Skeletal kinematics of the hyoid arch in the suction-feeding sharkChiloscyllium plagiosum

Abstract

White-spotted bamboo sharks, Chiloscyllium plagiosum, generate strong suction-feeding pressures that rival the highest levels measured in ray-finned fishes. However, the hyostylic jaw suspension of these sharks is fundamentally different from the actinopterygian mechanism, including more mobile hyomandibulae, with the jaws and ceratohyal suspended from the hyomandibulae. Prior studies have proposed skeletal kinematics during feeding in orectolobid sharks from indirect measurements. Here, we tested these hypotheses using XROMM to measure cartilage motions directly. In agreement with prior hypotheses, we found extremely large retraction and depression of the ceratohyal, facilitated by large protraction and depression of the hyomandibula. Somewhat unexpectedly, XROMM also showed tremendous long-axis rotation (LAR) of both the ceratohyal and hyomandibula. This LAR likely increases the range of motion for the hyoid arch by keeping the elements properly articulated through their large arcs of motion. XROMM also confirmed that upper jaw protraction occurs before peak gape, similarly to actinopterygian suction feeders, but different from most other sharks in which jaw protrusion serves primarily to close the mouth. Early jaw protraction results from decoupling the rotations of the hyomandibula, with much of protraction occurring before peak gape with the other rotations lagging behind. In addition, the magnitudes of retraction and protraction of the hyoid elements are independent of the magnitude of depression, varying the shape of the mouth among feeding strikes. Hence, the large variation in suction-feeding behavior and performance may contribute to the wide dietary breadth of bamboo sharks.

Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro

“…Notably, the range of motion about the major rotational axis (16 deg) was smaller than the hyomandibular rotations that have been described or inferred in other elasmobranchs (Dean and Motta, 2004b;Scott et al, 2019). In an XROMM analysis, the bamboo shark's hyomandibulae were found to rotate substantially about their long axes, which was not found here (Scott et al, 2019).…”

“…Notably, the range of motion about the major rotational axis (16 deg) was smaller than the hyomandibular rotations that have been described or inferred in other elasmobranchs (Dean and Motta, 2004b;Scott et al, 2019). In an XROMM analysis, the bamboo shark's hyomandibulae were found to rotate substantially about their long axes, which was not found here (Scott et al, 2019). From external video, dissection and manipulation, the hyomandibulae of the lesser electric ray (Narcine bancroftii) were inferred to depress in a similar ventromedial direction as in P. motoro, but to a far greater degree, in order to facilitate the extreme protrusion performance of N. bancroftii (Dean and Motta, 2004a).…”

Early shape divergence of developmental trajectories in the jaw of galeomorph sharks

“…The fixation was rinsed, and the bamboo shark embryos were transferred through an Ethanol/100 mM Tris pH 7.5 series (25%, 50% and 80%, with 25 mM MgCl 2 ), while the catsharks were transferred directly to Ethanol 100%. To estimate the developmental stage, the external morphology was compared with available defined stage tables for each species [ 33 , 40 ].…”

“…In particular, Scyliorhinus canicula (hereafter referred to as catshark), is considered a model species in experimental biology [ 35 ]. Recently, the orectolobiform bamboo shark has been used in many developmental [ 36 – 38 ], and biomechanical studies [ 39 , 40 ]. Both species have similar trophic ecologies, although with noticeable differences in their behaviours [ 35 , 41 ].…”

Long-Axis Rotation of Jaws of Bamboo Sharks (Chiloscyllium plagiosum) During Suction Feeding

“…Jaw LAR has been hypothesized for anteaters ( Naples 1999 ), bats ( Kallen and Gans 1972 ), Tenrec ( Oron and Crompton 1985 ), a cichlid fish ( Aerts 1985 ), oceanic sharks ( Frazzetta and Prange 1987 ; Chappell and Seret 2021 ), and white spotted bamboo sharks ( Ramsay and Wilga 2007 ). Since the advent of XROMM, LAR has also been confirmed for limb bones during locomotion ( Kambic et al 2014 ; Mayerl et al 2019 ) and hyoid elements during feeding ( Scott et al 2019 ).…”