Convergence in morphology and masticatory function between the pharyngeal jaws of grass carp,Ctenopharyngodon idella, and oral jaws of amniote herbivores

Abstract

The cellulose-rich walls that protect plant cells are difficult to digest, and therefore mechanical food processing is a key aspect of herbivory across vertebrates. Cell walls are typically broken down by translation of flattened teeth in the occlusal plane (i.e. grinding) as part of a complex, rhythmic chewing stroke. The grass carp, Ctenopharyngodon idella, is a voracious, invasive herbivorous fish that relies solely on its pharyngeal teeth, located in the back of the throat, for mechanical processing of plant material. Here, we describe the musculoskeletal anatomy of the pharyngeal jaws of grass carp and use XROMM to quantify chewing kinematics and muscle strain. The pharyngeal jaws are suspended in a sling of 11 muscles and maintain no bony articulation with any other skeletal elements in the head. The jaws bear long, serrated teeth that are worn during use into flattened tooth cusps. Our kinematic data show that this wear is the result of the teeth being elevated into occlusion against the basioccipital process and keratinous chewing pad, not tooth-on-tooth occlusion. Pharyngeal jaw elevation results from large strains in the jaw elevator muscle, the levator arcus branchialis V, to drive a pulley-like mechanism that rotates the jaws about a pivot point at the symphysis between the left and right pharyngeal jaws. These complex, rhythmic jaw rotations translate the teeth laterally across the chewing surface throughout the occlusion phase. The grass carp chewing system is strikingly similar in gross morphology and masticatory function to herbivorous chewing strategies in other vertebrates.