Forum. The evolution of reproductive systems in pinnipeds

Transcription

1 Behavioral Ecology Vol. 10 No. 5: Forum The evolution of reproductive systems in pinnipeds Marcelo H. Cassini Universidad Nacional de Luján and Organización PROFAUNA, Argentina The order Pinnipedia is the only mammalian group that shows a combination of marine feeding and terrestrial breeding (Bartholomew, 1970). This order comprises three families: Otariidae, Phocidae, and Odobenidae. The latter group contains only the walrus Odobenus rosmarus, whose behavior has been poorly investigated (Renouf, 1991) and thus will not be considered here. Table 1 summarizes the characteristics of the mating systems of otariids and phocids. In both groups, males play no role in rearing offspring, and the mating system is defined in terms of the degree of female monopolization by males (Boness et al., 1993). In most pinnipeds, parturition and mating are seasonal and highly synchroniszed (Stirling, 1975). Otariids are among the most sexually dimorphic mammals, and breeding females are particularly gregarious (Bartholomew, 1970). Their mating system has been characterized as extreme polygyny, based on observations showing that a few males monopolize most of the matings (Le Boeuf, 1991). In most phocids, breeding females are sparsely distributed, and their mating system has been classified as slight polygyny (a male can mate with two to five females during a breeding season; LeBoeuf, 1991). Only three species of phocids, the two species of elephant seals (Mirounga spp.) and the gray seal Halichoerus grypus, reproduce like otariids. In gregarious pinnipeds, there is substantial evidence of density-dependent pup mortality (in Southern fur seals Arctocephalus australis, Harcourt, 1992; in Northern elephant seals M. angustirostris, Le Boeuf and Briggs, 1977; in gray seals H. grypus, Anderson et al., 1979; in Antarctic fur seals A. gazella, Doidge et al., 1984; in Northern fur seals Callorhinus ursinus, Fowler, 1987). Pups die mainly because social events separate them from their mothers and they consequently starve, are crushed in fights between territorial males, or are injured by aggressive females. As density increases, the probability of mother pup separations increases, and the probability of reunion of the dyad decreases. Even when pup mortality reaches high values [e.g., Majluf (1989) reported 46% mortality in A. australis], females of these species continue to breed in crowded colonies. In this paper, I address the question of why otariid females reproduce in dense clusters instead of behaving as their relatives, the phocid females, that rear their pups in isolation or in small groups. In species where males do not provide parental care, the mating system is ultimately influenced by the distribution of resources required by females for reproduction (Davies, 1991). In pinnipeds, there is general agreement that the distribution of key resources favors the tendency of females to aggregate and is a primary factor in the evolution of polygyny (reviewed by Boness, 1991; Le Boeuf, 1991; Stirling, 1983). Females prefer pupping sites that are close to feeding areas, offer protection from predators and storms, and contain resources for thermoregulation in temperate and tropical regions. All otariid species are land-breeders (i.e., they use beaches, rocky shelves, caves, or flat areas on dry land to rear offspring). For these species, suitable sites are patchily distributed. Thus, the distribution of females is expected to match the heterogeneous distribution of resources. On the other hand, most phocids rear their young on pack or fast ice. In this type of habitat, space for breeding is abundant and homogeneously distributed, which would favor an even distribution of females. Therefore, habitat selection may explain some of the differences in the pattern of distribution between phocids and otariids and was probably a prerequisite for the evolution of polygyny in social pinnipeds (Stirling, 1975, 1983). However, the distribution of suitable breeding sites cannot entirely account for the extreme clustering observed in gregarious species. In many of these species, it is normal to find empty shorelines with similar characteristics to those of the rookeries that support high densities of pinnipeds, even in close proximity (see reviews by Boness, 1991; Le Boeuf, 1991). Three main hypotheses have been proposed with regard to the selective forces that modify the social system and gregariousness of pinnipeds. These hypotheses postulate that females cluster to (1) reduce predation risk, (2) find mates, or (3) avoid male harassment (see review by Boness, 1991). In the first part of this paper, the evidence supporting these three hypotheses will be discussed. In the second part of this paper, the male harassment hypothesis will be expanded by incorporating a new idea that links the role of male harassment with the substrate on which copulation takes place. The basic rationale of this view is (1) female otariids are phylogenetically constrained to copulate on land, while phocids mate in the water. (2) Land copulation and low mobility allow intense male harassment of female otariids. (3) Male harassment leads to pup mortality. (4) Females dilute the risk of this reproductive cost by joining other females. (5) Female aggregation intensifies male male competition, resulting in fewer males per female, less male harassment, and higher pup survival. (6) The benefit of group formation in reducing male harassment overcomes other costs, mainly female female competition. (7) In contrast, phocid females do not suffer significant harassment on land, and the costs associated with group formation promote breeding in isolation or in loose aggregations. Predation risk as determinant of female aggregation The predation risk hypothesis states that by forming colonies, pinnipeds can reduce predation risk (Boness, 1991). It has been postulated that ice-breeding seals reproduce in isolation because they lack natural predators in that type of environment. In contrast, in land-breeding pinnipeds that reproduce in places where many terrestrial and aerial predators may attack pups and adults, group formation would reduce predation by dilution effects or by group defense. Pup predation has been studied in a number of species, and the ecological pattern predicted by this hypothesis is not found. Bowen (1991) reviewed the literature on the causes of pup mortality in pinnipeds and found that predation is a significant source of pup mortality in several species of ice-breeding pinnipeds. Predation rates by arctic foxes may reach 58% of all pups born in some areas of ringed seal Phoca hispida distribution (Bonner, 1989). Polar bears Ursus maritimus swim between ice

2 Forum 613 Table 1 Characteristics of otariid and phocid mating systems Characteristic Otariids Most phocids H. grypus and Mirounga spp. No. of species Female density Gregarious Solitary to Gregarious moderately gregarious Mating system Polygyny Slight polygyny Polygyny Male parental care No No No Sexual dimorphism High Low High Breeding substrate Land Ice or land Land Mating substrate Land Water Land Lactation Long Short Short floes, prey on harp seals Phoca groenlandica and ringed seals, and wolves appear to be significant predators of Caspian seals Phoca caspica (Bowen, 1991). Steller s sea lions Eumetopias jubatus can prey on harbor seals Phoca vitulina and ringed seals (Gentry and Johnson, 1981). Leopard seals Hydrurga leptonyx are thought to be important predators of crabeater Lobodon carcinophagus and Weddell seals Leptonychotes weddelli (Bowen, 1991). Walrus prey on ringed, bearded seals Erignathus barbatus, and largha seals Phoca largha (Lowry and Fay, 1984). Predation by sharks and killer whales has been reported in several species and appears to be a significant source of mortality in Hawaiian monk seals Monachus monachus and harbor seals (Bowen, 1991; Le Boeuf, 1978; Stirling, 1983). Studies of pup mortality in land-breeding pinnipeds have suggested that density-dependent effects are the most common source of preweaning mortality, although there are some studies showing the impact of predation. In South African fur seals (A. pusillus pusillus) that breed on the mainland, pups are heavily preyed on by two species of canids: Canis mesmelas and Hyaena brunnea (David, 1987). Several species of sea lions have been reported to prey on other otariids (reviewed by Harcourt, 1992). Sharks and killer whales also prey on otariids (Le Boeuf, 1978). From a theoretical perspective, it is not obvious why predation should be a potential selective force operating in favor of pinniped clustering. In a recent review of the evolution of colonialism, Danchin and Wagner (1997) concluded that the influence of predation on breeding dispersion is far from clear. Clode (1993) went further and suggested that colonialism in seabirds, far from being a protection against predators, makes birds more vulnerable. Grouping might reduce predation risk of an individual by two mechanisms: encounter effect and dilution effect (Inman and Krebs, 1987). The encounter effect states that detection of a prey by a predator does not increase in direct proportion to group size. In colonies of otariids, social interactions produce visual and acoustic signals that can be used by predators to increase prey detection (e.g., females call to find their own pups among hundreds of other pups and threaten other females and other members of the colony, males fight and vocalize for territorial defense, and pups play with other pups). These behaviors would be absent if females bred in isolation. If colonies are proportionally more conspicuous than isolated individuals, then the encounter effect hypothesis predicts that females will avoid breeding in colonies. The dilution effect is the decrease in the probability of an individual being attacked because the predator does not eat all the prey available in a group. Pinniped colonies are very stable in time and space. Therefore, once a colony is detected, predators can use it as their main source of food and repeatedly prey on the pups. If the carnivore possesses social habits (most canids, killer whales, sharks), its impact on the colony can be enormous, as seems to be in the case in South African fur seals (David, 1987). In summary, although the predation defense hypothesis might explain the tendency to use rookeries that offer protection from terrestrial predators, it is not clear that it can explain the evolution of clustering in most pinniped species. Mate choice as determinant of female aggregation Another hypothesis on the evolution of gregariousness states that, in a colony, females have more opportunities for selecting mating partners. By doing so, females would gain genetic benefits for their pups (Kirkpatrick and Ryan, 1991). Bartholomew (1970) postulated that any female that moves to the periphery of the colony is likely to be fertilized by a male that has been unsuccessful in establishing himself among the herd, an indication of low genetic quality. Stirling (1975) first questioned this paradigm by postulating that a proportion of the marginal males are individuals that later become fully territorial males. For example, young males may pursue a longterm strategy of staying alive and avoid fights with dominant males until they are big enough to compete effectively. These males are not necessarily genetically inferior to the actual possessors of territories. If females copulate with these peripheral males, they will obtain similar genetic benefits to those copulating within the colony. In his recent review on the mating systems of Otariidae, Boness (1991) considered there to be a lack of evidence linking female fitness to the proximity of a dominant male. Cox and Le Boeuf (1977) described a mechanism by which females of Northern elephant seals apparently facilitate mating with the superior genotype. These authors observed that females rejected all copulatory attempts during early estrus. They proposed that female protests activate the male dominance hierarchy. Dominant (genetically superior) males interrupt mounting by subordinate males and thus monopolize most matings. However, some aspects of female M. leonina behavior are difficult to explain with this hypothesis. In early estrus, females protest in any social context, even when there is only one male in the harem. In contrast, they do not protest and are extremely receptive to all males (including peripheral males) at the end of estrus. Preweaning mortality in elephant seals is primarily socially induced (e.g., due to female pup aggressions), and it occurs normally after mother pup separations (Le Boeuf, 1972). During a copulation attempt, a female cannot protect her pup and prevent its separation. Thus, mating attempts represent a form of male harassment, and protests could be a direct attempt to reduce it. Female protests can signal to the dominant male that a subordinate male is present that must be chased away from the harem. In this way, females induce the dominant male to rid the harem of other males that can harass them. The end of estrus coincides with the end of lactation. Therefore, if females protest to reduce male harassment, it would be expected that they stop protesting and accept mating when the risk to the pup is minimal that is, around weaning. In summary, the protest behavior may alternatively be interpreted as a mechanism of male harassment avoidance. The second study of mate choice by pinnipeds was conducted by Amos et al. (1995). Genetic analysis of pups of gray seals revealed large numbers of full siblings. The authors suggested that this result could be generated by two mechanisms: either a female s mate is determined by the relatively proximity and dominance of neighboring males and colony organization changes little between seasons, or seals recognize and select previous partners. Amos et al. (1995) found support for

3 614 Behavioral Ecology Vol. 10 No. 5 the second mechanism, and they proposed that this partner fidelity should reduce the disturbance caused by aggressive interactions involving males, a main cause of preweaning mortality in gray seals. Again, male harassment appears to be a key factor in modulating female reproductive behavior. In conclusion, evidence of mate choice in pinnipeds does not demonstrate that females join reproductive aggregations to gain genetic benefits for their offspring. Male harassment as determinant of female aggregation The importance of male harassment in increasing gregariousness of females has already been stressed for pinnipeds (Campagna et al., 1992; Trillmich and Trillmich, 1984) and other mammals (Clutton-Brock et al., 1992, 1993). In most colonial pinnipeds for which data exist, females (whether in estrus or not) when away from their territories are constantly harassed by marginal males (Trillmich and Trillmich, 1984). Dominant males may also harass females depending on species and number of females in their territories (reviewed by Boness, 1991). Male harassment in Otariids appears to be facilitated because of extreme sexual dimorphism in size and strength. Adult males of several species can take and carry a female with its mouth (Campagna et al., 1988; Francis, 1987; Marlow, 1975). Low mobility on land and the need to protect the pup place females at high risk of harassment. Male harassment affects pup survival because it may lead to mother pup separation (Le Boeuf and Briggs, 1977; Marlow, 1975; Vilá and Cassini, 1990) and because males may attack pups (Campagna et al., 1988). Harassment can also cause serious injury or kill females in several species (in Callorhinus ursinus: Francis, 1987; in M. angustirostris: LeBoeuf, 1991; in O. flavescens: Cassini and Vilá, 1990). Because females enter estrus a few days after parturition, males herd females and attempt copulations when the pup is only a few days old. If this newborn pup becomes separated from the mother, the probability of reunion is expected to be low, and death is likely from starvation, aggression, or crushing. Although male harassment has been described in most otariid species, Campagna et al. (1992) conducted the only published study that directly tested the effect of harassment of males on female reproductive success. They compared mortality between pups born in the colony and those born in isolated pairs formed by a female and a marginal male. Mortality was 0.7% in pups born within the colony at the peak of the reproductive season, whereas it was 60% in pups born to females separated from the colony. These authors also demonstrated that the main cause of pup mortality in solitary pairs was male harassment. Other studies have suggested that male harassment is an important factor negatively affecting female reproductive success in social pinnipeds. For example, Bryden (1968, cited by Wartzok, 1991) compared pup survival in two colonies of southern elephant seals (M. leonina) and found that it was better in the colony where the density of males was reduced through harvesting. Male harassment and mating substrate Terrestrial copulation is characteristic for otariids, whereas most phocids demonstrate aquatic mating. Terrestrial male harassment is expected to be high when copulation occurs on land, but not in the water. In species with aquatic mating, males would gain more by patrolling the water searching for receptive females than by harassing females on land. Phocids also have a short lactation period and an abrupt weaning (reviewed by Bowen, 1991), and females enter estrus near or after the end of lactation. Therefore, phocid females are able to separate nursing from mating, which I predict reduces the risk of male harassment of pups. Observation seals on land supports this prediction. During the lactation period, the frequency of interactions between nursing females and males is normally low. In several species this is simply because males are not in the vicinity of nursing females (in Hawaiian monk seals, Johanos et al., 1994; in Weddell seals, Bartsh et al., 1992). When males have been found on land near female pup dyads, harassment attempts were rarely observed, and occurred mainly around weaning (in hooded seals, Perry and Stenson, 1992; in harp seals; Kovacs, 1987; in harbor seals, Walker and Bowen, 1993). Only in crabeater seals are male female interactions relatively frequent (Shaughnessy and Kerry, 1989; Siniff et al., 1979). The terrestrial interactions between males and females or pups of noncolonial seals have not been reported as a cause of preweaning mortality of pups (reviewed by Bowen, 1991). In summary, females of pinnipeds with aquatic mating normally rear their newborn pups without suffering male harassment, whereas solitary females of pinnipeds with terrestrial copulation are frequently harassed. The importance of the substrate for copulation on the reproductive system of pinnipeds was recognized early in the literature (Bartholomew, 1970; Stirling, 1975), but with no account taken of the detrimental effect of terrestrial male harassment on female reproductive success. Instead, the explanation given is based exclusively on male behavior, postulating that the difficulty in defending territories in the water prevented the evolution of polygyny in pinnipeds with aquatic mating. Stirling (1975, 1983) postulated that terrestrial mating in otariids represents a phylogenetic legacy. His argument is based on the classical diphyletic theory on the origin of the Pinnipedia (Wozencraft, 1991). This theory postulates that Otariidae and Ursidae represent one monophyletic group within the order Carnivora and the Mustelidae and the Phocidae represent another. The present ursids, which evolved from the same basic stock as the otariids, copulate terrestrially. Stirling (1975, 1983) suggested that their ancestors also did so at the time the otariids diverged. On the other hand, the present Lutrinae may copulate in the water (and they prefer it), thus the phocids probably diverged with the capacity for aquatic mating (Stirling, 1975, 1983). Therefore, terrestrial copulation can be interpreted as a phylogenetic constraint of otariid females that exposes them to male harassment. The evolutionary consequences of male harassment A plausible sequence for the evolution of extreme gregariousness is as follows. Initially, females may have concentrated on preferred sites, independently of the behavior of conspecifics. The clumped distribution of females selected for large males who monopolized matings, while marginal males were forced to attempt copulations with females that bred outside the territories of dominant males. Thus, male harassment started reducing the reproductive success of females that bred in isolation or in small groups. As a consequence, there was selection for more gregariousness, and females joined bigger aggregations to dilute the effect of male harassment. At this point, a positive feedback loop was created, with females joining bigger, denser groups to avoid male harassment, intensifying male intrasexual selection, and increasing the proportion of marginal males that harassed females and promoted female aggregation. With this feedback loop established, the environmental factors that originally favored female clustering became unnecessary to maintain the social system. When male harassment is not an important cost, as in most phocids, female female competition will prevent females

4 Forum 615 forming breeding clusters, and a less clumped distribution is expected. Thus, the consequence of this simple rationale is that the main determinant of the social evolution in pinnipeds is the substrate where copulation takes place because it determines the strength of male harassment, which in turn modifies female distribution and creates the conditions for sexual selection to operate. Phocids that copulate on land There are exceptions to the taxonomic pattern in the substrate of copulation. Elephant seals and gray seals are phocids that copulate mainly on land, although a small percentage of matings do occur in the water (Le Boeuf, 1991). These two species are also exceptions to the phocid pattern in that they show extreme polygyny and sexual dimorphism. Gray seals are especially interesting because there are some populations that breed on ice in triads of a female and her pup together with an accompanying male (Bonner, 1989). Although not well documented, it has been suggested that in this context, copulations occur in the water (Bonner, 1989; Boness et al., 1993). Conversely, several species of otariids can occasionally copulate in shallow water adjacent to the rookeries (in A. philippii, Francis and Boness, 1991; in A. pusillus, Rand, 1953; in N. cinerea and P. hookeri, Marlow, 1975; in O. flavescens, Cassini, personal observation; in C. ursinus, Bartholomew and Hoel, 1953). Most of these matings cannot be considered aquatic because males require the mechanical support afforded by solid ground for the successful completion of mating. Conclusions Many studies of the social behavior of gregarious pinnipeds have described frequent disturbance of solitary females by males trying to herd and mate with them. Nevertheless, most published explanations of the evolution of mating systems in this group have taken mate encounters, food distribution, male selection, and/or predation as the most important selective pressures, and they have relegated male harassment to a secondary role or a by-product of the intense sexual selection that generates a great variance in male reproductive success. In this paper, I have inverted the order of the factors by assuming that male harassment has played a fundamental role in the evolution of breeding aggregations. Recent findings have shown that in many birds, fish, anurans, and insects, females play a more active role in determining breeding systems by engaging in activities that increase mating benefits (reviewed by Reynolds, 1996). These can be direct benefits such as parental care for the offspring or genetic benefits. In this paper, I analyzed the other side of the coin by addressing the problem of mating costs. In particular, I investigated how the detrimental effects of male harassment and mating attempts on the probability of survival of current offspring can explain the breeding systems of pinnipeds. The ideas presented in this paper could be useful to explain the origin of reproductive systems in other mammalian taxa. I am very grateful to W Sutherland, M. L. Guichón, H. L. Cappozzo, and R. H. Wagner for their valuable comments on an early version of the manuscript, and to N. Reeve and A. Liebert for correcting the English. I especially thank H. L. Cappozzo for helpful discussions and for allowing me using his library. Key words: breeding system, evolution, Otariidae, phocidae, pinnipeds, reproductive behavior. Received 25 January 1998; revised 16 September 1998; accepted 31 March REFERENCES Amos B, Twiss S, Pomeroy P, Anderson S, Evidence of mate fidelity in the gray seal. Science 268: Anderson SS, Baker JR, Prime JH, Baird A, Mortality in grey seal pups: incidences and causes. J Zool 189: Bartholomew GA, A model for the evolution of pinniped polygyny. Evolution 24: Bartholomew GA, Hoel PG, Reproductive behavior of the Alaska fur seal Callorhinus ursinus. J Mammal 34: Bartsh SS, Johnston SD, Siniff DB, Territorial behavior and breeding frequency of male Weddell seals (Leptonychotes weddelli) in relation to age, size, and concentrations of serum testosterone and cortisol. Can J Zool 70: Boness DJ, Determinants of mating systems in the Otariidae (Pinnipedia). In: Behavior of pinnipeds (Renouf D, ed). London: Chapman and Hall; Boness DJ, Bowen WD, Francis JM Implications of DNA fingerprinting for mating systems and reproductive strategies of pinnipeds. Symp Zool Soc Lond 66: Bonner WN, The natural history of seals. Kent, UK: Christopher Helm Publishers. Bowen WD, Behavioral ecology of pinniped neonates. In: Behavior of pinnipeds (Renouf D, ed). London: Chapman and Hall; Campagna C, Bisioli C, Quintana F, Perez F, Vila A, Group breeding in sea lions: pups survive better in colonies. Anim Behav 43: Campagna C, LeBoeuf BJ, Cappozzo HL, Group raids: a mating strategy of male southern sea lions. Behaviour 105: Cassini MH, Vilá BL Male mating behaviour of southern sea lions. Bull Mar Sci 46: Clode D, Colonially breeding seabirds: predators or prey? Trends Ecol Evol 8: Clutton-Brock TH, Deutsch JC, Nefdt RJC, The evolution of ungulate leks. Anim Behav 46: Clutton-Brock TH, Price O, MacColl A, Mate retention, harassment, and the evolution of ungulate leks. Behav Ecol 3: Cox CR, LeBoeuf BJ, Female incitation of male competition: a mechanism in sexual selection. Am Nat 111: Danchin E, Wagner RH, The evolution of coloniality: the emergence of new perspectives. Trends Ecol Evol 12: David JHM South African fur seal, Arctocephalus pusillus pusillus. In: Status, biology and ecology of fur seals (Croxall JP, Gentry RL, eds), NOAA Technical Report NMFS, no. 51. Washington, DC: Government Printing Office; Davies NB Mating systems. In: Behavioural ecology: an evolutionary approach (Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific; Doidge DW, Croxall JP, Baker JR, Density-dependent pup mortality in the Antarctic fur seal Arectocephalus gazella at South Georgia. J Zool 202: Fowler CW, A review of density dependence in populations of large mammals. Curr Mammal 1: Francis JM, Interfemale aggression and spacing in the Northern fur seal, Callorhinus ursinus, and the California sea lion, Zalophus californianus (PhD dissertation). Santa Cruz: University of California. Francis JM, Boness DJ, The effect of thermoregulatory behavior on the mating system of the Juan Fernandez fur seal Arctocephalus philippii. Behaviour 119: Gentry RL, Johnson JH, Predation by sea lions on northern fur seal neonates. Mammalia 45: Harcourt R, Factors affecting mortality in the South American fur seal (Arctocephalus australis) in Peru: density-related effects and predation. J Zool 226: Inman AJ, Krebs JR, Predation and group living. Trends Ecol Evol 2: Johanos TC, Becker BL, Ragen TJ, Annual reproductive cycle of the female Hawaiian monk seal (Monachus schaunislandi). Mar Mammal Sci 10:13 30.

5 616 Behavioral Ecology Vol. 10 No. 5 Kirkpatrick M, Ryan MJ, The evolution of mating preferences and the paradox of the lek. Nature 350: Kovacs KM, Maternal behaviour and early behavioural ontogeny of harp seals. Anim Behav 35: Le Boeuf BJ, Sexual behaviour in the Northern elephant seals. Am Zool 14: Le Boeuf BJ, Social behavior in some marine and terrestrial carnivores. In: Contrasts in behavior (Reese ES, Lighter FJ, eds). New York: John Wiley and Sons; Le Boeuf BJ, Pinniped mating systems on land, ice and in the water: emphasis on the Phocidae. In: Behavior of pinnipeds (Renouf D, ed). London: Chapman and Hall; Le Boeuf BJ, Briggs KT, The cost of living in a seal harem. Mammalia 41: Lowry LF, Fay FH., Seal eating by walruses in the Bering and Chukchi Seas. Polar Biol 3: Majluf PJ, Reproduction ecology of South American fur seals in Peru. In: Proceedings of the International Centre for Living Aquatic Resources Management Conference, Callao, Perú, 1 2 September 1987 (Pauly D, Muck P, Mendo J, Tsukayama I, eds). Manila: International Centre for Living Aquatic Resource Management; Marlow BJ, The comparative behaviour of the Australasian sea lions Neophoca cinerea and Phocarctos hookeri (Pinnipedia: Otariidae). Mammalia 39: Perry EA, Stenson GB, Observations on nursing behaviour of hooded seals, Cystophora cristata. Behaviour 122:1 10. Rand RW, Reproduction in the female Cape fur seal Arctocephalus pusillus. Proc Zool Soc Lond 124: Renouf D (ed), Behavior of pinnipeds. London: Chapman and Hall. Reynolds JD Animal breeding systems. Trends Ecol Evol 11: Shaughnessy PD, Kerry KR, Crabeater seals Lobodon carcinophagus during the breeding season: observations on five groups near Enderby Land, Antartica. Mar Mammal Sci 5: Siniff DB, Stirling I, Bengston JL, Reichle RA, Social and reproductive behaviour of crabeater seals (Lobodon carcinophagus) during the austral spring. Can J Zool 57: Stirling I, Factors affecting the evolution of social behavior in the Pinnipedia. Rapp P-v Reun Conserv Int Explor Mer 169: Stirling I, The evolution of mating systems in pinnipeds. In: Advances in the study of mammalian behaviour (Eisenberg JF, Kleinman DG, eds), Special Publication no. 7. American Society of Mammalogists; Trillmich F, Trillmich KGK, Mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny. Biol J Linn Soc 21: Vilá BL, Cassini MH, Aggressiveness between females and mother pup separation in the southern sea lion, in Chubut, Argentina. Revista Chilena Hist Nat 63: Walker BG, Bowen WD, Behavioural differences among adult male harbour seals during the breeding season may provide evidence of reproductive strategies. Can J Zool 71: Wartzok D, Physiology of behaviour in pinnipeds. In: Behavior of pinnipeds (Renouf D, ed). London: Chapman and Hall; Wozencraft WC, The phylogeny of recent Carnivora. In: Carnivore behavior, ecology, and evolution (Gittleman JL, ed). Ithaca, New York: Cornell University Press;