Colubraria muricata

Oliverio, Marco & Modica, Maria Vittoria, 2010, Relationships of the haematophagous marine snail Colubraria (Rachiglossa: Colubrariidae), within the neogastropod phylogenetic framework, Zoological Journal of the Linnean Society 158 (4), pp. 779-800 : 788-792

MORPHOLOGY OF COLUBRARIA MURICATA

Head-foot ( Figs 1B , 2 )

Head small, with a pronounced neck, oriented markedly leftwards. Tentacles long and slender, tapering towards the tip. Eyes small, and placed on swellings near the base of the tentacles. Rhynchostome rounded and minute; sharp snout between the tentacles. Foot quite small, rounded posteriorly, with a propodium divided into two slightly marked flaps; pedal gland detected neither by visual inspection nor in sections. Columellar muscle simple, flat, quite robust, and about half a spire whorl long. In males, large penis, extending backwards from behind the right tentacle. Background colour whitish, with reddish brown areas on the tentacles, the head behind the eyes, the neck, and part of the propodium. Operculum elliptical and thin, corneous, brown (semitransparent brownish in juveniles), smaller than the aperture of the shell, and with a terminal nucleus.

Mantle organs ( Fig. 2 )

Pallial cavity quite broad and deep. Siphon long, thick, and pronounced. Osphradium occupying about one third of the mantle cavity, bipectinate, with the right filaments about double the length of the left filaments. Osphradial axis broad. Ctenidium long (about twice the osphradium length), narrow, and curved leftwards, with a narrow ctenidial vessel. Gill elements consisting of triangular lamellae. Roof of the pallial cavity occupied by a broad and whitish hypobranchial gland, which produces large quantities of mucus. Rectum extremely thin and narrow, opening in a simple anus in the anterior third of the mantle. Anal gland absent. In females, right side of the mantle occupied by a large pallial oviduct.

Visceral mass and digestive system ( Figs 2 , 3 ) Visceral mass about 3.5 spire whorls long, with the clearly visible stomach covering 1.5 whorls. Kidney whitish, with a single lobe and a branched structure. Heart relatively big (about a quarter of the kidney in volume). Broad renal afferent vessel, with two branches. Anterior aorta wide, running towards the mantle cavity. Proboscis extremely long (when extended, reaching far more than three times the shell length) and thin, with scarcely muscularized walls, and with strong reddish brown pigmentation. Retracted proboscis lying, highly coiled, in the very thin-walled, transparent rhynchodaeum. A pair of powerful proboscis retractor muscles originating ventrally near the base of the proboscis sheath, and attached to the floor of the body haemocoel. Buccal cavity extremely reduced, and placed at the tip of the proboscis. Highly reduced buccal mass, ventral to the buccal cavity, connected to the internal wall of the proboscis by a thin, short muscle (which might be considered a medial odontophore retractor). Radula extremely small (400–500-mm long), rachiglossate, with 70–90 rows. Central tooth multicuspidate, with ten equal cusps, and curved; lateral teeth also multicuspidate, with nine or ten (right) and ten or 11 (left) cusps.

Proboscis artery with quite robust walls, running from the body haemocoel to the tip of the proboscis, flanked by two nervous fibres originating from the left and right cerebral ganglia, respectively. Each fibre ramified, at the proboscis tip, with branches connecting to the internal proboscis wall. Anterior oesophagus thin, and surrounded by relatively reduced circular and longitudinal muscle layers.

The typical gland and valve of Leiblein are absent. However, a small bulge of tissue, where the gland of Leiblein is normally found, seemingly connected to the oesophagus by a short duct, was observed in a single specimen. Salivary glands acinous, whitish, and elliptical: with the left gland covering the rhynchodaeum dorsally, and with the right gland lying beneath the rhynchodaeum. The salivary ducts pass externally to the nerve ring before connecting to the oesophagus, and are lined internally by very long cilia, throughout the entire length ( Fig. 3G, H ), which are grouped in a single line of tufts. The salivary ducts contact the oesophagus very near their origin, and become embedded in a single structure, with the anterior oesophagus, a couple of nerve fibres, and the proboscis artery. The ducts soon become more deeply embedded in the oesophageal wall, and run from this position to their opening in the buccal cavity, at the tip of proboscis. The accessory salivary glands are absent. The oesophagus becomes extremely thick and broad, with internal transverse folds, immediately after its passage through the nerve ring. The oesophagus is internally lined by a glandular epithelium, in which at least two different cell types can be identified: one type is ciliated and filled with fine eosinophilic granules; the second type is characterized by a mucous basophilic cytoplasm. Both cell types are of considerable size (20–40 mm in diameter). This general appearance is maintained until the opening of the oesophagus into the stomach, which hampers the distinction between the mid and the posterior oesophagus. In the absence of other topographical references, we will use the term midposterior oesophagus to describe the section that runs posteriorly to the nerve ring. The terminal tract, entering the visceral mass and opening into the stomach, is very short, quite robust, and broader than the anterior oesophagus.

The stomach is particularly long, extending for about 1.5 visceral whorls, and is crescent shaped. Gastric lumen markedly reduced, resulting in a flattened stomach. Oesophageal opening located at the anterior end of the stomach, with the intestinal opening located at its posterior end. Gastric walls extremely thin. Stomach scarcely differentiated internally, with only a few recognizable features. Welldefined transverse folds particularly developed on the surface of the dorsal wall, and partially covered by the longitudinal oesophageal ridges near to the oesophageal aperture. Folds extending from a ciliated sulcus placed on the left side of the stomach. The single opening of the digestive gland is located in the posterior part of the stomach, where the intestine begins. The intestine runs along the ventral side of the visceral spire, and is extremely thin, with a small and barely detectable anal aperture. In some specimens examined, the rectum was more discernible because of the presence of dark, spherical faecal pellets.

Reproductive systems ( Fig. 4 )

The testis and visceral spermiduct was not observed in detail; however, the spermiduct appears to be closed for its entire length, with no evidence of a gonopericardial connection. The pallial spermiduct runs inside the body wall, along the connection with the mantle. The prostatic section of the spermiduct, which is about two-thirds the length of the pallial cavity, starts shortly after the posterior end of the mantle cavity, as a slightly enlarged, glandular, and thick-walled tube, yet is not differentiated into a separate structure. The duct is thin, with a translucid appearance for the remaining anterior third, and becomes strongly coiled in the area under the penial base. The penial duct is highly muscular, broad near the penial base, and gradually tapers towards the tip. The penis is cylindrical, with a small distal papilla.

In females, the ovary is located in the right and posterior side of the visceral mass, and consists of numerous branched tubules lined with a flat epithelium. The observed specimen was probably at the end of the reproductive season, with several empty follicles coexisting with early immature oocytes. Ovarian follicles leading to a thin-walled, nonciliated coelomic oviduct, running anteriorly along the ventral side of the visceral mass. No evidence of a gonopericardial connection. Pallial glandular oviduct consisting of a proximal albumen gland that is continuous with the distal capsule gland. In dissected specimens, only a slight topographical separation was detected between the two glands, with no anatomical differentiation evident by visual inspection. Capsule and albumen glands easily discriminated by histology. Albumen gland partially visceral, consisting of large, weakly basophilic cells, and lined by a cubic epithelium with short cilia. Ciliated ventral channel connecting the albumen gland with the capsule gland; open to the lumen of the capsule gland throughout its whole length. Capsule gland oval, elongated in outline, and divided in different regions. The principal region consists of two lateral lobes that are yellowish and granulated in dissected specimens. The glandular cells of these areas produce acidophilic and eosinophilic secretion granules. Two lobes on each side of the ventral channel (not detectable in dissected specimens) produce strongly acidophilic secretions. The distal part of the pallial oviduct is continuous with the glandular structures, is barely distinguishable from them by dissection, and gradually becomes free of the mantle edge, before finally protruding inside the mantle cavity. The ciliated ventral channel continues in a strongly muscular U-shaped tube, i.e. the bursa copulatrix, with the convex side oriented dorsally, and a very narrow lumen. Bursa copulatrix proximally lined by a ciliated epithelium in continuity with the ventral channel; distally, i.e. in the direction of the female opening, gradually substituted by nonciliated columnar cells with a granular cytoplasm. Masses of unoriented spermatozoa found in the bursa copulatrix. Muscular vagina opening externally with a female aperture, and bordered by small swellings.

Remarks on other Colubraria species

The specimens of other species of Colubraria are remarkably similar to C. muricata , both in the external morphology of the soft parts and in the gross anatomy, as observed in manual dissection. In the external morphology, some variations in the colour pattern were observed that may have some taxonomic value at the species level. In the gross anatomy, the most evident differences, beside the dimensions, were observed in the shape of the penis, which showed a bulbous distal papilla in C. muricata , a short filamentous papilla in C. reticulata , and an extremely long filamentous papilla in C. tenera (about half the length of the penis) ( Fig. 4B, C ), and in the presence of a pedal gland in females of C. nitidula and C. obscura , but not observed in C. muricata .

Figures

Figure 1. Colubraria muricata (Lightfoot, 1786), the type species of the genus. A, Colubraria muricata feeding on a Siganus sp. at Santo Island (Palliculo Bay; depth, 11 m; photo S. Schiaparelli). B, the cephalic region of C. muricata from Santo Island. C, shells of C. muricata from the Philippines (photo G. & P. Poppe).

Figure 2. Mantle organs of a dissected male specimen of Colubraria muricata. A, mantle dissected medially. B, body wall dissected dorsally. Abbreviations: an, anus; ct, ctenidium; dg, digestive gland; fo, foot; go, gonad; hyg, hypobranchial gland; lsg, left salivary gland; mtl, mantle; os, osphradium; pe, penis; pr, proboscis; re, rectum; ry, rhynchodaeum; st, stomach. Scale bar: 1 cm.

Figure 3. Digestive system of Colubraria muricata. A, radula. B, radular central tooth. C, the foregut from the proboscis tip to the mid-posterior oesophagus. D, the dissected stomach. E, longitudinal section of the proboscis tip, showing the buccal mass. F, transversal section of the proboscis. G, enlargement of the anterior oesophagus of F. H, transversal section of the anterior oesophagus at the base of the proboscis. Abbreviations: aoe, anterior oesophagus; bm, buccal mass; in, intestine; lsg, left salivary gland; mo, mouth; mpoe, mid-posterior oesophagus; nf, nerve fibre; nr, nerve ring; od, odontophore; pa, proboscideal artery; pr, proboscis; prr, proboscis retractor muscle; pw, proboscis wall; ra, radula; re, rectum; rsg, right salivary gland; sd, salivary gland duct; stl, stomach lumen. Scale bars: A, 50 mm; B, 25 mm; C, D, 10 mm; E–H, 100 mm.

Figure 4. Reproductive system of Colubraria muricata. A, a male with the body wall dissected dorsally. B, distal penis with papilla penialis of Colubraria tenera. C, distal penis with papilla penialis of Colubraria reticulata. D, distal portion of the spermiduct. E, semischematic drawings of the male reproductive system in C. muricata. F, semischematic drawings of the male reproductive system in some neogastropods [e.g. Nucella canaliculata (Duclos, 1832) or Anachis lyrata (Sowerby, 1832); modified after Houston (1976) and deMaintenon (1999)]. H, semischematic drawings of the female reproductive system in some neogastropods [e.g. Buccinum undatum Linnaeus, 1758, or Nucella emarginata (Deshayes, 1839); modifiend after Houston (1976) and deMaintenon (1999)]. I, semischematic drawings of the female reproductive system in C. muricata. Abbreviations: ag, albumen gland; bc, bursa copulatrix; cg, capsule gland; fgo, female genital opening; gpcd, gonopericardial duct; ig, ingesting gland; ki, kidney; ov, ovarium; pc, pericardium; pe, penis; ped, penial duct pp, papilla penialis; pro, prostatic opening in the mantle cavity; prs, prostate; te, testis; vd, vas deferens; ve, vestibulum. Scale bars: A, 1 cm; D, G, 1 mm.