Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Allometric cascade as a unifying principle of body mass effects on metabolism

Abstract

The power function of basal metabolic rate scaling is expressed as aMb, where a corresponds to a scaling constant (intercept), M is body mass, and b is the scaling exponent. The 3/4 power law (the best-fit b value for mammals) was developed from Kleiber's original analysis1 and, since then, most workers have searched for a single cause to explain the observed allometry. Here we present a multiple-causes model of allometry, where the exponent b is the sum of the influences of multiple contributors to metabolism and control. The relative strength of each contributor, with its own characteristic exponent value, is determined by the control contribution. To illustrate its use, we apply this model to maximum versus basal metabolic rates to explain the differing scaling behaviour of these two biological states in mammals. The main difference in scaling is that, for the basal metabolic rate, the O2 delivery steps contribute almost nothing to the global b scaling exponent, whereas for the maximum metabolic rate, the O2 delivery steps significantly increase the global b value.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Estimates of b values for maximum and basal metabolic rates in mammals using the multi-site allometry model.

Similar content being viewed by others

References

  1. Kleiber, M. Body size and metabolism. Hilgarida 6, 315–353 (1932)

    Article  CAS  Google Scholar 

  2. Hochachka, P. W. & Somero, G. N. Biochemical Adaptation—Mechanism and Process in Physiological Evolution (Oxford Univ. Press, New York, 2002)

    Google Scholar 

  3. Hochachka, P. W. Muscles as Molecular and Metabolic Machines (CRC Press, Boca Raton, Florida, 1994)

    Google Scholar 

  4. Jeneson, J. A., Westerhoff, H. V. & Kushmerick, M. J. A metabolic control analysis of kinetic controls in ATP free energy metabolism in contracting skeletal muscle. Am. J. Physiol. Cell Physiol. 279, C813–C832 (2000)

    Article  CAS  Google Scholar 

  5. Thomas, S. & Fell, D. A. A control analysis exploration of the role of ATP utilisation in glycolytic-flux control and glycolytic-metabolite-concentration regulation. Eur. J. Biochem. 258, 956–967 (1998)

    Article  CAS  Google Scholar 

  6. Jones, J. H. Optimization of the mammalian respiratory system: symmorphosis versus single species adaptation. Comp. Biochem. Physiol. B 120, 125–138 (1998)

    Article  CAS  Google Scholar 

  7. West, G. B., Brown, J. H. & Enquist, B. J. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677–1679 (1999)

    Article  ADS  MathSciNet  CAS  Google Scholar 

  8. Banavar, J. R., Maritan, A. & Rinaldo, A. Size and form in efficient transportation networks. Nature 399, 130–132 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Wagner, P. D. Algebraic analysis of the determinants of V̇O2 max. Resp. Physiol. 93, 221–237 (1993)

    Article  CAS  Google Scholar 

  10. Bishop, C. M. The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc. R. Soc. Lond. B 266, 2275–2281 (1999)

    Article  CAS  Google Scholar 

  11. Weibel, E. R. Symmorphosis, on Form and Function Shaping Life (Harvard Univ. Press, Cambridge, 2000)

    Google Scholar 

  12. Rolfe, D. F. S. & Brown, G. C. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731–758 (1997)

    Article  CAS  Google Scholar 

  13. Hulbert, A. J. & Else, P. L. Mechanisms underlying the cost of living in animals. Annu. Rev. Physiol. 62, 207–235 (2000)

    Article  CAS  Google Scholar 

  14. Lovegrove, B. G. The zoogeography of mammalian basal metabolic rate. Am. Nat. 156, 201–219 (2000)

    Article  Google Scholar 

  15. Porter, R. K. & Brand, M. D. Body mass dependence of H+ leak in mitochondria and its relevance to metabolic rate. Nature 362, 628–630 (1993)

    Article  ADS  CAS  Google Scholar 

  16. Porter, R. K., Hulbert, A. J. & Brand, M. D. Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am. J. Physiol. 271, R1550–R1560 (1996)

    CAS  Google Scholar 

  17. Suarez, R. K., Staples, J. F., Lighton, J. R. B. & West, T. G. Relationship between enzymatic flux capacities and metabolic flux rates: Non-equilibrium reactions in muscle glycolysis. Proc. Natl Acad. Sci. USA 94, 7065–7069 (1997)

    Article  ADS  CAS  Google Scholar 

  18. Nagy, K. A., Girard, I. A. & Brown, T. K. Energetics of free-ranging mammals, reptiles, and birds. Annu. Rev. Nutr. 19, 247–277 (1999)

    Article  CAS  Google Scholar 

  19. Stahl, W. R. Scaling of respiratory variables in mammals. J. Appl. Physiol. 22, 453–460 (1967)

    Article  ADS  CAS  Google Scholar 

  20. Bishop, C. M. Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals. Phil. Trans. R. Soc. Lond. B 352, 447–456 (1997)

    Article  ADS  Google Scholar 

  21. Lindstedt, S. L., Hoppeler, H., Bard, K. M. & Thornson, H. A. Jr Estimates of muscle-shortening rate during locomotion. Am. J. Physiol. 249, R669–R703 (1985)

    Google Scholar 

  22. Heglund, N. C., Taylor, C. R. & McMahon, T. A. Scaling stride frequency and gait to animal size: mice to horses. Science 186, 1112–1113 (1974)

    Article  ADS  CAS  Google Scholar 

  23. 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, 133–141 (1991)

    Article  CAS  Google Scholar 

  24. Szentesi, P., Zaremba, R., van Mechelen, W. & Stienen, G. J. M. ATP utilisation for calcium uptake and force production in different types of human skeletal muscle fibres. J. Physiol. Lond. 531, 393–403 (2001)

    Article  CAS  Google Scholar 

  25. Armstrong, R. B. & Laughlin, M. H. Metabolic indicators of fibre recruitment in mammalian muscles during locomotion. J. Exp. Biol. 115, 201–213 (1985)

    CAS  Google Scholar 

  26. Hochachka, P. W., Bianconcini, M., Parkhouse, W. D. & Dobson, G. P. On the role of actomyosin ATPase in regulation of ATP turnover rates during intense exercise. Proc. Natl Acad. Sci. USA 88, 5764–5768 (1991)

    Article  ADS  CAS  Google Scholar 

  27. Waterlow, J. C. Protein turnover with special reference to man. Q. J. Exp. Physiol. 69, 409–438 (1984)

    Article  CAS  Google Scholar 

  28. Brody, S. Bioenergetics and Growth (Hafner, New York, 1945)

    Google Scholar 

  29. Fuery, C. J., Withers, P. C. & Guppy, M. Protein synthesis in the liver of Bufo marinus—cost and contribution to oxygen consumption. Comp. Biochem. Physiol. A 119, 459–467 (1998)

    Article  CAS  Google Scholar 

  30. Weber, J. M., Fournier, R. & Grant, C. Glucose kinetics of the Virginia possum: Possible implications for predicting glucose turnover in mammals. Comp. Biochem. Physiol. 118, 713–719 (1997)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

P.W.H. and R.D.A. were supported by the NSERC, Canada; R.K.S. by the NSF in the USA. C.-A.D. was an NSERC and FCAR pre-doctoral fellow.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter W. Hochachka.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Darveau, CA., Suarez, R., Andrews, R. et al. Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166–170 (2002). https://doi.org/10.1038/417166a

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/417166a

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing