Panarona clavatula, (SOWERBY 1832)

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 : 475-477

PANARONA CLAVATULA (SOWERBY 1832)

Material examined

Playa Bique, Panama ( USNM 890943).

External anatomy and mantle cavity

Mantle edge papillate ( Fig. 7A ). Hypobranchial gland well-developed with pendulous, folded epithelium. Osphradium (os) large and bipectinate, lying behind inhalant margin. Siphon short and broad. Right cephalic tentacle bifid. Left tentacle bearing lateral flaps; flaps curving dorsally, becoming juxtaposed with siphon. Anterior pedal gland opening to moderately deep cleft along front of large propodium. Ventral pedal gland present in females, opening to elongate slit short distance back from anterior edge of foot sole. Operculum absent.

Reproductive system

Gonad extending along right from tip of viscera to kidney, penetrating tubules of digestive gland. Gonopericardial connection present behind base of mantle cavity ( Fig. 2F , gpc). Pallial oviduct closed. Albumen gland short with U-shaped lumen (ag). Approximately four, small, ciliated ducts emerging dorsally, along crest of gland, opening to small seminal receptacles bearing orientated sperm (rcs). Albumen gland lumen narrowing anteriorly to non-glandular, muscular duct connecting albumen and capsule glands. Connecting duct opening dorsally to ingesting gland (igl) containing unorientated sperm. Capsule gland (cg) large, composed of two parallel laminae with regionated epithelium. Large, deep, muscular bursa lying at anterior end of capsule gland, opening broadly to pallial cavity (fo). Bursa and capsule gland connected by small, ciliated duct, opening short distance back from female aperture.

Vas deferens emerging from testes, expanding into somewhat straight, lobulate seminal vesicle. Vas deferens narrowing behind base of mantle cavity, extending short distance across pallial floor, opening to glandular prostate. Prostate comprising convoluted tube opening proximally to mantle cavity via short, tubular diverticulum. Pallial vas deferens crossing neck, entering penis lying behind right cephalic tentacle. Penis long and spatulate with narrow base and pointed terminal papilla. Coiled penial duct running down midline of penis and opening to tip.

Alimentary system

Foregut. Foregut modified into large, muscular pleurembolic proboscis ( Fig. 7A ). Proboscis sheath (ps) attaching to walls of cephalic haemocoel near cephalic tentacles. Numerous protractor and retractor muscles connecting proboscis sheath to walls of head. Single, large retractor, originating ventro-laterally on left side of proboscis sheath, attaching to columellar muscle at back of head. Small mouth opening at tip of proboscis to short oral tube, rapidly becoming lined with cuticle. Cuticular tube gradually widening posteriorly to buccal mass. Buccal mass hanging free from posterior end of retracted proboscis. Odontophore narrow and elongate with deep sulcus, incompletely lined by subradular membrane ( Fig. 4H ). Anterior odontophore forming muscular, non-glandular, U-shaped shelf supporting long, slender nematoglossan teeth. Radular sac short, thin and slightly curved ( Fig. 7A , rs). Paired, ascinous salivary glands (sgl) with short ducts opening to buccal cavity posteriorly and dorsally. Paired accessory salivary glands (asg) long and tubular. Muscular ties attaching posterior tips of accessory glands to proboscis sheath. Accessory salivary glands narrowing upon entry to retracted proboscis sheath, to long, ciliated ducts running along cuticular tube, entering alimentary canal near transition between cuticle and oral tube.

Short anterior oesophagus; ventral folds absent ( Fig. 10C ). Valve of Leiblein ( Fig. 7A , vl) present short distance back from buccal mass. Long, slender midoesophagus bearing ventral, U-shaped strip of glandular epithelium liberating brown secretory droplets into oesophageal lumen. Transition from glandular midoesophagus to posterior oesophagus occurring at base of cephalic haemocoel, marked by narrowing of oesophageal lumen.

Midgut. Midgut small, U-shaped, partially embedded in digestive gland at back of kidney ( Fig. 17B ). Oesophagus (e) opening to midgut on left. Walls simple, lined with parallel, well-ciliated folds. Digestive gland opening via single large duct (dgd) to back wall. Two parallel, asymmetrical folds running along back wall of midgut, connecting oesophageal aperture with opening of digestive gland. Major typhlosole (t1) extending across floor of midgut and terminating adjacent to digestive gland duct. Style sac region bearing paired typhlosoles (t1, t2) and longitudinally folded epithelium with undifferentiated cilia. Ciliary currents flowing linearly within gastric chamber from oesophageal aperture to style sac region.

Hindgut. Intestine straight, narrow. Anal gland present along distal portion of rectum, terminating just before anus. Anal gland confluent with rectum along entire length of gland, secreting small, brown-black, granular concretions into lumen of rectum.

Reno-pericardial system

Kidney large ( Fig. 23C ), lumen internally subdivided into large posterior chamber and smaller anterior chamber. Anterior chamber extending into pallial roof, bearing nephropore (np) along anterior wall. Incomplete dorsal septum restricting communication between chambers, formed by excretory tissue and the dorsal afferent renal vessel ( DARV). Afferent renal vessel entering kidney floor at anterior end of posterior chamber to right of reno-pericardial canal, behind base of mantle cavity. Ventral afferent renal vessel ( VARV) running posteriorly within floor, supplying narrow strip of primary tubules along right wall and roof. DARV curving dorsally and to left from kidney floor, supplying secondary tubules along left side of kidney and in roof of anterior chamber. Three small branches near origin of DARV supplying primary tubules as well, along right wall and within anterior chamber roof on right. Primary and secondary tubules meronephridial. Nephridial gland present (ng).

Nervous system and sensory structures

Nervous system epiathroid, right zygoneurous, left dialyneurous, with all ganglia except visceral and supra-oesophageal ganglia concentrated in circumoesophageal nerve ring. Long buccal connectives originating from large nerve bundle innervating proboscis sheath and accessory salivary gland ducts. Buccal ganglia lying at posterior end of buccal cavity ( Fig. 7A ). Single, thick tentacle nerve (tn) splitting near eye into four nerves approximately equal in size, extending in parallel down centre of tentacle. Supraoesophageal ganglion lying to left of proboscis short distance behind cephalic tentacle. Small siphonal ganglion (sig) present at point of dialyneury between pallial nerve and branch from osphradial nerve. Siphonal nerve immediately bifurcating into two prominent nerves. Propodial ganglia present at anterior ends of pedal ganglia. Visceral loop bearing paired visceral ganglia (vg), straddling posterior oesophagus. Statocysts with large statoliths lying ventral to circumoesophageal nerve ring, adjacent to ventral pedal gland duct.

Discussion

Female reproductive anatomy is rather consistent among described species; in females, a gonopericardial canal may be present or absent ( Graham, 1966; Harasewych & Petit, 1982, 1984, 1986). One notable exception is the description by Graham (1966) who described two glandular structures, an ingesting gland and a seminal receptacle, posterior to the large capsule gland. Given the position of the gonopericardial canal, it seems likely that Graham confused the albumen gland for a receptacle. This inference is particularly likely given the numerous receptacles lining the dorsal crest of the albumen gland in Panarona clavatula . This interpretation would render the conditions of Cancellaria cancellata equivalent to other cancellariids in the presence of a single ingesting gland between the capsule and albumen glands. No receptacles were described by Harasewych & Petit (1982, 1984, 1986). Male reproductive anatomy seems somewhat more variable; the prostate may open to the inner end of the pallial cavity via a small diverticulum ( Graham, 1966) or a narrow slit ( Harasewych & Petit, 1982, 1986). In addition, the length of the prostate varies and may be convoluted or straight ( Graham, 1966; Harasewych & Petit, 1982, 1984, 1986).

All cancellariids share a nematoglossan radula consisting of a single row of teeth. As the radula travels forward, the teeth become divided into a posterior set and an anterior set, the latter projecting forward into the cuticular, tubular jaw ( Bouvier, 1887; Barnard, 1957; Olsson, 1970; Ponder, 1973; Oliver, 1982; Petit & Harasewych, 1986). Proboscis morphology and the glandular structures associated with the foregut are highly consistent in all species studied, with only subtle variations in the relative lengths of the salivary glands, oral tube, and jaw, with the two latter determining the placement of the buccal cavity within the proboscis sheath; the retracted proboscis may be tubular or ventrally flattened and papillose ( Bouvier, 1887; Amaudrut, 1898; Simroth, 1902; Graham, 1966; Harasewych & Petit, 1982, 1984, 1986). Several authors ( Ponder, 1973; Taylor & Morris, 1988; Kantor, 1996), apparently following Graham (1966), stated that the mid-oesophagus of Cancellarioideans occurs exclusively anterior to the nerve ring. In Panarona clavatula , the mid-oesophagus extends to the posterior end of the cephalic haemocoel. The midgut is typically small and sac-like bearing parallel folds ( Harasewych & Petit, 1982, 1984, 1986) and a single duct of the digestive gland ( Graham, 1966). The anal gland may be present or absent ( Harasewych & Petit, 1982, 1984, 1986). The precise connection between anal gland and rectum remain undescribed for other cancellariids. Thus, it is unknown if P. clavatula is unique, or if all cancellariids possess an anal gland that forms a glandular strip confluent with the rectum, rather than a separate tube opening via a duct to the rectum or pallial cavity as in other neogastropods (e.g. Ponder, 1973).

A nephridial gland is present; size of the kidney can vary substantially between species ( Harasewych & Petit, 1982, 1984, 1986).

The nervous system of cancellariids is known in detail only from Cancellaria cancellata ( Bouvier, 1887) , with some general information given by Graham (1966); with minor exceptions, both studies are in agreement with the description provided above. One exception is the number of visceral ganglia, and may be paired (Bouvier) or single (Graham). The long cerebro-buccal connectives are bound in nerve bundles from the cerebral ganglia that innervate the proboscis. However, there are two separate bundles in Panarona clavatula (present study) and C. cancellata (Bouvier) , and only a single median bundle in C. reticulata (Graham) . The tentacular nerve is single (Bouvier).

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 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 7. Morphology of cephalic haemocoel among derived caenogastropods. (A) Panarona clavatula. Siphon obscured by left cephalic tentacle and is not visible in this view. Note large, modified left cephalic tentacle and large proboscis retractor connecting to columellar muscle. (B) Ilyanassa obsoletus. Note second visceral ganglion lying below pericardium and large radular retractors connecting to base of proboscis sheath; ampulla of gland of Leiblein visible within afferent renal vessel. Duct of gland of Leiblein stippled. (C) Nitidiscala tinctum. Note compartmentalized tissue supporting jaw and buccal ganglia lying between salivary glands where the latter enter buccal cavity. (D) Prunum apicinum. Note duct of poison gland opening mid-ventrally to base of buccal cavity, just behind opening of accessory salivary gland. (E) Conus jaspideus. Siphon not visible in this view. Note long coiled duct of poison gland; buccal ganglion visible where short arm of radular sac enters buccal cavity. Base of proboscis sheath is shown, but rhynchocoel has not been opened. Scale bar = 1 mm. Abbreviations: asg, accessory salivary gland; dasg, duct of accessory salivary gland; e, oesophagus; ec, oesophageal caecum; gl, gland of Leiblein; j, jaw; kd, kidney; nr, circum-oesophageal nerve ring; os, osphradium; per, pericardium; ps, proboscis sheath; rs, long arm of radular sac; sb, sub-oesophageal ganglion; sgd, salivary gland duct; sgl, salivary glands; si, siphon; sig, siphonal ganglion; sp, supra-oesophageal ganglion; tn, tentacular nerve; vg, visceral ganglion; vl, valve of Leiblein; z, zygoneury.

Figure 10. Histology of anterior oesophagus; ventral folding absent. (A) Neverita duplicata. Scale bar = 0.5 mm. (B) Nitidiscala tinctum. Scale bar = 0.5 mm. (C) Panarona clavatula. Scale bar = 0.5 mm. (D) Prunum apicinum. Scale bar = 0.5 mm. (E) Conus jaspideus. Scale bar = 0.5 mm. (F) Ilyanassa obsoletus. Scale bar = 0.5 mm. (G) Urosalpinx cinerea. Scale bar = 1 mm. Abbreviations: asg, accessory salivary gland; ca, radular cartilage; ceg, cerebral ganglion; df, dorsal fold; dl, duct of gland of Leiblein; e, oesophagus; int, intestine; j, jaw; ps, proboscis sheath; r, radula; sgd, salivary gland duct; sgl, salivary gland; vc, ventral channel.

Figure 17. Midgut morphology. White arrows indicate direction of ciliary currents. (A) Nitidiscala tinctum, dorsal view. (B) Panarona clavatula, dorsal view. Note paired folds on midgut floor between oesophageal aperture and large digestive gland duct. Scale bar = 100 Mm. Abbreviations: dgd, digestive gland duct; e, oesophagus; gp, glandular pad; ig, intestinal groove; int, intestine; 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.