Hooded seals (Cystophora cristata) lactate for 3.6 days during which females simultaneously fast and transfer large amounts of energy to their pups through fat-rich milk. Pups grow rapidly, principally due to blubber deposition. Lipoprotein lipase (LPL), the primary enzyme responsible for tissue uptake of triglyceride fatty acids, may strongly influence both maternal milk fat secretion and pup blubber deposition. We measured the energetic costs of lactation (using hydrogen isotope dilution, 3H2O), milk composition, prolactin, and LPL activity (post-heparin plasma LPL [PH LPL], blubber, mammary gland and milk; U) in six females. PH LPL and blubber LPL were measured in their pups. Females depleted 216.3 MJ.day-1 of body energy and fat accounted for 59% of maternal mass loss and 90% of postpartum body energy loss, but maternal body composition changed little. Maternal blubber LPL was negligible (0.0-0.2 U), while mammary LPL was elevated (1.8-2.5 U) and was paralleled by changes in prolactin. Estimated total mammary LPL activity was high (up to 20,000 U.animal-1) effectively favoring the mammary gland for lipid uptake. Levels of total blubber LPL in pups increased seven-fold over lactation. Pups with higher PH LPL at birth had greater relative growth rates (P = 0.025). Pups with greater blubber stores and total blubber LPL activity had elevated rates of fat deposition (P = 0.035).
Lactation is the most energetically expensive period for female mammals and is associated with some of the highest sustained metabolic rates (SusMR) in vertebrates (reported as total energy throughput). Females typically deal with this energy demand by increasing food intake and the structure of the alimentary tract may act as the central constraint to ceilings on SusMR at about seven times resting or standard metabolic rate (SMR). However, demands of lactation may also be met by using a form of metabolic compensation such as reducing locomotor activities or entering torpor. In some phocid seals, cetaceans and bears, females fast throughout lactation and thus cannot offset the high energetic costs of lactation through increased food intake. We demonstrate that fasting grey seal females sustain, for several weeks, one of the highest total daily energy expenditures (DEE; 7.4 x SMR) reported in mammals, while progressively reducing maintenance metabolic expenditures during lactation through means not explained by reduction in lean body mass or behavioural changes. Simultaneously, the energy-exported in milk is progressively increased, associated with increased lipoprotein lipase activity in the mammary gland, resulting in greater offspring growth. Our results suggest that females use compensatory mechanisms to help meet the extraordinary energetic costs of lactation. Additionally, although the concepts of SusMR and ceilings on total DEE may be somewhat different in fasting lactating species, our data on phocid seals demonstrate that metabolic ceilings on milk energy output, in general, are not constrained by the same kind of peripheral limitations as are other energy-consuming tissues. In phocid seals, the high ceilings on DEE during lactation, coupled with metabolic compensation, are undoubtedly important factors enabling shortened lactation.
Metabolites of lipid (free fatty acids (FFA) and β-hydroxybutyrate (βHBA)) and protein (blood urea nitrogen (BUN)) oxidation were measured during lactation in 18 female grey seals (Halichoerus grypus) and 6 female hooded seals (Cystophora cristata) as indicators of nutrient depletion and possible cues for pup weaning. FFA levels were high during lactation in both grey seals (51.2 ± 2.3 mg·dL-1) and hooded seals (67.0 ± 8.1 mg·dL-1), and levels were primarily related to the rapid lipid mobilization required for their high respective milk-fat outputs (P = 0.002). βHBA concentrations were negligible throughout lactation in both species (0.30 ± 0.14 and 0.03 ± 0.01 mg·dL-1, respectively). Grey seals exhibited a decrease in BUN levels over the course of lactation (i.e., days 0-15, 39.3 ± 1.8 - 23.5 ± 3.3 mg·dL-1, P < 0.001), which suggests protein sparing despite the added energetic cost of milk production over the 16-d lactation period. In contrast, hooded seals showed higher levels and no change in BUN levels (i.e., days 0-3, 43.2 ± 2.1 - 45.8 ± 2.1 mg·dL-1, P > 0.3), suggesting that there is less need to spare protein in a species which lactates for only 3.6 d. Females of both species weaned their pups before entering stage III fasting, therefore metabolite levels do not appear to be a physiological cue for weaning.
Metabolites of lipid (free fatty acids (FFA) and β-hydroxybutyrate (βHBA)) and protein (blood urea nitrogen (BUN)) oxidation were measured during lactation in 18 female grey seals (Halichoerus grypus) and 6 female hooded seals (Cystophora cristata) as indicators of nutrient depletion and possible cues for pup weaning. FFA levels were high during lactation in both grey seals (51.2 ± 2.3 mg·dL -1 ) and hooded seals (67.0 ± 8.1 mg·dL -1 ), and levels were primarily related to the rapid lipid mobilization required for their high respective milk-fat outputs (P = 0.002). βHBA concentrations were negligible throughout lactation in both species (0.30 ± 0.14 and 0.03 ± 0.01 mg·dL -1 , respectively). Grey seals exhibited a decrease in BUN levels over the course of lactation (i.e., days 0-15, 39.3 ± 1.8 -23.5 ± 3.3 mg·dL -1 , P < 0.001), which suggests protein sparing despite the added energetic cost of milk production over the 16-d lactation period. In contrast, hooded seals showed higher levels and no change in BUN levels (i.e., days 0-3, 43.2 ± 2.1 -45.8 ± 2.1 mg·dL -1 , P > 0.3), suggesting that there is less need to spare protein in a species which lactates for only 3.6 d. Females of both species weaned their pups before entering stage III fasting, therefore metabolite levels do not appear to be a physiological cue for weaning.Résumé : Les métabolites de l'oxydation des lipides (acides gras libres (FFA) et $-hydroxybutirate ($HBA)) et des protéines (azote uréique du sang (BUN)) ont été mesurés au cours de la période d'allaitement chez 18 femelles du Phoque gris (Halichoerus grypus) et 6 femelles du Phoque à capuchon (Cystophora cristata) en tant qu'indicateurs de l'épuisement des réserves de nutriments et déclencheurs possibles du sevrage des petits. Les concentrations de FFA sont élevées au cours de l'allaitement chez le Phoque gris (51,2 ± 2,3 mg·dL -1 ) et le Phoque à capuchon (67,0 ± 8,1 mg·dL -1 ) et elles sont reliées surtout à la mobilisation rapide des lipides nécessaires à une abondante production de lait (P = 0,002). La concentration de $HBA est négligeable chez les deux espèces au cours de toute la période d'allaitement (0,30 ± 0,14 et 0,03 ± 0,01 mg·dL -1 , respectivement). Les Phoques gris subissent une diminution de leur BUN durant l'allaitement (i.e., 39,3 ± 1,8 -23,5 ± 3,3 mg·dL -1 du jour 0 au jour 15; P < 0,001) ce qui indique une économie de protéines malgré les coûts énergétiques additionnels de la production de lait au cours des 16 jours de l'allaitement. En revanche, chez le Phoque à capuchon, les concentrations de BUN, plus élevées, ne changent pas (i.e., 43,2 ± 2,1 -45,8 ± 2,1 mg·dL -1 du jour 0 au jour 3; P > 0,3), probablement parce que l'économie des protéines est moins néces-saire chez une espèce dont l'allaitement ne dure que 3,6 jours. Les femelles des deux espèces sèvrent leurs petits avant d'entreprendre la phase III de leur jeûne et donc, la concentration des métabolites ne semble pas être le facteur physiologique déclencheur du sevrage.[Traduit par la Rédaction] Mellish and Iverson 311
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