Urosalpinx cinerea, (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 : 484-486

UROSALPINX CINEREA (SAY 1822)

Material examined

Indian River, Delaware ( USNM 890947).

External anatomy and mantle cavity

Mantle edge smooth. Siphon opening to bipectinate osphradium approximately one half length of ctenidium. Anterior pedal gland opening under flap along broad margin of propodium. Paired ventral openings to foot sole comprising ventral pedal gland (in females) and accessory boring organ. Operculum present.

Reproductive system

Oviduct entering anterior end of large albumen gland ( Fig. 2H , ag). Posterior portion of albumen gland visceral, lying alongside kidney ( Fig. 2H ). Small, blind diverticulum present at junction between renal and glandular oviducts, representing vestigial gonopericardial canal, but not contacting pericardium. Capsule gland (cg) composed of regionated epithelium, comprising right, left and antero-ventral (right) lobes. Ventral channel extending anteriorly to vestibule at anterior end of capsule gland. Small duct connecting ventral channel with large, muscular bursa copulatrix (bc) lying below glandular oviduct. Vestibule narrowing to long vagina. Vagina curving around bursa, opening to mantle cavity via simple female opening (fo).

Proximal vas deferens convolute, functioning as seminal vesicle. Broad base of large, glandular prostate opening to mantle cavity via narrow slit. Prostate narrowing anteriorly. Closed pallial vas deferens crossing neck to short, narrowly triangular, spatulate penis lying behind right cephalic tentacle. Penial duct extending subcentrally to tip, connected to surface by visible suture.

Alimentary system

Foregut. Radula rachiglossate. Large pleurembolic proboscis present. Radular ribbon lying in deep sulcus between paired cartilages. Robust sclerite, composed of homogeneous cuticle, dorsally lining buccal cavity, juxtaposed with grooved, ventral cuticle. Salivary glands by-passing nerve ring, entering buccal cavity dorso-laterally. Accessory salivary glands present, opening via common duct. Ventral folds within anterior oesophagus absent ( Fig. 10G ).Valve of Leiblein present. Gland of Leiblein large and complex. Ampulla of gland of Leiblein entering afferent renal vessel.

Midgut. Midgut lying short distance behind kidney. Gastric lumen small, U-shaped ( Fig. 19B ). Oesophagus opening to posterior tip of gastric chamber from left (e). Posterior-most oesophagus elongating dorsoventrally, folds diminishing. Dorsal oesophageal roof becoming rounded, ventral floor becoming narrow, Vshaped channel. Ventral channel continuous with deep vestibule containing two large, asymmetrical ducts of digestive gland (dgd). Vestibule lying to right of oesophageal aperture, along inner wall of gastric chamber. Low fold (gp) bounding lip of vestibule continuous with major typhlosole (t1). Posterior tip of gastric chamber terminating in shallow pouch (po) ventral to oesophageal aperture. Gastric shield absent. Ciliary currents in vestibule flowing into intestinal groove. Ciliary currents flowing from left to right out of blind pouch, and clockwise in main gastric chamber, toward vestibule along ventral floor. Style sac region (ss) bearing paired typhlosoles (t1, t2), and long, broad region of irregularly transverse folds bearing differentiated cilia. Currents flowing clockwise in style sac. Crystalline style absent.

Hindgut. Intestine exiting style sac region ( Fig. 19B , int), extending anteriorly and towards left along surface of viscera. Intestine crossing from left to right ventrally behind pericardium and kidney, then turning anteriorly at right side of kidney. Branching anal gland lying under well-developed tissue of hypobranchial gland, opening to rectum just behind anus.

Reno-pericardial system

Afferent renal vessel entering kidney floor anteriorly, to right of nephropore in front of reno-pericardial canal. VARV extending posteriorly within floor, supplying approximately three main vessels that ramify along right wall. DARV branching soon after emerging from floor, supplying excretory tissue along front wall and in roof. DARV turning posteriorly near roof, continuing back alongside nephridial gland. Primary and secondary tubules pycnonephridial, interdigitating broadly within roof. Nephridial gland present.

Nervous system and sensory structures

Nervous system epiathroid, right zygoneurous, left dialyneurous. All ganglia except visceral ganglia concentrated in circum-oesophageal nerve ring. Many fine branches of single tentacular nerve innervating cephalic haemocoel and tentacle. Single, dominant tentacular nerve running to tip of tentacle. Small siphonal ganglion present at point of dialyneury between nerve from left pleural ganglion and nerve from anterior osphradial nerve originating from supra-oesophageal ganglion. Visceral loop bearing two visceral ganglia overlying posterior oesophagus. Statocysts with single statoliths just below circum-oesophageal nerve ring, near pedal ganglia.

Remarks

Houston (1976) provided an analysis of reproductive morphology of this species that is congruent in most respects to the description here. But Houston reported a centrally placed penial duct and did not describe the vestigial connection to the mantle cavity in the male, nor the vestigial gonopericardial canal in the female. Houston also found orientated spermatozoa attached to the ventral channel of the capsule gland; this could not be confirmed in the material examined here.

Carriker (1943) provided a thorough description of proboscis structure and function, foregut anatomy and the circum-oesophageal nerve ring, with the exception of tentacular nerve branching patterns and the siphonal ganglion.

Discussion

A wealth of anatomical data is available for muricids, revealing a rich source of variability in all organ systems. For example, in females, a gono-pericardial connection may be present ( Fretter, 1941; Houston, 1976) or absent ( Houston, 1976). Unlike other neogastropod families, the albumen gland displays two distinct morphologies, either linear or U-shaped ( Kool, 1993). There may be a connecting duct between the capsule and albumen glands, or only a simple constriction may separate the two ( Houston, 1976). Sperm storage structures between the albumen and capsule glands may comprise a single ingesting gland with the duct acting as a seminal receptacle ( Fretter, 1941), or paired storage structures, an ingesting gland anteriorly and a seminal receptacle posteriorly. The duct of the ingesting gland typically arises from the capsule gland ( Houston, 1976). In addition, orientated spermatozoa may be attached to the unciliated, columnar epithelium of the capsule gland’s ventral channel ( Fretter, 1941; Houston, 1976), or lie within outpocketings of the albumen gland ( Kool, 1993). The anteroventral lobe of the capsule gland may be present or absent ( Wu, 1973). The bursa copulatrix may be continuous with the capsule gland ( Kool, 1993) or separate from it, lying dorsally or ventrally to the oviduct ( Fretter, 1941; Houston, 1976; Kool, 1993). In females, the foot bears an accessory boring organ located within a pore that may or may not be separate from the ventral pedal gland ( Fretter, 1941; Ponder, 1973; Kool, 1993).

In males, the vas deferens is highly convoluted ( Fretter, 1941) or rather straight ( Houston, 1976). There may be a small diverticulum off the vas deferens that is connected to the pericardium by connective and muscle tissue, or there may be no trace of a gonopericardial connection ( Fretter, 1941). Communication between the prostate and mantle cavity is absent, or present via a slit or a short ciliated duct ( Fretter, 1941; Houston, 1976; Kool, 1993). The penis is dorso-ventrally flattened with ducts either centrally or subcentrally located ( Fretter, 1941; Houston, 1976); the pallial vas deferens may be open ( Kool, 1993) or closed with a visible suture connecting the duct to the surface ( Fretter, 1941; Kool, 1993).

The Muricidae is one of only several neogastropod families to possess a cuticular lining of the buccal epithelium ( Ponder, 1973), rendering homology of this structure to the jaws of other caenogastropods uncertain ( Ponder & Lindberg, 1997). Typically, the dorsal salivary glands are massive, but the accessory salivary glands are present or absent, paired or single, with paired accessory glands typically sharing a common duct ( Haller, 1888; Amaudrut, 1898; Wu, 1965; Ponder, 1973; Wu, 1973; Kool, 1993).

Muricids possess a large, complexly folded gland of Leiblein, with a well-developed terminal ampulla that varies in length ( Haller, 1888; Amaudrut, 1898; Hirsch, 1915; Wu, 1965; Kool, 1993) but is commonly described as lying within the afferent renal vein ( Haller, 1882; Carriker, 1943; Kool, 1993). The midoesophagus contains a region of highly glandular dorsal folds that also varies in length, which passes into the duct of the gland of Leiblein ( Haller, 1888; Hirsch, 1915; Graham, 1941; Wu, 1965; Ponder, 1973; Kool, 1993).

The midgut is U-shaped with paired ducts opening to an often large and deep vestibule ( Haller, 1888; Hirsch, 1915; Wu, 1965; Smith, 1967; Kool, 1993; Medinskaya, 1993). Similar to the present findings, Haller (1888) and Smith (1967) found a deep oesophageal groove that opens directly to the vestibule. The lip of the vestibule is formed by a fold of variable height, functionally separating the ducts from the gastric chamber. The fold passes more or less directly into the major typhlosole ( Wu, 1965; Kool, 1993; Medinskaya, 1993) and may bear a remnant of the gastric shield ( Smith, 1967).

The style sac region, comparable to the so-called ‘zone of compaction’ ( Smith, 1967; Medinskaya, 1993) or ‘intestine’ ( Kool, 1993), is characterized by the presence of parallel, transverse folds bearing differentiated cilia (present study), but has been reported to be cuticularized ( Medinskaya, 1993). The region of horizontal folding in the style sac varies considerably in length between species ( Wu, 1965; Smith, 1967; Kool, 1993; Medinskaya, 1993). Previous studies have consistently reported that ciliary currents beat out of the oesophagus and toward the duct vestibule ( Wu, 1965; Smith, 1967), clockwise within the gastric lumen and compacting area ( Wu, 1965; Smith, 1967; Medinskaya, 1993), and out of the vestibule into the intestinal groove ( Wu, 1965; Medinskaya, 1993).

Graham (1949) examined several muricids, including Urosalpinx cinerea . However, Graham’s description of the muricid midgut differs fundamentally from those discussed above; the major typhlosole bounds the inner edge of the duct vestibule, whereas in all other muricids, this typhlosole bounds the outer edge of the vestibule. This reversal of topological relationships may be a printing error. Moreover, ciliary currents flow away from, rather than toward, the duct vestibule along the ventral floor of the gastric chamber ( Fig. 19B ) and only a single duct of the digestive gland is present.

Muricid nervous systems are epiathroid, dialyneurous and zygoneurous ( Haller, 1882, 1888; Bouvier, 1887). A siphonal ganglion is present at the site of dialyneury ( Haller, 1882). All major ganglia except the visceral ganglia are incorporated in the circumoesophageal nerve ring, with the buccal ganglia separated from the nerve ring by short connectives (Bouvier); the supra-oesophageal connective may be somewhat long ( Haller, 1882). Two (Bouvier) or three ( Haller, 1882) visceral ganglia may be present.

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 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.