Abstract
Lactation is the most energetically expensive period for female mammals and is associated with some of the highest sustained metabolic rates (SusMR) in vertebrates (reported as total energy throughput). Females typically deal with this energy demand by increasing food intake and the structure of the alimentary tract may act as the central constraint to ceilings on SusMR at about seven times resting or standard metabolic rate (SMR). However, demands of lactation may also be met by using a form of metabolic compensation such as reducing locomotor activities or entering torpor. In some phocid seals, cetaceans and bears, females fast throughout lactation and thus cannot offset the high energetic costs of lactation through increased food intake. We demonstrate that fasting grey seal females sustain, for several weeks, one of the highest total daily energy expenditures (DEE; 7.4 x SMR) reported in mammals, while progressively reducing maintenance metabolic expenditures during lactation through means not explained by reduction in lean body mass or behavioural changes. Simultaneously, the energy-exported in milk is progressively increased, associated with increased lipoprotein lipase activity in the mammary gland, resulting in greater offspring growth. Our results suggest that females use compensatory mechanisms to help meet the extraordinary energetic costs of lactation. Additionally, although the concepts of SusMR and ceilings on total DEE may be somewhat different in fasting lactating species, our data on phocid seals demonstrate that metabolic ceilings on milk energy output, in general, are not constrained by the same kind of peripheral limitations as are other energy-consuming tissues. In phocid seals, the high ceilings on DEE during lactation, coupled with metabolic compensation, are undoubtedly important factors enabling shortened lactation.
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Selected References
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- Baldwin R. L., Smith N. E., Taylor J., Sharp M. Manipulating metabolic parameters to improve growth rate and milk secretion. J Anim Sci. 1980 Dec;51(6):1416–1428. doi: 10.2527/jas1981.5161416x. [DOI] [PubMed] [Google Scholar]
- Bowen W. D., Iverson S. J. Estimation of total body water in pinnipeds using hydrogen-isotope dilution. Physiol Zool. 1998 May-Jun;71(3):329–332. doi: 10.1086/515921. [DOI] [PubMed] [Google Scholar]
- Cañas R., Romero J. J., Baldwin R. L. Maintenance energy requirements during lactation in rats. J Nutr. 1982 Oct;112(10):1876–1880. doi: 10.1093/jn/112.10.1876. [DOI] [PubMed] [Google Scholar]
- Guppy M., Fuery C. J., Flanigan J. E. Biochemical principles of metabolic depression. Comp Biochem Physiol B Biochem Mol Biol. 1994 Oct-Nov;109(2-3):175–189. doi: 10.1016/0305-0491(94)90001-9. [DOI] [PubMed] [Google Scholar]
- Hammond K. A., Diamond J. Maximal sustained energy budgets in humans and animals. Nature. 1997 Apr 3;386(6624):457–462. doi: 10.1038/386457a0. [DOI] [PubMed] [Google Scholar]
- Hammond K. A., Lloyd K. C., Diamond J. Is mammary output capacity limiting to lactational performance in mice? J Exp Biol. 1996 Feb;199(Pt 2):337–349. doi: 10.1242/jeb.199.2.337. [DOI] [PubMed] [Google Scholar]
- Illingworth P. J., Jung R. T., Howie P. W., Leslie P., Isles T. E. Diminution in energy expenditure during lactation. Br Med J (Clin Res Ed) 1986 Feb 15;292(6518):437–441. doi: 10.1136/bmj.292.6518.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kovacs A., Weber M. L., Burns L. J., Jacob H. S., Vercellotti G. M. Cytoplasmic sequestration of p53 in cytomegalovirus-infected human endothelial cells. Am J Pathol. 1996 Nov;149(5):1531–1539. [PMC free article] [PubMed] [Google Scholar]
- Mellish J. A., Iverson S. J., Don Bowen W. Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol Biochem Zool. 1999 Nov-Dec;72(6):677–690. doi: 10.1086/316708. [DOI] [PubMed] [Google Scholar]
- Milligan L. P. Energetic efficiency and metabolic transformations. Fed Proc. 1971 Jul-Aug;30(4):1454–1458. [PubMed] [Google Scholar]
- Peterson C. C., Nagy K. A., Diamond J. Sustained metabolic scope. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2324–2328. doi: 10.1073/pnas.87.6.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reilly J. J., Fedak M. A. Measurement of the body composition of living gray seals by hydrogen isotope dilution. J Appl Physiol (1985) 1990 Sep;69(3):885–891. doi: 10.1152/jappl.1990.69.3.885. [DOI] [PubMed] [Google Scholar]
- Rogowitz G. L. Limits to milk flow and energy allocation during lactation of the hispid cotton rat (Sigmodon hispidus). Physiol Zool. 1998 May-Jun;71(3):312–320. doi: 10.1086/515923. [DOI] [PubMed] [Google Scholar]
- Romero J. J., Cañas R., Baldwin R. L., Koong L. J. Lactational efficiency complex of rats: provisional model for interpretation of energy balance data. J Dairy Sci. 1976 Jan;59(1):57–67. doi: 10.3168/jds.S0022-0302(76)84156-2. [DOI] [PubMed] [Google Scholar]
- Trayhurn P. Decreased capacity for non-shivering thermogenesis during lactation in mice. Pflugers Arch. 1983 Aug;398(3):264–265. doi: 10.1007/BF00657164. [DOI] [PubMed] [Google Scholar]
- Trayhurn P., Douglas J. B., McGuckin M. M. Brown adipose tissue thermogenesis is 'suppressed' during lactation in mice. Nature. 1982 Jul 1;298(5869):59–60. doi: 10.1038/298059a0. [DOI] [PubMed] [Google Scholar]