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First published online April 26, 2005
Journal of Experimental Biology 208, 1635-1644 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01548
Review article: Activity-induced variation of metabolism |
Exercise-induced maximal metabolic rate scales with muscle aerobic capacity
Institute of Anatomy, University of Bern, Baltzerstrasse 2 3000 Bern 9, Switzerland
* Author for correspondence (e-mail: hoppeler{at}ana.unibe.ch)
Accepted 17 February 2005
Summary
The logarithmic nature of the allometric equation suggests that metabolic
rate scaling is related to some fractal properties of the organism. Two
universal models have been proposed, based on (1) the fractal design of the
vasculature and (2) the fractal nature of the `total effective surface' of
mitochondria and capillaries. According to these models, basal and maximal
metabolic rates must scale as M3/4. This is not what we
find. In 34 eutherian mammalian species (body mass Mb
ranging from 7 g to 500 kg) we found
O2max to scale
with the 0.872 (±0.029) power of body mass, which is significantly
different from 3/4 power scaling. Integrated structure-function studies on a
subset of eleven species (Mb 20 g to 450 kg) show that the
variation of
O2max with body
size is tightly associated with the total volume of mitochondria and of the
locomotor musculature capillaries. In athletic species the higher
O2max is linked
to proportionally larger mitochondrial and capillary volumes. As a result,
O2max is
linearly related to both total mitochondrial and capillary erythrocyte
volumes, as well as to their surface areas. Consequently, the allometric
variation of maximal metabolic rate is directly related to the scaling of the
total effective surfaces of mitochondria and capillaries, thus confirming the
basic conjecture of the second fractal models but refuting the arguments for
3/4 power scaling. We conclude that the scaling of maximal metabolic rate is
determined by the energy needs of the cells active during maximal work. The
vascular supply network is adapted to the needs of the cells at their working
limit. We conjecture that the optimization of the arterial tree by fractal
design is the result rather than the cause of the evolution of metabolic rate
scaling. The remaining question is why the energy needs of locomotion scale
with the 0.872 or 7/8 power of body mass.
Key words: metabolic rate, scaling, locomotor muscle, aerobic capacity, mitochondria, capillary, fractal design, vascular supply network, energy demand
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