Variation in Milk Production and Lactation Performance in Grey Seals and Consequences for Pup Growth and Weaning Characteristics

Abstract

Phocid seals are one of the few groups of mammals capable of sustaining the energetic demands of lactation entirely through body nutrient stores while fasting. Lactation performance of the female in turn influences the rate and pattern of pup growth. We examined variation in and patterns of milk composition and production, maternal energy output, and pup growth and energy deposition over the entire lactation period in 18 grey seal mother-pup pairs using hydrogen isotope (3H2O and D2O) dilution. Milk composition was independent of maternal mass and nutrient stores, indicating dependence on other physiological and genetic factors. Heavier females lactated longer (r2=0.653, P<0.001), had higher total milk outputs (r2=0.652, P<0.001), and produced larger pups at weaning (r2=0.417, P=0.005). While fatter females lactated for longer periods of time (r2=0.595, P<0.001), females with a larger lean body mass at parturition produced more milk (r2=0.579, P<0.001). Total milk energy output was the strongest predictor of pup weaning mass, which, along with the pup's efficiency of energy storage, accounted for 91% of the variation in weaning mass. Nevertheless, there was sufficient plasticity in milk composition and energy output that some smaller females produced relatively large pups. Few females appeared to deplete body nutrients to the point where it might limit the duration of lactation.

Capital Expenditure and Income (Foraging) during Pinniped Lactation: The Example of the Weddell Seal (Leptonychotes weddellii)

“…Weddell seal females certainly lose a large amount of body mass: for example, females that we studied in 2006 and 2007 lost 40% of their two-day postpartum mass during about 40 days lactation (Figure 1). The daily mass loss of 1.0% of initial mass is lower than values of 1.5%-3.4% for fasting and lactating females of the northern elephant seal, southern elephant seal, land-breeding gray seal, and hooded seal (Costa et al, 1986;Carlini et al, 1997;Mellish et al, 1999aMellish et al, , 1999b, but Weddell seal lactation is so prolonged that overall mass loss (42%) is equal to or greater than that in the other species (14%-39%). If mass loss is standardized to a lactation length of 42 days, initial mass predicts 66% of the variation in mass loss, indicating that large females lose more mass than small females (Figure 2).…”

“…As both protein and carbohydrate in milk potentially derive from amino acids (either directly or via gluconeogenesis), this suggests that high protein demands may be selected against during the evolution of capital breeding (Oftedal, 1993). In the grey seal (Halichoerus grypus), daily milk production and fi nal offspring mass were signifi cantly correlated with initial maternal protein but not initial fat stores (Mellish et al, 1999a), despite the fact that most of maternal body energy reserves are stored as fat. Although phocid seals are often thought to be unusually effi cient at conserving protein during fasting, this assumption may have to be reconsidered (Eisert, 2003).…”

“…It is therefore also necessary to measure milk yield and milk composition to estimate reproductive costs associated with the output of milk constituents (Oftedal, 1984b). The most widely used method for estimating milk production in seals relies on the dilution of hydrogen isotope-labeled water in nursing young (e.g., Costa et al, 1986;Oftedal and Iverson, 1987;Oftedal et al, 1987b;Tedman and Green, 1987;Lydersen et al, 1992;Iverson et al, 1993;Lydersen and Hammill, 1993;Oftedal et al, 1993;Lydersen and Kovacs, 1996;Oftedal et al, 1996;Lydersen et al, 1997;Mellish et al, 1999a;Arnould and Hindell, 2002). If milk is the exclusive source of water (both free and metabolic) for the offspring, then milk consumption can be estimated from water turnover and milk composition (Oftedal and Iverson, 1987).…”

Primiparous and multiparous females differ in mammary gland alveolar development: implications for milk production

“…To ensure that the values for the females selected for this study were consistent with our previous observations for multiparous and primiparous females (Lang et al, 2009;Lang et al, 2011a) and to verify that our biopsy procedure did not adversely affect mammary gland function, we compared milk composition, daily milk output and pup growth patterns between the groups. Because changes in these characters with lactation stage have already been well characterized for this species (Iverson et al, 1993;Mellish et al, 1999a, Lang et al, 2009 P<0.001). Pup growth followed the same pattern in both groups throughout lactation.…”

“…Females give birth to a single pup, there is no alloparental or paternal support, and pups consume only milk during the lactation period. Females remain ashore with their pup throughout the relatively brief lactation period (16-18days) (Bowen et al, 1992), during which females secrete large quantities (average 3.2kgday -1 ) of high-energy milk (40-60% fat) (Iverson et al, 1993;Mellish et al, 1999a;Lang et al, 2011a). At the end of lactation, females abruptly wean their pups and depart the breeding colony.…”