Vulcanonemertes rangitotoensis

Gibson, Ray & Strand, Malin, 2002, A new genus and species of monostiliferous hoplonemertean (Enopla: Hoplonemertea: Monostilifera) from New Zealand, Zootaxa 50, pp. 1-20 : 3-14

Vulcanonemertes rangitotoensis gen. et sp. nov. ( Figs 1­20 )

Amphiporus sp. Morton & Miller, 1968

Etymology: The specific epithet, rangitotoensis , is derived by adding the Latin adjectival suffix – ensis (= belonging to) to the name of the island, Rangitoto, the site where the species was first discovered by RG in 1992.

Type specimens: Holotype: Te Papa Museum of New Zealand, Wellington, ZW 1511, 222 slides, transverse sections of complete female; Paratype: ZW 1512, 43 slides, sex not determined, transverse sections through head and foregut region of body; 2 complete voucher specimens, ZW 1513.

Type locality: West coast of Rangitoto Island, just south of Rangitoto Beacon, under stones or volcanic boulders in silty­sand, coarse sand with some silt or fine, compacted silty­clay, lower mid­shore to upper shore above upper limit of algae, collected 18­21 August 1992, 30+ specimens.

Associated fauna and flora: The dominant algal species was Hormosira banksii (Turner) Decne. , but Ecklonia radiata (C. Agardh) J. Agardh was also fairly abundant. Associated fauna included the molluscs Cellana radians (Gmelin, 1791) , Cominella virgata H. & A. Adams, 1853, Haliotis iris Gmelin, 1791 , Turbo smaragdus Gmelin, 1791 , Onithochiton neglectus Rochebrune, 1881 , and Scutus breviculus (Blainville, 1817) , crustaceans Chamaesipho columna (Spengler, 1790) , Pagurus novizelandiae (Dana, 1852) , and Palaemon affinis Milne Edwards, 1837 , and echinoderms Patiriella regularis (Verrill, 1867) and Evechinus chloroticus (Valenciennes, 1846) . On muddier surfaces, Onchidella nigricans (Quoy & Gaimard, 1832) was particularly common.

Additional material: Whangaumu Bay, 2 specimens, 25 August 1992; Pukerua Bay, 4 specimens, 30 August 1992; Whangaparaoa, 7 specimens, 1 September 1992; Leigh Harbour, 4 specimens, 2 September 1992. Intertidal beneath stones and boulders embedded in muddy silt, fine compacted silt clay or coarse sand with some silt.

Description

External features: The largest specimen found was about 8­8.5 cm long and 3­3.5 mm wide. The general appearance of the nemerteans closely resembles the ‘ Amphiporus sp.’ illustrated and briefly described by Morton & Miller (1968: 173­174, 231, pl. 8, fig. 5), although they record the species as “six inches [15 cm] or more long when uncoiled and outstretched”. The body has a more or less uniform width in its anterior region, but widens somewhat and is rather flattened dorsoventrally throughout most of the intestinal region, only narrowing as it approaches the bluntly pointed tail ( Fig. 1 A). The rather flattened head, which possesses a distinct median anterior notch ( Fig. 1 B), is slightly wider than the adjacent body region and forms an indistinct cephalic lobe in anaesthetised individuals. The four groups of eyes ( Fig. 1 B), which in life and in unstained sections are orange in colour, each contain up to about 10 ocelli. The two anterior groups are located close to the cephalic margins, the posterior groups are closer toward the mid­line. A single pair of shallow, oblique transverse cephalic furrows is situated near the rear of the head; the furrows do not meet mid­dorsally. The brain lobes are just visible as faint oval patches close behind the posterior groups of eyes.

Larger examples are typically orange, tending toward brown­orange in their more posterior regions, while smaller individuals are salmon­pink. The gut is often a dark greyishto orange­brown, the gonads in mature specimens appearing as greyish­white ovaries or testes throughout the intestinal regions of the body. Morton & Miller (1968) described their ‘ Amphiporus sp.’ as “[anteriorly] coral pink to reddish brown... The hinder part of the body is flattened and mauve brown, with darker gut diverticula”, though their colour plate clearly depicts the whitish gonads extending through approximately the posterior three­quarters of the body length.

The nemerteans secrete copious amounts of a fairly viscid mucus and readily evert and retract their proboscis when they are disturbed. When kept in clean seawater in a sealed container they tend to emerge and remain in the air space below the lid.

Body wall, musculature and parenchyma: The ciliated epidermis, 30­65 µ m or more thick in most parts of the body, conforms to the generalised hoplonemertean type described by Norenburg (1985) and contains mucous, serous and bacillary gland cells.

Mucous and serous cells comprise the commonest glands in most regions of the body, although the more posterior parts are dominated by acidophilic serous glands which vary in appearance from flask­shaped cells filled with finely granular cytoplasm to lozengeshaped structures with homogeneous contents. The proximal epidermal basal­cup zone and underlying basal lamina are mostly distinct.

Beneath the basal lamina a well­developed connective tissue dermis is mostly about 7­ 15 µ m across but, depending upon the degree of local body wall contraction, may appear almost as thick as the epidermis. The dermis is crossed by large numbers of slender, radial fibrils, similar to those described by Pedersen (1968).

The body wall musculature is well developed and comprises the basic hoplonemertean arrangement of outer circular and inner longitudinal layers, respectively some 7­30 µ m and 45­180 µ m or more in thickness. A distinct zone of diagonal muscle fibres, up to about 15 µ m across, is evident between the circular and longitudinal layers ( Figs 2 , 3 ). Circular and diagonal muscle layers extend forwards to the tip of the head, but together are only about 10­15 µ m thick anterior to the proboscis pore. The longitudinal layer is anteriorly divided. Close behind the brain bundles of longitudinal muscle fibres in the inner portion of the longitudinal muscle layer become enclosed by thin connective tissue membranes. These bundles form the origin of the inner longitudinal layer; dorsally they are separated from the fibres of the outer longitudinal zone only by their connective tissue membranes, but laterally and ventrally the two portions of the longitudinal musculature are divided by posterior extensions of the cephalic glands. The inner longitudinal muscles lead to the proboscis insertion, at the front of the brain, which has no contribution from the outer longitudinal zone, i.e., there is no pre­cerebral septum as defined by Kirsteuer (1974). Both inner and outer longitudinal muscle layers, however, contribute to the cephalic retractor muscles. In front of the proboscis insertion large numbers of diagonal and oblique muscle bundles criss­cross the head between the cephalic gland lobules ( Fig. 7 ). Throughout the postcerebral length of the body bundles of muscle fibres radiate inwards between the blocks of longitudinal muscles ( Figs 2 , 3 ). Peripherally, some of these radiating muscles have their origin in the diagonal muscle layer, others penetrate into the dermis. Both dorsally and ventrally these radiating muscle fibres loosely form an incomplete inner circular muscle coat ( Fig. 2 ); where the two layers meet laterally they form a strong muscle cross composed of interwoven fibres. In the foregut region of the body the dorsal half of the inner circular musculature is supplemented by fibres leading from the rhynchocoel circular muscle layer; as they extend ventrally some of these fibres branch off to pass close to the lateral walls of the foregut before merging with the ventral portion of the inner circular musculature.Most of these muscle fibres then turn to radiate outwards towards the body wall but isolated strands meet below the foregut. A weak but complete inner circular muscle layer is thus present in the foregut region of the body ( Fig. 4 ). On either side of the rhynchocoel and foregut the lateral blood vessels and nerve cords are located in the parenchyma between inner and outer bundles of muscle fibres ( Figs 2 , 5 ). Once the anterior pouches of the intestinal caecum begin to appear, however, the circular muscle fibres running close to the foregut wall become split up and no longer complete an inner circular muscle layer. Throughout the intestinal regions of the body the radiating muscle fibres unite to form strongly developed dorsoventral bundles which cross the body between the lateral intestinal diverticula, and no traces of the inner circular musculature remain.

Parenchymatous connective tissues are extensively developed along the lateral margins of the body from the cephalic region back. Towards the rear of, and posterior to, the rhynchocoel the parenchyma is also abundantly developed above and below the gut.

Proboscis apparatus: The proboscis pore is ventral and subterminal. It opens into a rhynchodaeum whose epithelium possesses neither cilia nor gland cells. Although many of the cephalic dorsoventral and oblique muscle fibres run immediately adjacent to the rhynchodaeal epithelium, they do not form a discrete circular muscle layer enclosing this portion of the proboscis apparatus.

The rhynchocoel terminates approximately 9.5 mm anterior to the tip of the body in the holotype, i.e., the rhynchocoel has a length of almost 90% of the total body length. Its wall contains separate circular and longitudinal muscle layers. For much of its length the rhynchocoel is between 60­75% of the body diameter. In the stomach region a small accumulation of acidophilic spheres to one side of the rhynchocoel ( Fig. 2 ) are interpreted as possibly representing parasite spores.

The retracted proboscis is between one third and one half of the body length. Its anterior portion ( Figs 2 , 6 ), up to about 1.1 mm in overall diameter (50% of the body width), forms the major part of the organ. It comprises an outer glandular epithelium, 40­45 µ m or more thick, distally dominated by basophilic glands and arranged into conical papillae. Below the epithelium a well developed connective tissue layer, mostly about 15 µ m across, is extended to form a central core into groups of papillae. The three muscle layers comprise an outer circular coat mostly 20­45 µ m across, a middle longitudinal layer 30­60 µ m thick in which the 22 proboscis nerves run in the inner (proximal) third and are circumferentially linked by a thin but distinct neural sheath, and an inner circular muscle zone 2­3 µ m deep. The longitudinal and inner circular muscle layers are separated by a thin (2­3 µ m) connective tissue region. The innermost lining of the proboscis is thin and delicate.

The stylet bulb region in general exhibits typical monostiliferous construction, although the epithelium of the large muscular bulb chamber, 15­20 µ m thick, contains acidophilic gland cells and is deeply folded. The stylet bulb canal, some 15 µ m in diameter and lined with an epithelium 25­30 µ m thick, extends anteriorly from this chamber and passes to one side of the stylet basis ( Fig. 8 ) before opening into the lumen of the anterior proboscis. The stylet basis ( Fig. 9 ) is up to about 120­130 µ m long and 50­55 µ m in maximum diameter, the central stylet varies from 95­150 µ m in length depending upon the size of the animal, usually with larger stylets occurring in larger individuals. In smaller, immature specimens the central stylet is approximately twice the length of its basis, but in larger, older individuals the stylet:basis ratio is about 1:1. The number of accessory stylet pouches varies between specimens from 2­5, mostly with 2­3 accessory stylets per pouch ( Fig. 8 ).

The posterior portion of the proboscis has a much simpler construction and comprises an outer epithelium, up to about 45 µ m thick, which is not developed in papillae; the epithelium is composed almost entirely of acidophilic gland cells. Below the epithelium the outer longitudinal and inner circular muscle layers, respectively some 15­25 µ m and 7­12 µ m thick, are separated by a thin but distinct connective tissue coat.

Alimentary system: The oesophagus separates off from the ventral wall of the rhynchodaeum approximately half way between the proboscis pore and the front of the brain lobes. Its unciliated epithelium, mostly 20­30 µ m tall, contains large numbers of acidophilic gland cells. As it passes below the ventral cerebral commissure the oesophagus begins to expand and its epithelium increases in thickness to 45 µ m or more as it merges into the ciliated epithelium of the stomach.The richly glandular stomach epithelium, 60­70 µ m or more thick, is moderately deeply folded ( Fig. 2 ) and regionally differentiated. A short anterior portion, approximately 120 µ m long, possesses only acidophilic glands, but for most of the stomach length both acidophilic and basophilic glands are present. Towards its rear the stomach gradually narrows and its epithelium becomes progressively less folded, thinner and increasingly dominated by basophilic glands as it leads into the slender, tubular, pyloric region. The total length of the stomach in the holotype is about 4.8 mm, of which slightly more than 1 mm comprises the pylorus. Muscle fibres of the body wall inner circular muscle layer extend ventrally adjacent to the stomach wall ( Fig. 4 ) to form a weak circular somatic muscle layer around the foregut.

The pylorus opens into the dorsal wall of the intestine ( Fig. 10 ). From this junction an intestinal caecum extends anteriorly for about 1 mm below the posterior portion of the foregut, terminating in a pair of long, tubular anterior pouches which reach, one on either side, to slightly more than half way along the length of the stomach ( Fig. 4 ). The epithelium of the pouches is only about 15­30 µ m thick and, unlike the main intestinal wall, contains very few gland cells. Both the caecum and its anterior pouches bear branched, tubular lateral diverticula. These diverticula are large close to the intestine but become progressively smaller farther anteriorly and are missing entirely from the anterior half of each pouch.

Below the rhynchocoel the intestine is dorsoventrally compressed but beyond the end of the rhynchocoel is much more tubular. Its gastrodermis, 45 µ m or more thick, possesses a typical hoplonemertean appearance with large numbers of acidophilic gland cells. Throughout its length the intestine bears large, distally branched lateral diverticula whose epithelium is generally thicker than that of the main intestinal canal. The anus opens ventrally a short distance in front of the posterior tip of the body.

Blood system: The blood system conforms with a basic hoplonemertean plan. In the head a simple transverse loop links the two spacious cephalic vessels which follow a tortuous, meandering route as they extend back towards the brain. The vessels possess thick walls, with associated muscle fibres, and are surrounded by enormous numbers of vacuolar ‘pouches’ ( Fig. 11 ), 15 µ m or more in diameter, which can occasionally be found opening into the lumen of the blood vessels. The vacuolar structures closely resemble the extra­vascular pouches described and illustrated by Moore & Gibson (1981) for Pantinonemertes species.

As they approach the front of the brain the cephalic vessels narrow before entering the cerebral ring. Behind the brain the three longitudinal vessels, paired lateral and single middorsal ( Fig. 2 ), extend to the posterior tip of the body where they meet via a supra­intestinal connective. All three are surrounded by large numbers of the vacuolate ‘pouches’, although these tend to be compressed around the mid­dorsal vessel where this extends between the gut and rhynchocoel walls. The mid­dorsal vessel arises as a branch from one of the cephalic vessels in the cerebral ring but does not, as in most hoplonemerteans, form a vascular plug. The lateral vessels twist and loop along the length of the body, so that in transverse sections there may appear to be two or three blood channels on either side of the body, above or below the intestinal diverticula, close to the lateral nerve cords or adjacent to the lateral margins of the rhynchocoel. There are, however, no pseudometameric transverse connectives linking the three longitudinal vessels.

Nervous system: The cerebral ganglia, of a moderate size (between 50­60% of the body width in the cerebral region), have dorsal lobes extending farther forward than the ventral. They are enclosed by a thin but distinct outer neurilemma but there is no inner neurilemma between the fibrous and ganglionic components. Dorsal and ventral cerebral commissures are respectively some 20­25 µ m and 55­60 µ m thick; the dorsal commissure forms a shallow anterior loop over the rhynchocoel. No evidence of neurochord cells could be found in any part of the brain. The lateral nerve cords possess both myofibrillae and a dorsal accessory neuropil ( Fig. 12 ) which extends the full length of the body. The origin of these accessory nerves can be traced to the fibrous tissues of the dorsal ganglionic lobes. Throughout the length of the body the accessory nerves irregularly emerge from the main nerve cords to run for a short distance close to, but quite separate from, their dorsal margins ( Fig. 13 ). A similar situation has been reported for the New Zealand terrestrial hoplonemertean, Antiponemertes pantini (Southgate, 1954) , by Moore (1973), but all three Antiponemertes species differ significantly from the present form in possessing a rhynchocoel musculature organised into a single wickerwork layer of interwoven longitudinal and circular fibres. The accessory nerves also irregularly bifurcate so that in transverse section a lateral nerve may appear to possess two accessory nerves ( Fig. 14 ); this condition has not been recorded for any other nemertean species. Occasional neural tracts also lead from the main neuropil towards the lateral body margins. The main nerves meet posteriorly via a subintestinal commissure. The main neuropil is up to about 65­70 µ m in diameter, the accessory nerves variable but mostly 50­55% of this width.

The peripheral nervous system includes several distinct tracts leading anteriorly from the front of the brain lobes and ventral cerebral commissure, although the ultimate fate of these was not traced. Foregut nerves are also distinguishable as a few small, irregularly distributed, nerves running close to the basement membrane of the stomach wall.

Excretory system: The well developed excretory system extends from close behind the brain back through the foregut region beyond the anterior limit of the anterior pouches of the intestinal caecum. It consists of three to five thick­walled, ciliated collecting tubules, up to 45 µ m or more in diameter, running in the parenchyma on each side of the body immediately adjacent to the body wall longitudinal muscle layer ( Figs 2 , 3 ). Anteriorly the collecting tubules lead to a single large chamber whose epithelium is about 7­8 µ m thick and densely ciliated. From this chamber a single efferent canal ( Fig. 15 ), characterised by a thinner (3­4 µ m) and less densely ciliated epithelium and only about 15­18 µ m in width, leads outwards through the body wall to open via a lateral nephridiopore. The nephridiopore on one side of the body opens farther back than on the other. No evidence of flame cells could be found in any part of the excretory system.

Apical organ and cephalic glands: The apical organ opens subterminally on the ventral surface of the head. It forms a tubular chamber, up to about 90 µ m in diameter whose epithelium, 8­10 µ m thick, is clad with long, dense cilia. Tracts of secretion are visible leading from the cephalic glands into the dorsal margin of the apical organ.

Cephalic glands consisting of irregularly shaped, pale blue­staining and vacuolate lobules ( Fig. 16 ), fill much of the pre­cerebral space around the rhynchodaeum. Anteriorly the glands discharge via the apical organ. The glands ventrally and ventrolaterally extend behind the brain, where they divide the body wall longitudinal muscle layer into inner and outer regions. On either side of the body blocks of the glands also continue far back into the foregut region of the body ( Figs 2 , 5 ), becoming progressively smaller as they extend posteriorly until they disappear completely a short distance in front of the pyloric region.

Basophilic submuscular glands are confined to the pre­cerebral regions, between the outer portion of the body wall longitudinal muscle layer and the cephalic glands ( Fig. 16 ). These glands are most abundant in the dorsal half of the head.

Sensory organs: The eyes ( Figs 1 , 17 ), are up to 60 µ m or more in diameter.

Two pairs of shallow cephalic furrows are distinguishable in sections, but only the posterior pair, forming oblique grooves towards the rear of the head which do not meet mid­dorsally, is visible in life. The short, horizontal, ventrolateral anterior furrows ( Fig. 18 ) are situated at or close behind the level of the proboscis pore, depending upon the degree of cephalic contraction. The ciliated cerebral canals, at first 40­45 µ m in diameter, emerge from the inner margin of these furrows, pass through the dermis and then turn posteriorly for a short distance before leading into the cerebral sensory organs. The cerebral organs ( Fig. 7 ), some 270 µ m long, 90 µ m wide and 150 µ m in dorsoventral height, are situated far forward in the head, about level with the posterior margins of the proboscis pore. For much of their length the organs possess an outer layer of strongly acidophilic glands which extend to form a posterior glandular cap. The cerebral organ nerve, 30 µ m diameter, is long and extends back laterally towards the brain between the cephalic gland lobules.

Reproductive system: The sexes are presumed separate; in larger living specimens ovaries were clearly visible in some individuals, what were interpreted as testes were seen in others. The holotype possesses occasional ovaries with a single egg in each ( Fig. 19 ) located in the parenchyma of the intestinal region. Their small number and irregular distribution, however, are unlike those reported for any other hoplonemertean species. Other, smaller but more numerous structures in the parenchyma contain strongly acidophilic bodies with a homogeneous cytoplasm; whether these represent immature ova or gonads degenerating under the influence of a parasitic infestation is uncertain, although other females with no evidence of parasitic infection also possess few mature ova.

Parasites: Throughout the intestinal region of the holotype the parenchyma contains large numbers of lightly basophilic, vacuolate spherical bodies ( Fig. 20 ), up to about 140­150 µ m or more in diameter, enclosed by thin but distinct connective tissue membranes. The identification of these structures, which are interpreted as some form of parasite, will form the basis of a future investigation.

Figures

FIGURE 1. Vulcanonemertes rangitotoensis gen. et sp. nov. Drawings of a complete specimen (A) and enlargement of the head viewed dorsally (B), based on sketches made in life, to emphasise the distribution of the eyes and appearance of the posterior pair of cephalic furrows.

FIGURE 2. Vulcanonemertes rangitotoensis gen. et sp. nov. Camera lucida drawing through the stomach region in cross­section to show the arrangement of the various body structures. AS, acidophilic spheres; CG, cephalic gland; CM, body wall circular muscle layer; DE, dermis; DM, body wall diagonal muscle layer; DV, mid­dorsal blood vessel; EP, epidermis; EX, excretory tubule; LM, body wall longitudinal muscle layer; LN, lateral nerve cord; LV, lateral blood vessel; PR, proboscis; RC, rhynchocoel; ST, stomach.

FIGURES 3 ­ 8. Vulcanonemertes rangitotoensis gen. et sp. nov. 3, Transverse section through part of the body wall in the foregut region, showing the organisation of the body wall muscle layers. The diagonal muscle layer is indicated by an arrowhead. LM, body wall longitudinal muscle layer. 4, Transverse section through the stomach region to show the thin circular somatic muscle layer, indicated by arrows. The anterior pouches of the intestinal caecum are indicated by stars. PR, proboscis. RC, rhynchocoel. ST, stomach. 5, Transverse section through the foregut region to show how the cephalic glands extend behind the brain as lateral blocks of tissue, and the dorsoventral muscle fibres, indicated by arrows, passing on either side of the lateral blood vessels and nerve cords. CG, cephalic glands. LM, body wall longitudinal muscle layer. LN, lateral nerve cord. LV, lateral blood vessel. 6, Transverse section to show the organisation of the anterior portion of the proboscis. PE, proboscis epithelium. RC, rhynchocoel. 7, Transverse section through part of the head, showing oblique and radial muscle fibres running between the cephalic glands. CG, cephalic glands. CO, cerebral sensory organ. 8, Transverse section through the proboscis stylet bulb to show five accessory stylet pouches. The stylet bulb canal is indicated by an arrow. RC, rhynchocoel. SB, stylet basis.

FIGURE 9. Vulcanonemertes rangitotoensis gen. et sp. nov. Drawings of the central stylet and basis from a young specimen (A), with a stylet: basis ratio of about 2: 1, and from a larger individual (B) where the ratio is about 1: 1. CS, central stylet. SB, stylet basis.

FIGURES 10 ­ 16. Vulcanonemertes rangitotoensis gen. et sp. nov. 10, Transverse section through the junction between the pyloric canal and intestine. IN, intestine. PR, proboscis. 11, Transverse section through a cephalic blood vessel to show the appearance of the vacuolar ‘ pouches’. 12, Transverse section through a lateral nerve cord to show the accessory lateral nerve, indicated by an arrow. LN, lateral nerve cord. 13, Transverse section through a lateral nerve cord with the accessory lateral nerve, indicated by an arrow, running separately above it. 14, Transverse section through a lateral nerve cord in a region where the accessory lateral nerve has divided to form two neural tracts. 15, Transverse section through an efferent excretory tubule. 16, Transverse section through part of the head to show the appearance of the cephalic glands. CG, cephalic glands. DE, dermis.

FIGURES 17 ­ 20. Vulcanonemertes rangitotoensis gen. et sp. nov. 17, Transverse section through part of the head to show two of the ocelli. 18, Transverse section through one of the short, anterior cephalic furrows; the arrow indicates a ciliated canal leading to a cerebral sensory organ. EP, epidermis. 19, Transverse section through an ovary to show an egg. OV, ovary. 20, Transverse section through the posterior region of the body showing several of the basophilic, vacuolar structures (indicated by arrows) which are interpreted as some form of parasite. IN, intestine.