Download The evolution of reproductive systems in pinnipeds

Behavioral Ecology Vol. 10 No. 5: 612–616
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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 re-
gions. 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
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Table 1
Characteristics of otariid and phocid mating systems
Characteristic
Otariids
Most phocids
No. of species
Female density
15
Gregarious
Mating system
Male parental care
Sexual dimorphism
Breeding substrate
Mating substrate
Lactation
Polygyny
No
High
Land
Land
Long
15
Solitary to
moderately
gregarious
Slight polygyny
No
Low
Ice or land
Water
Short
H. grypus and
Mirounga spp.
3
Gregarious
Polygyny
No
High
Land
Land
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 repeat-
edly 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
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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
Behavioral Ecology Vol. 10 No. 5
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
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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.
615
Received 25 January 1998; revised 16 September 1998; accepted 31
March 1999.
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