Intrinsic Mechanics and Control of Fast Cranio-Cervical Movements in Aquatic Feeding Turtles

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Abstract
Aquatic feeding strikes on agile prey in snake-necked turtles involve fast neck extension, bucco-pharyngo-oesophageal expansion, and head retraction. The ultimate, rectilinear acceleration of the head towards the prey requires complex vertebral rotations, that vary widely from strike to strike. This poses complex motor control issues for the numerous intrinsic neck-muscles, which are the sole neck extensors. Mathematical modelling reveals that extensor activity might be superfluous for this phase of the strike. The ultimate acceleration of the head at the end of the strike always coincides with forceful oropharyngeal expansion. The momentum of the induced flow of water is sufficient to pull the head (and the neck) straight towards the prey. This buccal expansion proceeds identically to that observed in primary aquatic feeders: a rostro-caudal expansion sequence characterized by an optimal timing of the functional components supporting the expansion wave. Yet distinct structural solutions, both at the skeletal, and muscular level, are involved. This points towards prominent hydrodynamic constraints. Head and neck are retracted by extrinsic neck muscles. Given the high number of degrees of freedom, this musculo-skeletal system is obviously under-determined, which compromises control. We propose that erroneous folding of the neck (i.e., diverging from the highly persistent retracted configuration) might be avoided through the presence of a subtle click system at the level of the joint between cervical vertebrae 5 and 6.