Olfactory discrimination ability of South African fur seals (Arctocephalus pusillus) for enantiomers

Using a food-rewarded two-choice instrumental conditioning paradigm we assessed the ability of South African fur seals, Arctocephalus pusillus, to discriminate between 12 enantiomeric odor pairs. The results demonstrate that the fur seals as a group were able to discriminate between the optical isomers of carvone, dihydrocarvone, dihydrocarveol, menthol, limonene oxide, α-pinene, fenchone (all p < 0.01), and β-citronellol (p < 0.05), whereas they failed to distinguish between the (+)- and (?)-forms of limonene, isopulegol, rose oxide, and camphor (all p > 0.05). An analysis of odor structure–activity relationships suggests that a combination of molecular structural properties rather than a single molecular feature may be responsible for the discriminability of enantiomeric odor pairs. A comparison between the discrimination performance of the fur seals and that of other species tested previously on the same set of enantiomers (or subsets thereof) suggests that the olfactory discrimination capabilities of this marine mammal are surprisingly well developed and not generally inferior to that of terrestrial mammals such as human subjects and non-human primates. Further, comparisons suggest that neither the relative nor the absolute size of the olfactory bulbs appear to be reliable predictors of between-species differences in olfactory discrimination capabilities. Taken together, the results of the present study support the notion that the sense of smell may play an important and hitherto underestimated role in regulating the behavior of fur seals.     

The composition of Australian fur seal (Arctocephalus pusillus doriferus) milk throughout lactation.

The proximate chemical composition of milk was determined throughout lactation in the Australian fur seal (Arctocephalus pusillus doriferus Wood Jones), a temperate species with an 11-mo lactation period typical of most temperate otariids. Average lipid and protein contents were 42% and 10%, respectively, which is similar to that recorded for the polar otariid species but higher than reported in other temperate, long-lactation species. Milk composition, however, varied substantially throughout lactation, with lipid content rising from 30% soon after parturition to 50% at 230 d postpartum before decreasing to 45% toward weaning. The trend in water content was opposite to that of lipid, while protein content increased only slightly during lactation from 10% to 12%. The peak in lipid content occurred at approximately 70% of the way through lactation, similar to that found in the Australian sea lion and several phocid seal species. Significant positive relationships were found between milk lipid content and both the duration of the preceding foraging trip and body mass. A highly significant and close correlation was found between milk water and lipid contents such that gross energy content may be accurately predicted from water content alone. Similar predictive equations have been found for several other otariid and phocid species, but these appear to differ between phylogenetic groups.     

The diet of the subantarctic fur seal Arctocephalus tropicalis at Marion Island

Scats of subantarctic fur seals Arctocephalus tropicalis at Marion Island were collected from 1996 to 2,000, to examine temporal variability in the diet, factors affecting the variability and how the diet differed from that of the Antarctic fur seal A. gazella in the same period. For A. tropicalis, 19 prey species, of which 18 were fish and one a cephalopod, were identified in 213 scats. Fish were the main prey, occurring in 98.1 % of scats, whereas the cephalopod was present in only 1.4 % of scats. Amongst fish species, Myctophidae were most abundant, with Gymnoscopelus piabilis, G. fraseri and Electrona carlsbergi being the commonest prey items. Other fish families present in the diet in small numbers were Channichthyidae, Paralepididae, Nototheniidae, Microstomatidae and Notosudidae. Fish eaten ranged in size from Protomyctophum bolini and Krefftichthys anderssoni of standard length (SL) 25 mm to a single Dissostichus eleginoides of SL 249 mm. Differences in the diet existed between summer and winter. However, prey type accounted for most variability in the diet. In previous studies based on scats, a dominance of fish in the diet of A. tropicalis was also found at Possession Island (Iles Crozet), Amsterdam Island and Macquarie Island, but the dominant prey species differed between the various localities, also suggesting that prey availability is a major determinant of diet. At Marion Island, from 1996 to 2000 the diet of A. gazella comprised similar prey to that of A. tropicalis, but the proportional contribution of prey types differed in instances.     

Killing of Cape fur seal (Arctocephalus pusillus pusillus) pups by brown hyenas (Parahyaena brunnea) at mainland breeding colonies along the coastal Namib Desert

Brown hyenas (Parahyaena brunnea) scavenge and kill seal pups at mainland Cape fur seal (Arctocephalus pusillus pusillus) colonies. The prey encounter interval and interval between kills depended on seal density, and increased density resulted in an increase of the capture rate and increase in hunting efficiency from 14% in November to 47% in January. The time brown hyenas spent at the seal colony decreased with increasing seal density and increasing air temperatures. Nevertheless, they were regularly active during the day when less adult seals were present at the colony, which indicates that the attendance of adult seals might play a role in the choice of foraging time. Brown hyenas killed seal pups throughout the study period. The predation rate was independent of the availability of non-violent mortalities, but the absolute number of kills was positively density-dependent. Mass kill events were recorded throughout the study period and are therefore not unusual occurrences. The overabundance of easy and vulnerable prey may lead to an over stimulus situation that triggers killing independent of the consumption of the prey or the hunger state.     

Fasting metabolism in Antarctic fur seal (Arctocephalus gazella) pups.

The metabolism of 52-73-day old Antarctic fur seal pups from Bird Island, South Georgia, was investigated during fasting periods of normal duration while their mothers were at sea foraging. Body mass decreased exponentially with pups losing 3.5-3.8% of body mass per day. Resting metabolic rate also decreased exponentially from 172-197 ml (O2) x min(-1) at the beginning of the fast and scaled to M(b)(0.74) at 2.3 times the level predicted for adult terrestrial mammals of similar size. While there was no significant sex difference in RMR, female pups had significantly higher (F(1,18)=6.614, P<0.019) mass-specific RMR than male pups throughout the fasting period. Fasting FMR was also significantly (t(15)=2.37, P<0.035) greater in females (823 kJ x kg(-1) x d(-1)) than males (686 kJ x kg(-1) x d(-1)). Average protein turnover during the study period was 19.3 g x d(-1) and contributed to 5.4% of total energy expenditure, indicating the adoption of a protein-sparing strategy with a reliance on primarily lipid catabolism for metabolic energy. This is supported by observed decreases in plasma BUN, U/C, glucose and triglyceride concentrations, and an increase in beta-HBA concentration, indicating that Antarctic fur seals pups adopt this strategy within 2-3 days of fasting. Mean RQ also decreased from 0.77 to 0.72 within 3 days of fasting, further supporting a rapid commencement of protein-sparing. However, RQ gradually increased thereafter to 0.77, suggesting a resumption of protein catabolism which was not substantiated by changes in plasma metabolites. Female pups had higher TBL (%) than males for any given mass, which is consistent with previous findings in this and other fur seal species, and suggests sex differences in metabolic fuel use. The observed changes in plasma metabolites and protein turnover, however, do not support this.     

Density-dependent pup mortality in the Antarctic fur seal Arctocephalus gazellu at South Georgia

The extent and causes of pup mortality in the Antarctic fur seal, Arctocephalus gazella , were investigated at sites of high and low density at South Georgia. Mortality was greater at the high density site, (17—31% of annual pup production) than at the low density site (36%). The main causes of death, starvation and skull injury, occur more frequently at the high density site. Most starvation was caused by failure of the mother-pup bond to form, often caused by disturbance induced by the activities of breeding bulls. In some seasons starvation of older pups may be influenced by reduced food availability but this was usually of minor importance. Injury to the skull resulted from bites inflicted by females either accidently during birth or when pups tried to suck from females other than their mother. Trampling of young pups by bulls was probably responsible for the appreciable incidence of ruptured livers. Infectious disease and drowning played minor roles in pup mortality. Pups born late in the season suffered disproportionately greater mortality which may relate to female age and condition. Food availability (both during and prior to the breeding season) and weather are likely to account for year to year variation in pup mortality rates but the basic rate is primarily determined by breeding density. Further population increase and colonization of new beaches is expected until food resources during the summer, or more probably the winter, become limiting.     

Distribution of post-weaning Antarctic fur seal Arctocephalus gazella pups at South Georgia

Potentially some of the biggest gaps in our knowledge about the ecology of Antarctic fur seals (Arctocephalus gazella) relate to juvenile animals. We investigated the at-sea distribution of five male and five female fur seal pups post-weaning. The study was carried out at Bird Island, South Georgia during two successive winters using satellite-linked platform transmitter terminals (PTTs). Our results are analysed in relation to pup sex and the physical environment and productivity of those 2 years, as well as in the context of our present knowledge of where post-breeding females and males forage. The available physical and biological data during both of the winters of this study suggest that both years were not unusual. We report marked differences between the sexes with male pups foraging significantly further away from land and their birth site than do females. The pups foraged in areas to the East of Bird Island seldom reported as foraging areas for the adult population. Also as winter progressed they showed a more oceanic distribution leaving the continental shelf, possibly to exploit a different prey source that was more readily available in the upper water column.     

Growth rates of Antarctic fur seal Arctocephalus gazella pups at South Georgia

Large numbers of pups of the Antarctic fur seal were weighed at regular intervals through their rearing period in six seasons between 1972 and 1981 at South Georgia. Growth rates and birth and weaning weights were estimated from linear regressions of mean weight on mean age. Female pups had significantly lower growth rates and weaning weights than males, but higher variances for all growth parameters. This may reflect the importance to males of polygynous species of attaining high body weight. Except for an inverse relation between growth rate and birth weight there were no systematic relationships between growth parameters. Seasonal differences in growth rates were substantial and there was no indication that the continuing rapid population increase was affecting pup growth rates. The use of these data in detecting seasonal variations in local food availability is discussed. Preliminary estimates of the energy costs of pup rearing indicate that pup existence metabolism consumes c. 80% and mass gain to weaning only c. 15% of the energy provided by the female.     

Reproduction in the male sub-Antarctic fur seal Arctocephalus tropicalis

The reproductive tracts of male sub-Antarctic fur seals Arctocephalus tropicalis ( n = 123), taken at Gough Island (40° 20'S, 9° 54'W) between November 1977 and October 1978, were examined. The presence of spermatozoa in the epididymal tubules showed that all males ≥4 years old had reached puberty, and the marked slower increase in mean testis weight and baculum length suggested that sexual (social) maturity was approached by 8-year-olds. Full adulthood was attained at 10–11 years of age based on the peak in mean testis and prostate weights, and mean baculum length. Secondary sexual characteristics were only fully developed in males ≥9 years old. A significant decline in mean testosterone concentration, and in testis, epididymis and prostate weights showed that adult males were reproductively quiescent during winter from May to July when seminiferous and epididymal tubules had lowest mean diameters with no spermatozoa present. Both the mean plasma testosterone concentration and mean testis weight peaked twice during the austral summer. The first peak coincided with the breeding season, and the second peak with the moulting period when adult males were impotent. Photoperiodic cueing might explain this seasonal trend.     

Hormonal responses to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups

Surviving prolonged fasting implies closely regulated alterations in fuel provisioning to meet metabolic requirements, while preserving homeostasis. Little is known, however, of the endocrine regulations governing such metabolic adaptations in naturally fasting free-ranging animals. The hormonal responses to natural prolonged fasting and how they correlate to the metabolic adaptations observed, were investigated in subantarctic fur seal (Arctocephalus tropicalis) pups, which, because of the intermittent pattern of maternal attendance, repeatedly endure exceptionally long fasting episodes throughout their development (1-3 mo). Phase I fasting was characterized by a dramatic decrease in plasma insulin, glucagon, leptin, and total l-thyroxine (T(4)) associated with reductions in mass-specific resting metabolic rate (RMR), plasma triglycerides, glycerol, and urea-to-creatine ratio, while nonesterified fatty acids (NEFA) and β-OHB increased. In contrast, the metabolic steady-state of phase II fasting reached within 6 days was associated with minimal concentrations of insulin, glucagon, and leptin; unchanged cortisol and triiodothyronine (T(3)); and moderately increased T(4). The early fall in insulin and leptin may mediate the shift to the strategy of energy conservation, protein sparing, and primary reliance on body lipids observed in response to the cessation of feeding. In contrast to the typical mammalian starvation response, nonelevated cortisol and minimal glucagon levels may contribute to body protein preservation and downregulation of catabolic pathways, in general. Furthermore, thyroid hormones may be involved in a process of energy conservation, independent of pups' nutritional state. These original hormonal settings might reflect an adaptation to the otariid repeated fasting pattern and emphasize the crucial importance of a tight physiological control over metabolism to survive extreme energetic constraints.     

Factors affecting early mortality in the South American fur seal (Arctocephalus australis) in Peru: density-related effects and predation

Early mortality in the South American fur seal ( Arctocephatus australis ) in Peru is considerably higher than that seen in any other population of fur seal; 31–49% in the first month as opposed to a maximum of 20% in other populations. In 1987 and 1988, pup mortality was found to be enhanced by density-related effects and predation on pups by the southern sea-lion ( Olaria byronia ). At a high density beach, where 60% of the fur seals bred, mortality correlated with the number of females ashore as did aggression. Female aggression was driven to high levels by a combination of high density and movement within the colony to thermoregulate. However, even at a low density, beach mortality remained high due to a high level of predation by male southern sea-lions (low density beach 5·0–8·3% of all pups; high density beach 0·2%). Predation rates were lower at the high density beach because male fur seals expelled most attacking sea-lions during the breeding season (low density beach 10·0% of attacking sea-lions expelled; high density beach 58·8%).     

Species-specific cell-matrix interactions are essential for differentiation of alveoli like structures and milk gene expression in primary mammary cells of the Cape fur seal (Arctocephalus pusillus pusillus).

Few models are in place for analysis of extreme lactation patterns such as that of the fur seals which are capable of extended down regulation of milk production in the absence of involution. During a 10-12 month lactation period, female fur seals suckle pups on shore for 2-3 days, and then undertake long foraging trips at sea for up to 28 days, resulting in the longest intersuckling bouts recorded. During this time the mammary gland down regulates milk production. We have induced Cape fur seal (Arctocephalus pusillus pusillus) mammary cells in vitro to form mammospheres up to 900 microm in diameter, larger than any of their mammalian counterparts. Mammosphere lumens were shown to form via apoptosis and cells comprising the cellular boundary stained vimentin positive. The Cape fur seal GAPDH gene was cloned and used in RT-PCR as a normalization tool to examine comparative expression of milk protein genes (alphaS2-casein, beta-lactoglobulin and lysozyme C) which were prolactin responsive. Cape fur seal mammary cells were found to be unique; they did not require Matrigel for rapid mammosphere formation and instead deposited their own matrix within 2 days of culture. When grown on Matrigel, cells exhibited branching/stellate morphogenesis highlighting the species-specific nature of cell-matrix interactions during morphological differentiation. Matrix produced in vitro by cells did not support formation of human breast cancer cell line, PMC42 mammospheres. This novel model system will help define the molecular pathways controlling the regulation of milk protein expression and species specific requirements of the extracellular matrix in the cape fur seal.     

Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi)

Population bottlenecks may lead to diminished genetic variability and correlative effects on fitness. The Guadalupe fur seal was nearly exterminated by commercial sealers during the late 18th and early 19th centuries. To determine the genetic consequences of this population bottleneck, we compared the variation at a 181 bp section of the mitochondrial DNA (mtDNA) control region from the bones of 26 prebottleneck fur seals versus variation in the extant population. We found 25 different mtDNA genotypes in the prebottleneck fur seals and only 7 genotypes among 32 extant fur seals, including only one of the ancient genotypes. These data demonstrate a substantial loss of genetic variability correlating with the recent population bottleneck. We also found from several genetic measures that the prehistoric population of Guadalupe fur seals was robust and that it had been increasing at some time during the late prehistoric period. Continued recovery of this species may, however, owe more to more immediate nongenetic factors, such as poaching and local availability of food resources during the breeding season and consequent effects on pup survival, than on the reduced genetic variability.