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

Abstract

SUMMARY 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±24μm2 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 O2demand) 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 PO2distribution suggests such integrated structural modifications are required to maintain adequate oxygen delivery (calculated PO2 5.15±0.02 kPa and 5.21±0.01 kPa in small and large fish, respectively).