Blood chemistry in southern elephant seal mothers and pups during lactation reveals no effect of handling

Serum clinical chemistry parameters were examined in lactating southern elephant seal Mirounga leonina mothers and their pups from the declining Macquarie Island population. There were significant changes in serum values from 2 to 21 days postpartum in both nursing mothers (increase: inorganic phosphate; decrease: creatinine, potassium, chloride, cholesterol, total protein, albumin, globulin, aspartate aminotransferase, creatine kinase) and suckling pups (increase: inorganic phosphate, globulin, cholesterol; decrease: albumin, alkaline phosphatase, gammaglutamyl transferase; increase followed by decrease: triglycerides, iron). We found no evidence that changes were due to chronic stress effects caused by repeated chemical immobilisations (mothers) or physical restraint (pups): at late lactation, clinical chemistry values were similar for mother-pup pairs of a control group (not handled previously), moderate treatment group (previously handled twice) and high treatment group (previously handled three to four times). We were not able to detect differences in clinical chemistry values between mother-pup pairs distributed over two areas differing in the frequency of human visits. The clinical chemistry values presented here can serve as reference ranges to allow future comparison with other southern elephant seal populations to investigate factors, e.g. food limitation, suspected to be involved in population declines.     

Energy gain and loss during lactation and postweaning in southern elephant seal pups (Mirounga leonina) at King George Island

Deuterium-labeled water was used to measure changes in the proximate body composition during the lactation period and after weaning in southern elephant seal pups at King George Island, South Shetland Islands, Antarctica. During the lactation period (23.0 ± 1.4 days) pups gained a mean of 4.9 ± 0.5 kg/day (n=7). Of the total mass gain (112 ± 8 kg), 38% was water, 48% was fat, and 11% was protein. This represented an increase in total body gross energy of 2437 ± 145 MJ. The proportion of body mass represented by fat was less than 2% at birth, increasing to 35 ± 2% at weaning. We followed the pups during a mean period of 36 ± 3 days after weaning. During this period, pups had a mean loss of 1.21 ± 0.10 kg/day (n=7) comprising 39% water, 48% fat, and 12% protein. The energy cost over this period was 952 ± 168 MJ, which represented, on average, 39% of the total energy gained during the suckling period. Accepted: 3 January 2000     

Mass transfer efficiency between harp seal (Phoca groenlandica) mothers and their pups during lactation

We investigated the efficiency of mass transfer in lactating harp seals through serial measurements on individual mother-pup pairs during the whelping seasons of 1988 and 1989. We also compared the influence of longitudinal versus cross-sectional sampling on estimates of the efficiency of mass transfer. Among longitudinally sampled pairs, pups grew at an average rate of 2·3 ± 0·5 (mean ± S.D.) kg/d (N = 20). The concomitant mass loss by females averaged 3·1 ± 0·8 kg/d (N = 19). The mean efficiency of mass transfer was 77·0 ± 13·6% (N= 19 pairs).
Estimates of pup growth and female mass loss from regressions of cross-sectional data were 2·0 kg/d and 3·1 kg/d, respectively. These values produce an estimate of 65% for the efficiency of mass transfer.
Consistent with the high efficiency of mass transfer, harp seal females contribute less of their total body mass to nursing ( c. 28%) than most other phocids examined. The resulting energy savings may be important for females of an ice-breeding species, which migrate a long distance shortly after weaning their pups     

Movements and diving of bearded seal (Erignathus barbatus) mothers and pups during lactation and post-weaning

Eleven bearded seals (Erignathus barbatus) were tagged with satellite-linked dive recorders in Kongsfjorden, Svalbard, Norway, in May 1994. These animals included four mother-pup pairs and three single pups. The seals were tracked for 21–258 days. A total of ˜207,000 dives were recorded. Bearded seal mothers showed limited movements during the nursing and moulting periods. After weaning, the pups moved out of the tagging area and dispersed coastally. One pup left Svalbard and moved far offshore to Greenland and Jan Mayen. Bearded seal adults displayed a bi-modal dive behaviour, with peaks of activity that were shallower than 10 m or from 50 to 70 m. Most dives for adult seals (97%) were shorter than 10 min. Young pups performed dives that were shallower and shorter in duration than their accompanying mothers, but diving skills improved rapidly with age. Six of the seven pups dived deeper than 448 m by the time they were 2 months old. Analyses of movement data with respect to separation of mother-pup pairs suggest a lactation period of about 24 days. Accepted: 31 January 2000     

Fatty acid metabolism in fasting elephant seal pups

Summary The turnover of two plasma free fatty acids (FFA) were measured in 5 northern elephant seal pups (Mirounga angustirostris) after approximately 2 months of post-weaning fasting. Turnover was determined using simultaneous bolus injections of¹⁴C-palmitate,³H-oleate and Evans blue (EB) administered via an indwelling extradural intravertebral catheter. At this time in their natural fast, the seals exhibited plasma FFA levels and turnover values higher than reported for other marine mammals and most terrestrial carnivores. There was no consistent difference between plasma FFA turnover measured by palmitate or oleate tracers. The results imply that FFA metabolism is the primary source of energy during fasting. This is interesting in light of previous observations of minimal ketoacid accumulation and low levels of glucose and protein energy production during fasting in these juvenile seals.     

Water conservation and protein metabolism in northern elephant seal pups during the postweaning fast

Urine production and N output were monitored in northern elephant seal (Mirounga angustirostris) pups progressing through 10 weeks of a natural postweaning fast. Urine output declind by 84% (to 69±12 ml·day^–1) at 10 weeks (P<0.05). Glomerular filtration rate at 10 weeks was 51% of the 67±3 ml serum·min^–1 observed during week 1 (P<0.05). Urine N excretion fell by 69% to 1.2±0.17 g·day^–1, while urinary concentration increased (P<0.05). Serum urea declined from an initial 11 mmol·1^–1 to 5–7 mmol·1^–1 by 5 weeks. The fall in urinary N loss (and thus amino acid oxidation) was concomitant with depressed metabolic rate. Therefore, protein contributed little toward meeting energy demands (i.e., <4% of average metabolic rate) throughout fasting. These data indicate that fasting pups improve water conservation and minimize protein catabolism during prolonged natural fasts without an exogenous source of water.Abbreviations AA amino acid(s) - AMR average metabolic rate - ANOVA one-way analysis of variance - BMR basal metabolic rate - BUN blood urea nitrogen - EP end product - EWL evaporative water loss - [Gr]_s serum creatinine concentration - GFR glomerular filtration rate - LBM lean body mass - LML Long Marine Laboratory - MR metabolic rate - NEFA non-esterified fatty acids - RMR resting metabolic rate - TCA tricarboxylic acid - U:C ulinary urea: creatinine concentration ratio     

Glucose metabolism during lactation in a fasting animal, the northern elephant seal

Fasting is associated with a series of physiological responses that protect body tissues from degradation by efficiently using expendable energy reserves while sparing protein. Lactation requires the mobilization of maternal nutrients for milk synthesis. The rare life history trait of fasting simultaneous with lactation results in the conflicting demands of provisioning offspring while meeting maternal metabolic costs and preserving maternal tissues for her own survival and future reproduction. Certain tissues continue to require glucose for operation during fasting and might constrain tissue mobilization for lactogenesis due to a need for gluconeogenic substrates. This study investigated glucose flux, glucose cycle activity, and the influence of regulatory hormones in fasting lactating northern elephant seals. Measurements were taken early (5 days) and late (21 days) during the lactation period and, as a nonlactating comparison, after the completion of molting. Glucose cycle activity was highly variable in all study groups and did not change over lactation (P > 0.3), whereas endogenous glucose production decreased during lactation (t = -3.41, P = 0.008). Insulin and insulin-to-glucagon molar ratio decreased across lactation (t = 6.48, 4.28; P = 0.0001, 0.002), while plasma cortisol level increased (t = 4.15, P = 0.002). There were no relationships between glucose production and hormone levels. The glucose production values measured exceeded that predicted from available gluconeogenic substrate, indicating substantial glucose recycling in this species.     

Southern elephant seal,Mirounga leonina: composition of milk during lactation

An analysis of milk constituents during various stages of lactation in the southern elephant seal Mirounga leonina was carried out. Forty-six milk samples were taken from 30 females throughout lactation during 1985, 1987, 1990 and 1991 on Stranger Point, King George Island, South Shetland Islands. Total nitrogen (TN), non-protein nitrogen (NPN), sugar, fat, ash and water were measured, and from some of these data true protein and energy content were calculated. The results showed a high degree of variation in water and fat concentrations among samples at different stages of lactation. During the first 20 days the fat content of milk increased from about 12 to approximately 52%, while water content fell from 70 to 33%. The composition of milk changes rapidly during the first days post-partum. Protein, minerals and sugar appear to remain stable after the fourth day of lactation. Milk samples contain significant levels of sugars; thin layer chromatography indicates the presence of lactose and glucose together with other unidentified components. There is evidence of a striking change in composition of the milk in the later part of lactation; the progressive increase in the fat:water ratio is abruptly reversed just prior to weaning.     

Circulatory water concentration in suckling and fasting northern elephant seal pups

Summary This study examined circulatory water concentrations in the neonatal northern elephant seal (Mirounga angustirostris) in order to determine how suckling and fasting would alter the percentage of water in the whole blood, plasma, and red blood cells (RBC). Plasma water concentration dropped by about 3% during suckling and recovered about 1% during the fast (92.38±0.48% <1 week old, 90.15±0.36% weaning, 91.02±0.68% end of fast). RBC water values during this time were more variable than plasma values: RBC water increased about 1% during the first 2 weeks of suckling (from 67.80±0.28% to 68.68±0.51%) but dropped to slightly below original neonatal values by weaning 67.15±0.63%. The first several weeks of fasting were marked by wide variability in RBC water, but by the end of the fast RBC water was comparable to that at weaning. These results indicate: 1) Northern elephant seal pups do not exhibit circulatory dehydration during 10 weeks of fasting; 2) Measurements of plasma or RBC metabolites (such as plasma glucose or RBC hemoglobin) may show variations or trends due not to metabolic regulation but rather to changes in circulatory water concentration.Abbreviations Hb Hemoglobin - Hct Hematocrit - MCHC Mean corpuscular - RBC Red blood cell - WB Whole blood     

Renal function in suckling and fasting pups of the northern elephant seal.

Elephant seals fast for prolonged periods without access to water. This is made possible, in part, by reductions in urine production. However, the mechanisms involved in reducing urine production are not understood. In this study, glomerular filtration rate (GFR) was measured in five northern elephant seal pups (Mirounga angustirostris) via the inulin clearance technique. Measurements were made during day 9 and day 18-22 of nursing and the second and eighth week of the postweaning fast. Plasma aldosterone and cortisol concentrations, quantified by radioimmunoassay, were measured in eight other weanlings during the second and eighth week of the fast. Mean GFR was 79.3+/-29.3 ml/min during the early suckling period and 78.2+/-17.1, 89.8+/-52.7, and 80.4+/-12.2 ml/min during the late suckling, early fasting and late fasting periods, respectively. Differences between nursing and fasting were insignificant, possibly because reduced protein oxidation during suckling and rapid recruitment of protein for tissue synthesis obviated the need for postprandial hyperfiltration. Alternatively, maintenance of GFR during fasting may facilitate urea concentration by compensating for reductions in the fractional excretion of urea. It is further hypothesized that aldosterone is primarily responsible for mediating renal water reabsorption in this system.     

Body water handling in response to hypertonic-saline induced diuresis in fasting northern elephant seal pups (Mirounga angustirostris)

During natural fasting conditions in postweaned northern elephant seal (NES) (Mirounga angustirostris) pups, urinary water loss is minimized and percent total body water (TBW) is maintained constant. However, following infusion of hypertonic saline, glomerular filtration rate (GFR) and urine output increased in fasting pups. Therefore, we quantified the magnitude of the hypernatremia-induced diuresis relative to the animal's total body water (TBW) pool and the percentage of filtered water reabsorbed. Following a 24 h control period, naturally fasting NES pups (n=7) were infused (4 ml min(-1)) with hypertonic saline (16.7%) at a dose of 3 mmol NaCl kg(-1) body mass. Total body water was estimated prior to infusion by tritium dilution, GFR was estimated by standard creatinine clearance, and urine output (V) was measured for 24 h during the control and post infusion periods. Percentage of filtered water reabsorbed was calculated as (1-(V/GFR))x100. Twenty-four hours following the infusion, GFR (control: 69+/-12 ml min(-1) and post-infusion: 118+/-19 ml min(-1); mean+/-S.E.) increased 77+/-28% above control and the percentage of filtered water reabsorbed was decreased 0.4+/-0.1%. The increase in urine output (control: 218+/-47 ml d(-1) and post-infusion: 883+/-92 ml d(-1)) accounted for 1.7+/-0.2% of the pups' TBW. The hypernatremia-induced diuresis was accompanied by the loss of body water indicating the lack of water retention. Although the 77% increase in GFR was only associated with a 0.4% decrease in the percentage of filtered water reabsorbed, this decrease was significant enough to result in a 4-fold increase in urine output. Despite the observed diuresis, fasting NES pups appear to possess an efficient water recycling mechanism requiring only a small percentage of body water to excrete an excess salt load. This water recycling mechanism may allow pups to avoid negative perturbations in body water as they initiate feeding in a marine environment following the fast.     

Differential changes of fat-soluble vitamins and pollutants during lactation in northern elephant seal mother-pup pairs

We investigated the changes of vitamins A and E as well as PCBs and DDTs during lactation in northern elephant seal (Mirounga angustirostris) mother-pup pairs. On average, milk vitamin A concentrations were 6 times higher during late lactation than during early lactation, a pattern that differs dramatically from terrestrial mammals. Vitamin A concentrations also significantly increased in the inner blubber throughout lactation, whereas they remained constant in the outer blubber. Similar dynamics were observed for PCBs and DDTs in maternal blubber and milk. Blubber appears to be an important storage site for vitamin A and organochlorines in seals and a direct transfer of those molecules to the mammary gland may occur. The dynamics of vitamin A, PCBs and DDTs differed from those of vitamin E. There was a significant drop in milk vitamin E concentrations between early and late lactation, which is the usual pattern observed in terrestrial mammals. The dynamics of vitamin E in the blubber layers also differed from those of vitamin A, suggesting different mechanisms of mobilization and transfer into the milk.     

Mass transfer from mothers to pups and mass recovery by mothers during the post-breeding foraging period in southern elephant seals (Mirounga leonina) at King George Island

Mass transfer from mother to pup during the lactation period, and mass recovery for the same females during the foraging period were measured in the southern elephant seal at King George Island, Antarctica. During the 19.2 ± 0.9-day lactation period measured (which represented 87% of the entire nursing), females lost a mean mass of 10.56 ± 1.76 kg/day (n = 27), while their pups gained a mean mass of 5.27 ± 1.1 kg/day. There was a correlation between daily body weight gain in pups and daily weight loss by their mothers. Pup weaning mass was positively related to maternal post-partum mass. Serial samples showed that weight losses by females and gains by their pups were not linear over lactation, but showed lower values at the beginning and at the end of lactation. During the 60.5 ± 6.2-day foraging phase between the end of lactation and molt, females gained 2.21 ± 0.65 kg/day (n = 12), or 54% of the mass lost during nursing. Growth rates reported here are higher than those reported in other breeding sites. However, the ratio of body mass loss by females to gain by their pups was similar, suggesting that higher growth rates and greater weaning mass at South Shetland are due to a higher mean weight of females on arrival at this breeding site. The foraging period was shorter and the mass gained greater than those measured at South Georgia; this could be related to relatively shorter distances to foraging areas. Received: 20 September 1996 / Accepted: 28 April 1997     

The founding of a southern elephant seal colony

The only large mainland colony of southern elephant seals (Mirounga leonina) is on Península Valdés, at 42°S, in Argentine Patagonia. Censuses of pups have been carried out regularly there since 1970, and the population grew five‐fold by 2010. Here we use Bayesian modeling tools to make rigorous estimates of the rate of population growth, r, and to estimate survival and recruitment parameters that could account for the growth, incorporating observation error across different census methods. In the 1970s, r= 8%/yr, but has slowed to <1%/yr over the past decade. Using explicit demographic models, we established that the high growth of the 1970s was consistent with adult and juvenile survival at the upper end of published values (0.87/yr adult female survival; 0.40 juvenile survivorship to age four); the decline in the rate of population growth from 1970 to 2010 can be described by density‐dependent reductions in adult and juvenile survival that fall well within published variation. Extrapolating empirical models of population growth rate backwards illustrates that the population could have been an established colony, with 100 pups born per year, between 1915 and 1945, consistent with qualitative observations prior to 1950. We conclude that the Valdés colony was founded by a few immigrants early in the 20th century and has been growing mostly by internal recruitment, with unknown density‐dependent processes causing a reduction in growth and stabilization at 15,000–16,000 pups born.     

Vocal signature recognition of mothers by fur seal pups

Subantarctic fur seals, Arctocephalus tropicalis, come ashore to breed in dense colonies and lactating females have to alternate foraging trips at sea with periods ashore during which they suckle their pups. The effectiveness of vocal recognition between mothers and pups, has been shown experimentally. To see whether the recognition abilities of females differ from those of their offspring, we investigated how pups recognize their mother's calls. We used artificially modified signals in playback experiments to determine which acoustic parameters support the recognition process. Pups used both the energy spectrum and the ascending frequency modulation occurring at the beginning of each call. However, they seemed to rely mainly on spectral analyses. The vocal identification process at a perceptual level is therefore asymmetrical, as mothers mainly use temporal structures to recognize their pup's calls. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Glut4 is upregulated despite decreased insulin signaling during prolonged fasting in northern elephant seal pups

Postprandial cellular glucose uptake is dependent on an insulin-signaling cascade in muscle and adipose tissue, resulting in the translocation of the insulin-dependent glucose transporter 4 (Glut4) into the plasma membrane. Additionally, extended food deprivation is characterized by suppressed insulin signaling and decreased Glut4 expression. Northern elephant seals are adapted to prolonged fasts characterized by high levels of plasma glucose. To address the hypothesis that the fasting-induced decrease in insulin is associated with reduced insulin signaling in prolonged fasted seals, we compared the adipose protein levels of the cellular insulin-signaling pathway, Glut4 and plasma glucose, insulin, cortisol, and adiponectin concentrations between Early (n = 9; 2-3 wks postweaning) and Late (n = 8; 6-8 wks postweaning) fasted seals. Plasma adiponectin (230 ± 13 vs. 177 ± 11 ng/ml), insulin (2.7 ± 0.4 vs. 1.0 ± 0.1 μU/ml), and glucose (9.8 ± 0.5 vs. 8.0 ± 0.3 mM) decreased, while cortisol (124 ± 6 vs. 257 ± 30 nM) doubled with fasting. Glut4 increased (31%) with fasting despite the significant decreases in the cellular content of phosphatidylinositol 3-kinase as well as phosphorylated insulin receptor, insulin receptor substrate-1, and Akt2. Increased Glut4 may have contributed to the decrease in plasma glucose, but the decrease in insulin and insulin signaling suggests that Glut4 is not insulin-dependent in adipose tissue during prolonged fasting in elephant seals. The reduction of plasma glucose independent of insulin may make these animals an ideal model for the study of insulin resistance.     

Acquisition of gliding skills by Weddell seal (Leptonychotes weddellii) pups during lactation

Pinnipeds give birth to their pups ashore or on ice and forage in water. Therefore, neonates initially lack the adaptations to sustain prolonged underwater diving activity. Although the physiological development for breath-holding during diving has been investigated in seal pups, little is known about the concurrent development of behavioral adaptations during lactation. In this study, multisensor data loggers were used to record diving behavior and swimming gaits of pre-weaned Weddell seal (Leptonychotes weddellii) pups. Experiments were conducted in 16 pups at the Syowa Station, Antarctica, from November to December 1999 and 2004. Swimming speeds, dive depths and flipper stroking rates were recorded for each individual for about 24 h. We found that the glide index during ascending was increased with body length, whereas the dominant stroke cycle frequency were not affected by body length, dive depth and descent or ascent phase. All pups had significantly higher stroke rates in descent than in ascent, but there was no difference between swimming speed. As we found a positive relationship between the body length and age, we considered body length as an index of growth. Therefore, we conclude that pups gradually acquire the ability to glide with utilizing positive buoyancy during ascending toward the end of lactation.     

Water flux and mass gain during lactation in free-living ringed seal (Phoca hispida) pups

Three ringed seal ( Phoca hispida ) pups were used to calculate water flux and milk intake, based on mass increase and dilution of injected tritiated water. Biological half life of tritium in ringed seal pups was 130 ± 17 h (mean ± S.D.). The plateau level of the isotope indicating equilibrium with the body water was, in all cases (N = 8), reached before the first blood sample was collected after 0·5 h. Daily water flux in the pups was 62·9 ± 21·5 ml kg^-1. Estimated daily milk intake of 1103 ± 388 ml milk resulted in a mass increase of 386 ± 104 g. Neonates had a fat content of 4·75%, and a water content of 70·1% (N = 3). Corresponding figures for a pup close to weaning were 36·5% and 46·3%. Isotope dilution calculations of body water gave an overestimate of 1·6% compared with body water content from desiccation. Ringed seal milk was found to contain 38·1% fat, 9·9% protein, 2·3% lactose and 1% ash.     

Mass of weaned elephant seal pups in areas of low and high human presence

On sub-Antarctic Macquarie Island, we examined pup weaning mass of southern elephant seals in relation to human presence. Pup weaning mass was previously found to be positively associated with 1st-year survivorship. Weaned pups were weighed in a remote area, Middle Beach, and in an area of relatively high human presence, Isthmus East. The areas were reasonably similar in beach topography, wind and surf conditions, numbers of seals present per kilometre of coastline, and numbers of males and females present in harems. For a sub-sample of measured pups, data on the respective maternal size were collected using photogrammetry. Both male and female weaned pups on Middle Beach were significantly heavier than those on Isthmus East. Estimated length of mothers was significantly higher on Middle Beach. In proportion to their own size, mothers in both areas produced weaners of similar mass, indicating no direct effect of human disturbance on the efficiency of lactation. It remained unclear whether the area differences in maternal and pup size were due to natural or human-related factors.