Defensive mechanisms in some nudibranchs

In a typical mollusc, the shell is the most important defensive mechanism. But the shell does not protect the mollusc from all predators, and it is for this reason that secondary defensive mechanisms have evolved in many species. In some cases, these secondary mechanisms become more important than the shell as a means of protection from predators, and where this occurs selection may favour the reduction and even the total loss of the shell. The shell has been lost independently in each of the nine orders of the Opisthobranchia except the Thecosomata, and in the Sacoglossa and the Nudibranchia it may have been lost two or three times. In all of these cases where the shell-less or nudibranch condition has evolved, the animal must be adequately protected by defensive mechanisms other than the shell. This thesis studies the defensive mechanisms of a number of nudibranch molluscs.
In the Sacoglossa there is a series of forms from the primitive Arthessa, with a well-developed defensive shell, through Oxynoandeuml; and Lobiger, with reduced shells, to the nudibranch Stiliger on the one hand and to the bivalved Berthelinia on the other. The defensive mechanisms of Berthelinia and Stiliger are compared. It is shown that even in Berthelinia. which is protected by a tightly closing bivalved shell, there is a secondary defensive mechanism in the form of a secretion from the hypobranchial gland. In Stiliger, the defensive mechanisms are located in the cerata. Three types of gland are present of which at least one, and probably all, are defensive. In addition the cerata can be autotomised and regenerated, and this may also be of defensive importance. It is also shown that the ceratal glands of Stiliger and the hypobranchial gland of Berthelinia are muscle-operated. It is concluded that in both Stiliger and Berthelinia the defensive system involves two or three defensive mechanisms; and there is evidence that these mechanisms act in series just as do the defensive mechanisms of many tropical insects.
The defensive mechanisms of the Doridacea are discussed. It is concluded that camouflage is of widespread occurrence, but that there is as yet no evidence for the occurrence of warning coloration. Many bright colours are deflection marks, but the importance of other bright colours is still not known. Dorsal papillae with a probable defensive function are present in some species of the Doridacea, and they are usually supplied with glands. The function of the caryphyllidia of certain species is not known. Autotomy of papillae has not been described, but autotomy of the mantle edge occurs in the Discodoridinae. Defensive glands are of widespread occurrence in the Doridacea. One type of defensive gland that has not been described before in dorids is the acid gland of Discodoris pusae and Anisodoris stellifera. Acid secretion is well known from certain other opisthobranch and prosobranch molluscs, and the discovery of its occurrence in dorids means that it has evolved independently at least four times in the Mollusca. In D.pusae and A.stellifera, the acid glands are large subepidermal pits with a mucous plug and a muscular sphincter. The acid is inorganic and contains sulphate ions. It may register pH 1 or 2 close to the skin of the mollusc. Another species of Discodoris was found to secrete acid of a similar pH. In this species acid-secretion is from the ordinary epidermal cells, and subepidermal glands are totally absent. In the light of these results, the evolution of acid-secretion is discussed.
In all four suborders of the Nudibranchia and in the Sacoglossa, species with dorsal papillae or cerata have evolved. In all cases where these have been studied, they have been found to be of defensive importance. Cerata usually contain glands, are mobile, can be autotomised without harm to the mollusc, and may have yet other defensive mechanisms. The Eolidacea are the best known of these groups with defensive dorsal papillae. In the eolids, some species are camouflaged, but none has been shown to possess warning coloration. Cerata may be brightly coloured to direct attacks away from the head, and the behaviour of the mollusc supports this view. Cerata can be autotomised and regenerated, but the ease with which autotomy occurs varies between different species, Cerata are especially sensitive at their tips, and it is shown that this is because there is a high concentration of neurosensory cilia in this region. Stimulation, by touch, of these cilia can cause ejection of nematocysts or of glandular secretions as a defensive response.
Ceratal glands are described for a number of species of solid. The role of the cellules spéciales is discussed, and it is concluded that these are not of defensive importance. Their content of RNA and of protein suggests that they synthesize protein, and their high glycogen content suggests that they are storage cells. They may have a duct in some species, and could thus be excretory.
Simple, unicellular mucous glands occur in probably all eolids, but they may be epidermal or subepidermal in different species. They probably protect the animal from abrasion. They may also be responsible for the mucin cuticle, or for the presence of a mucous film just outside the cuticle which is continuously being carried off the tips of the cerata by ciliary action. Mucous glands are the only glands present in some species, for example Eolis M and Tergipes despectus. In other acleioproct eolids there are glands which have a defensive functions the species of Catriona studied have two types of defensive gland, whilst the eubranchids studied have three and possibly five types of defensive gland. These defensive glands are usually concentrated at the tips of the cerata and are exuded when the animal is violently disturbed. Some of them are muscle-operated and are proteinaceous, others contain mucopolysaccharides or mucoproteins. In the smaller species of both Catriona and Eubranchus, the surface area of ceratal epithelium is limited, and the defensive glands are packed so as to utilize all available space. The method of packing the glands is different in the two genera, suggesting that it is a case of parallel evolution. It is further suggested that the defensive glands of Calma, Catriona and the Eubranchidae are convergent. In the cleioprocts studied, no such concentration of glands at the ceras tip was found, but all species possess two or more types of ceratal gland. There is evidence that some of these may be defensive in function.
Nematocysts are used in defence by many eolids, but for them to be effective, they must be ejected from the cnidosac and an appreciable percentage of them must explode. It is shown that whilst nematocysts are frequently ejected and exploded as a defensive reaction, there is considerable variation between different species. In Calma, glands are of considerable defensive value, but nematocysts are totally absent; whilst in Tergipes despectus, defensive glands are absent and nematocysts are important in defence. Other species utilize both defensive mechanisms, but to varying extents. In the Cleioprocta generally, and particularly in the Aeolidiidae, glands are not of great importance in defence whilst nematocysts are; but in the Eubranchidae and in Catriona glands are well-developed and of considerable defensive importance. There is even variation within one genus. Thus Catriona tina rarely uses glands but frequently uses nematocysts in defence, whilst C.perca rarely uses nematocysts but frequently uses glands. This interspecific variation in behaviour is probably related to the different predators which different species of eolid are likely to encounter.
The predators of nudibranchs in the sea are not well known, but laboratory experiments have demonstrated that many nudibranchs are relatively unpalatable to many species of fish. However, some species of fish are not deterred from eating eolids by nematocysts, and it is likely that it is with relation to these predators that glandular defensive mechanisms have evolved. Thus nematocysts may be protective against one set of predators whilst glands are protective against another set of predators.
Nematocysts may be damaging not only to potential predators of eolids, but also to the eolid itself when it crawls over coelenterates. The mechanism by which eolids escape damage from nematocysts is not known, but there is evidence that the vesicular structure of the epidermis is involved.
It is concluded that in many nudibranchs the defensive system involves several distinct mechanisms which come into action in series. There is some evidence that certain mechanisms are adapted to specific predators. The eolidiform condition is a particularly efficient defensive adaptation since it concentrates several mechanisms into that part of the mollusc which is expendible, and which is the first to be encountered by a potential predator.
Three papers are included in the appendix. The first describes the occurrence of Polycera elegans (Bergh) in Britain, and discusses its taxonomy. The second gives notice of a new species of bivalved gastropod from Jamaica, and the third is a description of this animal.