Redescription of Tubulanus mawsoni (Wheeler 1940) comb. nov. (Palaeonemertea: Tubulanidae) from the Bellingshausen Sea (Antarctica)

Abstract

Tubulanus mawsoni (Wheeler 1940) comb. nov. is redescribed based on the material collected during the Spanish Antarctic expedition Bentart-03 through the Bellingshausen Sea (Antarctica). Previously belonging to the genus Carinina Hubrecht 1885, the species is transferred to the genus Tubulanus based on the situation of the brain and lateral nerves between the basement membrane and the outer circular muscle layer, the presence of muscle crosses in the body wall, the position of the blood and excretory systems, the presence of proboscis nerves and the structure of the cerebral sensory organs, the rhynchocoel wall and the rhynchodaeal and buccal nerves. Microphotographs of the different regions of the body and the proboscis structure are provided for the first time. Based on the ambiguities between Tubulanus diagnosis and the species descriptions, as well as the possible paraphyletic status of the genus, the need for new morphological and molecular studies is suggested.

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Keywords:

• Tubulanus mawsoni
• Carinina, Nemertea
• Bellingshausen Sea
• Antarctica
• taxonomy

Introduction

In the most recent revision of Antarctic marine benthic diversity by Clarke and Johnston (2003), the Nemertea are considered to be a relatively well-known group in this geographic area. Mahon et al. (2010), using molecular methods, have shown the underestimation of Antarctic nemertean diversity. Although a large number of species of this phylum have been identified from Antarctic and sub-Antarctic waters (Bürger 1904; Joubin 1910; Baylis 1915; Dawson 1957; Gibson 1985), the class Palaeonemertea is poorly represented in Antarctic waters, by two species (Dawson 1969) of the genus Carinina Hubrecht 1885: C. antarctica Bürger 1904 and C. mawsoni Wheeler 1940. Müller (1965) reviewed the genus and regarded the attribution of these species to this genus doubtful. Carinina antarctica Bürger 1904 was considered a nomen dubium by Sundberg and Hylbom (1994).

During the Spanish Antarctic expedition (Bentart-03) nemerteans were collected from several locations, mainly in the Bellingshausen Sea and in surrounding areas at depths ranging from 10 to 2045 m. The Bellingshausen Sea, in the western sector of Antarctica, is one of the least explored Antarctic seas because of the prevalence of ice (Saíz et al. 2008, in press); its benthic communities have been researched relatively poorly. The collection includes hoplonemerteans (Uz et al. 2010), heteronemerteans (Fernández-Álvarez & Anadón 2012) and two specimens of palaeonemerteans. In the current study, one species of Tubulanidae Bürger 1904 (Palaeonemertea Hubrecht 1879) is redescribed on the basis of histological sections of the two specimens. Photomicrographs of the different regions of the body and the proboscis structure are provided for the first time. We conclude that morphological characteristics clearly place C. mawsoni in the genus Tubulanus. Therefore, the following new combination is proposed: Tubulanus mawsoni (Wheeler 1940) comb. nov.

Material and methods

The material examined was obtained during the ‘Bentart-03’ Spanish Antarctic expedition in February 2003, from the Bellingshausen Sea (Antarctica)—off Peter I Island (Antarctica)—68°56′47″ S, 90°35′13″ W (station 5), aboard the RV Hespérides. Peter I Island is an isolated oceanic island of volcanic origin (Kimura 1982) in the Antarctic sector corresponding to the Bellingshausen Sea (Fig. 1).

Figure 1 Position of station 5 during Bentart-03 survey, where Tubulanus mawsoni (Wheeler, 1940) comb. nov. was found.

The two specimens available were collected at a depth of 128 m with a Box-corer, from dark muddy-sand and gravel bed (81.1% silt and 0.3% gravel); organic matter (%) 1.431; redox (Eh) value 199.25.

The living animals were anaesthetized in 7.5% MgCl₂ in distilled water before fixation in Bouin's fluid. The specimens, for histology, were embedded in paraffin following the Peterfi method (Pantin 1968), sectioned at 7 µm, and stained using the Para-pak^® (Meridian Biosciences, Inc., Cincinnati, OH, USA) trichrome method.

The ratio of epidermal thickness to body diameter in the brain and intestinal regions was calculated as the index E, following the method of Kajihara (2006). The classification in all taxonomic levels has been taken from Kajihara (2007).

Family Tubulanidae Bürger 1904

Carinellidae McIntosh 1874: 137.

Tubulanidae Bürger 1904: 10; Bürger 1897–1907: 401, 402, 405.

Genus Tubulanus Renier 1804

Tubulanus Renier 1804: 20.

Carinella Johnston 1833: 232; synonymized by Bürger (1904).

Type species

Tubulanus polymorphus Renier 1804 by monotypic designation.

Diagnosis

The following diagnosis was given by Gibson (1994), Gibson and Sundberg (1999), Cantell (2001) and Ritger and Norenburg (2006).

Length at the onset of sexual maturation 2–10 cm; coloured, usually with a conspicuous pattern; head furrows present; body-wall musculature consisting of outer and inner circular and middle longitudinal layers; muscle crosses present between outer and inner circular muscles in some species; cerebral sensory organs consisting of ciliated pits or ciliated canals in the epidermis; side organs present in foregut region in some species; cephalic region with nerve layer; two nerves in rhynchodaeal epithelium; proboscis nerves present; brain and lateral nerves situated between epidermal basement membrane and outer circular muscles; epidermal basement membrane usually thick; buccal nerves present and paired; rhynchocoel wall with circular muscles only; proboscis musculature with inner longitudinal and outer circular layers; circular muscle layer in rear end of rhynchocoelic or in nephridial regions strongly developed; gland-like anterior part of excretory system entering lateral blood vessels; blood vascular system without mid-dorsal vessel; eyes absent; sexes separate.

A complete discussion of the nomenclatural history of the family and the genus is provided by Kajihara (2006, 2007) and Ritger and Norenburg (2006), respectively.

Tubulanus mawsoni (Wheeler 1940) comb. nov. (Figs. 2–5, Appendix 1)

Figure 2 Tubulanus mawsoni (Wheeler, 1940) comb. nov.A, Immature female specimen after fixation in Bouin's fluid. B, Detail of the head in ventral view. HE, head; MO, mouth; PP, proboscis pore. Scale bars: 1 mm.

Diagnosis

Tubulanus without a conspicuous colour pattern; blood-pink head; cream-coloured body with a pinkish tinge; body cylindrical in section; head not wider than trunk; epidermal basement membrane thick; dorsal and ventral muscle crosses present between outer and inner circular muscles; diagonal muscles absent; cerebral sensory organs consisting of ciliated pits; side organs absent; with nerve layer; neurochords into lateral nerve cords; muscle plate present between rhynchocoel and gut; intestine without lateral diverticula; excretory system present; rhynchocoel extending almost throughout the body.

Type locality

Antarctica (67°03′ S, 74°29′ E), at 437 m depth.

Material examined

Sexually immature female (Fig. 2), 18 mm long and 1 mm maximum width, February 2003, NA coll.; 7-µm transverse serial sections through the anterior portion of the body to the posterior tip of the body, 39 slides in total (MNCN 5.01/16 to MNCN 5.01/54).

Sexually mature male, 24 mm long and 1.2 mm maximum width, February 2003, NA coll.; 7-µm transverse serial sections through anterior body to foregut region (10 slides) and posterior tip (eight slides), 7-µm longitudinal serial sections in the middle of the body (10 slides) and unsectioned portions of intestinal region and a fragment of everted proboscis, 28 slides in total (MNCN 5.01/55 to MNCN 5.01/82).

The material is deposited at the Museo Nacional de Ciencias Naturales (MNCN), Madrid.

Collecting locality

Off the west Peter I Island, Bellingshausen Sea (Antarctica) (68°56′47″ S, 90°35′13″ W), at 128 m depth.

External features

The anaesthetized living specimens ranged from 2 to 2.5 cm long and 1 to 1.5 mm wide. The cephalic lobe is rounded and distinct, narrower than the trunk. Two pairs of shallow ventral cephalic furrows are present. The mouth is a small compressed slit at the rear of the head situated ventrally (Fig. 2B). The body is circular in section while the posterior region is slightly compressed dorsoventrally in the sexually mature specimen. The posterior end of the body presents a slightly pointed tip. The ground colour is cream with a pinkish tinge; head is blood pink with cephalic margins translucent white. In the original description the colour is ‘yellowish-brown at the ends, but brownish-purple in the middle’, but is based in fixed material (Wheeler 1940, p. 235) without any note about the colour of the living specimen.

Body wall, musculature and parenchyma

The epidermal thickness varies along the body length. It is thicker in the cephalic (88–131 µm) and medial (72–138 µm) regions than in the posterior region (59–71 µm). In the pre-cerebral region, the ciliated epidermis is pseudostratified; the dorsal side is twice the thickness of the ventral. A well-developed basal stratum (58–82 µm) of pink-stained serous glandular cells (Fig. 3A, D) is present in dorsal epidermal tissue and it extends and acquires more prominence in front of the brain (Fig. 3B). Behind the ventral cerebral commissure, this cellular stratum is poorly developed dorsally and reaches its maximum height ventrally. Posterior to this, the stratum decreases abruptly. At the level of the ventral cerebral commissure, mucous cells with unstained cytoplasm (Fig. 3C) appear. In the buccal region, cells with blue-staining mucus and weakly red-stained cells are present (Fig. 3E). In the foregut region, the proximal half of the epidermis shows a band of serous or bacillary deep-red-stained secretory cells with small granules; the upper half of the epidermis in this region is dominated by mucous cells (Fig. 3F). In the intestinal region, the mucous glandular cells occupy the greater part of the height of the epidermis at the expense of the deep-red-stained cells. Towards the back, the epidermis becomes progressively a monostratified tissue. In the posterior intestinal region the mucous cells are nearly the only glandular cell type observed. E(b)=0.13; E(i)=0.09.

Figure 3 Tubulanus mawsoni (Wheeler, 1940) comb. nov.A, Transverse section at the proboscis pore showing the dorsoventral fibres in cerebral lacunae. B, Transverse section through the posterior rhynchodaeal region showing the glandular cells shared by the epidermis and the rhynchodaeal epithelia. C, Transverse section through the cerebral region at level of the proboscis insertion. D, Transverse section through the rhynchodaeal region showing the connection between rhynchodaeal and epidermal serous glands (arrowhead). E, Transverse section through the buccal region; note two different types of epidermal glands. F, Transverse section through the foregut region, at what would be the level of the fixation band. G, Transverse section through the anterior buccal region showing the buccal nerve. H, Transverse section through the foregut region showing the muscular plate (MP). I, Transverse section through the intestinal region, arrowhead points to the dorsal muscle cross. J, Transverse section through the intestinal region, arrowhead points to the ventral muscle cross. BM, basal membrane; BN, buccal nerve; BS, blue-staining mucous cell; CL, cephalic blood lacuna; CN, cephalic neural layer; DG, dorsal ventral ganglion; CP, connective tissue processes; EP, epidermis; IC, body-wall inner longitudinal muscle layer; IC, body-wall inner circular muscle layer; LB, longitudinal muscles below horizontal transverse muscles; LM, body wall longitudinal muscle layer; LN, lateral nerve cord; MC, mucous cell; OC, body wall outer longitudinal muscle layer; PS, pink-stained serous glandular cell; PN, proboscis nerve; PP, proboscis pore; PR, proboscis; RC, rhynchocoel; RD, rhynchodaeum; RS, deep red-staining cell; UD, upper mid-dorsal nerve; VG, ventral cerebral ganglion; WE, weak red-staining cell. Scale bars: 100 µm.

In the preserved specimens the fixation band typical of several Tubulanus species is not observed. However, in serial transverse sections our specimens exhibit differences in cell type distribution (Figs. 3E, F, 4D, E; in anteroposterior sequence), which agrees with the observation by Ritger and Norenburg (2006; Fig. 3) observation. In accordance with what these authors presented, the fixation band is observable in formalin- and ethanol-fixed specimens. The material examined in this paper is preserved in Bouin's fluid.

The epidermal basement membrane is up to 6.2 µm thick. Connective tissue processes extend from the basement membrane into the epidermis (Fig. 3D), forming a mesh-like network in the pre-cerebral region. A very thin neural layer is observed between the body-wall outer circular muscle layer and the basement membrane.

The body wall comprises outer and inner circular muscle layers and middle longitudinal ones. The body-wall outer circular muscle layer appears immediately anterior to the rhynchopore and acquires width progressively. The body-wall longitudinal musculature is formed at the level of the rhynchodaeum and is always well-developed throughout the body (Fig. 3A). In the pre-cerebral region the blood lacunae are pierced by some dorsoventral fibres that connect the dorsal and ventral sides of the outer circular muscle layer (Fig. 3A, B).

In front of the cerebral commissure some horizontal transverse muscle fibres (3–4 µm) derived from the outer circular muscle layer occur in the dorsal part of the longitudinal muscle layer (Fig. 3G). These horizontal transverse muscles disappear posteriorly to the buccal cavity.

In the mouth region, the ventral portion of the longitudinal body wall branches off ventrally to both sides of the buccal cavity (Fig. 3G). Also, in this region the inner circular musculature is formed and surrounds the rhynchocoel and the gut.

Between the rhynchocoel and the foregut wall, there is a thin muscle plate that is one fibre thick; it extends back almost the posterior part of the rhynchocoel (Fig. 3H). No dorsoventral musculature is found post-cerebrally. In the foregut and intestinal regions, dorsal (Fig. 3I) and ventral (Fig. 3J) muscle crosses are observed between the two body-wall circular muscle layers in foregut and intestinal regions. The muscle crosses are formed by a scarce number of muscle fibres and are in close connection with the nervous connections between the upper and lower mid-dorsal nerves (Fig. 3I). The ventral muscle cross only is visible in several sections of the female specimen and in almost the whole mature male, which could be related with the corporal size.

Parenchymatous connective tissues are poorly developed and present between the gonadal sacs in the mature specimen.

Proboscis apparatus

The proboscis pore opens subterminally in the ventral tip of the head (Fig. 3A). The rhynchodaeum forms a tubular chamber lined by slender epithelial cells with long cilia, up to 18.8 µm, and numerous serous, pink-stained cells in its anterior portion. This is a pseudostratified epithelium and its thickness increases back to 125 µm tall. In the posterior rhynchodaeal region, cilia are scarcer and glandular cells are more vacuolated (Fig. 3B). The rhynchodaeal serous glands are connected with epidermal similar cells (Fig. 3D), as occurs in other tubulanids (Hylbom 1957; Senz 1994). The rhynchodaeum is enclosed by a thin circular muscle layer (two to four fibres thick).

The rhynchocoel extends throughout almost the entire length of the animal. The proboscis sheath comprises an epithelium and a circular muscle layer (11–16 µm) in contact with the body-wall inner circular muscle layer. In the posterior end of the rhynchocoel, near the retractor muscle insertion, the epithelium and rhynchocoel wall are separated by a deeply staining basal membrane.

The proboscis insertion is situated in front of the mouth at the level of the ventral cerebral commissure (Fig. 3C). Few fibres from the ventral side of the body-wall longitudinal musculature contribute to the proboscis insertion. There are two proboscis nerves that originate from each end of the ventral cerebral commissure and penetrate into the proboscis.

The proboscis (Fig. 4A) is composed of an outer glandular epithelium (70–78 µm), an outer circular muscle layer (6–10 µm), an inner longitudinal muscle layer (19–25 µm) and a thin endothelium. The two proboscis nerves are situated between the glandular epithelium and the outer circular muscle layer (Fig. 3E). In the mature male a thin basal membrane is observed between inner longitudinal musculature and endothelium. A bundle of longitudinal retractor muscles (30–66 µm) extends from the end of the proboscis to the proboscis sheath musculature. The proboscis does not exhibit any significant regional histological differentiation.

Figure 4 Tubulanus mawsoni (Wheeler, 1940) comb. nov.A, Transverse section through the proboscis. B, Transverse section through the mouth showing the buccal chamber. C, Transverse section through the anterior foregut region. D, Transverse section through the posterior foregut region. E, Transverse section through the intestinal region. F, Transverse section through the foregut region showing the arrangement of the nephridial ducts and the lateral blood vessel. G, Transverse section through the foregut region, showing an excretory collecting tubule (EX). EP, epidermis; FG, foregut; IN, intestine; LM, body-wall longitudinal muscle layer; LN, lateral nerve cord; LV, lateral blood vessel; MO, mouth; NE, nephridial duct; OC, body-wall outer circular muscle layer; PE, proboscis outer glandular epithelium; PC, proboscis outer circular muscle layer; PL, proboscis inner longitudinal muscle layer; PR, proboscis; RC, rhynchocoel. Scale bars: 100 µm.

Digestive system

The mouth is a small oval slit that opens just behind the brain (Fig. 2B). The buccal cavity is lined by ciliated and glandular cells of several types: serous pink, red and blue-staining with small granules and mucous glandular cells are present (Fig. 4B). The foregut epithelium is ciliated and is divided into two different histological regions. The principal elements of the anterior region (Fig. 4C) are bacillary red and violet-staining gland cells. Mucous glandular cells are present in the anterior region but only in the ventral surface, while at the rear all kinds of gland cells are observed in both surfaces. In the posterior region and anteriad to nephridia, the columnar epithelium bears long cilia and serous red-staining gland cells that are the main constituent (Fig. 4D). In the junction between foregut and intestine, the epithelium decreases in thickness. In the intestinal region the epithelium increases in thickness and is deeply folded (Fig. 4E). In the posterior tip of the body a thin basal membrane appears between the gut and the body-wall inner circular muscle layer. There are no lateral intestinal diverticula or pouches. The intestine of the mature male specimen is reduced and compressed laterally in the gonadal region (Fig. 5F). Behind the rhynchocoel, the gut occupies most of the inner space of the body (Fig. 5G).

Figure 5 Tubulanus mawsoni (Wheeler, 1940) comb. nov.A, Transverse section through the posterior portion of the brain showing the connection between the ventral cerebral commissure and the proboscis nerve. B, Transverse section through the lateral nerve cord showing its position between the outer circular muscle layer and the basal membrane; black arrowhead points to a neurochord. C, Transverse section through the upper mid-dorsal nerve; white arrowhead points to the basal membrane; black arrowhead points to the inner neurilemma. D, Transverse section through the posterior portion of the dorsal cerebral commissure showing the junction with the upper mid-dorsal nerve. E, Transverse section through the cerebral sensory organ pit (CP). F, Transverse section through the intestinal region in the mature male. G, Transverse section through the intestinal region in the immature female. BM, basal membrane; CL, cephalic blood lacuna; EP, epidermis; IC, body-wall inner longitudinal muscle layer; IN, intestine; LN, lateral nerve cord; LM, body-wall longitudinal muscle layer; LV, lateral blood vessel; PN, proboscis nerve; PR, proboscis; OC, body wall outer longitudinal muscle layer; OV, ovum; RM, retractor muscle; RS, deep red-staining cell; TE, testis; UD, upper mid-dorsal nerve; VG, ventral cerebral ganglion. Scale bars: 100 µm.

Blood system

In the head a pair of cephalic blood lacunae lies inside the body-wall outer circular musculature and meet anteriorly above the rhynchodaeal opening. Throughout their length, these lacunae are irregularly subdivided by dorsoventral muscle bundles (Fig. 3A,B) that flank the rhynchodaeum and rhynchocoel. Behind the ventral cerebral commissure (Fig. 5A), both lacunae reduce their lumen and give rise to the lateral blood vessels (Fig. 4D,F). Cephalic lacunae and lateral blood vessels are lined by a thin endothelium and some circular muscle fibres, surrounded by a scarce amount of parenchymatous tissue. The internal surface of the circular fibres of the lateral blood vessels is in contact with the inner circular muscle layer. In the sexually mature male specimen, these lateral vessels are displaced by gonadal sacs to a ventral position, losing contact with the body-wall inner circular muscle (Fig. 5F).

Excretory system

The nephridial excretory system consists of a single pair of main ducts (52–93 µm in diameter) located medial to the longitudinal musculature in the foregut region and close to lateral blood vessels (Fig. 4F). In the anterior region, nephridial glands are observed as protrusions in the lateral blood vessels. The nephridia have some branches near the posterior end of the excretory system, which are observed in the sexually mature male specimen and in accordance with the observation of Wheeler (1940, fig. 1F). The nephridial ducts run forward 623–756 µm and open dorsoventrally by a single excretory pore on either side. The efferent duct is about 12–18 µm in diameter (Fig. 4G).

Nervous system

The cerebral ganglia and lateral nerve cords are situated between the epidermal basement membrane and the body-wall outer circular muscle layer (Figs. 3C, F, 5A–D). The cerebral ganglia (Figs. 3C, 5A) are well developed and connected by dorsal and ventral commissures, 20–26 µm and 55–70 µm thick, respectively. The dorsal and ventral ganglia are fused and separate only for a short distance in the posterior part of the brain. The ventral ganglia posteriorly extend as the lateral nerve cords (Fig. 5B), which possess a single neurochord (Fig. 5B) asymmetrically distributed into the fibrous core of the lateral nerve cords. An inner neurilemma is present, but an outer neurilemma is not observed. Only in the larger specimen the neurilemma seems distinct from the basement membrane (Fig. 5C).

A pair of buccal nerves (Fig. 3G) arises as a single trunk from the mid-ventral region of the ventral ganglia and runs at the base of the buccal epithelium alongside the mouth and the foregut region; each nerve up to 56 µm in diameter. Each nerve gives rise to a dorsal branch near the middle of the mouth. The buccal nerves disappear in the proximal foregut region.

The slender dorsal commissure gives rise to an upper mid-dorsal nerve (Fig. 5D) that lies in the base of the epidermis. Only to the anterior to the cerebral region this nerve is conspicuously covered by the basement membrane. It extends to the rear of the rhynchocoel and connects with the lower mid-dorsal nerve.

Several short but distinct cephalic peripheral nerves (24 µm in diameter) run anteriorly from the brain and extend between the epidermis and the basement membrane, forming a cephalic neural layer (Fig. 3B).

Sense organs

There are no eyes. The cerebral sensory organs are located just behind the ventral ganglia (Fig. 5E). They are two simple ciliated pits, approximately 91 µm deep and 22 µm wide, lined with slightly differentiated epithelium with small reddish glandular cells. There are no statoliths. No evidence of lateral sensory organs was observed.

Reproductive system

Sexes are separate. One specimen is a nearly sexually mature male collected in February (austral summer). The testes are confined to the intestinal region (Fig. 5F) where gonadal sacs are in a lateral position on each side of the body, above the lateral blood vessels and compressing the gut. The outer surface of the testis sacs is lined by some muscle fibres.

In the immature female specimen, the oogonia are found in the parenchyma, located on the dorsolateral sides of the intestinal region above the lateral blood vessels (Fig. 5G).

Discussion

Morphological and histological characters indicate that the two Antarctic palaeonemerteans belong to C. mawsoni Wheeler 1940. This author based the description of this species on an incomplete specimen with no more than the stump of the proboscis at its anterior attachment. This species is not described in detail, lacking key data for external and internal characters. Therefore, Sundberg and Hylbom (1994) excluded this species from their cladistic analysis of the class Palaeonemertea. The search for the holotype in the Australian Museum and in the Natural History Museum, London, was unsuccessful and this material is considered lost and not available to study. Despite this, Wheeler's illustrations are very detailed and the identity of the specimens from histological slides is convincing.

In the current paper the species is redescribed using the proposed checklist of the character-matrix (Appendix 1) by Sundberg et al. (2009) to avoid ambiguities in morphological species and genus delimitation. The generic status of this species is controversial: Hylbom (1957), Müller (1965), Friedrich (1970), Kulikova (1984) and Sundberg and Hylbom (1994) have questioned its generic placement. Hylbom (1957) considered this species as belonging to the genus Tubulanus because ‘C. mawsoni is probably a Tubulanus species with the nervous system situated between the basement membrane and the outer circular muscle layer and with the lateral blood vessels and the nephridial canals situated outside the inner circular muscle layer.’ Nevertheless, this second character used by Hylbom to transfer C. mawsoni to Tubulanus is present in C. johnstoni Senz 2000. Although most of the Tubulanus species have a conspicuous body colour pattern, this character is not shared by several species, including T. mawsoni. Other features place this species in the genus Tubulanus: the arrangement of the body-wall muscle layers and the nervous system, the structure of the cerebral sensory organs, the basement membrane, the rhynchocoel wall, the rhynchodaeal and buccal nerves. The presence of muscle crosses between circular muscle layers and the proboscis nerves, considered by Sundberg and Hylbom (1994) as possible synapomorphies for the genus Tubulanus, supports the inclusion of this species into Tubulanus.

As in most of the nemertean genera, several species allocated to Tubulanus are considered not well-described species (see Sundberg and Hylbom 1994). In addition, the character ‘intestine with shallow lateral diverticula’ is not present in some of the species assigned to Tubulanus, as occurs in T. hylbomi Gibson and Sundberg 1999, T. longivasculus Gibson and Sundberg 1999, T. riceae Ritger and Norenburg 2006, nor in T. mawsoni. Similarly, no body-wall diagonal muscles are reported in several species, including T. hylbomi, T. longivasculus and T. mawsoni, but these may be difficult to detect. Although the Tubulanus diagnosis specifies ‘nervous system with neither neurochords nor neurochord cells’, neurochord cells are present in T. riceae, whereas in the current redescribed species a single neurochordal processes in the lateral nerves is observed. To avoid ambiguities, these three characters are deleted in the diagnosis for the genus Tubulanus provided here. Both cladistic and molecular phylogenetic studies (Sundberg and Hylbom 1994; Andrade et al. 2012, respectively) point to a possible paraphyletic status of the genus Tubulanus. All these facts lead to the need to carry out more taxonomic and phylogenetic studies so as to clarify the status of this genus and to avoid the inconsistencies between the genus diagnosis and the species descriptions.

To date, the only two species of palaeonemerteans recorded for Antarctica are C. antarctica and C. mawsoni (Dawson 1957, 1957). But as C. antarctica is considered nomem dubium (Sundberg and Hylbom 1994), T. mawsoni (Wheeler 1940) comb. nov. is the only valid palaeonemertean species recorded for Antarctic waters. However, molecular survey of Antarctic planktonic larvae, Mahon et al. (2010) found 19 distinct Antarctic lineages of hoplonemerteans and heteronemerteans not previously genetically characterized and probably representing undescribed taxa. The absence of molecular data for Antarctic palaeonemerteans in the study of Mahon et al. (2010) may reflect scarcity of planktonic larvae or that they were not sampled. Future morphological and molecular studies may reveal greater species richness of palaeonemerteans in Antarctic waters.

Acknowledgements

The Bentar-03 cruise was supported by the Antarctic Programme REN2001 1074/ANT of the Spanish Government. We are grateful to Dr Ana Ramos, the leader of Bentart's projects and to our colleagues from Bentart cruise 2003. Thanks are due to the crew and UTM technicians of RV Hespérides. We greatly appreciate Helen Stoddart (Australian Museum) and Emma Sherlock (The Natural History Museum, London) for their help in the search of Wheeler's material. We would like to thank C. Lastra for assistance and linguistic review of the text of an earlier draft of the manuscript. Thanks to three anonymous reviewers for their helpful comments and suggestions, which substantially improved the manuscript. Javier Cristobo of the Spanish Oceanographic Institute provided the map in Fig. 1.

Appendix

Character matrix for Tubulanus mawsoni (Wheeler, 1940) comb. nov. Character states and code from Sundberg et al. (2009).

Character	Character state	Code	Figure
1. Biology	Free-living	0
2. Habitat	Marine	0
3. Benthic divisions	Sublittoral	2
4. Pelagic divisions	N/A	N/A
5. Substrate	Mud	0
6. Behaviour	Not observed	–
External morphology
7. Cephalic furrows	Two pairs	2	2B
8. Distribution of anterior cephalic furrows	Ventral	0	2B
9. Shape of anterior (dorsal) cephalic furrows	N/A	N/A
10. Shape of posterior (dorsal) cephalic furrows	N/A	N/A
11. Head demarcated from body	Head not wider than trunk	2	2A, B
12. Position of cephalic furrows	N/A	N/A
13. Shape of head/cephalic lobe	Rounded	0	2B
14. Head viewed laterally	Without extensions	0	2A
15. Shape of posterior tip	Pointed	0	2A
16. Eyes	Absent	0	2A
17. Eye morphology	N/A	N/A
18. Relative eye size	N/A	N/A
19. Eye distinctiveness	N/A	N/A
20. Eye position relative to brain lobes	N/A	N/A
21. Colour pattern	Absent	0
22. Primary dorsal body colour	Pink	7
23. Body colour hue/tint	Light	2
24. Internal organs visible through dorsal epidermis	Not observed	–
25. Lateral margins	Appear paler than dorsal body surface	0
26. Distribution of bristles/cirri	Not seen	0
Body wall
27. Epidermis non-cellular inclusions	Absent	0
28. Epidermis of anterior body	Without intra-epithelial muscle network	0
29. Ratio of thickness of epidermis/lateral body diameter in brain region	>0.1	1	3C
30. Dermis	Forming a distinct zone between epidermis and circular muscle layer	0	3F
31. Thickness of dermis	Less than half epidermal height	0	3F
32. Muscle processes from dermis into epidermis	Absent	0	3D
33. Muscle layers	Outer circular, middle longitudinal and inner circular muscle layer	2	3J, 4C, D, 5G
34. Muscle crosses between body wall circular muscle layers	Both dorsal and ventral muscle crosses	2	3I, J
35. Body wall longitudinal muscle layer just behind brain	N/A	N/A
36. Precerebral septum	N/A	N/A
37. Central (medial) muscle plate	Between foregut and rhynchocoel	1	3H
38. Parenchyma	Barely distinguishable other than as a membrane enclosing various body organ systems	0
39. Muscles fibre in mouth/foregut region	Present	1	3G
Proboscis apparatus
40. Proboscis pore	Subterminal, ventral	1	2B, 3A
41. Mouth and proboscis pore connection	Open separately	0	2B, 3A, 4B
42. Gland cells of rhynchodaeum	Present	1	3A, B, D
43. Rhynchocoel musculature	Circular muscles only	1	3C, 5A, G
44. Rhynchocoel musculature in posterior end	Approximately as anterior part	0	4E
45. Rhynchocoel length	Extending to or almost to posterior region of body	2	5G
46. Rhynchocoelic caeca	Absent	0
47. Size of posterior third of proboscis region	Small, less than 50% of body diameter in retracted position	0	4E, 5G
48. Musculature of proboscis (everted state)	Outer circular and inner longitudinal muscle layer	0	4A
49. Musculature of posterior proboscis region (everted state)	Outer circular and inner longitudinal muscle layer	2	4E
50. Epithelium of anterior proboscis region when everted	Developed into barbs/pseudocnids (secretory products of the epithelium)	2
51. Number of proboscis nerves	2	1
52. Proboscis nerve arrangement	Peripheral neural sheath absent or indistinct	0
53. Secondary proboscis nerves	N/A
54. Proboscis armature	Absent	0
55. Number of accessory stylet pouches	N/A	N/A
56. Number of stylets in each accessory stylet pouch	N/A	N/A
57. Stylet basis/stylet ratio	N/A	N/A
58. Stylet shaft	N/A	N/A
59. Shape of stylet basis	N/A	N/A
60. Median waist of stylet basis	N/A	N/A
61. Proboscis used for locomotion	Unknown	0
Alimentary system
62. Position of mouth	Just behind the brain	2
63. Oesophagus	Absent	0
64. Oesophagus epithelium	N/A	N/A
65. Stomach	Not regionally differentiated	0
66. Stomach connection with intestine	N/A	N/A
67. Length of pyloric canal	N/A	N/A
68. Intestinal caecum	Absent	0
69. Anterior pouches of intestinal caecum	N/A	N/A
70. Lateral diverticula of intestinal caecum	N/A	N/A
71. Intestinal diverticula	Absent	0
Circulatory system
72. Cephalic vasculature	Forming a blood lacuna in front of cerebral ganglion	3	3A, B
73. Vascular plugs	N/A	N/A
74. Rhynchocoelic villus	Absent	0
75. Position of lateral blood vessels	Outside inner circular body wall muscle layer	2	4F, G, 5G
76. Mid-dorsal blood vessel	Absent	0
77. Length of mid-dorsal blood vessels	N/A	N/A
78. Extravascular pouches/valves	Absent	0
79. Pseudometameric transverse connectives linking mid-dorsal and lateral blood vessels in intestinal region	N/A	N/A
80. Vascular plexus in foregut region	Absent	0
Nervous system
81. Location of cerebral ganglia and lateral nerve cords	Cerebral ganglia and lateral nerve cords situated between epidermal basement membrane and outer circular body wall muscle layer	1	3C, F, 5A, B, C, D
82. Number of dorsal cerebral commissures	One	1
83. Distinct outer neurilemma of cerebral ganglion	Absent	0
84. Inner neurilemma of cerebral ganglion	Present	1	5A
85. Statocysts in brain tissue	Absent	0
86. Lateral nerve cords	N/A	N/A
87. Accessory lateral nerve	N/A	N/A
88. Four large nerves in head region	Absent	0
89. Number of dorsal nerves	Both upper and lower dorsal nerves	2
90. Posterior junction of lateral nerve cords	Not observed	–
91. Neurochord cell in brain	Absent	0
92. Neurochords in lateral nerve cords	Present	1	5B
93. Myofibrillae in lateral nerve cords	Absent	0
94. Position of myofibrillae in lateral nerve cords	N/A	N/A
95. Buccal nerves	Paired	1	3G
Excretory system
96. Excretory system	Present	1	4F, G
97. Extent of system	Confined to foregut region of body	0
98. Excretory canal	Canal outside inner circular muscle	1	4F
99. Nephridial gland	Present	1
100. Flame cells	N/A	N/A
101. Glandular components in excretory tubules	Present	1
102. Number of nephridiopores	Limited to one or two on each side of body	0	4G
103. Position of nephridiopores	Region of excretory system	2	4G
Reproductive system
104. Nature of sexes	Separate sexes	0	5F, G
105. Gonad arrangement in heterogamous taxa	In lateral rows/groups diverticula absent	3	5F, G
106. Gonad arrangement in hermaphroditic taxa	N/A	N/A
107. Testes	Simple	0	5F
108. Sexual colour dimorphism	Absent	0
109. Gonoduct position	Not observed	–
110. Nature of reproduction	Not observed	–
Sensory organs
111. Apical organ	Absent	0
112. Typical cephalic gland	Absent	0
113. Cephalic gland type	N/A	N/A
114. Opening of cephalic glands	N/A	N/A
115. Position of cerebral sensory organs in relation to brain	Behind brain	4
116. Position of cerebral sensory organs in relation to epidermis	Ciliated pits or ciliated canals in epidermis	0	5E
117. Size of cerebral sensory organs	Less than half size of brain lobes	0	5E
118. Ciliated cerebral canal	N/A	N/A
119. Side organs	Absent	0
120. Sensory pits in head region	Absent	0

Notes: N/A, no applicable character.