Metabolic scaling: A many-splendoured thing

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 139, Issue 3 SPEC.ISS., 2004, Pages 531-541

  Suarez, Raul K ^a   Darveau, Charles A ^b   Childress, James J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

BMR; Body size; Metabolic rate; Metabolic regulation; Symmorphosis; V O 2max

Indexed keywords

AEROBIC METABOLISM; ALLOMETRY; BODY MASS; ENERGY EXPENDITURE; ENERGY METABOLISM; EXERCISE; METABOLIC RATE; METABOLIC REGULATION; METABOLISM; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; REST; REVIEW;

ANIMALIA; ELEPHANTIDAE; SORICIDAE;

EID: 8444226449     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2004.05.001     Document Type: Review

References (111)

1. Atkinson D.E. Cellular Energy Metabolism and Its Regulation. 1977;Academic Press, New York
2. Banavar J.R., Maritan A., Rinaldo A. Size and form in efficient transportation networks. Nature. 399:1999;130-131
3. Banavar J.R., Damuth J., Maritan A., Rinaldo A. Supply-demand balance and metabolic scaling. Proc. Natl. Acad. Sci. U. S. A. 99:2002;10506-10509
4. Banavar J.R., Damuth J., Maritan A., Rinaldo A. Allometric cascades. Nature. 421:2003;713-714
5. Blank S., Chen V., Hamilton N., Salerno T.A., Ianuzzo C.D. Biochemical characteristics of mammalian myocardia. J. Mol. Cell. Cardiol. 21:1989;367-373
6. Brand M.D., Couture P., Else P.L., Withers K.W., Hulbert A.J. Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem. J. 275:1991;81-86
7. Brand M.D., Turner N., Ocloo A., Else P.L., Hulbert A.J. Proton conductance and fatty acid composition of liver mitochondria correlates with body mass in birds. Biochem. J. 376:2003;741-748
8. Brett J.R. The relation of size to the rate of oxygen consumption and sustained swimming speeds of sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Board Can. 24:1965;1491-1501
9. Brown G.C., Lakin-Thomas P.L., Brand M.D. Control of respiration and oxidative phosphorylation in isolated liver cells. Eur. J. Biochem. 192:1990;355-362
10. Brown J.H., West G.B., Enquist B.J. Scaling in biology: patterns, processes, causes and consequences. Brown J.H., West G.B. Scaling in Biology. 2000;1-21 Oxford Univ. Press, New York
11. Buttgereit F., Brand M.D. A hierarchy of ATP-consuming processes in mammalian cells. Biochem. J. 312:1995;163-167
12. Calder W.A. Scaling of physiological processes in homeothermic animals. Annu. Rev. Physiol. 43:1981;301-322
13. Calder W.A. Size, Function and Life History. 1984;Harvard Univ. Press, Cambridge, MA
14. Casey T.M., May M.L., Morgan K.R. Flight energetics of euglossine bees in relation to morphology and wing stroke frequency. J. Exp. Biol. 116:1985;271-289
15. Chai P., Harrykissoon R., Dudley R. Hummingbird hovering performance in hyperoxic heliox: effects of body mass and sex. J. Exp. Biol. 199:1996;2745-2755
16. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. 17:1956;65-134
17. Childress J.J., Somero G.N. Metabolic scaling: a new perspective based on scaling of glycolytic enzyme activities. Am. Zool. 30:1990;161-173
18. Clarke A., Johnston N.M. Scaling of metabolic rate with body mass and temperature in fish. J. Anim. Ecol. 68:1999;893-905
19. Couture P., Hulbert A.J. Relationship between body mass, tissue metabolic rate, and sodium pump activity in mammalian liver and kidney. Am. J. Physiol. 268:1995;R641-R650
20. Darveau C.-A., Suarez R.K., Andrews R.D., Hochachka P.W. Allometric cascade as a unifying principle of body mass effects on metabolism. Nature. 417:2002;166-170
21. Darveau C.-A., Suarez R.K., Andrews R.D., Hochachka P.W. Reply. Nature. 421:2003;714
22. 2max at the whole animal level. J. Exp. Biol. 115:1985;319-331
23. di Prampero P.E. Factors limiting maximal performance in humans. Eur. J. Appl. Physiol. 90:2003;420-429
24. Diamond J.M. The red flag of optimality. Nature. 355:1992;204-206
25. Diamond J.M. Evolution of biological safety factors: a cost/benefit analysis. Weibel E.R., Taylor C.R., Bolis L. Principles of Animal Design: The Optimization and Symmorphosis Debate. 1998;21-27 Cambridge Univ. Press, Cambridge
26. Dobson G.P., Headrick J.P. Bioenergetic scaling: metabolic design and body-size constraints in mammals. Proc. Natl. Acad. Sci. U. S. A. 92:1995;7317-7321
27. Dobson G.P., Himmelreich U. Heart design: free ADP scales with absolute mitochondrial and myofibrillar volumes from mouse to human. Biochim. Biophys. Acta. 1553:2002;261-267
28. Dodds P.S., Rothman D.H., Weitz J.S. Re-examination of the "3/4 law" of metabolism. J. Theor. Biol. 209:2001;9-27
29. Dudley R., Gans C. A critique of symmorphosis and optimality models in physiology. Physiol. Zool. 64:1991;627-637
30. Else P.L., Hulbert A.J. An allometric comparison of the mitochondria of mammalian and reptilian tissues: the implications for the evolution of endothermy. J. Comp. Physiol. 156:1985;3-11
31. Else P.L., Hulbert A.J. An allometric comparison of the mitochondria of mammalian and reptilian tissues: the implications for the evolution of endothermy. J. Comp. Physiol., B. 156:1985;3-11
32. Else P.L., Hulbert A.J. Mammals: an allometric study of metabolism at tissue and mitochondrial level. Am. J. Physiol. 248:1985;R415-R421
33. Else P.L., Windmill D.J., Markus V. Molecular activity of sodium pumps in endotherms and ectotherms. Am. J. Physiol. 271:1996;R1287-R1294
34. Emmett B., Hochachka P.W. Scaling of oxidative and glycolytic enzymes in mammals. Respir. Physiol. 45:1981;261-272
35. Fell D. Understanding the Control of Metabolism. 1997;Portland Press, London, Miami
36. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 125:1985;1-15
37. Frappell P.B., Hinds D.S., Boggs D.F. Scaling of respiratory variables and the breathing pattern in birds: an allometric and phylogenetic approach. Physiol. Biochem. Zool. 74:2001;75-89
38. Gans C. On the merits of adequacy. Am. J. Sci. 293-A:1993;391-406
39. Garland T. Physiological correlates of locomotory performance in a lizard: an allometric approach. Am. J. Physiol. 247:1984;R806-R815
40. Garland T., Carter P.A. Evolutionary physiology. Annu. Rev. Physiol. 56:1994;579-621
41. Garland T., Huey R.B. Testing symmorphosis: Does structure match functional requirements? Evolution. 41:1987;1404-1409
42. Garland T., Bennett A.F., Daniels C. Heritability of locomotor performance and its correlates in a natural population. Experientia. 46:1990;530-533
43. Garland T., Harvey P.H., Ives A.R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41:1992;18-32
44. Hafner R.P., Brown G.C., Brand M.D. Analysis of the control of respiration rate, phosphorylation rate, proton leak rate and protonmotive force in isolated mitochodria using the 'top-down' approach of metabolic control theory. Eur. J. Biochem. 188:1990;313-319
45. Hamilton N., Ianuzzo C.D. Contractile and calcium regulating capacities of myocardia of different sized mammals scale with resting heart rate. Mol. Cell. Biochem. 106:1991;133-141
46. Harrison J.F., Lighton J.R.B. Oxygen-sensitive flight metabolism in the dragonfly Erythemis simplicicollis. J. Exp. Biol. 201:1998;1739-1744
47. Harrison J.F., Camazine S., Marden J.H., Kirkton S.D., Rozo A., Yang X. Mite not make it home: tracheal mites reduce the safety margin for oxygen delivery of flying honeybees. J. Exp. Biol. 204:2001;805-814
48. Hawkins A. Protein turnover: a functional appraisal. Funct. Ecol. 5:1991;222-233
49. Hochachka P.W., Somero G.N. Biochemical Adaptation. Mechanism and Process in Physiological Evolution. 2002;Oxford Univ. Press, Oxford
50. Hochachka P.W., Emmett B., Suarez R.K. Limits and constraints in the scaling of oxidative and glycolytic enzymes in homeotherms. Can. J. Zool. 66:1988;1128-1138
51. Hochachka P.W., Darveau C.-A., Andrews R.D., Suarez R.K. Allometric cascade: a model for resolving body mass effects on metabolism. Comp. Biochem. Physiol., A. 134:2003;675-691
52. Hoppeler H., Lindstedt S.L., Claassen H., Taylor C.R., Mathieu O., Weibel E.R. Scaling mitochondrial volume in heart to body mass. Respir. Physiol. 55:1984;131-137
53. Hulbert A.J. Life, death and membrane bilayers. J. Exp. Biol. 206:2003;2303-2311
54. Hulbert A.J., Else P.L. Mechanisms underlying the cost of living in animals. Annu. Rev. Physiol. 62:2000;207-235
55. Hulbert A.J., Else P.L., Manolis S.C., Brand M.D. Proton leak in hepatocytes and liver mitochondria from archosaurs (crocodiles) and allometric relationships for ectotherms. J. Comp. Physiol. 172:2002;387-397
56. Hulbert A.J., Faulks S., Buttemer W.A., Else P.L. Acyl composition of muscle membranes varies with body size in birds. J. Exp. Biol. 205:2002;3561-3569
57. Hulbert A.J., Rana T., Couture P. The acyl composition of mammalian phospholipids: an allometric analysis. Comp. Biochem. Physiol., B. 132:2002;515-527
58. Jones J.H. Optimization of the mammalian respiratory system: symmorphosis versus single species adaptation. Comp. Biochem. Physiol., B. 120:1998;125-138
59. Jones J.H., Lindstedt S.L. Limits to maximal performance. Annu. Rev. Physiol. 55:1993;547-569
60. Joos B., Lighton J.R.B., Harrison J.F., Suarez R.K., Roberts S.P. Effects of ambient oxygen tension on flight performance, metabolism and water loss of the honeybee. Physiol. Zool. 70:1996;167-174
61. Kashiwaya Y., Sato K., Tsuchiya N., Thomas S., Fell D.A., Veech R.L., Passonneau J.V. Control of glucose utilization in working perfused rat heart. J. Biol. Chem. 269:1994;25502-25514
62. Kleiber M. Body size and metabolism. Hilgardia. 6:1932;315-353
63. Krebs H.A. Body size and tissue respiration. Biochim. Biophys. Acta. 4:1950;249-269
64. 2. J. Exp. Biol. 204:2001;3195-3199
65. Mansour T.E., Ahlfors C.E. Studies on heart phosphofructokinase. Some kinetic and physical properties of the crystalline enzyme. J. Biol. Chem. 243:1968;2523-2533
66. Mathieu O., Krauer R., Hoppeler H., Gehr P., Lindstedt S.L., Alexander R., Taylor C.R., Weibel E.R. Design of the mammalian respiratory system: VII. Scaling mitochondrial volume in skeletal muscle to body mass. Respir. Physiol. 44:1981;113-128
67. Maxwell L.K., Jacobson E.R., McNab B.K. Intraspecific allometry of standard metabolic rate in green iguanas, Iguana iguana. Comp. Biochem. Physiol., A. 136:2003;301-310
68. Mootha V.K., Arai A.E., Balaban R.S. Maximum oxidative phosphorylation capacity of the mammalian heart. Am. J. Physiol. 272:1997;H769-H775
69. Moyes C.D., Hood D.A. Origins and consequences of mitochondrial variation in vertebrate muscle. Annu. Rev. Physiol. 65:2003;177-201
70. Moyes C.D., Suarez R.K., Hochachka P.W., Ballantyne J.S. A comparison of fuel preferences of mitochondria from vertebrates and invertebrates. Can. J. Zool. 68:1990;1337-1349
71. Oikawa S., Itazawa Y. Relationship between summated tissue respiration and body size in a marine teleost, the porgy Pagrus major. Fish. Sci. 69:2003;687-694
72. Pennycuick C.J., Rezende M.A. The specific power output of aerobic muscle, related to the power density of mitochondria. J. Exp. Biol. 108:1984;377-392
73. Porter R.K. Allometry of mammalian cellular oxygen consumption. Cell. Mol. Life Sci. 58:2001;815-822
74. + leak in mitochondria and its relevance to metabolic rate. Nature. 362:1993;628-630
75. Porter R.K., Brand M.D. Causes of differences in respiration rate of hepatocytes from mammals of different body mass. Am. J. Physiol. 269:1995;R1213-R1224
76. Porter R.K., Brand M.D. Cellular oxygen consumption depends on body mass. Am. J. Physiol. 269:1995;R226-R228
77. Reynolds P.S., Lee R.M. Phylogenetic analysis of avian energetics: passerines and nonpasserines do not differ. Am. Nat. 147:1996;735-759
78. Rubner M. Ueber den Einfluss der Korpergrosse auf Stoffund Kraftweschel. Z. Biol. 19:1883;535-562
79. Schmidt-Nielsen K. Scaling. Why is Animal Size So Important? 1984;Cambridge Univ. Press, Cambridge
80. Seeherman H.J., Taylor C.R., Maloiy G.M.O., Armstrong R.B. Design of the mammalian respiratory system: II. Measuring maximum aerobic capacity. Respir. Physiol. 44:1981;11-23
81. Siebenaller J.F. Analysis of the biochemical consequences of ontogenetic vertical migration in a deep-living teleost fish. Physiol. Zool. 57:1984;598-608
82. Singer D., Schunck O., Bach F., Kuhn H.-J. Size effects on metabolic rate in cell, tissue, and body calorimetry. Thermochim. Acta. 251:1995;227-240
83. Somero G.N., Childress J.J. A violation of the metabolism-size scaling paradigm: activities of glycolytic enzymes in muscle increase in larger-size fish. Physiol. Zool. 53:1980;322-337
84. Somero G.N., Childress J.J. Scaling of oxidative and glycolytic enzyme activities in fish muscle. Gilles R. Circulation Respiration and Metabolism. 1985;250-262 Springer-Verlag, Berlin Heidelberg
85. Suarez R.K. Upper limits to mass-specific metabolic rates. Annu. Rev. Physiol. 58:1996;583-605
86. Suarez R.K., Staples J.F., Lighton J.R.B., West T.G. Relationships between enzymatic flux capacities and metabolic flux rates in muscles: nonequilibrium reactions in muscle glycolysis. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7065-7069
87. Symonds M.R.E., Elgar M.A. Phylogeny affects estimation of metabolic scaling in mammals. Evolution. 56:2002;2330-2333
88. Taylor C.R. Structural and functional limits to oxidative metabolism: insights from scaling. Annu. Rev. Physiol. 49:1987;135-146
89. Taylor C.R., Weibel E.R. Design of the mammalian respiratory system: I. Problem and strategy. Respir. Physiol. 44:1981;1-10
90. 2 demand in muscle: II. Allometric variation in energy demand. Gonzales N.C., Fedde M.R. Oxygen Transfer from Atmosphere to Tissues. 1988;171-181 Plenum, New York
91. Taylor C.R., Weibel E.R., Karas R., Hoppeler H. Matching structures and functions in the respiratory system. Allometric and adaptive variations in energy demand. Wood S.C. Comparative Pulmonary Physiology. Current Concepts. 1989;27-65 Marcel Dekker, New York, Basel
92. Thompson G.G., Withers P.C. Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiol. Zool. 70:1997;307-323
93. Tieleman B.I., Williams J.B. The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol. Biochem. Zool. 73:2000;461-479
94. Videler J.J. Fish Swimming. 1993;Chapman & Hall, New York
95. 2max. Respir. Physiol. 93:1993;221-237
96. 2max at sea level and altitude. Respir. Physiol. 106:1996;329-343
97. Wang Z., O'Connor T.P., Heshka S., Heymsfield S.B. The reconstruction of Kleiber's law at the organ-tissue level. J. Nutr. 131:2001;2967-2970
98. Weibel E.R. Scaling of structural and functional variables in the respiratory system. Annu. Rev. Physiol. 49:1987;147-159
99. Weibel E.R. Symmorphosis. On Form and Function in Shaping Life. 2000;Harvard Univ. Press, Cambridge, MA
100. Weibel E.R. The pitfalls of power laws. Nature. 417:2002;131-132
101. Weibel E.R., Taylor C.R., Hoppeler H. The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc. Natl. Acad. Sci. U. S. A. 88:1991;10357-10361
102. Weibel E.R., Bacigalupe L.D., Schmitt B., Hoppeler H. Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir. Physiol. Neurobiol. 140:2004;115-132
103. West G.B., Brown J.H., Enquist B.J. A general model for the origin of allometric scaling laws in biology. Science. 276:1997;122-126
104. West G.B., Brown J.H., Enquist B.J. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science. 284:1999;1677-1679
105. West G.B., Woodruff W.H., Brown J.H. Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc. Natl. Acad. Sci. U. S. A. 99:2002;2473-2478
106. West G.B., Savage V.M., Gillooly J., Enquist B.J., Woodruff W.H., Brown J.H. Why does metabolic rate scale with body size? Nature. 421:2003;713
107. 2/3. Proc. Natl. Acad. Sci. U. S. A. 100:2003;4046-4049
108. Wisniewski E., Gellerich F.N., Kunz W.S. Distribution of flux control among the enzymes of mitochondrial oxidative phosphorylation in calcium-activated saponin-skinned rat musculus soleus fibers. Eur. J. Biochem. 230:1995;549-554
109. Wu T.Y. Introduction to the scaling of aquatic animal locomotion. Pedley T.J. Scale Effects in Animal Locomotion. 1977;203-232 Academic Press, New York
110. Wu B.J., Else P.L., Storlien L.H., Hulbert A.J. Molecular activity of Na+/K+-ATPase from different sources is related to the packing of membrane lipids. J. Exp. Biol. 204:2001;4271-4280
111. Zhang J., Zhang Y.M., Cho Y.K., Ye Y., Gong G., Bache R.J., Ugurbil K., From A.H.L. Oxygen delivery does not limit cardiac performance during high work rates. Am. J. Physiol. 276:1999;H50-H57