Powering the hagfish "bite": The functional morphology of the retractor complex of two hagfish feeding apparatuses

Hagfish use forceful retractions of a dental plate to shear and ingest food. Retractile force is generated by the retractor muscle complex of the posterior hagfish feeding apparatus (HFA). While gross morphological descriptions exist, the organization of muscle and connective tissue fibers that form the soft tissue retractor complex do not. In this study, we used paraffin histology to prepare serial sections of Pacific (Eptatretus stoutii, Lockington, 1879) and Atlantic (Myxine glutinosa, Linnaeus, 1758) hagfishes in order to describe constituent soft tissue anatomy and fiber orientations. We generated 3D reconstructions in which digitized sections were segmented and fitted to volumetric scans of retractor complexes taken prior to microtomy. These models confirmed that the retractor complex is composed of a perpendicularis muscle that fits within the eye of a needle-shaped clavatus muscle, which anteriorly bears the dental plate tendon, and in turn fits within a sleeve-like tubulatus muscle. Analysis of fiber orientations within these muscles resulted in novel functional hypotheses: (a) The tubulatus muscle represents a novel tubular bipennate muscle with a considerable physiological cross-sectional area. Its activation may indirectly create tension in the dental plate tendon: as the tubulatus muscle forcefully extends, it displaces the terminal bulb and the clavatus muscle posteriorly. (b) Within the HFA terminal bulb, the muscle fibers of the clavatus and perpendicularis muscles are mutually perpendicular and may cocontract to form a swelling stopper knot-like muscular complex that resists being pulled through the tubulatus muscle. (c) While overall feeding apparatus muscle morphology is conserved, the physiological cross-sectional area of the tubulatus muscle in E. stoutii, is relatively larger than that of M. glutinosa, suggesting a more forceful retraction. The tubular bipennate construction of the tubulatus may represent a novel soft robotic actuator design.