The mechanical properties of the mantle muscle of European cuttlefish (Sepia officinalis)

Abstract

The circular muscles surrounding the mantle cavity of European cuttlefish (Sepia officinalis) generate the mechanical power to compress the cavity, forcing a jet of water out of the funnel propelling the animal during jet propulsion swimming. During ontogeny, jetting frequency decreases in adults compared to juveniles, and this is expected to be reflected in the contractile properties of the locomotory muscles. To develop greater insight into how the locomotion of these animals is powered during ontogeny, we determined the mechanical properties of bundles of muscle fascicles during isometric, isotonic and cyclic length changes in vitro, at two life stages: juveniles and adults. The twitch kinetics were faster in juveniles compared to adults (twitch rise time 257 ms compared to 371 ms; half twitch relaxation 257 ms compared to 677 ms in juveniles and adults, respectively), however, twitch and tetanic stress, the maximum velocity of shortening and curvature of the force-velocity relationship did not differ. Under cyclic conditions, net power exhibited a ∩-shaped relationship with cycle frequency in both juveniles and adults; the frequency at which maximum net power was achieved was shifted to lower cycle frequencies with increased maturity, which is consistent with the slower contraction and relaxation kinetics in adults compared to juveniles. The cycle frequency at which peak power was achieved during cyclical contractions in vitro, was found to match that seen in vivo in juveniles, suggesting power is being maximised during jet propulsion swimming.

Male and female syringeal muscles exhibit superfast shortening velocities in zebra finches

“…Even so, disparities between twitch speed and shortening velocities have been shown in other muscles. For example, in cuttlefish ( Sepia officinalis ) mantle muscle, juveniles have significantly faster twitches than adults, but shortening velocities do not differ between the two age groups ( Gladman and Askew, 2022 ). These disparities were suggested to result from twitch dynamics being more closely aligned with cyclic muscle performance than with shortening velocity ( Gladman and Askew, 2022 ; Marsh, 1990 ).…”

“…For example, in cuttlefish ( Sepia officinalis ) mantle muscle, juveniles have significantly faster twitches than adults, but shortening velocities do not differ between the two age groups ( Gladman and Askew, 2022 ). These disparities were suggested to result from twitch dynamics being more closely aligned with cyclic muscle performance than with shortening velocity ( Gladman and Askew, 2022 ; Marsh, 1990 ). Twitch activation and relaxation times are determined by the deactivation of cross-bridge cycling.…”

“…The high energetic costs associated with rapid deactivation mean that isometric contractile properties are usually tightly coupled with the operating frequency of muscle seen during movement and, in this case, song. This is achieved by maintaining a specific ratio between contraction kinetics and cycle duration, regardless of whether the muscle is activated through a single stimulus or through a burst of stimuli ( Askew and Marsh, 2001 ; Gladman and Askew, 2022 ; Marsh, 1990 ). Girgenrath and Marsh (1999) emphasised the close link between muscle operating frequency and twitch duration across a range of taxa, and demonstrated that faster twitches were strongly associated with greater cycle frequencies.…”

“…At higher frequencies (200 Hz) this declines to ∼2 W kg −1 . Disparities between cyclic and instantaneous power is a common feature, where cyclic power output is between 15 and 33% of instantaneous power in locomotory muscles ( Ellerby and Askew, 2007 ; Gladman and Askew, 2022 ; James et al, 1996 ). Our estimates of power output at 40°C suggest that the maximum cyclic power output is 15–26% of the instantaneous power output.…”

Male and female syringeal muscles exhibit superfast shortening velocities in Zebra finches

“…Therefore, we suspect that with additional birds, data distribution would separate more strongly. Additionally, disparities between twitch speed and shortening velocities have been shown in other muscles (Gladman and Askew, 2022;Marsh, 1990). For example, in cuttlefish (Sepia officinalis) mantle muscle, juveniles have significantly faster twitches than adults, but shortening velocities do not differ between the two age groups (Gladman and Askew, 2022).…”