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Elastic recoil action amplifies jaw closing speed in an aquatic feeding salamander.

ABSTRACT: Tendon springs often influence locomotion by amplifying the speed and power of limb joint rotation. However, less is known about elastic recoil action in feeding systems, particularly for small aquatic animals. Here, we ask if elastic recoil amplifies the speed of gape closing during aquatic food processing in the Axolotl (Ambystoma mexicanum). We measure activation of the adductor mandibulae externus via electromyography and strain of the jaw adductor muscle-tendon unit (MTU), and gape kinematics via fluoromicrometry. The muscle is pre-activated coincident with gape opening, which causes MTU stretch. Activation lasts significantly shorter for fish than cricket processing, and muscle shortening during MTU lengthening yields significantly greater elastic strain for cricket processing. The speed of MTU shortening, which dictates the speed of gape closing is 2.5-4.4 times greater than the speed of the initial shortening of the muscle fascicles for fish and cricket gape cycles, respectively. These data demonstrate a clear role for elastic recoil, which may be unexpected for a MTU in a feeding system of a small, aquatic animal. Amplification of jaw-closing speed resulting from elastic recoil likely confers ecological advantages in reducing prey escape risks during food processing in a dense and viscous fluid environment.

SUBMITTER: Rull M

PROVIDER: S-EPMC7287362 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Caecilians (Lissamphibia: Gymnophiona) are unique among vertebrates in having two sets of jaw-closing muscles, one on either side of the jaw joint. Using data from high-resolution X-ray radiation computed tomography scans, we modelled the effect of these two muscle groups (mm. levatores mandibulae and m. interhyoideus posterior) on bite force over a range of gape angles, employing a simplified lever arm mechanism that takes into account muscle cross-sectional area and fibre angle. Measurements of lever arm lengths, muscle fibre orientations and physiological cross-sectional area of cranial muscles were available from three caecilian species: Ichthyophis cf. kohtaoensis; Siphonops annulatus; and Typhlonectes natans. The maximal gape of caecilians is restricted by a critical gape angle above which the mm. levatores mandibulae will open the jaw and destabilize the mandibular joint. The presence of destabilizing forces in the caecilian jaw mechanism may be compensated for by a mandibular joint in that the fossa is wrapped around the condyle to resist dislocation. The caecilian skull is streptostylic; the quadrate-squamosal complex moves with respect to the rest of the skull. This increases the leverage of the jaw-closing muscles. We also demonstrate that the unusual jaw joint requires streptostyly because there is a dorsolateral movement of the quadrate-squamosal complex when the jaw closes. The combination of the two jaw-closing systems results in high bite forces over a wide range of gape angles, an important advantage for generalist feeders such as caecilians. The relative sizes and leverage mechanics of the two closing systems allow one to exert more force when the other has a poor mechanical advantage. This effect is seen in all three species we examined. In the aquatic T. natans, with its less well-roofed skull, there is a larger contribution of the mm. levatores mandibulae to total bite force than in the terrestrial I. cf. kohtaoensis and S. annulatus.

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Elastic recoil action amplifies jaw closing speed in an aquatic feeding salamander.

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