Abstract
Seahorses, pipefish and their syngnathiform relatives are considered unique amongst fishes in using elastic recoil of post-cranial tendons to pivot the head extremely quickly towards small crustacean prey. It is known that pipefish activate the epaxial muscles for a considerable time before striking, at which rotations of the head and the hyoid are temporarily prevented to allow energy storage in the epaxial tendons. Here, we studied the motor control of this system in seahorses using electromyographic recordings of the epaxial muscles and the sternohyoideus-hypaxial muscles with simultaneous high-speed video recordings of prey capture. In addition we present the results from a stimulation experiment including the muscle hypothesised to be responsible for the locking and triggering of pivot feeding in seahorses (m. adductor arcus palatini). Our data confirmed that the epaxial pre-activation pattern observed previously for pipefish also occurs in seahorses. Similar to the epaxials, the sternohyoideus-hypaxial muscle complex shows prolonged anticipatory activity. Although a considerable variation in displacements of the mouth via head rotation could be observed, it could not be demonstrated that seahorses have control over strike distance. In addition, we could not identify the source of the kinematic variability in the activation patterns of the associated muscles. Finally, the stimulation experiment supported the previously hypothesized role of the m. adductor arcus palatini as the trigger in this elastic recoil system. Our results show that pre-stressing of both the head elevators and the hyoid retractors is taking place. As pre-activation of the main muscles involved in pivot feeding has now been demonstrated for both seahorses and pipefish, this is probably a generalized trait of Syngnathidae.
Highlights
Constraints on muscular power generation have led to the evolution of mechanisms relying on elastic recoil to perform movements that are fast and powerful enough to capture exceptionally elusive prey
Examples of elastic energy storage and release during prey capture can be found in tongue-projection mechanisms in chameleons [1–3], salamanders [4] and toads [5], hyoid motions during intra-oral prey processing in knifefish [6], raptorial appendage strikes in mantis shrimps [7,8]), carnivorous terrestrial plants employing trap-snapping [9] or tentacle-snapping [10], and aquatic carnivorous plants generating a sudden trap inflation to produce suction [11]
The latter study showed that the epaxial muscle of the pipefish Syngnathus leptorhynchus is active for at least 200 milliseconds prior to the start of head rotation, allowing the storage of energy by stretching these tendons
Summary
Constraints on muscular power generation have led to the evolution of mechanisms relying on elastic recoil to perform movements that are fast and powerful enough to capture exceptionally elusive prey. Examples of elastic energy storage and release during prey capture can be found in tongue-projection mechanisms in chameleons [1–3], salamanders [4] and toads [5], hyoid motions during intra-oral prey processing in knifefish [6], raptorial appendage strikes in mantis shrimps [7,8]), carnivorous terrestrial plants employing trap-snapping [9] or tentacle-snapping [10], and aquatic carnivorous plants generating a sudden trap inflation to produce suction [11]. Since these movements rely on the same mechanical principles as catapults (i.e., a slow increase in strain in an elastic material during preparation, followed by a triggered release of the stored elastic energy during the launch), they are sometimes referred to as biological catapults [12]. Afterwards, the head is suddenly rotated over more than 20 degrees in less than 5 milliseconds, leaving prey almost no chance to react
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