Olav T. Oftedal

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.

The mammary gland and its origin during synapsid evolution.

Lactation appears to be an ancient reproductive trait that predates the origin of mammals. The synapsid branch of the amniote tree that separated from other taxa in the Pennsylvanian (>310 million years ago) evolved a glandular rather than scaled integument. Repeated radiations of synapsids produced a gradual accrual of mammalian features. The mammary gland apparently derives from an ancestral apocrine-like gland that was associated with hair follicles. This association is retained by monotreme mammary glands and is evident as vestigial mammary hair during early ontogenetic development of marsupials. The dense cluster of mammo-pilo-sebaceous units that open onto a nipple-less mammary patch in monotremes may reflect a structure that evolved to provide moisture and other constituents to permeable eggs. Mammary patch secretions were coopted to provide nutrients to hatchlings, but some constituents including lactose may have been secreted by ancestral apocrine-like glands in early synapsids. Advanced Triassic therapsids, such as cynodonts, almost certainly secreted complex, nutrient-rich milk, allowing a progressive decline in egg size and an increasingly altricial state of the young at hatching. This is indicated by the very small body size, presence of epipubic bones, and limited tooth replacement in advanced cynodonts and early mammaliaforms. Nipples that arose from the mammary patch rendered mammary hairs obsolete, while placental structures have allowed lactation to be truncated in living eutherians.

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.

Use of maternal reserves as a lactation strategy in large mammals.

The substrate demands of lactation must be met by increased dietary intake or by mobilization of nutrients from tissues. The capacity of animals to rely on stored nutrients depends to a large extent on body size; large animals have greater stores, relative to the demands of lactation, than do small animals. The substrate demands of lactation depend on the composition and amount of milk produced. Animals that fast or feed little during lactation are expected to produce milks low in sugar but high in fat, in order to minimize needs for gluconeogenesis while sustaining energy transfers to the young. The patterns of nutrient transfer are reviewed for four taxonomic groups that fast during part of or throughout lactation: sea lions and fur seals (Carnivora: Otariidae), bears (Carnivora: Ursidae), true seals (Carnivora: Phocidae) and baleen whales (Cetacea: Mysticeti). All these groups produce low-sugar high-fat milks, although the length of lactation, rate of milk production and growth of the young are variable. Milk protein concentrations also tend to be low, if considered in relation to milk energy content. Maternal reserves are heavily exploited for milk production in these taxa. The amounts of lipid transferred to the young represent about one-fifth to one-third of maternal lipid stores; the relative amount of the gross energy of the body transferred in the milk is similar. Some seals and bears also transfer up to 16-18 % of the maternal body protein via milk. Reliance on maternal reserves has allowed some large mammals to give birth and lactate at sites and times far removed from food resources.

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.

Lactation in whales and dolphins: evidence of divergence between baleen- and toothed-species.

Although it has been more than one hundred years since the first publication on the milks of whales and dolphins (Order Cetacea), information on lactation in these species is scattered and fragmentary. Yet the immense size of some cetaceans, and the recent evidence that another group of marine mammals, the true seals, have remarkable rates of secretion of milk fat and energy, make this group of great comparative interest. In this paper information on lactation patterns, milk composition and lactation performance is reviewed. Two very different patterns are evident. Many of the baleen whales (Suborder Mysticeti) have relatively brief lactations (5–7 months) during which they fast or eat relatively little. At mid-lactation they produce milks relatively low in water (40–53%), high in fat (30–50%), and moderately high in protein (9–15%) and ash (1.2–2.1%). From mammary gland weights and postnatal growth rates, it is predicted that their energy outputs in milk are exceptional, reaching on the order of 4000 MJ/d in the blue whale. This is possible because pregnant females migrate to feeding grounds where they can ingest and deposit great amounts of energy, building up blubber stores prior to parturition. On the other hand, the toothed whales and dolphins (Suborder Odontoceti) have much more extensive lactations typically lasting 1–3 years, during which the mothers feed. At mid-lactation their milks appear to be higher in water (60–77%) and lower in fat (10–30%) and ash (0.6–1.1%), with similar levels of protein (8–11%). At least some odontocetes resemble primates in terms of low predicted rates of energy output and a long period of dependency of the young. However, these hypotheses are based on small numbers of samples for a relatively small number of species. Much of the available data on milk composition is of rather poor quality; for example, it is not possible to determine if milk composition changes over the course of lactation among odontocetes. Additional research on cetacean mammary glands and their secretions is needed to understand the reproductive strategies of these fascinating animals.

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.

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.

Milk composition reflects pattern of material care in prosimian primates

Hypothesized relationships between milk composition and life history traits were examined by analyzing mid‐lactation milks of seven lemurs (Eulemur fulvus, E. macaco, E. rubriventer, E. mongoz, Varecia variegata, Hapalemur griseus, Lemur catta), three bushbabies (Otolemur crassicaudatus, O. garnettii, Galago moholi), and two lorises (Nycticebus coucang, Loris tardigradus); partial data were also obtained for the lemuroid Cheirogaleus medius. There were significant differences in milk composition among species within either Eulemur or Otolemur, but the four genera for which multiple samples were available (Eulemur, Varecia, Otolemur, and Nycticebus) exhibited large composition differences. Eulemur milk was, on average, very dilute (9.9% dry matter) and low in energy (0.49 kcal/g). These milks contained 0.9% fat, 1.2% protein, and 8.4% carbohydrate on a fresh weight basis. Protein energy comprised only about 15% of total milk energy. Varecia had significantly higher dry matter (13.5%), fat (3.2%), protein (4.2%), gross energy (0.80 kcal/g), and protein energy: total energy ratio (28%) than Eulemur. Milks of the lorisoid genera Otolemur and Nycticebus were very similar, and both had significantly higher dry matter (18.3, 16.3%), fat (7.6, 7.0%), and gross energy concentration (1.27, 1.13 kcal/g) than either lemuroid genus. Otolemur milk was higher in protein than Nycticebus milk. We conclude that lorises, bushbabies, and perhaps cheirogaleids produce relatively rich, energy‐dense milks in comparison with anthropoid primates. However, dilute milks appear to be uniformly found among species of Eulemur and perhaps in Lemur catta. The milk of Varecia (and perhaps Hapalemur) is intermediate in composition. Differences in milk composition among prosimians may be related to differences in maternal care: prosimians that carry their young during lactation produce more dilute milks than do species which leave their young unattended for prolonged periods. When looking at primates as a whole, however, the picture is somewhat less clear, since the milks of some “parkers” like Varecia do closely resemble those of large anthropoid primates who carry their young. Am. J. Primatol. 41:195–211, 1997.