Ilyanassa obsoletus, (SAY 1822)

Strong, Ellen E., 2003, Refining molluscan characters: morphology, character coding and a phylogeny of the Caenogastropoda, Zoological Journal of the Linnean Society 137 (4), pp. 447-554 : 482-484

ILYANASSA OBSOLETUS (SAY 1822)

Material examined

Cape Henlopen, Delaware ( USNM 890946).

External anatomy and mantle cavity

Mantle edge smooth. Siphon long with basal flaps ( Fig. 7B , si), opening to bipectinate osphradium (os). Anterior pedal gland opening under thick propodial flap. Ventral pedal gland present in females, opening mid-ventrally via small slit, just behind front edge of foot. Operculum present.

Reproductive system

Gonad dorsally overlying digestive gland on right, to base of gastric chamber. Gonopericardial canal present behind base of mantle cavity ( Fig. 2I , gpc); small flap marking entrance of canal to pericardium. Oviduct opening to small albumen gland with Ushaped lumen (ag). Three to four small pouches along crest of albumen gland possibly functioning in storage of sperm; no sperm present. Albumen gland narrowing and opening to ventral channel of capsule gland (cg), dorsally giving off narrow duct leading to lobate ingesting gland (igl). No sperm present in duct of ingesting gland. Capsule gland comprising paired, glandular laminae bearing regionated epithelium, enclosing tall, narrow lumen. Proximal capsule gland bordering albumen gland turning briefly to left, then turning anteriorly and continuing towards female opening. Ventral channel opening at anterior end of capsule gland, to short, narrow vagina, terminating in simple female opening (fo). Muscular bursa and vestibule absent; glandular tissue of distal capsule gland forming shallow pocket, possibly functioning as bursa. Vas deferens emerging from testis and expanding into large, convoluted seminal vesicle. Vas deferens narrowing near back wall of kidney. Several strands of connective tissue connecting vas deferens and pericardial wall; gonopericardial canal absent. Vas deferens opening to narrow, convoluted prostate at base of mantle cavity ( Fig. 3G ). Small diverticulum from proximal prostate ending blindly. Pallial vas deferens crossing neck and entering base of penis (pe). Penis long and dorso-ventrally flattened with spatulate tip. Penial duct (ped) running subcentrally to tip of penis.

Alimentary System

Foregut. Salivary gland ducts ( Fig. 7B , sgd) bypassing nerve ring, embedded anteriorly within dorsal folds, then curving around base of buccal cavity, opening ventrally under elongate odontophore. Accessory salivary glands and jaws absent. Three nerves from each buccal ganglion and each cerebral ganglion innervating large pleurembolic proboscis. Nerves and buccal artery entering proboscis ventrally, passing through proboscis basal septum.

Paired cartilages fused anteriorly. Lateral edges of cartilages curving dorsally, forming gutter supporting radular ribbon. Deep sulcus dorsally enclosing rachiglossate radula. Odontophore long, narrow, and dorsoventrally flattened. Radula passing over bending plane of anterior tip, extending posteriorly into deep sublingual cavity. Subradular organ absent. Unfused posterior tips of cartilages, becoming enveloped in thick sheath of muscle fibres, flanking long, straight radular sac. Paired retractor muscles connecting each bolster tip and radular sac to ventral proboscis wall (ps). Thick muscular sheet dorsally connecting bolsters. Two large sets of retractors, connecting inner sides of bolsters to dorso-lateral proboscis walls. Single, unpaired set of retractors attaching ventrally to buccal mass and posterior proboscis sheath. Two large protractors attaching laterally to posterior ends of bolsters and anteriorly to sides of proboscis. Large buccal mass filling cephalic haemocoel when retracted, projecting well past posterior end of proboscis sheath.

Dorsal folds beginning just behind mouth, continuing into anterior oesophagus, gradually migrating ventrally. Ventral folds absent within anterior most oesophagus ( Fig. 10F ). Walls of distal anterior oesophagus becoming uniformly highly folded. Valve of Leiblein ( Fig. 7B , vl) present proximal to nerve ring; gland of Leiblein present with terminal ampulla. Dorsal folds weakly developed within mid-oesophagus.

Midgut. Oesophagus opening ventrally on left ( Fig. 19A ). Well-developed sorting area present to left of oesophagus (sa). Paired digestive gland ducts (dgd) opening to right of oesophagus. Long, narrow glandular fold (gp), separating digestive gland ducts from small, ventro-lateral gastric shield (gs). Posterior gastric chamber extremely elongate (ce), lined with textured, knobby epithelium roughly arranged in longitudinal folds; irregular tufts of cilia crowning crests of folds. Ciliary currents within gastric chamber flowing posteriorly on left and anteriorly on right. Ciliary currents flowing clockwise in sorting area and adjacent to intestinal groove. Large, well-developed style sac region bearing two large typhlosoles, each possessing ciliated strip of raised cilia along inner (style sac) margins ( Figs 19A , 21H ). Typhlosoles flanking extensive region of transversely folded epithelium with differentiated cilia. Ciliary currents flowing clockwise within style sac. Crystalline style present.

Hindgut. Intestine exiting style sac, curving dorsally and slightly posteriorly around rear wall of kidney. Anal gland absent.

Reno-pericardial system

Kidney lumen elongate, projecting slightly into pallial cavity ( Fig. 23E ). Afferent renal vessel entering kidney floor anteriorly, to right of reno-pericardial canal (rpc). VARV extending posteriorly within floor, supplying numerous clusters of primary tubules along right wall. DARV extending dorsally attached to front wall of kidney, turning posteriorly within centre of kidney roof, supplying secondary tubules. Primary and secondary tubules pycnonephridial, broadly interdigitating along right side of roof. Simple, narrow, thinwalled gland of Leiblein ampulla present within afferent renal vessel, extending within DARV ( Fig. 7B , gl). Nephridial gland present.

Nervous system and sensory structures

Nervous system epiathroid, right zygoneurous, left dialyneurous ( Fig. 24G ). All ganglia except visceral ganglia concentrated in circum-oesophageal nerve ring. Cerebral (ceg) and pleural (plg) ganglia broadly fused. Single nerve splitting near nerve ring into tentacular and optic nerves. Tentacular nerve giving off several small branches before splitting into two nerves of equal size, extending length of tentacle ( Fig. 7B , tn). Buccal ganglia ( Fig. 24G , bg) present at anterior ends of cerebral ganglia. Large siphonal ganglion present ( Fig. 7B , sig) at dialyneury between nerve from left pleural and branch from anterior osphradial nerve. Posterior osphradial nerve giving rise to left arm of visceral loop. Propodial ganglia ( Fig. 24G , ppg) present at anterior ends of pedal ganglia (pdg). Paired, asymmetrical visceral ganglia ( Fig. 7B , vg) straddling posterior oesophagus. Highly asymmetrical statocysts with single statoliths present ventral to nerve ring ( Fig. 24G , sc).

Remarks

Dimon (1905) provided some preliminary observations on the external anatomy and mantle cavity, reproductive and alimentary systems. Brown (1969) gave a more detailed description of the alimentary system. The present description is congruent with that of Brown in many respects with several minor exceptions. For example, Brown described the salivary gland ducts as entering the buccal cavity dorso-laterally. Histological sections revealed here that fine ducts, embedded within the walls of the buccal mass, enter ventrally under the odontophore. Brown figured the gland of Leiblein as lacking a terminal ampulla. The ampulla was found here to enter the dorsal branch of the afferent renal vessel and is thin-walled and simpler than those in some muricids (e.g. Carriker, 1943).

Within the midgut, Brown (1969) indicated that ciliary currents adjacent to the intestinal groove flow towards the intestine. Here, these currents were found to flow transversely in the direction of the sorting area or, more posteriorly, toward the oesophageal aperture itself. In addition, Brown did not acknowledge the presence of an elongate glandular fold bounding the gastric shield.

Discussion

Like other nassariids, Ilyanassa obsoletus bears weak dorsal folds in the anterior oesophagus (= glande fromboisée) ( Graham, 1941). A valve of Leiblein and a small gland of Leiblein are present; accessory salivary glands and the anal gland are lacking ( Graham, 1941). The kidney is pycnonephridial ( Ponder, 1973).

Female reproductive anatomy of Ilyanassa obsoletus is consistent with described nassariids in the presence of a gonopericardial connection and an ingesting gland, but is unique in lacking a bursa ( Fretter, 1941; Johansson, 1957; Houston, 1976). Houston (1976) described the presence of an opening within the oviduct to the mantle cavity in Nassarius incrassatus , an aperture recorded only in several muricids ( Houston, 1976) and unknown among nassariids. Houston (1976) did not find a seminal receptacle or an ingesting gland, structures reported as present in a different analysis of the same species ( Johansson, 1957). The present study noted several outpocketings of the albumen gland. Although their function could not be confirmed, similar outpocketings are known to store sperm in other neogastropods (e.g. Kool, 1993).

In male nassariids, a diverticulum connecting the base of the prostate with the mantle lumen may be open ( Fretter, 1941), fused shut (present study), or lacking entirely ( Houston, 1976). The penial duct within the dorso-ventrally flattened penis may be subcentral (present study) or centrally located ( Fretter, 1941).

There appear to be two types of midgut organization within the Nassariidae . The midgut structure of N. incrassatus ( Smith, 1967) and Tritia fratercula ( Medinskaya, 1993) is congruent in many respects with that of Ilyanassa obsoletus , with several minor exceptions. For example, in the two former taxa, the depression bearing the paired ducts of the digestive gland is more pronounced than in I. obsoletus , and the sorting area to the left of the oesophagus is lacking. The ‘ciliary sorting area’ (Smith) of N. incrassatus is homologous to the style sac region, and the ‘posterior sorting area’, occurring ventrally in front of the intestinal groove, has no equivalent in I. obsoletus . The ‘posterior sorting area’ (Medinskaya) of T. fratercula is not equivalent to the structure of the same name in N. incrassatus , but is homologous to the style sac region. In contrast, the midgut organization of of Nassarius reticulatus ( Graham, 1949) and Cyclope neritea ( Morton, 1960) is characterized by an elongate fold bounding the oesophageal aperture to the left, separating the oesophagus from the sorting area; this fold is lacking in the other nassariids. In addition, the digestive gland ducts open to the sorting area to the left of the oesophagus and there is no fold bounding the gastric shield on the left.

The nervous system of Ilyanassa obsoletus differs from described nassariids only in minor detail ( Risbec, 1952; Fretter & Graham, 1962; Brown, 1982). For example, in I. obsoletus the left arm of the visceral loop branches from the posterior osphradial nerve near the osphradium; in other nassariids, the visceral loop arises much closer to the circum-oesophageal nerve ring (Brown) or from the nerve ring itself (Fretter & Graham). Three or five pairs of buccal nerves innervate the proboscis (Brown). The propodial ganglia may be lacking; a single visceral ganglion with two accessory ganglia may be present (Brown).

Figures

Figure 2. Female reproductive morphology. (A) Lampanella minima. Note connective tissue between renal oviduct and pericardium. (B) Crepidula plana. (C) Petaloconchus varians. (D) Strombus mutabilis. Note egg groove from capsule gland down side of foot. Dotted line indicates double-groove portion of albumen gland. (E) Cypraea robertsi. Note duct of receptacle at posterior end of albumen gland. (F) Panarona clavatula. (G) Prunum apicinum. Note that base of mantle cavity lies between the capsule and albumen glands. (H) Urosalpinx cinerea. Ventro-lateral lobe of capsule gland is shown by transparency. Note blind diverticulum off renal oviduct and small aperture connecting vestibule and bursa copulatrix. Base of mantle cavity indicated by arrow. (I) Ilyanassa obsoletus. Note shallow pocket in distal end of capsule gland, perhaps functioning as bursa. Scale bar = 1 mm. Abbreviations: ag, albumen gland; bc, bursa copulatrix; cg, capsule gland; fo, female opening; gpc, gonopericardial canal; igl, ingesting gland; mc, base of mantle cavity; per, pericardium; rcs, seminal receptacle; spb, spermatophore bursa; u, uterine ball; v, vagina.

Figure 3. Male reproductive morphology. (A) Lampanella minima. Note connective tissue between renal vas deferens and pericardium and accessory lobe of prostatic tissue on mantle cavity floor alongside proximal prostate. (B) Petaloconchus varians. (C) Crepidula plana. Note terminal papilla. (D) Strombus mutabilis. Note seminal groove continuous along ventral aspect of penis. (E) Cypraea robertsi. Note seminal groove continuous along ventral aspect of penis. (F) Prunum apicinum. Penial duct not shown. Arrow indicates slit-like communication between proximal prostate and mantle cavity. (G) Ilyanassa obsoletus. Arrow indicates fused, tube-like communication between proximal prostate and mantle cavity. Scale bar = 1 mm. Abbreviations: ped, penial duct; pe, penis; per, pericardium; pr, prostate; pvd, pallial vas deferens; sg, seminal groove.

Figure 7. Morphology of cephalic haemocoel among derived caenogastropods. (A) Panarona clavatula. Siphon obscured by left cephalic tentacle and is not visible in this view. Note large, modified left cephalic tentacle and large proboscis retractor connecting to columellar muscle. (B) Ilyanassa obsoletus. Note second visceral ganglion lying below pericardium and large radular retractors connecting to base of proboscis sheath; ampulla of gland of Leiblein visible within afferent renal vessel. Duct of gland of Leiblein stippled. (C) Nitidiscala tinctum. Note compartmentalized tissue supporting jaw and buccal ganglia lying between salivary glands where the latter enter buccal cavity. (D) Prunum apicinum. Note duct of poison gland opening mid-ventrally to base of buccal cavity, just behind opening of accessory salivary gland. (E) Conus jaspideus. Siphon not visible in this view. Note long coiled duct of poison gland; buccal ganglion visible where short arm of radular sac enters buccal cavity. Base of proboscis sheath is shown, but rhynchocoel has not been opened. Scale bar = 1 mm. Abbreviations: asg, accessory salivary gland; dasg, duct of accessory salivary gland; e, oesophagus; ec, oesophageal caecum; gl, gland of Leiblein; j, jaw; kd, kidney; nr, circum-oesophageal nerve ring; os, osphradium; per, pericardium; ps, proboscis sheath; rs, long arm of radular sac; sb, sub-oesophageal ganglion; sgd, salivary gland duct; sgl, salivary glands; si, siphon; sig, siphonal ganglion; sp, supra-oesophageal ganglion; tn, tentacular nerve; vg, visceral ganglion; vl, valve of Leiblein; z, zygoneury.

Figure 10. Histology of anterior oesophagus; ventral folding absent. (A) Neverita duplicata. Scale bar = 0.5 mm. (B) Nitidiscala tinctum. Scale bar = 0.5 mm. (C) Panarona clavatula. Scale bar = 0.5 mm. (D) Prunum apicinum. Scale bar = 0.5 mm. (E) Conus jaspideus. Scale bar = 0.5 mm. (F) Ilyanassa obsoletus. Scale bar = 0.5 mm. (G) Urosalpinx cinerea. Scale bar = 1 mm. Abbreviations: asg, accessory salivary gland; ca, radular cartilage; ceg, cerebral ganglion; df, dorsal fold; dl, duct of gland of Leiblein; e, oesophagus; int, intestine; j, jaw; ps, proboscis sheath; r, radula; sgd, salivary gland duct; sgl, salivary gland; vc, ventral channel.

Figure 19. Midgut morphology. White arrows indicate direction of ciliary currents. (A) Ilyanassa obsoletus, dorsal view. (B) Urosalpinx cinerea, dorsal view. Scale bar = 1 mm. Abbreviations: ce, caecal extension; dgd, digestive gland duct; e, oesophagus; gp, glandular pad; gs, gastric shield; ig, intestinal groove; int, intestine; po, pouch; sa, sorting area; ss, style sac; t1, major typhlosole; t2, minor typhlosole.

Figure 21. Style sac morphology; major typhlosole and ciliary tract (indicated by arrows). (A) Theodoxus fluviatilis. Scale bars (left to right) = 100 Mm, 10 Mm. (B) Neocyclotus dysoni ambiguum. Scale bars = 1 mm, 100 Mm. (C) Strombus mutabilis. Scale bars = 100 Mm, 10 Mm. (D) Crepidula plana. Scale bars = 100 Mm, 100 Mm. (E) Bithynia tentaculata. Scale bars = 1 mm, 100 Mm. (F) Cypraea robertsi. Scale bars = 1 mm, 100 Mm. (G) Conus jaspideus. Scale bars = 100 Mm, 10 Mm. (H) Ilyanassa obsoletus. Scale bars = 100 Mm, 10 Mm. Abbreviations: t1, major typhlosole; t2, minor typhlosole.

Figure 23. Kidney morphology; derived caenogastropods with two differentiated lobes of lamellae. (A) Neverita duplicata, dorsal view. Kidney opened between lobes of differentiated lamellae. (B) Cypraea robertsi, dorsal view. Intestine removed to reveal internal details. (C) Panarona clavatula, dorsal view, posterior chamber on left, anterior chamber on right. Kidney roof opened between lobes of primary and secondary lamellae. Note meronephridial condition (no interdigitation of lamellae) and that dorsal branch of afferent renal vessel supplies both primary and secondary tubules. (D) Prunum apicinum, dorsal view. Note small region of secondary tubules within kidney roof supplied by dorsal branch of afferent renal vessel. (E) Ilyanassa obsoletus, dorsal view. Note pycnonephridial condition (interdigitation of lamellae). Scale bar = 1 mm. Abbreviations: al, anterior kidney lobe; arv, afferent renal vessel; au, auricle; darv, dorsal branch of afferent renal vessel; int, intestine; ng, nephridial gland; np, nephropore; per, pericardium; pl, posterior kidney lobe; rpc, reno-pericardial canal; ve, ventricle.

Figure 24. Circum-oesophageal nerve ring morphology. (A) Neocyclotus dysoni ambiguum. Scale bar = 0.5 mm. (B) Lampanella minima. Scale bar = 0.5 mm. (C) Crepidula plana. Scale bar = 0.5 mm. (D) Cypraea robertsi. Upper diagram depicts cerebral, pleural, supra-esophageal, and sub-oesophageal ganglia; lower diagram depicts pedal ganglia and pedal cords. Scale bar = 1 mm. (E) Nitidiscala tinctum. Scale bar = 0.25 mm. (F) Prunum apicinum. Scale bar = 0.5 mm. (G) Ilyanassa obsoletus. Scale bar = 0.5 mm. Abbreviations: bg, buccal ganglion; ceg, cerebral ganglion; d, dialyneury; e, oesophagus; pc, pedal cord; pdg, pedal ganglion; plg, pleural ganglion; ppg, propodial ganglion; sb, sub-oesophageal ganglion; sc, statocone; sp, supra-oesophageal ganglion; z, zygoneury.