Autotomy of cerata by the nudibranchMelibe leonina(Mollusca): ultrastructure of the autotomy plane and neural correlate of the behaviour

Abstract

A strong aversive stimulus, such as a firm pinch, to a ceras of the nudibranch molluscMelibe leonina, is both necessary and sufficient to cause autotomy (rapid severance) of the ceras at a predictable site at its base (autotomy plane). Ceratal autotomy, in concert with swimming behaviour, may be a means of escaping crab predators. Cerata are innervated by ceratal nerves, which branch from the pleural nerves. Within each ceras, the corresponding ceratal nerve extends to a variable number of peripheral ceratal ganglia and an offshoot runs to two interconnected nerve rings within the ceratal autotomy plane. The nerve rings and their connectives contain innervated granule-filled cells. (GCs) that are morphologically distinct from gliointerstitial cells. Cytoplasmic processes of GCs impinge onto the basal laminae and associated connective tissue fibrils of the four structures that cross the autotomy plane: epidermis, digestive gland, longitudinal muscle bands and ceratal nerve. The distribution of GCs and their degranulation during autotomy suggests a role in the autotomy mechanism. Ceratal autotomy is accompanied by strong contraction of sphincter muscles flanking the autotomy plane and of longitudinal muscle bands within the ceras. Muscle contraction appears to assist in the autotomy mechanism by placing tensile stress on tissues at the level of the autotomy plane. Wound closure following autotomy is effected by contraction of the sphincter muscles. Extracellular recordings from nerves emanating from ceratal peripheral ganglia show a long-lasting train of large amplitude, compound spike bursts following an aversive stimulus to the ceratal epidermis or a suprathreshold stimulus to a nerve entering a peripheral ganglion. The patterned output precedes ceratal autotomy. Intracellular recordings from ceratal ganglia suggest that the patterned output is generated by a group of ganglion cells (synchronous response (SR) neurons) that fire synchronously. I argue that SR neurons are efferents to ceratal muscles and that SR neurons participate in ceratal autotomy by signalling strong, synchronous contractions of these muscles.