Theodoxus fluviatilis, (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 : 451-454

THEODOXUS FLUVIATILIS (LINNAEUS 1758)

Material examined

Poitiens, France ( USNM 836154). Only preserved material was available for study. Consequently, scanning electron micrographs of complete midgut morphology were difficult to obtain and were supplemented with camera lucida drawings of dissected material. In Theodoxus fluviatilis , the midgut is rotated ~45∞ counter-clockwise within the visceral mass relative to caenogastropods (see Discussion). Thus, to facilitate topological comparisons with ingroup taxa, the midgut of was opened by a longitudinal incision along the left side.

External anatomy and mantle cavity

Anterior pedal gland opening anteriorly to shallow flap along broad propodium. Operculum present. Vestigial right gill present at base of mantle cavity below pallial glandular gonoduct.

Reproductive system

Gonopericardial canal absent. Proximal tip of glandular gonoduct embedded in visceral mass. Pallial portion of glandular gonoduct closed and diaulic. One genital opening leading to connected copulatory bursa and seminal receptacle; the former storing unorientated sperm, the latter orientated sperm.

Distal vas deferens forming highly coiled seminal vesicle. Prostate closed with distal genital aperture. Open seminal groove leading from genital aperture to penis lying on cephalic lappet to left of right cephalic tentacle.

Alimentary system

Foregut. Radula rhipidoglossate. Three paired odontophoral cartilages and one unpaired sublingual cartilage present. Subradular membrane completely covering odontophore to base of deep sublingual cavity; subradular organ absent ( Fig. 4A ). Paired glands opening ventrally to sublingual cavity. Dorsal epithelium of buccal cavity cuticularized. Discrete jaw and salivary glands absent. Mid-ventral fold low in buccal cavity ( Fig. 8B , vf), continuous with dorsal lip of radular sac. Paired lobes of glandular tissue developing below mid-ventral fold within anterior oesophagus. Low, weakly glandular ventro-lateral folds present along inner aspect of ducts to oesophageal pouches ( Fig. 9B , vlf). Glandular mid-ventral fold persisting within anterior and mid-oesophagus, through region of torsion, before diminishing. Paired oesophageal pouches present, simple anteriorly, becoming increasingly folded and glandular posteriorly, comprising continuous buccal pouches ( Fig. 9B , bp) and oesophageal glands ( Fig. 8B , eg).

Midgut. Oesophageal aperture ( Fig. 12A, e ) and posterior digestive gland duct lying to left of gastric shield (gs); anterior digestive gland duct (dgd) within deep pocket between gastric shield and style sac. Gastric shield dorsal, functionally separating oesophageal aperture and posterior digestive gland duct from gastric lumen. Ciliated fold (cf) beginning at proximal tip of minor typhlosole (t2), extending posteriorly to left of oesophagus. Ciliated fold and glandular pad (gp) curving into caecum (c) lying behind shield. Major typhlosole (t2) and several folds continuous with intestinal groove terminating at oesophageal aperture. Raised ciliary tract on major typhlosole absent ( Fig. 21A ). Deep sac ( Fig. 12A , ds) present, bounded posteriorly by lip of style sac and anteriorly by second fold, both continuous with minor typhlosole. Mouth of sac surrounded by differentiated style sac cilia. Crystalline style absent.

Hindgut. Intestine completing approximately two loops. Rectum penetrating ventricle.

Reno-pericardial system

Transverse pallial vein extending dorsally from cephalopedal sinus, splitting into afferent branchial vein and afferent renal vein. Afferent branchial vein traversing anterior wall of kidney to afferent ctenidial membrane; afferent renal vein passing through thinwalled ventral chamber of kidney (= bladder), supplying dorsal chamber containing mass of excretory lamellae. Vestigial right gill present. Blood sinus of vestigial right gill communicating directly with cephalopedal sinus. Nephridial gland absent.

Nervous system and sensory structures Circum-oesophageal nerve ring surrounding buccal mass anteriorly, with buccal connectives passing posteriorly to buccal ganglia. Nervous system hypoathroid, right zygoneurous and left dialyneurous, with paired visceral ganglia. Labial commissure present. Single pedal commissure connecting pedal ganglia. Pedal cords present. Tentacular nerve single. Statocysts with single statolith present dorsally and medially, just behind pedal commissure. Eyes on tips of short ocular peduncles.

Remarks

This species has been the subject of many anatomical investigations, emphasizing the mantle cavity, reproductive and alimentary systems. Gilson (1896), Fretter & Graham (1962) and Fretter (1946) provided information for reproductive anatomy; the latter account is the most comprehensive and details gross morphology as well as histological fine structure for both males and females.

Lenssen (1899), Bourne (1908), Graham (1939) and Whitaker (1951) provided information for the foregut. Whitaker’s account, describing the structure and function of the foregut, is the first to suggest that the outpocketings of the foregut represent continuous buccal pouches and oesophageal glands; these structures had been variously interpreted as salivary glands ( Lenssen, 1899) or simply as oesophageal pouches ( Bourne, 1908; Graham, 1939). Whitaker was also the first to recognize the presence of paired sublingual glands in this species. Whitaker acknowledges the presence of the mid-ventral fold, but does not describe the presence of ventro-lateral folds. The species possesses a seventh unpaired cartilage ( Lenssen, 1899; Bourne, 1908; Fretter, 1946); however, this supports the cuticle of the sublingual pouch and is not considered to represent part of the odontophore (cf. Sasaki, 1998).

Preliminary observations on midgut and hindgut anatomy were provided by Lenssen (1899) and were described more completely by Graham (1939) and Fretter & Graham (1962); Graham clarified the absence of the crystalline style in this species. Several findings obtained here for midgut morphology differ subtly from those reported previously ( Graham, 1939; Fretter & Graham, 1962). In the present analysis, the oesophageal aperture and one digestive gland duct were found immediately to the left of the gastric shield such that, when the midgut is closed, the shield separates them from the gastric chamber. A second digestive gland duct is present within the deep pocket between the gastric shield and style sac.

Landsburg (1882) and Lenssen (1902) provided the main points of reno-pericardial morphology and circulation, which were elaborated by Bourne (1908); Fretter (1965) primarily described blood flow through the mantle and associated organs. Blood supply to the vestigial right gill, an organ first noted by Lenssen (1902), has been attributed to a diverticulum off the transverse pallial vein ( Bourne, 1908; Fretter, 1965). However, as described above, histological sections revealed that the vestigial gill sinus opens directly to the cephalopedal sinus.

Lenssen (1902) provided a relatively thorough account of the nervous system which was refined by Bourne (1908).

Discussion

Reproductive anatomy of most neritids is highly complex, particularly among females. The pallial oviduct is typically diaulic, one aperture leading to the bursa and seminal receptacle, the second leading to the glandular oviduct, which is posteriorly embedded in the visceral mass and subdivided into capsule and albumen glands ( Bourne, 1908; Fretter, 1946, 1965; Starmühlner, 1969; Berry, Lim & Sasekumar, 1973; Houston, 1990; Haynes, 1991; Sasaki, 1998). These two parallel portions of the oviduct communicate posteriorly via a narrow duct. Some neritids possess a triaulic pallial oviduct. The third aperture is referred to as the ductus enigmaticus ( Bourne, 1908) and, as the name implies, is of uncertain function but has been suggested to regulate internal pressure by allowing water into the oviduct or excess sperm to escape ( Bourne, 1908; Fretter, 1965; Houston, 1990; Haynes, 1991). In addition, some neritids have a small duct that leads from the renal oviduct and opens to the posterior end of the mantle cavity adjacent to the vestigial right gill ( Fretter, 1965). The presence of this duct, its position within the body and its positional relationship to the vestigial gill has been interpreted as evidence that the right kidney has been integrated into the glandular reproductive tract ( Fretter, 1965), rather than forming the seminal receptacle, as suggested by Thiele (1902). This connection between gonoduct and mantle cavity is absent in Theodoxus fluviatilis ( Fretter, 1946) . Bourne (1908) described the so-called oviduco-coelomic funnel (= gonopericardial canal), which connects the gonoduct with the extensive pericardial coelom. Despite careful searching, Fretter (1965) was unable to confirm this.

Male reproductive anatomy typically consists of a testis, a distal vas deferens that is highly coiled and functions in the storage of sperm, and a highly glandular prostate that forms the spermatophore. The prostate is closed, discharging through an aperture adjacent to the anus, and is subdivided into two distinct masses of glands. The penis, when present, lies on the cephalic lappet, to the left of the right cephalic tentacle ( Bourne, 1908; Andrews, 1937; Starmühlner, 1969; Houston, 1990; Sasaki, 1998).

The relatively conservative foregut anatomy consists of paired sublingual glands opening ventrally to the buccal cavity, and confluent buccal pouches and oesophageal glands lying anterior to the region of torsion; salivary glands are absent ( Thiele, 1902; Bourne, 1908; Whitaker, 1951; Fretter, 1965). There are typically three sets of paired cartilages ( Lenssen, 1899; Bourne, 1908; Fretter, 1946; Salvini-Plawen, 1988); the median cartilages may be fused or unfused and a seventh unpaired cartilage may be present below the anterior tip of the subradular membrane ( Sasaki, 1998).

In general, the neritid midgut consists of a globular gastric chamber that bears a highly variable number of digestive gland duct openings; a small, textured pouch posterior to the gastric shield may be present ( Haller, 1894; Bourne, 1908; Fretter & Graham, 1962; Fretter, 1965). A prominent fold associated with the minor typhlosole passes posteriorly into the caecum; this fold may be absent or elaborated into a well-developed sorting area ( Fretter, 1965). Theodoxus fluviatilis remains the only neritid described possessing a small transverse pouch just within the lip of the style sac ( Graham, 1939). However, a similar pouch has been observed in Neritina reclivata (pers. obs.).

The neritid reno-pericardial system comprises an enlarged pericardial coelom, a heart with two auricles, and a long, ciliated reno-pericardial canal that opens to the dorsal, glandular portion of the two-tiered kidney ( Fretter, 1965). The ventral portion of the kidney forms a bladder into which the nephropore opens ( Lenssen, 1902; Thiele, 1902; Bourne, 1908; Sasaki, 1998; Estabrooks, Kay & McCarthy, 1999). The intestine pierces not only the ventricle, but the lumen of the kidney as well ( Thiele, 1902), posteriorly separating a portion of the reno-pericardial coelom.

The neritid nervous system is right zygoneurous and left dialyneurous, with paired visceral ganglia – one lying in the transverse pallial vein and the second adjacent to the vestigial gill ( Bouvier, 1892; Bourne, 1908). The pedal ganglia are united by a single commissure ( Bourne, 1908; Sasaki, 1998). The identity and homology of the subintestinal ganglion, while previously in question ( Haller, 1894), consists of a swelling lying between and just behind the pleural ganglia ( Bouvier, 1892; Bourne, 1908; Starmühlner, 1969).

Figures

Figure 4. Morphology of odontophore; subradular organ (indicated by arrows). Except when noted, view is from the side and ventral is to the right. (A) Theodoxus fluviatilis, ventral view. Subradular organ absent. Scale bar = 100 Mm. (B) Neocyclotus dysoni ambiguum. Scale bar = 1 mm. (C) Marisa cornuarietis. Scale bar = 1 mm. (D) Lampanella minima. Scale bar = 100 Mm. (E) Littorina littorea. Scale bar = 100 Mm. (F) Neverita duplicata. Scale bar = 100 Mm. (G) Cypraea robertsi. Subradular organ absent. Scale bar = 1 mm. (H) Panarona clavatula. Ventral is down. Scale bar = 100 Mm.

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.