Bithynia tentaculata, (LINNAEUS 1758)

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 : 466-468

BITHYNIA TENTACULATA (LINNAEUS 1758)

Material Examined

Alexandria, Virginia ( USNM 890938).

External anatomy and mantle cavity

Mantle edge smooth. Pedal gland opening to shallow flap along anterior margin of propodium. Anterior kidney chamber extending into pallial roof. Short, monopectinate osphradium present along anterior one third of ctenidium. Operculum present.

Reproductive system

Gonopericardial canal present. Renal oviduct forming seminal receptacle bearing orientated sperm. Oviduct opening to posterior bursa just before entering glandular gonoduct. Pallial oviduct closed along entire length, opening anteriorly via short vagina. Bursa copulatrix extending posteriorly along surface of capsule gland, opening anteriorly to vagina. Vas deferens convoluted, functioning as seminal vesicle. Pallial vas deferens closed along entire length, from prostate at base of mantle cavity to tip of penis. Tubular, accessory prostate gland opening to subterminal lateral lobe of penis.

Alimentary system

Foregut. Weakly developed jaws present at anterior ends of dorsal folds; jaw composed of rods with laterally overlapping homogeneous layer. Subradular membrane incompletely covering odontophore. Subradular organ present forming vertical ridge of tissue within long, narrow sublingual cavity. Short, tubular salivary glands ( Fig. 6D , sgl) overlying nerve ring (nr). Radular sac short. Anterior oesophagus bearing single mid-ventral fold ( Fig. 9G , vf) and two, broad ventrolateral folds (vlf). Mid-ventral fold gradually merging with right glandular field posteriorly within anterior oesophagus, producing paired ventral folds with intervening ciliated groove. Ventral glandular folds diminishing through region of torsion within circumoesophageal nerve ring. Mid-oesophagus uniformly folded; septate oesophageal gland absent.

Midgut. Oesophagus ( Figs 15A, e ) opening to midgut ventrally to left of ventro-lateral gastric shield (gs). Paired, ciliated folds emerging from intestinal groove, extending posteriorly to left of oesophageal aperture. Left fold diminishing; right fold (cf) curving to right at posterior end of gastric chamber, terminating within shallow caecum (c) behind gastric shield (gs) on right. Development of fold (cf) variable, in some individuals forming shallow shelf subdividing base of gastric chamber. Glandular pad (gp) projecting only short distance posterior to gastric shield. Paired digestive gland ducts (dgd) present to left of gastric shield. Style sac region characterized by presence of paired typhlosoles (t1, t2), differentiated cilia and crystalline style. Broad tract of raised cilia (ctr) present on major typhlosole.

Hindgut. Intestine emerging from style sac, extending posteriorly beside style sac, curving around distal end of kidney, then turning anteriorly.

Reno-pericardial system

Kidney large and elongate, comprising posterior, visceral chamber and anterior pallial chamber. Visceral lumen large, extending posteriorly past pericardium ( Fig. 22B , per) to gastric chamber. Visceral lumen subdivided by vertical septum of excretory tissue beside pericardium. Pallial chamber alongside rectum, extending almost to anus, with weakly developed excretory tissue along walls surrounding large central lumen. Afferent renal vessel entering floor of visceral kidney lumen, at base of mantle cavity, in front of reno-pericardial canal (rpc) and septum. Ventral branches extending anteriorly and posteriorly, supplying excretory tissue within pallial and visceral chambers. Branch of afferent renal vessel extending dorsally, posteriorly passing nephropore (np), supplying small mass of excretory tissue, then entering nephridial gland (ng).

Nervous system and sensory structures

Nervous system epiathroid, right and left dialyneurous. Nerve ring lying just behind base of buccal mass. Tentacular nerve ( Fig. 6D , tn) with large basal swelling, splitting into three nerves of approximately equal size (one slightly larger) persisting length of tentacle. Metapodial and propodial ganglia present. Metapodial commissure present. Visceral loop bearing single visceral ganglion to right of posterior oesophagous. Statocysts with single statolith present dorso-laterally on pedal ganglia.

Remarks

There are several published descriptions on the anatomy of this species. Reproductive details have been provided in Krull (1935), Ankel (1936) and a thorough account by Lilly (1953) that is in agreement with the report here. However, Lilly, while noting the presence of sperm in the renal oviduct and unorientated sperm in the posterior bursa, identified the latter as a seminal receptacle; Fretter & Graham (1962) later identified the renal oviduct as a seminal receptacle. The gonopericardial canal has been described as present ( Krull, 1935) or absent ( Lilly, 1953).

Graham (1939) provided a brief description of the foregut, noting that the walls of the large buccal cavity are cuticularized, the salivary glands are small, and the dorsal folds conspicuous. Within the anterior oesophagus, Graham recorded the presence of paired ventral folds. Krull (1935) remarked that the jaw was composed of small scales. Gross midgut morphology was figured by Krull and elaborated by Graham. There are several discrepancies between these and the present description. Graham described both folds emerging near the minor typhlosole and intestinal groove as curving into the pocket behind the gastric shield; the latter was characterized as being dorsally situated. Digestive gland ducts have been cited as paired ( Krull, 1935) or single ( Graham, 1939; Fretter & Graham, 1962).

The pallial kidney extension was described by Lilly (1953); Fretter & Graham (1962) discussed the functional significance of this feature.

All basic features of the nervous system have been documented by Bouvier (1887); Krull (1935) made several clarifications, including the presence of a right dialyneury. Krull noted the presence of a bifid tentacular nerve and the absence of the tentacular basal swelling which disagree with the present description. The metapodial commissure has been recorded as absent ( Bouvier, 1887) or present ( Simroth, 1896 – 1907; Krull, 1935).

Discussion

Traditionally, bithyniids have been classified near ( Wenz, 1938 –44) or within ( Thiele, 1928a) the Hydrobiidae . However, bithyniids possess a number of features not found in hydrobiids, including features of the head-foot, mantle cavity, operculum, egg capsules, and differ in feeding and reproductive modes ( Taylor, 1966). In spite of these differences, Hershler & Thompson (1988) continued to support a close relationship between the Bithyniidae and the hydrobiid subfamilies Amnicolinae and Emmericiinae, based on the shared presence of a unique caecum-like accessory prostate within the penis. A preliminary phylogenetic analysis of rissooidean gastropods placed the Bithyniidae firmly within the superfamily, but suggested that the family is a divergent lineage within the group (Ponder, 1988). Preliminary results of molecular phylogenetic analysis suggest that the Bithyniidae and Hydrobiidae are not closely related ( R. Hershler, pers. comm.). In general, relationships of bithyniid gastropods to other rissooideans remains poorly understood. Despite this uncertainty, for comparative purposes discussion will be limited to hydrobiids and bithyniids.

The female reproductive system of hydrobiids consists of a coiled oviduct, a renal oviduct modified into a posterior bursa and seminal receptacle, and a closed pallial oviduct with a ventral channel; a gonopericardial duct may be present or absent ( Krull, 1935; Davis, 1980; Hershler & Davis, 1980; Davis, Mazurkiewicz & Mandravvhia, 1982; Davis & Pons da Silva, 1984; Davis & Mazurkiewicz, 1985; Hershler, 1985; Ponder et al. 1991; Hershler & Frest, 1996). In addition, much of the albumen gland lies posterior to the base of the mantle cavity. Bithynia tentaculata also possesses a coiled oviduct; the recurvent portion, rather than a discrete sac, forming a seminal receptacle as in B. caerulane ( Beliakova-Butenko, 1974) . Only the posterior bursa of B. tentaculata is visceral in position.

As in Bithynia tentaculata , hydrobiid male reproductive anatomy is characterized by the presence of a seminal vesicle, a closed prostate and pallial vas deferens and a lobate penis with the penial duct opening at its tip ( Davis, 1980; Hershler & Davis, 1980; Davis et al., 1982; Davis & Pons da Silva, 1984; Davis & Mazurkiewicz, 1985; Hershler & Frest, 1996). As stated above, bithyniids possess a unique accessory gland that opens to a lateral lobe of the penis ( Thiele, 1928a; Beliakova-Butenko, 1974), suggesting an affinity to the hydrobiid subfamilies Amnicolinae and Emmericiinae ( Seshaiya, 1930; Hershler & Thompson, 1988).

Hydrobiid and bithyniid foregut morphology is similar in that the salivary glands do not pass through the circum-oesophageal nerve ring, but lie on top of it ( Seshaiya, 1930; Hershler & Davis, 1980). Jaws are present ( Seshaiya, 1930; Ponder et al., 1991). In hydrobiids, the dorsal folds of the mid-oesophagus are so prominent as to subdivide the lumen of the oesophagus into three longitudinal channels ( Graham, 1939; Ponder et al., 1991). In one species, the central channel is completely closed off for a short distance by the fusion of the dorsal folds to the ventral wall of the oesophagus ( Bregenzer, 1916). No such subdivision occurs in Bithynia tentaculata .

Bithyniid and hydrobiid midgut morphology is rather complex, with diverse patterns of outpocketing and folding ( Hershler & Davis, 1980; Davis et al., 1982; Davis & Pons da Silva, 1984; Ponder et al., 1991; Davis & Mazurkiewicz, 1985 Hershler, 1985). Although sometimes lacking ( Seshaiya, 1930; Hershler & Davis, 1980), the caecal extension of other hydrobiids represents an outpocketing of a different part of the midgut as compared to Bithynia tentaculata , reaching its deepest dimension posteriorly or along the left side of the midgut ( Davis et al., 1982; Ponder et al., 1991). Several prominent folds originating near the oesophagus and/or intestinal groove extend across the midgut floor; a variable number of these folds terminate within the deepest part of the caecal extension ( Davis et al., 1982; Ponder et al., 1991). However, similar to B. tentaculata , one or sometimes two folds may continue around the posterior end of the midgut, terminating on the right behind the gastric shield ( Davis et al., 1982; Ponder et al., 1991).

The kidney of hydrobiids and bithyniids is large with a posterior ( Robson, 1920) or both an anterior and posterior extension ( Seshaiya, 1930; Krull, 1935). A nephridial gland is present ( Seshaiya, 1930; Krull, 1935; Ponder et al., 1991). Although Krull did not describe blood supply to the gland in Lithoglyphus naticoides , the diagrammatic representation of the kidney suggests that a large branch of the afferent renal vessel supplies the gland as in Bithynia tentaculata .

The nervous system of hydrobiids, as Bithynia tentaculata , is epiathroid and left dialyneurous ( Seshaiya, 1930; Hershler & Davis, 1980); Krull (1935) described also a right dialyneury in Lithoglyphus naticoides . Seven characteristic nerves emerge from the cerebral ganglia; the basal swelling of the tentacular nerve varies in size ( Krull, 1935; Hershler & Davis, 1980; Ponder et al., 1991). Tentacular nerve branching patterns have not been described, thus it is unknown if the trifid tentacular nerve of Bithynia tentaculata is typical. The pedal ganglia bear propodial and metapodial swellings. The metapodial commissure may be present ( Krull, 1935; Hershler & Davis, 1980) or absent ( Seshaiya, 1930).

Figures

Figure 6. Morphology of cephalic haemocoel among basal caenogastropods. (A) Neocyclotus dysoni ambiguum. For simplicity, large salivary glands removed. Scale bar = 1 mm. (B) Lampanella minima. Scale bar = 1 mm. (C) Cypraea robertsi. For simplicity, large salivary glands removed. Scale bar = 1 mm. (D) Bithynia tentaculata. Scale bar = 0.5 mm. (E) Crepidula plana. Scale bar = 1 mm. Abbreviations: bp, buccal pouch; d, dialyneury; e, oesophagus; eg, oesophageal gland; nr, circum-oesophageal nerve ring; os, osphradium; osg, osphradial ganglion; ps, proboscis sheath; sb, sub-oesophageal ganglion; sgd, salivary gland duct; sgl, salivary glands; sp., supra-oesophageal ganglion; tn, tentacular nerve; vg, visceral ganglion; z, zygoneury.

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 15. Midgut morphology. White arrows indicate direction of ciliary currents. (A) Bithynia tentaculata, dorsal view. Distal end of gastric chamber obscured in scanning electron micrograph, indicated by dotted line in diagram on right. (B) Littorina littorea, dorsal view. Stippling indicates ciliary tract within gastric chamber extending from oesophageal aperture. Scale bar = 1 mm. Abbreviations: c, caecum; ce, caecal extension; cf, ciliated fold; cs, ciliated strip; ctr, ciliary tract; dgd, digestive gland duct; e, oesophagus; gp, glandular pad; gs, gastric shield; sa, sorting area; ss, style sac; 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.