Strombus mutabilis, SWAINSON 1821

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 : 462-464

STROMBUS MUTABILIS SWAINSON 1821

Material examined

Okinawa, Japan ( USNM 890936 ). Only preserved material was available for study, thus SEM micrographs of complete midgut morphology were difficult to obtain and were supplemented with camera lucida drawings of dissected material .

External anatomy and mantle cavity

Anterior pedal gland opening to shallow groove along narrow tip of well-demarcated propodium. Operculum spatulate with free, pointed tip, bearing numerous small cusps along one edge. Head directed toward left, bringing left eye into inhalant margin. Mantle margin smooth with single, small pallial tentacle within exhalent margin. Hypobranchial gland large and well-developed.

Reproductive system

Gonad dorsally overlying digestive gland to base of kidney. Gonopericardial canal absent. Oviduct opening to glandular pallial oviduct at base of mantle cavity ( Fig. 2D ). Albumen gland (ag) comprising a highly complex and convoluted system of enclosed glandular folds. Capsule gland (cg) short and simple, open along entire length.

Renal oviduct opening to rounded base of albumen gland (= uterine ball) with complex, internally folded structure. Single-groove portion of albumen gland (no dotted line) proceeding anteriorly from uterine ball to base of oviductal groove. Albumen gland turning back upon itself at U-shaped junction with double groove portion (with dotted line) of albumen gland. Doublegroove portion of gland, accommodating bi-directional flow of eggs, extending posteriorly, past uterine ball, to uterine apex. Apex simple with no uterine arms. Albumen gland extending anteriorly from apex, terminating blindly past anterior tip of capsule gland. Capsule gland small, composed of two glandular laminae bordering deep oviductal groove. Narrow, ciliated egg groove traversing side of foot from tip of capsule gland to anterior pedal gland.

Bursa copulatrix (bc) and seminal receptacle (rcs) present. Bursa lying between capsule gland and blind tip of albumen gland, containing mass of unorientated sperm. Receptacle lying posterior to U-junction of single- and double-groove portions of albumen gland. Receptacle muscular and lobulate with many rounded chambers containing orientated sperm. Narrow ducts of receptacle and bursa opening to common muscular aperture inside oviductal groove near connection between albumen and capsule glands. Common aperture also opening to albumen gland at U-junction.

Vas deferens emerging from testis, rapidly expanding into large, convoluted seminal vesicle. Seminal vesicle narrowing slightly before discharging to base of pallial gonoduct. Proximal portion of gonoduct forming crescentic prostate ( Fig. 3D , pr), composed of two short laminae with open, shallow intervening groove. Seminal groove extending forward from prostate to penis (pe) lying behind right cephalic tentacle on side of neck. Penis long, muscular, with narrow base. Seminal groove continuing along ventral aspect of penis, terminating at bifid tip.

Alimentary system

Foregut. Mouth at tip of long, extensible snout. Paired jaws present at anterior ends of dorsal folds; jaw composed of rods with laterally overlapping homogeneous layer. Sub-radular membrane incompletely covering odontophore. Sub-radular organ present ( Fig. 5D , sro) forming small, rounded protuberance within shallow sublingual cavity. Radular sac straight, extending short distance back from buccal cavity. Salivary gland ducts passing through nerve ring. Glandular mid-ventral fold present ( Fig. 8E , vf), beginning within buccal cavity, extending into anterior oesophagus. Short ventro-lateral folds present within anterior oesophagus ( Fig. 9E , vlf). Glandular outpocketings of anterior oesophagus absent. Dorsal folds long and slender in cross-section, curving medially. Mid-oesophagus expanding into large, sac-like crop, lined with thin, pendulous longitudinal folds; septate oesophageal gland absent.

Midgut. Oesophagus entering midgut ventrally, on left ( Figs 12B, e ). Lumen of midgut elongate and roughly conical, curving and narrowing to shallow pouch (ce) on left side. Well-developed sorting area (sa) lining left wall, extending posteriorly from oesophageal aperture. Large, free-standing vertical flap (if) separating intestinal and oesophageal apertures. Several low folds (cf) on right side of sorting area, extending posteriorly and terminating near posterior tip of gastric chamber. Digestive gland ducts paired (dgd); anterior duct opening under lip of style sac (ss), posterior duct opening mid-ventrally to left of glandular pad (gp). Prominent gastric (gs) shield present ventrolaterally on right. Glandular pad barely projecting posteriorly past gastric shield. Proximal, free tip of major typhlosole extending into gastric chamber. Style sac (ss) and intestine (int) separate. Suture visible within style sac where typhlosoles have fused; ciliary tract of tall cilia on major typhlosole visible projecting from suture into style sac ( Fig. 21C ). Style sac epithelium bearing differentiated cilia. Crystalline style present. Ciliary currents unknown.

Hindgut. Intestine exiting directly from gastric chamber, looping under proximal style sac, extending to right through anterior lobe of digestive gland to kidney. Intestine curving dorsally over posterior end of kidney, then turning anteriorly.

Reno-pericardial system

Kidney large, elongate ( Fig. 22D ). Excretory lamellae extending within kidney roof and along right wall. Nephridial gland (ng) present forming broad, flat, narrowly triangular organ within roof. Afferent renal vessel entering kidney posteriorly, extending forward within kidney floor, supplying approximately four to six clusters of excretory tissue along right wall. Afferent renal vessel emerging from floor near renopericardial canal, curving dorsally past nephropore (np), supplying nephridial gland, traversing midline of gland.

Nervous system and sensory structures

Nervous system epiathroid, right and left dialyneurous. Nerve ring lying immediately behind buccal mass at base of snout. Buccal ganglia present at back of buccal mass just anterior to nerve ring. Supraoesophageal and sub-oesophageal connectives long. Accessory pedal ganglia present. Tentacular nerve bifid, bearing prominent tentacular ganglion at base of tentacle. Paired visceral ganglia present straddling oesophagus near base of cephalic haemocoel. Two statocysts with large, ovoid statoliths lying dorsolaterally on pedal ganglia behind pedal connectives. Large eyes well above tentacle bases. Osphradium long and bipectinate, extending from inhalant margin to base of mantle cavity.

Discussion

In general, existing descriptions of strombid female reproductive anatomy do not allow comparisons to homologous organs found in other caenogastropods. For example, Reed (1995b) described only a single type of glandular cell comprising the ‘uterus’ in six species of Strombus . However, there are two types of gland present in S. mutabilis , homologues of the albumen and capsule glands of other caenogastropods. The open ‘uterine terminus’ described by Reed (1995b) undoubtedly corresponds to the capsule gland, although this portion of the oviduct is much shorter in S. mutabilis .

Similarly, sperm storage organs of Strombus species have been rarely described (e.g. Haller, 1893; Woodward, 1894; Bergh, 1895a). While clarifying the presence of both a receptacle and a bursa, Reed (1995b) identified the anterior-most storage structure as a receptacle, the more posterior structure a bursa copulatrix, based on inferred functional criteria. However, the alternative interpretation offered here, based on the presence of orientated vs. unorientated sperm, is consistent with the position of putative homologues in other caenogastropods. Strombus mutabilis is noteworthy among strombids in possessing two openings to the albumen gland; one communicating with the joint receptacle/bursa aperture and a second opening broadly to the capsule gland.

Male reproductive anatomy of Strombus mutabilis is congruent with previous descriptions ( Bergh, 1895a; Risbec, 1927; Reed, 1995a). The penes in Strombus species vary in the presence or absence of ‘auxiliary prongs’ and the size and shape of finger-like projections at the tip of the verge ( Bergh, 1895a; Risbec, 1927; Reed, 1995a); alternatively, the penis may be long and narrow with a blunt, deeply incised tip ( Woodward, 1894).

The strombid mid-oesophagus is often described as a simple, conducting tube. However, the presence of a voluminous crop ( Woodward, 1894; Amaudrut, 1898; Risbec, 1927), as well as the presence of prominent, longitudinal folds ( Haller, 1893; Amaudrut, 1898; Graham, 1939) has been reported in several species.

Although existing descriptions are rarely sufficiently detailed to place all aspects of midgut morphology into a comparative context, it is clear that the strombid midgut is characterized by the presence of a separate style sac, a prominent curving gastric shield and two digestive gland apertures ( Haller, 1893; Woodward, 1894; Bergh, 1895a; Risbec, 1927). Little’s (1965) more detailed description identified several features congruent with the present description, including a sorting area to the left of the oesophagus, folds bounding the sorting area that extend into the gastric chamber, a glandular pad that extends a short distance posteriorly from the gastric shield, and a free major typhlosole tip projecting from the style sac lip. With rare exceptions ( Risbec, 1927), position of the digestive gland ducts is rather conservative: one adjacent to the style sac and a second near the gastric shield ( Haller, 1893; Woodward, 1894; Bergh, 1895a; Little, 1965).

Anatomical studies including the reno-pericardial system identify the presence of a nephridial gland in Strombus ( Haller, 1893; Bergh, 1895a; Risbec, 1927). Little’s (1965) more detailed investigation of Strombus gigas clearly described the dorsal branch of the afferent renal vessel supplying the nephridial gland and is depicted along the midline of the gland.

Strombid nervous systems have been described consistently as dialyneurous, zygoneurous, with two visceral ganglia ( Bouvier, 1887; Haller, 1893; Bergh, 1895a; Amaudrut, 1898; Risbec, 1927; Little, 1965). Minor differences include the condition of the tentacular nerve, which may be single ( Little, 1965), single with a tentacular ganglion ( Risbec, 1927) or bifid and lacking a tentacular ganglion ( Bouvier, 1887). Position of the statocysts appears to be variable within strombids, and has been described as anterior ( Bouvier, 1887; Haller, 1893; Bergh, 1895a; Little, 1965) or posterior ( Woodward, 1894) to the pedal ganglia.

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 5. Histology of subradular organ. (A) Neocyclotus dysoni ambiguum. Transverse section. Note bi-layered jaw. Scale bar = 0.5 mm. (B) Marisa cornuarietis. Sagittal section. Note bi-layered jaw. Scale bar = 0.5 mm. (C) Lampanella minima. Transverse section. Note jaw with exposed rods. Scale bar = 1 mm. (D) Strombus mutabilis. Transverse section. Scale bar = 0.5 mm. (E) Crepidula plana. Transverse section. Scale bar = 1 mm. (F) Littorina littorea. Sagittal section. Scale bar = 1 mm. (G) Neverita duplicata. Transverse section. Scale bar = 0.5 mm. (H) Panarona clavatula. Transverse section. Scale bar = 1 mm. Abbreviations: c., radular cartilage; j, jaw; mo, mouth; r, radula; srm, subradular membrane; sro, subradular organ.

Figure 8. Histology of anterior oesophagus; ventral fold. (A) Macleaniella moskalevi. Scale bar = 0.5 mm. (B) Theodoxus fluviatilis. Scale bar = 0.5 mm. (C) Neocyclotus dysoni ambiguum. Scale bar = 0.5 mm. (D) Lampanella minima. Scale bar = 1 mm. (E) Strombus mutabilis. Scale bar = 0.5 mm. (F) Littorina littorea. Scale bar = 0.5 mm. (G) Cypraea robertsi. Note that ventral fold is offset to the right. Scale bar = 0.5 mm. Abbreviations: bp, buccal pouch; bg, buccal ganglion; c., radular cartilage; ceg, cerebral ganglion; df, dorsal fold; e.g. oesophageal gland; r, radula; sgd, salivary gland duct; sgl, salivary gland; vf, ventral fold; vlf, ventro-lateral fold.

Figure 9. Histology of anterior oesophagus; ventro-lateral folds. (A) Macleaniella moskalevi. Scale bar = 0.5 mm. (B) Theodoxus fluviatilis. Scale bar = 0.5 mm. (C) Neocyclotus dysoni ambiguum. Scale bar = 0.5 mm. (D) Lampanella minima. Scale bar = 1 mm. (E) Strombus mutabilis. Scale bar = 0.5 mm. (F) Crepidula plana. Scale bar = 1 mm. (G) Bithynia tentaculata. Scale bar = 1 mm. (H) Littorina littorea. Scale bar = 0.5 mm. Abbreviations: bp, buccal pouch; bg, buccal ganglion; ca, radular cartilage; ceg, cerebral ganglion; df, dorsal fold; e, oesophagus; r, radula; sgl, salivary gland; vf, ventral fold; vlf, ventro-lateral fold.

Figure 12. Midgut morphology of taxa examined only from preserved material. (A) Theodoxus fluviatilis, left lateral view. Second digestive gland duct to right of oesophageal aperture obscured by gastric shield. (B) Strombus mutabilis, dorsal view. Scale bar = 1 mm. Abbreviations: c, caecum; ce caecal extension; cf, ciliated fold; dgd, digestive gland duct; ds, deep sac; e, oesophagus; gp, glandular pad; gs, gastric shield; if, intestinal flap; ig, intestinal groove; int, intestine; 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 22. Kidney morphology; basal caenogastropods with undifferentiated lamellae. (A) Neocyclotus dysoni ambiguum, lateral view. Dotted line indicates removed lateral lobe overhanging pericardium. Scale bar = 1 mm. (B) Bithynia tentaculata, dorsal view. Scale bar =.5 mm. (C) Petaloconchus varians, ventral view. Horizontal line indicates base of mantle cavity. Excretory tubules within pallial portion revealed by ventral incision. Scale bar = 0.5 mm. (D) Strombus mutabilis. Dorsal view. Scale bar = 1 mm. Abbreviations: arv, afferent renal vessel; au, auricle; ng, nephridial gland; np, nephropore; per, pericardium; rpc, reno-pericardial canal; ve, ventricle.