Daryl J. Boness

The Behavior, Physiology, and Anatomy of Lactation in the Pinnipedia

Lactation represents a major proportion of maternal reproductive effort. In ungulates the energetic costs of lactation comprise 75–80% of the total energetic costs of reproduction (Oftedal, 1985). Although pinnipeds feed at sea, they return to land or ice to give birth and to nurse their young (Fig. 1) (Bonner, 1984). Thus, the bulk of a female’s reproductive expenditure is in an environment in which she cannot feed. The temporal separation of feeding and lactation is achieved by a wide range of behavioral, physiological, and anatomic adaptations.

The Effect of Maternal Size and Milk Energy Output on Pup Growth in Grey Seals (Halichoerus grypus)

In phocid species in which females fast throughout lactation, maternal energy reserves at parturition must support lactation. Thus, differences in body size and energy stores may influence the magnitude of maternal energy transfer. We examined variation in milk energy transfer and its consequence for pup growth in grey seals over a wide range of maternal body sizes. Milk samples (n = 42) were collected from 28 females over the 16-d lactation period. Milk yields were measured in nine mother-pup pairs by deuterium oxide dilution. Milk fat and energy content increased dramatically over the first half of lactation. At mid-to late lactation milk composition averaged 71.1% dry matter, 59.8% fat, 9.2% protein, and 24.8 kJ/g (bomb calorimetry). Initial maternal mass (149-256 kg) and daily mass loss (3-9 kg/d) were correlated with daily milk output (1.3-4.1 kg/d). Milk energy output (29-92 MJ/d) in turn explained pup mass gain (0.8-2.8 kg/d, r² = 0.997). Pups with greater energy intakes had a greater ratio of fat to protein deposition and thus a greater efficiency of energy storage, increasing from 40% to 79%. Daily milk intake did not change over lactation, but growth rate was greater during the second half of lactation because milk energy intake was greater. Results of this study indicate that large females lose mass more rapidly, produce more milk, and wean larger, fatter pups than do small females. We conclude that differences in maternal mass and available energy stores may have substantial consequences for the pup and may account for much of the reported variation in pup growth both within and between populations of phocids such as the grey seal.

Mass and Energy Transfer during Lactation in a Small Phocid, the Harbor Seal (Phoca vitulina)

In true seals (family Phocidae), the large energetic costs of lactation are supported primarily by mobilization of stored fat. We studied the magnitude of fat and energy depletion in lactating harbor seals (n = 17) on Sable Island, and fat and energy storage in their pups, using cross-sectional morphometric and isotopic methods. Initial mass of mothers studied ranged from 87 to 94 kg. Maternal mass declined by 33% over the first 19 d of the 24-d lactation period. Most of this loss (68.8%) was from the sculp (i.e., skin and attached blubber). Estimated maternal body fat, derived from dilution of deuterium oxide, decreased from 24% at parturition to about 7% at 19 d postpartum. Mothers lost 163 kg (78.7%) of their stored fat and 3.1 kg (20.0%) of stored protein, representing 713.8 MJ (169 Mcal) or 60.5% of stored energy. Newborn pups contained 93.0 MJ (22.1 Mcal) of energy, divided similarly between fat (46 4%) and protein (53.6%). Pup body mass increased from 10.6 kg to 25.8 kg. Sculp mass accounted for 62. 7% of mass gained by the pup. Total body fat of pups increased from 11% at birth to 35% at 19 d. Pups deposited 346 8 MJ (82.2 Mcal) or 48. 7% of energy withdrawn by females from body stores. Unlike large phocid species, lactating harbor seals initiate feeding during lactation apparently because energy reserves are insufficient to cover the combined costs of lactation and maternal metabolism.

Milk and energy intakes of suckling California sea lion Zalophus californianus pups in relation to sex, growth, and predicted maintenance requirements

Isotope dilution was used to measure milk intake of 43 California sea lion pups on San Nicolas Island, California, from 1982 to 1984. Deuterium concentration was monitored in serial blood samples collected at about 5-day intervals for 3 wk after isotope administration. Estimated milk intakes differed significantly between male (723 ± 31.0 g ․ day⁻¹) and female (609 ± 24.0 g ․ day⁻¹) pups but did not increase from the first to second month postpartum. On a metabolic size basis (weight0.83), gross energy intakes did not differ between male and female pups but did differ between years, apparently as a consequence of the 1983 El Niño. The mean energy intakes (kcal ․ day⁻¹) of sea lion pups in the first (61 · W0.83) and second (308 · W0.83) months were high relative to terrestrial species. Regression of energy intake on growth rate predicted that maintenance energy requirements (kcal ․ day⁻¹) were also high (168 and 252 · W0.83 in the first and second months). The fact that California sea lion pups devote a large proportion of energy to maintenance rather than to growth or to blubber deposition may reflect both the energetic demands of an aquatic environment and limitations in the ability of lactating females to increase the rate of energy transfer to pups.

PRENATAL AND POSTNATAL TRANSFER OF FATTY ACIDS FROM MOTHER TO PUP IN THE HOODED SEAL

Unlike most mammals, hooded seal (Cystophora cristata) pups are born with a substantial layer of adipose tissue. Subsequently, during the brief lactation period of only 4 days, fasting mothers mobilize enormous amounts of lipid from blubber and secrete milk (60% fat) at rates of 10 kg·day-1. Pups gain 7 kg·day-1 due primarily to the deposition of fat in blubber. We measured blubber content and fatty acid composition of blubber and milk in hooded seal mother-pup pairs at birth and over the 4-day lactation period to examine the nature and source of fetal lipids, the incorporation of maternal blubber fatty acids into milk lipid, and patterns of fatty acid deposition in suckling young. The fatty acid composition of the blubber of the newborn was notably different from that of its mother. Fetal deposition was likely due to a combination of both fetal synthesis and direct placental transfer of maternal circulating fatty acids. The blubber of the newborn was characterized by high levels (>90% of total fatty acids) of saturated and monounsaturated fatty acids of primarily endogenous origin. In particular, the fetus appeared to have high Δ-9 desaturase activity as evidenced by the large amounts of 14:1n-5 (4.2%) and 16:1n-7 (37.0%) in newborn blubber compared to maternal blubber (0.2% and 14.1%, respectively). Nevertheless, essential and long-chain polyunsaturated fatty acids of the n-3 and n-6 families, which could only have originated by direct transfer from the mother, comprised>7% of pup blubber fatty acids and indicated greater rates of placental transfer than found in humans. In hooded seal mothers, rapid lipid transfer during the brief lactation period appeared to be facilitated by direct incorporation of mobilized fatty acids into milk. Although some differences in proportions of specific fatty acids were found between milk and maternal blubber, most of these differences declined over the course of lactation. However, selective mobilization of 20:5n-3 from maternal blubber into milk was apparent throughout lactation and resulted in elevated levels in pup blubber at weaning compared to maternal blubber. Ingested fatty acids were deposited directly and without modification into the blubber of pups, and by 4 days the fatty acid composition of pup blubber was virtually identical to that of the milk consumed.

Maternal and newborn life-history traits during periods of contrasting population trends: implications for explaining the decline of harbour seals ( Phoca vitulina ), on Sable Island

Annual censuses of the number of harbour seal Phoca vitulina pups born on Sable Island Canada showed an increasing trend during the 1980s, but a rapid decline through the 1990s from 625 pups in 1989 to only 32 by 1997. Weekly surveys of the North Beach of the island during the 1991–98 breeding seasons showed that the number of adults and juveniles also declined during the 1990s. Despite the dramatic demographic changes, maternal postpartum mass, pup birth mass, relative birth mass, lactation duration, pup weaning mass and relative weaning mass showed no significant trends during 1987–96. However, two traits did change. The age structure of parturient females increased significantly, indicating reduced recruitment to the breeding population. Mean birth date increased by 7 days during the early 1990s, suggesting nutritional stress of females and later implantation dates. This nutritional stress may in turn have been caused by increased competition from the rapidly increasing grey seal population on Sable Island. Although minimum estimates of shark-inflicted mortality can account for much of the decline, evidence suggests that food shortage arising from interspecific competition may have also played a role in causing the decline of the population through effects on fecundity and juvenile survival.

The effect of a natural environmental disturbance on maternal investment and pup behavior in the California sea lion

SummaryObserved changes in maternal investment due to an environmentally induced decrease in food supply (the 1983 El Niño-Southern Oscillation) are compared witha priori predictions for the California sea lion (Zalophus californianus). Changes in behavior, growth and mortality of off-spring were also examined. Data collected in the first two months postpartum for the years before (PRE), during (EN), and the two years after (POST1 and POST2) the 1983 El Niño indicate that females initiated postpartum feeding trips earlier during the food shortage, and spent more time away on individual feeding trips in both the El Niño year and the year after. Perinatal sex ratios (♀:♂) in the years PRE, EN, POST1 and POST2 were 1:1, 1.4:1, 1.1:1 and 1:1.4, respectively. Fewer copulations were observed during the El Niño year, but this difference was not statistically significant. Pups spent less time suckling in the food shortage year and the year following, but attempted to sneak suckle more. Pups were less active and played on land less in the El Niño and following year. Finally, maternal investment as measured by milk intake of offspring was decreased, pups grew more slowly, and suffered increased mortality during the food shortage year. Despite expected sex differences in maternal investment and pup behavior in response to food shortage, there were no sex-biased differences in response in either females or pups. As expected, the food shortage did not affect adult males since they migrate north during the non-breeding season where the environmental perturbation was less severe.

Energy Transfer by Lactating Hooded Seals and Nutrient Deposition in Their Pups during the Four Days from Birth to Weaning

Hooded seals (Cystophora cristata) have a lactation period of 4 d. The rate of milk energy transfer must be very high to ensure that pups are weaned with sufficient energy reserves to withstand the lengthy postweaning fast. Milk energy transfer was measured by isotope dilution (n = 6), and energy deposition was assayed by chemical analysis of pups at birth (n = 4) and weaning (n = 5). Estimates of body water content obtained by isotope dilution and direct analysis were not significantly different. Water constituted only 71.7% ± 0.50% (SE) of lean body mass at birth, indicating developmental maturity. Newborn pups were also high in fat (14.0% ± 0.78%) and energy (10.1 ± 0.25 MJ/kg). Pups consumed 7.52 ± 0.469 kg/d milk containing 187 ± 11.6 MJ/d. Total milk and energy yields were estimated as 30.1 kg and 746 MJ. Pups deposited 88% of ingested fat, 41% of protein, and 84% of energy. Of the weight gain, 82% was fat. The energy content of pups increased nearly fourfold from birth to weaning, but protein content increased by only 11%. At weaning, the energy content of the pup was similar, relative to maternal metabolic size (17. 7 MJ/kg0.75), to that in other species with longer lactation periods. We conclude that extreme abbreviation of lactation is feasible as a reproductive strategy in the hooded seal because (1) most of the growth of the lean body and 27% of the energy deposition in pups occur in utero, (2) females produce large amounts of high-fat milk, and (3) the pups are very eficient at converting milk fat to stored lipids.

Fostering behavior in Hawaiian monk seals : is there a reproductive cost?

SummaryFostering behavior has been reported in a large number of mammal and bird species although the relative frequency of its occurrence in most species is unknown. A commonly held view is that fostering is costly to the parent(s) engaged in it. However, empirical studies of fostering are few, and measures of either cost or benefit are even rarer. During a study of individually marked Hawaiian monk seal mothers and pups, observed over the course of maternal care, I found that 87% of 30 females fostered pups. Females sequentially fostered an average of 2.3 pups (range: 1–5 pups) during the approximately 40-day lactation. The median proportion of lactation spent fostering was 34% (range: 5%–90%). Confusion during aggressive interactions appeared to be the major antecedent of fostering and may be understandable in terms of the spatial pattern among females. The density of females with pups was relatively low for a land-breeding seal (1.5 females per 1000 m2), and the typical spatial pattern indicated a tendency toward dispersion. Yet, movements of females and pups to and from water occasionally leave females within a meter or two of each other. Several measures of the immediate reproductive cost of fostering were obtained, including: the length of time suckled by pups, the size of pups at the end of suckling, and survivorship to 1 year of age. There was no correlation between these measures for individual pups and the extent to which their mothers fostered, indicating that the high levels of fostering may be maintained in monk seals because they are not selected against.

Development of the Blood and Muscle Oxygen Stores in Gray Seals (Halichoerus grypus): Implications for Juvenile Diving Capacity and the Necessity of a Terrestrial Postweaning Fast.

To successfully transition from nursing to foraging, phocid seal pups must develop adequate diving physiology within the limited time between birth and their first independent foraging trip to sea. We studied the postpartum development of oxygen stores in gray seals (Halichoerus grypus, n = 40) to better understand the ontogeny of diving capacity in phocids. Hemoglobin (Hb), hematocrit (Hct), blood volume (BV), and myoglobin (Mb) levels in newborn (3 d postpartum [DPP]) and newly weaned (17 ± 0.4 DPP) pups were among the lowest measured across age classes. During the pups’ terrestrial postweaning fast (PWF), Hb, Hct, mass‐specific BV, and Mb increased by 28%, 21%, 13%, and 29%, respectively, resulting in a 35% increase in total body mass‐specific oxygen stores and a 23% increase in calculated aerobic dive limit (CADL). Although Hb and Hct levels at the end of the PWF were nearly identical to those of yearlings, total body mass‐specific oxygen stores and CADL of weaned pups departing for sea were only 66%–67% and 32%–62%, respectively, of those for yearlings and adult females. The PWF represents an integral component of the physiological development of diving capacity in phocids; however, newly independent phocids still appear to have limited diving capabilities at the onset of foraging.