Crepidula plana, 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 : 464-466

CREPIDULA PLANA SAY 1822

Material Examined

Cape Henlopen, Virginia ( USNM 890937).

External anatomy and mantle cavity

Foot narrow anteriorly, broadly rounded posteriorly. Duct of pedal gland opening to shallow propodial groove. Head flattened dorso-ventrally. Mantle cavity extending down left side of visceral mass. Hypobranchial gland large and well developed. Mantle edge folded anteriorly to form food pouch. Gill filaments long and slender with skeletal rods. Ctenidial axis glandular, forming endostyle.

Reproductive system

Protandrous hermaphrodites. In male phase, testis lying alongside tubules of digestive gland, extending down sides of visceral mass. Testis opening anteriorly to broad and tightly coiled seminal vesicle lying just behind base of mantle cavity. Short vas deferens emerging from seminal vesicle, opening to seminal groove ( Fig. 3C , sg) at base of mantle cavity. Prostate (pr) small, comprising small region of glandular cells at base of mantle cavity, extending short distance along seminal groove. Prostatic tissue forming two distinct concentric layers of basophilic cells. Seminal groove extending down neck and along ventral surface of elongate, narrow penis (pe) with curved terminal papilla.

Ovary dorsally overlying digestive gland. Broad renal oviduct opening to approximately four or five small seminal receptacles ( Fig. 2B , rcs) with narrow ducts. Gonopericardial canal absent. Oviduct opening to short, compact pallial oviduct comprising closed albumen (ag) and capsule (cg) glands. Long vagina (v) emerging from capsule gland, terminating in narrow, elongate female opening (fo).

Alimentary system

Foregut. Paired jaw weakly developed at anterior ends of dorsal folds; jaw composed of rods with laterally overlapping homogeneous layer. Subradular membrane incompletely covering odontophore. Small subradular organ present ( Fig. 5E , sro) in shallow sublingual cavity. Long, tubular salivary glands ( Fig. 6E , sgl) by-passing circum-oesophageal nerve ring. Short mid-ventral fold ( Fig. 9F , vf) and flanking ventro-lateral folds (vlf) present in anterior oesophagus. Mid-oesophagus uniformly folded; septate oesophageal gland absent ( Fig. 11D , me).

Midgut. Midgut occupying apex of visceral mass. Oesophagus opening mid-ventrally ( Fig. 14B, e ), near distal end of ventro-lateral gastric shield (gs). Sorting area (sa) well developed anterior to oesophageal aperture. Ciliary currents flowing toward intestinal groove within sorting area. Ciliated fold (cf) extending posteriorly from proximal end of minor typhlosole, passing to left of oesophageal aperture. Glandular pad (gp) extending posteriorly from gastric shield, paralleling ciliated fold to posterior end of midgut. Folds terminating within small caecum (c) on right behind gastric shield. Paired digestive gland ducts (dgd) opening at proximal end of major typhlosole (t1). Style sac region characterized by horizontally folded epithelium bearing differentiated cilia. Raised tract of cilia (ctr) present on both typhlosoles (t1, t2). Crystalline style present. Ciliary currents flowing clockwise within style sac region when viewed from behind.

Hindgut. Intestine exiting style sac and extending from left to right, looping broadly and slightly posteriorly around kidney, then turning anteriorly.

Reno-pericardial system

Kidney anteriorly surrounding pericardium, slightly overhanging pallial cavity. Afferent renal vessel entering kidney floor anteriorly, just in front of renopericardial duct, supplying excretory tissue along floor. Excretory tissue ramifying dorsally within roof and along walls. Nephridial gland present.

Nervous system and sensory structures

Nervous system epiathroid, right zygoneurous, left dialyneurous ( Fig. 24C ). Supra-oesophageal (sp) and sub-oesophageal (sb) connectives extremely short. Circum-oesophageal nerve ring ( Fig. 6E , nr) lying well posterior to buccal mass. Tentacular nerve (tn) splitting upon entering tentacle into two nerves of equal size. Visceral loop short bearing two small visceral ganglia (vg) straddling oesophagus. Statocysts with statoliths ( Fig. 24C , sc) present on dorso-lateral surfaces of pedal ganglia. Osphradium unipectinate ( Fig. 6E , os).

Remarks

In a series of papers on development of the sex organs, emphasizing the transformations that occur during sex change, Gould (1917, 1949, 1952) provided the essential features of reproductive anatomy for Crepidula plana which are congruent with those provided above. This includes the presence of a tightly coiled seminal vesicle, seminal groove and penis behind the right cephalic tentacle in males and, in females, the presence of the gonopericardial canal, the presence of the seminal receptacle, and the absence of the bursa copulatrix. However, the detailed morphology of neither the seminal receptacles nor glandular pallial oviduct was described. In contrast to Gould (1917), the presence of a gonopericardial canal could not be confirmed in the present study.

Discussion

The mantle cavity and mechanism of ciliary suspension feeding in the Calyptraeidae has been well studied (e.g. Orton, 1912, 1913; Yonge, 1938; Werner, 1953). Calyptraeids possess a triangular mantle cavity extending over an elongate neck and along the left side of a flattened visceral mass; a large gill bearing skeletal rods is present, with an elaborate mucusproducing ‘endostyle’ along its axis ( Orton, 1912, 1913; Kleinstüber, 1913; Yonge, 1938; Graham, 1952). Members of the family are unique among ciliary feeders because they obtain food particles from a food groove on the right side of the neck, in addition to a food pouch that collects particles at the anterior edge of the mantle skirt via a modification of the rejection current of other caenogastropods ( Yonge, 1938).

Calyptraeids typically possess seminal receptacles at or near the junction of the renal and pallial oviducts; the number of receptacles and the nature of their connection to the oviduct can vary (single duct or one per receptacle). A gonopericardial canal is present only in females and generates during the transition between male and female phases ( Giese, 1915; Ishiki, 1939; Graham, 1952; Fretter & Graham, 1962; Yipp, 1983). The pallial oviduct of calyptraeids is characterized by the absence of a bursa copulatrix and a narrow vagina that can vary greatly in length ( Kleinstüber, 1913; Fretter & Graham, 1962; Yipp, 1983). The pallial vas deferens lacks prostatic development ( Graham, 1952; Yipp, 1983), but rudiments of female glands in the male phase may have a prostatic function ( Giese, 1915; Graham, 1952).

Midgut features are conservative among described calyptraeids, including the development and position of sorting areas, the extension of the minor typhlosole and parallel glandular pad across the midgut floor, the presence of a caecum, the position of the gastric shield, and the concavity of the major typhlosole ( Fretter & Graham, 1962; Yipp, 1980; pers. obs.). One variable feature includes the position and number of digestive gland ducts. Graham (1939) found four ducts within the midgut of Crepidula fornicata and Calyptraea chinensis ; two opening at the proximal end of the major typhlosole, and two opening within the caecum. Development of the major typhlosole terminal lappet also varies between species ( Fretter & Graham, 1962; pers. obs.). In addition, the ciliary tract on the minor typhlosole, present in Crepidula plana , is lacking in C. fornicata (pers. obs.).

Calyptraeid nervous systems have been described as right zygoneurous and left dialyneurous ( Graham, 1952). A notable exception is Crepidula fornicata , which has a connection between the left dialyneury and a nerve from the left visceral ganglion, in addition to a dialyneurous connection between nerves from the right visceral and the sub-oesophageal ganglia (Graham). Crepidula plana lacks secondary connections involving nerves from the visceral ganglia. Bouvier (1887) reported the presence of a left zygoneury in C. fornicata ?. This could not be confirmed by Graham.

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 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 11. Histology of mid-oesophagus; oesophageal gland. (A) Macleaniella moskalevi. Scale bar = 0.5 mm. (B) Neocyclotus dysoni ambiguum. Scale bar = 0.5 mm. (C) Lampanella minima. Scale bar = 1 mm. (D) Crepidula plana. Scale bar = 1 mm. (E) Littorina littorea. Scale bar = 0.5 mm. (F) Neverita duplicata. Scale bar = 0.5 mm. (G) Cypraea robertsi. Scale bar = 0.5 mm. (H) Nitidiscala tinctum. Note transition to muscular posterior oesophagus. Scale bar = 0.5 mm. Abbreviations: asg, accessory salivary gland; ca, radular cartilage; df, dorsal fold; eg, oesophageal gland; int, intestine; me, midoesophagus; r, radula; sgl, salivary gland; sp, supra-oesophageal ganglion.

Figure 14. Midgut morphology. White arrows indicate direction of ciliary currents. (A) Petaloconchus varians, dorsal view. (B) Crepidula plana, dorsal view. Scale bar = 1 mm. Abbreviations: c, caecum; cf, ciliated fold; ctr, ciliary tract; dgd, digestive gland duct; e, oesophagus; gp, glandular pad; gs, gastric shield; if, intestinal flap; sa, sorting area; ss, style sac; t1, major typhlosole; t2, minor typhlosole.

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.