obviously well adapted for life in the water, though they differ in the degree to which they have become obligate residents of this habitat alone. Pinnipeds, sea otters, and polar bears are amphibious, spending some time on land or ice where they give birth, molt, and rest, whereas cetaceans and sirenians are fully aquatic. A few major aquatic adaptations are briefly reviewed in this chapter and are covered in 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 in a few cases even freshwater. Perhaps the most notable sensory adaptations are the high-frequency sounds produced by some whales for use in navigation and foraging. Other marine mammals (e.g., polar bears and sea otters) have an acute sense of smell; these same groups along with pinnipeds also possess well-developed whiskers with sensitive nerve fibers that serve as tactile sense organs. Pinnipeds have front and hindlimbs modified as flippers that propel them in the water and still provide serviceable limbs for locomotion on land. In cetaceans and sirenians, the hindlimbs are virtually absent and locomotion is accomplished by vertical movements of the powerful hind flukes. Most marine mammals cope with living in saltwater 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 tremendous pressures encountered at great depths. The long dives of these animals are accomplished by a variety of circulatory changes including a slowed heart rate, reduced oxygen consumption, and shunting blood to only essential organs and tissues.

Figure 1.1  Diversity of marine mammals. †= extinct taxa.

1.3. Scope and Use of this Book

Our goal for this third edition remains the same as for the other editions of this book: to provide an up-to-date overview of the biology of marine mammals with emphasis on their evolution, anatomy, behavior, ecology, and conservation. These topics are presented and discussed using, insofar as possible, an explicit phylogenetic context. In so doing we consider different ways of incorporating evolutionary history into comparative analyses of marine mammal biology. The phylogenetic approach advocated in this book continues to be a vigorous research field that we believe has much to offer marine mammal science. Over the past decade, 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 mammal biodiversity.

The book is divided in three sections: Part 1, Evolutionary History, in which the origin and diversity of marine mammals are revealed; Part 2, Evolutionary Biology, Ecology and Behavior, in which we attempt to explain how this diversity arose by examining patterns of morphological, behavioral, and ecological diversity; and Part 3, Exploitation, Conservation and Management, in which problems associated with the impacts of humans on marine mammals are examined. We have attempted 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 information that is more detailed about particular topics.

Figure 1.2  Chronological ranges of marine mammal taxa. Solid bars show reported maximum ranges. Ma   =   million years ago. Time scale and correlations are from Gradstein et al. (2012).

1.4. Time Scale

A historical discussion of marine mammals requires a standard time framework for relating evolutionary events. Figure 1.2 presents the geologic time scale that is used throughout this book (based on Gradstein et al. 2012). 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. The ancestory of pinnipeds can be traced back to 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 more recently, during the late Pleistocene (<0.5  Ma). The desmostylians, extinct relatives of sirenians, range from the early Oligocene through the late Miocene. The extinct carnivoran Kolponomos is known from a brief time interval during the early Miocene, and the extinct marine sloth Thalassocnus lived during the late Miocene through until the late Pliocene (7–3  Ma).

1.5. Early Observations of Marine Mammals

Marine mammals have always fascinated people, and coastal communities have used them as resources throughout history. Drawings of seals and dolphins on pieces of reindeer antler and on cave walls have been found from Paleolithic times. The Greek philosopher Aristotle (384–322 BC) 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 AD). 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 1000 years after Aristotle and Pliny during the Dark Ages. During the Renaissance, a rapid increase in exploration of the oceans was followed by the publication of scientific reports from various expeditions. The earliest of these was the Speculum Regale, an account of Iceland in the thirteenth century that considered whales the only truly interesting sight the island had to offer. Its author correctly distinguished between northern right whales (Eubalaena spp.) and bowhead (Balaena mysticetus) whales, which were still confused by many naturalists five centuries later. In the sixteenth century, explorers discovered the rich marine mammal 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 1.3).

A walrus is also illustrated in Gesner’s work (Figure 1.4(a)). Among the earliest drawings of seals, Vitulus marinus (Figure 1.4(b)) in Pierre Belon’s De Aquatilibus (1553) is remarkable for its accuracy, particularly in the detail of the hindlimbs. In Guillaume Rondelet’s De Piscibus (1554–1555), two seals are illustrated, one probably representing the harbor seal (Phoca vitulina) and the other the Mediterranean monk seal (Monachus monachus) (Figure 1.4(c) and (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 (Mirounga spp.) is depicted as a cheerful sea lion with a seaweed tail (Figure 1.4(e); King, 1983).

In 1596, the Dutch navigator Wilhelm Barents discovered Spitsbergen (the largest island in the Svalbard Archipelago, Norway), and early in the seventeenth century commercial whalers were sent there by Dutch and English companies to establish a whaling town. Although these expeditions were concerned primarily with harvesting whale products, they also produced a number of publications that provided reasonably accurate descriptions of the external appearance of the most common kinds of whales found in the North Atlantic. The best of these are found in Spitzbergische oder Groenlandische Reisen Beschreibung (1675) by Frederich Martens and Bloyeyende Opkomst der Aloude en Hedendaagsche Groenlandsche Visschery (1720) by C.G. Zorgdrager, both of which contained engravings that continued to be reproduced in books until the early nineteenth century. Georg Wilhem Steller, the ship’s naturalist and physician for Vitus Bering’s second expedition to North America, was among the first Europeans to explore Alaska and the Aleutian and Commander Islands. His notes of marine mammals living in the Bering Sea, The Beasts of the Sea (1751), contained natural history accounts of sea otters, sea lions, fur seals, and perhaps most notably the now extinct Steller’s sea cow (Hydrodamalis gigas). His were the only firsthand scientific observations of this species.

Figure 1.3  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 1.4  Early illustrations of pinnipeds. (a) Walrus from Conrad Gesner’s Historia Animalium , probably 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) .

Another naturalist, Lacépède, compiled a volume on whales (1804), in which most of the illustrations were copied from previous publications (Figure 1.5). Lacépède acknowledged that, not having ever seen a whale, he had compiled his descriptions from the accounts made by other naturalists. In the first half of the nineteenth century, additions to the literature included Peter Camper’s Observations Anatomiques sur Plusiers Especes de Cétacés (1820). The foremost European cetologist of the second half of the nineteenth century was P.-J. Van Bénéden, a Belgian zoologist whose many monographs on whales and pinnipeds (including Histoire Naturelle des Cétacés des Mers d’Europe, 1889) were published in Brussels between 1867 and 1892. John Edward Gray, who became Keeper of the Zoology Department at the British Museum of Natural History, published his Catalogue of Seals and Whales in the British Museum in 1866. John Allen (1880), in his comprehensive monograph of North American pinnipeds, provided detailed morphological descriptions and keys to the families and genera of North American species, and also gave accounts of pinniped species in other parts of the world.

Meanwhile, the whaling industries of several countries were making other contributions to the study of whales. Whaling captains, such as William Scoresby and Charles Scammon, made their own observations in the field and collected those of their colleagues. Scoresby published An Account of the Arctic Regions (1820), which is still a valuable source of information on the northern right whale (Eubalaena glacialis). Scammon’s book, The Marine Mammals of the North-Western Coast of North America, was published in 1874 and has become a classic, particularly valued for its description of the natural history of the gray whale (Eschrichtius robustus) in California. Land-based whaling stations used in more recent whaling periods provided the material for Frederick True’s (1904) monograph The Whalebone Whales of the Western North Atlantic and Roy Chapman Andrews’s (1916) monograph on the Sei whale (Balaenoptera borealis) in the Pacific.

Apart from whalers, the only people seriously interested in the study of whales (cetology) in these early days were comparative anatomists (for a more detailed account of the beginnings of cetology, see Matthews, 1978). Among their ranks were Rondelet, Bartholin, Camper, Cuvier, Hunter, and Owen. These pioneers in the study of cetacean anatomy made the most of specimens that they encountered, and the writings that many of them produced show that they made accurate observations and amazing connections to the lifestyles of their research subjects. Cuvier in particular made several fundamental advances in cetology. His Le Régne Animal (1817) and Recherches sur les Ossemens Fossiles (1823) contain original descriptions and illustrations of the three species of cetacean that he named (Cuvier’s beaked whale, Ziphius cavirostris, Risso’s dolphin, Grampus griseus, and the spotted dolphin, Stenella attenuata).

During this time of the early natural historians and the pioneering anatomists, confusion over affinities of some marine mammal groups appeared. For example, the outward appearance of dugongs led some to consider them an unusual tropical form of walrus. In a publication from 1800, the manatee is inaccurately shown as being hog-nosed (Figure 1.6(a)). However, the earliest illustration of a sirenian to be published, one of a West Indian manatee, from the 1535 edition of La Historia General y natural de la Indias by Gonzalo Fernandez de Oviedo y Valdes, is little changed from depictions more than two centuries later (Figure 1.6(b)).

Descriptions of the anatomy of various pinnipeds followed during the 1800s, including the walrus (Odobenus rosmarus) (Murie, 1870) and the Steller sea lion (Eumetopias jubatus) (Murie, 1872, 1874). Another accomplished anatomist, W.C.S. Miller (1888), dissected a variety of pinnipeds including the Antarctic fur seal (Arctocephalus gazella) and southern elephant seal (Mirounga leonina), recovered on the H.M.S. Challenger expedition to the Antarctic during the years 1873–1875. Thompson (1915) published the first account of the osteology of Antarctic seals including the Ross seal (Ommatophoca rossii), the Weddell seal (Leptonychotes weddellii), and the leopard seal (Hydrurga leptonyx). A short time later, Howell (1929) published his well-known comparative study of phocids and otariids, based on the California sea lion (Zalophus californianus) and the ringed seal (Pusa hispida). He followed this with a book on aquatic adaptations in mammals (Howell, 1930).

Figure 1.5  Woodcut of baleen whales from Lacépède (1804) .

Figure 1.6  Early illustrations of manatees. (a) An American manatee (species, unknown) from a lithograph ( Reynolds and Odell, 1991 ). (b) West Indian manatee ( Trichechus manatus ) from the 1535 edition of La Historia General de la Indias by Gonzalo Fernandez de Oviedo y Valdes.

1.6. Emergence of Marine Mammal Science

Marine mammal science has emerged as a discipline in its own right only in the last 30–40  years. This increasing interest in marine mammals is clearly shown by the expansion of the literature dealing with these animals. J.A. Allen’s bibliography of cetaceans and sirenians (1882), covering the 350  years from 1495 to 1840, contains 1014 titles, just under three publications per year. In the period from 1845 to 1960, between 3000 and 4000 articles were published, with a conservative estimate of about 28 titles a year (Matthews, 1966). By comparison, around 24,000 papers on marine mammals were published between 1961 and 1998 according to the Zoological Record, a rate of 646 per year. From 1999 to 2004, marine mammal publications increased to a rate of more than 850 per year, and from 2005 to 2013 this number has remained close to this figure. Among the major influences that contributed to the birth of marine mammal science was the growing recognition that exploitation of marine mammal populations had to be regulated if these animals were going to survive into the future (Boyd, 1993). The aim of many early studies was to obtain accurate information about the biology of these animals for use in establishing an effective management policy for sustainable exploitation. It is somewhat ironic that the declines in whale stocks heralded the beginnings of the scientific study of marine mammals. For example, because of concerns regarding stock viability, the Discovery investigations (1925–1951) were undertaken to examine the biology of whale stocks in the Southern Ocean. Not only was the biology of whales examined but also their food supplies and their distributions and abundances in relation to oceanographic conditions. For example, the British scientists N.A. Mackintosh and J.F.G. Wheeler (1929) examined 1600 carcasses for gut contents to produce their report on blue (Balaenoptera musculus) and fin whales (Balaenoptera physalus) feeding. Leonard Harrison Matthews had comparable samples in his reports on the humpback whale (Megaptera novaeangliae), sperm whale (Physeter macrocephalus), and southern right whale (Eubalaena australis) in 1938 (Watson, 1981).

In the 1950s, the theme of the Discovery investigations was continued by the Falkland Islands Dependencies Survey (later known as the British Antarctic Survey) when it established a research program on the southern elephant seal on South Georgia Island under the directorship of R.M. Laws. In parallel with these and other studies, which focused on population ecology, there also was growing interest in the anatomy and physiology of marine mammals that built upon early studies by Irving (1939) and Scholander (1940) (Slijper, 1962; Norris, 1966; Andersen, 1969; Ridgway, 1972; Harrison, 1972–1977). The establishment of various scientific committees (e.g., the International Whaling Commission’s Scientific Committee in 1946 and the US Marine Mammal Commission in 1972) created to provide advice on the status of various marine mammal populations also required knowledge and data on the general biology of these animals and thus served to stimulate research. Since the early 1980s, the biology of various marine mammal species has been the subject of many notable books, beginning with Ridgway and Harrison’s series entitled Handbook of Marine Mammals (1981–1998). This has been followed by detailed separate accounts of the biology of the Pacific walrus (Fay, 1982), gray whale (Jones et al. 1984; Sumich, 2014), bowhead whale (Burns et al. 1993), right whale (Kraus and Rolland, 2010), bottlenose dolphin (Leatherwood and Reeves, 1990; Reynolds et al. 2000), Hawaiian spinner dolphin (Norris et al. 1994), harbor porpoise (Read et al. 1997), sperm whale (Whitehead, 2003), harp and hooded seal (Lavigne and Kovacs, 1988), elephant seal (Le Boeuf and Laws, 1994), and the northern fur seal (Gentry, 1998). Comprehensive treatments of marine mammal groups are available for pinnipeds (King, 1983; Bonner, 1990; Riedman, 1990; Renouf, 1991), whales (Matthews, 1978; Gaskin, 1982; Evans, 1987; Mann et al. 2000; Estes et al. 2006), manatees and dugongs (Hartman, 1979; Reynolds and Odell, 1991; Marsh et al. 2011), sea otters (Kenyon, 1969; Riedman and Estes, 1990), and polar bears (Stirling, 1998, 2012; Derocher, 2012). Many valuable field identification guides for marine mammals are available; the most recent and wide ranging include Shirihai and Jarrett (2006), Jefferson et al. (2008), Allen et al. (2011), and Berta (2015). Recent additions to the growing literature on marine mammal biology include Parsons (2013) and edited books on health and medicine (Dierauf and Gulland, 2001), cell and molecular biology (Pfeiffer, 2002), conservation biology (Evans and Raga, 2001; Reynolds et al. 2005; Boyd et al. 2010; Hoyt, 2011; Hines et al. 2012), evolutionary biology (Hoelzel, 2002), and even an encyclopedia on marine mammals (Perrin et al. 2002, 2009). Serving an important archival role, the journal Aquatic Mammals has published essays and video interviews since 2008 entitled Historical Perspectives, featuring marine mammal scientists who have worked in the field for more than 25  years.

Matthews (1966) wrote the greatest revolution in the study of the Cetacea … has come with the possibility of keeping living cetaceans in oceanariums. However, one of the most significant advances in marine mammal science in recent years has undoubtedly been the move toward studying animals in the wild, under unrestrained conditions at sea. This is in large part the result of technological advances in microelectronics (e.g., satellite telemetry and time–depth recorders). For example, the application of microelectronics led to the discovery that elephant seals regularly dive to depths in excess of 1000  m with consistently long dive durations, typically lasting 15–45  min. This feature of elephant seal biology, in addition to studies on a variety of other species, has forced physiologists to reexamine our understanding of the biochemical pathways used by these animals to maximize the efficiency of their oxygen utilization. Studies with crittercams have provided visual records of everything that a marine mammal sees on foraging trips. For example, crittercams have revealed Weddell seals flushing prey from crevices in the ice and humpbacks performing highly cooperative feeding maneuvers in Alaskan waters.

Technological advances in molecular biology (e.g., genome studies that combine analysis of DNA variation and bioinformatics) have also provided unparalleled opportunities to examine interactions among populations and the roles of individuals within those populations. For example, using DNA fingerprinting and other techniques, it is possible to assess paternity and kinship among whales, animals for which this has previously been virtually impossible owing to the difficulty of observing them mating underwater. These techniques have also made it possible to measure effective population sizes and interpret historical events such as population bottlenecks. Molecular techniques have also contributed to our knowledge of the systematics and taxonomy of various marine mammal groups. Recently, the sequencing of entire genomes of various marine mammals has been applied to studies that include population genetics and speciation, adaptation, evolution, disease, and conservation genetics.

As pointed out 30  years ago by Watkins and Wartzok (1985), information and research about marine mammals range from intensive to eclectic. Much of the available data is difficult to synthesize because techniques vary widely and sample sizes are often small. This is not a reflection of poor science, but rather the environmental, practical, financial, and legal complications implicit in conducting marine mammal research. It is apparent that the global databases must continue to expand. Even within a relatively homogeneous group like odontocete whales, one well-known species (the bottlenose dolphin, Tursiops truncatus) cannot be used reliably to characterize all toothed whales. With this in mind, we hope that as readers of this book you will be able to identify areas in which future research is most essential (e.g., Evans et al. 2014). We encourage you to pursue research on marine mammals—many gaps still remain in our knowledge of this diverse and unique assemblage of mammals.

1.7. Further Reading and Resources

Several Internet addresses contain information about marine mammal programs and organizations; a few that we consider the most useful are listed here:

http://www.marinemammalogy.org—Society for Marine Mammalogy (SMM), a professional international organization of marine mammal scientists, which publishes a journal (quarterly) of original research on marine mammals: Marine Mammal Science.

http://acsonline.org—American Cetacean Society (ACS) and http://www.EuropeanCetaceanSociety.eu—European Cetacean Society (ECS), professional biologists and others interested in whales and dolphins (recent issues of Whale Watcher published by the ACS that highlight the biology, ecology, and conservation of sperm whales, killer whales, and gray whales are notable).

http://www.earthwatch.org—Earthwatch Institute, offers opportunities for marine mammal enthusiasts to work as volunteers with research scientists.

A new digital textbook for marine mammal science Cachalot, distributed free on the Apple iTunes Store, provides lessons, photos, video, audio, and animations.

Also, for career and hobbyist information about marine mammals, see books by Glen (1997) The Dolphin and Whale Career Guide, Samansky (2002) Starting Your Career as a Marine Mammal Trainer, as well as Strategies for Pursuing a Career in Marine Mammal Science, published by SMM and available online.

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Part 1

Evolutionary History

Outline

Chapter 2. Phylogeny, Taxonomy, and Classification

Chapter 3. Pinniped Evolution and Systematics

Chapter 4. Cetacean Evolution and Systematics

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

Chapter 6. Evolution and Geography

Chapter 2

Phylogeny, Taxonomy, and Classification

Abstract

Introduction is provided to the basic terminology and concepts involved in systematics and reconstruction of the evolutionary history of marine mammals. The construction of phylogenetic trees is reviewed as are methods for testing phylogenetic hypotheses. Also explored is the application of phylogenetic trees to elucidate evolutionary and ecological patterns using various marine mammal examples. The chapter concludes with presentation of the principles of taxonomy and classification as they relate to marine mammals.

Keywords

Classification; Systematics; Taxonomy

2.1. Introduction: Investigating Evolutionary Histories

The study of biological diversity has at its roots the reconstruction of phylogeny, the evolutionary history of a particular group of organisms (e.g., species). Knowledge of evolutionary history provides a framework for interpreting biological diversity. This context makes it possible to examine the ways in which attributes of organisms change over time, the direction in which attributes change, the relative frequency with which they change, and whether change in one attribute is correlated with change in another. It is also possible to compare the descendants of a single ancestor to look for patterns of origin and extinction or relative size and diversity of these descendant groups. Phylogenies can also be used to test hypotheses of adaptation. For example, consider the evolution of large heads in some of the baleen whales. One hypothesis for how baleen whales evolved such big heads suggests that they facilitated lunge feeding. However, based on a study of allometry, which is the change in the proportion of various body parts as a consequence of growth in whales, Goldbogen et al. (2010) proposed that the big heads of some baleen whales (e.g., in particular, balaenopterids such as blue and fin whales, Balaenoptera musculus and B. physalus) may have evolved for a different function. In this case, large heads may have evolved simply because of an overall expansion of body size, which in turn facilitated the deposition of fat stores required for fasting and long-distance migration. According to this hypothesis, the large heads of these baleen whales may be an exaptation associated with large body size. An exaptation is defined as any adaptation that performs a function different from the function that it originally held. A more complete understanding of the evolution of large heads in baleen whales requires examination of other characters involved in large body size (see Chapter 12).

An understanding of the evolutionary relationships among species can also assist in identifying priorities for conservation (May-Collado and Agnarsson, 2011). For example, the argument for the conservation priority of sperm whales is strengthened by knowing that this major lineage consisting of this single species occupies a key phylogenetic position relative to the other species of toothed whales. This pivotal branch is of particular importance in providing baseline comparative data for understanding the evolutionary history of the other species of toothed whales. Sperm whales provide information on the origin of various morphological characters that permit suction feeding and the adaptive role of these features in the early evolution of toothed whales.

Perhaps most importantly, phylogenies predict current properties of organisms. For example, as discussed by Promislow (1996), it has been noted that some toothed whales (e.g., pilot whales, Globicephala spp. and killer whales, Orcinus orca) that have extended parental care also show signs of reproductive aging (i.e., pregnancy rates decline with increasing age of females), whereas baleen whales (e.g., fin whales) demonstrate neither extended parental care nor reproductive aging (Marsh and Kasuya, 1986). Phylogenetic inference predicts that these patterns would hold more generally among other whales and that we should expect other toothed whales to show reproductive aging. We look forward to readers exploring the large-scale patterns of diversification seen in marine mammals as well as hypotheses about processes underlying these patterns.

Finally, the reconstruction of phylogenies provides a useful foundation from which to study other biological patterns and processes. Numerous examples of the use of a phylogenetic tree to consider the evolution of characters among marine mammals exist including the evolution of feeding in pinnipeds (Adam and Berta, 2002); body size in phocids (Wyss, 1994); diving capacity in pinnipeds, cetaceans, and sirenians (Mirceta et al. 2013); large eyes and deep diving in pinnipeds (Debey and Pyenson, 2013); pinniped recognition behavior (Insley et al. 2003); pelage coloration in pinnipeds (Caro et al. 2012); hearing in whales (Nummela et al. 2004); hindlimb loss in cetaceans (Thewissen et al. 2006); and suction feeding in cetaceans (Johnston and Berta, 2011). Male social behavior among cetaceans has also been studied using a phylogenetic approach (Lusseau, 2003), and Kaliszewska et al. (2005) explored the population structure of right whales (Eubalaena spp.) based on genetic studies of lice that live in association with these whales.

2.2. Some Basic Terminology and Concepts

The discovery and description of species and the recognition of patterns of relationships among them is founded on the concept of evolution. Patterns of relationships among species are based on changes in the features or characters of an organism. Characters are diverse, heritable attributes of organisms that include DNA base pairs that code for anatomical and physiological features and behavioral traits. Two or more forms of a given character are termed the character states. For example, the character locomotory pattern might consist of the states alternate paddling of the four limbs (quadrupedal paddling), paddling using the hindlimbs only (pelvic paddling), lateral undulations of the vertebral column and hindlimb (caudal undulation), or vertical movements of the tail (caudal oscillation). Evolution of a character may be recognized as a change from a preexisting, or ancestral (also referred to as plesiomorphic or primitive), character state to a new derived (also referred to as apomorphic) character state. For example, in the evolution of locomotor patterns in cetaceans, the pattern hypothesized for the earliest whales is one in which they swam by paddling with the hindlimbs. Later diverging whales modified this feature and show two derived conditions: (1) lateral undulations of the vertebral column and hindlimbs and (2) vertical movements of the tail.

The basic tenet of phylogenetic systematics, or cladistics (from the Greek word meaning branch), is that shared derived character states constitute evidence that the species possessing these features share a common ancestry. In other words, the shared derived features or synapomorphies represent unique evolutionary events that may be used to link two or more species together in a common evolutionary history. Thus, by sequentially linking species together based on their common possession of synapomorphies, the evolutionary history of those taxa (named groups of organisms) can be inferred.

Relationships among taxonomic groups (e.g., species) are commonly represented in the form of a cladogram, or phylogenetic tree, a branching diagram that conceptually represents the best estimate of phylogeny (Figure 2.1). The lines or branches of the cladogram are known as lineages or clades. Lineages represent the sequence of ancestor–descendant populations through time. Branching of the lineages at nodes on the cladogram represents speciation events, a splitting of a lineage resulting in the formation of two species from one common ancestor. Trees can be drawn to display the branching pattern only or, as in the case of molecular phylogenetic trees, patterns drawn with proportional branch lengths that correspond to the amount of evolution (approximate percentage sequence divergence) between the two nodes they connect.

The task in inferring a phylogeny for a group of organisms is to determine which characters are derived and which are ancestral. If the ancestral condition of a character or character state is established, then the direction of evolution, from ancestral to derived, can be inferred and synapomorphies can be recognized. The methodology for inferring direction of character evolution is critical to cladistic analysis. Outgroup comparison is the most widely used procedure. It relies on the argument that a character state found in close relatives of a group (the outgroup) is likely also to be the ancestral or primitive state for the group of organisms in question (the ingroup). Usually more than one outgroup is used in an analysis, the most important being the first or genealogically closest outgroup, called the sister group. However, in many cases, the primitive state for a taxon can be ambiguous. The primitive state can only be determined if the primitive states for the nearest outgroup are easy to identify, and those states are the same for at least the two nearest outgroups (Maddison et al. 1984).

Figure 2.1  A cladogram illustrating general terms discussed in the text.

Using the previous example, determination of the primitive cetacean locomotor pattern is based on its similarity to that of an extinct relative to the cetaceans, a group of four-legged even-toed hoofed mammals known as the raeollids (i.e., an outgroup), which are thought to have used all four limbs to wade or walk on shallow sea bottoms. Locomotion in whales went through several stages. Ancestral whales (i.e., Ambulocetus) swam by pelvic paddling propelled by the hindlimbs only. Later diverging whales (i.e., Kutchicetus) went through a caudal undulation stage, propelled by the feet and tail. Finally, extinct dorudontid cetaceans and extant whales adopted caudal oscillation using vertical movements of the tail as their swimming mode (Figure 2.2; Fish, 1993).

Derived characters are used to link monophyletic groups, groups of taxa that consist of a common ancestor plus all descendants of that ancestor. In contrast to a monophyletic group, paraphyletic and polyphyletic groups (designated by quotation marks) include a common ancestor and some, but not all, of the descendants of that ancestor. A real example of a paraphyletic group is the recognition of an extinct group of cetaceans known as archaeocetes. A rapidly improving fossil record and phylogenetic knowledge of whales now support the inclusion of archaeocetes as the ancestors of both baleen whales and toothed whales rather than as a separate taxonomic category (e.g., Thewissen et al. 1996). In a polyphyletic group, taxa that are separated from each other by more than two ancestors are placed together without including all the descendants of their common ancestor. For example, recent molecular data support river dolphins as a polyphyletic group because the Ganges or Indian river dolphins (Plantanista spp.) do not share the same common ancestor as other river dolphins (Figure 2.3).

Figure 2.2  Distribution of character states for locomotor patterns among cetaceans. Illustrated by C. Buell.

Monophyletic groups can be characterized in two ways. First, a monophyletic group can be defined in terms of ancestry, and second, it can be diagnosed in terms of characters (see Appendix). For example, whales or cetaceans can be defined as including the common ancestor of Pakicetus (an extinct whale) and all of its descendants including both modern toothed and baleen whales. Note that this definition is based on ancestry and does not change because there will always be a common ancestor for whales. On the other hand, cetaceans can be diagnosed by a number of characters (e.g., the shape of the skull and the morphology of the cusps on posterior teeth; see also Chapter 4). The usefulness of the distinction between definition and diagnosis is that, although the definition may not change, the diagnosis can be altered to reflect changes in our knowledge of the distribution of characters. New data, new characters, or reanalysis of existing characters can modify the diagnosis. For example, in the early 1990s discoveries of new fossil cetaceans (e.g., Ambulocetus and Rodhocetus) have provided new characters illuminating the transition between whales and their closest ungulate relatives. The definition of Cetacea has not changed, but the diagnosis has been modified according to this new character information. A third term also used in this book, characterization, refers to a list of distinguishing features, both shared primitive and shared derived characters, that are particularly useful in field or laboratory identification of various species.

Figure 2.3  Alternative hypotheses for the phylogeny of river dolphins. (a) Molecular view supporting river dolphin polyphyly. (b) Morphological view of river dolphin monophyly. Illustrated by C. Buell.

Important concepts when defining members of a monophyletic group or clade are stem and crown groups. A crown group is the smallest monophyletic group, or clade, to contain the last common ancestor of all extant members, and all of that ancestor’s descendants. For example, the crown group Cetacea or Neoceti is the clade of living whales. Some taxa fall close to but outside a particular crown group. A good example is the fossil whale Dorudon, which can be classified within the stem group of Cetacea along with all of the other extinct ancestral forms that are closely related, excluding living forms (Figure 2.2).

A concept critical to cladistics is that of homology. Homology can be defined as the similarity of features resulting from common ancestry. Two or more features are homologous if their common ancestor possessed the same feature. For example, the flippers of a seal and the flippers of a walrus are homologous as flippers because their common ancestor had flippers. In contrast to homology, similarity not due to homology is termed homoplasy. The flippers of a seal and the flippers of a whale are homoplasious as flippers because their common ancestor lacked flippers. Homoplasy may arise in one of two ways: convergence (parallelism) or reversal. Convergence is the independent evolution of a similar feature in two or more lineages that often share similar ecological challenges (e.g., the need to swim well to forage). Thus, seal flippers and whale flippers evolved independently as swimming appendages; their similarity is homoplasious by convergent evolution. Recent research provides molecular evidence for convergence among bats and dolphins in numerous genes related to hearing and vision (e.g., Parker et al. 2013). Reversal is the loss of a derived feature coupled with the reestablishment of an ancestral feature. For example, in phocine seals (e.g., Erignathus, Cystophora, and the Phocini) the development of strong claws, lengthening of the third digit of the foot, and de-emphasis of the first digit of the hand are character reversals because none of them characterize ancestral phocids, but these features are present in terrestrial arctoid carnivores.

It is a common, but incorrect, practice to refer to taxa as being either primitive or derived. This is deceptive, because individual taxa that have diverged earlier than others may have undergone considerable evolutionary modification on their own relative to taxa that have diverged later in time. For example, otariid seals have many derived characters, although they diverged earlier than phocid seals. In short, taxa are not primitive, although characters may be.

2.3. How Do You Build a Phylogenetic Tree?

A phylogeny or cladogram represents a hypothesis about evolutionary relationships. They are constructed using the following steps:

1. Choose the taxa. Select a group whose evolutionary relationships interest you. Name and define all taxa for that group. Assume that the taxa are monophyletic.

2. Determine the characters. Select and define characters and character states for each taxon.

3. Determine the polarity of characters. For each character, determine which state is ancestral (primitive) and which is derived and arrange the characters and their states in a data matrix (see example in Table 2.1). This latter step is done using outgroup comparisons. For example, if the distribution of character #1, thick fat layers of the skin, is taken into consideration, two character states are recognized: absent and present. In Table 2.1, the outgroup (bears) have the former condition, which is equivalent to the ancestral state. This same state is also seen in one of the ingroup taxa, the fur seals and sea lions. The other ingroup taxa have thick fat layers present, which is a synapomorphy that unites walruses and seals to the exclusion of fur seals and sea lions.

Table 2.1

Data Set for Analysis of Recent Pinnipeds Plus an Outgroup Showing Five Characters and their Character States

4. Group taxa by synapomorphies. Construct all possible phylogenies by sequentially grouping taxa based on the common possession of one or more shared derived character states (circles around character states in Table 2.1) and choose the one that has the most shared derived character states distributed among monophyletic groups (Figure 2.4(b)). Note that the tree in Figure 2.4(a) shows no resolution of relationships among taxa, referred to as a polytomy, and that the trees in Figure 2.4(c) and (d) show mostly characters that are unique to one taxon and tell us nothing about relationships among the different taxa.

Figure 2.4  Four possible cladograms of relationship and character-state distributions for the three ingroups listed in Table 2.1 . Part b has the most shared, derived characters.

The use of molecular characters (i.e., nucleotide sequence data) to reconstruct phylogenies follows the same logic as other types of character data. Molecular data chosen for this purpose should be nonrecombinant, maternally inherited alleles, or fixed attributes, and most phylogenies are derived using sequences from homologous genes. Recently, comparison of whole genomes has been used to reconstruct phylogenies. Nevertheless, whether using part or all of the genome, the next step involves generating sequences from these sources. The main repository for these sequences is the public nucleotide database (e.g., GenBank in the US). Third, align the sequences. This is based on the assumption that sequence similarity equals sequence homology. This is a critical step, and the identification of homologous nucleotide sequences can be as difficult in molecular phylogeny as it is in morphological studies. Finally, construct trees from the aligned sequence data.

2.4. Testing Phylogenetic Hypotheses

An important aspect of the reconstruction of phylogenetic relationships is known as the principle of parsimony. The basic tenet of the principle of parsimony is that the cladogram that contains the fewest evolutionary steps, or changes between character states of a given character summed for all characters, is accepted as being the best estimate of phylogeny. For example, for all of the possible cladograms for the data set of Table 2.1, the one illustrated in detail in Figure 2.5(a) is the shortest because it contains the fewest evolutionary steps.

An alternative method to parsimony that is most often used with molecular data is maximum likelihood. This method is based on assumptions about how characters evolve. The approach begins with a mathematical formula that describes the probability that different types of nucleotide substitutions will occur. Given a particular phylogenetic tree with known branch lengths, a computer program can evaluate all possible tree topologies and compute the probability of producing the observed data, given a specified model of character change. This probability is reported as the tree’s likelihood. The criterion for accepting or rejecting competing trees is to choose the one with the highest likelihood. One advantage of this approach is that by giving an exact probability for each tree this method facilitates quantitative comparison among trees. Closely related to likelihood methods are Bayesian methods for inferring phylogenies (Hulsenbeck et al. 2001). Bayesian inferences of phylogeny employ a Markov chain Monte Carlo algorithm to solve the computation aspects of sampling trees according to their posterior probabilities. The posterior probability of a tree can be interpreted as the probability that the tree is correct. To obtain posterior probabilities this approach requires a likelihood model and various parameters (e.g., phylogeny, branch lengths,