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First published online October 16, 2009
Journal of Experimental Biology 212, 3564-3575 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.029512

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Allometry of skeletal muscle fine structure allows maintenance of aerobic capacity during ontogenetic growth

Steven Young and Stuart Egginton^*

Department of Physiology, University of Birmingham, Vincent Drive, Edgbaston, Birmingham B15 2TT, UK

^* Author for correspondence (s.egginton{at}bham.ac.uk)

Accepted 6 August 2009

Controversy exists over the scaling of oxygen consumption with body mass in vertebrates. A combination of biochemical and structural analyses were used to examine whether individual elements influencing oxygen delivery and demand within locomotory muscle respond similarly during ontogenetic growth of striped bass. Mass-specific metabolic enzyme activity confirmed that glycolytic capacity scaled positively in deep white muscle (regression slope, b=0.1 to 0.8) over a body mass range of 20–1500 g, but only creatine phosphokinase showed positive scaling in lateral red muscle (b=0.5). Although oxidative enzymes showed negative allometry in red muscle (b=–0.01 to –0.02), mass-specific myoglobin content scaled positively (b=0.7). Capillary to fibre ratio of red muscle was higher in larger (1.42±0.15) than smaller (1.20±0.15) fish, suggesting progressive angiogenesis. By contrast, capillary density decreased (1989±161 vs 2962±305 mm^–2) as a result of larger fibre size (658±31 vs 307±24 µm² in 1595 g and 22.9 g fish, respectively). Thus, facilitated and convective delivery of O₂ show opposite allometric trends. Relative mitochondrial content of red muscle (an index of O₂ demand) varied little with body mass overall, but declined from 40% fibre volume in the smallest to 30% in the largest fish. However, total content per fibre increased, suggesting that mitochondrial biogenesis supported aerobic capacity during fibre growth. Heterogeneous fibre size indicates both hypertrophic and hyperplastic growth, although positive scaling of fibre myofibrillar content (b=0.085) may enhance specific force generation in larger fish. Modelling intracellular P_O2 distribution suggests such integrated structural modifications are required to maintain adequate oxygen delivery (calculated P_O2 5.15±0.02 kPa and 5.21±0.01 kPa in small and large fish, respectively).

Key words: enzyme activity, capillaries, oxygen tension, mitochondria, red muscle, fish

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