Frontonemertes serpentina, Iwata, 2006

Iwata, Fumio, 2006, On four monostiliferous hoplonemerteans, including three new genera and species from Washington state and British Columbia, Journal of Natural History 40 (15 - 16), pp. 873-913 : 875-884

Frontonemertes serpentina gen., sp. nov.

Type specimen

Holotype: USNM 1072177 ; 28 slides of stained serial section of one specimen, including transverse sections of the anterior portion of the body (17) and midgut (11) . Paratype: USNM 1072178 ; 17 slides of stained serial section of head region (8) and tail (9). Three pieces of the holotype and long piece of the paratype were not sectioned .

Type locality Satellite Channel, Vancouver Island, British Columbia, Canada (Lat. 48 ° 41.9 9 N, Long.

123 ° 28 9 W), depth 15–22 fathoms, September 9, 1964.

Description

External features

Holotype 13 cm long and 2 mm wide when moving, narrowing gradually towards posterior end ( Figure 1.1 ). Body, however, can stretch to 30 cm and width of 3 mm in foregut region. Paratype 17 cm long and 2 mm wide.

Body soft, contractile, and semitransparent, becoming very slender in the posterior portion when elongated. The animal could attach itself to glass and could raise its anterior portion like a snake’s head. Many folds extended transversely across the dorsal surface. The color was whitish, with two wide lateral orange bands. Along the midline, between the orange bands, there was a slender whitish line. The head, not demarcated from the rest of the body by a constriction, had a pair of orange bars on the dorsal surface ( Figure 2a, c , df)). On the ventral surface, a slender cephalic groove ran transversely across the anterior portion of the head ( Figure 2b, c ). Two cephalic grooves situated farther posteriorly ( Figure 2b, c ) a nearly V-shaped configuration, but the grooves did not quite meet.

There were four groups of ocelli. The number of ocelli in each anterior group was about 30 and in each posterior group there were about 10. The ocelli in the anterior group could be seen from the dorsal- and ventral side of the head ( Figure 2b ). The brain, reddish in color, was observed in the space between the orange-coloured bars on the head and the anterior ends of the wide orange lateral bands ( Figure 2a ). At the anterior tip of the head there were two small pores; one was the proboscis pore, the other was the opening of the apical organ ( Figure 2b ). When the head was raised ( Figure 2 d–f), the proboscis pore and the opening of the apical organ, the two orange bars, the ocelli and the anterior ends of the two orange bands were visible. The raising of the head seems to be effected by numerous bundles of retractor muscles ( Figure 3g, h ).

Body aeall, musculature, and parenchyma

The epidermis is of uniform thickness both in the cephalic region (average 70 mm) and in the midgut region (average 50 mm) ( Figure 3a ). Large unicellular glands are distributed over the entire body and are especially well developed in the midgut region. Small columnar cyanophilic glands are embedded between the large glands.

In the anterior half of the head, between its tip and the brain, a median dorsoventral furrow, measuring 70 mm wide at the bottom, 200 mm deep and 400 mm long can be seen in transverse section on the ventral side of the head ( Figure 3b, c ). On the dorsal side of the head, the epidermis sinks inward in the dorsolateral portions and forms a pair of deep furrows; these become shallower posteriorly and disappear behind the brain ( Figure 3b, d ). The dermis, 5–20 mm thick, is one-third to one-fifth as thick as the epidermis ( Figure 3a ). It has transverse fibrils and contains no cellular bodies or small nerves. Sub-epithelial glands found in the members of Paranemertes are lacking.

The body wall musculature consists of a very thin outer circular coat, 20 mm thick in the brain region and an inner longitudinal layer 70 mm wide ( Figure 3a ). There is a very sparse lattice-type diagonal muscle layer and dorsoventral muscles are absent. Parenchyma is extremely well-developed in the holotype and especially in the paratype.

Rhynchodeum, rhynchocoel and proboscis

The proboscis pore, 130 mm long and 100 mm wide, opens on the dorsal side of the deep cephalic furrow ( Figure 3b, c ). Its wall is 20 mm thick and has crowded long cilia but no glands. The rhynchodeum behind the proboscis pore is flattened dorsoventrally and protrudes dorsally owing to the cephalic furrow ( Figure 3d ). Behind the level at which the oesophagus opens into it, the rhynchodeum is covered by a weakly-developed sphincter of circular muscles ( Figure 3e, f ). Above the oesophagus, the rhynchodeum becomes cylindrical for a length of 570 mm. About 500 mm from the opening of oesophagus, a row of longitudinal muscle fibres covers the rhynchodeum ( Figure 3f ). This muscular coat becomes thicker posteriorly for 70 mm and then its thickness gradually increases to 30 mm at the posterior end of the rhynchodeum ( Figure 3g ). The rhynchodeum wall, 30 mm thick, consists of a row of columnar cells with dense cilia in anterior portion ( Figure 3 e–g). At its posterior end, where the proboscis insertion occurs ( Figure 3h ), it becomes somewhat laminated into outer nucleated and inner cytoplasmic portions. The longitudinal muscle coat is derived from the inner portion of the body wall longitudinal layer.

Close behind the brain, the body wall longitudinal muscle is divided into inner and outer portions, separated by parenchyma ( Figure 4a ), instead of forming a single layer. The outer layer continues into the tip of the head without contributing to the proboscis insertion; a pre-cerebral septum is lacking. The inner layer consists of both large and small bundles, with surrounding membrane, and anteriorly it forms a closed cylinder covering the brain ( Figure 4 b–e). The muscle fibres run transversely, covering the anterior end of the cerebral ganglia; together with the rhynchodeal wall, they contribute to the proboscis insertion ( Figures 3h and 4e ).

At the proboscis insertion, the rhynchodeal wall and inner longitudinal fibres are transformed into the layers of the proboscis: proboscis epithelium, circular and longitudinal muscle layers containing 12 proboscis nerves, rhynchocoel and proboscis sheath consisting of longitudinal and circular muscle layers ( Figures 3g, h and 4d, e ). The transformation occurs in front of the brain and 120 mm in length.

The head retractor muscles, forming a number of bundles with surrounding membranes, are derived from the outer portion of the longitudinal muscle layer of the body wall ( Figure 3 f–h).

The rhynchocoel is short, being less than one-third the body length. The proboscis apparatus is found in the pyloric region and is about 1 mm long ( Figure 4h ). In its anterior portion, the proboscis is provided with outer circular and inner longitudinal muscle layers, but posteriorly the outer circular layer is not recognizable. Proboscis armature consists of a single central stylet and three accessory stylet pouches. The basis of the central stylet is conical in form and surrounded by thick radial muscles. The central stylet is 30 mm long ( Figure 4f ). There are three accessory stylet pouches, two arranged as a pair and the other situated posterior to the pair. There are three, four and five accessory stylets. Each has a posterior cyanophilic protrusion and an umbrella-like edge at its posterior end ( Figure 4g ). The ductus ejaculatorius is joined to the stylet bulb by a narrow canal. The stylet bulb is surrounded by a thick circular muscle layer ( Figure 4h ).

Alimentary canal

The alimentary canal has five major divisions: oesophagus, stomach, pylorus, midgut (with anteriorly directed caecum and lateral diverticula) and hindgut. The oesophagus opens into the rhynchodeum ( Figure 3e ) 220 mm behind the proboscis pore. The oesophagus and stomach lack a longitudinal and circular musculature.

The oesophagus, compressed between the rhynchodeum and the longitudinal muscle layer of the body wall, is flattened dorsoventrally ( Figure 3h ). It extends far posterior to the brain ( Figure 5b, c ); the distance between the oesophageal–rhynchodeal junction and the posterior end of the brain is about 0.9 mm and that between the end of the brain and posterior end of the oesophagus is 320 mm. The transition of the oesophagus into the stomach is long, about 420 mm ( Figure 5c ). In this area, the oesophagus becomes about three times as wide as the oesophageal–rhynchodeal junction.

The stomach, 420 mm long, and has more than 10 folds in transverse section ( Figure 5d ). Measured from the antero-posterior limits of the gastric length, the stomach is about two and a half times as long as the brain.

The pylorus, which succeeds the stomach, is about 1.7 mm long and about four times as long as the stomach. It is wide and flattened dorsoventrally in transverse sections, being 1.4 mm wide at its junction with the stomach. At the point where it opens into the midgut, it narrows to 0.2 mm ( Figure 5e ). The ciliated epithelium of the pylorus contains cyanophilic glands similar to those of the stomach ( Figure 4h ).

The intestinal caecum lacks anterior tubular branches and its anterior end is situated 2 mm from the posterior end of the brain. The caecum has five pairs of lateral diverticula. The intestine is flattened dorsoventrally has only short lateral diverticula.

In the series of sections of the holotype, the posterior end of the body was missing. In the paratype, there is a long and deep furrow, measuring 240 mm long and 130 mm deep on the ventral side of the body. The anus and rectum were not observed.

Blood υascular system

The blood vascular system has three longitudinal vessels. The two cephalic blood vessels lateral to the rhynchodeum anastomose above the rhynchodeum near the tip of the head to form the cephalic loop, 100 mm wide, 20 mm high and 30 mm in length. Farther posteriorly, however, the cephalic vessels turn medially in front of the proboscis insertion ( Figure 3h ). At the level of the anterior end of the brain, they enter the brain ring without giving off cerebral vessels, and then run posteriorly alongside the ventro-lateral portions of the rhynchocoel ( Figure 4d, e ). Near the posterior end of the brain, the right vessel communicates with the dorsal vessel, which then enters the proboscis sheath behind the brain as a single median vascular plug. This plug, about 200 mm long, extends medioventrally in the sheath as far as the posterior end of the oesophagus ( Figure 5a, b ). This portion of the vascular plug seems to form a specialized communication with the rhynchocoel ( Figure 5b ). The dorsal vessel then continues posteriorly under the proboscis sheath between the rhynchocoel and the alimentary canal ( Figure 5c ). The three postcerebral vessels are not transversely linked by pseudometameric transverse connectives.

Behind the brain, the lateral vessels enter the nephridial region, which extends from the level far posterior of the brain to that of the transitional area of the oesophagus into the stomach. The lateral vessels are situated inside the lateral nerves and exhibit no branches that contact the nephridia. There are no transverse anastomoses of the lateral vessels in the intestinal region.

In the paratype, which lacks the cephalic region of the body, the dorsal and lateral vessels anastomose at about 3 mm anterior to the posterior end of the body.

Nerυous system

The cerebral ganglia are large and have neither neurochord cells nor an inner neurilemma. The ventral ganglia are not distinctly separated from the dorsal ganglia except posteriorly ( Figure 5a ). They become completely separated for a distance of 30 mm.

The dorsal and ventral fibre cores are not divided anterior to the middle portion of the brain; the dorsal cores are more voluminous than the ventral cores ( Figure 4b ). Behind the posterior end of the dorsal ganglia, the ventral ganglia soon extend laterally, forming the lateral nerve cords ( Figures 4b and 5a, b ). Posteriorly, the dorsal ganglia do not branch into dorsal and ventral lobes.

The right and left ganglia are connected by a short, thin dorsal commissure, 40 mm thick, and a short, much thicker ventral commissure, 90 mm thick, at about the same transverse level ( Figure 4c ).

In the intestinal region, the lateral nerve cords, situated ventrolaterally, lie in the parenchyma above the longitudinal musculature of the body wall. They give off dorsal or dorsoventral peripheral nerves that extend toward the dorsal and ventral sides of the body ( Figure 5f ).

Several slender but conspicuous nerves originate from the brain. They branch out pre- and post-cerebrally to supply various structures. A proboscis nerve trunk arises from the dorsal surface of the brain at the root of the ventral commissure and extends dorsally into the proboscis sheath where the proboscis is inserted ( Figure 4d ). Both trunks of the proboscis nerves soon branch into 12 nerves that lie in the proboscis sheath ( Figure 4e ). A small nerve, 320 mm long, extends from the lateral side of each dorsal ganglion to the posterior end of each cerebral sensory organ ( Figure 4b ). The rhynchodeum nerves emanate from the ventral surface of the ventral commissure and extend anteriorly along the dorsal side of the oesophagus ( Figures 3h and 4d ). The foregut nerves, which are paired, originate internally from the posterior ends of the ventral ganglia and run posteriorly in the parenchyma above the oesophagus ( Figure 5a, b ). A conspicuous nerve originates from the lateral surface of each dorsal and ventral ganglion ( Figure 5a ). The mid-dorsal nerve lies in the dermis just above the circular muscle layer of the body wall ( Figure 3a ).

The lateral nerve cords have one fibrous core which lacks myofibrillae and accessory nerves. The commissure on the dorsal side of the rectum was not observed in the paratype specimen.

Special sensory organs and apical organ

The ocelli are distributed in four groups and 68 could be counted in transverse sections. They are large and confined to an area, 550 mm long, between the anterior end of the rhynchodeum and the posterior end of the cerebral sensory organs, which are far anterior to the brain. There are 35 ocelli on the right side of the head and 33 on the left. Two groups are recognizable on each side; 26 and nine on the right side and 23 and 10 on the left. The ocelli are of the inverted pigment-cup type and have dimensions of up to 50 mm wide and 60 mm height ( Figure 5g ).

The apical organ consists of a pore and cluster of minute glands in the mid-dorsal portion of the worm, above the anterior end of the proboscis pore ( Figures 5h and 6a ).

The mass of frontal glands, in the dorsal side of the head, extends posteriorly for a distance of 320 mm; the posterior end of the mass is separated by a distance of about 400 mm from the cerebral sensory organs ( Figure 3 b–d). The opening of the frontal gland mass is found at the anterior tip of the mid-dorsal furrow of the head below the minute glands forming the apical organ ( Figure 6a ).

The cephalic glands, confined to the lateral sides of the head, are separate from the frontal glands ( Figures 3b, c and 6a ). They occupy an area 260 mm long.

The frontal and cephalic glands end a short distance anterior to the opening of the oesophagus ( Figure 3e ). The distance between the posterior end of the cephalic glands and the brain is considerable, about 600 mm. Sub-muscular glands are very small and few in number and located only on the ventral side of the head.

The cerebral sensory organs are very small (120 mm) and lie 140 mm in front of the brain. The cerebral organs are nearly circular in transverse section, 65X 55 mm in their posterior portions ( Figure 6b ).

The cerebral organ canal is ciliated and measures 50 mm in length. It begins at the ventrolateral side of the anterior oblique cephalic groove of the head and extends posteriorly inside the longitudinal musculature of the body wall ( Figure 6c, d ). Its epithelium is 10 mm thick. The canal widens just before entering the cerebral organ, but does not have a U-shaped ciliated sensory portion. At the entrance of the cerebral organ, there is a pair of thickenings of the ganglion cells ( Figure 6e ). The sensory canal (40X 30 mm in dimension) is situated medially in the cerebral organ ( Figure 6b ). The canal soon disappears. Its glandular cells form a mass ( Figure 6b ). A slender nerve, 320 mm long, runs from the lateroventral corner of the dorsal ganglion to the posterior end of the cerebral organ ( Figure 4b ).

Excretory and reproductiυe systems

The excretory system is weakly developed in the foregut region. Excretory tubules winding around and along the lateral blood vessels were not observed. The efferent duct is not conspicuous and extends laterally to the lateral nerve cord, reaching the excretory pore on the lateroventral side of the body ( Figure 6f ). The pore is ventral to the lateral nerve cord and is at the level of the posterior portion of the oesophageal region. An efferent duct on the left side of the body was not found.

Sexes are separate and fully mature eggs are independently arranged between the body wall and the intestine; there are no distinct gonad sacs ( Figure 6g, h ). No eggs were found in the foregut region.

Figures

Figure 1. (1) Dorsal view, sketch of living holotype specimen of Frontonemertes serpentina, new genus and species; (2) dorsal view, sketch of living holotype specimen of Satellitenemertes satellitensis, new genus and species; (3) dorsal view, sketch of living specimen of Nipponnemertes bimaculata (Coe) from Satellite Channel; (4) dorsal view, sketch of living holotype specimen of Sanjuannemertes aeilloaesi, new genus and species.

Figure 2. Frontonemertes serpentina, new genus and species, holotype. (a) Anterior portion, dorsal view; (b) anterior portion, ventral view; (c) anterior portion, lateral view; (d–f) views of anterior end of head, from anterior side. Abbreviations: ai, anterior group of ocelli; ap, anterior cephalic groove; br, brain lobe; ob, orange bar; or, lateral orange band; pa, pore of apical organ; pg, posterior cephalic groove; pi, posterior group of ocelli; po, proboscis pore; wb, whitish line.

Figure 3. Frontonemertes serpentina, new genus and species, holotype. (a) Transverse sections between 22 and 194 from anterior end of body, showing body wall and mid-dorsal nerve; (b) mid-ventral furrow and a pair of lateral grooves, frontal glands and cephalic glands; (c) anterior dorsal wall of proboscis pore, frontal glands and cephalic glands enlarged from (b); (d) mid-ventral furrow and pair of lateral grooves, rhynchodeum and frontal glands; (e) opening of oesophagus into rhynchodeum and circular musculature surrounding rhynchodeum; (f) rhynchodeum near anterior end of the head, with row of longitudinal muscles surrounding it; (g) rhynchodeal wall and its longitudinal muscular coat derived from inner longitudinal muscle layer; (h) proboscis insertion developing from the posterior end of the rhynchodeal wall, inner longitudinal muscle of rhynchodeal wall derived from the body wall longitudinal muscle layer, retractor muscles, cephalic blood vessel extending toward rhynchodeal wall and oesophagus. Scale 100 mm (a, c, e–h), and 200 mm (b, d). Abbreviations: bc, body wall circular muscle layer; bl, body wall longitudinal muscle layer; cb, cephalic blood vessel; cg, cephalic glands; cm, circular muscles of rhynchodeum; df, dorso-lateral deep furrow; dp, dorsal wall of proboscis pore; dr, dermis; es, oesophagus; fg, frontal glands; hr, head retractor muscles; ic, inner, cytoplasmic portion of rhynchodeal epithelium; lf, longitudinal muscle fibres of rhynchodeum; lm, inner longitudinal muscle coat of rhynchodeum; lp, longitudinal muscle layer of proboscis; mc, muscular coat of longitudinal muscle fibres of rhynchodeum; md, middorsal nerve; mf, median dorso-ventral furrow; oc, ocellus; oe, opening of oesophagus into rhynchodeum; ol, body wall outer longitudinal muscle layer; on, outer, nucleated portion of rhynchodeal epithelium; rd, rhynchodeum; rn, rhynchodeum nerve; wr, wall of rhynchodeum.

Figure 4. Frontonemertes serpentina, new genus and species, holotype. (a) Transverse sections between 115 and 552 from anterior end of body, showing indistinct inner longitudinal fibres separated from the longitudinal muscle layer of the body wall in parenchyma above the brain lobes and circular muscle layer around rhynchocoel; (b) dorsal and ventral fibre cores of brain, nerve of cerebral sensory organ from right dorsal brain lobe and inner longitudinal muscle fibres surrounding brain; (c) brain with dorsal and ventral commissures at same transverse level and inner longitudinal muscle coat surrounding brain; (d) a pair of trunks of proboscis nerve from the ventral commissure of brain, a pair of cephalic blood vessels, and proboscis sheath and proboscis; (e) proboscis insertion in front of brain lobes and cephalic blood vessels inside brain ring; (f) central stylet on its basis; (g) accessory stylets in accessory stylet pouch; (h) stylet bulb surrounded thick circular muscle layer, pylorus, and intestinal caecum with lateral diverticula. Scale 50 mm (f, g), 100 mm (a, d, e), and 200 mm (b, c, h). Abbreviations: as, accessory stylet; bp, beginning of nerve to cerebral sensory organ; cb, cephalic blood vessel; cp, circular muscle layer of proboscis sheath; cs, central stylet; cu, intestinal caecum; dc, dorsal commissure of brain; dg, dorsal ganglion; ep, epithelium of proboscis; es, oesophagus; il, inner longitudinal muscular bundles; im, inner longitudinal muscular coat covering brain lobes; ld, lateral diverticula of intestinal caecum; lm, inner longitudinal muscle coat of rhynchodeum; ln, lateral nerve; lp, longitudinal muscle layer of proboscis; ol, body wall outer longitudinal muscle layer; pa, pouch of accessory stylets; pn, proboscis nerve; pr, proboscis; pt, proboscis nerve trunk; rc, rhynchocoel; rn, rhynchodeum nerve; sb, stylet bulb; vc, ventral commissure of brain; vg, ventral ganglion.

Figure 5. Frontonemertes serpentina, new genus and species, holotype. (a) Transverse sections between 11 and 839 from anterior end of body, showing dorsal blood vessel branched from right cephalic vessel and two nerves derived from right brain lobes; (b) single median vascular plug with a communication to rhynchocoel, a pair of foregut nerves and oesophagus; (c) dorsal blood vessel, transitional wall of stomach in oesophagus and body wall longitudinal muscle layer with muscular bundles for inner longitudinal fibres in cephalic region; (d) stomach with 10 folds and anterior portion of proboscis in rhynchocoel; (e) opening of pylorus into intestine; (f) peripheral nerve of lateral nerve cord in stomach region; (g) ocellus composed of outer cellular portion and central cytoplasmic area, and a nerve from its anterior end; (h) pore of apical organ, its minute glands and cephalic glands. Scale 50 mm (g), 100 mm (a–c, e, f, h) and 200 mm (d). Abbreviations: cg, cephalic glands; cp, circular muscle layer of proboscis sheath: db, dorsal blood vessel; dg, dorsal ganglion; dv, dorsal blood vessel separated from right cephalic blood vessel; es, oesophagus; fd, fold of stomach; fn, foregut nerve; ga, glands of apical organ; hr, head retractor muscle; il, inner longitudinal muscular bundles; in, intestine; lb, lateral blood vessel; ln, lateral nerve; 1v, left cephalic blood vessel; mf, median dorso-ventral furrow; nb, nerves originated from brain; oc, ocellus; op, opening of pylorus; pa, pore of apical organ; ph, peripheral nerve; pr, proboscis; rc, rhynchocoel; rv, right cephalic blood vessel; st, stomach; ts, transitional wall of stomach in oesophagus; vg, ventral ganglion; vp, vascular plug inside proboscis sheath.

Figure 6. Frontonemertes serpentina, new genus and species, holotype. (a) Transverse sections between 14 and 234 from anterior end of body and 206 from middle portion of body showing minute glands of apical organ, opening of frontal glands and cephalic glands; (b) posterior portion of cerebral sensory organ showing sensory canal, ganglionic mass and eosinophilic glands; (c) opening of cerebral organ canal and cephalic groove; (d) posterior end of cerebral organ canal; (e) anterior portion of cerebral sensory organ with sensory canal and ganglionic masses; (f) right efferent duct and its opening, peripheral nerve of lateral nerve cord and lateral blood vessel in stomach region; (g) intestine and row of eggs; (h) enlargement of egg in (g). Scale 50 mm (b, d, e), 100 mm (a, c, f, h) and 200 mm (g). Abbreviations: bl, body wall longitudinal muscle layer; cg, cephalic glands; cn, cerebral organ canal; cs, cerebral sensory organ; dr, dermis; ed, efferent duct; eo, eosinophilic glandular mass; gc, ganglionic mass; ga, glands of apical organ; hr, head retractor muscles; in, intestine; lb, lateral blood vessel; le, egg enlarged; ln, lateral nerve; mf, median dorso-ventral furrow; ne, nephridia; of, opening of frontal glands; oo, opening of cerebral organ canal; ph, peripheral nerve; rg, right cephalic groove; sa, sensory canal of cerebral sensory organ; st, stomach.