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Lambertsen, R. H. (1983). Internal mechanism of rorqual feeding. J. Mammal. 64(1), 76–88. Mead, J. G. (1975). Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia: Cetacea). Smithson. Contrib. Zool. 207, 1–72. Mead, J. G., and Fordyce, R. E. (in press, 2008). The Therian Skull—a lexicon with emphasis on the odontocetes. Smithson. Contrib. Zool. 627. Miller, G. S., Jr. (1923). The telescoping of the cetacean skull. Smithson. Miscell. Collect. 76(5), 1–71. Molvaer, O. I. (2003). Otorhinolaryngological aspects of diving. In “Bennett and Eliot’s Physiology and Medicine of Diving” (A. O. Brubakk, and T. S. Neuman, eds), 5th ed. Saunders, New York. Moore, W. J. (1981). “The Mammalian Skull.” Cambridge University Press, New York. Nickel, R., Schummer, A., Seiferle, E., Wilkens, H., Wille, K.-H., and Frewein, J. (1986). “The Locomotor System of the Domestic Mammals.” Verlag Paul Parey, Berlin. Norris, K. S., and Harvey, G. W. (1974). Sound transmission in the porpoise head. J. Acoust. Soci. Am. 56(2), 659–664. Pabst, D. A., Rommel, S. A., and McLellan, W. A. (1999). Functional morphology of marine mammals. In “Biology of Marine Mammals” (J. E. Reynolds, and S. A. Rommel, eds), pp. 15–72. Smithsonian Institution Press, Washington, D.C. Pivorunas, A. (1979). The feeding mechanisms of baleen whales. Am Sci. 67, 432–440. Popesko, P. (1979). “Atlas of Topographical Anatomy of the Domestic Animals.” Saunders, Philadelphia. Reidenberg, J. S., and Laitman, J. T. (1994). Anatomy of the hyoid apparatus in Odontoceti (toothed whales): specializations of the skeleton and musculature compared with those of terrestrial mammals. Anat. Rec. 240, 598–624. Reynolds, J. H., Odell, D. K., and Rommel, S. A. (1999). Marine mammals of the world. In “Biology of Marine Mammals” (J. E. Reynolds, and S. A. Rommel, eds), pp. 1–14. Smithsonian Institution Press, Washington, D.C. Romer, A. S., and Parsons, T. S. (1977). “The Vertebrate Body.” Saunders College, Philadelphia. Rommel, S. A. (1990). Osteology of the bottlenose dolphin. In “The Bottlenose Dolphin” (S. Leatherwood, and R. R. Reeves, eds), pp. 29–49. Academic Press, San Diego, CA. Rommel, S. A., Costidis, A. M., Fernandez, A., Jepson, P. D., Pabst, D. A., McLellan, W. A., Houser, D. S., Cranford, T. W., van Helden, A. L., Allen, D. M., and Barros, N. B. (2006). Elements of beaked whale anatomy and diving physiology, and some hypothetical causes of sonarrelated stranding. J Cetacean Res. Manage. 7, 189–209. Schaller, O. (1992). “Illustrated Veterinary Anatomical Nomenclature.” Ferdinand Enke Verlag, Stuttgart. Werth, A. J. (2004). Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. J. Exp. Biol. 207, 3569–3590.

Sociobiology FRITZ TRILLMICH I. The Nature of Sociobiological Inquiry

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ociobiology is the study of social behavior and social evolution based on the theory of adaptation through selection. As such it is primarily concerned with the adaptiveness of social behavior and the selective processes producing and maintaining adaptiveness. Understanding the selective processes involved includes studying the ecology, physiology, and behavior, as well as the demography and

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population genetics, of the species in question. Sociobiological investigation also increasingly attempts to characterize the genetic breeding system, as well as the population dynamics and structure, which importantly influence the effectiveness of evolutionary processes in molding species characteristics. The sociobiological approach assumes that selection at the individual level is the force producing adaptation. A proper understanding of social phenomena, therefore, needs an understanding of the benefits and costs that the individual derives from its interaction with the social environment. Explicitly, group selection is relegated to a secondary position as in most circumstances selection operates more strongly at the individual than at the group level because fertility, dispersal, and mortality events are more frequent and act much more forceful on individuals than on groups. Explaining social phenomena such as group formation, parental care, and mating systems from the action of selection at the level of the individual forms the core of sociobiological inquiry. As the majority of sociobiological research in the field of marine mammals has been done on whales and pinnipeds, these two groups form the focus of the following sections. Relevant information on sea otters (Enhydra lutris) and manatees (Trichechus spp.) is mentioned briefly in Section V.

II. Group Formation The most obvious phenomenon of social life is group formation. Suitable feeding or breeding habitat may initially lead to an aggregation of individuals, thus setting the stage for selective processes molding the evolution of elaborate social interactions. In contrast to the term “aggregation,” “group” implies that individuals come together to derive benefits from interactions that follow from this proximity. Such a grouping may serve social, foraging, predator avoidance, or defense against predators. Groups may also be established for mating and to share parental care. These kinds of advantages constitute the selective processes that promote group formation in a wide variety of animals. Sociobiology tries to explain groupings from the advantages and disadvantages incurred by individuals (Krause and Ruxton, 2002).

A. Whales The open ocean habitat offers few options for hiding from predators. Consequently, predation by large sharks and killer whales (Orcinus orca), particularly on newborns, is one important factor selecting for group formation in whales and dolphins. Direct observational evidence for this hypothesis is scarce, but signs of scarring provide evidence of frequent encounters with predators. For example, about one-third of all humpback whale (Megaptera novaeangliae) calves carry tooth marks on their flukes when arriving in the foraging areas, presumably from encounters with killer whales or sharks during migration to the feeding grounds (Mann et al., 1999). The most spectacular groupings are found in open ocean species such as spotted dolphins (Stenella spp.) which benefit most from the advantages of grouping as protection against predators, but such species may also benefit from group foraging. Several effects play a role in the protection offered to an individual by a group. The “dilution effect” acts by reducing the probability of an individual to be attacked by a predator who has noticed the group, if the predator takes only one individual out of the group. This effect thus dilutes the chances of an attack on a given individual dramatically (to 1/group size). The “confusion effect,” many individuals rushing back and forth through the visual field of an attacking

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predator, makes it more complicated for the predator to concentrate on one prey to catch. Finally, animals in the middle of a group can in effect use other individuals around them as shields against predatory attack, as there will always be other individuals geometrically closer to a predator that attacks from the edge of a group. This is the so-called “geometry of the selfish herd,” which allows an individual to use other group members as protection. These effects may also partly protect individuals in groups against parasites, such as the cookie cutter shark (Isistius brasiliensis), which takes little bites out of the side of its victim. The advantages of grouping using dilution, confusion, or cover against predation do not depend on individual recognition or social bonds among individuals, but also function perfectly well in a totally anonymous group. Eventually, the advantage of gaining protection in the group will be counteracted by increasing food competition among individuals in a large group and will thereby determine the upper size of groups. Because food competition depends on abundance, distribution, and behavior of food organisms, which are little known for whale prey, the importance of food competition is largely unknown. However, signs of territorial behavior between killer whale groups provide at least some evidence for the role of food competition in limiting group size. For more powerful animals such as killer and sperm whales (Physeter macrocephalus), grouping offers the additional option to defend smaller, more vulnerable individuals against predators by taking them into the middle of the group. This kind of group action has a completely different quality than the examples given earlier because it involves bonds among the individuals in the group, which are presumably well cemented by individual recognition. Individuals in these groups actively take some risk to defend others, mostly calves, against predators. This has traditionally been explained by the fact that the individuals involved in such cooperative behaviors are kin to each other (Hamilton, 1964). However, it may also be based on mutualistic cooperation or group augmentation (Kokko et al., 2001). The evolution of mutualism would be eased in kin groups through kin selection, but group augmentation involves a different mechanism. Here individuals attach to a group because survival and reproduction are enhanced or only possible in the protection of a group. However, grouping can also be of advantage for a predator. Foraging groups have perhaps been best analyzed for killer whales. For the mammal-hunting the so-called transient killer whales in British Columbia, groups of three individuals proved most efficient in terms of energy intake per unit time when hunting harbor seals (Phoca vitulina) (Baird and Dill, 1996). Optimal efficiency of this group size results because a group of three cooperatively hunting whales seems to be better at detecting and catching prey than single animals or duos. At the same time, competition in such a small group is less than in a larger group, once it comes to sharing a harbor seal carcass. For more evasive prey such as Dall porpoise (Phocoenoides dalli), larger groups may be more successful because more animals are better at intercepting fleeing prey. Dusky dolphins (Lagenorhynchus obscurus) herd schools of fish cooperatively toward the surface and presumably thereby increase food intake. Such activities have also been observed in other dolphins that herded fish schools into bays or against fishing nets and thereby may increase food intake for all individuals in the group. Social systems in whales differ widely between mysticetes and odontocetes. Mysticetes often live solitarily and, except for the mother–calf association during the rearing period, show little evidence of long-term social bonds. This is most likely caused by the nature of their food resources and the fact that due to their body size they have largely escaped predation. They may, however, aggregate during

feeding in particularly productive areas and during the mating season (see Section IV). In contrast, almost all odontocetes are quite social. The social groupings of sperm whales, killer whales, pilot whales (Globicephala spp.), and bottlenose dolphins (Tursiops spp.) are best documented. In whales, groupings represent matrilines in which male offspring may (in killer and pilot whales) or may not (sperm whales) remain for life. In sperm whales, the grouping of kin serves protection of offspring. During foraging, these animals routinely dive to 400 m depth and stay at depth for 40–60 min. During this period, young would be unprotected, waiting at the surface. This is avoided by adults in a group staggering their diving in such a way that one or more adults almost always attend the calves at the surface. Clearly, such behavior provides indirect fitness gains if the individuals in a group are relatives (such as mother, daughter, granddaughter). Kin selection effects may also explain the lack of dispersal of young in killer whales (in this case of both sexes). In resident, fish-eating groups, male offspring in a matrilineal group may offer protection to relatives as well as help in the defense of foraging areas. Females that stay with their mother may likewise gain fitness from cooperation with close relatives. The size of the group will be limited by food competition, and indeed large groups split up, when they have grown too much, into smaller units along matrilineal kinship lines. Limitation of group size by the potential for food competition is particularly evident, as the so-called transient, mammal-eating groups are much smaller (no more than three–five animals) than those of fish-eating residents, presumably because otherwise the disadvantage of food competition would offset the advantage of close cooperation with kin. Pilot whales show a similar social structure where male and female offspring stay with mothers (Amos et al., 1993). Advantages and disadvantages of this social structure are less understood for the pilot whale than for the other species mentioned previously. Bottlenose dolphins and some other inshore odontocetes live in quite open fission–fusion societies in which females associate frequently with many different partners. These associations may be useful in foraging or vigilance and maybe defense against predators, but the last hypothesis seems less likely because females with calves tend to be less gregarious. Whether this is due to food competition is unclear. Females may also sometimes group to avoid harassment by males (see Section IV). Male associations vary between study sites and seem to serve mating purposes (Mann et al., 1999).

B. Pinnipeds As a group, pinnipeds are characterized by an amphibious lifestyle. They forage at sea but females need to return to a firm substrate, land or ice, for parturition. A strong selective force during this period of birth and subsequent pup rearing is predation on mother and pup. In land-breeding pinnipeds, mostly otariids but also elephant seals (Mirounga spp.), monk seals (Monachus spp.), and the largest populations of gray seals (Halichoerus grypus), predator avoidance has led to the choice of predator-free oceanic islands for breeding. In comparison to the wide expanse of ocean used for foraging, these islands are limited in area, automatically leading to high densities of females on land. Otariid females come into estrus shortly after parturition, which sets the stage for sexual selection on males trying to station themselves in these female aggregations to breed (see Section IV). Primarily, the concentration of females on land has all the characteristics of an aggregation, but females of most land-breeding species stay closer together than necessitated by available habitat. Indeed,

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sea lion colonies were found to show internal social network structure (Wolf et al., 2007). One reason for such active groupings may be to avoid harassment by ardent males trying to mate with females (Bartholomew, 1970; Trillmich and Trillmich, 1984). In addition, subadult males of some species of otariids abduct and herd pups, molesting them to the extent that they may die. In this dangerous situation, grouped pups profit from the dilution effect, which might select for tighter grouping of females (Campagna et al., 1992). Thermoregulation may also further grouping: Sea lions and the South African (Arctocephalus pusillus pusillus) and Australian (A. p. doriferus) fur seals tend to rest in body contact after leaving the water, which may serve to keep the body shell warm at minimal metabolic cost to the individual. This is not necessary for a fur seal with its highly insulating, air-trapping fur, and the function of clumping in the South African and Australian fur seal is therefore doubtful. In contrast, ice-breeding seals tend to be more widely dispersed, be it on pack ice or fast ice. In these species, different factors select for some gregariousness. Most important for many species is predation: in the Arctic by polar bears (Ursus maritimus) and in the Antarctic by leopard seals (Hydrurga leptonyx) and killer whales. Some kind of a grouping advantage is perhaps operating that might equally benefit animals resting between foraging excursions and animals breeding on the ice. Indeed, harp seals (Pagophilus groenlandicus) are well known for breeding—even if dispersed—in well-defined local concentrations. It is not certain whether these concentrations are true social groupings or could also be induced by the characteristics of the ice in combination with the food resources below it, i.e., are aggregations due to resource distribution. It may actually be a combination of both. Weddell seals (Leptonychotes weddellii) group around tide cracks in fast ice, which offer holes for entry into the water where the seals forage under the ice. Because suitable holes are limited, this leads to a concentration of animals around entry holes and importantly influences the mating system. Principally, pinnipeds are solitary foragers. There is little evidence for social foraging except occasional observations of sea lions herding fish into bays and communally preying on the trapped schools of fish. Aggregations of foraging sea lions and fur seals occur quite frequently near large fish schools where pinnipeds, birds, and whales may gather in so-called feeding frenzies. True cooperativity in these aggregations has not been demonstrated. This does not exclude that loose groups of pinnipeds may be more likely to locate food and through signs of foraging activity attract other animals to the site, an advantage frequently exploited by group-foraging birds.

III. Parental Investment Strategies There is no convincing evidence of paternal investment in the rearing of young in any whale or pinniped. Lack of paternal care is typical for the majority of mammals and reflects that females alone provide for offspring during pregnancy and lactation, which frees males of parental duties (Clutton-Brock, 1991). Only in a few whale societies, e.g., killer whale matrilineal groups, males—most likely never the fathers of young in the group—act as helpers in defense and perhaps feeding of young. Maternal strategies in whales and pinnipeds are characterized by massive energetic investment in young through the production of large precocial young and extremely lipid-rich milk. However, parental investment is measured not by energy expenditure, but rather by a reduction in future fitness, a cost incurred by the mother through a loss in subsequent fertility or an increase in mortality due to a expenditure that benefits the offspring by increasing its fitness

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(Trivers, 1972). Evidence of parental investment, so defined, is rare in whales and pinnipeds. The patterning of parental effort differs widely between mysticete whales and odontocetes. Mysticete females gather the material and energy for pregnancy (lasting about 1 year) and lactation during a feeding season of about half a year when food is plentiful and starve for the other half-year. Extraordinary fast fetal growth rates in blue whales (Balaenoptera musculus, 27 mm/day) permit even the largest mysticete whale—with the exception of the bowhead (Balaena mysticetus), sei (Balaenoptera borealis), and gray (Eschrichtius robustus) whale—to produce a calf within 1 year. By migrating to warmer oceans in the non-feeding period, mysticete whale females seem to minimize the metabolic overhead for themselves and newborn and sucking calves. Females suckle their young for a short period of 6–8 months on very lipid-rich milk, which is produced from maternal body stores, and wean abruptly. After lactation, mothers need to replenish body reserves, which usually takes a year. Females, therefore, generally breed every other or every third year. Females of the tropical Bryde’s whale (Balaenaptera edeni) have similar gestation and lactation lengths but show much less of a seasonal breeding pattern. Despite the impressive energy flux involved in pregnancy and lactation in mysticetes, there is no strong evidence that this reproductive effort incurs fitness costs. In other words it does not constitute parental investment, for example, by reducing the probability of a successful pregnancy in the year following lactation. Large odontocetes have pregnancy periods lasting longer than 1 year and take 8–36 months to wean their young, but reports on 13-year-old sperm whales with milk in their stomachs also exist. All larger odontocetes need more than a year to wean. Females consequently need much longer than 2 years to complete one reproductive cycle. The long period of nursing, even in dolphins, allows young to profit from the milk supply while gradually developing independent hunting skills. It is presently speculated that the difference in rearing strategy between the two groups depends largely on the difference in hunting strategy. Mysticetes prey on small schooling prey, which are supposedly easy to catch for recently weaned young, particularly since weaning seems to coincide with the annual peak abundance of prey. In contrast, odontocetes hunt large prey individually, which forces them to use more complex foraging tactics. They may need to learn more about prey distribution and behavior before young can feed themselves successfully. This may even involve teaching by mothers as is likely for the technique of beaching used by southern killer whales hunting pinnipeds as observed on Southern sea lion (Otaria flavescens) breeding beaches of Argentina. Another peculiar feature of some odontocetes is the occurrence of menopause. This phenomenon was documented for short-finned pilot whales (Globicephala macrorhynchus), and killer whales. One idea about the functional significance of menopause, which finds some support in studies on humans (Mace, 2000), is that menopausal females may help their last born and previous daughters in the group through prolonged maternal and allomaternal care, respectively, and by representing a living memory of how to deal with scarce resources and rare ecological disturbances. In matrilineal societies, menopause could be selected through indirect effects on the fitness of kin if the benefit to kin was larger than the benefit an old female could gain through further reproduction. Sperm whales, long-finned pilot whales (Globicephala melas), false killer whales (Pseudorca crassidens), and bottlenose dolphins show evidence of reduced fertility with age, perhaps caused by extended periods of lactation. This change in maternal lactation strategy is expected from life history theory because old females have

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a lower reproductive value and may therefore invest more in current offspring than young females. Alternatively, prolonged lactation in older mothers might be a sign of senescence or it may be caused by a reduction in condition through previous parental care episodes and could then be considered a cost of reproduction. Despite marked sexual size dimorphism in many species, there is little evidence for sex-biased investment in sons versus daughters. In short-finned pilot whales sons may be suckled for longer than daughters. Males had milk in their stomachs up to an age of 15 years, but females only up to an age of 7 years. This fits with the observation that males grow faster than females and are consistently larger at weaning than female juveniles. Similar observations have been reported for sperm whales. If such a difference in effort expended on the two sexes were consistent in the population, one would predict from models of sex allocation (Frank, 1990) that the sex ratio at birth or at weaning should be biased toward females. There is as yet no evidence for such a sex ratio bias.

A. Pinnipeds

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Pinniped females produce one pup per year, instances of twinning are exceptional. Otariids have a postpartum estrus, whereas phocids copulate around the time of or after weaning of young. Implantation is delayed for 3–4 months and is then followed by an 8–9-month pregnancy. The young are reared on lipid-rich milk and are usually weaned at an age less than 1 year, thus allowing an annual cycle of reproduction. Pinnipeds follow one of two alternative pup-rearing strategies. Females may nurse pups for a short time, a few weeks, from body reserves and then wean abruptly. This is termed the fasting strategy and is typical for larger phocids. Smaller phocids and otariids nurse young post-partum from body reserves for a short period, in otariids lasting about 1 week. Thereafter they alternate regularly between foraging close to the colony and nursing ashore; they follow a foraging cycle strategy of pup rearing. Phocids wean pups after a shorter duration of lactation, 4–65 days, at a about 25–35% of maternal mass, whereas otariids wean after 120 days to 3 years, at 35–55% of maternal mass (Costa, 1993; Trillmich and Weissing, 2006). The rearing strategy appears to depend on both female body mass and on phylogenetic grouping (Boyd, 1998; Schulz and Bowen, 2005). The larger a female, the richer a food resource she needs to support pup rearing by foraging during lactation. This is because the energetic costs of traveling to and from the food resource and maintaining the metabolism of mother and pup during the foraging sojourn become too high for large pinnipeds to make foraging during lactation a feasible strategy. Therefore, large species separate foraging completely from lactation, store massive energy reserves during a long foraging period in rich feeding areas often far away from breeding sites, and then fuel lactation out of body reserves. Because phocid females are on average larger (median maternal mass for all species 140 kg) than otariid females (median 55 kg), this might explain why phocids usually follow a fasting strategy and otariids a foraging cycle strategy (Boyd, 1998; Schulz and Bowen, 2005; Trillmich and Weissing, 2006). The largest otariid, the Steller sea lion (Eumetopias jubatus) with a female mass around 250 kg, needs to take its unweaned young close to the foraging areas to maintain lactation by alternate foraging and suckling. Similarly, walrus (Odobenus rosmarus) females take their young to foraging areas where they are suckled while the mother can forage nearby. Ecological constraints thus play a role in shaping maternal strategy, but phylogenetic constraints also importantly influence presently found lactation strategies. Evidence is mixed that the energetic effort expended on pup rearing induces fitness costs of reproduction (Boness and Bowen,

1996; Trillmich, 1996). In the northern elephant seal (Mirounga angustirostris) primiparous—giving birth for the first time—young females are less likely to bear a pup in the year following birth than older females, thus suffering reduced fertility as a consequence of early onset of reproduction. Also, survival seems to be reduced when females first reproduce at 3 rather than 4 years of age, implying a mortality cost. However, these results were obtained at one but not another site on the Californian islands and the interpretation is not entirely clear. In otariids, Galápagos fur seal (Arctocephalus galapagoensis) females incur fitness costs of reproduction in terms of reduced fertility because they frequently lose a newborn pup when still accompanied by their previous young, be it a yearling or a 2-year-old, by the time the next pup is born. This arises because young Galápagos fur seals grow extremely slowly and therefore take unusually long, up to 3 years, to become independent of their mothers. They may suckle for a second or third year if environmental conditions are poor, and thus preclude rearing of another pup by their mother (Trillmich and Wolf, 2007). Clear evidence for a fertility cost of reproduction was also found for Antarctic fur seals (Arctocephalus gazella). Parturient females of all ages were significantly less likely to reproduce in the subsequent year than nonparturient females. In addition, females that reproduce in a given year are less likely to survive to the following year than nonreproducing females—a clear mortality cost of reproduction (Boyd et al., 1995). In this species and the northern fur seal (Callorhinus ursinus), females older than about 13 years appear to show reproductive senescence. These old females are less fertile and produce smaller newborns than prime-age females. Particularly for otariids, there is thus evidence that the high energetic effort expended by females on pup rearing indeed constitutes maternal investment because it produces fitness costs to the mother. It has been claimed repeatedly that female pinnipeds of highly polygynous species invest differentially in male and female offspring. Following sociobiological arguments, this would be expected if an increased investment in males, the larger sex showing greater variance in reproductive success would lead to a greater expected reproductive success of such males. In many polygynous pinnipeds, males are born heavier and grow faster than females. This was taken as evidence for greater maternal investment in sons. However, this is no proof of greater investment in male offspring because male pups of some otariids store less fat and produce more lean body mass than female pups. Fat has a higher energy density than lean body mass, and consequently smaller female pups may have taken as much energy from their mothers as the larger, leaner male pups. Also, the most important growth spurt determining later male adult size and probably reproductive success occurs generally after weaning, thus making it less likely that male offspring derive direct benefits for their future reproductive success from increased maternal investment (Trillmich, 1996). Nevertheless, recent data demonstrate a greater cost of male offspring at least for one otariid species (Trillmich and Wolf, 2007).

IV. Mating Systems Mammalian females are producers that are limited by the time and resources needed for pregnancy and lactation, as well as by the recovery of condition after a reproductive cycle. This constitutes strong selection to optimize acquisition and efficiency of resource use before and during reproduction. Because the maximal reproductive rate of female mammals is necessarily much lower than that of males, which in the extreme need only the time of one copulation to produce offspring, females become a limiting resource for the reproduction of males. This leads to sexual selection on males for an

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increased ability to get access to and breed with as many females as possible leading to often extreme sexual size dimorphism. In mammals such as whales and pinnipeds, where males do not contribute to the care of offspring, males are expected to conform to the description of “ardent” males, eagerly searching for females and even harassing them for copulation. Females distribute themselves in relation to the distribution of resources, food, and adequate habitat for reproduction, and males map onto this distribution of females. This difference in the selection on reproductive strategies of males and females leads to the phenomenon that quite often the sexes behave and morphologically look as if they belonged to different, competing species. Sociobiological reasoning therefore leads to the expectation that observed mating systems represent the compromise arising from the conflict of the sexes. Competition among males for access to females can take the form of aggressive competition, but can also occur via sperm competition when several males copulate with one female, as demonstrated for northern elephant seals. Such sperm competition, if occurring regularly, is expected to lead to the evolution of large testis mass, as larger testes produce more sperm and thus increase a male’s chances to fertilize the ova of females in competition with sperm of other males. Such an increase in relative testis mass was documented in other mammalian orders where species in which multiple copulation is frequent have larger testes than species where only one male copulates with a given female, whether the social system is monogamous or polygynous.

A. Whales Whale mating systems are still largely unknown partly due to the problem that copulations are hard to observe. Except for a few particularly observable species, this leaves only indirect methods of investigation, such as genetic analyses, to determine the mating pattern in the more elusive species (Connor et al., 1998). Among mysticete whales, much is known about the humpback whale, so well known for its spectacular songs. During the mating season, males station themselves well spaced out and advertise their position. This is very similar to the lek structures observed in many birds. The song may attract females and keep competing males away, but there is presently no firm evidence for this inference. Alternatively, males follow females, and several males may be doing this simultaneously, leading to competition for proximity to the female. Apparently these males compete over mating access to a female. Because humpback whales have small testes for their size, it is unlikely that females will copulate with several males, thus inducing sperm competition. In contrast, sperm competition is likely to occur regularly in right whales (Eubalaena spp.), which—weighing about 50 tons—have testes weighing 1 ton, in strong contrast to blue whales, which weigh about 100 tons but have a testis mass of only about 70 kg. Copulation is observed frequently in right whales but has never been described convincingly in humpbacks, despite much more study of the latter. Mating patterns in odontocetes are somewhat better known from a few species (Connor et al., 1998). Male strategies vary from singly roving males in the sperm whale to males that cooperate to herd and perhaps force females into copulation in the bottlenose dolphins. Sperm whales show a mating pattern similar to that of elephants in which single fully adult, highly aggressive males rove among female groups in search of receptive females. They stay only briefly with each one of the female groups and then go on. Presumably, the long intervals between estrus in females make it unprofitable for these males to stay with any one group of females waiting for one of the females to enter estrus. Only fully adult males appear able to compete in this system, and

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subadult males as well as non-roving males stay at higher latitudes, often in small schools, feeding and maximizing energy intake in this way to grow to a competitive size. It is unclear why these males might stay in small groups as bachelors because they are certainly not endangered by predation and it is unknown which foraging advantages they might derive from grouping. The killer and pilot whale mating system is the most surprising, least understood of the whale mating systems and has no parallel in terrestrial mammals. Genetic evidence shows that males who remain philopatrically in their maternal group never father offspring in their own group, but apparently in other groups. Some evidence suggests that several related males of one group may mate with several females in another group, presumably during repeated encounters of these pods. This was concluded from the genetic observation that offspring in a group seem to be paternally related.

B. Pinnipeds The pattern of mating interactions among individuals depends greatly on the dispersion of females during the breeding season, which in turn reflects the availability of a suitable habitat for pupping and foraging. In pinnipeds, pack ice, fast ice, and land-breeding species differ widely in this respect (Boness, 1991; Le Boeuf, 1991). Phocids breeding on ice floes seem to have a mating system best described as serial monogamy in which a male stays with a female that has recently pupped until she comes in estrus. He then leaves after copulation to search for another female. The reproductive success for males in such a mating system depends more on their aptness to locate females ready to mate than on fighting abilities. In such species, sexual dimorphism tends to be small, slightly reversed (males smaller than females), or nonexistent. Some fast-ice breeding species also show reversed sexual dimorphism, which is best analyzed in the mating system of the Weddell seal. Females gather around cracks in the fast ice where they dive for food from holes in the ice. During the reproductive season, they pup near these holes and males claim territories under the ice and defend the holes against other males. Under these conditions, maneuverability is considered more important than sheer size in male–male competition. This may be the reason for the observed reversed sexual size dimorphism. Alternatively, females may be selected for larger size, enabling the production of larger young or the storage of more massive fat reserves for lactation, and males may have remained smaller for lack of such selection. Copulation is underwater and consequently little is known about the reproductive success of males in this mating system. Phocid seals, such as the harbor seal, which breed in the water close to land areas where females loosely aggregate, seem to engage in fights for the best stations where females have to pass by, and such males are often wounded. Fighting males seem to have the highest reproductive success and, in some places, the mating system of this species may be similar in structure to a lek. When female otariids or land-breeding phocids come together on predator-free islands, the resulting high female density permits males to station themselves among females and attempt to monopolize access to females. This competitive situation sets up sexual selection for an ever increasing male size, leading to impressive sexual size dimorphism in a few phocid and many otariid species (Lindenfors et al., 2002), such as the northern fur seal in which males weigh six times as much as females. In addition, a larger size also enables males of these species to remain fasting on territory for long periods, thus increasing their chances to mate with females.

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Otariid mating systems have been described as resource defense, female defense, or leks. The presence of resources important to females with pups, such as shade or access to tide pools, on male territories was demonstrated experimentally for a few species. However, resource distribution is not sufficient to predict the exact location of female aggregations nor does it explain female gregariousness, i.e., an active tendency of females to approach each other. Because high female density correlates with increased pup mortality in breeding colonies, there is a marked cost to female gregariousness, which must be compensated by comparable benefits. Bartholomew (1970) suggested that female choice of genetically superior males was responsible for female gregariousness, but little evidence supporting this view has come forward. New studies suggest a strong selection of female gregariousness through avoidance of interaction with large males, whether territorial or not. In many otariid species and in elephant seals, interactions with a much larger male can be dangerous or even deadly to a female. Females can minimize the probability of interaction with territorial males by aggregating into a “selfish herd.” Through this effect and by avoidance of dangerous and sometimes directly fatal harassment of females and pups by marginal males, females are selected to group much more closely than can be explained by resource distribution. Thus, the stationing of large adult males on clustered territories among parturient and estrous females creates a resource “peace from marginal male harassment” (Trillmich and Trillmich, 1984). Except for this socially created resource, the system could also be described as one in which males are lekking on areas where females are forced to stay for a while because they spend the period between parturition and postpartum estrus near-stationary on land. Males may benefit from clustered territories by the reduced chances of losing females when disturbed by marginal subadult or adult males. Within this system, the male defense of access to females varies intra- and interspecifically with habitat and female density, from female defense to territorial site defense with larger or smaller territories reminiscent, respectively, of a resource defense or a lekking system. Dominating males in these land-based breeding systems gain most copulations and can reach quite extreme reproductive success, sometimes up to 100 copulations in one breeding season. However, genetic studies have shown that observed number of copulations does not always correlate well with actual paternity, suggesting that peripheral, apparently “excluded” males may also gain some reproductive success by keeping close to female groups. There is no evidence of female choice beyond the mechanism that females in dense groups attract the strongest males in the best condition because only these are competitive enough to station themselves in the middle of female groups. Female elephant seals protest when they are attacked and forced into copulation by subadult or peripheral males, thereby attracting the attention of the dominant male who will often chase off the smaller male and copulate with the female. In this way females indirectly choose dominant males as copulation partners. Gray seal mating systems on land strongly resemble the otariid system. Whether female choice plays a more important role in gray seal colonies remains to be seen. Genetic analysis of subsequent offspring of individual females suggests that females copulate year after year with the same male, even though they may stay in the territories of different males. This would suggest that they actively choose a particular male or, in case of multiple copulations, have mechanisms to choose among sperm of several males. In more dispersed breeding species, such as harbor seals, males have no chance to defend access to females as these are too mobile and not available continually in the same areas, depending on tide level and sea conditions. In situations in which females breed on sandbanks, harbor seal males

were observed to station themselves in areas where females are likely to pass by and make themselves obvious through vocal display. Whether this and similar observations on walrus males that station themselves near females and produce bell-like sounds can be considered a lek display needs further investigation.

V. Sirenians and Sea Otters Much less is known about the social life of sirenians and sea otters and, therefore, these two groups are treated only briefly here. The only clearly recognizable social structure in sirenians is the mother–offspring bond, which may last for up to 3 or 4 years. Other than that, it appears that the dispersion of most sirenians relates directly to the distribution pattern of food, aquatic macrophytes, fresh water for drinking (in the Florida manatee, Trichechus manatus) and, particularly in winter, warm water areas. Animals may migrate for large distances between such resources. However, it seems possible that underlying the apparent asocial pattern may be a subtle pattern of individualized relationships. This might be hypothesized from “greeting” displays exchanged between individuals that meet only occasionally at widely distant sites. Cows in estrus seem to induce male scramble competition. In Florida, manatee herds of up to 20 males may follow an estrous female and compete by pushing to get into a favorable position for mating. In dugong (Dugong dugon) males, competition may take a more aggressive form in which males may wound each other with their tusks. For West Australian dugongs, mating competition may lead to a form of lekking (Anderson, 2002). However, the evidence is largely circumstantial. Sea otter spatial dispersion is related to the need to live close to the coast where they forage relatively shallowly for macroinvertebrates. Females claim year-round foraging territories along the coastline that often overlap. They sometimes aggregate in small groups—so-called “rafts.” Young males, and fully adult males outside the reproductive season, also frequently form rafts close to areas of rich feeding resources. Such rafting is presumably related to the reduction of predation risk. During the reproductive period, fully adult males establish territories that may overlap with more than one female territory. This provides males with a chance for a mild form of polygyny, but hard evidence for paternity of such males is at present missing.

VI. Concluding Remarks Much of the sociobiological interpretation of observations on marine mammals is still in an early stage. This situation reflects our lack of detailed knowledge about the marine environment and in particular the macro- and microdistribution of resources and predators of marine mammals. More observation, more comparative studies, and especially more experimental work are urgently needed to understand the sociobiology of these magnificent animals. Obviously, experimental work will be particularly challenging and can only be successful if built on the thorough knowledge of marine mammal natural history. However, a well-founded functional understanding of the social behavior of marine mammals cannot be achieved without experimental tests of our many assumptions. Ingenious instrumentation and molecular genetic tools, developed during the last decade, should prove most helpful in making this summary of marine mammal sociobiology soon outdated.

See Also the Following Articles Energetics ■ Feeding Strategies and Tactics ■ Group Behavior ■ Mating Systems ■ Parental Behavior ■ Predator–Prey Relationships ■ Thermoregulation

Song

References Amos, B., Schlötterer, C., and Tautz, D. (1993). Social structure of pilot whales revealed by analytical DNA profiling. Science 260, 670–672. Anderson, P. (2002). Habitat, niche, and evolution of Sirenian mating systems. J. Mamm. Evol. 9, 55–98. Baird, R. W., and Dill, L. M. (1996). Ecological and social determinants of group size in transient killer whales. Behav. Ecol. 7, 408–416. Bartholomew, G. A. (1970). A model for the evolution of pinniped polygyny. Evolution 24, 546–559. Boness, D. J. (1991). Determinants of mating systems in the Otariidae, Pinnipedia. In “The Behaviour of Pinnipeds” (D. Renouf, ed.), pp. 1–44. Chapman & Hall, London. Boness, D. J., and Bowen, W. D. (1996). The evolution of maternal care in pinnipeds. Bioscience 46, 645–654. Boyd, I. L. (1998). Time and energy constraints in pinniped lactation. Am. Nat. 152, 717–728. Boyd, I. L., Croxall, J. P., Lunn, N. J., and Reid, K. (1995). Population demography of antarctic fur seals: the costs of reproduction and implications for life-histories. J. Anim. Ecol. 64, 505–518. Campagna, C., Bisioli, C., Quintana, F., Perez, F., and Vila, A. (1992). Group breeding in sea lions: pups survive better in colonies. Anim. Behav. 43, 541–548. Clutton-Brock, T. H. (1991). “The Evolution of Parental Care.” Princeton University Press, Princeton. Connor, R. C., Mann, J., Tyack, P. L., and Whitehead, H. (1998). Social evolution in toothed whales. Trends Ecol. Evol. 13, 228–232. Costa, D. P. (1993). The relationship between reproductive and foraging energetics and the evolution of the pinnipedia. Symp. Zool. Soc. Lond. 66, 293–314. Frank, S. A. (1990). Sex allocation theory for birds and mammals. Ann. Rev. Ecol. Syst. 21, 13–55. Hamilton, W. D. (1964). The genetical theory of social behaviour. J. Theor. Biol. 7, 1–25. Kokko, H., Johnstone, R. A., and Clutton-Brock, T. H. (2001). The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187–196. Krause, J., and Ruxton, G. D. (2002). “Living in Groups.” Oxford University Press, New York. Le Boeuf, B. J. (1991). Pinniped mating systems on land, ice and in the water: emphasis on the Phocidae. In “The Behaviour of Pinnipeds” (D. Renouf, ed.), pp. 45–65. Chapman & Hall, London. Lindenfors, P., Tullberg, B. S., and Biuw, M. (2002). Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav. Ecol. Sociobiol. 52, 188–193. Mace, R. (2000). Evolutionary ecology of human life history. Anim. Behav. 59, 1–10. Mann, J., Connor, R. C., Tyack, P. L., and Whitehead, H. (eds) (1999). “Cetacean Societies: Field Studies of Dolphins and Whales.” Chicago University Press, Chicago. Schulz, T. M., and Bowen, W. D. (2005). The evolution of lactation strategies in pinnipeds: a phylogenetic analysis. Ecol. Monogr. 75, 159–177. Trillmich, F. (1996). Parental investment in pinnipeds. Adv. Stud. Behav. 25, 533–577. Trillmich, F., and Trillmich, K. G. K. (1984). The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny. Biol. J. Linn. Soc. 21, 209–216. Trillmich, F., and Weissing, F. J. (2006). Lactation patterns of pinnipeds are not explained by optimization of maternal energy delivery rates. Behav. Ecol. Sociobiol. 60, 137–149. Trillmich, F., and Wolf, J. B. W. (2008). Parent-offspring and sibling conflict in Galápagos fur seals and sea lions. Behav. Ecol. Sociobiol. 62, 363–375. Trivers, R. (1972). Parental investment and sexual selection. In “Sexual Selection and the Descent of Man 1871–1971” (B. Campbell, ed.), pp. 136–179. Aldine Atherton, Chicago.

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Song JIM DARLING I. Characteristics A. First Descriptions

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lthough likely heard by sailors for millennia, the first recordings of humpback (Megaptera novaeangliae) songs were made via US Navy hydrophones in the 1950s off Hawaii and Bermuda. Scientists first recognized these sounds in the 1960s as coming from humpback whales. The first technical description was published in Science in 1971 by Roger Payne and Scott McVay with the revealing subheading, “Humpbacks emit sounds in long, predictable patterns ranging over frequencies audible to humans.” Their analysis led to a structural context in which to view the sounds introducing the terms units, phrases, themes, and song. With the observation that humpback whales “produce a series of varied sounds then repeat the same series with considerably precision” these authors called the performance “singing” and the repeated series of sounds the “song.” The biological definition of song is a series of sounds that are repeated over and over. Many animals, therefore, have songs, ranging from the simple “ribet” of frogs, to the huge variety of bird songs, to the loud repetitive signals of the whales. Although whale song was introduced and has been virtually synonymous with the humpback whale, recent studies indicate that other species of baleen whales, including bowheads (Balaena mysticetus), blues (Balaenoptera musculus), fins (Balaenoptera physalus), and minkes (Balaenoptera acutorostrata), also repeat patterned sequences of sounds that fit the song definition. Studies of the songs of other mysticetes are young— although this is changing quickly. To date, no known songs are quite as complex and dynamic as those of the humpback whale.

B. Song Structure The humpback whale song is composed of a sequence of highly varied sounds ranging from high-pitched squeaks to midrange trumpeting and screeches to lower frequency ratchets and roars, and combinations of all these. This sequence is typically about 10–15 min in duration, although it may range from 5 to 30 min. It is then repeated without a break (Payne and McVay, 1971; Winn and Winn, 1978). The song has a predictable structure or framework. Discrete sounds are termed units. Several different sounds or units in a sequence compose a phrase. A phrase is repeated some variable number of times (for example, 10 times), and this series of the same phrase is called a theme, say, “theme 1.” After several minutes of singing theme 1 the singer changes to a different set of phrases (composed of different units or sounds) and repeats it a number of times. This might be called “theme 2.” This pattern repeats until the whale cycles back to its theme 1. A typical song may contain six themes. A singer may sing in order themes 1–2–3–4–5–6 and then start at 1 again. The number of themes in a song varies from population to population and

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