Nemertina
Introduction

The phylum Nemertina (= Nemertea or Rhynchocoela) contains more than 1100 species currently recognised as valid (Gibson, 1995), although many are inadequately described. The worms are almost exclusively marine, with only a small number of terrestrial or freshwater species known. Nemertines are typically defined as unsegmented, bilaterally symmetrical, acoelomate invertebrates, although studies by Turbeville and Ruppert (1985) and Turbeville et al. (1992) have suggested that they may be more closely related to protostome coelomates than to any acoelomate group, and some of the interstitial taxa exhibit pseudosegmentation (Norenburg, 1988). The principal anatomical features of nemertines are that they possess a gut with separate mouth and anus, a closed blood system consisting of distinct vessels or lacunae, and an eversible muscular proboscis contained, when retracted, in a fluid-filled chamber (the rhynchocoel) extending above the alimentary canal. They also possess a well developed nervous system with lobed cerebral ganglia and paired longitudinal nerve cords, a ciliated epidermis and gut epithelium and, in most taxa, a protonephridial excretory system.

The identification, and thus classification, of nemertines rests largely upon histological studies of their anatomy, yet for almost half of the named species their internal morphology is completely undescribed (Riser, 1989). Many systematic changes have been made or proposed during recent years, at almost all taxonomic levels from the species upwards, and to a large extent both the classification and phylogeny of the phylum remain open to discussion. At present there is no universally accepted classification for the group.

Nemertines can broadly be divided into two major morphological groups on the basis of their proboscis morphology: those with no stylet apparatus constituting the Anopla, and those in which the proboscis is armed with one or more stylets forming the Enopla. The higher systematic affinities of certain taxa, notably the highly aberrant New Zealand species, Arhynchonemertes axi Riser, 1988, which completely lacks a proboscis apparatus, the mesopsammic anoplan Riserius pugetensis Norenburg, 1993, which can only be identified as probably belonging in the anoplan order Heteronemertina, or the entocommensal genus Malacobdella, whose members are leech-like with a posterior ventral sucker, are at present unknown or subject to discussion, but the enoplan group Hoplonemertina (Hoplonemertea) is divisible into the Monostilifera (proboscis armed with a single central stylet borne on a cylindrical basis) and the Polystilifera (proboscis armed with a shield- or pad-like basis bearing numerous small stylets). The Polystilifera, in turn, comprises two ecological groups, the benthic species being placed in the Reptantia and the pelagic forms in the Pelagica.

The earliest reference to a pelagic nemertine, although it was reported as a mollusc, was probably the account of Pterosoma plana Lesson, 1830, found in large numbers between the Moluccas and Papua New Guinea. Moseley (1875a: 382) concluded after consulting Lesson's (1830) original illustration of Pterosoma that "On the whole . . . there seems little doubt that the animal seen and figured . . . was a Nemertine and not a mollusk; but it seems to have been a distinct form, with a pair of eyes and an unbranched digestive tract." Hubrecht (1887), who reproduced Lesson's original illustrations, concurred with Moseley's conclusion, but Gibson (1995: 501) was more cautious, stating that "if this form is a nemertean, as appears probable, its taxonomic affiliations remain unknown." The first certain description of a pelagic nemertine was given by Moseley (1875b) when he recorded Pelagonemertes rollestoni Moseley, 1875, from the Indian Ocean. The internal anatomy of this specimen was later partly elucidated by Hubrecht (1887), who was the first worker to both affiliate pelagic nemertines with the Hoplonemertina and examine them histologically. In his second paper (Moseley, 1875a), in which he described what he believed to be a juvenile specimen of Pelagonemertes rollestoni, Moseley proposed a new family, the Pelagonemertidae, to accommodate the species; Bürger (1895) regarded this individual as a different taxon and renamed it Pelagonemertes moseleyi Bürger, 1895, a distinction maintained by subsequent authors.

During the next two decades many other pelagic nemertines were described from the Atlantic (Verrill, 1892; Joubin, 1904, 1906), Pacific (Woodworth, 1899; Cravens and Heath, 1906) and Indian Oceans (Laidlaw, 1906; Bürger, 1909), Bürger's article containing the first report of a pelagic nemertine from the South Atlantic, a specimen of Nectonemertes mirabilis Verrill, 1892, being obtained in an open net hauled vertically to the surface from a depth of 3000 m.

It was, however, a number of papers by August Brinkmann (1912, 1915, 1917a, b, 1920) which led to the most significant advances in the systematics of pelagic nemertines and, indeed, formed the basis for the classification of the group still in use today. Brinkmann (1917a) (republished verbatim in 1932) was the first to propose a classification for the pelagic nemertines, although he noted in his Introduction that the "demand for space altogether transcending the limits assigned to [his] chapter" prevented him from fully describing the anatomy of the many species established; these were extensively covered in a separate monograph (Brinkmann, 1917b). Brinkmann (1917a) distinguished between the monostiliferous and polystiliferous hoplonemertines as separate suborders; he also divided the Polystilifera into two tribes, which he called the Reptantia (bottom dwelling Polystilifera with cerebral sensory organs, an excretory system and lateral rhynchocoel diverticula) and Pelagica (pelagic Polystilifera with no cerebral organs, excretory system or rhynchocoel diverticula). In this paper he established the seven families Armaueriidae, Bathynemertidae, Buergeriellidae, Chuniellidae, Dinonemertidae, Phallonemertidae and Planktonemertidae, emended the definitions of the Nectonemertidae and Pelagonemertidae, and described nine new genera (Armaueria, Bathynemertes, Buergeriella, Chuniella, Crassonemertes, Natonemertes, Pendonemertes, Phallonemertes, Plotonemertes) and eleven new species.
(Ne 1 , morphological features)

Brinkmann's (1917b) monograph, using the same classification as that given in his 1917a paper, was the first major treatise on pelagic nemertines, most of the 37 species he recognised being both described and illustrated in detail. He defined the Pelagica (Brinkmann, 1917b: 145) "Pelagische Polystilifera. Cerebralorgane, Exkretionsorgane, Rhynchocoelomdivertikel und metamere Gefässkommissuren fehlen. ` Gonaden nur in der Kopfregion entwickelt." The detailed histological studies made by Brinkmann enabled him to discuss the comparative anatomy of the pelagic nemertines, particularly their epidermis, body wall and other musculature, parenchyma, alimentary tract, sensory organs, proboscis apparatus and blood, nervous and reproductive systems; anatomical features which can be used to distinguish between pelagic species are illustrated in the following figures.

Ne 1 , morphological features
Ne 2abc , anatomical features
Ne 2de
Ne 2fg
Ne 2hi
Ne 2jk
Ne 2l

Brinkmann's (1917b) discovery of a small crustacean in the intestine of a Nectonemertes mirabilis was the first evidence on the food of bathypelagic nemertines and, though few data exist on their diets, it is generally believed that Crustacea and other pelagic invertebrates probably constitute the food of these worms; nemertines as a phylum are typically carnivorous (McDermott and Roe, 1985).

It was in 1920 that the first of Coe's many articles dealing with pelagic nemertines appeared. During the next 36 years Coe added much to the knowledge of bathypelagic nemertines, his various articles covering not just descriptions of many new taxa and the systematics of the group but also the adaptations shown by pelagic nemertines to their way of life, details of unusual features of the nervous system, zoogeographic distribution and the means whereby these animals are dispersed in the oceans. Coe's (1926) monograph was the second major treatise on pelagic nemertines to be published. In this work Coe followed the familial arrangement proposed by Brinkmann (1917a, b) but established several new genera as well as eight new species. The introduction to this extensive work includes a history of the subject, with reference to the various expeditions during which pelagic nemertines had been collected, and is followed by a detailed comparative discussion of what he called the 'morphological peculiarities', commenting (p. 18) that "The special adaptations of these worms to a pelagic existence far beneath the surface of the ocean have led to numerous modifications of the organ-systems as found in their littoral relatives. Most of these modifications... are due to the loss or reduction of structures which are found in a more highly organized condition in the Drepanophorus-like forms from which the pelagic nemertines are thought to have been descended." It was in the section summarising the ecology of pelagic nemertines that Coe (p. 91) commented that at the depths the nemertines live they "swim slowly to and fro or float idly with a very slight muscular effort", although later (p. 93) he refers to the violent undulatory swimming movements earlier noted for Pelagonemertes and Nectonemertes by Moseley and Brinkmann respectively. This supposed feeble locomotion has been widely restated in subsequent literature, but video film of several north Pacific species shown at the 1995 international nemertine conference in Monterey, California, by Drs. Pam Roe and Jon Norenburg demonstrated that many of the pelagic species can swim actively at least for short periods of time.

Coe (1926) also commented on the great variation in size between species of bathypelagic nemertines, noting that whilst some species of, for example, Balaenanemertes, attained sexual maturity at lengths of only 6-10 mm, other forms were much larger. He cited one specimen of Dinonemertes investigatoris Laidlaw, 1906, which was 203 mm long, 56 mm wide and 15 mm thick, although other species of Dinonemertes and Nectonemertes may attain lengths of 60-85 mm. The largest South Atlantic form yet discovered is Calonemertes hardyi (Wheeler, 1934).

Although virtually nothing is known about the reproductive biology of pelagic nemertines, Coe (1926) extensively discussed the structure of the gonads, spermatogenesis and ovogenesis in the Pelagica. Except for Proarmaueria pellucida Coe, 1926, which appears to be irregularly hermaphroditic, bathypelagic nemertines are dioecious, with both the position and morphology of their gonads modified in comparison to those found in benthic nemertines. In one pelagic form, Phallonemertes murrayi (Brinkmann, 1912), the spermaries are prolonged to form slender, muscular penes (Ne 2l), regarded as true copulatory organs by Coe, which may serve as spermatophores by being retained within the female ovaries after mating.

Three of Coe's publications (Coe, 1935, 1936, 1945) were principally concerned with collections of bathypelagic nemertines made within the Bermuda region. His 1935 paper included a discussion of the distribution of pelagic species in relation to water temperature, density, salinity, oxygen levels, phosphate content and pH with the view of showing how stable conditions permit a great vertical range and almost unlimited geographical dispersal of species below 1200 m depth. In the last of these three articles on the pelagic nemertines of Bermuda Coe (1945) extended his discussion of the means whereby these animals were distributed to include south Atlantic species, later publishing this discussion as a separate article (Coe, 1946). He explained the dispersal of pelagic organisms in terms both of superficial and deep currents. During this period Wheeler (1934, 1937) described new species from the South Atlantic and Indian Oceans, later (Wheeler, 1940) reporting new records of pelagic nemertines from Antarctic waters.

By 1954 57 species of pelagic nemertines had been described worldwide, of which 12 were known from the Pacific. Coe (1954a) added a further 17 species to the known Pacific fauna, seven of which were previously known only from the Atlantic (Coe, 1945). Coe's (1954a) classification of the Pelagica listed 11 families, with the Balaenanemertidae and Pachynemertidae being the only two not included in Brinkmann's (1917a, b) publications. Coe established four new genera (Chunianna, Plenanemertes, Tononemertes, Tubonemertes) and ten new species for the Pacific, providing keys to both families and genera. Many of the taxa he recorded in this paper came from collections made in the submarine canyon off Monterey Bay, California, and Coe's (1954b) article was principally concerned with this region. His last paper on pelagic nemertines (Coe, 1956) gave keys to the families and genera of pelagic nemertines known to occur in the eastern and central north Atlantic Ocean. Apart from Brinkmann and Coe, only one other zoologist, the Russian Korotkevich, has made major contributions to our present knowledge of bathypelagic nemertines. Korotkevich (1955a) listed a total of 73 species of pelagic nemertines from Russian seas, 16 of which were described as new. Korotkevich's classification of the group, however, was very different from that given by Brinkmann and Coe in that she recognised only three families (Armaueriidae, Nectonemertidae, Pelagonemertidae) and seven genera (Armaueria, Dinonemertes, Mesarmaueria, Nectonemertes, Pelagonemertes, Planktonemertes, Proarmaueria). Other articles by Korotkevich (1955b, 1956, 1960, 1962, 1963, 1964, 1967) dealt with diverse topics relating to pelagic nemertines, including lists of far eastern and Antarctic species, a discussion of the polyphyletic origin of the group, and the suggestion that the Middle Cambrian Burgess Shale fossil Amiskwia sagittiformis Walcott, 1911, originally described as a chaetognath, was a pelagic nemertine; she affiliated it with the family Pelagonemertidae, but Conway Morris (1977) fully redescribed this fossil and concluded that its phyletic position could not be determined.

In her most recent discussion on the systematics of the Pelagica Korotkevich (1977a) recognised only three families and eight genera; these families, with their contained genera listed in parentheses, were the Armaueriidae (Armaueria, Mesarmaueria, Proarmaueria), the Nectonemertidae (Dinonemertes, Nectonemertes, Planktonemertes) and the Pelagonemertidae (Obnemertes, Pelagonemertes).

Comparatively few new taxa of pelagic nemertines have been described since about the middle 1960's; Friedrich (1969b) and Van der Spoel (1988) described new species from the Gulf of Guinea and Indonesia respectively, whilst Chernuishev (1992a) used supposed cases of homonymy, unavailability of names and nomina nuda to propose new names for a number of nemertine taxa, including some pelagic forms, later (Chernuishev, 1992b) reclassifying the family Armaueriidae with the suggestion that this group was derived from primitive Nectonemertidae. Chernuishev's proposals have not met wide acceptance.