The natural history, embryology, larval biology and post-larval development of Adalaria proxima (Alder and Hancock) (Gastropoda Opisthobranchia)

Abstract

Sparse and conflicting evidence concerning the mechanism and nature of developmental torsion and detorsion in the Opisthobranchia rendered necessary a full re-examination of these problems. Many contemporary general works either state or imply that during ontogeny opisthobranchs undergo 180° torsion (being identical with diotocardian prosobranchs in this respect) which is reversed in an unknown manner at some later stage of development. This theory is based on the work of Pelseneer (1911); the more detailed work of Saunders & Poole (1910) on Aplysia conflicts with Pelseneer’s views, but nevertheless these views have found wide currency. For this study, a species of dorid nudibranch, Adalaria proxima , was selected, for certain singular features of its biology rendered it possible to rear small populations through the com plete life cycle in the laboratory. A. proxima has an annual life cycle, the adults in nature dying after spawning, and their place being taken by the new generation of juvenile dorids. Death after spawning is correlated not with exhaustion of the germ cells, but with exhaustion of the food reserves built up in the pre-sexual phases of the life cycle. The species feeds mainly on an encrusting polyzoan, Electra pilosa , the dorid buccal pump playing an important part in the feeding mechanism . The spawn of Adalaria proxima shows the typical features characteristic of the egg masses of northern benthic invertebrates. The eggs are large, the number of eggs produced is small, the embryo hatches at a relatively advanced stage after a protracted em bryonic period. The early cleavage stages follow in all important respects the sequence and arrangement found in all dextrally organized gastropods. Gastrulation takes place by epiboly and the veliger form is rapidly assumed. Torsion in Adalaria is pushed back so far into development that it is no longer recognizable as a mechanical process. All the organs, as they become recognizable in sectioned postgastrulae, are arranged in the post-torsional positions, although the process of torsion has been halted far short of the full 180° found in living Diotocardia. The appearance of eyes, the development of the propodium and the structural and histological changes undergone by the mantle fold approximately 3 weeks after oviposition mark a departure from the pattern of embryonic development found in other species of dorid nudibranchs (Thompson 1957). Most of the organ systems are relatively greatly advanced in the hatching larva o Adalaria . The enlargement of the left midgut diverticulum brings about a slight rotation (continued during pelagic life) of the stomach; this is a process which is independent of torsion and was mentioned by Saunders & Poole, who, however, placed a slightly different interpretation upon it. Both dextral and sinistral components are present in the relations between the visceral and cephalopedal parts of the embryonic and larval body, but there can be no doubt that the dorids are truly dextral organisms. A complex arrangement of embryonic body cavities is present; it seems clear that the ‘coelom’ of Aplysia (Saunders & Poole 1910) corresponds to the inner perivisceral cavity of Adalaria , and that the term coelom in this connexion is a misnomer. The pelagic phase is divided into two distinct stages, during the first of which the larvae swim upwards, this behaviour being reversed at the start of the second stage. Searching behaviour characterizes the second stage alone, the selection of a suitable substrate for settlement being governed by an elaborate and highly specific sensory mechanism. Metamorphosis will only occur on a live colony of the encrusting polyzoan Electra pilosa . The cephalopedal ciliary apparatus directs a feeding current into the mouth; normal further development will, however, take place even in sterile sea-­water. The larval shell is a hyperstrophic one. Retraction of the larval body is brought about by the larval retractor muscle aided in a co-ordinatory capacity by contraction of muscular elements of the inner perivisceral membrane and of the cephalopedal subepidermal muscle complex. Metamorphosis involves drastic changes, but no change in basic orientation. Detorsion and reversal of visceral flexure are brought about in two stages as the mantle fold first becomes inverted and then spreads over the dorsal surface of the post-larva. The widely stated view that the dorsal integument of the adult dorid is the product o f the evolutionary enclosure of the shell by epipodial folds is contradicted by the embryological evidence. The larval retractor muscle disappears and the muscle complex of the adult is derived from the larval subepidermal muscle complex. The perivisceral cavities are obliterated and the adult haemocoel is derived from the larval cephalopedal subepidermal blastocoelic spaces. Calcareous spicules are laid down in the mantle. Concentration and fusion of the nerve ganglia result in a symmetrical arrangement, the embryonic system having shown traces of the ancestral streptoneury. A discussion of the nature of torsion in opisthobranchs almost entirely disagrees with the views of Pelseneer (1911). All the available evidence implies that torsion in opisthobranchs is greatly modified and never approaches the full 180° twisting found in living Diotocardia. It is not, of course, suggested that Pelseneer’s basic conclusion, that the prosobranchiate condition is ancestral to the opisthobranchiate, is in need of revision. Torsion in lying as it does at the extreme opposite end of the scale from the Diotocardia, is greatly modified and is no longer recognizable as a mechanical process ; torsion in Adalaria does not occur for the same reasons as were important to the ancestral veliger, for in the dorids the larval mantle cavity does not serve to accommodate the head during retraction. The Suggestion is made that the usual manner of referring to torsion during development as involving a movement of the pallial complex from a posterior to an anterior position, is inaccurate and results from any attempt to describe ontogenetical torsion from the study of the adult gastropod alone. Finally, attention is drawn to the paradox that, although the dorid nudibranchs are the most highly evolved gastropods living (speaking in terms of gross structure), the com plex evolutionary steps which have led to the dorid have resulted in a secondary return, in many respects, to the original condition. In the adult dorid, only unimportant traces remain of the three most important steps in the structural evolution of the gastropods, visceral flexure, torsion, and bilateral asymmetry.