Cypraea robertsi, Hidalgo, 1906

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 : 471-473

CYPRAEA ROBERTSI HIDALGO 1906

Material examined

Playa Bique, Panama ( USNM 890940).

External anatomy and mantle cavity

Anterior pedal gland opening to deep propodial groove. Mantle surface pustulose with conical papillae; short siphonal fringe. Anterior kidney chamber extending into pallial roof. Osphradium triradiate. Hypobranchial gland extensive, comprising large, pendulous folds. Operculum absent.

Reproductive system

Gonad occupying terminal whorls, anteriorly bounding digestive gland and midgut on right. Gonopericardial canal absent. Vestigial gonopericardial canal present, forming small, blind pericardial diverticulum. Oviduct entering capsule gland near base of mantle cavity. Capsule gland ( Fig. 2E , cg) long and crescentic, narrow posteriorly, expanding anteriorly. Albumen gland (dg) lying along dorsal margin of capsule gland, opening to capsule gland anteriorly via narrow duct. Large, lobate seminal receptacle (rcs) opening to blind posterior end of albumen gland. Finely grooved tract extending anteriorly from aperture of albumen gland, expanding at distal end of capsule gland, continuous with narrow vagina (v). Vagina terminating at small female opening (fo).

Vas deferens forming large and complexly coiled seminal vesicle. Seminal vesicle narrowing anteriorly and opening to closed, narrow, glandular, basophilic prostate at base of mantle cavity ( Fig. 3E , pr). Vas deferens emerging from pallial roof, opening to large pocket and open seminal groove lined with acidophilic cells. Seminal groove extending across neck and along ventral surface of long, simple, narrowly triangular penis (pe).

Alimentary system

Foregut. Radula taenioglossate. Foregut modified into muscular, acrembolic proboscis ( Fig. 6C , ps). Jaw absent; buccal cavity uncuticularized. Subradular membrane completely covering ventral surface of odontophore; subradular organ absent ( Fig. 4G ). Short mid-ventral fold ( Fig. 8G ) present forming dorsal lip of radular sac. Paired muscular, non-glandular pouches present opening to anterior oesophagus. Shallow ridge running transversely across floor of oesophagus between pouches; ventro-lateral folds absent. Salivary gland ducts passing through broad nerve ring, under long pedal connectives. Salivary gland massive, filling left side of cephalic haemocoel and overlying oesophageal gland. Radular sac long and coiled. Midoesophagus with well-developed, septate oesophageal gland and open dorsal food groove.

Midgut. Oesophagus opening to left limb of large, Ushaped midgut ( Fig. 16B, e ). Gastric shield absent. One digestive gland duct (dgd) opening near oesophagus, draining small posterior lobe of digestive gland. Second digestive gland duct draining large anterior lobe of digestive gland, forming caecum. Broad mouth of caecum opening ventrally, along anterior wall of midgut. Anterior extension of major typhlosole (t1) bounding caecum on right. Style sac region characterized by single (major) typhlosole and transversely folded epithelium bearing uniform cilia; minor typhlosole absent. Ciliated strip on major typhlosole absent. Ciliary currents flowing clockwise within style sac region. Major typhlosole turning to right at distal end of style sac. Transverse lip of major typhlosole bounding deep pyloric caecum (pyc), extending posteriorly under style sac. Minor typhlosole beginning within pyloric caecum, paralleling major typhlosole straight out of caecum. Posterior digestive gland lobe occupying terminal visceral whorls; anterior lobe extending into pallial cavity.

Hindgut. Major and minor typhlosoles continuing only short distance within proximal intestine. Intestine straight.

Reno-pericardial system

Kidney large, differentiated into posterior and anterior, histologically distinct lobes ( Fig. 23B ). Posterior lobe (pl) overlying visceral kidney lumen. Anterior lobe (al) long and narrow, extending within pallial roof under intestine (int), along digestive gland and pallial gonoduct. Nephridial gland present (ng). Afferent renal vessel entering kidney posteriorly, extending anteriorly along floor, producing numerous small branches supplying lamellae along ventral surface of digestive gland. Afferent renal vessel splitting near nephropore (np) into two large branches of equal size. Ventral branch supplying anterior lobe of kidney. Dorsal branch supplying anterior and posterior lobes.

Nervous system and sensory structures

Nervous system epiathroid, left zygoneurous, possibly right dialyneurous ( Fig. 24D ). Circum-oesophageal nerve ring ( Fig. 6C , nr) lying obliquely within cephalic haemocoel, with concentrated cerebro-pleural complex near left cephalic tentacle. Buccal ganglia present just anterior to buccal pouches (bp). Tentacular nerve (tn) dividing into nerve plexus upon entering tentacle. Long pedal connectives passing over anterior oesophagus. Pedal ganglia ( Fig. 24D , pdg) large with pedal cords (pc) forming numerous cross connections. Supraoesophageal (sp) connective very short; suboesophageal (sb) connective long. Single large visceral ganglion ( Fig. 6C , vg) lying within cephalopedal sinus. Four smaller accessory visceral ganglia (vg) present straddling posterior oesophagus and along left side of cephalic haemocoel. Statocysts with single statolith ( Fig. 24D , sc) present on dorsal surface of pedal ganglia.

Discussion

The foregut of cypraeoideans is modified to form a muscular, acrembolic proboscis ( Vayssière, 1923; Kay, 1960). The position, number and glandular development of pouches within the anterior oesophagus is variable. They may be paired ( Kay, 1960; present study) or unpaired and thin-walled or glandular ( Amaudrut, 1898; Vayssière, 1923; Thiele, 1929; Rau, 1934; Fretter, 1951; Fretter & Graham, 1962). Such unpaired mucus diverticulae have been described as opening to the oesophagus at the origin of the oesophageal gland, slightly posterior to that described here. It seems likely that these glandular and nonglandular diverticulae are homologues (cf. Kay, 1960) despite slight differences in position within the anterior oesophagus. In fact, given that twisting of the anterior oesophagus brings the left pouch into a hidden ventral position, it suggests that many of the described single diverticulae may be paired with asymmetrical development of glandular tissue.

Cypraeoideans display an extraordinary conservatism of midgut morphologies. The structure and development of such features as the digestive caecum, the major typhlosole, and the intestinal groove are remarkably similar in many species ( Haller, 1890; Rau, 1934; Kay, 1960). Cypraea robertsi differs in that it lacks both the gastric shield and the ciliated strip on the major typhlosole, which might otherwise confound attempts to interpret midgut homologies. However, the ovulid Jenneria pustulata has a midgut that is similar in overall organization, and also possesses both the shield and the ciliated strip (pers. obs.). Owing to this basic conservatism, midgut morphology of J. pustulata permits an interpretation of cypraeoidean midgut homologies and a reinterpretation of the hypotheses offered by Kay (1960), even in those taxa lacking structures such as the gastric shield.

As stated above, Jenneria pustulata possesses a gastric shield and a ciliated strip on the major typhlosole. The gastric shield and a prominent horizontal fold distal to the shield (= lip of style sac) in J. pustulata are similar to style-bearing caenogastropods in their position and connection to other landmarks. This suggests that the portion of the midgut along the major typhlosole referred to as the ‘cuticular area’ by Kay (1960), represents the style sac region of other caenogastropods. Kay suggested instead that the region of the gut distal to the transverse segment of the major typhlosole is comparable to the style sac region. This reinterpretation indicates that the transverse segment of the major typhlosole lies at the distal end of the style sac, not at the proximal end as suggested by Kay, confirming the identification of a pyloric caecum at the distal end of the style sac in C. robertsi . Kay did not describe a pyloric caecum under the transverse segment of the major typhlosole. However, a depression appears to be visible in the appropriate position. Cypraea robertsi is unique in lacking a minor typhlosole in the style sac region.

As in naticids, the excretory tissue of cypraeids is subdivided into two lobes that are histologically and macroscopically distinct ( Haller, 1890; Simroth, 1896 – 1907). Haller’s detailed description of the kidney in C. testudinaria also clearly documented the branching of the afferent renal vessel to supply the anterior and posterior lobes. Rau (1934) provided a largely erroneous interpretation of the reno-pericardial system of Cypraea arabica , referring to the anterior kidney lobe as the right kidney, complete with a rudimentary nephropore near the anus.

Cypraeoidean nervous systems are displaced to the left of the buccal mass, with highly concentrated cerebral and pleural ganglia; the supra-oesophageal and left pleural ganglia are in close proximity, and the suboesophageal ganglion is widely separated from the others ( Haller, 1890; Amaudrut, 1898; Vayssière, 1923; Riese, 1931). Riese’s (1931) detailed analysis of the nervous system of Cypraea moneta described at least two anastomoses of the sub-oesophageal and supra-oesophageal ganglia that pass through the mantle roof; presence or absence of these dialyneuries could not be confirmed in sections of the highly glandular mantle roof of C. robertsi . Pedal cords with numerous cross connections are present ( Haller, 1890; Shaw, 1909; Riese, 1931). In contrast to the present findings, the tentacular nerve typically is shown as a simple, unbranched nerve ( Haller, 1890; Vayssière, 1923). The number of visceral ganglia is somewhat inconsistent among existing descriptions. For example, Haller (1890) depicted a single main ganglion with only a single accessory ganglion, while Riese (1931) described one main and three accessory ganglia. The position of the accessory ganglia is also variable. This inconsistency may be due to differing interpretations of the swellings along the visceral loop, several of which were only visible in C. robertsi with the aid of histological sections; these are highly variable in size and not all produce nerves.

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 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 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 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 16. Midgut morphology. White arrows indicate direction of ciliary currents. (A) Neverita duplicata, dorsal view. Scale bar = 1 mm. (B) Cypraea robertsi, dorsal view. Abbreviations: cf, ciliated fold; dgd, digestive gland duct; e, oesophagus; ig, intestinal groove; pyc, pyloric caecum; sa, sorting area; ss, style sac; t1, major typhlosole; t2, minor typhlosole.

Figure 23. Kidney morphology; derived caenogastropods with two differentiated lobes of lamellae. (A) Neverita duplicata, dorsal view. Kidney opened between lobes of differentiated lamellae. (B) Cypraea robertsi, dorsal view. Intestine removed to reveal internal details. (C) Panarona clavatula, dorsal view, posterior chamber on left, anterior chamber on right. Kidney roof opened between lobes of primary and secondary lamellae. Note meronephridial condition (no interdigitation of lamellae) and that dorsal branch of afferent renal vessel supplies both primary and secondary tubules. (D) Prunum apicinum, dorsal view. Note small region of secondary tubules within kidney roof supplied by dorsal branch of afferent renal vessel. (E) Ilyanassa obsoletus, dorsal view. Note pycnonephridial condition (interdigitation of lamellae). Scale bar = 1 mm. Abbreviations: al, anterior kidney lobe; arv, afferent renal vessel; au, auricle; darv, dorsal branch of afferent renal vessel; int, intestine; ng, nephridial gland; np, nephropore; per, pericardium; pl, posterior kidney lobe; rpc, reno-pericardial canal; ve, ventricle.

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.