A comparative investigation of cranial morphology, mechanics, and muscle function in suction and bite feeding sharks

Jason B Ramsay, University of Rhode Island


Investigation of ligament morphology and musculoskeletal mechanics in elasmobranchs that use suction (white-spotted bamboo shark, Chiloscyllium plagiosum and Ornate wobbegong, Orectolobus ornatus), bite (sandbar shark, Carcharhinus plumbeus) and generalist (suction and bite, spiny dogfish, Squalus acanthias) feeding mechanisms reveal ligament morphologies and musculoskeletal mechanics specific to feeding mode, and novel ligament linkages in obligate suction feeders ( C. plagiosum and O. ornatus) that couple jaw and hyoid depression. In vivo data of muscle strain, activation, skeletal kinematics and buccal pressure during suction capture and prey processing in C. plagiosum support the function of linkage systems in suction feeders during both behaviors. The arrangements of the postspiracularis (LPI), hyomandibuloceratohyal (LHCC), hyoidiomandibular (LHMM) and hyomandibuloceratohyomandibular ligaments (LHCM) morphology at the chondrocraniohyomandibular (CHMA), hyomandibuloceratohyal (HMCA) and hyomandibulomandibular (HMMA) articulations are specific to feeding mode. The LPI and LHCC in Chiloscyllium plagiosum and Orectolobus ornatus and Squalus acanthias forms a moveable pulley and tether system that link hyomandibula (HMD) depression with ceratohyal (CER) in suction feeders and feeding generalists. The LHMM is split into two divisions in the four species the LHMM (medial division) and LHML (lateral division). The LHMM of C. plumbeus and S. acanthias forms a twisting linkage between the HMDs and CERs that results in anterolateral and ventral motion of the HMD in bite and generalist feeders. Musculoskeletal morphology and mechanics underlining jaw and hyoid depression and jaw adduction in Chiloscyllium plagiosum, Carcharhinus plumbeus, and Squalus acanthias reveal a mosaic of convergent and divergent features. Coracomandibularis (CM, jaw depressor) physiological cross-sectional PSCA is the main contributor to variation in force output to the lower jaw during jaw depression in the three species. Morphology of the coracohyoideus (CH) and coracoarcualis (CA) (hyoid depressors) are similar in the three species. Mechanics of hyoid depression in C. plagiosum differ from C. plumbeus and S. acanthias in that the initial in-lever is much smaller than the other species due to alignment of the hyoid with the hyomandibuloceratohyal articulation. Application of four-bar linkage mechanics to the jaws and hyoid of C. plagiosum suggests that the jaw and hyoid depression are linked by the lateral hyoidiomandibular ligament (LHML-linkage) and result in levels of force transfer to the jaws and hyoid during suction feeding that are greater than that possible from un-linked systems. The jaw adductors and protruders in the three species, quadratomandibularis (QM), preorbitalis (PO) and levator palatoquadrati (LP, a jaw proturder in C. plumbeus only), are subdivided and complex in architecture. Simultaneously measurement of hyoid and jaw kinematics, buccal pressure and fascicle shortening and muscle activity in the CM, CH and CA using Sonomicrometry in Chiloscyllium plagiosum reveal interaction of the feeding muscles and the LHML-linkage. Active shortening of the CM occurs prior to the onset of jaw opening and buccal pressure decrease, while jaw depression to peak gape occurs during CM lengthening. The CH actively lengthens and the CA actively shortens prior to jaw and hyoid depression. Peak active CM shortening, onset of active CH shortening, depression of the hyoid, and buccal pressure decrease occur simultaneously. A catch mechanism involving the LHML, LHMM and CM that would allow the CH to be lengthened by the CA and released, resulting in high-powered expansion during suction feeding is proposed. The CM initiates jaw lower depression while the CH and CA drive the jaw and hyoid to peak depression. The LHML in bamboo sharks appears to be a biomechanical link coupling lower jaw and hyoid depression that is convergent with the mandibulohyoid ligament in bony fishes. During bite processing, the CM shortens to depress the lower jaw and hyoid. Elevation of the hyoid prior to the onset of jaw depression results in increased positive orobranchial pressure and may help to secure prey in the mouth when the jaws are repositioned to deliver a processing bite. However, the LHML-linkage may constrain PO and QM function. (Abstract shortened by UMI.)

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Recommended Citation

Jason B Ramsay, "A comparative investigation of cranial morphology, mechanics, and muscle function in suction and bite feeding sharks" (2012). Dissertations and Master's Theses (Campus Access). Paper AAI3526224.