Intraspecific allometry of neonatal size in the antarctic fur seal (Arctocephalus galapagoensis)

Summary Intraspecific allometry of pup mass as a function of maternal mass was analysed in Antarctic fur seals (Arctocephalus gazella), a highly dimorphic species. The allometric exponent was 0.6, much lower than in interspecific comparisons. Slopes were the same for mother-son pairs as for mother-daughter pairs, but adjusted means were significantly higher for the former, indicating higher reproductive effort of mothers of sons. The correlation of maternal mass with pup mass explained 59% of the variance in female pup mas but only 18% of that in male pup mass. Females appeared to produce sons which were as big as possible. Relative pup mass decreased with increasing maternal mass indicating a lower reproductive effort of bigger and presumably older mothers, contrary to expectations from life history theory. Sex ratio of pups showed no relation to maternal mass.     

High male reproductive success in a low-density Antarctic fur seal (Arctocephalus gazella) breeding colony

Understanding how population density influences mating systems may lead to important insights into the plasticity of breeding behavior, but few natural systems allow for such studies. Antarctic fur seals (Arctocephalus gazella) provide an interesting model system because they breed in colonies of varying densities. Previous studies have largely focused on a high-density site at Bird Island, South Georgia. Here, 13 highly polymorphic microsatellite loci were used to conduct a genetic analysis of a low-density breeding colony of this species at Livingston Island, approximately 1,600 km south of South Georgia. The majority of adults seen ashore (n?=?54) were sampled together with every pup born (n?=?97) over four consecutive years. Paternities were confidently assigned for 34 out of the 97 pups. Two out of 23 sampled males accounted for the paternity of 28 % of all pups sampled during the study and 82 % of the pups with an assigned father. Moreover, a full likelihood pedigree inference method assigned a further eight paternities to a single unsampled male seal that is inferred to have held a territory during the season before the study began. The most successful males in our study easily surpassed the previous record for the total number of pups sired per male seal for the species. Furthermore, we identified two triads of full siblings implying that their parents remated in three consecutive years. These findings suggest that territorial male fur seals may achieve greater success in monopolizing access to breeding females when population density is relatively low.     

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     

Sex differences in mass loss rate and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island

We investigated the relationship between the mass gained by a pup during a period of maternal attendance (as an index of milk intake) and the duration of the preceding foraging trip in relation to the mass-specific rate of mass loss during fasting periods and the growth rate of Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island. We found that (1) serially weighed male pups grew significantly faster than females pups and that (2) fasting female pups lost mass at a significantly higher rate (2.55% day⁻¹) than male pups (2.12% day⁻¹) of the same mass; (3) during periods of maternal attendance, there were no intersexual differences in the amount of mass gained by pups of the same size, hence (4) female pups required a higher daily mass gain to grow at the same rate as male pups. Our results show that intersexual differences in growth rate may be accounted for by intersexual differences in mass-specific rate of mass loss, because females lost 0.42% more of their total mass per day (i.e. 4.2 g kg⁻¹ day⁻¹) compared with male pups of the same body mass. Despite intersexual differences in growth rates, our results indicate equality of maternal expenditure between the sexes. Intersexual differences in the rate of mass loss may be due to differences in the metabolic rate, activity level and/or body composition of male and female pups. Received: 19 August 1998 / Received in revised form: 19 April 1999 / Accepted: 19 April 1999     

Mitochondrial DNA sequence data of the Cape fur seal (Arctocephalus pusillus pusillus) suggest that population numbers may be affected by climatic shifts

The Cape fur seal, Arctocephalus pusillus pusillus is distributed along the southern African coastline from northern Namibia to the south-east coast of South Africa. The species has been impacted by sealing operations since the 1600s, and historical records suggest that the taxon experienced a bottleneck prior to the 20th century. Mitochondrial DNA control region sequences were generated for 106 individuals belonging to six breeding colonies. Haplotype diversity was found to be high (0.975±0.014) whereas levels of nucleotide diversity were much lower compared to other seal species (0.011±0.006). An analysis of molecular variance indicated that the largest percentage of haplotype diversity is distributed within colonies rather than among them. This could be attributed to either extensive gene flow among colonies, a lack of substantial female site philopatry, or incomplete lineage sorting of haplotypes. Mismatch distribution and Fu’s F _S test indicated that the population has experienced a historical population expansion probably between c. 37,000–18,000 YBP and this date coincides very well with the height of the last glacial maximum when food resources were abundant in the South Atlantic. These results also suggest that the recent sealing-induced bottleneck did not have a profound influence on the haplotype diversity and a historical bottleneck prior to a demographic expansion may have been severe enough to reduce nucleotide diversity substantially.     

An energy–distance trade-off in a central-place forager,the Antarctic fur seal (<Emphasis Type="Italic">Arctocephalus gazella</Emphasis>)

We tested the prediction that lactating fur seals (Arctocephalus gazella) at South Georgia will take prey of greater energy density with increasing distance of foraging from the colony. The study investigated the differences in diet of fur seals foraging within two regions, one near the breeding colony and the other at greater distance. Diet varied significantly in relation to foraging location. Dietary items of low quality were eaten in both regions but more food items with a high-energy content appeared in the diet of seals travelling to distant oceanic waters. We conclude that there is likely to be a trade-off between energy gain and distance travelled which enables female fur seals to maintain a relatively constant rate of energy delivery to their offspring irrespective of the distance travelled to find food.     

Spatial and temporal variation in the diet of a high trophic level predator,the Australian fur seal (<Emphasis Type="Italic">Arctocephalus pusillus doriferus</Emphasis>)

This study quantifies the manner in which Australian fur seals, Arctocephalus pusillus doriferus, use their prey in a spatial and temporal context. We analysed 977 scat and 66 regurgitate samples collected from Tasmanian breeding colonies and haul-outs between 1994 and 2000. Diagnostic prey remains identified in the scats represented 35 fish taxa and 8 cephalopod taxa. The main taxa identified in scats, where frequency of occurrence was 10%, were leatherjacket species (family Monocanthidae), redbait (Emmelichthys nitidus), barracouta (Thyrsites atun), jack mackerel (Trachurus declivis) and red cod (Pseudophysis bachus). Regurgitates were dominated by cephalopods, primarily Goulds squid (Nototodarus gouldi), Octopus maorum, O. berrima/pallidus and Sepia apama. Discriminant function analyses indicated that there were generally no significant differences in the composition of the diet between colonies within a year, suggesting that prey distribution is fairly uniform throughout Bass Strait at those time scales. The diet at breeding colonies, however, exhibited significant inter- and intra-annual variation, determined by the presence of several key taxa, such as barracouta and a species of scorpionfish (family Scorpaenidae). The diet composition also varied regionally, between Bass Strait and southern Tasmania in spring 1999 and autumn 2000, with redbait, barracouta and a species of scorpionfish identified as the main taxa contributing to this difference. Redbait occurred in the diet only in southern Tasmania, whereas barracouta and scorpionfish occurred only in Bass Strait.Electronic Supplementary Material Supplementary material is available in the online version of this article at http://dx.doi.org/10.1007/s00227-003-1219-0.Communicated by G.F. Humphrey, Sydney     

Pre-natal investment in reproduction by female Antarctic fur seals

Summary Maternal investment, in terms of pup birth mass, in gestation by Antarctic fur seals (Arctocephalus gazella) was related to the date of birth in two consecutive years. There were significant differences in birth mass between years and between the sexes within years. Birth mass was used to calculate the mean energetic cost of producing a pup to parturition. The cost for a male pup in 1986 was 173 MJ while it was 191 MJ in 1987. For female pups the cost was 152 and 166 MJ in 1986 and 1987 respectively. Given the probable pattern of foetal growth, this constitutes a minimum of 5–15% of the maternal energy budget in the final months of gestation. Birth mass varied inversely with date of birth, but more strongly for male than for female pups. The sex ratio at birth was unity in both years and this did not vary with time through the birth season. In a subsample of mothers (n=79) which were captured on the day of birth, there was a decline in the body mass and standard length with date of birth. Male birth mass was directly related to maternal mass and maternal condition (mass/length) but there was no significant relationship for females. These results suggest that the growth of male foetuses is limited by maternal resources while female foetuses do not exploit fully maternal resources.     

Maternal investment, sex-differential prospects, and the sex ratio in wild house mice

In a population of first-generation offspring from wild-caught house mice (Mus musculus domesticus), previous evidence suggested that male fitness is more strongly affected by an increase in body weight than female fitness. This paper shows that in these mice the young are weaned at heavier weights the smaller the litter and the better the maternal body condition. These effects persisted into adulthood and were less pronounced in female young. However, contrary to expectation from conventional sex ratio theory, maternal condition and litter size had no detectable effect on sex ratios. Also, litter size did not affect sex ratios in two populations of laboratory-kept, wild-caught western (M. m. domesticus) and eastern house mice (M. m. musculus). Wild house mice, therefore, appear not to adaptively manipulate the sex ratio of offspring. It is argued that this absence of sex ratio trends might not be maladaptive, but rather that models currently used to predict sex ratio trends in rodents may not be valid. Received: 13 March 1997 / Accepted after revision: 9 August 1997     

Maternal investment in mountain baboons and the hypothesis of reduced care

It has been argued that female mammals should terminate expensive forms of infant care earlier as habitat quality declines. More recently it has been shown that among a variety of mammalian species, early termination of care is also associated with highly favourable conditions. In this paper we present data on maternal investment decisions among baboons (Papio cynocephalus ursinus) inhabiting the Drakensberg Mountains of South Africa, and compare these with data from East African baboon studies. Mothers in the mountain habitat face a set of environmental conditions where the problem of resource allocation to offspring is expected to be particularly acute. We begin by using the model of Altmann (1980) of maternal time budgets to demonstrate that mountain baboon mothers experience greater perturbations to their activity budgets while suckling than do mothers in other populations. They also provide consistently greater levels of care to their infants and do so in the absence of any form of overt conflict over access to the nipple. Although this investment results in a relative lengthening of the interbirth interval (IBI), it is accompanied by relatively higher infant survival. We argue that factors that influence the maternal strategy adopted by mountain baboons include slow infant growth rates and a lack of predation in the habitat which influences probability of offspring survival beyond the immediate postnatal period. We suggest that both “care-dependent” sources of mortality (e.g. female reproductive condition, the amount of milk transferred to offspring) as well as “care independent” sources of mortality (e.g. predation, infectious disease) should be considered in studies of parental investment. Received: 26 May 1997 / Accepted after revision: 9 August 1997     

Male-biased sex ratios in New Zealand fur seal pups relative to environmental variation

A number of models have been proposed to provide adaptive explanations of sex-ratio variation in mammals. Two models have been applied commonly to primates and ungulates with varying success—the Trivers-Willard (TW) hypothesis, and the local resource competition (LRC) hypothesis. For polygynous, sexually dimorphic mammals, where males are larger and disperse more readily, these models predict opposite outcomes of sex-ratio adjustment within the same environmental context (high-resource years: TW—more sons; LRC—more daughters). However, many of the predictions of these two models can vary depending on factors influencing resource availability, such as environmental stochasticity, resource predictability, and population density. The New Zealand fur seal (Arctocephalus forsteri) is a polygynous mammal showing marked sexual dimorphism (larger males), with higher variation in male reproductive success expected. We provide clear evidence of male-biased sex ratios from a large sample of A. forsteri pups captured around South Island, New Zealand during 1996/1998, even after accounting for a sex bias in capture probability. The extent of the bias depended upon year and, in 1998, strong climatic perturbations (El Niño/Southern Oscillation, ENSO) probably reduced food availability. Significant male-biased sex ratios were found in all years; however, there was a significant decline in the male bias in 1998. There was no relationship between sex ratio and population density. We suggest that the sex-ratio bias resulted from the production of relatively more male pups. Under the density-independent scenario, the strong male bias in A. forsteri sex ratios is support for the TW model within an environment of high resource predictability. We suggest that some plasticity in the determination of pup sex among years is a mechanism by which A. forsteri females in New Zealand, and perhaps other otariid seals, can maximise fitness benefits when living in regions of high, yet apparently predictable, environmental variability. We also suggest that much of the inconsistency in the reported sex ratios for otariid seals results from the complex interaction of population density and environmental stochasticity influencing relative food availability over time.     

Maternal investment and sex ratio adjustment in American bison calves

Summary Cow-calf behavior was observed in American bison (Bison bison) to determine if mothers invested differentially in sons and daughters. Cows nursed sons significantly longer than they did daughters in their first three months of life. The increased nursing time for sons was not compensated for by increased grazing time by their mothers. Grazing and activity patterns did not differ significantly between sons and daughters. Cows that had sons bred later in the breeding season than nulliparous cows, barren cows, or cows with daughters. Nine yearling sons compared to only two yearling daughters continued to suckle from their mothers for up to 15 months of age. Cows that had sons the previous year were more apt to be barren in the current year than cows that had daughters in the previous year.     

Maternal investment in sons and daughters: problems of methodology

Summary The prediction that mothers should invest more in sons than daughters was briefly examined in American bison (Bison bison) by Wolff (1988). He concluded that (a) male calves suckle more than females, (b) cows that had previously produced sons were more likely to be barren, and (c) cows that had male calves became estrous later in the year than other cows. In this paper we present data from two long term studies at different sites to show that Wolff's conclusions are equivocal at best and difficult to reconcile with predictions of the hypothesis because of questionable methods and assumptions. Offprint requests to: W.C.H. Green     

Ontogeny of early diving and foraging behavior of northern fur seal (Callorhinus ursinus) pups from Bering Island,Russia

The ontogeny of diving and foraging behavior of northern fur seal pups from a stable population on Bering Island, Russia, was recorded with animal-borne instruments during their first few months at sea, a critical period during their first year at sea. Thirty-five pups were instrumented with satellite-linked time-depth recorders and stomach temperature pills. Diving occurred predominantly at night with deeper and longer dives as the pups matured. Mean dive depths were correlated with lunar illumination, whereas mean dive durations were also correlated with time of day and sex. Foraging success did not differ between sexes, and there was no relationship between meal size (as indicated by feeding event duration and minimum stomach temperature) and lunar illumination fraction or maximum foraging depth. Although most pups were able to successfully forage within 3 days of starting their migration, the number of feeding events recorded each day remained low (mean 1.6 events day^?1). There was no indication of an appreciable increase in meal size after the first 2 weeks of the migration despite an increase in dive frequency and depth. The results are consistent with observations that pups do not gain mass during their first year and emphasize the risk of starvation from infrequent foraging in cold water.     

A Bayesian hierarchical model of Antarctic fur seal foraging and pup growth related to sea ice and prey abundance

We created a Bayesian hierarchical model (BHM) to investigate ecosystem relationships between the physical ecosystem (sea ice extent), a prey measure (krill density), predator behaviors (diving and foraging effort of female Antarctic fur seals, Arctocephalus gazella, with pups) and predator characteristics (mass of maternal fur seals and pups). We collected data on Antarctic fur seals from 1987/1988 to 1994/1995 at Seal Island, Antarctica. The BHM allowed us to link together predators and prey into a model that uses all the data efficiently and accounts for major sources of uncertainty. Based on the literature, we made hypotheses about the relationships in the model, which we compared with the model outcome after fitting the BHM. For each BHM parameter, we calculated the mean of the posterior density and the 95% credible interval. Our model confirmed others' findings that increased sea ice was related to increased krill density. Higher krill density led to reduced dive intensity of maternal fur seals, as measured by dive depth and duration, and to less time spent foraging by maternal fur seals. Heavier maternal fur seals and lower maternal foraging effort resulted in heavier pups at 22 d. No relationship was found between krill density and maternal mass, or between maternal mass and foraging effort on pup growth rates between 22 and 85 days of age. Maternal mass may have reflected environmental conditions prior to the pup provisioning season, rather than summer prey densities. Maternal mass and foraging effort were not related to pup growth rates between 22 and 85 d, possibly indicating that food was not limiting, food sources other than krill were being used, or differences occurred before pups reached age 22 d.     

Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki

Sea lions are generally considered opportunistic feeders. However, studies from different areas suggest their diet consists mostly of four to five types of prey. Previous studies in Galapagos sea lions have identified at least three feeding strategies for this species, suggesting diversification of their diet. Diet diversification is favored in organisms with relatively high trophic position and subject to high intra-specific and low inter-specific competition. Zalophus wollebaeki meet these criteria as the only pinniped on San Cristobal Island, where three sea lion rookeries are located within 11 km: a distance considerably shorter than their 41 km foraging range. To measure the degree of diet diversification, we used scats and stable isotope analyses. A total of 270 scat samples from lactating females and 142 fur samples from sea lion pups were collected during the breeding season 2006. The scat analysis identified distinct diets among rookeries, with minimal trophic overlap (Cλ = 0.19), a trophic level TL = 4.5 (secondary–tertiary carnivore), and trophic breadth of a specialist predator (B _i  = 0.37). The mean δ¹⁵N and δ¹³C values were 13.07 ± 0.52 and −16.34 ± 0.37, respectively. No significant difference was found in the δ¹⁵N values from the sea lion rookeries, but differences were found inter- and intra-population in δ¹³C values for pups from different groups (ANOVA P < 0.05). Our results indicate that diet diversification is present in the Galapagos sea lion and may play important role to the survival of the species in a habitat where pinniped populations are limited.     

Evidence of equal maternal investment in the sexes in the polygynous and sexually dimorphic grey seal (Halichoerus grypus)

In polygynous and sexually dimorphic mammals, parents may be expected to bias their investment towards sons because variation in reproductive success is usually higher among males than among females. Moreover, male reproductive success often depends on adult body size, which, in turn, may depend on the level of parental investment. We therefore predicted that in the grey seal (Halichoerus grypus), a polygynous and sexually dimorphic phocid seal, females should invest more in individual sons than in individual daughters. We found that male pups were born heavier than female pups, but that the growth rates and suckling behaviour were similar for the two sexes. The growth rates and the birth weights were not correlated for the pups of either sex. Mothers did not behave differentially towards offspring of the two sexes, except that mothers of male pups spent more time in visual contact with their pups. Male and female pups had similar activity levels and begged at similar rates. We argue that reports of equal expenditure on the two sexes can be accepted as evidence of equal investment, provided that three assumptions are fulfilled. First, parental care must be costly to the parent. Second, energy expenditure must be the most important component of parental investment. Third, there must be no negative correlation between maternal body condition and the ratio of sons to daughters produced. We argue that these assumptions are met in our study, and that our results provide evidence of equal maternal investment in the sexes in grey seals.     

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness. Received: 23 July 1999 / Received in revised form: 23 February 2000 / Accepted: 13 March 2000