The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures in Xenopus laevis

Abstract

Metabolic energy (ATP) supply to muscle is essential to support activity and behaviour. It is expected, therefore, that there is strong selection to maximise muscle power output for a given rate of ATP use. However, the viscosity and stiffness of muscle increases with a decrease in temperature, which means that more ATP may be required to achieve a given work output. Here, we tested the hypothesis that ATP use increases at lower temperatures for a given power output in Xenopus laevis. To account for temperature variation at different time scales, we considered the interaction between acclimation for 4 weeks (to 15 or 25°C) and acute exposure to these temperatures. Cold-acclimated frogs had greater sprint speed at 15°C than warm-acclimated animals. However, acclimation temperature did not affect isolated gastrocnemius muscle biomechanics. Isolated muscle produced greater tetanus force, and faster isometric force generation and relaxation, and generated more work loop power at 25°C than at 15°C acute test temperature. Oxygen consumption of isolated muscle at rest did not change with test temperature, but oxygen consumption while muscle was performing work was significantly higher at 15°C than at 25°C, regardless of acclimation conditions. Muscle therefore consumed significantly more oxygen at 15°C for a given work output than at 25°C, and plastic responses did not modify this thermodynamic effect. The metabolic cost of muscle performance and activity therefore increased with a decrease in temperature. To maintain activity across a range of temperature, animals must increase ATP production or face an allocation trade-off at lower temperatures. Our data demonstrate the potential energetic benefits of warming up muscle before activity, which is seen in diverse groups of animals such as bees, which warm flight muscle before take-off, and humans performing warm ups before exercise.

Keywords: Locomotion; Metabolic cost; Muscle performance; Temperature; Thermal acclimation.