Adaptations for extremely high muscular power output: why do muscles that operate at intermediate cycle frequencies generate the highest powers?

The pectoralis muscles of the blue-breasted quail Coturnix chinensis generate the highest power output over a contraction cycle measured to date, approximately 400 W kg(− 1). The power generated during a cyclical contraction is the product of work and cycle frequency (or standard operating frequency), suggesting that high powers should be favoured by operating at high cycle frequencies. Yet the quail muscles operate at an intermediate cycle frequency (23 Hz), which is much lower than the highest frequency skeletal muscles are capable of operating (~ 200 Hz in vertebrates). To understand this apparent anomaly, in this paper I consider the adaptations that favour high mechanical power as well as the trade-offs that occur between force and muscle operating frequency that limit power. It will be shown that adaptations that favour rapid cyclical contractions compromise force generation; consequently, maximum power increases with cycle frequency to approximately 15–25 Hz, but decreases at higher cycle frequencies. At high cycle frequencies, muscle stress is reduced by a decrease in the crossbridge duty cycle and an increase in the proportion of the muscle occupied by non-contractile elements such as sarcoplasmic reticulum and mitochondria. Muscles adapted to generate high powers, such as the pectoralis muscle of blue-breasted quail, exhibit: (i) intermediate contraction kinetics; (ii) a high relative myofibrillar volume; and (iii) a high maximum shortening velocity and a relatively flat force-velocity relationship. They are also characterised by (iv) operating at an intermediate cycle frequency; (v) utilisation of asymmetrical length trajectories, with a high proportion of the cycle spent shortening; and, finally, (vi) relatively large muscles. In part, the high power output of the blue-breasted quail pectoralis muscle can be attributed to its body size and the intermediate wing beat frequency required to generate aerodynamic force to support body mass, but in addition specialisations in the contractile and morphological properties of the muscle favour the generation of high stress at high strain rates. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10974-022-09640-2.