The energy cost of reproduction in small rodents

Acta Theriologica Sinica

Volumn 27, Issue 1, 2007, Pages 1-13

  Speakman, John R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Energy cost; Energy intake; Reproduction; Small rodent; Thermogenesis

Indexed keywords

ENERGY DISSIPATION; ENERGY FLOW; HEAT PRODUCTION; LACTATION; PARENTAL CARE; PREGNANCY; REPRODUCTION; RODENT; TEMPERATURE EFFECT;

ANIMALIA; MAMMALIA; MUS; MUS MUSCULUS; RODENTIA;

EID: 34247869694     PISSN: 10001050     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (105)

1. Abdalla E B, Kotby E A, Johnson H D. 1993. Physiological-responses to heat-induced hyperthermia of pregnant and lactating ewes. Small Ruminant Res, 11: 125-134.
2. Akesson A, Vahter M, Berglund M, Eklof T, Bremme K, Bjellerup P. 2004. Bone turnover from early pregnancy to postweaning. Acta Obstetricia et Gynecologica Scandinavica, 83: 1049-1055.
3. Agius L, 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.
4. Bates A, Adels L, Leon M. 1985. Thermal control of maternal contact bouts: the interbout interval. Physiol Behav, 34: 835-837.
5. Biggerstaff S, Mann M. 1992. Consummatory behaviors and weight regulation in pregnant, lactating, and pregnant-lactating mice. Physiol Behav, 52: 485-491.
6. Black J L, Mullan B P, Lorschy M L, Giles L R. 1993. Lactation in the sow during heat-stress. Livest Prod Sci, 35: 153-170.
7. Bridges R S, Grimm C T. 1982. Reversal of morphine disruption of maternal-behavior by concurrent treatment with the opiate antagonist naloxone. Science, 218: 166-168.
8. Brody S, Ragsdale A C, Yeek R G, Worstell D. 1958. Environmental physiology and shelter engineering with special reference to domestic animals XXXIII. Milk production, feed and water consumption and body weight of Jersey and Holstein cows in relation to several diurnal temperature rhythms. Mo AES Res Bull, 1958: 578.
9. Cannon B, Nedergaard J. 2004. Brown adipose tissue: function and physiological significance. Physiol Rev, 84: 277-359.
10. Charlesworth B C. 1994. Evolution in Age-Structured Populations. Second edition. Cambridge: Cambridge University Press.
11. Charnov E L. 1993. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford: Oxford University Press.
12. Cobble J W, Herman H A. 1951. The influence of environmental temperature on the composition of milk of the dairy cow. Mo AES Res Bull, 1951: 485.
13. Cox B, Ary M, Chesarkek W, Lomax P. 1976. Morphine hyperthermia in the rat: an action on the central thermostats. Eur J Pharmacol, 36: 33-39.
14. Croskerry P G, Smith G K, Leon M. 1978. Thermoregulation and the maternal behaviour of the rat. Nature, 273: 299-300.
15. Degen A A, Khokhlova I S, Kam M, Snider I. 2002. Energy requirements during reproduction in female common spiny mice (Acomys cahirinus). Journal of Mammalogy, 83: 645-651.
16. Denis R G P, Williams G, Vernon R G. 2003. Regulation of serum leptin and its role in the hyperphagia of lactation in the rat. J Endocrinol, 176: 193-203.
17. Drummond H, Vazquez E, Sanchez-Colon S, Martinez-Gomez M, Hudson R. 2000. Competition for milk in the domestic rabbit: Survivors benefit from littermate deaths. Ethology, 106: 511-526.
18. Fink R, Tauson A H, Hansen K B, Wamberg S, Kristensen N B. 2001. Energy intake and milk production in mink (Mustela vison) - Effect of litter size. Arch Anim Nutr, 55: 221-242.
19. Fisher R A. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press.
20. Gandelman R, Simon N G. 1978. Spontaneous pup-killing by mice in response to large litters. Developmental Psychobiology, 11: 235-241.
21. Giralt M, Villarroya F, Mampel T, Iglesias R. 1986. Impaired basal and noradrenaline induced isodothyrionine 5 ' deiodinase activity in brown adipose tissue form pregnant and lactating rats. Biochem Biophys Res Commun, 138: 1315-1321.
22. Gittleman J L, Thompson S D. 1988. Energy allocation in mammalian reproduction. American Zoologist, 28: 863-875.
23. Glazier D S. 1985. Energetics of litter size in five species of peromyscus with generalisations for other mammals. J Ma, 66: 629-642.
24. Hacklander K, Tataruch F, Ruf T. 2002. The effect of dietary fat content on lactation energetics in the European hare (Lepw europaeus). Physiol Biochem Zool, 75: 19-28.
25. Hammond K A, Diamond J. 1992. An experimental test for a ceiling on sustained metabolic-rate in lactating mice. Physiol Zool, 65: 952-977.
26. Hammond K A, Diamond J. 1994. Limits to dietary nutrient uptake and intestinal nutrient uptake in lactating mice. Physiological Zoology, 67:282-303.
27. Hammond K A, Diamond J. 1997. Maximal sustained energy budgets in humans and animals. Nature, 386: 457-462.
28. Hammond K A, Konarzewski M, Torres R M, Diamond J. 1994. Metabolic ceilings under a combination of peak energy demands. Physiol Zool, 67: 1479-1506.
29. Hammond K A, Kristan D M. 2000. Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Biochem Zool, 73: 547-556.
30. 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.
31. Havera S P. 1979. Energy and nutrient costs of lactation in fox squirrels. Journal of Wildlife Management, 43: 958-965.
32. Hayes J P, Garland T, Dohm M R. 1992. Individual variation in metabolism and reproduction of Mus: are energetics and life history linked? Functional Ecology, 6: 5-14.
33. Hill R W. 1992. The altricial/Precocial contrast in the thermal relations and energetics of small mammals. In Tomasi T, Horton T eds. In Mammalian Energetics: Interdisciplinary Views of Metabolism and Reproduduction. New York, Ithaca: Cornell University Press, 122-159.
34. Isler D, Trayburn P, Lunn P G. 1984. Brown adipose-tissue metabolism in lactating rats-the effect of litter size. Ann Nutr Metab, 28: 101-109.
35. Jansen G R, Binard R. 1991. Effect of dietary-protein and environmental-factors on lactation performance in rats. Physiol Behav, 50: 297-304
36. Johnson M S, 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.
37. Johnson M S, Thomson S C, Speakman J R. 2001a. Limits to sustained energy intake I. Lactation in the laboratory mouse Mus musculus. J Exp Biol, 204: 1925-1935.
38. Johnson M S, Thomson S C, Speakman J R. 2001b. Limits to sustained energy intake III. Effects of concurrent pregnancy and lactation in Mus musculus. J Exp Biol, 204: 1947-1956.
39. Johnston S L, Grune T, Bell L M, Murray S J, Souter D M, Erwin S S, Yearsley J M, Gordon I J, Illius A W, Kyriazakis I, Speakman J R. 2006. Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity. Proceedings of the Royal Society of London Series B-Biological Sciences.
40. Johnston S L, Souter D M, Erwin S S, Tolkamp B, Yearsley J M, Gordon I J, Illius A W, Kyriazakis I, Speakman J R. 2006. Associations between BMR and reproductive performance in C57BL/6 mice. Journal of Experimental Biology (in press).
41. Kaczmarski F. 1966. Bioenergetics of pregnancy and lactation in the bank vole. Acta theriologica, XI 19: 409-417.
42. Kam M, Cohen-Gross S, Khokhlova I S, Degen A A, Geffen E. 2003. Average daily metabolic rate, reproduction and energy allocation during lactation in the Sundevall jird Meriones crassus. Functional Ecology, 17: 496-503.
43. Kam M, Khokhlova I S, Degen A A. 2006. Partitioning of metabolizable energy intake in sucking altricial and precocial rodent pups. J Zool, 269: 502-505.
44. Kittrell E M W, Satinoff E. 1988. Diurnal rhythms of body-temperature, drinking and activity over reproductive-cycles. Physiol Behav, 42: 477-484
45. Kønig B, Riester J, Markl H. 1988. Maternal care in house mice (Mus musculus): II. The energy cost of lactation as function of litter size. Journal of Zoology (London), 216: 195-210.
46. Koiter T R, Moes H, Valkhof N, Wijkstra S. 1999. Interaction of late pregnancy and lactation in rats. J Reprod Fertil, 115: 341-347.
47. Król E. 1985. Reproductive energy budgets of hedgehogs during lactation. Zesz Nauk Filii UW Biol, 10: 105-117.
48. Król E, Speakman J R. 2003a. Limits to sustained energy intake VI. Energetics of lactation in laboratory mice at thermoneutrality. J Exp Biol, 206: 4255-4266.
49. Król E, Speakman J R. 2003b. Limits to sustained energy intake VII. Milk energy output in laboratory mice at thermoneutrality. J Exp Biol, 206: 4267-4281.
50. Król E, Johnson M S, Speakman J R. 2003. Limits to sustained energy intake VII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality. J Exp Biol, 206: 4283-4291.
51. Leon M, Croskerry P G, Smith G. 1978. Thermal control of mother-young contact in rats. Physiol Behav, 21: 793-811.
52. Leon M, Adels L, Coppersmith R. 1985. Thermal limitation of mother-young contact in Norway rats. Dev Psychobiol, 18: 85-105.
53. Liu H, Wang D H, Wang Z W. 2003. Energy requirements during reproduction in female Brandt's voles (Microtus brandtii). Journal of Mammalogy, 84: 1410-1416.
54. Loudon A S, Racey P A. 1987. Reproductive energetics in mammals. (Eds). Symposia of the Zoological Society of London, 57.
55. Lough D S, Beede D L, Wilcox C J. 1990. Effects of feed-intake and thermal-stress on mammary blood-flow and other physiological measurements in lactating dairy-cows. J Dairy Sci, 73: 325-332.
56. Lublin A, Wolfenson D. 1996. Lactation and pregnancy effects on blood flow to mammary and reproductive systems in heat-stressed rabbits. Comp Biochem Physiol A Mol Integr Physiol, 115: 277-285.
57. Martin R D, MacLarnon A M. 1985. Gestation period, neonatal size and maternal investment in placental mammals. Nature, 313: 220-223.
58. Martin R D. 1989. Size, shape and evolution. In: keynes M ed. In Evolutionary Studies a Centenary Celebration of the Life of Julian Huxley London: Eugenics Society, 96-141.
59. Mattingly D K, McClure P A. 1982. Energetics of reproduction in large littered cotton rats (Sigmodon hispidus). Ecology, 63: 183-195.
60. Mattingly D K, McClure P A. 1985. Energy allocation during lactation in cotton rats (Sigmodon hispidus) on a restricted diet. Ecology, 66: 928-937.
61. Migula P. 1969. Bioenergetics of pregnancy and lactation in the common vole. Acta theriologica, 13: 167-179.
62. Millar J S, Innes D G. 1985. Breeding by Peromyscus maniculatus over an elevational gradient. Can J Zool, 63: 124-129.
63. Millar J S. 1977. Adaptive features of mammalian reproduction. Evolution, 31: 370-386.
64. Millar J S. 1985. Life cycle characteristics of Peromyscus maniculatus nebrascensis. Can J Zool, 63: 1280-1284.
65. Millar J S. 1978. Energetics of reproduction in Peromyscus leucopus: the cost of lactation. Ecology, 59: 1055-1061.
66. Myrcha A, Ryskowski L, Walkowa W. 1969. Bioenergetics of pregnancy and lactation in the white mouse. Acta Theriol, 12: 161-166.
67. Newkirk K D, Cheung B L W, Scribner S J, Wynne-Edwards K E. 1998. Earlier thermoregulation and consequences for pup growth in the Siberian versus Djungarian dwarf hamster (Phodopus). Physiol Behav, 63: 435-443.
68. Nizielski S E, Billington C J, Levine A S. 1993. Bat thermogenic activity and capacity are reduced during lactation in ground squirrels. Am J Physiol Regul Integr Comp Physiol, 264: R16-R21.
69. Oftedal O T. 1984. Body size and reproductive strategy as correlates of milk energy output in lactating mammals. Acta Zoologica Fennica, 171: 183-186.
70. 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.
71. Peterson C C, Nagy K A, Diamond J. 1990. Sustained metabolic scope. Proc Natl Acad Sci USA, 87: 2324-2328
72. Quiniou N, Noblet J. 1999. Influence of high ambient temperatures on performance of multiparous lactating sows. J Anim Sci, 77: 2124-2134.
73. Randolph P A, Randolph J C, Mattingly K, Foster, M M. 1977. Energy costs of reproduction in the cotton rat (Sigmodon hispidus). Ecology, 58: 31-45.
74. Renaudeau D, Noblet J. 2001. Effects of exposure to high ambient temperature and dietary protein level on sow milk production and performance of piglets. J Anim Sci, 79: 1540-1548.
75. Renaudeau D, Noblet J, Dourmad J Y. 2003. Effect of ambient temperature on mammary gland metabolism in lactating sows. J Anim Sci, 81: 217-231.
76. Reznick D N, Bryga H, Endler J A. 1990. Experimentally induced life history evolution in natural population. Nature, 346: 357-359.
77. Ricklefs R E, Wikelski M. 2002. The physiology-life history nexus. Trends in Ecology and Evolution, 17 (10):462-468.
78. Roff D A. 1992. The Evolution of Life Histories: Theory and Analysis. Chapman & Hall, New York, USA.
79. Rogowitz G L, McClure P A. 1995. Energy export and offspring growth during lactation in cotton rats (Sigmodon hispidus). Functional Ecology, 9: 143-150.
80. Rogowitz G L. 1998. Limits to milk flow and energy allocation during lactation in the hispod cotton rat (Sigmodon hispidus). Physiol Zool, 71: 312-320.
81. Sano H, Ambo K, Tsuda T. 1985. Blood glucose kinetics in whole body and mammary gland of lactating goats exposed to heat. J Dairy Sci, 68: 2557-2564.
82. Scribner S J, Wynne Edwards K E. 1994a. Disruption of body-temperature and behavior rhythms during reproduction in dwarf hamster (Phodopus). Physiol Behav, 55: 361-369.
83. Scribner S J, Wynne Edwards K E. 1994b. Thermal constraints on maternal-behavior during reproduction in dwarf hamsters (Phodopus). Physiol Behav, 55: 897-903.
84. Sikes R S. 1995. Costs of lactation and optimal litter size in northern grasshopper mice (Onychomys leucogaster). Journal of Mammalogy, 76: 348-357.
85. Smith C C, Fretwell S D. 1974. The optimal balance between size and number of offspring. American Naturalist, 108: 499-506.
86. Speakman J R. 2006. The physiological cost of reproduction. Philosophical transactions of the Royal Society. (in press).
87. Speakman J R, Król E. 2005. Limits to sustained energy intake IX: a review of hypotheses. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 175: 375-394.
88. Speakman J R, Gidney A, Bett J, Mitchell I P, Johnson M S. 2001. Limits to sustained energy intake IV. Effect of variation in food quality on lactating mice Mus musculus. J Exp Biol, 204: 1957-1965.
89. Stearns S C. 1992. The Evolution of Life Histories. OUP, Oxford.
90. Stern J M, Azzara A V. 2002. Thermal control of mother-young contact revisited: Hyperthermic rats nurse normally. Physiol Behav, 77: 11-18.
91. Studier E H. 1979. Boenergetics of growth, pregnancy and lactation in the laboratory mouse Mus musculus. Comp Biochem Physiol, 64A: 473-481.
92. Thompson S D. 1992. Gestation and lactation in small mammals: basal metabolic rate and the limits of energy use. In: Tomasi T E, Horton T H eds. Mammalian Energetics: Interdiciplinary Views of Metabolism and Reproduction. Ithaca, New York: Cornell University Press.
93. Thompson S D, Nicoll M E. 1986. Basal metabolic rate and energetics of reproduction in therian mammals. Nature, 321: 690-693.
94. Trayhurn P. 1983. Decreased capacity for non-shivering thermogenesis during lactation in mice. Pflügers Archiv, 398: 264-265.
95. Trayhurn P. 1989. Thermogenesis and the energetics of pregnancy and lactation. Can J Physiol Pharmacol, 67: 370-375.
96. Trayhurn P, Douglas J B, McGuckin M M. 1982. Brown adipose-tissue thermogenesis is suppressed during lactation in mice. Nature, 298: 59-60.
97. Trayhurn P, Jennings C. 1987. Functional atrophy of brown adipose-tissue during lactation in mice-effects of lactation and weaning on mitochondrial gdp binding and uncoupling protein. Biochem, J, 248: 273-276.
98. Trayhurn P, Jennings G. 1988. Non-shivering thermogenesis and the thermogenic capacity of brown fat in fasted/re-fed mice. Am J Physiol Regul Integr Comp Physiol, 254: R11-R16.
99. Trayhurn P, Wusterman M C. 1987. Sympathetic activity in brown adipose-tissue during lactation in mice. Proc Nutr Soc, 46: A27.
100. Ulmershakibaei C, Plonait H. 1992. Studies of lactational hyperthermia in sows. Tierarztliche Umschau, 47: 605-611.
101. Veloso C, Bozinovic F. 2000. Effect of food quality on the energetics of reproduction in a precocial rodent, Octodon degus. Journal of Mammalogy, 81: 971-978.
102. Wade G N, Jennings G, Trayhurn P. 1986. Energy balance and brown adipose tissue thermogenesis during pregnancy in Syrian hamsters. Am J Physiol, 250: R845-R850.
103. Weiner J. 1987. Limits to energy budget and tactics in energy investments during reproduction in the Djungarian hamster (Phodopus sungorus sungorus Pallas 1770). Symp Zoo Soc Lond, 57: 167-187.
104. Weiner J. 1992. Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends Ecol Evol, 7: 384-388.
105. Williams G C. 1966, Adaptation and natural selection. Princeton University Press, Princeton N J.