Allometric scaling of mammalian metabolism

Journal of Experimental Biology

Volumn 208, Issue 9, 2005, Pages 1611-1619

  White, Craig R ^a,b   Seymour, Roger S ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Allometry; Basal metabolic rate; Scaling

Indexed keywords

ANIMAL; BASAL METABOLIC RATE; BIOLOGICAL MODEL; BODY SIZE; BODY TEMPERATURE; ENERGY METABOLISM; MAMMAL; PHYSIOLOGY; REGRESSION ANALYSIS; REVIEW;

ANIMALS; BASAL METABOLISM; BODY SIZE; BODY TEMPERATURE; ENERGY METABOLISM; MAMMALS; MODELS, BIOLOGICAL; REGRESSION ANALYSIS;

ANIMALIA; CANIS FAMILIARIS; MAMMALIA;

EID: 18944396944     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01501     Document Type: Review

References (111)

1. Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2002a). Modelling universality and scaling. Nature 420, 626.
2. Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2002b). Supply-demand balance and metabolic scaling. Proc. Natl. Acad. Sci. USA 99, 10506-10509.
3. Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2003). Allometric cascades. Nature 421, 713-714.
4. Banavar, J. R., Maritan, A. and Rinaldo, A. (1999). Size and form in efficient transportation networks. Nature 399, 130-131.
5. Bejan, A. (2000). Shape and Structure, From Engineering to Nature. Cambridge: Cambridge University Press.
6. Benedict, F. G. (1938). Vital Energetics: A Study in Comparative Basal Metabolism. Washington, DC: Carnegie Institution of Washington.
7. Blackburn, T. M. and Gaston, K. J. (1998). The distribution of mammal body masses. Diversity Distrib. 4, 121-133.
8. Blaxter, K. L. (1962). The Energy Metabolism of Ruminants. London: Hutchinson and Co. Ltd.
9. Blaxter, K. L. (1989). Energy Metabolism in Animals and Man. New York: Cambridge University Press.
10. Bligh, J. (1976). Temperature regulation. In Environmental Physiology of Animals (ed. J. Bligh, J. L. Cloudsley-Thompson and A. G. MacDonald), pp. 413-430. London: Blackwell.
11. Bodley, K. B., Mercer, J. R. and Bryden, M. M. (1999). Rate of passage of digesta through the alimentary tract of the New Zealand fur seal (Arctocephalus forsteri) and the Australian sea lion (Neophoca cinerea) (Carnivora: Otariidae). Aust. J. Zool. 47, 193-198.
12. Brody, S. (1945). Bioenergetics and Growth. New York: Reinhold Publishing Corporation.
13. Brown, J. H. and West, G. B. (2000). Scaling in Biology. pp.352. New York: Oxford University Press.
14. Calder, W. A., III (1984). Size, Function, and Life History. Cambridge: Harvard University Press.
15. Campbell, K. L., McIntyre, I. W. and MacArthur, R. A. (1999). Fasting metabolism and thermoregulatory competence of the star-nosed mole, Condylura cristata (Talpidae: Condylurinae). Comp. Biochem. Physiol. 123A, 293-298.
16. Caton, J. M., Hill, D. M., Hume, I. D. and Crook, G. A. (1996). The digestive strategy of the common marmoset, Callithrix jucchus. Comp. Biochem. Physiol. 114A, 1-8.
17. Chappell, M. A. and Dawson, T. J. (1994). Ventilatory accommodation of changing oxygen consumption in dasyurid marsupials. Physiol. Zool. 67, 418-437.
18. Clements, F., Hope, P., Daniels, C., Chapman, I. and Wittert, G. (1998). Thermogenesis in the marsupial Sminthopsis crassicaudata: effect of catecholamines and diet. Aust. J. Zool. 46, 381-390.
19. Cohen, J. E., Jonsson, T. and Carpenter, S. R. (2003). Ecological community description using the food web, species abundance, and body size. Proc. Natl. Acad. Sci. USA 100, 1781-1786.
20. Comport, S. S. and Hume, I. D. (1998). Gut morphology and rate of passage offungal spores through the gut of a tropical rodent, the giant white-tailed rat (Uromys caudimaculatus). Aust. J. Zool. 46, 461-471.
21. Costa, D. P. and Kooyman, G. L. (1984). Contribution of specific dynamic action to heat balance and thermoregulation in the sea otter Enhydra lutris. Physiol. Zool. 57, 199-203.
22. Darveau, C. A., Suarez, R. K., Andrews, R. D. and Hochachka, P. W. (2002). Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166-170.
23. Darveau, C. A., Suarez, R. K., Andrews, R. D. and Hochachka, P. W. (2003). Reply to West et al. and Banavar et al. Nature 421, 714.
24. Dawson, T. J. and Hulbert, A. J. (1970). Standard metabolism, body temperature, and surface areas of Australian marsupials. Am. J. Physiol. 218, 1233-1238.
25. Diamond, P., Brondel, L. and LeBlanc, J. (1985). Payability and postprandial thermogenesis in dogs. Am. J. Physiol. 248, E75-E79.
26. Dodds, P. S., Rothman, D. H. and Weitz, J. S. (2001). Re-examination of the '3/4-law' of metabolism. J. Theor. Biol. 209, 9-27.
27. Elgar, M. A. and Harvey, P. H. (1987). Basal metabolic rates in mammals: Allometry, phylogeny and ecology. Funct. Ecol. 1, 25-36.
28. Felicetti, L. A., Shipley, L. A., Witmer, G. A. and Robbins, C. T. (2000). Digestibility, nitrogen excretion, and mean retention time by North American porcupines (Erethizon dorsatum) consuming natural forages. Physiol. Biochem. Zool. 73, 772-780.
29. Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15.
30. Gallivan, G. J. and Ronald, K. (1981). Apparent specific dynamic action in the harp seal (Phoca groenlandica). Comp. Biochem. Physiol. 69A, 579-581.
31. Garland, T., Jr (1984). Physiological correlates of locomotory performance in a lizard: an allometric approach. Am. J. Physiol. 247, R806-R815.
32. Garland, T., Jr, Harvey, P. H. and Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18-32.
33. Geiser, F. (1988). Reduction of metabolism during hibernation and daily torpor in mammals and birds: Temperature effect or physiological inhibition? J. Comp. Physiol. B 158, 25-38.
34. Gibson, L. A. and Hume, I. D. (2000). Digestive performance and digesta passage in the omnivorous greater bilby, Macrotis lagotis (Marsupialia: Paramelidae). J. Comp. Physiol. B 170, 457-467.
35. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. and Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science 293, 2248-2251.
36. Gould, S. J. (1966). Allometry and size in ontogeny and phylogeny. Biol. Rev. 44, 587-640.
37. Green, A. J. (2001). Mass/length residuals: Measures of body condition or generators of spurious results? Ecology 82, 1473-1483.
38. Haldane, J. B. S. (1928). On being the right size. In Possible Worlds, pp. 18-26. London: Chatto and Windus.
39. Harvey, P. H. and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology. New York: Oxford University Press.
40. Hayssen, V. and Lacy, R. C. (1985). Basal metabolic rates in mammals: Taxonomic differences in the allometry of BMR and body mass. Comp. Biochem. Physiol. 81A, 741-754.
41. Hemmingsen, A. M. (1960). Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep. Steno Memorial Hosp. Nordisk Insulinlab. 9, 1-110.
42. Heusner, A. A. (1991). Size and power in mammals. J. Exp. Biol. 160, 25-54.
43. Hinds, D. S., Baudinette, R. V., MacMillen, R. E. and Halpern, E. A. (1993). Maximum metabolism and the aerobic factorial scope of endotherms. J. Exp. Biol. 182, 41-56.
44. Hinds, D. S. and Rice-Warner, C. N. (1992). Maximum metabolism and aerobic capacity in heteromyid and other rodents. Physiol. Zool. 65, 188-214.
45. Hochachka, P. W., Darveau, C. A., Andrews, R. D. and Suarez, R. K. (2003). Allometric cascade: a model for resolving body mass effects on metabolism. Comp. Biochem. Physiol. 134A, 675-691.
46. Holloway, J. C. and Geiser, F. (2001). Effects of helium/oxygen and temperature on aerobic metabolism in the marsupial sugar glider, Petaurus breviceps. Physiol. Biochem. Zool. 74, 219-225.
47. Hulbert, A. J. and Else, P. L. (2000). Mechanisms underlying the cost of living in animals. Ann. Rev. Physiol. 62, 203-235.
48. Hume, I. D., Smith, C. and Woolley, P. A. (2000). Anatomy and physiology of the gastrointestinal tract of the Julia Creek dunnart, Sminthopsis douglasi (Marsupialia: Dasyuridae). Aust. J. Zool. 48, 475-485.
49. Huxley, J. S. (1932). Problems of Relative Growth. London: Methuen and Co.
50. Kleiber, M. (1932). Body size and metabolism. Hilgardia 6, 315-353.
51. Kleiber, M. (1961). The Fire of Life. New York, London: John Wiley and Sons, Inc.
52. Konarzewski, M. and Diamond, J. (1995). Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49, 1239-1248.
53. Koteja, P. (1987). On the relation between basal and maximum metabolic rate in mammals. Comp. Biochem. Physiol. 87A, 205-208.
54. Krockenberger, M. B. and Bryden, M. M. (1994). Rate of passage of digesta through the alimentary tract of southern elephant seals, Mirounga leonina (Carnivora: Phocidae). J. Zool. 234, 229-237.
55. Lovegrove, B. G. (2000). The zoogeography of mammalian basal metabolic rate. Am. Nat. 156, 201-219.
56. Lovegrove, B. G. (2003). The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J. Comp. Physiol. B 173, 87-112.
57. Lusk, G. (1915). An investigation into the causes of the specific dynamic action of foodstuffs. J. Biol. Chem. 20, 555-617.
58. MacArthur, R. A. and Campbell, K. L. (1994). Heat increment of feeding and its thermoregulatory benefit in the muskrat (Ondatra zibethicus). J. Comp. Physiol. B 164, 141-146.
59. Markussen, N. H., Ryg, M. and Øritsland, N. A. (1994). The effect of feeding on the metabolic rate in harbour seals (Phoca vitulina). J. Comp. Physiol. B 164, 89-93.
60. Marquet, P. A. (2002). Of predators, prey, and power laws. Science 295, 2229-2230.
61. McClelland, K. L., Hume, I. D. and Soran, N. (1999). Responses of the digestive tract of the omnivorous northern brown bandicoot, Isoodon macrourus (Marsupialia, Paramelidae), to plant- and insect-containing diets. J. Comp. Physiol B 169, 411-418.
62. McDonald, R. B., Wickler, S., Horwitz, B. and Stern, J. S. (1988). Meal-induced thermogenesis following exercise training in the rat. Med. Sci. Sport. Exer. 20, 44-49.
63. McKechnie, A. E. and Wolf, B. O. (2004). The allometry of avian basal metabolic rate: Good predictions need good data. Physiol. Biochem. Zool. 77, 502-521.
64. McMahon, T. A. and Bonner, J. T. (1983). On Size and Life. New York: Scientific American.
65. McNab, B. K. (1988). Complications inherent in scaling the basal rate of metabolism in mammals. Quart. Rev. Biol. 63, 25-54.
66. McNab, B. K. (1997). On the utility of uniformity in the definition of basal rate of metabolism. Physiol. Zool. 70, 718-720.
67. Morris, S., Curtin, A. L. and Thompson, M. B. (1994). Heterothermy, torpor, respiratory gas exchange, water balance and the effect of feeding in Gould's long-eared bat Nyctophilus gouldi. J. Exp. Biol. 197, 309-335.
68. Mueller, P. and Diamond, J. (2001). Metabolic rate and environmental productivity: Well-provisioned animals evolved to run and idle fast. Proc. Natl. Acad. Sci. USA 98, 12551-12554.
69. Nagy, K. A., Girard, I. A. and Brown, T. K. (1999). Energetics of free-ranging mammals, reptiles and birds. Ann. Rev. Nutr. 19, 247-277.
70. Nespolo, R. F., Bacigalupe, L. D., Rezende, E. L. and Bozinovic, F. (2001). When nonshivering thermogenesis equals maximum metabolic rate: Thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyamis (Rodentia). Physiol. Biochem. Zool. 74, 325-332.
71. Niklas, K. J. (2004). Plant allometry: is there a grand unifying theory? Biol. Rev. 79, 871-889.
72. Niklas, K. J. and Enquist, B. J. (2001). Invariant scaling relationships for interspecific plant biomass production rates and body size. Proc. Natl. Acad. Sci. USA 98, 2922-2927.
73. Nowak, R. M. (1999). Walker's Mammals of the World. Baltimore: Johns Hopkins University Press.
74. Nunn, C. L. and Barton, R. A. (2000). Allometric slopes and independent contrasts: A comparative test of Kleiber's law in primate ranging patterns. Am. Nat. 156, 519-533.
75. Packard, G. C. and Boardman, T. J. (1999). The use of percentages and size-specific indices to normalize physiological data for variation in body size: Wasted time, wasted effort? Comp. Biochem. Physiol. 122A, 37-44.
76. Pei, Y.-X., Wang, D.-H. and Hume, I. D. (2001). Selective digesta retention and coprophagy in Brandt's vole (Microtus brandti). J. Comp. Physiol. 171, 457-464.
77. Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge: Cambridge University press.
78. Renecker, L. A. and Hudson, R. J. (1986). Seasonal energy expenditures and thermoregulatory responses of moose (Alces alces). Can. J. Zool. 64, 322-327.
79. Reynolds, P. S. (1997). Phylogenetic analysis of surface areas of mammals. J. Mammal.78, 859-868.
80. Rogerson, A. (1968). Energy utilisation by the eland and wildebeest. Symp. Zool. Soc. Lond. 21, 153-161.
81. Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution 55, 2143-2160.
82. Rosen, D. A. S. and Trites, A. W. (1997). Heat increment of feeding in stellar sea lions, Eumetopias jubatus. Comp. Biochem. Physiol. 118A, 877-881.
83. 2. Am. J. Physiol. 226, 490-495.
84. Rubner, M. (1883). Über den einfluss der körpergrösse auf stoff- und kraftwechsel. Z. Biol. 19, 536-562.
85. Savage, V. M., Gillooly, J. F., Woodruff, W. H., West, G., B., Allen, A. P., Enquist, B. J. and Brown, A. C. (2004). The predominance of quarter-power scaling in biology. Funct. Ecol. 18, 257-282.
86. Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Size so Important? Cambridge: Cambridge University Press.
87. Secor, S. M. and Diamond, J. (1997). Determinants of the postfeeding metabolic response of Burmese pythons, Python molurus. Physiol. Zool. 70, 202-212.
88. Secor, S. M. and Faulkner, A. C. (2002). Effects of meal size, meal type, body temperature, and body size on the specific dynamic action of the marine toad, Bufo marinus. Physiol. Biochem. Zool. 75, 557-571.
89. Seeherman, H. J., Taylor, C. R., Maloiy, G. M. O. and Armstrong, R. B. (1981). Design of the mammalian respiratory system. II. Measuring maximum aerobic capacity. Resp. Physiol. 44, 11-23.
90. Sherwood, L. (1997). Human Physiology: From Cells to Systems. Melbourne: Wadsworth.
91. Sokal, R. R. and Rohlf, F. J. (1995). Biometry. W. H. Freeman and Co.
92. Speakman, J. R. (1997). Doubly Labelled Water: Theory and Practice. London: Chapman and Hall.
93. Speakman, J. R., Ergon, T., Cavanagh, R., Reid, K., Scantlebury, D. M. and Lambin, X. (2003). Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic factors. Proc. Natl. Acad. Sci. USA 100, 14057-14062.
94. Speakman, J. R., McDevitt, R. M. and Cole, K. R. (1993). Measurement of basal metabolic rates: Don't lose sight of reality in the quest for comparability. Physiol. Zool. 66, 1045-1049.
95. Stevens, C. E. and Hume, I. D. (1995). Comparative Physiology of the Vertebrate Digestive System. Cambridge: Cambridge University Press.
96. Symonds, M. R. E. and Elgar, M. A. (2002). Phylogeny affects estimation of metabolic scaling in mammals. Evolution 56, 2330-2333.
97. Taylor, C. R., Maloiy, G. M. O., Weibel, E. R., Langman, V. A., Kamau, J. M. Z., Seeherman, H. J. and Heglund, N. C. (1981). Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic mammals. Resp. Physiol. 44, 25-37.
98. Thomas, D. W., Pacheco, M. A., Fournier, F. and Fortin, D. (1998). Validation of the effect of helox on thermal conductance in homeotherms using heated models. J. Therm. Biol. 23, 377-380.
99. Weibel, E. R. (2002). The pitfalls of power laws. Nature 417, 131-132.
100. Weibel, E. R., Bacigalupe, L. D., Schmidt, B. and Hoppeler, H. (2004). Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as a determinant factor. Resp. Physiol. Neurobiol. 140, 115-132.
101. Weiner, J. (1977). Energy metabolism of the roe deer. Acta Theriol. 22, 3-24.
102. West, G. B., Brown, J. H. and Enquist, B. J. (1997). A general model for the origin of allometric scaling laws in biology. Science 276, 122-126.
103. West, G. B., Brown, J. H. and Enquist, B. J. (1999). The fourth dimension of life: Fractal geometry and allometric scaling of organisms. Science 284, 1677-1679.
104. West, G. B., Enquist, B. J. and Brown, J. H. (2002a). Modelling universality and scaling - Reply. Nature 420, 626-627.
105. West, G. B., Savage, V. M., Gillooly, J. F., Enquist, B. J., Woodruff, W. H. and Brown, J. H. (2003). Why does metabolic rate scale with body size? Nature 421, 713.
106. West, G. B., Woodruff, W. H. and Brown, J. H. (2002b). Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc. Natl. Acad. Sci. USA 99, 2473-2478.
107. White, C. R. (2003). The influence of foraging mode and arid adaptation on the basal metabolic rate of burrowing mammals. Physiol. Biochem. Zool. 76, 122-134.
108. 2/3. Proc. Natl. Acad. Sci. USA 100, 4046-4049.
109. White, C. R. and Seymour, R. S. (2004). Does BMR contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological and life-history variables. Physiol. Biochem. Zool. 77, 929-941.
110. Whitfield, J. (2001). All creatures great and small. Nature 413, 342-344.
111. Withers, P. C., Thompson, G. G. and Seymour, R. S. (2000). Metabolic physiology of the north-western marsupial mole, Notoryctes caurinus (Marsupialia: Notoryctidae). Aust. J. Zool. 48, 241-258.