Limits to sustained energy intake. X. Effects of fur removal on reproductive performance in laboratory mice

Journal of Experimental Biology

Volumn 210, Issue 23, 2007, Pages 4233-4243

  Król, Elzbieta ^a   Murphy, Michelle ^a   Speakman, John R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Daily energy expenditure; Digestive efficiency; Heat dissipation limit; Lactation; Metabolizable energy intake; Milk production; Pup energy content

Indexed keywords

WATER;

ANIMAL; ARTICLE; BODY WEIGHT; CALORIC INTAKE; DIGESTION; ENERGY METABOLISM; FEEDING BEHAVIOR; FEMALE; HAIR; ISOTOPE LABELING; LACTATION; MILK; MOUSE; NEWBORN; PHYSIOLOGY; REPRODUCTION;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; DIGESTION; ENERGY INTAKE; ENERGY METABOLISM; FEEDING BEHAVIOR; FEMALE; HAIR; ISOTOPE LABELING; LACTATION; MICE; MILK; REPRODUCTION; WATER;

ANIMALIA; AVES; MUS;

EID: 38349051288     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.009779     Document Type: Article

References (99)

1. Agius, L. and Williamson, D. H. (1980). Lipogenesis in interscapular brown adipose tissue of virgin, pregnant and lactating rats. The effects of intragastric feeding. Biochem. J. 190, 477-480.
2. Anderson, K. J. and Jetz, W. (2005). The broad-scale ecology of energy expenditure of endotherms. Ecol. Lett. 8, 310-318.
3. Baldwin, R. L., Smith, N. E., Taylor, J. and Sharp, M. (1980). Manipulating metabolic parameters to improve growth rate and milk secretion. J. Anim. Sci. 51, 1416-1428.
4. Barnett, S. A. (1959). The skin and hair of mice living at low environmental temperature. J. Exp. Physiol. 44, 35-42.
5. Berteaux, D., Thomas, D. W., Bergeron, J.-M. and Lapierre, H. (1996). Repeatability of daily field metabolic rate in female Meadow Voles (Microtus pennsylvanicus). Funct. Ecol. 10, 751-759.
6. Biggerstaff, S. and Mann, M. (1992). Consummatory behaviors and weight regulation in pregnant, lactating, and pregnant-lactating mice. Physiol. Behav. 52, 485-491.
7. Blaxter, K. (1989). Energy Metabolism in Animals and Man. Cambridge: Cambridge University Press.
8. Bohning-Gaese, K., Halbe, B., Lemoine, N. and Oberrath, R. (2000). Factors influencing the clutch size, number of broods and annual fecundity of North American and European land birds. Evol. Ecol. Res. 2, 823-839.
9. Conley, K. E. and Porter, W. P. (1980). Heat loss from deer mice (Peromyscus): evaluation of seasonal limits to thermoregulation. J. Exp. Biol. 126, 249-269.
10. Cooper, C. B., Hochachka, W. M., Butcher, G. and Dhondt, A. A. (2005). Seasonal and latitudinal trends in clutch size: thermal constraints during laying and incubation. Ecology 86, 2018-2031.
11. Coward, W. A. and Prentice, A. M. (1985). Isotope method for the measurement of carbon dioxide production rate in man. Am. J. Clin. Nutr. 41, 659-661.
12. Croskerry, P. G., Smith, G. K. and Leon, M. (1978). Thermoregulation and the maternal behaviour of the rat. Nature 273, 299-300.
13. Drent, R. H. and Daan, S. (1980). The prudent parent: energetic adjustments in avian breeding. Ardea 68, 225-252.
14. Drozdz, A. (1975). Metabolic cages for small mammals. In Methods for Ecological Bioenergetics, International Biological Programme Handbook No. 24 (ed. W. Grodzinski, R. Z. Klekowski and A. Duncan), pp. 346-351. Oxford: Blackwell Scientific Publications.
15. Freetly, H. C., Nienaber, J. A. and Brown-Brandl, T. (2006). Partitioning of energy during lactation of primiparous beef cows. J. Anim. Sci. 84, 2157-2162.
16. Hammel, H. T. (1955). Thermal properties of fur. Am. J. Physiol. 182, 369-376.
17. Hammond, K. A. and Diamond, J. (1992). An experimental test for a ceiling on sustained metabolic rate in lactating mice. Physiol. Zool. 65, 952-977.
18. Hammond, K. A. and Diamond, J. (1994). Limits to dietary nutrient intake and intestinal nutrient uptake in lactating mice. Physiol. Zool. 67, 282-303.
19. Hammond, K. A. and Diamond, J. (1997). Maximum sustained energy budgets in humans and animals. Nature 386, 457-462.
20. Hammond, K. A. and Kristan, D. M. (2000). Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol. Biochem. Zool. 73, 547-556.
21. Hammond, K. A., Konarzewski, M., Torres, R. M. and Diamond, J. (1994). Metabolic ceilings under a combination of peak energy demands. Physiol. Zool. 67, 1479-1506.
22. Hammond, K. A., Lloyd, K. C. K. and Diamond, J. (1996). Is mammary output capacity limiting to lactational performance in mice? J. Exp. Biol. 199, 337-349.
23. Hart, J. S. (1956). Seasonal changes in insulation of the fur. Can. J. Zool. 34, 53-57.
24. Hayes, J. P., Speakman, J. R. and Racey, P. A. (1992). The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis). Physiol. Zool. 65, 742-762.
25. Heldmaier, G. (1974). Temperature adaptation and brown adipose tissue in hairless and albino mice. J. Comp. Physiol. 92, 281-292.
26. Humphries, M. M., Thomas, D. W. and Speakman, J. R. (2002). Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418, 313-316.
27. Jacobsen, N. K. (1980). Differences in thermal properties of white-tailed deer pelage between seasons and body regions. J. Therm. Biol. 5, 151-158.
28. Johnson, M. S. and Speakman, J. R. (2001). Limits to sustained energy intake. V. Effect of cold-exposure during lactation in Mus musculus. J. Exp. Biol. 204, 1967-1977.
29. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001a). Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus. J. Exp. Biol. 204, 1925-1935.
30. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001b). Limits to sustained energy intake. II. Inter-relationships between resting metabolic rate, life-history traits and morphology in Mus musculus. J. Exp. Biol. 204, 1937-1946.
31. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001c). Limits to sustained energy intake. III. Effects of concurrent pregnancy and lactation in Mus musculus. J. Exp. Biol. 204, 1947-1956.
32. Kauffman, A. S., Cabrera, A. and Zucker, I. (2001a). Torpor characteristics and energy requirements of furless Siberian hamsters. Physiol. Biochem. Zool. 74, 876-884.
33. Kauffman, A. S., Cabrera, A. and Zucker, I. (2001b). Energy intake and fur in summer- and winter-acclimated Siberian hamsters (Phodopus sungorus). Am. J. Physiol. 281, R519-R527.
34. Kauffman, A. S., Paul, M. J., Butler, M. P. and Zucker, I. (2003). Huddling, locomotor, and nest-building behaviors of furred and furless Siberian hamsters. Physiol. Behav. 79, 247-256.
35. Kauffman, A. S., Paul, M. J. and Zucker, I. (2004). Increased heat loss affects hibernation in golden-mantled ground squirrels. Am. J. Physiol. 287, R167-R173.
36. Kenagy, G. J. and Pearson, O. P. (2000). Life with fur and without: experimental field energetics and survival of naked meadow voles. Oecologia 122, 220-224.
37. Kenagy, G. J., Stevenson, R. D. and Masman, D. (1989). Energy requirements for lactation and postnatal growth in captive golden-mantled ground squirrels. Physiol. Zool. 62, 470-487.
38. Kirkwood, J. K. (1983). A limit to metabolisable energy intake in mammals and birds. Comp. Biochem. Physiol. 75, 1-3.
39. Klaassen, M. (1996). Metabolic constraints on long-distance migration in birds. J. Exp. Biol. 199, 57-64.
40. Knight, F. M. (1987). The development of pelage insulation and its relationship to homeothermic ability in an altricial rodent, Peromyscus leucopus. Physiol. Zool. 60, 181-190.
41. Koiter, T. R., Moes, H., Valkhof, N. and Wijkstra, S. (1999). Interaction of late pregnancy and lactation in rats. J. Reprod. Fertil. 115, 341-347.
42. Koteja, P. (1996). Limits to the energy budget in a rodent, Peromyscus maniculatus: the central limitation hypothesis. Physiol. Zool. 69, 981-993.
43. Król, E. and Speakman, J. R. (1999). Isotope dilution spaces of mice injected simultaneously with deuterium, tritium and oxygen-18. J. Exp. Biol. 202, 2839-2849.
44. Król, E. and Speakman, J. R. (2003a). Limits to sustained energy intake. VI. Energetics of lactation in laboratory mice at thermoneutrality. J. Exp. Biol. 206, 4255-4266.
45. Król, E. and Speakman, J. R. (2003b). Limits to sustained energy intake. VII. Milk energy output in laboratory mice at thermoneutrality. J. Exp. Biol. 206, 4267-4281.
46. Król, E., Johnson, M. S. and Speakman, J. R. (2003). Limits to sustained energy intake. VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality. J. Exp. Biol. 206, 4283-4291.
47. Künkele, J. (2000). Effects of litter size on the energetics of reproduction in a highly precocial rodent, the guinea pig. J. Mammal. 81, 691-700.
48. Laurien-Kehnen, C. and Trillmich, F. (2003). Lactation performance of guinea pigs (Cavia porcellus) does not respond to experimental manipulation of pup demands. Behav. Ecol. Sociobiol. 53, 145-152.
49. Leon, M., Croskerry, P. G. and Smith, G. K. (1978). Thermal control of mother-young contact in rats. Physiol. Behav. 21, 793-811.
50. Leon, M., Adels, L. and Coopersmith, R. (1985). Thermal limitation of mother-young contact in Norway rats. Dev. Psychobiol. 18, 85-105.
51. Léger, J. and Larochelle, J. (2006). On the importance of radiative heat exchange during nocturnal flight in birds. J. Exp. Biol. 209, 103-114.
52. Lifson, N. and McClintock, R. (1966). Theory of use of the turnover rates of body water for measuring energy and material balance. J. Theor. Biol. 12, 46-74.
53. 18. J. Appl. Physiol. 7, 704-710.
54. McDonald, J. M. and Nielsen, M. K. (2006). Correlated responses in maternal performance following divergent selection for heat loss in mice. J. Anim. Sci. 84, 300-304.
55. Meijer, H. A. J., Neubert, R. E. M. and Visser, G. H. (2000). Cross contamination in dual inlet isotope ratio mass spectrometers. Int. J. Mass Spectrom. 198, 45-61.
56. Morrison, P. R. and Tietz, W. J. (1957). Cooling and conductivity in three small Alaskan mammals. J. Mammal. 38, 78-86.
57. Mount, L. E. (1971). Metabolic rate and thermal insulation in albino and hairless mice. J. Physiol. Lond. 217, 315-326.
58. 18O) Method: A Guide to its Use (UCLA Publication no. 12-1417). Los Angeles, CA: University of California.
59. Nielsen, M. K., Jones, L. D., Freking, B. A. and DeShazer, J. A. (1997a). Divergent selection for heat loss in mice: I. Selection applied and direct response through fifteen generations. J. Anim. Sci. 75, 1461-1468.
60. Nielsen, M. K., Freking, B. A., Jones, L. D., Nelson, S. M., Vorderstrasse, T. L. and Hussey, B. A. (1997b). Divergent selection for heat loss in mice: II. Correlated responses in feed intake, body mass, body composition, and number born through fifteen generations. J. Anim. Sci. 75, 1469-1476.
61. Nizielski, S. E., Billington, C. J. and Levine, A. S. (1993). BAT thermogenic activity and capacity are reduced during lactation in ground squirrels. Am. J. Physiol. 264, R16-R21.
62. Parry, G. D. (1983). The influence of the cost of growth on ectotherm metabolism. J. Theor. Biol. 101, 453-477.
63. Pearson, O. P. (1960a). The oxygen consumption and bioenergetics of harvest mice. Physiol. Zool. 33, 152-160.
64. Pearson, O. P. (1960b). Habits of Microtus californicus revealed by automatic photographic recorders. Ecol. Monogr. 30, 231-249.
65. Perrigo, G. (1987). Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Anim. Behav. 35, 1298-1316.
66. Peterson, C. C., Nagy, K. A. and Diamond, J. (1990). Sustained metabolic scope. Proc. Natl. Acad. Sci. USA 87, 2324-2328.
67. Reynolds, P. S. (1993). Effects of body size and fur on heat loss of collared lemmings, Dicrostonyx groenlandicus. J. Mammal. 74, 291-303.
68. 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.
69. Rogowitz, G. L. and McClure, P. A. (1995). Energy export and offspring growth during lactation in cotton rats (Sigmodon hispidus). Funct. Ecol. 9, 143-150.
70. Romero, J. J., Canas, R., Baldwin, R. L. and Koong, L. J. (1976). Lactational efficiency complex of rats: provisional model for interpretation of energy balance data. J. Dairy Sci. 59, 57-67.
71. Scantlebury, M., Hynds, W., Booles, D. and Speakman, J. R. (2000). Isotope recycling in lactating dogs (Canis familiaris). Am. J. Physiol. 278, R669-R676.
72. Scholander, P. F., Walters, A., Hock, R. and Irving, L. (1950). Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99, 225-236.
73. Scribner, S. J. and Wynne-Edwards, K. E. (1994). Thermal constraints on maternal behavior during reproduction in dwarf hamsters (Phodopus). Physiol. Behav. 55, 897-903.
74. Snapp, B. D. and Heller, H. C. (1981). Suppression of metabolism during hibernation in ground squirrels. Physiol. Zool. 54, 297-307.
75. Speakman, J. R. (1997). Doubly Labelled Water: Theory and Practice. London: Chapman & Hall.
76. Speakman, J. R. (1998). The history and theory of the doubly labeled water technique. Am. J. Clin. Nutr. 68, 932S-938S.
77. Speakman, J. R. (2000). The cost of living: field metabolic rates of small mammals. Adv. Ecol. Res. 30, 177-297.
78. Speakman, J. R. and Król, E. (2005a). Limits to sustained energy intake IX: a review of hypotheses. J. Comp. Physiol. B 175, 375-394.
79. Speakman, J. R. and Krol, E. (2005b). Comparison of different approaches for the calculation of energy expenditure using doubly labeled water in a small mammal. Physiol. Biochem. Zool. 78, 650-667.
80. Speakman, J. R. and 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.
81. Speakman, J. R. and Racey, P. A. (1987). The equilibrium concentration of O-18 in body-water - implications for the accuracy of the doubly-labeled water technique and a potential new method of measuring RQ in free-living animals. J. Theor. Biol. 127, 79-95.
82. Speakman, J. R. and Racey, P. A. (1988a). Validation of the doubly labeled water technique in small insectivorous bats by comparison with indirect calorimetry. Physiol. Zool. 61, 514-526.
83. 2 production for accuracy of the doubly labeled water technique - the importance of recapture interval. Comp. Biochem. Physiol. 90A, 337-340.
84. Speakman, J. R., Nagy, K. A., Masman, D., Mook, W. G., Poppitt, S. D., Strathearn, G. E. and Racey, P. A. (1990). Interlaboratory comparison of different analytical techniques for the determination of O-18 abundance. Anal. Chem. 62, 703-708.
85. Speakman, J. R., Racey, P. A., Haim, A., Webb, P. I., Ellison, G. T. H. and Skinner, J. D. (1994). Interindividual and intraindividual variation in daily energy expenditure of the pouched mouse (Saccostomus-campestris). Funct. Ecol. 8, 336-342.
86. Thomas, D. W., Blondel, J., Perret, P., Lambrechts, M. M. and Speakman, J. R. (2001). Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291, 2598-2600.
87. Trayhurn, P. (1989). Thermogenesis and the energetics of pregnancy and lactation. Can. J. Physiol. Pharmacol. 67, 370-375.
88. Trayhurn, P., Douglas, J. B. and McGuckin, M. M. (1982). Brown adipose tissue thermogenesis is 'suppressed' during lactation in mice. Nature 298, 59-60.
89. Villarroya, F., Felipe, A. and Mampel, T. (1986). Sequential changes in brown adipose tissue composition, cytochrome oxidase activity and GDP binding throughout pregnancy and lactation in the rat. Biochim. Biophys. Acta 882, 187-191.
90. Virgos, E., Cabezas-Diaz, S. and Blanco-Aguiar, J. A. (2006). Evolution of life history traits in Leporidae: a test of nest predation and seasonality hypotheses. Biol. J. Linn. Soc. Lond. 88, 603-610.
91. Visser, G. H. and Schekkerman, H. (1999). Validation of the doubly labeled water method in growing precocial birds: the importance of assumption concerning evaporative water loss. Physiol. Biochem. Zool. 72, 740-749.
92. Visser, G. H., Dekinga, A., Achterkamp, B. and Piersma, T. (2000a). Ingested water equilibrates isotopically with the body water pool of a shorebird with unrivaled water fluxes. Am. J. Physiol. 279, R1795-R1804.
93. Visser, G. H., Boon, P. E. and Meijer, H. A. J. (2000b). Validation of the doubly labeled water in Japanese Quail Coturnix c. japonica chicks: is there an effect of growth rate? J. Comp. Physiol. B 170, 365-372.
94. Weiner, J. (1987). Limits to energy budget and tactics in energy investments during reproduction in the Djungarian hamster (Phodopus sungorus sungorus Pallas 1770). Symp. Zool. Soc. Lond. 57, 167-187.
95. Weiner, J. (1992). Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends Ecol. Evol. 7, 384-388.
96. Weir, J. B. de V. (1949). New methods for calculating metabolic rate with special reference to protein metabolism. J. Physiol. 109, 1-9.
97. Wieser, W. (1994). Cost of growth in cells and organisms: general rules and comparative aspects. Biol. Rev. Camb. Philos. Soc. 69, 1-33.
98. Xiao, X. Q., Grove, K. L., Grayson, B. E. and Smith, M. S. (2004). Inhibition of uncoupling protein expression during lactation: role of leptin. Endocrinology 145, 830-838.
99. Zhang, X. Y. and Wang, D. H. (2007). Thermogenesis, food intake and serum leptin in cold-exposed lactating Brandt's voles Lasiopodomys brandtii. J. Exp. Biol. 210, 512-521.