The comparative energetics and growth strategies of sympatric Antarctic and subantarctic fur seal pups at Iles Crozet

The period of maternal dependence is a time during which mammalian infants must optimise both their growth and the development of behavioural skills in order to successfully meet the demands of independent living. The rate and duration of maternal provisioning, post-weaning food availability and climatic conditions are all factors likely to influence the growth strategies of infants. While numerous studies have documented differences in growth strategies at high taxonomic levels, few have investigated those of closely related species inhabiting similar environments. The present study examined the body composition, metabolism and indices of physiological development in pups of Antarctic fur seals (Arctocephalus gazella) and subantarctic fur seals (Arctocephalus tropicalis), congeneric species with different weaning ages (4 months and 10 months, respectively), during their overlap in lactation at a sympatric breeding site in the Iles Crozet. Body lipid reserves in pre-moult pups were significantly greater (t₂₈=2.73, P<0.01) in subantarctic (26%) than Antarctic fur seals (22%). Antarctic fur seal pups, however, had significantly higher (t₂₆=3.82, P<0.001) in-air resting metabolic rates (RMR; 17.1±0.6 ml O₂ kg^-1 min^-1) than subantarctic fur seal pups (14.1±0.5 ml O2 kg^-1 min^-1). While in-water standard metabolic rate (SMR; 22.9±2.5 ml O2 kg^-1 min^-1) was greater than in-air RMR for Antarctic fur seal pups (t₉=2.59, P<0.03), there were no significant differences between in-air RMR and in-water SMR for subantarctic fur seal pups (t₁₂=0.82, P>0.4), although this is unlikely to reflect a greater ability for pre-moult pups of the latter species to thermoregulate in water. Pup daily energy expenditure was also significantly greater (t₂₇=2.36, P<0.03) in Antarctic fur seals (638±33 kJ kg^-1 day^-1) than in subantarctic fur seals (533±33 kJ kg^-1 day^-1), which corroborates observations that pups of the former species spend considerably more time actively learning to swim and dive. Consistent with this observation is the finding that blood oxygen storage capacity was significantly greater (t₉=2.81, P<0.03) in Antarctic (11.5%) than subantarctic fur seal (8.9%) pups. These results suggest that, compared with subantarctic fur seals, Antarctic fur seal pups adopt a strategy of faster lean growth and physiological development, coupled with greater amounts of metabolically expensive behavioural activity, in order to acquire the necessary foraging skills in time for their younger weaning age.

The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups

The physiological and behavioural development of diving was examined in Australian fur seal (Arctocephalus pusillus doriferus) pups to assess whether animals at weaning are capable of exploiting the same resources as adult females. Haematocrit, haemoglobin and myoglobin contents all increased throughout pup development though total body oxygen stores reached only 71% of adult female levels just prior to weaning. Oxygen storage components, however, did not develop at the same pace. Whereas blood oxygen stores had reached adult female levels by 9 months of age, muscle oxygen stores were slower to develop, reaching only 23% of adult levels by this age. Increases in diving behaviour corresponded to the physiological changes observed. Pups spent little time (<8%) in the water prior to moulting (age 1–2 months) whereas following the moult, they spent >27% of time in the water and made mid-water dives (maximum depth 35.7 ± 2.9 m) with durations of 0.35 ± 0.03 min. By 9 months (just prior to weaning), 30.5 ± 9.3% of all dives performed were U-shaped benthic dives (maximum depth 65.0 ± 6.0 m) with mean durations of 0.87 ± 0.25 min, significantly shorter than those of adult females. These results suggest that while Australian fur seal pups approaching the age of weaning are able to reach similar depths as adult females, they do not have the physiological capacity to remain at these depths for sufficient durations to exploit them to the same efficiency.

Body composition changes, metabolic fuel use and energy expenditure during extended fasting in subantarctic fur seal (Arctocephalus tropicalis) pups at Amsterdam Island

The fasting metabolism of 71- to 235-d-old subantarctic fur seal (Arctocephalus tropicalis) pups from Amsterdam Island, southern Indian Ocean, was investigated during the long foraging trips of their mothers. Body lipid reserves were proportionally greater in female than male pups and higher in postmoult (37%) than premoult (10%) animals. The mass-specific rate of mass loss did not differ between the sexes but was lower than observed in other species. Daily mass loss was estimated to 56% fat, 10% protein, and 34% water. The rate of protein catabolism (15 g d⁻¹) was negatively related to the size of initial lipid stores and accounted for 9% (±1%) of total energy expenditure. However, body composition changes during the fast were not equal between the sexes, with females relying more on protein catabolism than males (11% and 5% of total energy expenditure, respectively). Energy expenditure (270 kJ kg⁻¹ d⁻¹) and metabolic water production (11.5 mL kg⁻¹ d⁻¹) rates are the lowest reported for an otariid species. These results suggest that subantarctic fur seal pups greatly reduce activity levels to lower energy expenditure in addition to adopting protein-sparing metabolic pathways in order to survive the extreme fasts they must endure on Amsterdam Island.

Fasting metbabolism in Antarctic fur seal (Artocephalus 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)·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 (F₁,₁₈=6.614, P<0.019) mass-specific RMR than male pups throughout the fasting period. Fasting FMR was also significantly (t₁₅=2.37, P<0.035) greater in females (823 kJ·kg⁻¹·d⁻¹) than males (686 kJ·kg⁻¹·d⁻¹). Average protein turnover during the study period was 19.3 g·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 β-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.

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.

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.

Analysis of zinc transporter, hZnT4(Slc30A4), gene expression in a mammary gland disorder leading to reduced zinc secretion into milk

Zinc deficiency, causing impaired growth and development, may have a nutritional or genetic basis. We investigated two cases of inherited zinc deficiency found in breast-fed neonates, caused by low levels of zinc in the maternal milk. This condition is different from acrodermatitis enteropathica but has similarities to the "lethal milk" mouse, where low levels of zinc in the milk of lactating dams leads to zinc deficiency in pups. The mouse disorder has been attributed to a defect in the ZnT4 gene. Little is known about the expression of the human orthologue, hZnT4 (Slc30A4). Sequence analysis of cDNA, real-time PCR and Western blot analysis of hZnT4, carried out on control cells and cells from unrelated mothers of two infants with zinc deficiency, showed no differences. The hZnT4 gene was highly expressed in mouthwash buccal cells compared with lymphoblasts and fibroblasts. The hZnT4 protein did not co-localise with intracellular free zinc pools, suggesting that hZnT4 is not involved in transport of zinc into vesicles destined for secretion into milk. This observation, combined with phenotypic differences between the "lethal milk" mouse and the human disorder, suggests that the "lethal milk" mouse is not the corresponding model for the human zinc deficiency condition.

Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer

1.Foraging behaviours of the Australian sea lion (Neophoca cinerea) reflect an animal working hard to exploit benthic habitats. Lactating females demonstrate almost continuous diving, maximize bottom time, exhibit elevated field metabolism and frequently exceed their calculated aerobic dive limit. Given that larger animals have disproportionately greater diving capabilities, we wanted to examine how pups and juveniles forage successfully.
2.Time/depth recorders were deployed on pups, juveniles and adult females at Seal Bay Conservation Park, Kangaroo Island, South Australia. Ten different mother/pup pairs were equipped at three stages of development (6, 15 and 23 months) to record the diving behaviours of 51 (nine instruments failed) animals.
3. Dive depth and duration increased with age. However, development was slow. At 6 months, pups demonstrated minimal diving activity and the mean depth for 23-month-old juveniles was only 44 ± 4 m, or 62% of adult mean depth.
4. Although pups and juveniles did not reach adult depths or durations, dive records for young sea lions indicate benthic diving with mean bottom times (2·0 ± 0·2 min) similar to those of females (2·1 ± 0·2 min). This was accomplished by spending higher proportions of each dive and total time at sea on or near the bottom than adults. Immature sea lions also spent a higher percentage of time at sea diving.
5. Juveniles may have to work harder because they are weaned before reaching full diving capability. For benthic foragers, reduced diving ability limits available foraging habitat. Furthermore, as juveniles appear to operate close to their physiological maximum, they would have a difficult time increasing foraging effort in response to reductions in prey. Although benthic prey are less influenced by seasonal fluctuations and oceanographic perturbations than epipelagic prey, demersal fishery trawls may impact juvenile survival by disrupting habitat and removing larger size classes of prey. These issues may be an important factor as to why the Australian sea lion population is currently at risk.

Ontogeny of movements and foraging ranges in the Australian sea lion

This study tracked the movements of Australian sea lion (Neophoca cinerea) pups, juveniles, and adult females to identify home ranges and determine if young sea lions accompanied their mothers at sea. Satellite tags were deployed on nine 15- mo-old pups, nine 23-mo-old juveniles, and twenty-nine adult female Australian sea lions at Seal Bay Conservation Park, Kangaroo Island, South Australia. Females did not travel with their offspring at sea, suggesting young Australian sea lions learn foraging behaviors independently. Although home ranges increased with age,  23-mo-old juveniles had not developed adult movement capacity and their range was only 40.6% of the adult range. Juveniles traveled shorter distances (34.8 ± 5.5 km) at slower speeds (2.0 ± 0.3 km/h) than adults (67.9 ± 3.5 km and 3.9 ± 0.3 km/h). Young sea lions also stayed in shallower waters; sea floor depths of mean locations were 48±7m for juveniles and 74±2m for females. Restricted to shallow coastal waters, pups and juveniles are more likely to be disproportionately impacted by human activities. With limited available foraging habitat, young Australian sea lions appear particularly vulnerable to environmental alterations resulting from fisheries or climate change.