Feeding kinematics and morphology of the alligator gar (Atractosteus spatula, Lacépède, 1803)

Abstract

Living gars are a small clade of seven species that occupy an important position on the actinopterygian phylogenetic tree as members of Holostei, sister‐group to teleosts, and exhibit many plesiomorphic traits used to interpret and reconstruct early osteichthyan feeding mechanisms. Previous studies of gar feeding kinematics have focused on the ram‐based, lateral‐snapping mode of prey capture found in the narrow‐snouted Lepisosteus genus, whereas this study focuses on a member of the broad‐snouted Atractosteus sister‐genus, the alligator gar (Atractosteus spatula, Lacépède, 1803). High‐speed videography reveals that the feeding system of alligator gars is capable of rapid expansion from anterior to posterior, timed in a way to generate suction, counteract the effects of a bow‐wave during ram‐feeding, and direct a unidirectional flow of water through the feeding system. Reconstructed contrast‐enhanced μCT‐based cranial anatomy and three‐dimensional modeling of linkage mechanics show that a lateral‐sliding palatoquadrate, flexible intrasuspensorial joint, pivoting interhyal, and retractable pectoral girdle increase the range of motion and expansive capabilities of the alligator gar feeding mechanism. Reconstructions of muscular anatomy, inferences from in vivo kinematics, and in situ manipulations show that input from the hyoid constrictors and hypaxials play an important role in decoupling and modulating the dual roles of the sternohyoideus during feeding: hyoid retraction (jaw opening) and hyoid rotation (pharyngeal expansion). The alligator gar possesses an intricate feeding mechanism, capable of precise control with plesiomorphic muscles that represent one of the many ways the ancestral osteichthyan feeding mechanism has been modified for prey capture.

The feeding system of Tiktaalik roseae : an intermediate between suction feeding and biting

“…3B and SI Appendix, Fig. S2A), which may allow separate axes of rotation similar to that reported for gars (34). Lateral expansion of the cheeks is used during suction feeding (5,38,45) and spiracular respiration (35).…”

“…The premaxilla and frontals form an elongate, nonsutural scarf joint with the palate and lacrimomaxillae (SI Appendix, Figs. S1J and S3B, magenta line) that spreads apart during lateral sliding of the palate (34). The posterior connection of the palate is a sliding joint with the metapterygoid and a convergently evolved basipterygoid process (Fig.…”

“…The "holostean" hyomandibula is vertically oriented, and the shallow plane of the long axis of the suspensorium (Fig. 3C, light dashed line) was thought to limit the range of lateral abduction of the cheek (38); however, the connection between hyosymplectic and palatoquadrate is entirely cartilaginous (32) and forms a flexible, "intrasuspensorial" joint that allows for a much greater range of motion during lateral abduction of the palate (34). The preopercle, quadratojugal, and circumorbitals are integrated with the hyosymplectic into a hyomandibular module (SI Appendix, Fig.…”

“…In contrast, the lacrimomaxillae are sutured to the bones of the palate (SI Appendix, Fig. S1J) and are thus part of the palatoquadrate module, which can be seen flexing relative to the circumorbitals during feeding (34). The palate and rostrum share many convergent similarities with T. roseae.…”

“…Cranial joints were compared with possible modern analogs, alligator gar (Atractosteus spatula) (32-34) and ornate bichir (Polypterus ornatipinnis) (5,32,35), which were selected on the basis of convergent feeding morphologies with T. roseae. Finally, joints between the palate, hyomandibula, and braincase were modeled with the same kinematic range of motion as reported in A. spatula for comparison purposes (34).…”