Kukumia solomonensis, Gibson & Sundberg, 2002

Gibson, Ray & Sundberg, Per, 2002, Some heteronemerteans (Nemertea) from the Solomon Islands, Journal of Natural History 36 (15), pp. 1785-1804 : 1792-1803

Kukumia solomonensis sp. nov.

(gures 4–26)

Type specimen

HOLOTYPE, MTQ G20020, series of transverse sections through anterior body and various mid-body regions, 66 slides. The 18S rDNA gene sequence of the holotype is deposited with Genbank (accession number AY039665 ).

Type locality

Intertidal, under a small boulder in the upper littoral, just outside the Fisheries Research Laboratory, Kukum area just west of Honiara, Guadalcanal, Solomon Islands .

External features

Single specimen about 15 cm long, 4 mm maximum width. In life, head long, pointed, distinctly narrower than remainder of body; posterior end of head more attened (gure 4). Neither eyes nor cephalic furrows distinguished in life, but in sections shallow, gaping horizontal lateral cephalic furrows very obvious. Brain lobes visible through dorsal body surface as dark, reddish patches, at rear of head. Body pale cream-brown, with no markings, intestinal region a darker brownish tinge. Lateral nerve cords visible as ne reddish lines extending along each side of body. Specimen coiled when disturbed.

Body wall, musculature and parenchyma

Epidermis (gures 5, 6) mostly comparatively thin (15–30 m m), after preservation distinctly wrinkled or corrugated, possibly a consequence of contraction; internally lined by distinct connective tissue basal membrane. Thin outer circular (about 5 m m maximum width) and inner longitudinal subepidermal muscle layers run immediately below epidermal basement membrane. Longitudinal muscles of bre bundles, about three to four times as thick as circular layer, i.e. up to about 20 m m. Within dermis glandular and connective tissue regions recognisable, but mainly intermingled with bundles of longitudinal muscle bres derived from outermost portion of main body wall outer longitudinal musculature. Dermal glands mostly small, irregular in shape and exhibit no particular staining aYnities (gure 5), although many contain dark, granular cytoplasm (gure 6) throughout much of intestinal region. In foregut region of body dermal connective tissues arranged into 5–10 concentric layers, separated by bundles of longitudinal muscle bres (gures 5, 7); further back number of layers reduced (gure 6). Glandular and connective tissue dermal components in anterior body regions together extend some 200–250 m m below subepidermal muscle layers, less than this in posterior parts of body.

Body wall musculature comprises typical heteronemertean arrangement, outer longitudinal, middle circular and inner longitudinal layers, respectively, about 380– 400 m m, 170–200 m m and 55–60 m m maximum thickness in anterior body regions. Outer longitudinal muscle layer composed of large bre bundles penetrated more or less regularly by radial connective tissue and muscle bre strands (gure 8) extending from body wall circular muscle layer to subepidermal musculature. Inner margin of outer longitudinal muscle layer abuts against thick peripheral neural sheath (12–15 m m maximum) bearing distinct upper mid-dorsal nerve which is up to 30 m m diameter (gure 9). In anterior body regions there is also lower dorsal nerve situated internal to body wall circular muscle layer (gure 9); occurrence of upper and lower dorsal nerves well known for some palaeonemertean genera, such as Tubulanus ( Sundberg and Hylbom, 1994) , is an unusual feature in heteronemerteans.

On either side of body lateral nerve cords possess both outer and inner neurilemma. Outer ganglionic zone of lateral nerve cords penetrated by radial connective tissue and muscle brils which cross outer longitudinal muscle layer (gure 10). Five or six small bundles of longitudinal muscle bres run adjacent to inner neurilemma on outer margin of neuropil (gure 10), but there are no neurochords.

In foregut region of body a horizontal, longitudinal muscle plate, in places up to 30 m m or more thick, is situated between rhynchocoel and gut walls. Medially, below rhynchocoel, bres of this muscle plate are interwoven with outermost circular muscles of rhynchocoel wall (gure 11), but this arrangement diVers from that described for some heteronemertean genera where lateral parts of circular musculature are interwoven with adjacent body wall longitudinal muscle bres.

Bulk of cephalic region consists of large numbers of bundles of longitudinal muscle bres scattered between parenchyma and cephalic nerves; we could nd no evidence of cephalic or submuscular glands.

Proboscis apparatus

Rhynchodaeum thin-walled, spacious, its epithelium underlain by thin layers of longitudinal and circular muscle bres, each only one or two bres thick but quite distinct from remaining muscle bres of head. Rhynchocoel musculature consists of separate outer circular and inner longitudinal layers, outer circular bres not interwoven with adjacent body wall inner longitudinal muscles. In foregut region longitudinal muscle layer 5–45 m m thick, circular layer 5–140 m m, but both extremely variable. In general, rhynchocoel wall muscle layers thinnest mid-dorsally, thickest ventrolaterally. Posteriorly both rhynchocoel wall muscle layers much thicker (gure 14). Relative length of rhynchocoel not determined but it does not extend to posterior tip of body.

Extreme anterior end of proboscis, leading from proboscis insertion, contains three muscle layers, arranged as inner and outer longitudinal zones of similar thickness (15–75 m m), divided by thin but distinct middle circular muscle layer and neural sheath which, on each side, is enlarged to form distinct nerves (gures 12, 13). Circular muscle layer at most only about 2–3 m m across. Inner and outer epithelia of this proboscis region thin but distinct.

Proboscis comparatively small relative to overall size of animal. In retracted position it has overall diameter of about 500 m m, i.e. about 13% of body diameter in foregut region. For most of its length it possesses thick, folded epithelium, 30 m m or more thick, containing large numbers of acidophilic and basophilic glands, distal wall of epithelium housing large numbers of rhabditoid pads. Pads in many places about 15–20 m m in diameter, individual barbs being regularly 4–5 m m tall and uniformly rod-like in appearance. Beneath epithelium distinct connective tissue layer, in places more than 15 m m deep, extends distally to form cores of epithelial folds (gure 15). Beneath connective tissue layer proboscis neural sheath is irregularly thickened to form obvious nerves. Proboscis contains two muscle layers, outer circular (15–20 m m maximum thickness) and inner longitudinal (up to about 60 m m thick, but in most parts much less than this), with two muscle crosses. Innermost lining thin but distinct. Proboscis has somewhat asymmetrical construction, especially with regard to distribution of its gland cells and distal barbs, and its outer circular muscle layer in several places appears divided into inner and outer layers by additional peripheral neural sheath.

Alimentary canal

Large and obvious mouth leads to buccal cavity which bulges forwards below rear of brain.

Foregut well developed. Beneath its densely ciliated epithelium, up to about 30 m m thick, subepithelial gland cell zone dominated by nely granular and irregularly shaped acidophilic glands which appear to be of composite type (gure 16); irregular in shape, many possessing secretory tracts leading towards epithelial surface. Epithelium and its underlying glandular zone not as distinctly separated as in many heteronemertean taxa which have similar foregut arrangement, though in a few places traces of an epithelial basement structure evident. Foregut epithelium and subepithelial gland cell zone together up to about 125 m m in maximum thickness. No obvious somatic muscles associated with foregut.

Intestinal wall extremely variable in height, typically ranging from 15 to 150 m m or more depending upon local folding. Lateral diverticula deep and branched.

Blood system

Single median blood vessel forms compressed ‘saddle’ in head over dorsal surface of rhynchodaeum. Vessel divides close to rear of rhynchodaeum to form pair of bilaterally compressed channels which enter cerebral ring. Above ventral commissure, behind origin of proboscis nerve supply, the two blood vessels meet medially below rhynchocoel to form U-shaped compressed channel. Towards rear of ventral commissure, mid-dorsal vessel branches oV to enter rhynchocoel oor and form origin of rhynchocoelic villus (gure 17). U-shaped channel expands behind this point and then separates to form three vessels, one on either side of rhynchocoel adjacent to inner margins of dorsal brain lobes, and one mid-ventrally below mid-dorsal blood vessel and separated from it by transverse horizontal muscle bres (gure 18). Spacious blood channel on either side of head also leads forwards alongside and bathing cerebral sensory organs (gure 19). Outer and inner lateral vessels meet posteriorly above rear of each dorsal brain lobe. Median ventral vessel expands behind ventral commissure, continues back over anterior bulge of buccal chamber and then branches to form origin of foregut vascular plexus. The two lateral vessels on each side of rhynchocoel fuse behind rear of cerebral organs to form single spacious lacuna, separated from rest of foregut vascular plexus by transverse and horizontal muscle bres. Spacious dorsolateral vessel farther back on each side of rhynchocoel communicate with vessels of foregut vascular plexus irregularly. Around foregut vascular blood plexus consists of about 14–16 interconnected longitudinal channels mostly separated by radial muscle and connective tissue brils (gure 16).

Rhynchocoelic villus (gures 11, 20) extends posteriorly to end of foregut region before emerging to continue posteriorly below rhynchocoel wall.

Blood vessels in intestinal region possess thick, distinct walls (gure 21), lateral vessels in particular following tortuous route so that in places there appear to be several vessels running close together (gure 22). Pseudometameric transverse connectives link mid-dorsal and lateral vessels in intestinal region. In many parts of blood system discoid and mononucleate acidophilic blood cells, about 6– 7 m m diameter, appear locally aggregated.

Nervous system

Brain lobes enclosed by distinct outer neurilemma, their brous and ganglionic regions separated by equally distinct inner equivalent (gures 17, 18). Dorsal cerebral bre cores extend farther forwards than ventral, anterior bre cores of ventral ganglionic lobes only appearing towards rear of ventral cerebral commissure. Dorsal and ventral cerebral commissures lie in more or less same plane. Dorsal cerebral ganglia anteriorly unbranched but divide posteriorly into upper and lower forks. Upper branch of each dorsal brain lobe ends blindly, but ventral lobe extends laterally outwards to enter cerebral sensory organs. Lateral nerve cords originate from ventral lobes by moving directly outwards before bending to run posteriorly (gures 17, 18).

Each lateral nerve cord with ve or six small bundles of longitudinal muscle bres running adjacent to inner neurilemma on outer margin of neuropil (gure 10). Number of myo brillae appears greater than recorded for other heteronemerteans. In anterior regions of body both upper and lower mid-dorsal nerves are distinguishable, upper nerve running on peripheral neural sheath of body wall, lower nerve immediately below circular muscle layer (gure 9). Posterior limit of lower dorsal nerve not traced. Origin of proboscis nerves is a thick nerve root emerging from upper surface on each side at front of ventral commissure.

Frontal organ and cephalic glands

The presence or absence of frontal (apical) organ was not determined, because extreme tip of head lost during sectioning. There were, however, no typical lightly basophilic frontal glands, as found in many species of nemerteans.

Sense organs

Species does not possess eyes.

Though not visible in life, in histological sections the single pair of lateral horizontal cephalic furrows very evident, forming wide lateral bays on either side of head (gure 23). Furrows especially spacious and deep close to anterior brain region. Towards rear of brain, where dorsal and ventral lobes separate, lateral cephalic furrows close oV externally (gure 24) before leading at their rear to ciliated cerebral canals. Cerebral sensory organs lie tight against outer margin of dorsal brain lobes (gures 17, 18), ventral lobes extending outwards immediately below them. In anterior part of each cerebral organ ventral third composed of glandular structures, remaining tissues being neural with large ciliated canal lying about medial in position (gure 25). Posterior half of each cerebral sensory organ bathed by large dorsolateral blood lacuna located alongside rhynchocoel (gure 19). Cerebral organs extend back beyond rear of ventral brain lobes, their cerebral canals ending close to their posterior limit in vacuolate glandular pouch.

Excretory system

Excretory system located in posterior foregut regions and consists of up to three or four tubules each side of body, situated dorsolaterally to gut (gure 26). Tubules in many places penetrate branches of foregut vascular plexus.

Reproductive system

No observations possible on sexual state of species; none of sections examined contains any evidence of gonads.

Phylogenetic analysis

The phylogenetic analysis based on the 18S rDNA gene resulted in one most parsimonious tree (gure 27A) with length 1250 and consistency index of CI 50.81. Kukumia solomonensis gen. et sp. nov. is in a sister-group position to the three lineid species included in the analysis. Lineus is not monophyletic according to this analysis, a conclusion supported by the analysis in Sundberg and Saur (1998). The mean genetic distances between included species vary between 0.03 and 0.05 within the Lineus / Micrura clade and up to 0.40 between ingroup and outgroup species ( table 1).

Systematic discussion

The phylogeny indicates that the new species belongs in the same clade as the lineid species but this position is not strongly supported by the molecular data alone, as evident from the bootstrap analysis (gure 27B). However, the possession of an unbranched proboscis containing outer circular and inner longitudinal muscle layers is additional support for placing this species in the heteronemertean family Lineidae sensu Gibson (1985a) .

The taxon Lineidae contains at present 27 genera ( table 2) which can largely be distinguished from each other on the basis of diVerences in the state of eight anatomical characters ( table 2). The Solomon Islands nemertean possesses two muscle crosses in its proboscis wall, a foregut with a subepithelial gland cell layer but no obvious somatic musculature, a blood system in the foregut region developed into a vascular plexus, and neither a caudal cirrus nor neurochord cells in its nervous system. Each of these character states is known to occur in at least one, usually several, of the existing lineid genera, although for several of them data on these characteristics are incomplete. Kukumia solomonensis gen. et sp. nov. can be excluded by its character states from the genera Eousia , Flaminga , Hinumanemertes , Micrella , Zygeupolia and some species of Micrura , all of which possess a caudal cirrus; from Apatronemertes , Australineus , Flaminga , Hinumanemertes , Kirsteueria , Micrella , Micrellides , Micrura , Paralineus , Paramicrurinella , Pontolineus and possibly Lineopsella , Micrurimorpha , Micrurinella , Pussylineus and Siolineus , none of which have a subepithelial gland cell zone associated with their foregut; from Corsoua , Craticulineus , Flaminga , Paralineus , Paramicrurinella , Pontolineus and some species of Lineus , in which the foregut blood supply consists of a single pair of vessels rather than a vascular plexus; and from Antarctolineus , Apatronemertes , Eousia , Flaminga , Hinumanemertes , Kirsteueria , Lineopsella , Lineopselloides , Micrella , Micrellides , Micrurimorpha , Micrurinella , Neolineus , Paralineus , Paramicrurinella , Planolineus , Pontolineus , Pussylineus , Siolineus , Utolineus , Zygeupolia and some species of Lineus and Micrura , none of which possess a connective tissue layer between their dermal gland cells and outer body wall longitudinal muscle layer.

There are three features of Kukumia solomonensis gen. et sp. nov. not reported for any other heteronemertean genus. These are the ways in which the dermal connective tissues in the anterior body region are formed into concentric circumferential layers interwoven with muscle bundles derived from the distal portion of the body wall outer longitudinal muscle layer, the manner whereby the rhynchocoel wall circular muscle bres are ventrally interwoven with longitudinal bundles of the horizontal muscle plate running between the gut and rhynchocoel, and the presence of upper and lower mid-dorsal nerves in the foregut region of the body. These anatomical features are interpreted as synapomorphies which enable the taxon Kukumia gen. nov. to be identi ed as monophyletic, of which only the species Kukumia solomonensis sp. nov. so far is known.