The functional morphology of the British Ellobiidae (Gastropoda, Pulmonata) with special reference to the digestive and reproductive systems

Abstract

The four British members of the primitive pulmonate family Ellobiidae areLeucophytia bidentata, living in crevices between tide-marks,Ovatella myosotisinhabiting salt-marshes (with an intertidal subspecies,denticula), and the fully terrestrialCarychium tridentatumandC. minimumIn the present paper we have throughout regarded the Ellobiidae as primitive pulmonates. In the following discussion, it is not intended to deal in detail with the interrelations of the various genera included within this family. InLeucophytia bidenta, the arrangement of the organs in the pallial cavity and the distribution of mucus glands upon the foot and pallial margin probably corresponds to the primitive condition of the sub-class Pulmonata. There is an unspecialized supra-anal lobe, representing the adaptive ‘ gill' of higher Basommatophora, and within the mantle cavity the gill and hypobranchial gland are unrepresented. There is a small muscular buccal mass, with a broad radula, bearing unspecialized, multiseriate teeth. Into the buccal mass opens a pair of small salivary glands. The oesophagus broadens posteriorly to form a rather more distensible crop-like region. The stomach has lost most of the features of the generalized molluscan condition. The oesophagus opens into a thin-walled ciliated oesophageal atrium, receiving the single digestive diverticulum. The atrium opens backwards into the anterior chamber of the stomach, which is capable of considerable muscular movement, and communicates in turn with a spherical gizzard, lined with cuticle and very strongly muscular. The posterior end of the stomach, corresponding to the posterior caecum, is inversible into the gizzard to form a tongue-like valve whose function is discussed. The digestive gland undergoes a cycle of ingestion, digestion, and fragmentation and excretion. Its histology during each stage is fully described and the nature of the digestive cycle is discussed. The intestine is a short tube, of simple structure, thrown into a single loop, and conveying a mucus-bound faecal string to the anus.Leucophytiais a protandrous hermaphrodite, showing a sexual succession, which is in evidence both in the condition of the gonad and in the degree of development of the genital ducts. A male phase terminates about December, followed by a stage of egg maturation, terminating with oviposition in May. The gonad leads by a little hermaphrodite duct to the point where male and female ducts. become completely divided. The female portion consists of a fertilization pouch and a posterior and anterior mucus gland, opening close to the aperture of the pallial cavity by a short muscular vagina. A long stalked bursa copulatrix opens into the genital vestibule. The male duct consists of a short posterior vas deferens, continued forward by a glandular prostate. Along the right side of the head proceeds an anterior vas deferens, which passes anteriorly into the haemocoele of the head, to open through a muscular penis which is invaginated into a preputial sac. An account is given of the egg capsules, and of the embryo, which is operculate, with a shell showing reduced heterostrophy, and with prominent vestiges of a velum. There is no free swimming stage.Ovatella myosotisshows in the alimentary canal a similar general structural pattern toLeucophytia. The chief differences lie in the structure of the stomach which is a good deal more primitive, and perhaps represents an original or basic type in the Ellobiidae. The gizzard is thinner walled but still muscular, and the posterior caecum retains its primitive form, with the posterior diverticulum still represented, opening at the mouth of the caecum into the stomach. Ciliated excurrent grooves run from both anterior and posterior diverticula to the proximal part of the intestine, and this region preserves some features of the structure, but little of the function, of the style sac. The reproductive system is also more primitive than inLeucophytiaand probably of a type basal to the family Ellobiidae. The male and female portions of the large hermaphrodite duct, though functionally divided, remain in open communication. The prostate shares a common lumen with the anterior mucus gland. The relations of the anterior vas deferens and the penis are similar to those ofLeucophytia. The egg capsules and the embryos are described, and show one or two differences fromLeucophytia. The mantle cavity in the terrestrial Carychium is characterized by a pallial gland, a tubular structure opening outside the cavity in an anterior position. Its structure, homologies and possible functions are discussed. unctions are discussed. The alimentary canal agrees in most of its features with a basic ellobiid plan, but the stomach shows a number of differences from other ellobiids studied. In particular, there is no oesophageal atrium, and both of the digestive diverticula open close together into a ciliated, spherical chamber, which also receives the oesophagus, and forms the posterior end of the stomach. The gizzard is strongly muscular and barrel-shaped, lined with cuticle. It opens anteriorly into the narrow intestine, and in the first part of the intestine the ciliary coat shows a rotatory beat reminiscent of that of the style sac. The structure and cycle of activity of the digestive gland is described in detail, with an account of the mode of formation of fragmentation phagocytes. The reproductive system shows a protandrous sexual succession like that of other ellobiids. The little hermaphrodite duct is dilated into a single pocket forming a seminal vesicle. The albumen gland is small, and opens, with the little hermaphrodite duct, into a cylindrical mucus gland, of simple structure. At the same point opens a very large, strap-shaped shell gland, a structure not represented in other ellobiids, which secretes the tough, leathery egg-capsule, surrounding each of the singly deposited eggs. There is no secretion of a common mucus coat enclosing a cluster of eggs as in marine ellobiids. For a portion of the year, during the female part of the sexual cycle, Carychium appears to be aphallic. The penis and the anterior vas deferens were found only in July, the penis being small, and of extremely simple structure. The evidence on the functional morphology of the Ellobiidae, presented in this paper, is reviewed in a discussion on the position of the family, with relation to the rest of the Pulmonata. The conclusion is reached that the Ellobiidae are by far the most primitive of existing pulmonates, and— in structure and mode of life—cannot be far removed from the earliest members of this sub-class. The alimentary canal and the reproductive system are discussed as they appear in primitive members of the three subclasses Prosobranchia, Pulmonata and Opisthobranchia. The primitive members of each of the three subclasses draw close together in a number of common characters, revealed in both the digestive and the reproductive systems. The relationship of the higher freshwater Basommatophora to the primitive marine pulmonates is dealt with in light of our knowledge of the Ellobiidae, and it is concluded that the Lymnaeidae and the families related to them show fundamental differences setting them apart from the marine pulmonates.