Three-Dimensional Kinematics of the Jaws and Hyoid During Feeding in White-Spotted Bamboo Sharks

Abstract

Elasmobranchs (sharks, skates and rays) use a distinct set of cartilaginous endochondral elements to capture and process prey using suction or bite mechanisms. In contrast, teleost use a complex linkage of dermal and endochondral bones to capture prey whether by suction or biting. This difference in complexity has, in part, enabled teleosts to radiate into a variety of different feeding styles where the jaw and hyoid arches are linked and function as a unit. However, elasmobranchs have decoupled depression of the lower jaw from depression of the hyoid arch and expand the buccal cavity using a different mechanism than teleosts. White-spotted bamboo sharks, Chiloscyllium plagiosum, are trophic generalists that use suction and crushing behaviors to take a wide variety of prey items. This study reconstructs the three-dimensional kinematics of the mandibular and hyoid arches during suction food capture in three bamboo sharks using X-ray Reconstruction of Moving Morphology (XROMM). In this method, two biplanar high-speed x-ray video cameras are used to record skeletal motions during feeding strikes, after which tracking data is applied to animate CT scans, from which kinematic data are compared to hypotheses regarding the feeding mechanism. This research reveals that the mandibular and hyoid arches of bamboo sharks move in previously unsuspected ways when feeding. The hyomandibular cartilage swings backward and downward up to 58° while the ceratohyal simultaneously swings backward and downward up to 66° while suction feeding. At the same time, both cartilages undergo long-axis rotation up to 50°.: the dorsal surface of the hyomandibula rotates rostrally while the dorsal surface of the ceratohyal rotates caudally. The lower jaw supinates as the mouth opens and pronates past resting position as the jaws close. The upper jaw mirrors this motion, pronating as the mouth opens and supinating as the mouth closes. The extra degrees of rotation in the hyoid arch elements may explain the remarkable variation in feeding performance of bamboo sharks. This variation in motion of hyoid motions is achieved without limiting expansion of the oral cavity, which could comprise suction generation. Long-axis rotation of the jaws may function to enhance grasping of prey by exposing more tooth rows to the prey when feeding, while otherwise maintaining a more hydrodynamic profile. The additional motions and mechanisms of the jaws and hyoid during feeding may provide bamboo sharks with an adaptation to take to a wide variety of prey items despite specializations for suction feeding.