Anatomical changes in nervous and vascular systems during the transition from prosobranch to opisthobranch organization

Abstract

SUMMARYConsideration is given to the changes in organization of the nervous and vascular systems which accompanied the posterior migration of the mantle complex and assumption of slug‐like form, major adaptations incurred during the transition from prosobranch to opisthobranch organization which allowed assumption of an infaunal mode of life.An anatomical account is provided of the visceral nerve loop of several tectibranch opisthobranchs ranging from primitive to advanced: Acteon tornatilis (L.), Bulla striata Bruguiere, Akera bullata Miiller and Scaphander lignarius (L.), together with descriptions, of the vascular supply to the mantle cavity roof of Acteon and Scaphander and of circulation in the cephalopedal mass.Three major changes appear in the early evolution of the nervous system: (1) separation of pallial ganglia from the pleurals, concurrent with anterior elongation of the head‐foot, (2) initial shortening of the rear portion of the loop (Acteon) upon reduction of the nuchal area, and (3) change of innervation of part of the mantle from the right pallial ganglion to the suboesophageal, consequent upon posterior migration of the skirt. This migration caused the suboesophageal ganglion to move posteriorly, to lie adjacent to the visceral (Bulla, Akera, Scaphander), with the effect that the pallial nerve which in Acteon emerges from the suboesophageal ganglion, in these forms leaves from the visceral. Despite changes in disposition and proportion of the skirt, the fields of innervation of emergent nerves of the visceral loop, most of which wholly or partially innervate the mantle, remained relatively unchanged, though with lengthening of the free border, the left pallial ganglion came to innervate, a relatively greater length than the corresponding left pleural of proso‐branchs. The evolution of the genital ganglion, changing importance of the visceral ganglion, re‐routing of nerve tracts at the rear of the loop, and further minor changes in innervation are discussed.Vestiges of streptoneury linger at the rear of the loop, a feature explained by the relative disposition of structures innervated by ganglia there.Upon removal of the mantle complex posteriorly, the mantle cavity roof received blood from the visceral haemocoel rather than from the kidney as in prosobranchs. Acteon, which retains the typical monotocardian venous return from the cephalopedal haemocoel utilizing an afferent renal vessel, still accepts some, for the kidney lies in the thickness of the mantle skirt. With complete reduction of the nuchal region in more advanced tecti‐branchs (Scaphander), virtually all blood entering the mantle cavity roof is derived from the visceral haemocoel.Much evidence indicates that early opisthobranchs were small and lacked a gill. With subsequent increase in size, features including the siting of the kidney in the mantle cavity roof, and formation of a pallial caecum alleviated possible inadequate respiratory exchange under adverse infaunal conditions. Also a gill was re‐developed which, together with the kidney, utilizes the once efferent branchial vessel in order to return blood to the heart; it receives blood from the visceral haemocoel through the short rectal sinus (efferent renal vessel of prosobranchs) which lies on the mantle cavity floor below the gill. Separation of inflows into (1) caecum and kidney, and (2) gill then took place to ensure adequate passage of blood through both routes, especially important in Scaphander, for the gill acts as a co‐ordinated, accessory heart providing a favourable return route. A second pump is required in Scaphander in order to draw blood from the spacious visceral haemocoel, in turn drawn from a relatively more spacious cephalic haemocoel than is characteristic of prosobranchs.