Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T19:43:55.109Z Has data issue: false hasContentIssue false
  • English
  • Français

Use of maternal reserves as a lactation strategy in large mammals

Published online by Cambridge University Press:  03 March 2008

Olav T. Oftedal
Olav T. Oftedal*
Affiliation:
Nutrition Laboratories, Department of Zoological Research, National Zoological Park, Smithsonian Institution, Washington, DC 20008, USA
*
*Corresponding author: Dr Olav T. Oftedal, fax +1 202 673 4686, email ooftedal@nzp.si.edu
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

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.

Keywords

LactationFastingMilk compositionSealsBearsWhales
Type
Animal Nutrition and Metabolism Group Symposium on ‘Regulation of maternal reserves and effects on lactation and the nutrition of young animals’
Information
Proceedings of the Nutrition Society , Volume 59 , Issue 1 , February 2000 , pp. 99 - 106
Copyright
Copyright © The Nutrition Society 2000

References

Agricultural Research Council (1980) The Nutrient Requirements of Ruminant Livestock. Slough, Berks: Commonwealth Agricultural Bureaux.Google Scholar
Ando, K, Mori, M, Kato, I, Yusa, K & Goda, K (1979) General composition and chemical properties of the main components of Yeso brown bear (Ursus arctos yesoensis) milks. Journal of the College of Dairying 8, 9–21.Google Scholar
Arnould, JPY (1997) Lactation and the cost of pup-rearing in Antarctic fur seals. Marine Mammal Science 13, 516–526.CrossRefGoogle Scholar
Arnould, JPY & Boyd, IL (1995a) Inter- and intra-annual variation in milk composition in Antarctic fur seals (Arctocephalus gazella). Physiological Zoology 68, 1164–1180.CrossRefGoogle Scholar
Arnould, JPY & Boyd, IL (1995b) Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). Journal of Zoology, London 237, 1–12.CrossRefGoogle Scholar
Arnould, JPY, Boyd, IL & Socha, DG (1996a) Milk consumption and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups. Canadian Journal of Zoology 74, 254–266.CrossRefGoogle Scholar
Arnould, JPY, Boyd, IL & Speakman, JR (1996b) Measuring the body composition of Antarctic fur seals (Arctocephalus gazella): Validation of hydrogen isotope dilution. Physiological Zoology 69, 93–116.CrossRefGoogle Scholar
Arnould, JPY & Ramsay, MA (1994) Milk production and milk consumption in polar bears during the ice-free period in western Hudson Bay. Canadian Journal of Zoology 72, 1365–1370.CrossRefGoogle Scholar
Atkinson, SN & Ramsay, MA (1995) The effects of prolonged fasting on the body composition and reproductive success of female polar bears (Ursus maritimus). Functional Ecology 9, 559–567.CrossRefGoogle Scholar
Beck, GG, Smith, TG & Hammill, MO (1993) Evaluation of body condition in the northwest Atlantic harp seal (Phoca groenlandica). Canadian Journal of Fisheries and Aquatic Sciences 50, 1372–1381.CrossRefGoogle Scholar
Bell, AW & Bauman, DE (1997) Adaptations of glucose metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia 2, 265–278.CrossRefGoogle ScholarPubMed
Boness, DJ & Bowen, WD (1996) The evolution of maternal care in pinnipeds. Bioscience 46, 645–654.CrossRefGoogle Scholar
Boness, DJ, Bowen, WD & Oftedal, OT (1994) Evidence of a maternal foraging cycle resembling that of otariid seals in a small phocid, the harbor seal. Behavioral Ecology and Sociobiology 34, 95–104.CrossRefGoogle Scholar
Bowen, WD (1991) Behavioural ecology of pinniped neonates. In Behaviour of Pinnipeds, pp. 66–127 [D, Renouf, editor]. London: Chapman and Hall.CrossRefGoogle Scholar
Bowen, WD, Boness, DJ & Oftedal, OT (1987) Mass transfer from mother to pup and subsequent mass loss by the weaned pup of the hooded seal, Cystophora cristata. Canadian Journal of Zoology 65, 1–8.CrossRefGoogle Scholar
Bowen, WD, Oftedal, OT & Boness, DJ (1992) Mass and energy transfer during lactation in a small phocid, the harbor seal (Phoca vitulina). Physiological Zoology 65, 844–866.CrossRefGoogle Scholar
Carl, GR & Robbins, CT (1988) The energetic cost of predator avoidance in neonatal ungulates: hiding versus following. Canadian Journal of Zoology 66, 239–246.CrossRefGoogle Scholar
Costa, DP (1991) Reproductive and foraging energetics of pinnipeds: implications for life history patterns. In Behaviour of Pinnipeds, pp. 300–344 [D, Renouf, editor]. London: Chapman and Hall.CrossRefGoogle Scholar
Costa, DP, LeBoeuff, BJ, Huntley, AC & Ortiz, CL (1986) The energetics of lactation in the northern elephant seal Mirounga angustirostris. Journal of Zoology, London 209, 21–33.CrossRefGoogle Scholar
Cripps, AW & Williams, VJ (1975) The effect of pregnancy and lactation on food intake, gastrointestinal anatomy and the absorptive capacity of the small intestine in the albino rat. British Journal of Nutrition 33, 17–32.CrossRefGoogle ScholarPubMed
Derocher, AE, Andriashek, D & Arnould, JPY (1993) Aspects of milk composition and lactation in polar bears. Canadian Journal of Zoology 71, 561–567.CrossRefGoogle Scholar
Dosako, S, Taneya, S, Kimura, T, Ohmori, T, Daikoku, H, Suzuki, N, Sawa, J, Kano, K & Katayama, S (1983) Milk of northern fur seal: composition, especially carbohydrate and protein. Journal of Dairy Science 66, 2076–2083.CrossRefGoogle ScholarPubMed
Farley, SD & Robbins, CT (1995) Lactation, hibernation and mass dynamics of American black bears and grizzly bears. Canadian Journal of Zoology 73, 2216–2222.CrossRefGoogle Scholar
Forsyth, DJ (1976) A field study of growth and development of nestling masked shrews (Sorex cinereus). Journal of Mammalogy 57, 708–721.CrossRefGoogle ScholarPubMed
Gittleman, JL & Oftedal, OT (1987) Comparative growth and lactation energetics in carnivores. Symposia of the Zoological Society of London 57, 41–77.Google Scholar
Hammond, K & Diamond, J (1994) Limits to dietary nutrient intake and intestinal nutrient uptake in lactating mice. Physiological Zoology 67, 282–303.CrossRefGoogle Scholar
Hilderbrand, GV, Farley, SD & Robbins, CT (1998) Predicting body condition of bears via two field methods. Journal of Wildlife Management 62, 406–409.CrossRefGoogle Scholar
Hudson, RJ & Christopherson, RJ (1985) Maintenance metabolism. In Bioenergetics of Wild Herbivores, pp. 121–142 [RJ, Hudson and RG, White, editors]. Boca Raton, FL: CRC Press.Google Scholar
Iverson, SJ, Bowen, WD, Boness, DJ & Oftedal, OT (1993) The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiological Zoology 66, 61–88.CrossRefGoogle Scholar
Iverson, SJ & Oftedal, OT (1992) Fatty acid composition of black bear (Ursus americanus) milk during and after the period of winter dormancy. Lipids 27, 940–943.CrossRefGoogle ScholarPubMed
Iverson, SJ, Oftedal, OT, Bowen, WD, Boness, DJ & Sampugna, J (1995) Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal. Journal of Comparative Physiology 165B, 1–12.CrossRefGoogle ScholarPubMed
Jenness, R, Erickson, AW & Craighead, JJ (1972) Some comparative aspects of milk from four species of bears. Journal of Mammalogy 53, 34–47.CrossRefGoogle ScholarPubMed
Johnson, JD (1975) Comparative aspects of lactose digestion and synthesis in mammals – the California sea lion. Modern Problems in Paediatrics 15, 194–200.Google Scholar
Kretzmann, MB, Costa, DP, Higgins, LV & Needham, DJ (1991) Milk composition of Australian sea lions, Neophoca cinerea: variability in lipid content. Canadian Journal of Zoology 69, 2556–2561.CrossRefGoogle Scholar
Linzell, JL (1968) The magnitude and mechanism of the uptake of milk precursors by the lactating mammary gland. Proceedings of the Nutrition Society 27, 44–52.CrossRefGoogle Scholar
Linzell, JL (1972) Milk yield, energy loss in milk, and mammary gland weight in different species. Dairy Science Abstracts 34, 351–360.Google Scholar
Lockyer, C (1981) Growth and energy budgets of large baleen whales from the southern hemisphere. Mammals in the Seas. FAO Fisheries Series no. 5, Vol. 3, pp. 379–487.Rome: FAO.Google Scholar
Lockyer, C (1984) Review of baleen whale (Mysticeti) reproduction and implications for management. Reports of the International Whaling Commission, special issue 6, pp. 27–50.Cambridge: International Whaling Commission.Google Scholar
Loveridge, GG (1986) Bodyweight changes and energy intake of cats during gestation and lactation. Animal Technologist 37, 7–15.Google Scholar
Lydersen, C & Hammill, MO (1993) Activity, milk intake and energy consumption in free-living ringed seal (Phoca hispida) pups. Journal of Comparative Physiology 163B, 413–438.Google ScholarPubMed
Lydersen, C, Hammill, MO & Kovacs, KM (1995) Milk intake, growth and energy consumption in pups of ice-breeding grey seals (Halichoerus grypus) from the Gulf of St. Lawrence, Canada. Journal of Comparative Physiology 164B, 585–592.CrossRefGoogle Scholar
Lydersen, C & Kovacs, KM (1996) Energetics of lactation in harp seals (Phoca groenlandica) from the Gulf of St. Lawrence, Canada. Journal of Comparative Physiology 166B, 295–304.CrossRefGoogle Scholar
Lydersen, C, Kovacs, KM & Hammill, MO (1997) Energetics during nursing and early postweaning fasting in hooded seal (Cystophora cristata) pups from the Gulf of St Lawrence, Canada. Journal of Comparative Physiology 167B, 81–88.CrossRefGoogle Scholar
Lydersen, C, Kovacs, KM, Hammill, MO & Gjertz, I (1996) Energy intake and utilisation by nursing bearded seal (Erignathus barbatus) pups from Svalbard, Norway. Journal of Comparative Physiology 166B, 405–411.CrossRefGoogle ScholarPubMed
Muelbert, MMC & Bowen, WD (1993) Duration of lactation and postweaning changes in mass and body composition of harbour seal, Phoca vitulina, pups. Canadian Journal of Zoology 71, 1405–1414.CrossRefGoogle Scholar
Oftedal, OT (1984) Milk composition, milk yield and energy output at peak lactation: a comparative review. Symposia of the Zoological Society of London 51, 33–85.Google Scholar
Oftedal, OT (1985) Pregnancy and lactation. In The Bioenergetics of Wild Herbivores, pp. 215–238 [RJ, Hudson and RG, White, editors]. Boca Raton, FL: CRC Press.Google Scholar
Oftedal, OT (1993) The adaptation of milk secretion to the constraints of fasting in bears, seals and baleen whales. Journal of Dairy Science 76, 3234–3246.CrossRefGoogle Scholar
Oftedal, OT (1997) Lactation in whales and dolphins: Evidence of divergence between baleen- and toothed-species. Journal of Mammary Gland Biology and Neoplasia 2, 205–230.CrossRefGoogle ScholarPubMed
Oftedal, OT, Alt, GL, Widdowson, EM & Jakubasz, MR (1993a) Nutrition and growth of suckling black bears (Ursus americanus) during their mothers' winter fast. British Journal of Nutrition 70, 59–79.CrossRefGoogle ScholarPubMed
Oftedal, OT, Boness, DJ & Bowen, WD (1988) The composition of hooded seal (Cystophora cristata) milk: an adaptation for postnatal fattening. Canadian Journal of Zoology 66, 318–322.CrossRefGoogle Scholar
Oftedal, OT, Boness, DJ & Tedman, RA (1987a) The behavior, physiology, and anatomy of lactation in the Pinnipedia. Current Mammalogy 1, 175–245.CrossRefGoogle Scholar
Oftedal, OT, Bowen, WD & Boness, DJ (1993b) Energy transfer by lactating hooded seals, and nutrient deposition in their pups, during the four days from birth to weaning. Physiological Zoology 66, 412–435.CrossRefGoogle Scholar
Oftedal, OT, Bowen, WD & Boness, DJ (1996) Lactation performance and nutrient deposition in pups of the harp seal, Phoca groenlandica, on ice floes off southeast Labrador. Physiological Zoology 69, 635–657.CrossRefGoogle Scholar
Oftedal, OT, Bowen, WD, Widdowson, EM & Boness, DJ (1989) Effects of suckling and the postsuckling fast on weights of the body and internal organs of harp and hooded seal pups. Biology of the Neonate 56, 283–300.CrossRefGoogle ScholarPubMed
Oftedal, OT, Hintz, HF & Schryver, HF (1983) Lactation in the horse: milk composition and intake by foals. Journal of Nutrition 113, 2096–2106.CrossRefGoogle ScholarPubMed
Oftedal, OT & Iverson, SJ (1995) Phylogenetic variation in the gross composition of milks. In Handbook of Milk Composition, pp. 749–789 [RG, Jensen, editor]. New York: Academic Press.CrossRefGoogle Scholar
Oftedal, OT, Iverson, SJ & Boness, DJ (1987b) Milk and energy intakes of suckling California sea lion Zalophus californianus pups in relation to sex, growth, and predicted maintenance requirements. Physiological Zoology 60, 560–575.CrossRefGoogle Scholar
Owen-Smith, RN (1988) Megaherbivores: The Influence of Very Large Body Size on Ecology. New York: Cambridge University Press.CrossRefGoogle Scholar
Pan, W, Oftedal, OT, Zhu, X, Childs, S, Wang, D & Kleiman, DG (1998) Milk composition and nursing in a giant panda (Ailuropoda melanoleuca). Acta Scientarium Naturalium Universitatis Pekinensis 34, 350–351.Google Scholar
Pilson, MEQ & Kelly, AL (1962) Composition of the milk from Zalophus californianus, the California sea lion. Science 135, 104–105.CrossRefGoogle ScholarPubMed
Ramsay, MA & Dunbrack, RL (1986) Physiological constraints on life history phenomena: the example of small bear cubs at birth. American Naturalist 127, 735–743.CrossRefGoogle Scholar
Reese, EO & Robbins, CT (1994) Characteristics of moose lactation and neonatal growth. Canadian Journal of Zoology 72, 953–957.CrossRefGoogle Scholar
Reilly, JJ & Fedak, MA (1990) Measurement of the body composition of living gray seals by hydrogen isotope dilution. Journal of Applied Physiology 69, 885–891.CrossRefGoogle ScholarPubMed
Ryg, M, Smith, TG & Oritsland, NA (1990) Seasonal changes in body mass and body composition of ringed seals (Phoca hispida) on Svalbard. Canadian Journal of Zoology 68, 470–475.CrossRefGoogle Scholar
Scheffer, VB (1962) Pelage and Surface Topography of the Northern Fur Seal. North American Fauna no. 64.Washington, DC: US Fish Wildlife Service.Google Scholar
Shennan, DB (1998) Mammary gland membrane transport systems. Journal of Mammary Gland Biology and Neoplasia 3, 247–258.CrossRefGoogle ScholarPubMed
Swartz, SL (1986) Gray whale migratory, social and breeding behavior. Reports of the International Whaling Commission, special issue 8, pp. 207–229.Cambridge: International Whaling Commission.Google Scholar
Tedman, R & Green, B (1987) Water and sodium fluxes and lactational energetics in suckling pups of Weddell seals (Leptonychotes weddellii). Journal of Zoology, London 212, 29–42.CrossRefGoogle Scholar
Thompson, SD, Ono, KA, Oftedal, OT & Boness, DJ (1987) Thermoregulation and resting metabolic rate of California sea lion (Zalophus californianus) pups. Physiological Zoology 60, 730–736.CrossRefGoogle Scholar
Tønnessen, JN & Johnsen, AO (1982) The History of Modern Whaling. Berkeley, CA: University of California Press.Google Scholar
Urashima, T, Kusaka, Y, Nakamura, T, Saito, T, Maeda, M & Messer, M (1997) Chemical characterization of milk oligosaccharides of the brown bear, Ursus arctos yesoensis. Biochimica et Biophysica Acta 1334, 247–255.CrossRefGoogle ScholarPubMed
Vernon, RG & Pond, CM (1997) Adaptations of maternal adipose tissue to lactation. Journal of Mammary Gland Biology and Neoplasia 2, 231–241.CrossRefGoogle ScholarPubMed
White, RG & Luick, JR (1984) Plasticity and constraints in the lactational strategy of reindeer and caribou. Symposia of the Zoological Society of London 51, 215–232.Google Scholar
Williamson, DH, Lund, P & Evans, RD (1995) Substrate selection and oxygen uptake by the lactating mammary gland. Proceedings of the Nutrition Society 54, 165–175.CrossRefGoogle ScholarPubMed