Nematoda

George Poinar, Jr, Oregon State University, Corvallis, Oregon, USA

The Nematoda are a group of non-segmented worm-like invertebrates that occur worldwide in a wide range of habitats.

Introductory article
Article Contents
. Introduction . Basic Design . Diversity . Habitats and Abundance

Introduction
The Nematoda is a phylum comprised of invertebrates commonly known as roundworms lacking true segments and appendages. They are worldwide in distribution and occur in a wide range of habitats. While many are freeliving with activities inconsequential to humans, others parasitize plants and animals, including humans, and are of economic importance. The rst reported human parasite (Ascaris) dates from the Papyrus Ebers around 1550 bc. Discovery of the smaller soil, plant and invertebrate parasites occurred much later, in the seventeenth and eighteenth centuries, after the microscope was invented. While the majority of nematode species still await discovery, most of the species attacking humans, domestic animals and crop plants have been identied and studied. Several species of free-living nematodes (especially Caenorhabditis elegans) have been used experimentally to study cell development and have contributed greatly to our understanding of the molecular organization of metazoans.

. Habits and Life Histories . Fossil History . Phylogeny

Basic Design
Nematodes are non-segmented, worm-like invertebrates which lack jointed appendages and possess a complete digestive tract at least during one stage in their development. They possess a body cavity usually described as a pseudocoelom, but lack specialized respiratory and circulatory systems and (unusually) have no circular muscles. They do possess a nervous system, excretory system and longitudinal muscles. Nematodes are bilateral animals with a trid three-angled pharynx, circumpharyngeal nerve ring, copulatory spicules in the male (with few exceptions) and one or two tubular gonads opening at the vulva in the female and into the rectum (forming a cloaca) in the male. The exterior wall of all nematodes is composed of a non-cellular, exible, multilayered structure called the cuticle. This semipermeable layer is secreted by underlying rows of hypodermal cells whose nuclei are arranged in rows termed hypodermal cords located between the muscle elds. The hypodermal cords also contain the somatic nerve cords, and the excretory canals in some nematodes, and can serve as storage sites for lipids and glycogen, since

there are no specialized fat cells in nematodes (for a schematic illustration of nematode anatomy, see Figure 1.). Nematode movement is snake-like and controlled by the contractions of alternating rows of longitudinal muscles running the length of the body. Most nematodes crawl on their sides but some of the aquatic forms can swim by rapid vibratory side-to-side movements of the body. All nematodes at some stage contain a continuous alimentary tract composed of a mouth, stoma, pharynx, intestine and anus. The excretory system occurs in two basic forms. One consists of a renette cell, connected to a duct leading to an excretory pore which opens near the head end on the ventral side of the animal. The second type consists of one or two longitudinal excretory canals located in the hypodermal cords which then connect to the excretory duct and pore. The excretory system may also play an osmoregulatory role by removing water from the body cavity. The majority of nematodes are aerobic although many can survive for short periods under anaerobic conditions. Nematodes absorb and release gases by simple diusion across the body surface. The nervous system consists of a central brain or nerve ring, which is a collection of ganglionic cells and bres circling the pharynx in the anterior portion of the animal. From this centre, nerves run anteriorly and posteriorly to innervate the body tissues, as well as sensory organs. Nematodes have a wide range of reproductive strategies. While most reproduce by amphimixis (sperm and eggs originate in separate individuals), autotoky or uniparent reproduction also occurs. The latter can be represented by hermaphroditism, where the sperm and egg mature and combine in the same individual, or by parthenogenesis, where the egg matures without the presence of sperm. Perhaps the most curious reproduction occurs in the insect parasite Heterogonema, where after mating with the female, the male produces eggs in its body, fertilizes its own eggs and dies as the young break out through his body wall.

Diversity
While over 15 000 species of nematodes have been described, estimates place the number of actual species in
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parasite of the sperm whale and reaches some 8 metres in length. While most nematodes are quite small, many of the vertebrate parasites can be detected easily, which explains why the rst nematode recorded (around 1550 bc ) was a human intestinal parasite. While their size can greatly vary, their body plan remains remarkably conservative. There is no complete agreement regarding the higher classication of nematodes. Normally, the phylum is divided into two classes, the Adenophorea and the Secernentea, with the former containing the majority of the free-living marine and freshwater forms and the latter the majority of the animal parasites. Most authorities cite from 16 to 20 orders and some 200 families of nematodes in their system of classication.

Habitats and Abundance

Nematodes occur in a variety of habitats. The majority of individuals occur in the marine and soil environments. A number also frequent fresh water and these can be collected from stream beds and lake bottoms. Special habitats include hot springs, arctic ice packs, and subterranean caves. Then there are the plant parasites which feed on a wide variety of trees, shrubs and herbs. Other groups parasitize both vertebrates (Figure 2) and invertebrates (Figure 3). The groups that cause damage to crops, humans and livestock have been most studied because of the need to control them. Benecial nematodes include those that attack pest insects and other invertebrates, and several species are presently being sold by commercial companies.

Habits and Life Histories

Nematodes can be arranged in either ecological or nutritional categories. Most nematodes found in soil can be placed in the ecological group of free-living nematodes. Other ecological categories include those intimately associated with plants, invertebrates and vertebrates. Nutritional categories include the microbotrophic nematodes that utilize bacteria and other microorganisms as a source of nourishment; the predaceous forms that attack micro-invertebrates in the environment; those that obtain nourishment from plants; and others that parasitize invertebrates and vertebrates. The plant parasites are equipped with an anteriorly placed stylet or micro-syringe to transfer cell sap into their alimentary tract. Plant parasites may be ectoparasites, feeding on plant roots from the outside, or endoparasites, which enter the tissues and then either remain sedentary or migrate through the plant. The main result of injury by plant nematodes is yellowing, wilting and stunting of plants. Some plant parasitic nematodes are able to vector plant viruses. Approximately 10% of agricultural crops are

Figure 1 Basic anatomy of nematodes as illustrated by a female (left) and male (right) of Rhabditis sp., a secernentean, microbotrophic nematode of the family Rhabditidae, order Rhabditida. A, anus; B, bursa; B.b, basal bulb of pharynx; C, corpus of pharynx; E, egg; E.p, excretory pore; G, gubernaculum; I, intestine; N, nerve ring; O, ovary; R, rectum; R.g., rectal gland; S, spicule; Sp, sperm; St, stoma; T, testis; U, uterus; V, vulva; Va, vagina; V.d, vas deferens.

the phylum at over 500 000. Many nematodes are microscopic in size and are rarely observed. The smallest is a free-living marine species that reaches only 82 mm in length. On the other hand, the largest nematode is a
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Figure 2 Adults of Ascaris lumbricoides removed from a child who died as a result of the infection. This nematode was the first to be recorded around 1550 BC.

destroyed annually by nematodes, resulting in the largescale use of nematicides, which is the only current practical method of control. Nematodes also have a wide range of associations, including phoresis and facultative and obligate parasitism, with invertebrates. Some of the insect-parasitic Mermithidae (Figure 3) cause external morphological modications of their hosts, resulting in intersexes (host shows both male and female characters) or intercastes (hosts show characters of two castes, such as ants with characters of both queens and workers). Many vertebrate parasites require an invertebrate intermediate host in which the parasite develops from rst to third juvenile, which is then the infective stage for the nal vertebrate host. Two genera of nematodes, Steinernema and Heterorhabditis, are commercially sold for controlling a variety of pest insects. The insecticidal features of these nematodes reside in symbiotic bacteria which are carried in the alimentary tracts of the infective stages and released when they enter the body cavity of insect hosts. Some six nematode orders contain vertebrate parasites. Many vertebrates are susceptible to a range of nematodes. For instance, over 40 dierent nematode species have been reported from dogs, and over 35 from humans worldwide.

Figure 3 Long, white coils of a mermithid nematode that developed inside the body cavity of a spider. The host died after the nematode exited.

Most human deaths, amounting to tens of thousands each year, occur from infections with Ascaris (Figure 2), Onchocerca and hookworms. Perhaps the most common human nematode parasites in Western cultures are pinworms, often found in children. The nematodes occur in the rectum of their victims and deposit sticky eggs in the peranal area that adhere to toilet seats and reinfect others. Most marine nematodes are microbotrophic, feeding on bacteria, fungi and algae, but amongst them are the freeliving stages of parasites whose developmental stages occur in a wide range of marine invertebrates and vertebrates. All nematodes pass through six stages in their development, including an egg, rst stage juvenile (sometimes the term larva is used for the immature stages of nematodes, but since that term indicates some type of morphological change to the adult state beyond the fully developed sexual organs, juvenile is the preferred term), second stage juvenile, third stage juvenile, fourth stage juvenile and adult. Moults separate each juvenile stage from the preceding stage. Sometimes one or even two moults occur
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within the egg. Often one of the cast skins is retained around the succeeding juvenile stage. This is especially common with infective stages of animal parasites. Usually the second stage cuticle is retained as a protective sheath around the third stage infective juvenile, which then searches for a potential host. These infective stages normally do not feed or grow and can be regarded as resistant stages. Resistant stages are common in nematodes found in soil but are unknown in aquatic nematodes and seem to have developed as a means of survival under conditions of low moisture. All nematodes require some degree of moisture during their developmental stages since they are susceptible to desiccation. Some soil and plant parasitic nematodes possess stages (adult or juvenile) that can enter anhydrobiosis and withstand desiccation, sometimes surviving for decades. In some animal parasites, the eggs are quite resistant to desiccation and in these cases, they are usually the infective stage in the life cycle. Nematodes are attacked by a variety of multicellular predators and suer diseases caused by bacteria, protozoa, fungi and viruses.

lecida, Enolpida and Dorylaimida. The latter group also radiated onto land, where they developed lines predaceous on other soil invertebrates as well as parasitic on plants and in terrestrial invertebrates and vertebrates. A second branch developed into the Secernentea group, which consisted of the basic terrestrial lineage Rhabditida. This in turn produced lines that evolved into the plant and invertebrate parasites (Tylenchida and Aphelenchida) and the vertebrate parasites (Strongylida, Spirurida, Ascaridida and Oxyurida).

Phylogeny
While the nematodes are an obviously ancient group, there has been considerable diversity of opinion concerning their phylogeny. More recent theories suggest that nematodes are allied with other pseudocoelomate groups within the Aschelminthes; perhaps they arose from the Gastrotricha although they share similarities with the Nematomorpha. Recently molecular techniques have been used to show relationships between nematode species and genera and hopefully will reveal a natural classication of the higher categories as well. There are characters that relate nematodes to a number of other invertebrate groups but there are reasons why the Nematoda are an ancient group with no direct relationship to any other now in existence.

Fossil History
The oldest undisputed nematode fossil is preserved inside its y host in Lebanese amber from the Lower Cretaceous (120135 million years ago). Amber (fossilized resin) contains the clearest remains of fossil insect parasitic, plant parasitic and free-living microbotrophic nematodes. The most recent fossils are prehistoric nds of nematodes associated with vertebrates, including humans. Strongyles have been recovered from the intestines of Upper Pleistocene horses and encysted juveniles of Trichinella have been recovered from the Egyptian mummy, Nakht, dated at about 1200 bc . Nematodes have also been recovered from 3000-year-old human coprolites from Lovelock Cave in Nevada, USA. Nematodes as a group are undoubtedly much older than the oldest fossils indicate and probably evolved in the Cambrian or Precambrian with free-living microbotrophic forms that fed on bacteria in aquatic or semi-aquatic habitats. These early nematodes formed one branch (the Adenophora) that continued to develop in the marine habitat and gave rise to the Monhysterida, Desmodorida, Chromadorida, Descosco-

Further Reading
Chitwood BG and Chitwood MB (1974) Introduction to Nematology. Baltimore, Maryland: University Park Press. Dropkin VH (1980) Introduction to Plant Nematology. New York: John Wiley & Sons. Grasse PP (1965) Traite de Zoologie, Tome IV, Nemathelminthes (Nematodes). Paris: Masson et Cie, Fasc. 2 and 3. Levine ND (1968) Nematode Parasites of Domestic Animals and of Man. Minneapolis, MN: Burgess Publishing. Poinar, Jr GO (1975) Entomogenous Nematodes. A Manual and Host List of Insect Nematode Associations. Leiden: EJ Brill. Poinar Jr GO (1983) The Natural History of Nematodes. Englewood Clis, New Jersey: Prentice-Hall. Thorne G (1961) Principles of Nematology. New York: McGraw-Hill. Yamaguti S (1961) Systema Helminthum, vol. III. The Nematodes of Vertebrates. Parts 1 and 2. New York: Interscience Publishers, Inc. Zuckerman BM, Mai WF and Rohde RA (eds) (1971) Plant Parasitic Nematodes, vols. 1 and 2. New York: Academic Press.

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net