Annalisa Berta

Chapter 3: Pinnipedimorph Evolutionary Biogeography

Abstract Previous hypotheses for the origin and diversification of pinnipeds have followed a narrative approach based mostly on dispersalist (i.e., center of origin) explanations. Using an analytical approach, we present a testable hypothesis to explain the evolutionary biogeography of pinnipedimorphs (fur seals, sea lions, walruses, seals, and their fossil relatives) based on both dispersal and vicariant events in the context of a species-level phylogenetic framework. This integrated hypothesis considers many lines of evidence, including physical and ecologic factors controlling modern pinniped distributions, past geologic events related to opening and closing of seaways, paleoceanographic models, the improving pinniped fossil record, and pinniped phylogenetic analyses based on both morphologic and molecular data sets. Oceanic biogeographic regions and faunal provinces are defined and oceanic circulation patterns discussed with reference to the distribution of extant and fossil species. Paleobiogeographic hypotheses for each of the major pinniped lineages are presented using area cladograms and paleogeographic maps showing oceanographic and tectonic changes during successive intervals of the Cenozoic. Our biogeographic hypothesis supports an eastern North Pacific origin for pinnipedimorphs during the late Oligocene coincident with initiation of glaciation in Antarctica. During the early Miocene, pinnipedimorphs remained restricted to the eastern North Pacific, where they began to diversify. Otariids (fur seals and sea lions) are first known from the late Miocene in the North Pacific, where they remained restricted until the late Pliocene. A transequatorial dispersal into the western South Pacific at this time preceded the rapid diversification of this group that occurred during the Pleistocene in the Southern Ocean. Odobenids (walruses) evolved in the North Pacific during the late early Miocene and underwent dramatic diversification in the late Miocene with later members of the odobenine lineage dispersing into the North Atlantic, most likely via an Arctic route. Extinct archaic phocoids, the desmatophocids, known only from the early to late Miocene, were confined to the eastern and western North Pacific. Phocids, although postulated here to have a North Pacific origin, are first known as fossils from the middle Miocene in the eastern and western North Atlantic region, as well as the Paratethys. Both monachine and phocine seals are distinct lineages beginning in the middle Miocene in the eastern and western provinces of the North Atlantic. During the late Miocene, phocids underwent a dramatic diversification. The early biogeographic history of phocine seals is centered in the Arctic and North Atlantic. Subsequent dispersal of phocines into the Paratethys and Pacific occurred during the Pleistocene. In contrast, monachine seals have a southern hemisphere center of diversity, especially the lobodontines of the Southern Ocean. Southern dispersal of this clade most likely occurred through the Neogene Central American Seaway prior to its closure in the mid-Pliocene. The pagophilic nature of extant phocine and lobodontine seals is largely a function of Pleistocene glacioeustatic events.

Population Structure and Dynamics

Attempts to understand the ecology of marine mammals and the ecological roles they play in marine ecosystems necessitate the knowledge of their abundance and the trends in their numbers. Yet, despite the high levels of interest in these animals, few good estimates exist for the population sizes of marine mammals. Many marine mammal populations are broadly dispersed much of the year, and virtually all species spend considerable amounts of their time under water and are therefore unavailable to normal census methods. Hence, estimation methods for almost all marine mammal species must include estimates for the unseen portions of a population under study. There are two basic approaches for determining marine mammal abundances: total population counts or counts of a sample of individuals and extrapolation to the whole population. Techniques for the repeated identification of marine mammals include flipper tagging, photo identification, radio and satellite telemetry, and a variety of molecular genetic methods. Growth rates vary considerably between species over several orders of magnitude. Among the common causes of natural mortality in marine mammal populations are predators, parasites, diseases, and trauma.

Exploitation and Conservation

The overexploitation of whales, seals, sea cows, and sea otters has resulted in seriously reduced population sizes, the extinction of several species, and the endangered status of several others. The recognition of marine mammals as crucial natural resources and valued ecosystem components that require protection has resulted in the establishment of several international legal frameworks for their conservation. Overexploitation has resulted in the extinction of three marine mammal species: Stellers sea cow, the Atlantic gray whale, and the Caribbean monk seal. Despite the establishment of legal frameworks to address exploitation, many other species have been and continue to be affected by human activities, such as bycatch in commercial fisheries, net entanglements, and environmental contaminants. Information about mortality patterns, disease, and levels of environmental contaminants has been obtained from beached and stranded marine mammals, from studies designed to address these issues in wild populations, or from laboratory tissue studies. The future of marine mammal conservation requires better information on the population status and the relationships of marine mammals with their ecosystems, as well as greater understanding of the effects of human-induced activities.

Cetacean Evolution and Systematics

Cetaceans, together with sirenians, are the earliest recorded marine mammals—appearing in the Eocene about 53–54 Ma. Cetaceans are also the most diverse mammalian group to adapt to a marine existence. New discoveries of fossil whales provide compelling evidence for both the phylogenetic connections of cetaceans as well as the evolutionary transformation from a terrestrial to a fully aquatic existence. Most morphologic and all molecular data are in general agreement that artiodactyls are the closest relatives of cetaceans. Odontocete monophyly is also widely accepted. There is evidence that some archaic mysticetes possessed both teeth and baleen. Later, diverging mysticetes lost teeth but retained baleen. The relationships among modern families of baleen whales are unclear because of conflicting morphological results versus molecular data. The relationships among odontocetes are no less controversial. However, there is general agreement of both molecular and morphological data that beaked whales and sperm whales are basal odontocetes. The divergence estimates for baleen and toothed whales from a common archaeocete ancestor approximate 35 Ma based on molecular data that are in accord with the fossil record.

Diet, Foraging Structures, and Strategies

This chapter examines the diets of marine mammals, and several of the more obvious structural and behavioral specializations employed by marine mammals to capture their prey. The foraging energetics and the anatomy and physiology of digestion are also examined. Marine mammal diets and foraging strategies are direct consequences of the patterns of primary productivity, although most species prey on relatively large animals several trophic levels from the primary producers. Research on the foraging activities of marine mammals is difficult because feeding typically occurs below the sea surface. Standard approaches to analyzing foraging behavior, in addition to direct observations of predators pursuing and capturing prey, include stomach content analysis of dead, stranded, or net-entangled animals; stomach lavage of healthy restrainable animals; studies of fecal remains; and dietary patterns derived from stable isotope signatures in various tissues. The cheek teeth of pinnipeds and odontocetes are typically homodont with single pointed cusps adapted for feeding on fish and squid. Walruses employ a suction feeding strategy using the tongue as a piston to suck clams out of their shells. Tusks are used in social display rather than for feeding. The seasonal migration of the elephant seal, one of the best-studied feeding patterns among pinnipeds, involves an annual double migration with prolonged periods of offshore feeding. A specialized suction feeding strategy evolved independently in several pinniped lineages.

Sirenians and Other Marine Mammals: Evolution and Systematics

Sirenians (manatees and the dugong) are defined using anatomical characters. The affinities, origin, and diversification of both stem and crown sirenians are reviewed. The evolutionary history of other marine mammals (i.e., marine otters and polar bear) are discussed including the only known wholly extinct order of marine mammals, the desmostylia. Brief summary is also provided of the evolutionary history of an extinct aquatic sloth and members of two living carnivore groups, the polar bear and marine otters.

Musculoskeletal System and Locomotion

This chapter focuses on comparing and considering variations in the musculoskeletal anatomy of the major marine mammal groups, especially as it relates to locomotion. Propulsion for swimming in marine mammals is derived from paired flipper movements or vertical movements of the caudal flukes. Paired flipper propulsion is more efficient at low speeds when maneuverability is critical. The evolution of locomotion in each of the major groups of marine mammals is also reviewed. Large orbits, a relatively short snout, a constricted interorbital region, and large orbital vacuities characterize the pinniped skull. The modern walrus skull is easily distinguished from that of other pinnipeds by being foreshortened and having large maxillae for accommodation of the upper canine tusks. The axial skeleton is differently developed among otariids, phocids, and the walrus. The cetacean skull differs profoundly from the typical mammalian skull because it is telescoped—the result of migration of the external narial opening to a dorsal position on the skull. In cetaceans, the vertebral column does not contain a sacral region because the pelvic girdle is absent. The subdermal connective tissue sheath provides an enlarged surface to anchor the flexor and extensor muscles of the fluke. The elbow joint of modern cetaceans is uniquely immobile. The sirenian skull is distinguished from that of other marine mammals by its down-turned premaxilla. The skull is more sharply inclined in the dugong than in manatees. Terrestrial locomotion involves walking and running, with the large paws helping in weight distribution.

Sound Production for Communication, Echolocation, and Prey Capture

This chapter deals with the production, transmission, and reception of the sounds produced by vocalizing marine mammals in air and under water. The manner in which vocalizations are produced and received differs in the marine mammal taxa and also according to the medium in which vocalizations are produced. The purpose of vocalizations includes communicating with individuals of the same species and locating unseen targets with echolocation. The majority of airborne sounds of pinnipeds are produced in the larynx. Other airborne pinniped vocalizations include those of the walrus, produced by the teeth and throat pouches. Echolocation involves producing short duration sounds (clicks) and listening for reflected echoes as sounds bounce off objects. The echolocation abilities of toothed whales have been the subject of intense research. The source of production of echolocation sounds has been determined to be a structural complex associated with the upper nasal passages (MLDB complex). The periodic opening and closing of monkey lips break up the airflow between the lips and determine the click repetition rate. In air, vocalizations of pinnipeds include mother–pup calls and those used to communicate breeding status. Underwater sounds of pinnipeds range from the soft lyrical sounds of the leopard seal to the aggressive sounding grunts, barks, and groans of most other phocids. Sirenian vocalizations described as chirps and squeaks, which are short-frequency modulated signals, are identified. The issue of how anthropogenic sound affects marine mammals is contentious, and additional research is necessary to address the gaps in the current understanding of this issue.

Chapter 7 – Integumentary and Sensory Systems

This chapter summarizes the functional anatomy and physiology of the integumentary and sensory systems of marine mammals. The review of the integumentary system includes description of components of the system (i.e., skin, hair, glands, vibrissae, and claws). Discussion of the nervous system highlights how relative brain size is measured (and what it means) and how enlargements of different segments of the spinal cord are correlated with different patterns of locomotion. Similarities and differences among marine mammals with respect to the development of the visual, olfactory, and taste sensory systems are also described in this chapter.

Chapter 14 – Population Structure and Dynamics

The chapter reviews abundance and its determination in marine mammals and techniques for monitoring populations (i.e., photo identification, telemetry, and molecular genetics). Also considered are growth rates, age of sexual maturity, and age determination and longevity. The chapter concludes with brief review of natural mortality in marine mammals (i.e., disease, competition, and predators).