Nemertea

The phylum Nemertea is an invertebrate phylum that contains over 1,000 species within 250 genera of mostly marine organisms known variously as ribbon, proboscis, or nemertean worms. Only a few taxa inhabit freshwater, and there are several terrestrial species. Most are free living; however, a few are known to be parasitic. The name means one of “Nereis” (unerring one), which refers to the unerring aim of the proboscis. Ribbon worms are unique in having an eversible muscular proboscis that is used for grasping prey. It lies free inside of a cavity above the alimentary canal known as the rhynchocoel. This muscular tube can be swiftly thrust out to catch prey items. This phylum is also occasionally called the Rhynchocoela, which refers to the rhynchocoel. Because nemerteans are nearly completely soft-bodied, there are no definitive examples of fossils. Ribbon worms (Prostoma sp.) were first reported from Arkansas in 2011 from the Ouachita River in Montgomery County.

Taxonomy of the Nemertea was formerly straight forward, as there are only two classes: Enopla and Anopla. The Class Enopla includes two orders (Bdellonemertea and Hoplonemertea) with about 650 species that have a proboscis usually armed with stylets and a mouth that opens in front of the brain. The Class Anopla includes two orders (Paleonemertea and Heteronemertea) with about 500 species; they are defined as those having a proboscis lacking stylets and a mouth that opens below or posterior to the brain. However, it is now known that the Anopla are paraphyletic, as one order is more closely related to Enopla than to the other order within Anopla. The phylum Nemertea is monophyletic, and traditional taxonomy says that nemerteans are closely related to flatworms and that both are relatively “primitive” acoelomates. Now, both phyla are regarded as members of the Lophotrochozoa, a very large “super-phylum” that also includes annelids, brachiopods, bryozoans, mollusks, and several other protostomes.

The first report of a marine worm (thought to be a nemertean) was in 1555 when Olaus Magnus (1490–1557) noted an individual that was apparently “40 cubits” or 17.8 meters (58.3 feet) long. In 1758, William Borlase (1696–1772) mentioned a “sea long worm,” and in 1770, Johan Ernst Gunnerus (1718–1773) provided a description of this organism, which he named Ascaris longissima. Its proper current name, the bootlace worm (Lineus longissimus), was first used in 1821 by James De Carle Sowerby (1787–1871). The phylum Nemertea was named by German microscopist Max Johann Sigismund Schultze (1825–1874) in 1851.

Nemertean worms are ribbon-shaped, bilaterally symmetrical worms that are usually less than twenty centimeters (7.9 inches) long, although a few reach several meters in length. For example, L. longissimus is the longest animal in the world, reaching fifty-four meters in length, yet it is only five to ten millimeters in width. Coloration of ribbon worms ranges from dull or pallid to brightly colored yellow, red, orange, or green. Another species of interest is Emplectonema neesii, common around the coasts of Great Britain and Ireland, where it is found beneath stones and boulders, in rock crevices and fissures, among the holdfasts of Laminaria kelp, and in the byssus threads of Mytilus mussel colonies. In addition, Parborlasia corrugatus lives in marine environments down to 3,590 meters (11,780 feet). It is a scavenger and predator that is widely distributed in southern oceans.

The general body plan of ribbon worms is very similar to that of turbellarians. They exhibit bilateral symmetry and have a body shape that is cylindrical anteriorly yet flattened posteriorly. The body of a ribbon worm is triploblastic, meaning they have three layers of tissue (endoderm, mesoderm, and ectoderm). Ribbon worms have an epidermis with external cilia to help them move, as well as specialized gland cells. In addition, ribbon worms possess a complete digestive system (i.e., mouth, foregut, stomach, and intestine with an anus at the tip of their tail). Although the rhynchocoel is a true coelomic cavity, its unusual position and function as part of the proboscis mechanism has lead many to question whether it is homologous to the coelom of other protostomes. Ribbon worms have a nervous system that usually consists of a four-lobed brain with ganglia positioned around the rhynchocoel and connected to paired longitudinal nerve trunks or, in some, middorsal and midventral trunks. Most ribbon worms have chemoreceptors and ocelli that detect light but cannot form actual images. Movement in some species is by muscular peristalsis using powerful muscles, while others use the proboscis to pull themselves forward. Their excretory system has two coiled canals that are branched with specialized flame cells to filter out soluble waste products. While ribbon worms respire through the skin and thus have no respiratory system, they are the simplest animals to possess a closed-loop blood-vascular system without a heart but with two or three longitudinal trunks.

Ribbon worms differ from traditional flatworms in their reproductive system. Most ribbon worms are dioecious (meaning that the male and female sexual organs are in separate individuals), and fertilization is external. However, a few are hermaphroditic, some have internal fertilization, and some even have ovoviviparous development. There are also planuliform (free-swimming, flattened, ciliated, bilaterally symmetric larval form) and pilidium (free-swimming hat-shaped) larvae in some species. The pilidium larva develops from an initial simple ciliated larva and is variable in shape depending on species. It has a domed body with a tuft of sensory cilia sprouting from the top of the apical plate. The young nemertean worm develops within the pilidium, which continues to feed. Development is completed when the mature ribbon worm breaks out, often feeding on the remnants of the pilidium.

The favorite prey items of nemerteans are annelids (segmented worms), clams, crustaceans, and other small invertebrates. Most nemerteans are voracious carnivores, a few species are scavengers, and a few species live commensally inside the mantle cavity of mollusks. In addition, some species have devastated commercial fishing of clams and crabs. Indeed, a few are specialized egg predators on brachyuran crabs and, in high numbers, can consume all the offspring in their host’s clutch. Nemerteans have few predators due to their skin’s secretion of toxins, though some crabs have been observed cleaning captured nemerteans with one claw before eating them. Other predators include some sea birds and even other nemerteans, though some bottom-feeding fish also consume nemerteans, most notably the American Cerebratulus lacteus and the South African Polybrachiorhynchus dayi (both called “tapeworms” in their respective localities), which are sold as fish bait.

Some species have well-developed chemical senses and appear to detect prey items only when they physically contact the prey, while others are capable of tracking prey when it is detected. Nemerteans seize them with a proboscis that lies in an anterior cavity of its own, the rhynchocoel, which lies above the alimentary tract but is not connected to it. The proboscis is a long, blind muscular tube that opens at the anterior end at a proboscis pore above the mouth. Muscular pressure on fluid in the rhynchocoel causes the long, tubular proboscis to be everted rapidly through the proboscis pore. When the proboscis is everted, a sharp barb, the stylet, is exposed; however, some do not have a stylet. The sticky, slime-covered proboscis coils around the prey and stabs it with the stylet, while pouring a toxic secretion on the prey. This neurotoxin has been identified as tetrodotoxin, which is the same poison as occurs in the puffer fish. The prey is drawn near the mouth and swallowed whole as the nemertean retracts the proboscis.

As noted above, while most nemerteans inhabit marine waters, a few occur in moist soil and in freshwater environments. Prostoma rubrum (twenty millimeters or less in length) is the most well-known enoplid freshwater species. In marine habitats, most nemerteans can be found under stones at low tide often coiled up, while at high tide they are thought to be most active as predators on small invertebrates. Other marine nemerteans live in empty mollusk shells or among seaweeds. Life span has been reported in one species Paranemertes peregrina at about eighteen months. Interestingly, this species also feeds on annelids and has the ability to follow the prey’s mucus trails.

The phylogenetic position of nemerteans is open to debate. The type of development is controversial, as is the nemertean body plan. Zoologists are not sure whether nemerteans are acoeolomate (lacking a cavity between the body wall and digestive tract) or coelomate (having a body cavity with a complete lining). The rhynchocoel is an internal cavity lined by mesoderm that forms by schizocoely, making it a true coelom; however, a typical coelom forms a fluid-filled cavity around the digestive tract. Instead, the rhynchocoel lies above the digestive tract and extends about three-quarters the length of the body from the anterior end. It is important to note that the rhynchocoel differs from a typical coelom in both function and position. Typically, a coelom surrounds, cushions, and protects the gut, but it also forms part of the hydrostatic skeleton and stiffens when the surrounding muscles contract. A rhynchocoel is fluid-filled and surrounded by muscles, and muscular contraction increases hydrostatic pressure and eventually everts the proboscis. Whether the coelom and the rhynchocoel are homologous structures is a question that will continue to be debated by scientists.

The first report of ribbon worms (Prostoma sp.) from Arkansas was the collection of fifteen specimens in 2011 from the Ouachita River in Montgomery County. These individuals were collected in the main river from a shallow riffle area vegetated by the aquatic plant Podostemum ceratophyllum in water with swift current 25.4 to 38.1 centimeters (10 to 15 inches) deep. Eight voucher specimens subsequently sent to Harvard University for specific identification using molecular analyses revealed that the haplotypes were all identical to a particular haplotype that has been seen from all over the United States and Australia. Thus, it is a widespread and easily dispersing species, common in many habitats. It was also suggested that the name be currently listed in GenBank as Prostoma cf. eilhardi. In addition, ribbon worms have also been previously reported from the adjacent states of Oklahoma and Louisiana.

For additional information:

Davison, Paul, Henry W. Robison, and Chris T. McAllister. “First Record of Ribbon Worms (Nemertea: Tetrastemmatidae: Prostoma) from Arkansas.” Journal of the Arkansas Academy of Science 68 (2014): 146–148. Online at http://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1237&context=jaas (accessed August 28, 2018).

Gibson, Ray. “Nemertean Genera and Species of the World: An Annotated Checklist of Original Names and Description Citations, Synonyms, Current Taxonomic Status, Habitats and Recorded Zoogeographic Distribution.” Journal of Natural History 29 (1995): 271–561.

Gibson, Ray, and J. Moore. “Freshwater Nemerteans.” Zoological Journal of the Linnean Society 58 (1976): 177–218.

Harmann, W. J. “A Freshwater Nemertine from Louisiana.” Proceedings of the Louisiana Academy of Science 25 (1962): 32–34.

Harrell, R. C. “Benthic Macroinvertebrates of the Otter Creek Drainage Basin, Northcentral Oklahoma.” Southwestern Naturalist 14 (1969): 231–248.

Hickman, Cleveland P., Jr., Larry S. Roberts, Susan L. Keen, David J. Eisenhour, Allan Larson, and Helen I’Anson. Integrated Principles of Zoology. 17^th ed. New York: McGraw-Hill, Inc., 2014.

Maslakova, Svetlana A. “The Invention of the Pilidium Larva in an Otherwise Perfectly Good Spiralian Phylum Nemertea.” Integrative and Comparative Biology 50 (2010): 734–743.

McDermott, J., and Pamela Roe. “Food, Feeding Behavior and Feeding Ecology of Nemerteans.” American Zoologist 25 (1985): 113–125.

Podsladlowski, L., A. Braband, T. H. Struck, J. von Doehren, and T. Bartolomaeus. “Phylogeny and Mitochondrial Gene Order in Lophotrochozoa in the Light of New Mitogenomic Data from Nemertea.” BMC Genomics 10: 364–377.

Schockaert, E. R. Turbellarians. In Methods for the Examination of Organismal Diversity in Soils and Sediments, edited by G. S. Hall. Wallingsford, UK: CAB International, 1996.

Sundberg, P., and R. Gibson. “Global Diversity of Nemerteans (Nemertea) in Freshwater.” Hydrobiologia 595 (2008): 61–66.

Thollesson, Mikael, and Jon L. Norenburg. “Ribbon Worm Relationships: A Phylogeny of the Phylum Nemertea.” Proceedings of the Royal Society B 270 (2003): 407–415.

Turbeville, J. M. “Progress in Nemertean Biology: Development and Phylogeny.”Integrative and Comparative Biology 42 (2005): 692–703.

Henry W. Robison
Sherwood, Arkansas

Chris T. McAllister
Eastern Oklahoma State College