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9

SOCIAL BEHAVIOR IN SOME MARINE AND TERRESTRIAL

CARNIVORES

1 Introduction

BURNEY J. LE BOEUF Crown College

University of California, Santa Cruz

2 Morphological Comparisons 3 Prey, Food Habits, and Feeding Behavior 4 Social Behavior and Reproduction 5 Summary

1 INTRODUCTION

251 255 257 263 274

Once upon a time, around 37 million years ago, when primitive fissiped carnivores were evolving from their miascid predecessors, some of them forsook their way of life on land and went to sea to find food. This move must have worked out well, because many of the descendants of these pioneers-the seals, sea lions, and walruses-are still making a living in the sea today. Of course, descendants of the carnivores that remained on land fared well, too. Because land and sea are such different environ­ments, we might expect the two animal groups to have diverged in many ways since their separation. Indeed, it should be interesting to compare representatives of the two groups because of what they have in common, an ancestor, and because of the obvious differences in the environments in which they live. In this chapter, I point out some differ-

251

252 Social Behavior In Some Carnivores

ences and similarities between seals and their terrestrial conterparts with respect to gross morphology, feeding and predatory behavior, reproduc­tive behavior, and various aspects of social life. As is necessary when comparing two large groups of animals, I document points with exam­ples from a few selected species. My selection is biased toward those species that have been studied most systematically, those that are of greatest theoretical interest, and those studies with which I am familiar.

The similarities between seals and land carnivores were obvious to laymen and early scientists (Fig. 9.1). Fifteenth and 16th century sailors described the seals they saw as marine carnivores and called them "sea lions," "sea bears," or "Iobos de mar" (sea wolves). Linnaeus and sev­eral later taxonomists classified seals, sea lions, and walruses in the order Carnivora. However, as early as 1811, there was an attempt to place these animals in a separate order (Illiger, 1811). At present, many investigators class these marine mammals in their own separate order, the Pinnipedia (e.g., King, 1964). However, classification of these ani­mals is far from settled. Some maintain that the new order is inapprop­riate and that pinnipeds should be considered merely a suborder of the Carnivora (McKenna, 1969). Others argue that the pinnipeds can be classified into two living families (walruses are placed in the same family as sea lions) under the superfamily, Canoidea, in the order Carnivora (Mitchell and Tedford, 1973).

Before I make specific comparisons, it may be useful to present a sketch of pinniped evolutionary history. Their history, although poorly documented, may provide clues to differences we might expect between them and terrestrial carnivores.

The earliest pinnipeds probably entered the sea in one of the following areas: the Arctic Basin, the northwest coast of Nor.th America, or the Tethyan-Mediterranean area (Matthew, 1939; Davies, 1958a; McLaren, 1960; Repenning, 1970). It is not clear whether seals and sea lions (includ-

. ing the walrus) were already differentiated at this time. The oldest pin­niped remains; ar,e from the Miocene era, a time when they were already well adapted for aquatic life and when seals and sea lions were already distinguishable (Downs, 1956; Mitchell and Tedford, 1973). One opinion holds that all pinnipeds derived from canoid or dog-bear stock (e.g., Matthew, 1939; Simpson, 1945; Davis, 1958a; Sarich, 1969). An opposing view is that sea lions and the walrus derived from ursine stock, and seals derived from lutrine stock (e.g., Mivart, 1885; McLaren, 1960; King, 1964; Repenning, 1970). This question is far from settled. Nevertheless, there is agreement that all pinnipeds are more closely related phylogenetically to members of the superfamily Canoidea of the order Carnivora--:-the

,...

Gi UI a: ::;) CJ ii:

253

254 Social Behavior In Some Carnivores

dogs, raccoons, bears, weasels, and the Iike--than to the feloid carni­vores.

After they entered the water, the distribution and diversity of pin-. nipeds were influenced by geomorphic and climatic barriers, distance

between land falls, ocean currents, and water temperature (Davies, 1958a; King, 1964; Hendey, 1972). Davies (1958b) hypothesizes that pin­nipeds are, and always have been, tied to a cold-water environment. He argues very persuasively that the distribution and differentiation of present-day northern pinnipeds reflects periods of expansion and con­traction of sea and glacial ice that occurred during the Pleistocene era. Scheffer (1958, p. 37) points out that "as local shore lines and islands rose and fell and glacial barriers came and went, pinnipeds moved back and forth in order to maintain favorable breeding grounds along the edge of the sea." On land, many contemporary carnivores were being forced into extinction by periodic fires, floods, droughts, and dust storms.

Scheffer suggests that the early pinnipeds moved out along the shores of continents, from island to island and later to polar ice fields. The rate of evolution was faster at the frontiers of the advancing lines where immigration was unidirectional. He speculates further:

The primitive populations were small, composed of family groups, not very sociable. The members did not wander far, had no well-developed homing instinct, were not migratory, and did not need to rendezvous in special places in order to find mates. Polygyny had not developed in any of the pinniped stocks. The animals were perhaps smaller than most recent pinnipeds (Cope's rule), had less fat, lived in more temperate waters, and perhaps made crude dens in beach grasses and among boulders. The advancing pinnipeds met, from sea birds and cetaceans, little competition for food. They met no competition for breeding room, nor do they often today. Pinnipeds early lost the habit of feeding on beach organisms such as crabs, mussels, periwinkles, and blennies. [Scheffer, 1958, p. 36-371

As each generic stock became isolated, it was transformed in response to the local physical and biotic environment and adapted to its peculiar niche. Among species frequenting isolated bays, gulfs, islands, inland seas, or lakes, there has been, and still is, rapid evolution.

In the last few centuries, the effect of commercial sealing upon island and continental pinniped populations has been catastrophic. Millions of seals have been slaughtered and entire breeding populations wiped out. It is doubtful that some species will ever recover genetically from under­going such a severe population "bottleneck" (Le Boeuf, 1977). In one recently exploited species, absolutely no polymorphic variation was

Morphological Comparisons 255

found in 21 blood proteins from 159 se<lls representing five rookeries (Bonnell and Selander, 1974)! In this regard, some land carnivore popu­lations have suffered a similar f<lte at the hands of man-for example, the wolf. The increasing range of human populations is changing the distribution of both land carnivores and pinnipeds.

Although pinnipeds are marine, all species have retained an attach­ment to land. In this respect, they differ from the Cetacea, descendants of a primitive ungulate ancestor, who have become completely aquatic. All pinnipeds 'give birth on land or ice, and some species spend the majority of their time resting out of the water.

Pinnipeds have exploited the marine niche for food. A few carnivores, such as the sea otter,' Enhydra /utris, and the polar bear, Thalarctos maritimus, also obtain food from the sea, but they have not undergone the same degree of morphological transformation to aquatic living as the pinnipeds. The anatomical and behavioral adaptations of the pinnipeds to life in the sea clearly distinguishes them from the land carnivores. Since these adaptations influence their behavior on land, it is worth reviewing some of the major ones.

2 MORPHOLOGICAL COMPARI�ONS

Many morphological differences between pinnipeds and land carnivores are simply a reflection of the different environments in which they live. The average body size of pinnipeds is greater than that of ca!nivores. The smallest pinniped, the ringed seal, Pusa hispida, weighs 90 kg. The largest pinniped, the southern elephant seal, Mirounga leonina, weighs about 3,629 kg and is 650 cm long (Scheffer, 1958). Several seal species are larger than the largest land carnivore, the grizzly bear, Ursus arctos, which weighs 771 kg (Erdbrink, 1953). Many land carnivores, such a� the foxes of Africa (Bekoff, 1975), weigh less than 4 kg. The Fennec fox, Fennecus zerda, weighs less than 1 kg! The greater body size of pinnipeds evolved mainly in response to the marine environment. Large body size is b-etter for heat retention in the told sea. Moreover, since the water medium gives more support than air, large size could mote easily evolve in the sea than on land.

The pinniped body is adapted for swimming and diving. Body shape is streamlined to reduce drag. The external ears are reduced or absent, external genitalia and mammary teats are drawn into the body, limbs are enclosed within the body and extremities are flattened-the tail is short and the head is flattened, and the eyes are situated well forward. The neck, in particular, is thick and muscular and considerably more flexible

256 Social Behavior In Some Carnivores

than in most large carnivores. The skin is adapted to a water environ­ment (Montagna and Harrison, 1957), and the hair is flattened. Pin­nipeds never groom the pelage with the mouth or tongue (Scheffer, 1958) . The terrestrial carnivore body is a picture of contrast. The canid body, especially the large one, is designed for long-distance running (see Romer, 1966; Mech, 1970; Fox, 1975) .

Subcutaneous fat forms a substantial part of all pinniped bodies. Skin and blubber make up more than 25% of the weight of the Weddell seal, LeptonycllOtes weddell; (Bruce, 1951) and almost 50% of the body weight of the southern elephant seal (Laws, 1953). Blubber provides reserve energy during fasts and lactation, thermal insulation, buoyancy, and the padding necessary for a streamlined profile. The proportion of body fat to total weight in land carnivores is apparently much smaller, even in dormant or hibernating bears, skunks, and raccoons.

Although the pinniped brain has not been studied in great detail, it is evidently large, like that of terrestrial carnivores, but more spherical and more highly convoluted (King, 1964). The sea lion brain resembles that of bears, while the seal brain looks more like that of cats and dogs. Compared to a dog's brain, the cerebellum is large, probably because of the increased coordination demanded in swimming. The auditory nerve is large and the olfactory lobes are reduced. Pinniped eyes (the walrus excepted) are larger than those of land carnivores, and they function well at low levels of illumination. Seal vision is excellent both in water and on land (Schusterman, 1972).

Pinnipeds have fewer and more uniform teeth than most land carni­vores (except for the walrus, a special case once again). All species have the pronounced upper and lower canines but lack the carnassial cusps characteristic of land carnivores. The postcanines in most species are rudimentary pegs functioning to hold prey that is swallowed whole. Variation in pinniped teeth reflects the type of flesh the animal feeds on, and, as in many mammals, it is a useful taxonomic indicator. Generally, the teeth, mouth, jaw, and associated structures of pinnipeds are de­signed for grasping, tearing, and swallowing prey whole or in chunks, rather than for chewing, shearing, or crushing large bones. In contrast with land carnivores, the deciduous teeth of pinnipeds disappear before or soon after birth.

Pinnipeds have made numerous physiological adjustments to aquatic life that set them apart from land carnivores. These adaptations in respi­ration, circulation, renal physiology, and the like are important and interesting, but it would be too much of a digression to cover these topics here. Ridgeway (1972) provides an excellent review of marine mammal adaptation to the aquatic environment.

:

Prey, Food Habits, and Feeding Behavior

3 PREY, FOOD HABITS, AND FEEDING BEHAVIOR

257

Pinnipeds deviated from land carnivores in form and function because of adaptations that took place as a result of seeking food in the sea. It is therefore most important to compare these two animal groups from the point of view of hunting and feeding habits, and in relation to their respective prey.

Both pinnipeds and land carnivores are meat eaters, but only the marine mammals eat flesh exclusively. Seals and sea lions feed mainly on crustacea, molluscs, fish, penguins, and other sea birds. Although diet varies with the species, the majority of pinnipeds feed on a variety of prey. The Alaska fur seal, Callorizilllls ursillus, is the best stu

'died pin­

niped from the point of view of food habits. Its catholic diet is represen­tative of the wide range of fishes and squid eaten by the Otariids (the earred s,eals or sea lions and fur seals, as opposed to the Phocids, the earless, true seals). Alaska fur seals feed on more than 30 kinds of marine organisms: at least 27 species of fish, 1 species of octopus, and 5 species of squid (Fiscus, Niggol, and Wilke, 1961). The most common prey of fur seals are northern anchovy, Ellgraulis lIIordax, squid, and Pacific herring (C/lipea izamlgus). Various rockfish, Pacific hake, Merluc­cius Prodllctlls, Pacific saury, Cololabis saira, salmon, OncorizYllclluS spp. , and American shad, Alosa sapidissimia, are eaten in lesser quantities. Hermit crabs, amphipods, and various diving sea birds (e. g. , Rhinocer­ous Auklet, Ceror/lillen lIIollocerata, Red-throated Loon, Cavia stellata, and Beal Petre\' Oceal/odrollla leucorizoa beali) are eaten occasionally, but they seem 'to play only a minor role in the seals' diet (Niggol, Fiscus and Wilke, 1959) .

Fur seals, like most other pinnipeds, are opportunistic feeders. What is eaten depends on the seasonal distribution and the abundance of prey. Since fur seals commonly feed on sc�ooling fishes, stomach con­tents of several animals collected in the same area often contain only one type of, fish. The Steller sea lion, Eumetopias jubatq (Spaulding, 1964), a�d the California sea lion, Zalophus cali/ornianus (Fiscus and Baines, 1966), eat similar fishes and squid, especially where the feeding range of the three s

'pecies overlaps. Steller males in the Bering Sea and off Alaskan

islands supplement their diet with Alaska fur seal pups (Roger Gentry, personal communication).

Most true seals, such as the harbor seal, Phoca vitulina, and the grey seal, Halichoerus grypus, are mainly fish eaters, but they occ�sionally feed on an assortment of crustacea, octopus, eels, and molh,lscs (Spaulding, 1964; Kenyon, 1965; Anderson et al . , 1974) . The northern elephant seal, Mirouna angustirostris, is a deep diving seal that feeds primarily on squid,

258 Social Behavior In Some Carnivores

skates, rays, small sharks, and ratfish, Hydrolages collier (Huey, 1930; Morejohn and Baltz, 1970). The small ringed seal, Pusa Hispida, which inhabits the circumpolar Arctic coasts, feeds on up to 72 different species of small pelagic amphipods, euphausians, and other crustacea, as well as on small fish (King, 1964).

Only two of the 32 different pinniped species in King's classification (King, 1964) are rather specialized feeders that exploit one type of prey species almost exclusively. The Crabeater, Lobodon carcinophagus, feeds on krill, small shrimp-like animals that it catches in quantity and strains from the water through its multicusped cheek teeth, much as a mysticete whale sieves krill through its baleen. The walrus, Odobenus rosmarus, feeds primarily on three genera of bivalve molluscs, Mya, Saxicava, and Cardium, for which it forages in shallow coastal waters less than 40 fathoms deep. Bivalves on the sea bottom are examined and sorted by the lips and whiskers; feet and fleshy parts are torn off and swallowed whole or sucked out. But when molluscs are scarce, the walrus may eat young ringed seals, bearded seals, Erignathus barbatus, and even young walruses. It is the only pinniped that apparently feeds on Cetacea. Occa­sionally a narwhal, Monodon monoceros, or a beluga, Delphinapterus leu cas is eaten. However, it is not known whether walruses acturally kill them or feed on corpses (King, 1964).

The diversity of foods eaten by canids and ursids is even greater than that of pinnipeds. According to Mech (1970), "probably every kind of backboned animal that lives in the range of the wolf has been eaten by the wolf." Wolves, Canis lupus, eat mice, mink, muskrats, squirrels, rabbits, various birds, fish, lizards, snakes, grasshoppers, earthworms, and berries. But predation on small animals plays only a minor role in the wolf's diet. The main prey of the wolf, like those of the African wild dog, Lymoll pictlls, are large animals. The wolf's primary prey in the United States and Canada are: white-tailed deer, mule deer, moose, caribou, elk, Dall sheep, bighorn sheep, and beaver. Wild dogs kill mostly Thomson's gazelles, juvenile wildebeests and Grant's gazelles (Estes and Goddard, 1967), and, occasionally, warthogs and zebras (van Lawick-Goodall and van Lawick-Goodall, 1971). African foxes feed mostly on rodents and small reptiles, birds's eggs, insects and vegetable matter; jackals eat similar foods in addition to small mammals and carr­ion (Bekoff, 1975). Additional information on other canids can be found in Fox (1975).

Of all the land carnivores, bears have the most diverse tastes. The grizzly, before man virtually annihilated it, was an omnivorous oppor­tunist par excellence . The California grizzly (Storer and Tevis, 1955) ate almost anything and everything that was available. This long list in-

Prey, Food Habits, and Feeding Behavior 259

cluded: meat, fresh or putrid from whales, water birds, fish, elk, deer, antelope, gophers, lizards, frogs, and domestic livestock; a wider variety of plant materials than herbivorous animals ate, some of which were various berries, clovers, nuts, wheat, corn, potatoes, tree bark, and vari­ous bulbs; and assorted foods like honey, ants and their larvae, yellow­jacket nests, and mushrooms. Polar bears, Tlwlarctos maritimus, have a much mQre restricted diet. Although they consume some vegetation and carrion during the summer (Russell, 1975), they feed primarily on the ringed seal during most of the year (Stirling and McEwan, 1975).

The remarkable thing about the feeding habits of the large canids is that the prey is often larger than the predator. In this respect, the large canids differ from all of the pinnipeds. Wild dogs, whose average weight does not exceed 18 kg, bring down impala and reedbucks that are double or triple their size (Estes and Goddard, 1967) and zebras that are even larger. Wolves weighing 36 to 45 kg kill moose and bison that may weigh over 500 kg. These canids overcome large prey by hllnting in packs that range from a few animals up to a score or more of. them. One dog usually selects a quarry from a retreating herd of g"zelles, and the other dogs follow it. The quarry is coursed for 1 to 3 km until it becomes exhausted. The lead dog catches up to it and grabs it or bowls it over. Once overta­ken, the prey is fallen on by all the following dogs, and it is dismem­bered and eaten with great dispatch. Wolves bring down deer or moose in a similar way (Mech, 1970) . The first wolf to catch up to the fleeing prey attempts to grab hold of the rump, flanks, neck, or nose. Once the prey is down, others attack from every side. Although the technique may vary with prey species, the strategy of the individual quarry, and the composition of the hunting pack, it is clear that these pack hunters get help from each other in getting their food. Lone wolves or even small packs are at a disadvantage in bringing down large prey. In black­backed jackals, Canis mesome/as,. Wyman (1967) observed that two hun­ters were more than four times as successful as one in bringing down gazelle fawns. ,

Like land carnivores, the size of prey eaten by pinnipeds varies greatly, but, except for the dubious possibility that walruses kill small whales, pinnipeds always kill and eat animals that are much smaller than themselves. Prey size determines how Alaska fur seals, Steller sea lions, and harbor seals eat their food. Small fishes less than 30 cm long, such as anchovy, herring, saury, or squid, are consumed whole under water (Niggol, Fiscus, and Wilke, 1959; Spaulding, 1964). Except for very small food items like lanternfish, the p�ey is swallowed head first. Larger prey measuring more than 30 cm long, such as hake, rockfish, or salmon, is brought to the surface, grasped by the head, shaken vio-

260 Social Behavior In Some Carnivores

lently, and reduced to chunks that are swallowed piecemeal. As fur seals get older and larger, large fish up to 92 cm make up an increasingly high proportion of their diet (Spaulding, 1964).

Some pinnipeds feed in groups, but, unlike the case with canids, grouping does not enable them to exploit larger animals. Rather, group­ing seems to make it easier for them to exploit large aggregations of small prey. Fiscus and Baines (1966) saw Steller sea lions leaving their hauling grounds in the vicinity of Unimak Pass, Alaska, in compact groups of several hundred to several thousand animals. They swam out to feeding areas, where they dispersed into smaller groups of less than 50 animals containing both sexes and mixed sizes of animals. Massings of this type fed on large schools of fish or squid. Casual observations suggest that groups of sea lions feed more effiCiently on schools of fish because cooperation among the hunters enables them to herd and con­trol the movements of the school. When large fish schools are absent, sea lions feed singly or in small groups of two to five animals. Similar behavior has been observed in the California sea lion (Fiscus and Baines, 1966; Michael Bonnell, personal observation).

Before Steller sea lion females leave the rookery and their pups to go to sea and feed, they may engage in activities that resemble, and that may have an analogous function to, the prehunt greeting ceremony of wild dogs (Estes and Goddard, 1967; van Lawick-Goodall and van Lawick-Goodall, 1971). Several females may gather at water's edge, where they mill about restlessly in close contact with each other. They may vocalize repeatedly and engage in what appears to be low-intensity aggressive behavior before swimming off as a group to feed. In both species, these activities may reinforce group cohesion and unity as well as synchronize the time of departure.

Similarly, canids and pinnipeds may travel several kilometers to get a meal. Van Lawick-Goodall and van Lawick-Goodall (1971) report that wild dogs did not start their first chase until they were 8 km from where they started. The chase itself covered a distance of 51/2 km. Wolves may pursue moose or caribou for up to 5 to 8 km but usually give up sooner (Mech, 1970). They may range up to 32 km from their den (Kelsall, 1957). Steller sea lions and California sea lions travel much further from their rookeries or hauling grounds to feed. The former have been seen feed­ing as far as 112 to 136 km from land (Kenyon and Rice, 1961) and the latter as far as 62 km from land (Fiscus and Baines, 1966; Le Boeuf, unpublished data). Usually, only small groups of less than 30 individu­als are seen this far from land. Large groups of sea lions (100 or more) are seldom seen feeding more than 16 to 24 km from a hauling ground or rookery. It would be interesting to compare land carnivores and pin-

Prey, Food Habits, and Feeding Behavior 261

nipeds on the success of thei r respective h u n ti ng and fi shing expedi­tions , but the di fficu l ti es i nherent in observ i n g sea ls feeding in the wa ter makes this impossible at presen t . H owever, some indirect evidence is pertinent . Virtual ly all fur seals collected early in the day by the U. S . Fish a nd Wildl i fe Service had food i n their stomachs (Niggol , Fiscu s , and Wi lke, 1959).

Al though both pinnipeds and the la rger land carnivores are nomadic, the former travel grea ter distances in their a n nual feeding migra tions . Th e record holder is the Ala ska fur seal , which migra tes from i ts breed­ing grounds i n the Beri ng Sea to i ts wi nter feeding grou nds along the shores' of the ea stern and western Paci fiC as far sou th as San Diego, California, and H okkai do, Ja pan , a dista nce of some 5000 km . · Wolves may follow caribou on their a n nual migra tions (Kelsall , 1968).

Wild dogs a nd d h oles, Ceron a/pinus, prefer to hunt in early morning or early afternoon or evening, a l though hu nts occur on moonlight nights a s well (Estes a n d God dard, 1967; v,a n Lawi ck- G o oda l l a n d v a n Lawick-G ooda ll, 1971; Davidar, 1975). Wolves and bears may h u n t by day or nigh t . Most of th e smalfer foxes are nocturna l feeders (Bekoff, 1975). Fur seals a n d sea l ions are primari l y night and early morning feeders. Stomach con tents of animals col lected at vari ous hours after su nrise show decrea sing amounts of food. However, in some area s where large schools of fish are present, daytime feedi ng also occurs . Typically, the midday hours are spent resti ng, and feeding activities gradually resume in late afte�noon (Niggol , Fiscu s , and Wilke, 1959; Spaulding, 1964). Th e harbor seal is a daytime feeder (Spaulding, 1964).

Ca nids ea t grea t amou n ts of food in a single feeding bout . A wolf may gorge 9 kg of mea t in a single meal; thi s may represent 20% of its body weigh t . However, 'estimates of a li ttle more tha n half tha t amou nt per day per wolf may be more representa tive (Mech , 1970). Estes a nd Go.d­dard (1967) estima te that wild dogs average 2.72 kg of mea t per day, or approxima tely 6.7% of their body weigh t . But these canids may have to go withou t eating for several days a t a time. Fi 've to 7 day fas ts have been recorded in wolves, and one wolf went for 17 days without food (Mech , 1970). It is common knowledge that domestic dogs ca n go for several days withou t ea ting, particu larly when sexual activi ty is probable . Grizzlies and black bears in the more northerly parts of N<;>rth America may go dorma nt for varyi ng periods of time during the win ter when food is scarce. I n general, all of ,the land carnivores will feed regularly if possibl e . Even bears will actively feed throughou t the year when food is available.

Most pinnipeds feed daily except a t certa in times of the year, usually the breedi ng season, when they u ndergo long fasts . Thu s, feas ts and

262 Social Behavior In Some Carnivores

fa mine are even more extreme in their annual cycle. Wh en they are feedi ng, fu r seals and sea l ions ingest less food relative to body weight than the ca nids menti oned above. Spaulding (1964) estima tes tha t fur seal , sea lion, a nd ha rbor seal food requi rements ra nge from 2 to 11 % of body weight per day, with 6% being th e average. During th e breeding season, fu r seal a nd sea l ion males fa st for approxima tely 6 weeks; har­bor seals do not appear to fa st duri ng th i s time. The record for long fasts in pinni peds goes to male north ern elepha n t seals. They may go wi th out food for 3 mon ths (Le Boeu f, and Peterson 1969). Throughout this time they are actively fighti ng and a ttem p ti ng to copula te, and they may lose over 450 kg. Females of this species fas t for an average of 34 days during the period in which they give birth a nd nurse their pups daily for 28 days (Le Boeu f, Whiting, a n d G antt, 1972). A female's total body weight may be redu ced by almost 50% during this fast. During the nonbreeding season, males and females fa st aga i n for approxima tely 30 days while undergoing the a nnual mol t.

Most ca nids and ursids scavenge for food at some time. Perhaps bears exploi t carrion more tha n any other land carnivore. Carrion was a major part of the Cal i fornia grizzly's diet more than 100 years ago, before man killed th e grizzly and i ts prey. It is said tha t these bears kept th e Califor­nia coa st clea n of pinniped and whale carcasses tha t repea tedly washed ash ore. There are numerou s reports of 12 to 15 bears feedi ng at the same time on a s ingle whale ca rca ss (S torer and Tevis , 1955). Many of the larger land carnivores typically desert the rema ins of a kill and cache it away and return to ea t from it la ter. Polar bears are an exception to this rule. They do not cache ringed seal carcasses tha t they kill, despite the fact tha t they may only feed on the blubber a n d leave the meat behind (Sti rl ing and McEwa n, 1975). In marked contrast to these feeding habits of la nd carnivores , pinnipeds do not cache food, nor do they scavenge, although the walru s may be an exception to this rule. Pinnipeds con­sume most of their prey en tire and discard only the heads of large fish, particularly rockfish.

One drawback that pinnipeds experience i n their marine habitat to which the larger land carnivores are rela tively i mmune is predation. In carving their niche in the sea, pinnipeds became exposed to large pre­dators who were also adapted to aquati c l i fe and more formidable than themselves. A t sea, the main predators on pinnipeds are large sharks, particu larly the great white shark, Carcharodon carcharias, and the killer whale, Orcinus orca. All pinniped species living in the Pacific are preyed on by these animal s . The degree of preda tion is u nknown. When pin­nipeds return to land or ice to give birth and nurse their young, they are vulnerable to preda tion by large land carnivores such as polar bears and

Social Behavior and Reproduction 263

grizzly bears, perhaps wolves, and, of course, man. Small carnivores, such as foxes, and skuas, gulls, and hawks, may prey on their young. Being adapted prima rily for locomotion i n wa ter, they are no match defendi ng themselves against large land preda tors. Thu s, it would ap­pear that predator pressure wa s important in ca using pinnipeds to breed in remote sanctuaries free from these preda tors; that is, offshore islands or rocks, sa ndbars and ice floes, and offshore breeding areas are limi ted . This is parti cularly true of the food-rich wa ters of the temperate north Padfic, the north Atlan tic, and the circu mpolar Anta rctic .

4 SOCIAL BEHAVIOR AND REPRODUCTION

Given this set of circumsta nces, it is li kely that pinnipeds were forced to share limited breeding areas, and this led to the high degree of sodality and the large soda I gatherings that we fin d i n pinnipeds toda y . In terms of the sheer number of a nimals tha t congregate together, the pinnipeds are much more social than any land carnivore. As many as 2 million Alaska fur seals ca n be found every summer on two tiny Pribilof Islands in the Bering Sea . Three thousand northern elephant seals may be found packed together tigh tly on one beach on Isla de Guadalupe, Mexico, during the peak of the breeding season (Fig . 9.2). Two thousand California sea lions may be found sleeping together in close contact 1/2 km inland on San Miguel Isla nd, California, during the nonbreeding season (Fig. 9.3). The largest wolf or wild dog packs are miniscule in comparison.

Pinnipeds are a mong the most p olygynous mammal s . Apparently, this mode of life developed v ery early in their his tory, and i t was closely tied to their amphibious habi ts (Bartholomew, 1970). When females bega n clustering in time and space, the condi tions became ideal for promoting male- male competi tion, polygyny, and sexual dimorphism (see Trivers, 1972). Males must have competed to mate with as many females as possible. Those who kept other males away from areas con­taining

' females sired more pup s . In their short breeding seasons on

traditional rookeries, fur seals and sea lions developed a social s tructure characterized by territoriality among males (Fig . 9.4 and 9.5). Males withou t territories do not copula te, or they copulate only rarely; those who secure the most well-placed territories-territories containing the most estrous females--do most of the breeding (Bartholomew, 1953; G entry, 1970). Another system that developed was for males to domi­nate other males and thus gain access to more estrous females wherever they were situated . This was the s trategy adopteq by northern elephant

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Social Behavior and Reproduction 267

FIGURE 9.5 Two Steller sea lion males engaged in a mutual threat at the boundary between their respective territories.

seal males. They fight for social status in a dominance hierarchy. The highest ranking male or males--depending on the number of females present-locate themselves nearest the females and keep all others away. One or a few of the highest-ranking males do most of the breed­ing in a harem; most males in a colony do not breed at all. One male may dominate a harem for several years and inseminate more than 200 females (Le Boeuf, 1974). Grey seal society is similar to that of elephant seals.

Thus, in most of the well-studied pinnipeds, males are polygynous and are either territorial or exhibit a dominance hierarchy during the breeding season. This is a reflection of the manner in which the largest and strongest males go about monopolizing a large number of females. Since size and physical aggression convey such a great reproductive advantage to males, these traits have become increasingly elaborated in time. Sexual dimorphism is greater in some seals and sea lions than in other mammals. For example, the Alaska fur seal male is five times larger than the female (Fig. 9.6).

268 Social Behavior In Some Carnivores

FIGURE 9.6 Northern fur seal harem on Kitovi Rookery, Pribilof Islands, Alaska, during the

breeding season. The male in the foreground has eight females in his territory; the male

immediately behind him has none. Note the extreme sexual dimorphism. Photographed by R. S. Peterson in June, 1963.

Canids are "social" i n quite a differen t way from pinnipeds . Social orga niza tion is characterized by seasonal or permanent pair bonds i n foxes (Storm, 1965; MacPherson, 1969) and jackals (e. g. , van Lawick­Goodall and van Lawick-G oodall, 1971; Eisenberg and Lockhard, 1972) a n d by cooperative hunting and group l ife in the wolf, dhole, a n d wild dog (Kleiman and Eisenberg, 1973; Mech , 1975). Black bears are essen­tially solitary, but female-cub associ a tions are long lasti ng, and strong and female cubs inherit their mother's feeding territories (Rogers, 1974). Wolf packs are orga nized i n to separate male and female social hierar­chies . Although the female hierarch y is more a mbiguous, it is clearly more pronounced than the size-related dom inance observed in female elephant seals. Hu nti ng dog packs have similar h ierarchies, particularly

Social Behavior and Reproduction 269

during the breeding season, but it is the female h ierarchy tha t is most evident (van Lawick-G ooda ll and van Lawick- G ooda ll , 1971). I n wolves and wild dogs , the domina nt breeding female may prev ent subordinate females from breeding or may drive them ou t of th e pack and kil l their pups . Domina nt females may also enlist the help of males , and they may prevent other adults from feeding the su bordina te female or her you ng.

Although many ca nids and ursids are territoria l in the sense tha t they defend a feeding or home ra nge against other individuals or groups of

� individ uals , this behavior is qu ite different from the defense of rigid individual territories by fu r seal males a nd S teller sea lion males agains t conspecific males d u ring t h e breeding season.

Wh en it comes to reprodu ctiv e behav ior and parenta l care, pinnipeds and terrestria l carnivores differ in many ways . Most ca nids and u rsids , like pinnipeds, h a v e o n e es tru s per year (Asdell , 1964; Kleiman, 1968). H owever, male-female sexual in tera cti ons in the land ca rnivores ca n be prolonged a nd complex . Ca nids exhibit extensive precopulatory court­ship, frequent olfactory exa mina tion of the partners, and frequ ent u rine a nd fa ecal ma rking (Kleima n, 1968) . In some domestic canids, females activ ely solicit males (Le Boeu £, 1967) . Ca nid copula tion is characterized by a ge nita l lock or tie . After intromission is achieved, the pair remains joined together by the genita l ia and fa ce in opposite directions for sev­eral minu tes or as long as an hour. Females may be in es trus for several days and may copulate several times with different males . Usually, only th e alpha female in a wolf pack breeds (Kleima n and Eisenberg , 1973; Rabb, Wool py, and G insburg, 1967; Zimen, 1975, 1976) .

I n contrast, there is l ittle or no courts h ip in pin niped sexual behavior (Le Boeu f, 1972) . Male north ern elepha nt sea ls pounce on fema les and a ttempt to force copulation at any t ime d u ring the breeding sea son, regardless of the female's reprodu ctive condition ( Cox and Le Boeu£, 1977) . Sea lions and fur seals may inves tiga te the female's genitalia be­fore mou nting, but there is little parallel to the direct solicita tion of males by females seen in the domestic dog (Beach and Le Boeuf, 1967; Beach, 1976) . Male seals do not mark with urine or feces , and they do not exhibit a copula tory lock . Copulation dura tion is equally long in both a nimal grou ps, lasting 3 to 7 min in elephant sea ls and 15 to 20 min in Steller sea lions . Some ph ocid females are in estrus for several days; most otariid females (in which the males are territoria l) copulate only once during the estrous period (Le Boeu£, 1972) . Copula tion is more can em excep t in elephant seals , wh ere the male mou nts from th e rear a n d to one side, perhaps a necessity because of the large bulk of th e animal s . Elephant seal males, like male wolves, prevent or interrupt each oth er's cop u la­tions; female seals , u nlike wolf bitch es, do not prevent other females

270 Social Behavior In Some Carnivores

from ma ting, but they threa ten, attack, and on occa sion kill pups of neigh bori ng females (Le Boe u f and Briggs, 1977) .

Canids have a short gesta tion period o f about 2 months and a l itter size tha t ra nges from 2 to 15, with 5 being the mode (Asdell, 1964; Kleiman, 1968) . The gesta ti on peri od of bears is 6 to 7% months, and the li tter size is usually 2 to 4 (Asdell, 1964) . Wild canid pups are born in dens or burrows. Wea ning from moth er's milk is at abou t 40 days in the domestic dog. B u t during the transition to solid food in most canids, the altricial young are provisioned by regurgi ta tion feeding of partially mas­ticated food . This is done by the parent male as well a s by the mother in the smaller pair-bonding ca nids. In wolves and wild dogs, al l adults in the pack, male a n d female, regurgitate to young pups as well as to the nursing mother not involved in the hunt. It is not clear how long this type of provisioni ng of the young goes on, but apparently it lasts until the you ng are able to obtain food on their own (see Mech , 1970; several reviews in Fox, 1975) .

Females of all pi nniped species give birth to a single pup once a year. They do not eat the placenta as the carnivores do . Within a few days or weeks after parturi tion, copula tion takes place. G esta tion, including de­layed implanta tion, lasts 1 year. Thu s , females give birth a t about the same time each year and u sually in the same place (except for seals that breed on ice). Most species give birth i n the open, whether it is on sand, rock or ice; the ri nged seal is a n exception and gives birth in subnivean lairs in the pressure ridges of sea ice ( S tirling and McEwan , 1975). New­borns of all species are physically well developed at birth. Pups are nursed for a minimum of 3 weeks (southern elephant seal, Laws, 1956) to more tha n a year (Steller sea lion, Gentry, 1970; walrus, Brookes, 1954) . The northern elephant seal female is a mammalia n phenomenon i n that she doesn't feed during the entire 4 week nursing period! Wean­ing is abrupt i n species l ike the elephant seal and gradual in others like the Pacific sea lions. Apparently, mothers feed their pups excl usively by nursing; they have not been observed carrying food to the young or regurgitating to them. Females of several species that breed colonially wil l not nurse pups other tha n their own. Northern elephan t seal females bite and sometimes kill orphaned pups that attempt to suckle them. Adoption of orphaned pups by females who have lost their own pups may occur in elephant seals, grey seals , and, rarely, in Steller sea lions. Unlike the canids, male pinnipeds that breed in colonies do not help in rearing or feeding the young. So far as I know, no male seal helps the female in any way . Quite the contrary, males are inadvertently responsible for a sizeable portion of pup mortality i n elephant seals and

j

Social Behavior and Reproduction 271

grey seals (Le Boeuf, Wh i ti ng, and Ga ntt, 1972; Le Boeuf and Briggs, 1977; Coulson a nd Hickling, 1964).

Evidently, there are fu ndamenta l di fferences in the social and repro­ductive behavior of these two rela ted groups of animals . Two basic differences having to do with the origin of sociality and the rate of reproductive behavior stand ou t .

Social behavi or seems to have quite a differen t origin in th ese two animal groups; that is, they must have been exposed to qui te different sel ection p ressu res . In the carnivores, there developed a premium on grou ping together, coopera ti ng in the h u nt, and feeding other pack members, because these behaviors increa sed the efficiency of predation (Wilson, 1975) . Being socia l enhanced surviva l through the process of kin selection (Maynard Smith, 1964; Hamilton, 1964). On the other hand, pinniped social ity seems to have developed first because of a paucity of breeding sites free of preda tors; la ter, this trend became elaborated through the opera tion of sexual selection . It is unique to pin nipeds that feeding and breeding have a lways been spatially separated and have occurred in di fferent habitats (Bartholomew, 1970). Unlike the typical terrestrial carnivore with an extensive home ra nge i n which mating also ta kes place, pinni peds opted to tra vel great distances to breed on tradi­tional sa nctuaries . Since such sanctuaries were limited, females were forced to clump together; this situation predisposed males to maximize their reproductive success by attempting to inseminate as many females as possible (see Trivers, 1972). Successful males were belligerent and big . Unbridled male-male competition led q u ickly to extreme polygyny, sex­ual dimorphism, lack of parental beha vior on the part of the male, sex differences in beha vior, and conti nued gathering of a large number of animals for breeding. Once this system was started, the inertia of sexual selection kept it moving in the sam«;; direction . For example, females that move from the main aggregation of fema les are apt to be fertilized by a male who is unsucces sful in competing with other males-that is, a "marginal" male . I f he is subordinate because of genetic factors, his progeny will be less successful in the next genera tion . Thus, any ten­dency of females to become less gregarious would be selected against and would be self- limiting (McLaren, 1967). G regariousness in females should be positively reinforced as long as competition among males-­whether for territories or for social status-results in the exclusion of some males (Bartholomew, 1970).

The second fundamental difference between pinnipeds and terrestrial carnivores has to do with reproductive turnover. In general, natural selection has favored two contrasting responses to the problems of

272 Socia l Behavior In Some Carnivores

popu lation replacement a n d the col onization of new habita ts . According to MacArth ur and Wilson (1 967) , in environments where there i s l i ttle crowding and food is abu n d a n t, r - selection will fa vor a nimals tha t u ti l ize the most food and rea r the larger fa m i l ies-that is, those with a high popu lation growth ra te . On the other h a n d , when there is crowding and i n tense com peti tion for food, K - selection wi l l fa vor a nimals that can replace themselves with the lowest possible i n take of food . The fi rst is a stra tegy of prod uctivity, a n d the second is one of efficiency of reproduc­tion .

In genera l , p i n n i peds a p pear to have been K - selected and terrestrial ca rni vores r - selected-Pi a n ka's (1970) a d monit ion that all orga nisms represent a compromise on this conti n u u m is certa in ly a pplicable here . One of the most i n teresti ng correlates of r - a nd K - selection is the pair of com plexes that Martin (1 975) ca l l s , respectively, the a l tricial and preco­cial comp lex . Pi nni peds con form to many of the a ttribu tes of the preco­cia l complex . Only one pup is born per year (one every 2 years in the walrus, a ccording to Brooks, 1 954) a n d the young exhibit adva nced physical development at birth . Alaska fu r seals ca n locomote and voc­alize within a moment of birth , and they are as adva nced at birth as d omestic dogs abou t 3 weeks old ( B a rtholomew, 1 959) . Northern elepha nt seal pups open their eyes and may exhibit the characteristic sa nd- fl i pping movements of the forefl ippers before completely expelled from the birth ca n a l . Harbor seal pups are able to swim a nd dive at birth (Bishop, 1967) . Lacta tion i s of long duration, lasting more than a year in some sea lions a n d the walru s . Even in seals having a relatively short nursing period, energy in vestment in the offspring may be enormou s . Elepha nt seal mi lk is approximately 55% fa t, and a l though pups are weaned a t 4 weeks of age, they are left with a tremendous fa t store (Fig. 9 .7) . These pups weigh more a t weaning than they do a year later! Other a ttribu tes of the precocial complex are la te sexua l maturity and a long l i fe . Most pinniped females ovulate for the first ti me at about 2 to 5 years of age; males reach sexua l maturity at about 3 to 6 years of age (e . g . , harbor seals, Bigg, 1969; Alaska fur seals, Bartholomew a n d Hoe!, 1953; anonymous, 1975; northern elephant seals, Le Boeu£, u npublished data ) . I n the colonial species, males d o not complete successfully for females until much later in l i fe, u n ti l approximately 10+ years of age in the northern elephant seal (Le Boeuf, 1974) . Pinnipeds may live a long time . Harbor seals live for 20 to 29 years (Biggs, 1969) . Alaska fur seals for up to 26 years (Niggo!, Fiscu s, and Wilke, 1959) , and the life span o f the northern elephant seal is typical ly abou t 14 years (Le Boeuf and Briggs, unpublished data ) . Like that in pri mates a nd other long-lived mammals,

Social Behavior and Reproduction 273

FIGURE 9.7 A suckling northern elephant seal pup appears almost as large as its mother shortly before it is weaned. At this time, it is four or five times larger than it was at birth, and

heavier than it will be a year later. Its sole nurturance has come from mother's milk. The mother

has provided this enormous fat store to her offspring during a four-week period in which she did not feed.

the trend i n pinni ped reproduction has been toward qual i ty rather than quantity.

Terrestri a l carni vores, especially the smaller ca nids, exhibit the altri­cial complex . Most can ids give birth in a shelter to a la rge l i tter of pups that are poorly developed and i nca pable of coordinated behavior except suckling. G esta tion is short and lactation brief compared to most pin­niped s . Sexual ma tu rity occu rs at a n early age, at the end of the second year in wild wolves (Mech , 1970) , and a t the end of the fI rst year is some captive wolves (Medj o and Mech , 1976) and i n the Arctic fox (Chese­more, 1975) . Life spans are short compared to those of pinnipeds . Al­though wolves have lived 10 to 16 years in captivity (Young, 1944), 10 is considered very old (Mech, 1970) . Seven is considered old age in large dogs (Fuller and DuBuis, 1962) . The l i fe spa n of faxes is considerably less, 6 years of age i n the gray fox, Urocyon littoralis (Laughlin, 1973) . Apparently, canids and ursids have been selected for quantity i n repro­duction . The paradoxically low fecundity rate in wolf and wild dog packs, where only one female may give birth , may be related to low availabil i ty of food . It i s interesting to note that if only one female gives birth i n a pack, i t is usually the most dominan t one. One might expect the 'fecundity rate to go up when food was abundan t . Whether this

274 Social Behavior In Some Carnivores

happens or not, the point is tha t the potential for a high reprod uctive ra te is there .

Unl ike l a n d ca rni vores, pi n n i peds m ll s t d e a l with problems t h a t arise from making a living to two quite different habitats . The high metabolic rate a nd th ick layer of blubber that a re so adapti ve in cold water crea te d i fficulties in thermoregulation on l a n d , pa rticu l a rly when the ambient temperature is h igh, or a fter sll stained activi ty has taken place . Numer­ous behavioral adj ustments are important in preventing overheating (White a nd Odel l , 1 971 ; G en try, 1 973; Odell, 1 974; Whittow, 1974 ) . In addition, one negative conseq uence of the large social gatherings on land is that the a ni mals are more vuln erable to disease and parasite transmi ssion . The colonia l breeding sea l i on s contain a wide variety of internal and externa l pa rasi tes (Dai ley and Brownell, 1 972) . For exa mple, seven species of trematod es, eigh t s peci es of nematodes, one cestode, and variou s speci es of Aca n thocephala , Aca ri n a , a n d Anoplura have been identi fied i n the Ca li fornia sea l i on . Lungworm infesta tion is par­ticu larly heavy in this speci es and may be a n i mporta n t ca use of j u venile morta l i ty . La nd carnivores do not seem to harbor the variety or the same high levels of parasi te i n festation as do these ma rine mammals . How­ever, this comparison needs to be i n vestiga ted more systema tical ly .

5 SUMMARY

I n summary, these two groups of a nimals have obvious similari ties , some of which ca n be a ttribu ted to having a common ancestor . Pin­nipeds bear the stamp of their ca nine, u rsine, and lu trine rela tives, especial ly i n the stru ctu re of the head and the pronou nced ca nine teeth . Most species in both orders are flesh ea ters; they ea t grea t quan ti ties a t a time, and they ea t a wi de variety of prey . However, subsistence in different habitats and exposure to differential selection for at least 20 million years have produ ced some even more obvious and interesting differences in social behavi'or. The larger canids evidently were selected to join social groups, in which there is a high degree of cooperation, because this allowed them to exploi t large prey . Canids tha t prey on a nimals smaller than themselves are far less social , and kin-network welfare is reduced . Pi nnipeds are social for a different reason . The most gregarious of them congrega te in immense gath erings tha t may include thousa nds of individuals . These aggregations are l oca ted o n offshore areas that are free from preda tors . Si nce these l oca tions are restricted in number a nd size, it appears tha t pinnipeds were forced to group to­gether in order to avoid preda tors . Once this s tep was taken, sexual

References 275

selecti on put a premi um on conti n u ed socia l l iv i ng; for exa mple, males who d omina ted oth er males in th e large social gatherings probably bore more offspring tha n those who pair- bonded with single females a way from th e grou p . The few pinniped species tha t are soli tary live in a habitat wh ere there a re few or no preda tors and wh ere hauling-out a reas, such a s pack ice, are vi rtual ly unl i m i ted . Final ly , s tra tegies of reprod u ction seem to d i ffer i n the two groups of a n imal s . I n general , the terres tria l ca rni vores a p pea r to have been selected to produce a grea t quanti ty of offspring quickly, a stra tegy tha t works best in a varying envi ron ment , wh ile pinnipeds a ppea r to have been selected to produce fewer progeny of h igh qual i ty, a stra tegy that is most characteri stic of stable envi ron ments .

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A n derso n , S. S . , W. N. Bonner, j . R. Ba ker, a n d R. Richards . 1974 . Grey seals, Halichoems grYl'lI s , of the Dee Estuary and observa t ions on a ch a racteristic skin lesion in British seals . j. Zool . ( Lond . ) 174 : 429-440.

Asde l l , S . A . 1 964. Pattems of Mallllllaliml Rel'roductioll . 2nd ed . Cornell University Press, New York. 670 p.

Bartholomew, G. A. 1953. Behavioral factors affecting social structure in the Alaska fur sea l . Trans. 18th No. Amer. Wildl . Conf. 481-502.

Bartholomew, G . A . 1959 . Mother-young rela tions and the matu ration of pup behavior in the Alaska fur sea l . Ani m . Behav . 7: 163--171 .

Bartholomew, G . A . 1970. A model for the evolution of pinniped polygyny. Evolution 24: 546-559.

Bartholomew, G . A . and P. G . Hoel . 1953 . Reproductive behaviour of the Alaska fur seal, Callorh il lus ursill us . j. Mamm. 34: 417-436.

Beach , F . A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm . and Beha v . 7: 105-138 .

Beach, F. A. and B. J . Le Boeuf. 1967. Coital behavior in dogs: I. Preferential mating in the bitch . Anim. Behav . 15: 546-558 .

Bekoff, M . 1975. Social behavior and ecology of the African Canidae: A review. III : M . W. Fox, Ed. The Wild Canids . Van Nostrand Rei nhold, New York. P . 120-142.

Bigg, M. A. 1969. The harbour seal in British Columbia . Fisheries Research Board of Canada Bulletin, Ottawa. 33 p .

Bishop, R . H . 1967. Reproduction, age determination , a n d behavior o f t h e harbor seal, Phoca vitu lina L . , in the Gulf of Alaska . Unpublished M. S . thesis, University of Alaska, 121 p.

Bonnel l , M. L. and R . K . Selander. 1974 . Elephant seals : genetic variation a nd near extinc­tion. Science 184: 908--909.

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