The role of an overlooked adductor muscle in the feeding mechanism of ray-finned fishes: Predictions from simulations of a deep-sea viperfish

摘要

In a majority of ray-finned fishes (Actinopterygii), effective acquisition of food resources is predicated on rapid jaw adduction. Although the musculoskeletal architecture of the feeding system has been the subject of comparative research for many decades, individual contributions of the major adductor divisions to closing dynamics have not been elucidated. While it is understood that the dorsal divisions that arise from the head and insert on the posterior of the lower jaw are major contributors to closing dynamics, the contribution of the ventral components of the adductor system has been largely overlooked. In many ray-finned fishes, the ventral component is comprised of a single division, the A(omega), that originates on an intersegmental aponeurosis of the facialis divisions and inserts on the medial face of the dentary, anterior to the Meckelian tendon. This configuration resembles a sling applied at two offset points of attachment on a third-order lever. The goal of this study was to elucidate the contributions of the A(omega) to jaw adduction by modeling jaw closing in the deep-sea viperfish Chauliodus sloani. To do this, we simulated adduction with a revised computational model that incorporates the geometry of the A(omega). By comparing results between simulations that included and excluded A(omega) input, we show that the A(omega) adds substantially to lower-jaw adduction dynamics in C. sloani by acting as a steering motor and displacing the line of action of the dorsal facialis adductor muscles and increasing the mechanical advantage and input moment arms of the jaw lever system. We also explored the effect of the A(omega) on muscle dynamics and found that overall facialis muscle shortening velocities are higher and normalized force production is lower in simulations including the A(omega). The net effect of these changes in muscle dynamics results in similar magnitudes of peak power in the facialis divisions between simulations, however, peak power is achieved earlier in adduction Modifications of muscle mechanics and posture result in significant increases in closing performance, including static bite force, angular velocity, and adduction time. We compare this configuration to a similar design in crocodilians and suggest that the A(omega) configuration and similar sling configurations across the vertebrate tree of life indicate the importance of this musculoskeletal design in feeding.