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Antarctic Convergence illustration Antarctic convergence

Adenorhagas aurantiafrons Riser, 1990  Species

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“Adenorhagas aurantiafrons n.g., sp.n.

Description.

EXTERNAL FEATURES. The largest specimen was female, 24 mm long by 1.1 mm diameter fully extended while gliding. Anterior and posterior ends of living individuals are bluntly rounded, and the body is round with a uniform diameter. Upon preservation, some specimens contracted so that the anterior quarter to a half formed an inflated, elongated cone. Several individuals fragmented, even though apparently well-anaesthetised. Basic body color of small individuals was chalky-white with a bright orange cap at the tip of the head. An orange stripe continued down the dorsum of most specimens > 10 mm long, and the entire dorsum of individuals > 18 mm long was a dirty orange colour except for the bright orange cap. A minute, papilla-like caudal cirrus is present. The lateral cephalic furrows are short, shallow, and difficult to see, reaching to the level of the minute pore-like mouth. Eyes are absent.

BODY WALL. The epidermis is of rather uniform thickness throughout the body. It is dominated by densely packed (Fig. 6, 7) goblet cells 26-32 μm tall containing an homogeneous, strongly azanophilous secretion. Cyanophilous (mucous) goblet cells are widely scattered in the epidermis (surficial sections indicate a ratio of about 1:100 azanophilous cells), and the necks of subepidermal glands are present. Gland cells are rare in the epidermis of the caudal cirrus (Fig. 5). The epidermis rests on a relatively thick basement membrane, at least half as thick as the subepidermal muscle layers, of which the circular layer is very thin. This muscle layer appears to give rise via radial fibres to the horizontal muscle bar between the anterior end of the cephalic blood lacuna and the bases of the apical sensory organs. The subepidermal longitudinal muscle layer is one to two bundles thick, depending upon contraction or expansion of the body wall. Each bundle contains three to six fibres and is surrounded by a thin membrane. The cell bodies of the subepidermal glands are packed together immediately beneath these bundles.

A small number of homoserous gland cells are present in the subepidermal gland layer, which is dominated by mucous and basophilic bacillary glands and not separated from the outer longitudinal muscle layer (OLM) by a connective tissue layer. Cell bodies of the mucous glands are packed against the OLM. The cell bodies of a few of the bacillary glands abut the OLM, but the majority occur in the outer half of the gland layer. Subepidermal mucous glands are absent around the mouth. Mucous glands dominate in the pre-cerebral region where two groupings occur, i.e., frontal glands, which are not abundant, and the more peripheral subepidermals, which discharge through the epidermis, especially near to but outside the cephalic furrows.

The postoral OLM is more than twice as thick as the inner circular muscle layer (ICM), and is separated from it by a thin layer of connective tissue which is thickest over the lateral nerve cords. The ICM extends as a ring from the posterior end of the body almost to the anterior end of the cephalic blood lacuna but is somewhat disorganised between that point and the horizontal muscle bar. It is thicker than the internal longitudinal layer (ILM). Both of these layers are disrupted at the mouth, at the proboscis diaphragm (by the passage of the OLM fibres into the proboscis), and at the entrance of the cerebral canals into the cerebral organs. The OLM and ILM do not unite at the mouth to pass around it as a composite muscle. The ILM splits around the

buccal cavity but does not extend ventrally beneath the esophageal nerves and as a result, is absent between the ICM ring and the ventral wall of the initial portion of the esophagus. The ventral arms of the ILM do not meet around the esophagus until shortly before the esophageal nerves become indistinct. A few fibres from the ICM become isolated beneath the esophageal epithelium but this situation does not occur posteriorly where the ILM forms a continuous layer. The ILM and rhynchocoelic LM unite at the proboscideal sphincter and continue as a thin layer in the outer walls of the cephalic blood lacuna and beyond the lacuna to the anterior tip of the body. It is not strongly developed as a compact muscle in the wall of the lacuna. Radial muscle fibres are present throughout the body and pass through the subepidermal gland layer and OLM to insert in the ICM or through it to the tunica propria of the gut. Some ventro-lateral radial fibres branch to form isolated circular fibres beneath the epithelium of the esophagus ventrally. In the pre-cerebral region, radial fibres pass through the ICM and ILM, to form the rhynchodaeal/rhynchocoel circular muscle layer (Fig. 2) and divide the blood lacuna into three channels. Dorsoventral muscles are present in the intestinal region of the body between the caeca. No muscles are present between the esophagus and rhynchocoel, and with the exception of the previously mentioned branches of the radial fibres which produce short strands of circular fibres beneath the esophagus, there are no muscle layers associated with that portion of the foregut.

Parenchyme is present around the gonads but otherwise is evident only around the rhynchocoel.

PROBOSCIS APPARATUS. The ciliated proboscideal furrow extends almost to the apex of the head, but its characteristic epithelium continues forward to the tip as a band on the ventral surface. Goblet cells and the necks of subepidermal glands are absent from the epithelium of the band, furrow, and rhynchodaeum, and the rhynchodaeal cells arc unciliated. The basement membrane is exceedingly thin so that the longitudinal muscle bundles accompanying the furrow seem almost to be in contact with the epithelium. A thick nerve plexus, which is broken dorsally and incomplete ventrally, lies outside of these muscle bundles behind the rhynchodaeal pore. The dorsal expansion of the rhynchodaeum is in contact with the ventral wall of the cephalic blood lacuna. A small dorsolateral bundle of longitudinal fibres is trapped between the ventral wall of the lacuna and the rhynchodaeum on each side. The ventral expansion of the lacuna is blocked by bundles of longitudinal muscle fibres along the lateral walls of the rhynchodaeum (Fig. 2). These "rhynchodaeal" muscles are a thickened part of the ILM which is continued dorsally as a thin layer enclosing the outer wall of the lacuna. The two lateral bundles do not meet in the mid-ventral line. A few radial fibres pass through this point of communication to form a sparse rhynchodaeal circular muscle layer beneath the epithelium. Fibres from the inner side of the OLM bend mediad at the proboscideal diaphragm immediately in front of the dorsal brain commissure and form the longitudinal muscle layers of the proboscis. These fibres enter primarily through the dorsal and ventral gaps in the nerve plexus around the rhynchodaeum, although a few fibres also pass through the lateral walls of the plexus. The two lateral proboscideal nerves enter ventro-laterally at the diaphragm, initially between the epithelium and the longitudinal muscles, but shortly come to lie within the longitudinal layer. As the neural plexus forms between the two proboscideal nerves, small blocks of longitudinal fibres, isolated between the nerves and the epithelium, expand to form the outer longitudinal muscle layer of the proboscis. Circular muscles adjoin the plexus forming a loop with fibres passing through the inner longitudinal muscles as a single muscle cross to encircle the proboscis as a layer one fibre thick, beneath the endothelium. The circular muscles adjacent to the plexus thicken and throughout the major portion of the proboscis appear to be bipartite, i.e., a layer of concentric fibres against the plexus separated by a thin layer of parenchymatous connective tissue from the fibres participating in the loop.

The epithelium of the proboscis initially consists of simple columnar cells. Slightly behind the initial muscle cross, the epithelium becomes glandular, but retains a uniform height. Cells producing the rhabditoids (nematocysts of Hubrecht 1887; acidophilic rods of Jennings & Gibson 1969; cytoplasmic masses of Iwata 1970; rhabdites of Gontcharoff 1957; Ling 1971; Gibson 1981) occur on the side opposite the muscle cross and thus the rhabditoid packets at first are present in only one side of the lumen (Fig. 9). The epithelial spines (Fig. 10) appear at the same time. Their relationship to the cells on the rhabditoid side is unclear, but on the opposite side, they form a dense rake-like denticulated surface. The spines (Iwata 1967,1970; Anadon 1971, 1976, referred to them as stylets, but this term, usually applied to a totally different enoplan proboscis organelle, is not applicable to the insoluble hollow thorn-like structures of the heteronemertine proboscis), vary in length up to 38 μm in length. Our TEM observations show that the "accessory rods" recorded by Ling (1971) enclosing the flagellum of his putative "sensory" cells are the walls of the spines. In the main body of the inverted proboscis, three or four longitudinal ridges covered with glandular cells are apparent in cross sections, but may be fixation artifacts resulting from contraction of the circular muscle fibres. Cells producing rhabditoids are uniformly distributed in the epithelium of the main body of the proboscis. The rhabditoids are neatly bundled into packets with the long axes directed toward the lumen of the proboscis. The distal surface of each packet is round, and the packets appear as rectangles when viewed from the side. Extruded rhabditoids range from less than 3 μm to almost 10 μm in length. In the main body of the proboscis, they are mostly in the 9-10 μm range in the large packets which dominate in this region.

The proboscis is attached to the wall of the rhynchocoel in the region of the first appearance of gonads.

The rhynchocoel extends to the posterior end of the body. Its walls are very thin and the two muscle layers do not intermingle. The weak development of the muscles and the absence of supporting tissue between the rhynchocoel and foregut allow for two artifacts in the esophageal region; if the proboscis is ejected, the rhynchocoel can inflate to occupy most of the diameter of the body, and if the proboscis is forced forward on fixation, the rhynchocoel usually takes on a figure-8 shape as if there were a ventral diverticulum. The circular muscle layer of the dorsal wall of the rhynchocoel is in intimate contact with the ILM in the foregut region of the body but there is no intermingling of fibres.

The wall of the rhynchocoel beneath the epithelium, initially consists of connective tissue. A short distance behind the diaphragm, a single row of longitudinal muscle fibres is present dorsally in the connective tissue. Near the ventral brain commissure, additional longitudinal fibres are present in the lateral walls. The ring of longitudinal fibres is completed behind the origin of the rhynchocoelic villus. Transverse muscle fibres between the dorsal ganglia and lateral nerve cords pass between the rhynchocoelic epithelium and the ILM with branches (or extensions) spreading beneath the epithelium to augment the rhynchocoelic CM. Fibres from the ICM above the buccal cavity form a broad attachment to the rhynchocoel further enhancing the circular muscle layer.

ALIMENTARY CANAL. The small, pore-like mouth (Fig. 7, 8) opens on the ventral surface a short distance behind the brain. The epithelium of the mouth is non-glandular and the underlying basement membrane is not apparent at the light microscope level of observation. The oral epithelium extends inwards a short distance and meets the epithelium of the buccal cavity without intergradation. The epithelium of the buccal cavity and esophagus is dominated by acidophilic and basophilic gland cells, some of which expand beneath the epithelium but do not form a subepithelial gland layer. The epithelium of the buccal cavity contains a higher proportion of mucous cells than does that of the esophagus. Nuclei of the ciliated "support" cells lie near the distal ends of those cells. The division of the foregut into two regions is arbitrary and based upon the presence of the subepidermal circular muscles which allow for the eversion of the walls of the buccal cavity through the mouth. Sections show a slight admixture of foregut and intestinal cells at the juncture of those two regions. The intestine almost immediately expands laterally to form the first pair of diverticulations. Very few of the intestinal cells beneath the dorsal blood vessel contain digestive granules.

BLOOD VASCULAR SYSTEM. The dorsal and two ventro‑lateral (intestinal) blood vessels anastomose in a sinusoidal mesh around the posterior end of the intestine. Toward the anterior end of the intestine, a connective tissue wall is distinctly visible around the dorsal vessel; however, the dorsal CT disappears near the juncture of the intestine and foregut and the endothelium bulges into the rhynchocoel as the rhynchocoelic villus. The two intestinal vessels dissolve in the same region producing a sinusoidal mesh around the foregut. This mesh becomes dorsal around the buccal cavity expanding to form two lacunae near the anterior end of the cavity to either side of the rhynchocoel. Connective tissue and dorso-ventral muscles to the rhynchocoel separate the two lacunae ventrally, and strands of connective tissue passing between the fibres of the dorsal band of ILM to the wall of the rhynchocoel attach these two together and restrict communication between the lateral lacunae. Transverse muscle fibres passing between the lateral nerve cords and the cerebral organs divide the lacunae into four chambers. The dorsal blood vessel exits the rhynchocoel and the ventral suspensor of the rhynchocoel ceases to continue forward, and thus, a single lacuna exists ventrally. The cerebral organs fill the lateral lacunae which meet over the rhynchocoel forming a single horseshoe-shaped space. Near the ventral cerebral commissure, the lacunae unite to form a ring around the rhynchocoel. The lacuna is broken up into a number of small spaces at the proboscideal diaphragm. The vascular tissue forms an arch around the rhynchodaeum which is attached to the adjacent tissues ventrally. A distinct lumen was not apparent in this portion of the vascular system of any of the specimens which were examined; however, the cavity was present in the prerhynchodeal lacuna at the anterior end of the system. (The sinusoidal appearance of parts of the vascular system may be an artifact resulting from the collapse of lacunar walls; however, in the genus Micrura, comparable parts of the system have a similar appearance.)

EXCRETORY SYSTEM. Excretory tubules are absent, and no organelles which could be interpreted as excretory in function could be found.

NERVOUS SYSTEM. The pre-rhynchodaeal tissue contains much material which stains as if of a neural nature but distinct nerve tracts are not evident. The neural tissue condenses around the rhynchodaeum as a plexus of anastamosing longitudinal tracts (Fig. 1). The two sides of the plexus are of equal thickness (Fig. 2), but dorsally and ventrally only occasional strands are present.

The dorsal and ventral cerebral lobes are united anteriorly, and the lobes of each side are connected by commissures; the ventral commissure is about three times as thick as the dorsal. The longitudinal tracts from the rhynchodaeal/rhynchocoel plexus extend along the medial sides of the cerebral ring, the majority eventually disappear in a dorso-medial lobe of the ventral ganglion. A thin connective tissue sheath encloses the cerebral neuropil and demarcates the lobes of the ganglia. A proboscideal nerve arises from the anterior end of each ventral ganglion. The dorsal ganglia are bifurcated posteriorly (Fig. 4). A thin commissure links the two lateral nerve cords anterior to the buccal cavity and gives rise to two esophageal nerves which extend around the buccal cavity and ventro-laterally beneath the anterior one-fifth of the esophagus. The lateral nerve cords are united by a continuous plexus in the connective tissue between the CM and ILM behind the mouth. A dorsal nerve is not evident in the plexus. Neurochord cells are absent.

SENSORY SYSTEM. A small quadripartite group of frontal gland cells discharge amongst the three apical sensory organs. The frontal glands arise slightly anterior to the rhynchodaeal pore but far enough in front to not be confused with the anterior end of the cephalic blood lacuna.

The epithelium of the cephalic fissures is densely ciliated and sharply demarcated (Fig. 6) from the epithelium of the body surface. It contains mucous and pale azanophilous flask cells, and the necks of a few small basophilic subepidermal gland cells which are not arranged in packets. The basement membrane beneath the floor of the fissure is thick. Sensory cells in the epithelium were not evident anterior to the brain. The opening of the cerebral organs is at the tip of a glandular papilla toward the posterior end of each fissure and the fissures are flask shaped posteriorly, i.e., with a broad floor. The epithelium of the papilla consists primarily of large azanophilous flask cells and a few mucous flask cells (Fig. 3), both similar to those of the body epidermis. The epithelium of the floor around the papilla consists almost entirely of sensory cells, the nuclei of which form a compact ring beneath the epithelial layer (Fig. 3).

The cerebral organs are massive. The canal enters through the papilla and the epithelium is dominated by sensory cells. The canal turns posteriad and then ventrad. The secretory glands occur dorsally and ventrally and are not divided into anterior or posterior fields. They discharge into the canal near the initial flexure. The cell bodies of the vesicular glands are associated with the terminus of the canal and occupy the entire posterior end of each organ (Fig. 9). The cerebral organ nerve branches at the initial flexure of the canal, one branch passing into the ventral neuronal mass and one into the dorsal mass, while a main branch accompanies the canal almost to its posterior end. The dorsal and ventral branches subdivide to ramify through the neuronal masses. The cerebral organs are encased in a well-developed connective tissue tunic. The organs are fused with the large ventral lobe of the dorsal ganglia. The dorsal lobe (Fig. 4) forms a hood over the anterior ends of the organs, separated from them by the connective tissue sheath. The organs project into the cephalic blood lacunae which, in the absence of a dorsal septum, are not restricted symmetrically to one side or the other.

REPRODUCTIVE ORGANS. Two of the specimens contained gonads. Both were female and the oocytes were not undergoing vitellogenesis nor were any evidences of ducts present. The number of oocytes developing in each gonad was small.

Type data. Holotype. AMNH 307 serial cross section, 12 slides. Paratype. AMNH 308, serial longitudinal section, 2 slides; USNM 131997, serial cross section, 13 slides

Other material. Seventeen living specimens from type locale and source; one specimen from holdfast of Ecklonia radiata washed up on Goat Island Beach, Leigh, N.Z., March 1986. Longitudinal serial sections of one specimen and serial transverse sections of seven others were utilised in this study.

Etymology. Gr.; adeno, gland; rhagas, fissure.

Type locality. Kaikoura, New Zealand, from holdfast of Lessonia variegata, 6 March 1986.

Remarks. Gibson (1981) produced a table based upon the morphological characters which Friedrich (1960) had advocated for generic diagnosis in the Heteronemertinea. In 1985, Gibson furnished a table, with additional characters in which he distinguished groups based upon the arrangement of the muscles layers in the proboscis. This table pointed out critical problems not only in generic diagnoses, but also in any efforts in phylogenetic systematics. Most heteronemertine species have been placed in the genera Cerebratulus, Lineus, and Micrura. The majority of the descriptions of species assigned to these genera are incomplete or inadequate, and as Table 2 of Gibson (1985) clearly shows, these genera are not self-contained groups of species, e.g., autapomorphies are not evident. Phylogenetic relationships within each of the groups of genera remains to be analysed. Taxonomists have long recognised that a genus is what the authority determines it to be, and, in establishing a phylogenetic system, supraspecific taxa are

"arbitrary labels" (Ax 1987: 237). The proliferation of monotypic genera diagnoses in the Heteronemertinea as the result of more complete descriptions will facilitate rather than handicap phylogenetic analyses.

The occurence of secretory cells in the epithelium of the cephalic fissures of Adenorhagas aurantiafrons to which the generic name refers, is unusual but not restricted to the genus. They increase in abundance posteriorly until the sensory cells become dominant in the epithelium.

There is no separation into OLM and subepidermal LM in the absence of subepidermal glands around the mouth. Among heteronemertines, compression of the oral epithelium between the epithelium of the buccal cavity and body epidermis as the result of contraction, usually inhibits observation of this feature. Densely arranged glands are responsible for the arbitrary (but useful in descriptions) division of what really is one muscle layer into two. Stiasny-Wijnhoff (1942) referred to the subepidermal glands of Micrurina occuring between the bands of OLM which extended between the subepidermal CM and the ICM. She stated that a subepithelial LM was absent. In areas where the subepidermal glands of Lineus bicolor Verrill, 1892 are packed together, I have observed that longitudinal muscle bundles of about equal size occur either subepidermally or between the bases of the glands and the ICM, and where the glands are less numerous (or densely packed) a single layer (one bundle thick) occupies this space. An examination of lineid heteronemertines at my disposal indicates that the ILM also blends into the longitudinal muscle organisation around the mouth, except in those species in which the subepidermal buccal glands press against (Cerebratulus bicornis, Joubin & Francois, 1892) or pass through (Micrura alaskensis, Coe, 1901) the ICM below the buccal nerves. In Adenorhagas aurantiafrons the ILM is blocked by the esophageal nerves from combining with the other longitudinal muscles. The combination of subepidermal LM, ILM, and OLM around the mouth is distinct in Micrura fasciolata, Ehrenberg, 1831 (= M. affinis Gerard, Stimpson, 1853) from Massachusetts Bay. This may account for the diagram by Cantell (1975, fig. 1A) who worked with this species, being more accurate than that of Stiasny-Wijnhoff (1923, fig. 6) which unfortunately has been accepted as portraying the actual relationships of heteronemertine muscles.

Contraction of the precerebral region of heteronemertines during fixation results in a button-hooking of the longitudinal muscles at the proboscis diaphragm. In well-anesthetised specimens, the common origin of the rhynchocoelic and internal longitudinal muscles is clearly apparent, as is the origin of the proboscideal longitudinal muscles from the outer longitudinal layer of the body wall in common with all other nemertines.

The small papilliform caudal cirrus of A. aurantiafrons is not readily seen on preserved specimens. It is a distinct postanal structure (Fig. 5) but could easily be overlooked. It is possible that other heteronemertine species also have papilliform caudal cirri that have not been recorded.

Dewoletzky (1887) concluded that certain nuclei beneath the epithelium of the cephalic fissures belonged to ganglion cells and that their connection with the modified epithelium of the walls and bottom of the fissures indicated a sensory function. Modern techniques have allowed us to determine that these

"ganglienkerne" are the subepithelial nuclei of sensory cells which extend into the epithelium. The sensory nature of the epithelium is frequently mentioned in descriptions of species, but the distribution of the sensory cells is neglected. In some species they occur in the walls as well as the floor, and in some throughout the entire length of the fissures. The apparent concentration of the sensory cells to the limited area around the papilla in Adenorhagas is unusual.

The morphology of Micrura fasciolata, the type species of the genus, was described by Friedrich (1960) and later with additions and illustrations by Cantell (1975). Friedrich (p. 53) noted the absence of a connective tissue layer in the cutis, that only two muscle layers with one muscle cross were present in the proboscis, and that the presence of longitudinal muscles between the rhynchocoel and foregut could not be ascertained. Cantell (fig. 2E) showed two layers and two muscle crosses, and referred to extensive development of CT in the cutis. He also noted the presence of longitudinal muscles between the foregut and rhynchocoel and correctly showed their derivation from the subepidermal LM in his diagram (fig. 1A). In 1976, Cantell (p. 120) stated that "a thick connective tissue layer in the interior cutis" was absent in all of the heteronemertines, including M. fasciolata, which he had described in 1975. His earlier references to a "cutis rich in connective tissue" was concerned with CT enclosing the subepidermal glands and did not refer to a CT layer.

Cantell (1976) verified the presence of two muscle layers and two muscle crosses in the proboscis of Lineus longissimus (Gunnerus, 1770) as figured by McIntosh (1873/74, Pl. XXI, fig. 5). Thus, the type species of the genera Lineus and Micrura are in group B (Lineidae) of Gibson (1985). Adenorhagas with inner and outer longitudinal muscle layers separated by a circular, belongs to Group A (Cerebratulidae) according to the scheme suggested by Gibson (1985). The flask-shaped posterior portion of the cephalic fissures, with a glandular papilla bearing the opening of the cerebral organ canal, the absence of a CT layer beneath the subepidermal glands, as well as the absence of a complete connective tissue sheath enclosing the ganglion layer of the brain, and the presence of a caudal cirrus, would induce most workers to place the species in the genus Micrura if the proboscis was not retained. Historically, heteronemertine species missing a proboscis, have been described and named, or have been assigned to a genus, e.g., Cerebratulides Stiasny-Wijnhoff, 1942. This has not only produced many names of species which cannot be identified, but also disrupts efforts to clarify genera. Punnett & Cooper (1909) placed all heteronemertines with a subepidermal connective tissue layer in the genus Lineus (a valid character), and all without this layer in Cerebratulus (also valid). In the Appendix to their paper they referred to the genus Micrura as a valid entity, but, based on the single character used in their paper, all valid species of Micrura would have had to be placed in Cerebratulus. Thus, while they simplified their own work, they created havoc with heteronemertine systematics and the Lineus and Cerebratulus species which they described will probably all have to be considered nomina dubia. Adenorhagas probably is related to those species described in the genus Micrura which have three muscle layers in the proboscis, one muscle cross, lack longitudinal muscles between the rhynchocoel and foregut, and lack a CT layer between the subepidermal glands and the OLM. These species must be removed from the genus and reassigned.

According to the characters listed by Gibson (1985), Adenorhagas is most similar to Micrurina among the 13 genera remaining in group A, following the transfer of Lineus and Micrura to group B. Stiasny-Wijnhoff (1942) described Micrurina from an incomplete specimen which left unresolved the presence or absence of a caudal cirrus. Micrurina lacks apical sensory organs. Its rhynchodaeum is attached dorsally as well as ventrally, separating the cephalic blood lacuna into two spacious lateral lacunae. Lateral blood vessels are present in the intestinal region and an excretory system is present. Also, there is no distinction between subepidermal longitudinal muscles and the OLM; the subepidermal glands pass inwards between the longitudinal bundles.”

(Riser, 1990: 597-606)

Specimens

Type Status Catalog No. Date Collected Location Coordinates Depth (m) Vessel
Paratype 131997 3/1/1986 South Pacific Ocean 42.4° S, 173.7° E