The contractile efficiency of the mantle muscle of European common cuttlefish (Sepia officinalis) during cyclical contractions.

Abstract

Escape jet propulsion swimming in cuttlefish (Sepia officinalis) is powered by the circular muscles surrounding the mantle cavity. This mode of locomotion is energetically costly compared with undulatory swimming. The energetic cost of swimming is determined by the mechanical power requirements and the efficiency with which chemical energy is transferred into useful mechanical work. One step in this energy transduction process is the transfer of energy from ATP hydrolysis into mechanical work by the muscles. Here, we determined the efficiency of this step, termed the contractile efficiency. Muscle preparations from the circular muscles of the mantle cavity were subjected to sinusoidal length changes at different cycle frequencies, and stimulated with a phase and duration that maximised initial net work. Changes in ATP, arginine phosphate and octopine content between control and exercised muscles were determined and used to calculate the energy released from ATP hydrolysis (Emet). The maximum contractile efficiency (the ratio of net work to Emet) was 0.37, occurring at the same cycle frequency at which mechanical power was maximal and that was used during jet propulsion swimming, suggesting that cuttlefish muscle is adapted to generate muscular power efficiently. The overall efficiency of cuttlefish jet propulsion swimming was estimated to be 0.17, which is broadly comparable to that measured during animal flight and human-powered pedalled locomotion, indicating the high energetic costs of jet propulsion swimming are not due to inefficient locomotion per se; instead, they result from the relatively high mechanical power requirements.