Metabolic compensation during high energy output in fasting, lactating grey seals (Halichoerus grypus): Metabolic ceilings revisited

Proceedings of the Royal Society B: Biological Sciences

Volumn 267, Issue 1449, 2000, Pages 1245-1251

  Mellish, Jo Ann E ^a   Iverson, Sara J ^a   Bowen, W Don ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b BEDFORD INSTITUTE OF OCEANOGRAPHY   (Canada)

Author keywords

Energetic ceilings; Lactation; Metabolic compensation; Phocid seals

Indexed keywords

LIPOPROTEIN LIPASE;

ENERGETICS; LACTATION; METABOLISM; PINNIPED;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; DIET RESTRICTION; ENERGY EXPENDITURE; ENERGY METABOLISM; FEMALE; LACTATION; LEAN BODY WEIGHT; MALE; MAMMARY GLAND; METABOLIC RATE; MILK; NEWBORN; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; PROGENY; SEAL;

HALICHOERES GRYPUS;

EID: 0034702257     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2000.1134     Document Type: Article

References (51)

1. Baldwin, R. L. & Smith, N. E. 1974 Molecular control of energy metabolism. In The control of metabolism (ed. J. D. Sink), pp. 17-34. University Park, PA: Pennsylvania State University Press.
2. Baldwin, R. L., Smith, N. E., Taylor, J. & Sharp, M. 1980 Manipulating metabolic parameters to improve growth rate and milk secretion. J. Anim. Sci. 51, 1416-1428.
3. Blaxter, K. 1989 Energy metabolism in animals and man. Cambridge University Press.
4. Boily, P. & Lavigne, D. M. 1997 Developmental and seasonal changes in resting metabolic rates of captive female grey seals. Can. J. Zool. 75, 1781-1789.
5. Boness, D. J., Bowen, W. D. & Iverson, S. J. 1995 Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance? Behav. Ecol. Sociobiol. 36, 1-10.
6. Bowen, W. D. 1991 Behavioural ecology of pinniped neonates. In Behaviour of pinnipeds (ed. D. Renouf). pp. 66-127. London: Chapman & Hall.
7. Bowen, W. D. & Iverson, S. J. 1998 Estimation of total body water in pinnipeds using hydrogen-isotope dilution. Physiol. Zool. 71, 329-332.
8. Canas, R., Romero, J. J. & Baldwin, R. L. 1982 Maintenance energy requirements during lactation in rats. J. Nutr. 112, 1876-1880.
9. Costa, D. P., LeBoeuf, B. J., Huntley, A. C. & Ortiz, C. L. 1986 The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J. Zool. Lond. 209, 21-33.
10. Fedak, M. A. & Anderson, S. S. 1982 The energetics of lactation: accurate measurements from a large wild mammal, the grey seal (Halichoerus grypus). J. Zool. Lond. 198, 473-479.
11. Geiser, F. & Masters, P. 1994 Torpor in relation to reproduction in the mulgara, Dasycercus cristicauda (Dasyuridae: Marsupialia). J. Therm. Biol. 19, 33-40.
12. Gittleman, J. L. & Thompson, S. D. 1988 Energy allocation in mammalian reproduction. Am. Zool. 28, 863-875.
13. Guppy, M., Fuery, C. J. & Flanigan, J. E. 1994 Biochemical principles of metabolic depression. Comp. Biochem. Physiol. B 109, 175-189.
14. Haller, M. A., Kovacs, K. M. & Hammill, M. O. 1996 Maternal behaviour and energy investment by grey seals (Halichoerus grypus) breeding on land-fast ice. Can. J. Zool. 74, 1531-1541.
15. Hammond, K. A. & Diamond, J. 1992 An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiol. Zool. 65, 952-977.
16. Hammond, K. A. & Diamond, J. 1997 Maximal sustained energy budgets in humans and animals. Nature 386, 457-462.
17. Hammond, K. A., Lloyd, K. C. K. & Diamond, J. 1996 Is mammary output capacity limiting to lactational performance in mice? J. Exp. Biol. 199, 337-349.
18. Illingworth, P. J., Jung, R. T., Howie, P. W., Leslie, P. & Isles, T. E. 1986 Diminution in energy expenditure during lactation. Br. Med. J. 292, 437-441.
19. Iverson, S. J. 1993 Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symp. Zool. Soc. Lond. 66, 263-291.
20. Iverson, S. J., Bowen, W. D., Boness, D. J. & Oftedal, O. T. 1993 The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol. Zool. 66, 61-88.
21. Iverson, S. J., Hamosh, M. & Bowen, W. D. 1995a Lipoprotein lipase activity and its relationship to high milk transfer during lactation in grey seals. J. Comp. Physiol. B 165, 384-395.
22. Iverson, S. J., Oftedal, O. T., Bowen, W. D., Boness, D. J. & Sampugna, J. 1995b Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal. J. Comp. Physiol. B 165, 1-12.
23. Kenagy, G. J., Masman, D., Sharbaugh, S. M. & Nagy, K. A. 1990 Energy expenditure during lactation in relation to litter size in free-living golden-mantled ground squirrels. J. Anim. Ecol. 59, 73-88.
24. Kleiber, M. 1975 The fire of life: an introduction to animal energetics. New York: Kreiger Publishing Co.
25. Lavigne, D. M., Innes, S., Worthy, G. A. J., Kovacs, K. M., Schmitz, O. J. & Hickie, J. P. 1986 Metabolic rates of seals and whales. Can. J. Zool. 64, 279-284.
26. McClean, J. A. & Speakman, J. R. 1999 Energy budgets of lactating and non-reproductive brown long-cared bats (Plecotus auritus) suggests females use compensation in lactation. Funct. Ecol. 13, 360-372.
27. Mellish, J. E. 1999 Physiology of milk fat secretion and neonatal fat deposition during lactation in phocid seals. PhD thesis, Dalhousie University, Halifax, Nova Scotia.
28. Mellish, J. E., Iverson, S. J. & Bowen,W. D. 1999a Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol. Biochem. Zool. 67, 677-690.
29. Mellish, J. E., Iverson, S. J., Bowen, W. D. & Hammill, M. O. 1999b Fat transfer and energetics during lactation in the hooded seal: the roles of tissue lipoprotein lipase in milk fat secretion and pup blubber deposition. J. Comp. Physiol. B 169, 377-390.
30. Milligan, L. P. 1971 Energetic efficiency and metabolic transformations. Fed. Proc. 30, 1454-1458.
31. Oftedal, O. T. 1984 Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. Lond. 51, 33-85.
32. Oftedal, O. T. & Iverson, S. J. 1987 Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling seals. In Approaches to marine mammal energetics (ed. A. C. Huntley, D. P. Costa, G. A. J. Worthy & M. Castellini), pp. 67-96. Lawrence, KS: Allen Press.
33. Ortiz, C. L., Costa, D. P. & LeBoeuf, B. J. 1978 Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool. 51, 166-178.
34. Peterson, C. C., Nagy, K. A. & Diamond, J. M. 1990 Sustained metabolic scope. Proc. Natl Acad. Sci. USA 87, 2324-2328.
35. Poppitt, S. D., Speakman, J. R. & Racey, P. A. 1993 The energetics of reproduction in the common shrew (Sorex araneus): a comparison of indirect calorimetry and the doubly labeled water method. Physiol. Zool. 66, 964-982.
36. Racey, P. A. & Speakman, J. R. 1987 The energy costs of pregnancy and lactation in heterothermic bats. Symp. Zool. Soc. Lond. 57, 107-125.
37. Reilly, J. J. & Fedak, M. A. 1990 Measurement of the body composition of living gray seals by hydrogen isotope dilution. J. Appl. Physiol. 69, 885-891.
38. Reilly, J. J., Fedak, M. A., Thomas, D. H., Coward, W. A. A. & Anderson, S. S. 1996 Water balance and the energetics of lactation in grey seals (Halichoerus grypus) as studied by isotopically labeled water methods. J. Zool. Lond. 238, 157-165.
39. Ricklefs, R. E., Konarzewski, M. & Daan, S. 1996 The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am. Nat. 147, 1047-1071.
40. Rogowitz, G. L. 1998 Limits to milk flow and energy allocation during lactation of the hispid cotton rat (Sigmodon hispidus). Physiol. Zool. 71, 312-320.
41. Romero, J. J., Canas, R., Baldwin, R. L. & Koong, L. J. 1976 Lactational efficiency complex of rats: provisional model for interpretation of energy balance data. J. Dairy Sci. 59, 57-67.
42. Slonaker, J. R. 1924 The effect of copulation, pregnancy, pseudopregnancy and lactation on the voluntary activity and food consumption of the albino rat. Am. J. Physiol. 71, 362.
43. Speakman, J. R. 1997 Doubly labelled water: theory and practice. London: Chapman & Hall.
44. Speakman, J. R. & McQueenie, J. 1996 Limits to sustained metabolic rate: the link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus. Physiol. Zool. 69, 746-769.
45. Stirling, I. 1983 The evolution of mating systems in pinnipeds. In Advances in the study of mammalian behavior (ed. J. F. Eisenberg & D. G. Kleiman), pp. 489-527. Shippensburg, PA: American Society of Mammalogists Special Publication no. 7.
46. Thompson, S. D. 1993 Gestation and lactation in small mammals: basal metabolic rate and the limits to energy use. In Mammalian energetics: interdisciplinary views of metabolism and reproduction (ed. T. E. Tomasi & T. H. Horton), pp. 213-260. New York: Comstock.
47. Trayhurn, P. 1983 Decreased capacity for non-shivering thermogenesis during lactation in mice. Pflügers Arch. 398, 264-265.
48. Trayhurn, P., Douglas, J. B. & McGulkin, M. M. 1982 Brown adipose tissue thermogenesis is 'suppressed' during lactation in mice. Nature 298, 59-60.
49. Wang, G. H. 1924 The changes in the amount of daily food intake of the albino rat during pregnancy and lactation. Am. J. Physiol. 71, 735-741.
50. Weiner, J. 1989 Metabolic constraints to mammalian energy budgets. Acta Ther. 34, 3-35.
51. Williams, J. D. 1995 Fasting and lactation in female northern elephant seals (Mirounga angustirostris): reconciling conflicting energetic and nutritional demands. PhD thesis, University of California at Santa Cruz, USA.