Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups : metabolic rates, energy reserve utilization, and water fluxes

Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups: metabolic rates, energy reserve utilization, and water fluxes. Am J Physiol Regul Integr Comp Physiol 297: R1582–R1592, 2009. First published September 23, 2009; doi:10.1152/ajpregu.90857.2008.— Surviving prolonged fasting requires various metabolic adaptations, such as energy and protein sparing, notably when animals are simultaneously engaged in energy-demanding processes such as growth. Due to the intermittent pattern of maternal attendance, subantarctic fur seal pups have to repeatedly endure exceptionally long fasting episodes throughout the 10-mo rearing period while preparing for nutritional independence. Their metabolic responses to natural prolonged fasting (33.4 ± 3.3 days) were investigated at 7 mo of age. Within 4–6 fasting days, pups shifted into a stage of metabolic economy characterized by a minimal rate of body mass loss (0.7%/day) and decreased resting metabolic rate  (5.9 ± 0.1 ml O₂ ·kg^-1·day^-1) that was only 10% above the level predicted for adult terrestrial mammals. Field metabolic rate (289 ± 10 kJ·kg^-1 ·day^-1) and water influx (7.9 ± 0.9 ml·kg^-1 ·day^-1) were also among the lowest reported for any young otariid, suggesting minimized energy allocation to behavioral activity and thermoregulation. Furthermore, lean tissue degradation was dramatically reduced. High initial adiposity (>48%) and predominant reliance on lipid catabolism likely contributed to the exceptional degree of protein sparing attained. Blood chemistry supported these findings and suggested utilization of alternative fuels, such as β-hydroxybutyrate and de novo synthesized glucose from fat-released glycerol. Regardless of sex and body condition, pups tended to adopt a convergent strategy of extreme energy and lean body mass conservation that appears highly adaptive for it allows some tissue growth during the repeated episodes of prolonged fasting they experience throughout their development.

Terrestrial apnoeas and the development of cardiac control in Australian fur seal (Arctocephalus pusillus doriferus) pups

The development of cardiac control in association with terrestrial respiration patterns was examined throughout the period of maternal dependence in Australian fur seal pups. Resting eupnoic heart rate and respiration rate were significantly correlated (r² = 0.49) and both decreased with age (P < 0.05 in both cases). From an early age (1 month), pups displayed terrestrial apnoeas (18.1 ± 0.5 s) accompanied by substantial bradycardia (127 beats min^-1, a 13% decrease from eupnoic HR). Terrestrial apnoea duration increased significantly with age reaching a mean of 41 s just prior to weaning, slightly lower than the mean dive duration (52 s) previously recorded for pups of the same age. Correspondingly, mean apnoic heart rate decreased with age to 74 beats min^-1 just prior to weaning, representing a 25% decrease on eupnoic heart rate. Importantly, concomitant with the decrease in mean apnoic heart rate with age, an increase in the control
of bradycardia was evident with the variability in instantaneous apnoic heart decreasing such that older pups were able to maintain a low steady heart rate for the duration of the apnoea. The changes seen in these parameters are similar to those reported during postnatal development in elephant seals (Mirounga spp.) and harbour seals (Phoca vitulina), and are considered indicative of the development of cardiac control. These findings suggest a common strategy for the development of bradycardia control in both otariid and phocid seals.

Genetic status of an endemic marine mammal, the Australian fur seal, following historical harvesting

Genetic variation, and the way in which it is partitioned among populations, has implications for a species’ survival and evolutionary potential. Such information is particularly important for the successful conservation and management of species that have experienced past human impacts and potential losses of genetic diversity. Overharvesting of the Australian fur seal Arctocephalus pusillus doriferus in the 18th and 19th centuries resulted in severe population reductions and elimination of an estimated 17 of 26 colonies. Currently, the subspecies is recovering and c. 20 000 pups are produced annually at 13 colony sites, most of which are situated in Bass Strait in south-eastern Australia. Genetic analysis of samples collected from pups captured at nine colonies revealed no difference in allelic diversity or heterozygosity at five microsatellite loci and no differences in haplotype diversity within a 344 bp region of the mitochondrial DNA control region. There was some evidence for isolation by distance but the program STRUCTURE predicted a single cluster of individuals. Gene flow among colonies appears to be substantial at present, indicating that the Australian fur seal is currently a single, panmictic unit.

Environmental and senescent related variations in Weddell seal body mass : implications for age-specific reproductive performance

Recent studies have found age-specific variations in reproductive performance amongst Weddell seals, Leptonychotes weddellii, and we hypothesized age-related variations in maternal body mass as a mechanism linking maternal age and the observed patterns of reproductive performance. We evaluated the effects of maternal traits such as age and reproductive experience and the effects of environmental variations on maternal body mass at parturition. Maternal body mass at parturition showed substantial age- and environmental-related variations. Maternal body mass increased with age through the young and middle ages, and evidence of senescent declines in body mass was found amongst the oldest ages. Additionally, body mass at parturition was strongly influenced by environmental variations during the pregnancy period, specifically sea-ice extent and the state of the El-Niño Southern Oscillation. Patterns of age-specific variations in body mass were consistent with age-specific patterns of offspring survival probability, which supported our hypothesis that changes in body mass link maternal age and reproductive performance in the Weddell seal. Further, environmental conditions during pregnancy may be an important component of Weddell seal reproductive performance.

Vocal individuality of in-air Weddell seal (Leptonychotes weddellii) pup "primary" calls

As a result of selective pressures faced during lactation, vocal recognition may play a crucial role in maintaining the phocid mother–pup bond during the period of dependence. To investigate this possibility, we examined whether Weddell seal (Leptonychotes weddellii) pups produce individually distinctive “primary” calls. One temporal, nine fundamental frequency features, and two spectral characteristics were measured. A discriminant function analysis (DFA) of 15 Vestfold Hills pups correctly classified 52% of calls, while the cross-validation procedure classified 29% of calls to the correct pup. A second DFA of 10 known-age McMurdo Sound pups correctly classified 44% of “test” calls. For novel calls, the probabilities of attaining such classification rates by chance are low. The relationship between age and call stereotypy indicated that pups 2 wk and older may be more vocally distinctive. Overall, findings suggest that Weddell seal pup “primary” calls are moderately distinctive and only exhibit sufficient stereotypy to aid maternal recognition by approximately two weeks of age.

The fur seal — a model lactation phenotype to explore molecular factors involved in the initiation of apoptosis at involution

Mammary gland involution requires co-ordination of milk production, immune responses, apoptosis and remodeling. Initiation and progression of each of these components involves integral control by the mammary gland. Although cell-based culture models and genetically manipulated animals have shed light on these processes, the factors controlling each step in the involution cascade are still poorly understood. The fur seal displays a unique lactation phenotype. During the lactation cycle the mammary gland downregulates milk production and initiates an immune response but fails to initiate the apoptotic phase of involution, allowing the female fur seal to undertake long foraging trips of up to 28 days between suckling bouts. Upon return to shore the female continues feeding her pup following resumption of lactation and milk production. Expression profiling of genes involved in this lactation cycle provides valuable tools for investigation of the factors responsible for the initiation of apoptosis at involution.

Changes in muscle composition during the development of diving ability in the Australian fur seal

During development the Australian fur seal transitions from a terrestrial, maternally dependent pup to an adult marine predator. Adult seals have adaptations that allow them to voluntarily dive at depth for long periods, including increased bradycardic control, increased myoglobin levels and haematocrit. To establish whether the profile of skeletal muscle also changes in line with the development of diving ability, biopsy samples were collected from the trapezius muscle of pups, juveniles and adults. The proportions of different fibre types and their oxidative capacity were determined. Only oxidative fibre types (Type I and IIa) were identified, with a significant change in proportions from pup to adult. There was no change in oxidative capacity of Type I and IIa fibres between pups and juveniles but there was a two-fold increase between juveniles and adults. Myoglobin expression increased between pups and juveniles, suggesting improved oxygen delivery, but with no increase in oxidative capacity, oxygen utilisation within the muscle may still be limited. Adult muscle had the highest oxidative capacity, suggesting that fibres are able to effectively utilise available oxygen during prolonged dives. Elevated levels of total creatine in the muscles of juveniles may act as an energy buffer when fibres are transitioning from a fast to slow fibre type.

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 (T4) 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 (T3); and moderately increased T4. 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.