Speciation and Timeâšrelationships of the Nemertines to The

BULLETIN OF MARINE SCIENCE, 45(2): 531-538, 1989

SPECIATION AND TIME-RELATIONSHIPS OF THE NEMERTINES TO THE ACOELOMATE METAZOAN BILATERIA

Nathan W Riser

ABSTRACT The discovery of a marine nemertine, lacking a proboscis apparatus, in kelp holdfasts in New Zealand induces a re-evaluation of the phylum Nemertinea and its relationship to the Bilateria, Morphological features, which can be interpreted as primitive, are analyzed and a time frame for changes in the basic morphology is suggested.

Soft-bodied invertebrates have a very poor fossil record: Valentine (1987, fig. 2, 7) reports that first records of Nemertinea appear in the Carboniferous and Platyhelminthes and related Gnathostomulida in Recent (Quaternary) times. Schram (1973: 989) concluded that Archisymplectes rhothon Schram from the middle Pennsylvanian ofIllinois " ... shows remarkable similarities to nemertines, and demonstrates the ancient status of that phylum." Conway Morris (1977) considered Amiskwia sagittijormis Walcott, originally placed in Chaetognatha, difficult to place in a phylum although Owre and Bayer (1962) advocated inclusion in Nemertinea. This imprint from the middle Cambrian Burgess Shales of British Columbia, if a nemertinean, would have to be placed in the Tribe, Pelagica. Brasier (1979: 125) noted that the " ... Cambrian radiation event" possibly lasted only 10 million years and that it produced a "variety of body plan" which during the Cambrian " ... may have exceeded that at any other time in earth history." Gibson (1988) in agreement with Stiasny- Wijnhoff (1923), considered the Pelagica to be the most primitive polystiliferous nemertine taxon. However, the tribe is highly specialized for a bathypelagic existence. Amiskwia, if a nemertine, would indicate extensive involvement of the phylum in the Cambrian radiation event. Just as the Vendian (Precambrian) and Cambrian medusoids cannot be placed definitely in a taxon, the relationship of Amiskwia to other known groups remains hypo- thetical. As a nemertine, it would serve as an indication of the degree to which the acoelomate Metazoa Bilateria radiated during the Precambrian and Cambrian. Even without such evidence, we must assume that the group was part of the radiation event and as with other groups, many lines "were geologically short- lived" (Brasier, 1979: 125). Cataclysms during recorded geological times have decimated entire groups of animals and reduced others to a few relict species. As an example, the Permian/ Triassic crisis had a marked effect on the diversity of ammonoid cephalopods which, however, recovered and were then wiped out by the Cretaceous/Tertiary crisis. The effects of these crises are not as evident in the nautiloid cephalopods which underwent extensive radiation (seven orders) in the early paleozoic and then a steady decline in diversity to one genus today and the extinction of six of the orders. Riser (1985) asked the rhetorical question as to what nemertinean hierarchial units had been extinguished in those two crises. We only know the groups that are present today which survived all of the cataclysms and the selection processes that impacted upon the diversity offorms during the Cambrian radiation event. Twenty three species ofnemertineans, of which eighteen were abundant enough to permit identification, were collected by the author from holdfasts of the brown

531 532 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 alga, Lessonia variegata at Kaikoura, New Zealand in 1986. One ofthese, Arhyn- chonemertes axi Riser, has certain primitive morphological characteristics (Riser, 1988b) which indicate that the species might be a relict of significance analogous to the coelocanth, Latimeria and the monoplacophoran, Neopilina. Distinctive Morphological Characters of Arhynchonemertes axi: 1. Nervous system internal to body-wall musculature; 2. Blood vascular system a simple loop; 3. Excretory system unilateral with dorso-lateral pore behind mouth, much coiled vessel extending posteriorly to initial portion of intestine; 4. Vitellogenic oocytes free in parenchyma; 5. Proboscis apparatus including rhynchocoel absent; 6. Mouth ventral, small, beneath brain; 7. Brain bilobed with single commissure; 8. Cerebral organs lacking; 9. Outer circular and inner longitudinal muscle layers one fiber thick, dorso-ventral muscle fibers abundant from mouth to posterior end of body; 10. Submuscular gland cells not in packets; necks extend individually through epidermis; at least three different types of secretory cells filling parenchyma between body wall musculature and organ systems for the entire length of body; 11. Epidermis and pharyngeal epithelium meet at mouth without intergradation; 12. Tall, ciliated, simple columnar pharyngeal epithelium with neither epithelial nor subepithelial gland cells; 13. No morphological nor histological division offoregut into esophagus and stomach; 14. Intestine straight, without diverticula or caeca; bases of intestinal cells project into surrounding parenchyme; tunica propria not evident; 15. Monoecious, gonads along total length of intestine, testes dorso- lateral, ovaries ventro-lateral, both with preformed ducts and pores. Many of the nemertineans encountered in the holdfasts were also found in other cryptic habitats. It is assumed that A. axi may be cryptic and not restricted to the holdfast habitat, especially that of S. variegata, an austral species. The unilateral excretory system (3) with lateral nephridiopore near the mouth, and no elements of the system anterior to the pore, is unique among nemertines. The taxonomic significance of the unilateral system is unclear especially since the extensively coiled tubules oflarge cells intimately associated with the lateral blood vessels may be compensating for the lack of an excretory system on the other side of the body. The location of the nephridiopore and the absence of the system anterior to the excretory duct leading to the pore may well have phylogenetic significance beyond the species level.

PHYLOGENETIC CONSIDERA nONS The simplistic, and thus easiest, interpretation of the systematic position of A. axi is that the species has lost a proboscis apparatus and therefore is specialized. It has been suggested that the species might be an herbivore, based upon the histology of the gut, and that a proboscis would not be required for food capture; that the extensive development of subepidermal glands might indicate production of a toxic or noxious mechanism negating need for a proboscis for defense; and that a proboscis as a locomotor organ would not be required by this small hard surface dwelling species. Malacobdella. a commensal on the gills of clams, has been recognized as the exception to the "rule" that nemertineans are scavengers! carnivores but its feeding mechanism is specialized and furnishes no morphological evidence that would be distinctive of an herbivore. It is a filter feeder with an apical mouth and vast pharynx which serves as a pump in feeding, and into which the proboscis opens. The small, morphologically distinctive proboscis, has geen retained and is used in the occasional entrapping of food (Gibson and Jennings, 1969). The absence of a dorsal cerebral commissure in A. axi could be RISER: RELATIONSHIPS OF THE NEMERTINEA 533 explained if the species was degenerate and had lost its proboscis apparatus, above which the dorsal commissure would pass. In tum, the absence of cerebral organs the nerves of which are normally associated with the dorsal cerebral ganglia could imply regression of the dorsal lobes of the brain associated with the loss of the proboscis apparatus, however, dorsal ganglia are present in archinemertines, pe- lagic enoplans, Malacobdella, and Carcinonemertes which lack cerebral organs. Brinkmann (1917) considered the lack of cerebral organs in Pelagica to be a secondary loss, while Stiasny- Wijnhoff (1923) maintained that they had never developed in this group. The proboscis nerves of extant nemertines arise from the ventral cerebral ganglia or the ventral commissure, thus degeneration of the dorsal ganglia would appear to have no relationship to the presence or absence of the proboscis. The simple blood vascular system (2) could be attributed to the absence of the proboscis, except that a similar vascular system is present among some archinemertines. The morphology of A. axi cannot be accounted for by the "loss" of a proboscis apparatus. The relationship of the mouth to the brain is the only anoplan characteristic. It is borderline however, since the plasticity of the precerebral region of a nemertinean (see Riser, 1988a: 131) can influence such a relationship and with the two organs as close to one another as in this animal, a definitive statement- anterior to or posterior to, cannot be applied. Character 1 is definitive for the class Enopla. The nervous system of Archi- and Hoplonemertinea develops in the blastocoel according to Iwata (1960: 48) and external to "the mesodermal layers of the body wall" in the paleo- and heteronemertines. The system in archinemertines comes to lie in the internal longitudinal muscle layer and in hoplonemertines it comes to lie internal to that layer. Enoplans do have submuscular epidermal glands but they are usually of one type and are arranged in packets rather than as different types of gland cells (mucous, homoserous, and granular bacillary) indiscriminately mixed and each reaching the surface independently. Some anoplans have subepidermal packet glands extending into the muscle layers, and some of these glands in Baseodiscus are submuscular. The packets of subepidermal glands in the enoplans Carcino- nemertes and Malacobdella are present throughout most of the body length. Kir- steuer (1963) reported that the quantity of subepidermal glands varied between species of Tetrastemma in which they were present. There is an extensive development of subepidermal acidophilic and basophilic gland cells throughout the entire length of the body of Nemertopsis quadripunctata (Quoy and Gaimard) and a new species in this genus (R. Gibson, pers. comm.), but the cell bodies tend to be unitized according to secretion type. Ax (1963), Ivanov and Mamkaev (1973), and Kading (1974) included a frontal organ in their turbellarian archetypes. Graff (1891) described and figured this organ in acoel turbellarians and determined it to be secretory. Smith and Tyler (1986) verified the morphology with TEM and reported that the pore was enclosed by three specialized epidermal cells. They recommended (p. 77) that in acoelomorph Turbellaria, the term "frontal organ should refer only to" subepidermal mucous glands the necks of which extend forward to open in a specialized apical pit, designated as the "frontal pore" and that "other glands at the anterior tip" be called "frontal glands." In addition, they restricted the definition of frontal pore by features identifiable by TEM, and reported sensory cells peripheral to the pore but not as a part of its morphology. The acoelomorph frontal organ is thus strictly secretory. If the term frontal glands is applied to all subepidermal mucous gland cells complices sending necks to the apex whether associated with a spe- 534 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 cialized pore or not, considerable confusion can be avoided. The rhammite tracts of Macrostomum are not homologues of mucoid glands and should no longer be referred to as frontal glands (see Klauser et al., 1986). Some nemertines have one or more apical pits which usually are referred to as frontal organs and sometimes are seen to be everted papillae. Mucous glands with long necks open into (some hoplonemertines) or around (heteronemertines) these pits. Other gland cells, mucous, homo serous, and bacillary discharging through the epidermis may be present in the precerebral region ofturbellarians and nemertines. Nemertinologists refer to these, often including the frontal glands, as cephalic glands. As a result, Hyman (1951: 469) stated that the "homology" of the cephalic glands of nemertines with the frontal glands of turbellarians was "obvious." Ferraris (1979) described three types of mucous cells in nemertine cephalic glands based upon histochemical reactions and morphology. Only two of these cell types occurred in the archinemertine Procephalothrix spiralis Coe in which the cephalic glands discharge into the cephalic blood lacunae rather than through the epidermis. In the hoplonemertine Amphiporus lactifloreus (Johnston) and the heteronemertine Lineus socia lis (Leidy), all three types of mucous cells discharged through the precerebral epidermis but the necks of one type also opened into the bottom of the apical sensory pit of A. lactifloreus. Ruppert (1978) reported that the frontal organ of G6tte's and Muller's larvae (Polycladida) consisted of sensory cells enclosed in a ring of necks of frontal gland cells, Similarly (pers. obs.), the "cephalic gland" fields of Lineus ruber originate above and below the brain while those of L. viridis begin a short distance in front of the brain and in both species, the necks of the cells constituting the frontal gland discharge around the three apical sensory pits. The frontal glands of nemertines and turbellarians appear to be homologues, which introduces the question of the frontal pore which Ax (1984) postulated to have evolved a single time in the stem line of the Eu- plathelminthes. The morphology of the frontal pore of the acoelomorpha is unique to that group. Smith and Tyler (1986) were not able to demonstrate an intimate relationship of sensory elements to the pore and it is not clear how the frontal organs mentioned by Antonius (1970) fit into the picture. The apical organ of some acoelomate Bilateria consists of a combination of sensory elements, either internal to, or surrounded by the necks of the frontal glands. These apical organs (frontal pores, apical pits) are homologous (synapomorphies) within groups, but are not between groups. Whether the complices of sensory cells and frontal glands of flatworms and nemertines which Burger (1895) referred to as frontal organs and noted to be surprisingly alike, are homologous or analogous is debatable. If scattered openings of specialized mucous cells as well as scattered sensory cells at the apex of the body is pleisomorphic, then the various combinations of these elements concentrated to form a unit at the apex could be apomorphic since the origins are similar. A. axi has both cephalic (submuscular) and frontal glands, the latter originating immediately anterior to the mouth and discharging individually at the anterior apex of the body. Their presence, in the absence of an apical sensory organ, cerebral organs, and the proboscis apparatus all of which regenerate in all known fissiparous nemertines, makes the suggestion that A. axi is paratomic or architomic difficult to support. Sundberg (1985) observed that nemertinologists have dealt with phenotypes and that the scheme of classification which they use would have to be "assigned to the phenetic school if any." The internal morphology of almost half of the named species is unknown and the significant morphological features of many which have been serially sectioned have not been recorded or have been misin- terpreted as the result of distortion resulting from contraction induced by fixation. RISER: RELATIONSHIPS OF THE NEMERTINEA 535

Gibson (1985) gave a comprehensive account of the problems in nemertine systematics and questioned the validity of 30% of the species. It is difficult "to get a complete three-dimensional picture of the animal" (Sundberg, 1985: 248) and thus there is difficulty even in distinguishing species. Standardization of descriptions as advocated by Gibson (1985) is essential for the identification of species and can furnish a means toward postulating nemertine phylogeny. Among the terrestrial nemertines, adequate data is available so that Moore and Gibson (1985) have proposed a phylogenetic scheme based upon similarities (i.e., phenetic) for this group of species which Pantin (1961) postulated arose in the Pleistocene. Efforts to derive the nemertineans from Turbellaria still concentrate on the proboscis apparatus in spite of the absence of homology clearly noted by Beklemi- shev (1969). Attempts to derive other phyla from the nemertineans also continue, but there has been little change in classification within the phylum in the past half century even though species descriptions have improved. Iwata (1960) divided the anoplan order Palaeonemertina into two orders, primarily on embry- ological evidence. Gibson (1988) proposed a total revision of the taxonomy of the class Enopla which he divided into two new orders. The morphology of the nervous, reproductive, integumentary, and blood vascular systems and the complete digestive tract identifies A. axi as a nemertinean. Characters 7-15 are considered, by the author, to be primitive acoelomate bilaterian traits retained by A. axi. Extra-ovarian vitellogenesis (4) occurs among some Acoela and the Nemertodermatida and may also be primitive. In general, these correspond to the pleisomorphies of the Bilateria outlined by Ax (1984). Riser (1985) considered the blood vascular system of nemertineans to be coen- ogenetic, not a primitive character. The enterocoelic formation of the proboscis apparatus and blood vascular system, developed in response to the creeping mode of life postulated by Korotkevich (1980), is not supported by the morphology of Arhynchonemertes. The proboscis apparatus (rhynchodaeum, proboscis, rhynchocoel) is unique to the phylum and is not present in the larvae of archi- and palaeonemertines according to Iwata (1960). The rhynchodaeum, which disappears during development in Malacobdella, is a simple invagination of the anterior end of the body. The proboscis and rhynchocoel develop as a unit which becomes attached to the posterior end of the rhynchodaeal invagination. The epidermal proboscis rudi- ment is surrounded by mesodermal cells which separate to form the muscle wall of the proboscis and that of the rhynchocoel. This splitting is not the same as the formation of splanchnic and somatic muscles of coelomates, since it does not produce the body wall musculature. The relationship of the circular layer of the proboscis to that of the body wall is not obvious, which, in part, contributed to the difficulty ofWynhoff(1914) in explaining the disrupted circular layer in the probosces of some archi- and palaeonemertines. Details of organogenesis of mesodermal tissues is poorly known in the Nem- ertinea. Developmental studies are few, and have depended upon availability of material for study. Among the primary sources of information are the careful observations of Salensky (1884, 1909) on the development of the ovoviviparous Prosorhochmus, and (1886, 1912) on necrobiotic heteronemertine pilidia larvae, Coe (1904) on the terrestrial Pantinonemertes agricola (Willimoes-Suhm) and Hammarsten (1918) on the commensal, Malacobdella. Lebedinsky (1897) and Iwata (1960) have been responsible for most of the available information on organogenesis in species with direct development. Pedersen (1968) noted that the connective tissue ofnemertines is a continuum from the fibrous basement mem- brane, to the dermis and parenchyma containing a few cells and anchored as 536 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989

membranes (including the tunica propria ofthe gut) enclosing the internal organs. Lateral diverticulation of the gut occurs in the Plathelminth taxon Trepaxonemata in which the dorso-ventral muscles are aggregated as bundles between the diverticula. Ax (1984) noted that this could not be an ancestral character for the Plathelminthomorpha nor the Bilateria. The connective tissue of A. a.xi is weakly developed, and the dorso-ventral muscles occur as fibers passing between the bases of the intestinal cells. Incomplete knowledge of ontogeny coupled with inadequate morphological information has handicapped development of a cohesive comprehension of the relationships of the disparate groups constituting the Nemertinea. During the radiation event, some acoelomate bilaterian metazoans developed a complete digestive tract. The sequence of morphological changes, building around that modification, can only be postulated. We know the results millions of years later. A possible scenario for the nemertines would require One or more of those forms with a complete digestive tract to have (ancestrally or derived) sac-like gonads with direct egress through the body wall, and one of these would evolve a nervous system in which the nerve cords were neuron encased extensions of the brain. It is at this stage that the animal is a nemertine, and also when confusion arises since we know so little about the sequencing of mesoderm differentiation in the phylum. If A. axi is a relict, as postulated, the vascular system could have arisen prior to the proboscis apparatus. Both systems are unique and could only have arisen once. The addition of an outer longitudinal muscle layer in the body wall (and also in the proboscis apparatus) ofheteronemertines had to occur later. The absence of cerebral organs in archinemertines (and in A. axi) implies their origin after that of the proboscis apparatus. Riser (1985) referred to the Nemertinea as polyphyletic (i.e., that the AnopIa and Enopla were derived from different ancestral stocks, and not one from the other). It appears that this was simplistic and that in fact the present hierarchial scheme for the phylum is artificial con- centrating on characters of recent origin. Ax (1984) considered the dioecious condition of the Metazoa to be primitive and the monoecious condition of flatworms to be derived. Riser (1985) noted that both conditions "are very old" but that the question of which was primitive for the animal kingdom could not be determined and suggested that the monoecious state occurring in nemertines was derived. The factors involved in sex determination in dioecious nemertines is unknown at present. Among monoecious forms, Coenemertes caravela Correa, 1966, some species of Prostoma, and the genus Prosorhochmus have combined (hermaphroditic) gonads, a derived condition. Apatronemertes albimaculosa Wilfert and Gibson, 1974, a freshwater heteronemertine, is the only non-hoplonemertine which has been shown to be definitely monoecious. The fact that the monoecious condition has been found primarily in freshwater and terrestrial species of hoplonemertines has resulted in the parsimonius approach that the condition is a specialization which has evolved in response to the way of life of the animals. The possibility that the acoelomate bilaterian ancestors of the flatworms and nemertines were monoecious has been bypassed because among flatworms the monoecious condition has been retained and extant nemertines are primarily dioecious. The alternative could be that monoecious freshwater and terrestrial nemertines have retained a primitive character, which was not disadvantageous, while specializing in other ways to meet their environment and the dioecious condition has evolved among marine forms. The genera Notogaeanemertes, Prosadenoporus, and Prosorhochmus which in- clude marine, littoral, and marine supralittoral species are monoecious and related to the terrestrial forms. The terrestrial and freshwater nemertines belong to two RISER: RELATIONSHIPS OF THE NEMERTINEA 537 different families which probably left the sea at different times and independently. The morphology of Arhynchonemertes axi furnishes no reasons to consider the species to be a descendent of monoecious terrestrial (or freshwater) nemertines which reentered the sea; but rather that it is a member of a marine group that retained the character while other marine nemertines evolved with the major modifications we see in species today. A successful phylum attempts to invade all available living spaces. Modifications of the integument which have allowed nemertines to utilize a variety of spaces have been discussed by Norenburg (1985). The bony fishes arose in freshwater in the Paleozoic and moved into the marine environment in the Mesozoic and underwent major organic radiation with some forms later moving back into freshwater. The nemertines arose in a less haline aquatic environment than today, but the ancestral osmoregulatory system discussed by Ax (1984: 272) has been retained, and is most specialized in terrestrial species and cephalothricid archinemertines. Halinity would not appear to have had any inhibitory effect upon adaptive radiation in the phylum, which must have carried out its major evolution in a haline environment. Bony fish organic radiation in the Paleozoic and Mesozoic is known; for the nemertines, we have no record. Arhynchonemertes axi may be a relict species as suggested by Riser (l988b) but its major significance lies in the primitive bilaterian characters (7-15) which it exhibits uniquely and which allow for new insights into the phylogeny of the "phylum" Nemertinea and its relationship to the other acoelomate bilaterians. The rejection of the Linnaean hierarchic categories by Ax (1984) allows us to look more clearly at the taxon Bilateria.

ACKNOWLEDGMENTS

Drs. R. Gibson and J. Norenburg, neither of whom agreed with my assessment of the phyletic position of Arhynchonemertes axi, served conscientiously as Devil's Advocates in reviewing early drafts of this manuscript. Helpful comments from Drs. G. Jones and J. P. S. Smith have been incorporated into the final draft. It is hoped that their contributions have been answered in a way that will induce fellow workers to reevaluate nemertine and acoelomate metozoan bilaterian systematics. The various drafts were typed by Mrs. Elaine Cole. This manuscript represents Contribution Number 171 of the Marine Science Center of Northeastem University.

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DATEACCEPTED: August 23, 1988.

ADDRESS: Marine Science Center, Northeastern University, East Point, Nahant, Massachusetts 01908.