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Behavioral Ecology Vol. 10 No. 5: 612-616
© 1999 International Society for Behavioral Ecology
Forum |
The evolution of reproductive systems in pinnipeds
Universidad Nacional de Luján and Organización PROFAUNA, Argentina
Received 25 January 1998; revised 16 September 1998; accepted 31 March 1999.
Key words: breeding system, evolution, Otariidae, phocidae, pinnipeds, reproductive behavior.
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).
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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 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 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 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.
ACKNOWLEDGEMENTS
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.
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