Functional morphology and biomechanics of cuticular fracture at the elytrophoral autotomy plane of the scaleworm Alentia gelatinosa (Annelida: Polynoidae)

Autotomy of the elytra (scales) in the annelid Alentia gelatinosa occurs at a breakage plane near the junction between the elytron and its elytrophore (stalk), and requires fracture of the external epidermal cuticle. The mechanism of cuticular fracture was investigated by light and electron microscopy, glycoconjugate histochemistry, direct observation of autotomy in isolated preparations, and mechanical tests. The breakage plane crosses the elytrophoral wall at a cuticular thickening and passes through the subelytral cavity between the elytron and the terminal septum of the elytrophore. At the cuticular breakage zone (CBZ), the collagenous framework of the normal cuticle is replaced with non-collagenous microfibrils. The CBZ has a complex glycoconjugate composition and includes a strongly sulfated, uronic acid-containing glycosaminoglycan and a high proportion of disulfide or sulfydryl linkages. Tonofilament-rich epidermal cells (tendon cells) are attached to the thick cuticle on the dorsal and ventral sides of the CBZ. Dorsal tendon cells have long processes that extend into the elytron near the roof of the subelytral cavity. Ventral tendon cells are linked by connective tissue to the longitudinal and terminal sphincter muscles of the elytrophore. Mechanical tests showed that the elytrophoral wall is not inherently weaker at the autotomy plane than elsewhere. It is hypothesized that at autotomy (i) contractile force generated by the sphincter muscle is transmitted through elytrophoral tendon cells to the ventral side of the CBZ and (ii) contraction of the longitudinal and main circular muscles of the elytrophore increases hydrostatic pressure in its lumen, everts the terminal septum, and generates tension that is transmitted through elytral tendon cells to the dorsal side of the CBZ. This results in stress concentration at the basal edge of the CBZ and initiates fracture. The distinctive microstructure and macromolecular composition of the CBZ may reduce its fracture toughness and make it more susceptible to brittle failure.