Schultze, 1853
See page Ne. 1 Introduction and further for more about nemertinans. The systematics of pelagic nemertines have still not been satisfactorily resolved, with the two conflicting classifications (Coe's system, based upon Brinkmann's pioneering work, and Korotkevich's system) differing widely in the number of families and genera that they recognise. One of the major difficulties with this group of nemertines is that for so many of the taxa only individual, or at best a very small number, of specimens has been found; this problem is compounded by the lack of anatomical data for many of them, especially the older established species, and insufficient knowledge of either intraspecific variation or possible sexual dimorphism. Recent collections of pelagic nemertines from the north Pacific have yielded many specimens, several of which appear to be new (Drs. Pam Roe and Jon Norenburg, pers. comm.), and it is to be hoped that with the possibility of molecular techniques being applied to systematic studies on these pelagic animals that future studies will resolve the conflicting classifications of Coe and Korotkevich.
The classification used in the present chapter follows the Brinkmann/Coe system, but Korotkevich's classification is also shown to emphasise the differences between these two schemes. Gibson (1995) lists 40 genera and 97 species of pelagic nemertines as currently valid, of which 11 species have now been recorded from the South Atlantic.
The following classification is based upon Coe's (1954a) work, but with the higher taxonomic categories named after Sundberg's (1991) revised terminology for the phylum. Families shown in bold include genera and species which have either been recorded from the south Atlantic or are likely to occur within the region; these taxa are covered in detail in the present work.
Outline classification
Phylum Nemertina Schultze, 1853
Class Enopla Schultze, 1853
Subclass Hoplonemertina Hubrecht, 1879
Superorder Polystilifera Brinkmann, 1917
Order Pelagica Brinkmann, 1917
Family Armaueriidae Brinkmann, 1917
Genus Armaueria Brinkmann, 1917
Genus Neoarmaueria Chernuishev, 1992
Genus Proarmaueria Coe, 1926
Genus Proarmaueriella Chernuishev, 1992
Genus Xenoarmaueria Chernuishev, 1992
Genus Zinarmaueria Chernuishev, 1992
Family Balaenanemertidae Coe, 1954
Genus Balaenanemertes Bürger, 1909
Family Buergeriellidae Brinkmann, 1917
Genus Buergeriella Brinkmann, 1917
Family Chuniellidae Brinkmann, 1917
Genus Chunianna Coe, 1954
Genus Chuniella Brinkmann, 1917
Family Dinonemertidae Brinkmann, 1917
Genus Alexandronemertes Chernuishev, 1992
Genus Dinonemertes Laidlaw, 1906
Genus Paradinonemertes Brinkmann, 1915
Genus Planonemertes Coe, 1926
Genus Plionemertes Coe, 1926
Genus Tubonemertes Coe, 1954
Family Nectonemertidae Verrill, 1892 emend. Brinkmann, 1917a
Genus Nectonemertes Verrill, 1892
Family Pachynemertidae Coe, 1954
Genus Pachynemertes Coe, 1936
Family Pelagonemertidae Moseley, 1875b emend. Brinkmann, 1917a
Genus Cuneonemertes Coe, 1926
Genus Gelanemertes Coe, 1926
Genus Loranemertes Chernuishev, 1992
Genus Nannonemertes Wheeler, 1937
Genus Natonemertes Brinkmann, 1917
Genus Nemertobus Chernuishev, 1992
Genus Obnemertes Korotkevich, 1960
Genus Parabalaenanemertes Brinkmann, 1917
Genus Pelagonemertes Moseley, 1875
Genus Probalaenanemertes Brinkmann, 1917
Family Phallonemertidae Brinkmann, 1917
Genus Phallonemertes Brinkmann, 1917
Family Planktonemertidae Brinkmann, 1917
Genus Crassonemertes Brinkmann, 1917
Genus Mergonemertes Brinkmann, 1917
Genus Mononemertes Coe, 1926
Genus Neuronemertes Coe, 1926
Genus Planktonemertes Woodworth, 1899
Genus Plenanemertes Coe, 1954
Genus Tononemertes Coe, 1954
Family Protopelagonemertidae Brinkmann, 1917
Genus Calonemertes Coe, 1945
Genus Pendonemertes Brinkmann, 1917
Genus Plotonemertes Brinkmann, 1917
Genus Protopelagonemertes Brinkmann, 1917
Korotkevich's (1977a) classification, which is not used in the present chapter, recognised the following families and genera:
Family Armaueriidae: Armaueria, Mesarmaueria (Chernuishev, 1992b, synonymised this genus with Proarmaueria), Proarmaueria.
Family Nectonemertidae (Korotkevich, 1955a, included in this family the Buergeriellidae, Chuniellidae, Phallonemertidae, Planktonemertidae and Protopelagonemertidae): Dinonemertes (Dinonemertes, Planonemertes and Plionemertes were synonymised with Dinonemertes by Korotkevich, 1955a), Nectonemertes (Korotkevich, 1955a, included Buergeriella, Chuniella (partim) and Drepanophorus (partim) as synonyms of Nectonemertes), Planktonemertes (Korotkevich, 1955a, included the following genera as synonymous with Planktonemertes: Calonemertes, Chuniella (partim), Crassonemertes, Mergonemertes, Mononemertes, Neuronemertes, Pachynemertes, Paradinonemertes, Pendonemertes, Phallonemertes, Plotonemertes, Protopelagonemertes).
Family Pelagonemertidae (The family Balaenanemertidae was included in this taxon by Korotkevich, 1955a): Obnemertes, Pelagonemertes (Korotkevich, 1955a, included as synonymous with Pelagonemertes the following genera: Balaenanemertes, Cuneonemertes, Gelanemertes, Nannonemertes, Natonemertes, Parabalaenanemertes, Probalaenanemertes).
(To complete all classifications ETI has added the Kingdom and the Phyla of all the different taxa treated on this DVD-ROM without higher classification descriptions. Texts from Lynn Margulis and Karlene V. Schwartz, Five Kingdoms. CD-ROM Copyright 2002 ETI / Freeman & Co Publishers)
Nemertina is a phylum consisting mostly of free-living worms found in marine, freshwater, and soil habitats. Their common name ribbon worm refers to their flat bodies and the brilliant color patterns of many species. A long, sensitive anterior proboscis that is separate from the digestive tract characterizes nemertines. This unusual organ is branched in some species. The proboscis resides in a body cavity (rhynchocoel), from which the worm rapidly everts its proboscis as much as three times the length of its body. Muscular pressure on the fluid-filled proboscis chamber forces explosive eversion of the proboscis. So accurate is its aim that another common name for these worms is nemertine, based on the Greek term meaning the unerring one. Nemertines use the proboscis to explore the environment, to capture prey, to defend themselves, and for locomotion. Annoyed nemertines release their proboscises, which they then regenerate.
Most ribbon worms live in the sea, in the intertidal marine sands, and in estuaries and are more abundant in temperate than in tropical oceans. Carinina is found in the abyss down to 4000 m. Some species are symbionts; Gononemertes lives in the branchial chambers of tunicates (urochordates, Subphylum Urochordata). Tubulanus secretes a mucus dwelling tube, whereas Linnaeus takes over empty burrows of Chaetopterus and other marine polychaete annelids (Phylum Annelida). Prostoma lives on aquatic plants in quiet fresh water along the Atlantic, Gulf, and Pacific coasts, in the U.S. Midwest, and in Europe. The terrestrial ribbon worm Geonemertes inhabits moist soil of subtropical forests, between pandanus leaf bases, and, when introduced, thrives in greenhouse soils. Parasitic Carcinonemertes lives on crustaceans and feeds on the host’s developing eggs as well as the host.
About 900 nemertine species are known. They range from less than 0.5 mm to 30 m in length. Lineus longissimus, the iridescent bootlace worm, about 30 m long, is one of the longest invertebrates known. Cerebratulus lacteus can extend itself from about 1 to 10 m. Emplectonema is the only bioluminescent nemertine described. Most nemertines, especially the bottom dwellers, are pale, though a few are striped, speckled, or marbled multicolor ribbons.
Nemertines are abundant in the intertidal zone, although rarely seen; most are active at night, burrowing and feeding. They bur-row by everting their proboscises into the mud; then they dilate the proboscis, forming an anchor. Nemertines pull themselves into their burrows by contracting body and proboscis muscles, pulling their bodies through the sediment. Like many other boneless animals, the nemertine’s support is the incompressible liquid enclosed within its body wall. On tidal mud flats, nemertines can be found among algae, mussels, and tube-dwelling annelids. Nemertines sometimes creep out of seaweed placed in a dish of seawater.
Pelagic species (open ocean dwellers), such as Nectonemertes, tend to be more leaf-shaped and have less well developed muscles than do benthic (seafloor dwelling) nemertines. Pelagic nemertines float passively or swim with lateral undulations. Benthic nemertines crawl by muscular contractions, secreting a slime track. The smallest glide with their cilia against the resistance of their viscid mucus. Rarely, nemertines use their proboscises to attach themselves to an object and pull themselves forward.
Nemertines, unlike flatworms (Phylum Platyhelminthes), have a blood vascular system through which contractile vessels and body muscle contractions pump blood. Unidirectional valves and heart are lacking. The heme-containing blood cells in a few species may carry oxygen. Nemertine blood may be colorless, red, yellow, purple, or green, depending on the species. Some rhythmically take water into the vascularized foregut, presumably for gas exchange; most respire through the epidermis, like flatworms. The excretory system of these worms consists of protonephridia with flame cells that regulate ions, water, and possibly dissolved waste, which exits through lateral pores. Nemertina is the first phylum with openings at both ends of the digestive tract; solid waste leaves through the anus.
The nemertine nervous system resembles that of flatworms: a bilobed cerebral ganglion (brain) and longitudinal nerve cords with connecting nerves. Their light-sensitive eyespots number from zero to as many as several hundred. Functions suggested for the cephalic slits (those in the head) include chemotactic, auditory, excretory, respiratory, and endocrine. A cerebral organ opens into the cephalic slits. Papillae on the anterior end are sensory.
Three of the four orders of nemertines are predators, feeding on a wide variety of prey: annelids (Phylum Annelida), crustaceans (Phylum Crustacea), flatworms (Phylum Platyhelminthes), molluscs (Phylum Mollusca), roundworms (Phylum Nematoda), and even small fish (Phylum Craniata). One of the three orders of predaceous nemertines has stylets. The proboscis of predaceous Prostoma has a venomous stylet with which the worm repeatedly stabs and paralyzes prey. The sticky proboscis wraps around prey and transfers captured prey to the mouth. Mouth and proboscis may share a common opening, depending on the species. Prey are sucked whole into the mouth; however, if the prey is too large to swallow, juices are sucked out of it instead. Cilia move food from the mouth along the foregut. Phagocytosis and extra- and intracellular digestion take place in the intestine, which has numerous pouches (diverticula). Malacobdella is the unique filter-feeding nemertine, living commensally within the mantle cavity of clams (Phylum Mollusca). Malacobdella filters bacteria, algae, diatoms, and other protoctists from water within its host’s mantle cavity through ciliated papillae in its foregut.
Nemertines are the prey of crustaceans, annelids, and other marine invertebrates. Along the Atlantic coast of North America, ribbon worms serve as fish bait, but people do not eat ribbon worms.
Nemertines’ prodigeous regeneration is a potential research model for tissue culture. The worms reproduce asexually by fragmentation—each fragment regenerates a complete worm. Carcinonemertes reproduces by parthenogenesis. Nemertines can also reproduce sexually. In most species, the sexes are separate. In sexual reproduction, numerous temporary gonads form during the breeding season in mesenchyme tissue between intestinal pouches. Each gonad opens to the outside through its own surface pore. Eggs are laid in gel strings. Fertilization typically takes place in the water but is internal in some species. The eggs develop either directly into adults or first into pilidium (free-swimming) larvae, which look like ciliated caps with ear flaps and apical tuft. Still other species have Iwata larvae or Desor larvae—named for embryologists. Desor larvae are characteristic of Lineus and other heteronemertines. The Desor is a ciliated, oval, postgastrula stage that stays within the egg membrane (unlike pilidium larvae); it lacks oral lobes and the apical tuft of pilidia. A few species are protandric hermaphrodites—each individual is first male and then becomes female. Members of the hermaphroditic terrestrial genus Geonemertes bear live young. In Nectonemertes, a genus of active swimmers, males clasp females with special attachment organs during mating. Knotted balls of about 30 Cephalothrix have been observed—perhaps mating—in breeding season beneath stones along the Yorkshire coast.
The fossil record of nemertines is sparse. The Cambrian Amiskwia was regarded as a nemertine fossil or as a chaetognath (Phylum Chaetognatha). Its phyletic position is obscure. Structures common to both nemertines and flatworms are parenchyma tissue that encloses organs; lack of body cavity, respiratory organs, and segmentation; ciliated epidermis that moves the animal along a mucus track; similar sensory and excretory organs; and multiple reproductive organs. Some flatworms, annelids, and molluscs also have anterior proboscises but only those of nemertines are in fluid-filled, cell-lined cavities separate from the gut. Common features were thought to point to a close relationship between flatworms and nemertines despite their differences in food getting, digestive systems (the one-way nemertine gut is assumed more efficient than the dead-end flatworm gut), and oxygen–carbon dioxide exchange. However, comparison of ribosomal RNA sequences places Cerebratulus—the nemertine studied—near sipunculids, annelids, and molluscs (protostomous coelomates—the embryonic blastopore is the site of the adult mouth) and more distant from flatworms (acoelomates). These molecular data are supported by ultrastructural evidence that places nemertines as protostomous coelomates; the blood vascular system, gonadal sacs, and the rhynchocoel cavity are modified coelomic cavities, originating from mesoderm. It appears that the acoelomate attributes of nemertines may have evolved secondarily from a more typical coelomate ancestor. If this affiliation is accepted, nemertines will move to the protostome coelomate position in the phylogenetic tree.