Harem choice and breeding experience of female southern elephant seals influence offspring survival

Female mammals can increase their lifetime fitness through modification of investment potential and by providing better rearing environments with improved breeding experience. We examined the relationships between reproductive fitness and the behavioural decisions that female southern elephant seals (Mirounga leonina) made during the breeding season. We examined whether mother age and breeding experience influenced reproductive success (measured as 1st-year survival probability), and whether there was a change in the choice of harem size with increasing age. Pups produced by young mothers had lower 1st-year survival probability than pups produced by older mothers. A significant increase in mean female mass with age required an analysis of both these effects on offspring survival. There was a significant positive effect of both female age and mass, and the interaction between the two, on 1st-year pup survival. The proportion of young mothers (<5 years old) decreased and the proportion of older mothers (>6 years old) increased with increasing harem size (harems surveyed from 1997 to 2001). Females chose larger harems in which to breed as they aged. Females demonstrated fidelity to breeding areas among successive breeding seasons, with older females displaying greater breeding-site fidelity than younger females. The mean number of previous breeding attempts per female within a harem (breeding experience) increased significantly with increasing harem size. Breeding females returned to breed later in the breeding season as they aged—we hypothesize that young, subordinate females gain a priority advantage by returning earlier. These results lend support to the hypothesis that there are fitness advantages, in terms of offspring survival, that are conferred to females that breed in successively larger harems with age. Potential mechanisms that select for females to improve their breeding conditions include improved mate selection and the avoidance of conspecific harassment in harems.Communicated by F. Trillmich     

Parental investment and the secondary sex ratio in northern elephant seals

Summary Data on northern elephant seals, Mirounga angustirostris, bearing on sex ratio theory were collected at Año Nuevo, California, and other Californian and Mexican Islands, during the period 1967 to 1988. The mass of males exceeded that of females by 7–8% at birth and at weaning. The sex ratio was biased to males at birth (51.2%) and was near unity at weaning (49.6% males). The sex ratio did not vary as a function of maternal age or maternal mass except in 6-year-old females, who produced significantly more males. Although sons cost more to rear in energetic terms than daughters, and mothers were more successful weaning the latter, the sex of the pup reared exerted no significant effect on the mother's reproductive performance the following year or on her subsequent survival. These data suggest that parents invest equally in sons and daughters when investment is measured in terms of future reproduction (Fisher 1930) and provide no support for the theory of adaptive shifts in sex ratio (Trivers and Willard 1973). The small sex difference in mass due to maternal effort reflects the fact that females fast during lactation and all energy transferred is from limited body stores. Because of these circumstances, selection for superior condition at the end of the period of parental investment may act more strongly on pups, who have the opportunity to steal milk, than on their mothers.     

Mother-pup separation and adoption in northern elephant seals

Summary The evolution of fostering behavior, parental care directed toward another's young, has been the focus of much recent interest. During a five-year study of northern elephant seals (Mirounga angustirostris) at Año Nuevo, California, we recorded the frequency of mother-pup separation, reunion, and adoption of orphaned pups in crowded and low-density breeding areas. While most females nursed their own pup exclusively until it was weaned, many females, especially young mothers (age 3–5 years), were unable to raise a pup successfully. In the crowded main breeding harem on Año Nuevo Island, 24 to 47 percent of the pups born each year were separated from their mothers from 1977 to 1980. Mother-pup separation and pup mortality were associated with the following inter-related factors: 1) female density; 2) weather and tidal conditions; 3) topographical features of the breeding areas (i.e., degree of exposure to high tides and surf); and 4) the proportion of young, maternally inexperienced females pupping in a particular area. Most motherpup separations were caused directly by 1) adult males moving through the harem; 2) pups wandering from their mothers; 3) female aggression; and 4) inclement weather. Most of the separations, as well as adoptions, occurred when pups were quite young. Mother-pup recognition appeared to be based on a combination of acoustic, visual, and olfactory cues, and most mother-pup reunions were effected by the female rather than her pup. On the main island breeding area, 572 orphans were marked. Of these, five percent relocated their mother, 27 percent were adopted or frequently cared for by foster mothers, and 68 percent were not adopted, or rarely fostered. The survival of an orphan was clearly contingent on the amount of care it received; most orphans which were not nursed or protected by females died before reaching 6 weeks of age. Frequently, an adopted orphan's foster mother was in the stage of lactation which corresponded closely to that of its own mother. The most common fostering event involved females that had lost their own pup and adopted a single orphan. Other pupless females attempted to steal a pup, cared for a pup while it was still with its mother, adopted a weaned pup, adopted two pups, or indiscriminately nursed any orphaned pup that approached. Some females kept their own pup in addition to fostering in alien pup. Most foster mothers were young and had little or no previous maternal experience. The formation of large, high-density breeding rookeries, due to a scarcity of suitable breeding sites, results in frequent mother-pup separations, especially during inclement weather and tidal conditions. Many opportunities for adoptive behavior are therefore presented, because of the great number of orphans and pupless females. Increased maternal experience appears to be a benefit associated with adoption. Some instances of fostering behavior may also be based on reproductive errors on the part of the foster mother.     

Offspring sex ratio in relation to female size in southern elephant seals,Mirounga leonina

Southern elephant seals Mirounga leonina display extreme sexual dimorphism. In addition females show great variation in size and stored resources at parturition. Therefore they present an excellent opportunity for examination of responses of sex ratio to resource availability. We studied the relationships between the size of southern elephant seal females at parturition and the size and sex of their pups at South Georgia over four breeding seasons. We found a large individual variation in maternal post-partum mass (range 296–977 kg, n=151). Larger mothers gave birth to larger pups, irrespective of the sex of their pup. Male pups were on average 14% larger than females at birth and consequently more costly to bring to parturition. Our results suggest that female southern elephant seals must weigh more than 300 kg if they are to breed at all, and more than 380 kg if they are to give birth to a male pup. Above this threshold the proportion of males among offspring rapidly increases with maternal mass, and stabilizes at a level not significantly different from parity. These results show that smaller females of southern elephant seals vary offspring sex ratio in a way that is consistent with theories on adaptive offspring sex ratio. A smaller mother with a male foetus may benefit from terminating her pregnancy and allocating the resources she saves to her own growth. She could then give birth to and raise a larger pup in the subsequent season.     

Socially induced delayed primiparity in brown bears Ursus arctos

Reproductive suppression through behavioral or physiological means is common in group-living and cooperative breeding mammals, but to our knowledge it has not been shown in wild large carnivores other than those with a clear form of social organization. Brown bear (Ursus arctos) females form matrilinear assemblages with related females using a common and largely exclusive area. Behavioral reproductive suppression might develop due to a hierarchical system among females within a matrilinear assemblage or due to inbreeding avoidance, because male brown bears can overlap with their daughters. We tested whether natal dispersal influenced the age of primiparity. We predicted that emigrant females, geographically removed from maternal or paternal influence, would reproduce earlier than philopatric females. The average age of primiparity was 4.3 years in females that dispersed outside their mother’s home range (n=8) and 5.2 years in philopatric females (n=10). Only the overlap with the mother’s home range, and not body size, body mass, growth, local population density, or overlap with the father’s home range, had a significant influence on the age of primiparity. The ultimate role of reproductive suppression for brown bears is likely to avoid inbreeding or to minimize resource competition. Due to the low risk of inbreeding and frequent exposure of young females to unrelated males, we conclude that resource competition within female hierarchies causes reproductive suppression in young females.     

The cost of success: reproductive effort in male southern elephant seals (<Emphasis Type="Italic">Mirounga leonina</Emphasis>)

Reproductive effort is a key parameter of life history because it measures the resources allocated to reproduction at the expense of growth and maintenance. Male reproductive effort always had a minor role with respect to female effort both in the development of theories and in field research. Elephant seals are an ideal subject for reproductive effort studies because they fast during the breeding season, splitting the phase of energy acquisition from the phase of energy use for breeding. In this paper, we present results on male reproductive effort (weight loss estimated by photogrammetry) in southern elephant seals (Mirounga leonina), the most dimorphic and polygynous of all mammal species. We show that total reproductive effort increases with age, with no sign of late decrease or senescence. Male reproductive effort in this species depends mostly on behavioral factors, i.e., the success in competition with other males, and the intensity of interaction with females. A large effort results in large gains in both mating success and fertilizations. The large reproductive success that a few males are able to achieve come at a big cost in terms of energy expenditure, but this cost does not seem to affect the likelihood of survival to the following breeding season.     

Parental investment in southern elephant seals,Mirounga leonina

Summary The southern elephant seal is among the most sexually dimorphic and polygynous of all mammals: males may be more than 10 times the weight of reproducing females and only the largest 2–3% of males are likely to breed. Current optimization theories of sexual selection predict that evolution would favor greater parental investment in individual males than in females. Because southern elephant seals represent an extreme of polygyny and sexual dimorphism, they might be expected to show a dramatic difference in parental investment in male and female pups. However, in a study of parental investment in elephant seals at South Georgia, using several different methods, we found no such difference after parturition. Mother-pup pairs were immobilized and weighed early in lactation, recaptured near the end of lactation and reweighed. A further 30 pups were weighed an average of five times during lactation to establish the shape of the growth curve and to serve as partial controls for the previous set of animals. Initial post-partum weight in females ranged from 346 to 803 kg (=506, SD=111, n=26). Pup birth weight was related to mothers' post-partum weight in female pups but small females often gave birth to large male pups. Male pups were significantly heavier at birth than females. However, this size difference did not persist. Male and female pups were suckled for the same period, grew at the same rate and were not significantly different in weight at weaning. Mothers lost weight at the same rate regardless of their pup's sex.     

Paternity analysis shows experience,not age,enhances mating success in an aquatically mating pinniped,the Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>)

For polygynous mammals with no paternal care, the number of offspring sired is often the sole measure of male reproductive success. The potential for polygyny is highest when resources or other environmental factors such as restricted breeding sites force females to aggregate. In these circumstances, males compete intensely for females and mating success may vary greatly among males, further intensifying selection for those traits that confer an advantage in reproduction. Hence, determinants of male success in competition for females are likely to be under strong sexual selection. Paternity analysis was used in conjunction with measures of age, site fidelity, and behavior during the breeding season to assess variance in male breeding success in Weddell seals (Leptonychotes weddellii) breeding at Turtle Rock, McMurdo Sound (77.727S, 166.85E) between 1997 and 2000. Paternity could be assigned to 177 pups at relaxed or 80% confidence level or 111 pups at strict or 95% confidence levels. Weddell seals at Turtle Rock show a modest degree of polygyny with the greatest number of pups sired by any individual male in a single season equalling 5 or ∼10% of the pups born. Over four consecutive years, most (89.2%) males sired at least one pup. In a generalized linear model (GLM), age and the age first seen at the study site as an adult were unrelated to mating success, but adult experience, either site-specific or elsewhere in McMurdo Sound, over the reproductive life span of males explained nearly 40% of variance in total mating success with 80% confidence and 24% of variance at 95% confidence. While learning where females are likely to be may enhance male reproductive success, aquatic mating reduces the ability of males to monopolize females, and thereby increases equity in mating success.     

Social organization in the bat Pipistrellus pipistrellus

Summary The social organization of the pipistrelle bat (Pipistrellus pipistrellus) was studied by means of bat boxes in southern Sweden. The males set up territories around a roosting site in the beginning of the summer at the same time as the females formed nursing colonies. After breeding, the females joined the single males in their day roosts establishing transient mating harems. Subsequently, immatures arrived at the mating grounds. The immature females, which probably attained sexual maturity during their first autumn, were admitted to the day roosts of the harem males, in contrast to the immature males. The size of the harem was dependent on the total number of females present on the mating grounds. The size, however, was also restricted by some factor, presumably the quantity of food resources in the surroundings of the specific roost site, or the capability of the harem male for mating. The mating system in the pipistrelle bat is best characterized as a resource defence polygyny. Available data on other related temperate species indicate a similar social organization in Pipistrellus nathusii and Nyctalus noctula.     

Maternal investment in Antarctic fur seals: evidence for equality in the sexes?

Studies of the otariids (fur seals and sea lions), a highly sexually dimorphic group, have provided conflicting evidence of differential maternal expenditure in male and female offspring and, thus, suggestions that they conform to predictions of investment theory are equivocal. Since the mid-1970s, a diversity of research on Antarctic fur seals (Arctocephalus gazella) including studies of their reproductive ecology, lactation energetics, and foraging behaviour have been conducted at Bird Island, South Georgia that have resulted in one of the more complete and diverse data sets for any species of otariid. These long-term data were reviewed to determine whether there was any evidence to support that differential maternal expenditure occurred in Antarctic fur seals. Most of the data examined were collected during five consecutive austral summers from 1988 through 1992 and included years in which local food resources were abundant and scarce. We were unable to detect differences in the sex ratios of pups at birth or sex-biased differences in growth rates estimated from serial data, the number of foraging trips made, the duration of attendance ashore, diving behaviour, suckling behaviour, or milk consumption in any year and in the duration of foraging trips or age at weaning in 2 of 3 years. In addition, we found no evidence of greater reproductive costs between mothers with sons or daughters relative to their reproductive performance the following year. In contrast, sex-biased differences were only found in the duration of foraging trips in 1990, the age at weaning in 1988, and consistently in growth rates estimated from cross-sectional data. We suggest that differential maternal expenditure does not occur in Antarctic fur seals because male pups probably do not gain greater benefit from additional maternal expenditure than female pups. After weaning, males experience a period of rapid juvenile growth over 3–4 years during which time body mass nearly trebles. This growth will almost certainly be dependent upon available food resources then rather than on any maternal expenditure received over the first 4 months of life and, thus, the assumptions of the Trivers and Willard hypothesis are probably invalid for Antarctic fur seals. Received: 10 July 1996 / Accepted after revision: 3 March 1997     

Age-related shifts in the diet composition of southern elephant seals expand overall foraging niche

Southern elephant seals are important apex predators in a highly variable and unpredictable marine environment. In the presence of resource limitation, foraging behaviours evolve to reduce intra-specific competition increasing a species’ overall probability of successful foraging. We examined the diet of 141 (aged 1–3 years) juvenile southern elephant seals to test the hypotheses that differences between ages, sexes and seasons in diet structure occur. We described prey species composition for common squid and fish species and the mean size of cephalopod prey items for these age groups. Three cephalopod species dominated the stomach samples, Alluroteuthis antarcticus, Histioteuthis eltaninae and Slosarczykovia circumantarcticus. We found age-related differences in both species composition and size of larger prey species that probably relate to ontogenetic changes in diving ability and haul-out behaviour and prey availability. These changes in foraging behaviour and diet are hypothesised to reduce intra-specific food competition concomitant with the increase in foraging niche of growing juveniles.     

A Population Viability Analysis for African Elephant (Loxodonta africana): How Big Should Reserves Be?

We present an age-structured, density-dependent model of elephant population dynamics in a fluctuating environment, drawing primarily upon the life history parameters obtained from studies in semi-arid land at Tsavo National Park, Kenya. Density regulation occurs by changes in the age of first reproduction and calving interval. We model environmental stochasticity with drought events affecting sex- and age-specific survivorships. Results indicate a maximum population growth rate of 3% per year and an equilibrium elephant density of 3.1/mile². Analysis of the demographic results and their sensitivity to changes in juvenile survivorship and drought frequencies, supported by genetic considerations, suggests that in semi-arid regions a minimum reserve size of 1000 mile² is necessary to attain a 99% probability of population persistence for 1000 years. The effect of age-independent culling on population viability is also analyzed.     

Life history costs and consequences of rapid reproductive maturation in female rhesus macaques

Summary Life history theory suggests that reproduction at one point in time involves costs in terms of energy, reduced survival, or probability of reproduction at a future point in time. ln long-lived iteroparous organisms, initiating reproduction at a relatively young age may exact a cost in terms of reduced survivorship, but an early age of first reproduction could be beneficial if it lengthens the breeding lifespan. Data collected over 30 years from one population of rhesus macaques, Macaca mulatta, were analyzed to determine the fertility and survivorship costs of initiating reproduction at a relatively young age. Low population density and high social status increased the chances of accelerating age at first parturition, but high dominance rank was not associated with greater lifetime reproductive success. Rapid reproductive maturation neither reduced short-term survivorship nor decreased lifespan. Fertility costs arose if young females reared a male, but not female, offspring. The fitness consequences of rapid reproductive maturation depend upon longevity, with age at death having a significantly greater impact on lifetime reproductive success than age at first parturition.Correspondence to: F.B. Bercovitch     

Female aggression and male peace-keeping in a cichlid fish harem: conflict between and within the sexes in Lamprologus ocellatus

Summary Conflicts of interest within and between the sexes are important processes leading to variability in mating systems. The behavioral interactions mediating conflict are little documented. We studied pairs and harems of the snail-shell inhabiting cichlid fish Lamprologus ocellatus in the laboratory. Due to their larger size, males controlled the resource that limited breeding: snail shells. Males were able to choose among females ready to spawn. Females were only accepted if they produced a clutch within a few days of settling. When several females attempted to settle simultaneously the larger female settled first. Females were least aggressive when guarding eggs. Secondary females were more likely to settle when the primary female was guarding eggs. In established harems females continued to be aggressive against each other. The male intervened in about 80% of female aggressive interactions. Male intervention activity correlated with the frequency of aggression among the females in his harem. The male usually attacked the aggressor and chased her back to her own snail shell. When a male was removed from his harem, aggression between females increased immediately and usually the secondary female was expelled by the primary female within a few days. Time to harem break-up was shorter the more mobile the primary females' young were and did not correlate with the size difference between harem females. Male L. ocellatus interfere actively in female conflict and keep the harem together against female interests. Female conflict presumably relates to the cost of sharing male parental investment and to the potential of predation by another female's large juveniles on a female's own small juveniles.Correspondence to: F. Trillmich     

Maternal investment and sex-allocation in the Galapagos fur seal,Arctocephalus galapagoensis

Summary Maternal investment and sex-allocation were measured in a large, sexually dimorphic mammal, the Galapagos fur seal (Arctocephalus galapagoensis). The sex ratio at birth was 1.06. Males were always heavier than females and, at least initially, grew faster. Growth was variable from year to year suggesting energetic constraints on maternal investment. Sucking time conrrelated with milk intake. Mothers suckled yearling and 2-year-old sons more than daughters of the same age. Age at weaning appeared to be the same in both sexes or even slightly greater in males. No sex differences was found in mortality prior to weaning or in post-weaning dispersal. Birth rates of females with yearlings or 2-year-olds were significantly lower than those of females with no dependent young. Mothers invested more in sons than in daughters until weaning. It is unlikely that higher post-weaning investment in daughters balances the higher pre-weaning investment in sons. Data on sex ratio at birth, different growth rates, and weaning age of the sexes are typical of otariid seals as a group. The results of this study fit Maynard Smith's (1980) model of the evolution of sex allocation better than Fisher's (1930).     

An Age-Structured Demographic Model for the Endangered Stephens' Kangaroo Rat

Effective conservation of endangered species often is hampered by inadequate knowledge of demography. We extracted information on survival and fecundity from an 18-month, live-trapping study of Dipodomys stephensi , and from this we developed an age-structured demographic model to assess population viability. Adult Stephens' kangaroo rats persisted longer than juveniles, and adult females persisted longer than adult males. Disappearance rates were high in the first months after initial capture. Thereafter, the fraction of animals persisting decreased slowly and in an approximately linear fashion on a semilogarithmic scale, suggesting age-independent mortality factors such as predation. Juvenile persistence did not differ substantially between two years of strikingly different rainfall. Onset of breeding followed the start of winter rains. Length of the breeding season, average number of litters per female, and the fraction of first-year females breeding were much greater in the year of higher rainfall. We propose a birth-pulse demographic model for D. stephensi that distinguishes juvenile and adult age classes. Temporal environmental variation can be modeled adequately with a constant survivorship schedule and variable fecundity determined by yearly precipitation. Several issues should be resolved, however, before conservation decisions are based on the model. Better estimates of juvenile survivorship are critical, the quantitative relationship between precipitation and fecundity must be determined, and the potential for density dependence and source-sink population dynamics must be evaluated.     

Why do female Belding's ground squirrels disperse away from food resources?

We examined the effects of food provisioning on the natal dispersal behavior of Belding's ground squirrels (Spermophilus beldingi). We provided extra food to adult and yearling females in their maternal territories during pregnancy and lactation, and to offspring of these females in their natal areas for 6 weeks after weaning. We used unprovisioned young of unprovisioned mothers as controls. Provisioning influenced the probability of dispersal from the natal area by female but not male S. beldingi. All surviving male S.␣beldingi dispersed by 55 weeks of age, regardless of whether they and their mothers received extra food. By contrast, we observed a significant trend, beginning 3 weeks after weaning and continuing through the yearling year, for a greater proportion of provisioned than control female S. beldingi to emigrate from the natal area. Competition for food did not appear to influence natal dispersal of females. However, overall population density, density of females weaning litters, and rates of aggression and vigilance among these females, were higher in provisioned than control areas, suggesting that competition for non-food resources was unusually intense in provisioned areas. We propose that juvenile female, but not juvenile male, S. beldingi may emigrate from the natal site to increase access to areas with low densities of conspecifics. Together with findings of earlier workers, our results suggest that spatial and temporal distributions of environmental resources are important influences on the dispersal behavior of female ground squirrels. Received: 28 February 1996 / Accepted after revision: 16 October 1996     

Water column use and forage strategies of female southern elephant seals from Marion Island

The at-sea behaviour of marine top predators provides valuable insights into the distribution of prey species and strategies used by predators to exploit patchily distributed resources. We describe the water column usage and dive strategies of female southern elephant seals from Marion Island tracked between 2004 and 2008. Dives representing increases in forage effort were identified using a method that combines dive type analyses and the calculation of relative amounts of time that animals spend in the bottom phases of dives. Results from this analysis indicate that female elephant seals from Marion Island tend to display lower levels of forage effort closer to the island and display intensive opportunistic forage bouts that occur at a minimum distance of approximately 215 km from the island. Females from Marion Island dived deeper and for longer periods of time, compared to females from other populations. Most animals displayed positive diel vertical migration, evidently foraging pelagically on vertically migrating prey. A few animals displayed periods of reverse (negative) diel vertical migration, however, diving to deeper depths at night, compared to daytime. This behaviour is difficult to explain and prey species targeted during such periods unknown. Our results illustrate plasticity in foraging behaviour of southern elephant seals, as well as inter-population differences in forage strategies.     

Stable isotopes document winter trophic ecology and maternal investment of adult female southern elephant seals (<Emphasis Type="Italic">Mirounga leonina</Emphasis>) breeding at the Kerguelen Islands

Individual specialisation is widespread and can affect a population’s ecological and evolutionary dynamics. Whether intra-specific niche differences can influence reproductive investment was examined in a marine mammal, the southern elephant seal (Mirounga leonina), whose females were known to forage in two different areas during the austral winter. The study was conducted at Kerguelen Islands (49°21′S, 70°18′E), southern Indian Ocean, in late winter–early spring 2006. Pups were used as proxies of their mothers’ biology and combined information on their weaning mass (a proxy of females’ foraging success and short-term fitness) together with their blood δ¹³C value (a proxy of female foraging zone). First, the use of isotopic signature of pups was validated to study the female foraging ecology during their pre-breeding trip by demonstrating that δ¹³C and δ¹⁵N values of pups and their mothers were positively and linearly correlated. Then, blood samples were taken from a large number of newly-weaned pups, which were also weighed, to provide information at the population level. Estimated δ¹³C values of female seals encompassed a large range of values (from −23.7 to −19.1‰) with an unimodal frequency distribution, suggesting no contrasted foraging areas within the population. No significant relationship was found between pup weaning mass and their carbon signature, indicating no link between female foraging areas and maternal foraging success and investment. Finally, blood δ¹³C and δ¹⁵N values gave new insights into southern elephant seal ecology, suggesting that females mainly foraged north of the Polar Front where they preyed upon myctophid fish in late winter.     

Social organization and space-use in Gunnison's prairie dog

Summary Social organization of the Gunnison's prairie dog, Cynomys gunnisoni, was studied in two populations in south-central Colorado. Gunnison's prairie dogs live in complex, interactive societies fitting current definitions of highly social ground squirrels. Members of harems (coteries) cooperatively use and defend a common territory. Spatial overlap is extensive between the adult male(s) and adult females, and among adult females within the harem through the active season. Amicable behavioral interactions are frequent within the harem, whereas interactions between members of different harems are primarily agonistic and spatial overlap is minimal. Although their behavioral repertoire is more limited, social organization of the Gunnison's prairie dog most closely resembles that of the black-tailed prairie dog, C. ludovicianus. Although body size, age of first reproduction, and age of emigration differed between the two study populations (Rayor 1985a), a comparison of social traits did not reveal substantial differences.