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Acanthocephala

Contributed by: Donald V. Moore

Publication year: 2014

A distinct phylum (or class, according to some classifications) of helminths, the adults of which are parasitic in the alimentary canal of vertebrates. They are commonly known as the spiny-headed worms. The phylum comprises the orders Archiacanthocephala, Palaeacanthocephala, and Eoacanthocephala. Over 500 species have been described from all classes of vertebrates, although more species occur in fish than in birds and mammals and only a relatively few species are found in amphibians and reptiles. The geographical distribution of acanthocephalans is worldwide, but genera and species do not have a uniform distribution because some species are confined to limited geographic areas. Host specificity is well established in some species, whereas others exhibit a wide range of host tolerance. The same species never occurs normally, as an adult, in cold-blooded and warm-blooded definitive hosts. More species occur in fish than any other vertebrate; however, Acanthocephala have not been reported from elasmobranch fish. The fact that larval development occurs in arthropods gives support to the postulation that the ancestors of Acanthocephala were parasites of primitive arthropods during or before the Cambrian Period and became parasites of vertebrates as this group arose and utilized arthropods for food. See also: ARCHIACANTHOCEPHALA ; EOACANTHOCEPHALA ; PALAEACANTHOCEPHALA .

Morphology

Adults of various species show great diversity in size, ranging in length from 0.04 in. (1 mm) in some species found in fish to over 16 in. (400 mm) in some mammalian species ( Fig. 1 ). Most of the larger species are from mammals; however, some mammalian forms are relatively small ( Corynosoma ) even though they parasitize seals and whales. When observed undisturbed in the intestine, the elongate body is distinctly flattened, but on removal to water or saline and after preservation the body becomes cylindrical. Living worms are translucent or milky white, although they may take on a distinctive color from the intestinal contents. The body of both sexes has three divisions: the proboscis armed with hooks, spines, or both; an unspined neck; and the posterior trunk.

Proboscis

The proboscis is the primary organ for attachment of Acanthocephala to the intestinal wall of the host. In some species, the proboscis is parallel with the main axis of the body, but frequently it is inclined ventrally. The proboscis may be globular, or elongate and cylindrical, in shape and is invariably armed with sharp pointed hooks, spines, or both (Fig. 1). These structures vary in shape and number and are usually arranged radially or in spiral rows. Electron microscopy studies have revealed that proboscis hooks consist of a central core of AccessScience from McGraw-Hill Education Page 2 of 10 www.accessscience.com

ImageFig. 1 Variousof 1 acanthocephalan examples, adult forms drawn to same scale. ( a ) Moniliformis dubius , 4–12 in. (10–30 cm) long. ( b ) Proboscis of same. ( c ) Macracanthorhynchus hirudinaceus , 10–24 in. (25–60 cm) long. ( d ) Proboscis of same. ( e ) Oncicola canis , 0.5–0.8 in. (1–2 cm) long. ( f ) Proboscis of same. ( After A. C. Chandler and C. P. Read , Introduction to Parasitology , 10th ed ., Wiley , 1961 )

ImageFig. 2 Diagrams of 2 showing mechanics of proboscis attachment of Neoechinorhynchus emydis in intestinal wall of a turtle. ( a ) Proboscis fully introverted. ( b ) Most basal hooks in contact with host tissue. ( c–e ) Progr essive stages in extroversion of the proboscis. ( After H. J. Van Cleave, Experimental Parasitology, vol. 1, 1952 )

cytoplasm covered by hard nonliving material. In species with an elongate proboscis, the hooks seem to be in longitudinal rows with a quincuncial arrangement.

In most species, the proboscis is capable of introversion into a saclike structure, the proboscis receptacle. When in this position, the tips of the hooks are all directed anteriorly and are on the inside of the introverted proboscis.

As the proboscis is everted and extended, these hooks engage the mucosa of the host’s intestine, with the tips turning posteriorly as they reach their functional position on the exterior of the proboscis. The recurved points of the hooks anchor the worm firmly to the intestinal wall ( Fig. 2 ). The proboscis receptacle and neck can be retracted into the body cavity, but without inversion.

Within the anterior end of the trunk are found the proboscis receptacle; musculature for retracting the proboscis, receptacle, and neck; and the lemnisci ( Fig. 3 ). The proboscis receptacle is attached to the inner surface of the AccessScience from McGraw-Hill Education Page 3 of 10 www.accessscience.com

ImageFig. 3 Anteriorof 3 end of Moniliformis dubius.

proboscis. Muscles known as inverters of the proboscis are attached to the anterior tip of this structure and pass through the proboscis and receptacle, emerging from the posterior of the receptacle, and continue some distance posteriorly, where they attach to the trunk wall. Usually one inverter is attached dorsally and one ventrally. Contraction of the inverter fibers introverts the proboscis into the receptacle, while further contraction of these fibers pulls the receptacle deep into the body cavity.

Body wall

Electron microscopy studies show that the body wall is covered by a thin mucopolysaccharide known as the epicuticle secreted onto the surface of the worm. Beneath the epicuticle is the thin cuticle with an outer membrane and a homogeneous layer perforated by numerous pores of canals, which pass through the striped layer beneath. Many of the canals are filled with an electron-dense material. Below the striped layer is the felt layer composed of many fibrous strands extending in various directions. Mitochondria and numerous vesicles are present in the felt layer. Some vesicles seem to be connected to the canals of the striped layer. The radial layer beneath the felt layer contains fewer fibrous strands, large thin-walled lacunar channels with mitochondria arranged around the channels. Lipids and glycogen are present in the radial layer. Circular and longitudinal muscle layers are found beneath the radial layer separated by plasma membranes. Some investigators consider all body-wall layers beneath the stripped layer as hypodermis.

Giant nuclei

The wall of the trunk has an external cuticula beneath which lies the thick syncytial hypodermis, or subcuticula.

The hypodermis contains a relatively small number of giant nuclei, which may be round, oval, ameboid, or elongate with a number of lateral branches ( Fig. 4 ).

Lacunae

Within the hypodermis is a series of intercommunicating spaces, the lacunar system. Usually the lacunar system is composed of two longitudinal vessels either dorsal and ventral or ventral and lateral. In some species, only the AccessScience from McGraw-Hill Education Page 4 of 10 www.accessscience.com

ImageFig. 4 Crossof 4 sections showing body plans of acanthocephalans. ( a ) Palaeacanthocephalan. ( b ) Archiacanthocephalan. ( After L. H. Hyman, The Invertebrates, vol. 3, McGraw-Hill, 1951 )

ImageFig. 5 Lacunarof 5 system of Moniliformis , dorsal view, showing regular circular branches. ( After L. H. Hyman, The Invertebrates, vol. 3, McGraw-Hill, 1951 )

dorsal vessel is present. The longitudinal vessels are connected by a series of smaller vessels, the lacunae, which ramify throughout the body. In species exhibiting pseudosegmentation ( Moniliformis ), the regularly spaced lateral lacunae and the body musculature divide the wall into transverse folds ( Fig. 5 ). These folds have no effect on the arrangement of internal organs.

Pseudocoele

The body cavity, or pseudocoele, contains all the internal organs, the most conspicuous of which are the reproductive organs enclosed in axial connective-tissue ligament sacs. These ligament sacs are hollow tubes that extend most of the length of the cavity of the trunk. They are single in both males and females of the

Palaeacanthocephala, but are divided into dorsal and ventral sacs that communicate anteriorly in females of the other orders. There is no vestige of a digestive system in any stage of the life cycle. AccessScience from McGraw-Hill Education Page 5 of 10 www.accessscience.com

Reproductive system

The reproductive organs of the male consist of a pair of testes and specialized cells, the cement glands. In most species, there is a saclike structure behind the cement glands, Saefftigen’s pouch, through which run the sperm ducts and the ducts from the cement glands ( Fig. 6 a ). The products of the testes and cement glands are discharged through a penis, which is surrounded by a posteriorly located bell-shaped copulatory bursa, which is usually introverted into the posterior extremity of the trunk. At copulation, the bursa is extended and applied to the posterior extremity of the female, where it is held firmly in place by the secretions of the cement glands. This material hardens, forming a copulatory cap on the female, which is an internal cast of the bursa of the male, and remains attached to the posterior extremity of the female for some time following copulation.

Female Acanthocephala are unique in that the ovary exists as a distinct organ only in the very early stages of development and later breaks up to form free-floating egg balls. The eggs are fertilized as they are released from the egg balls and are retained within the ligament sacs until embryonation is complete. The genital orifice is posterior. A vagina provided with a strong sphincter extends anteriorly from the orifice and a saccular uterus is anterior to the vagina. The anterior end of the uterus is surrounded by a series of guard cells, the selective apparatus. From this extends a funnel-like structure, the uterine bell, the broad anterior end of which opens into the body cavity or one of the ligament sacs holding the developing eggs (Fig. 6 b ). During embryonation in the body cavity, the eggs acquire a series of membranes and a hard outer shell. Eggs which have not completed embryonation are passed back into the body cavity through special openings in the selective apparatus, whereas eggs which are fully mature are passed into the saccular uterus and eliminated through the vaginal sphincter and genital orifice into the intestinal contents of the host.

Lemnisci

The trunk and presoma are demarcated by an infolding of the cuticula and the presence of two elongate contractile structures, the lemnisci, which arise from the hypodermis and extend posteriorly into the body cavity.

The lemnisci are provided with a definite number of nuclei which migrate from the hypodermis into the lemnisci as they are formed during larval development. The function of the lemnisci is unknown. One explanation offered for their function is that they act as reservoirs for the fluid of the lacunar system when the presoma and proboscis are invaginated.

Nervous system

The nervous system is composed of a chief ganglion or brain located within the proboscis receptacle. Most of the nerve trunks are inconspicuous, but two of them, the retinacula, associated with muscle fibers, pass through the wall of the proboscis receptacle to innervate the trunk wall. AccessScience from McGraw-Hill Education Page 6 of 10 www.accessscience.com

ImageFig. 6 Reproductiveof 6 system of Moniliformis dubius. ( a ) Posterior end of male. ( b ) Posterior end of female. ( After A. C. Chandler and C. P. Read, Introduction to Parasitology, 10th ed., Wiley, 1961 )

Excretory system

In members of the Archiacanthocephala, modified protonephridial organs are found closely adherent to the reproductive system. However, in most species, specialized excretory organs are completely lacking. The protonephridial organs consist of a mass of flame bulbs attached to a common stem. The canals unite to form a single canal, which joins the sperm duct in the male and the uterus in the female. AccessScience from McGraw-Hill Education Page 7 of 10 www.accessscience.com

Embryology

The Acanthocephala are obligatory parasites throughout their entire life cycle; no known member of this phylum exists as a free-living organism.

Acanthor

The eggs passed in the feces of the host contain a mature embryo, the acanthor, which is surrounded by three membranes ( Fig. 7 a ). The life cycle always involves an intermediate host, which is usually an arthropod. Among these are small crustaceans for parasites of aquatic vertebrates, and grubs, roaches, and grasshoppers for those which parasitize terrestrial vertebrates. The eggs hatch after being ingested by the appropriate arthropod and release the spindle-shaped acanthor, which has a spiny body and is armed with retractile bladelike rostellar hooks used in the penetration of the intestinal wall of the intermediate host (Fig. 7 b ). The central portion of the body of the acanthor contains a column of dense undifferentiated nuclei, the entoblast, from which develop the structures of the ensuing stages. After penetration of the wall of the digestive tract, the acanthor comes to lie beneath the delimiting membrane of the gut wall, becomes quiescent, and begins to grow (Fig. 7 c ). It soon drops free into the host’s hemocoele, where it undergoes a gradual transformation into the various larval stages (Fig. 7 d and e ).

Acanthella

The term acanthella is applied to the series of stages in which the rudiments of the reproductive organs, lemnisci, proboscis, and proboscis receptacle are formed (Fig. 7 f ). As development progresses, the acanthella becomes elongate, and is surrounded by a hyaline cyst produced by the larva.

Cystacanth

When the proboscis and the proboscis receptacle of the acanthella develop to the point of retractility, the larva becomes infective and is known as the cystacanth (Fig. 7 g and h ). The mature or infective cystacanth lies in the hemocoele of the intermediate host with the proboscis and receptacle retracted into the body cavity. The body cavity of the cystacanth contains all of the structures of the adult worm in an immature form.

In the least complicated life cycle, the cystacanth remains in the hemocoele of the arthropod until it is ingested by a suitable vertebrate host, in which it excysts and attaches to the intestinal wall by the proboscis and grows to sexual maturity. In some forms, the life cycle may be prolonged and complicated by the introduction of one or more transport hosts, usually a vertebrate, in which the cystacanth becomes established as a visceral cyst awaiting ingestion by a suitable vertebrate host in which sexual maturity can be attained. AccessScience from McGraw-Hill Education Page 8 of 10 www.accessscience.com

ImageFig. 7 Lifeof 7 history of Moniliformis dubius. ( a ) Mature egg containing acanthor. ( b ) Acanthor in process of escaping from egg shells and membranes. ( c ) Acanthor dissected from gut wall tissue of Periplaneta americana 5 days after infection. ( d ) Median sagittal section of larva removed from the body cavity of P. americana 29 days after infection. ( e ) Larva removed from body cavity of P. americana 42 days after infection. ( f ) Acanthella dissected from its enveloping sheath. ( g ) Encysted cystacanth from body cavity of P. americana with proboscis invaginated. ( h ) Cystacanth freed from its cyst and with proboscis evaginated. AccessScience from McGraw-Hill Education Page 9 of 10 www.accessscience.com

Cell constancy

The somatic tissues of Acanthocephala are made up of a restricted number of nuclei, which is more or less fixed for each tissue. This condition is termed cell constancy or more correctly eutely or nuclear constancy, because the majority of acanthocephalan tissues are syncytial in nature. The nuclei of the early embryonic cells that are destined to become syncytial in nature are large, regular, and spheroidal or elliptical in shape. During the transformation of the acanthella into the cystacanth, the nuclei begin to assume the shape and form of the hypodermal nuclei seen in the adult by passing through an integrated series of ovoid, rosette, ameboid, elongate with lateral branches, and arboroid or dendritic forms. These diverse expressions of nuclear shape and modifications are instrumental in maintaining a favorable ratio between nuclear surface and surrounding cytoplasm. At the conclusion of the cleavage process, the embryo, or acanthor, contains all of the cellular elements of the adult. No mitotic divisions take place, although in the rearrangement of nuclei during larval development certain nuclei may undergo amitotic divisions. The extent of the metamorphoses of the embryonic cells and nuclei varies greatly in the different groups and genera. In the more highly specialized genera, the nuclei of the embryo lose all of their original appearance during larval development. In contrast, the nuclei of the adults of the less specialized genera retain the distinctive embryonic nuclei with little change. Varying changes, intermediate between these two extremes, are observed in other groups. See also: CELL CONSTANCY .

Physiology

Since acanthocephalans lack a gut, they undoubtedly obtain nutrients through the metasomal surface from material in the host’s intestinal lumen. The role of the pores in this process is not really known, but it is likely that absorption of nutrients is facilitated by the increased surface area resulting from the plasma membrane lining the pores. It has been suggested that digestion may take place in the region of the presoma, which is in continuous contact with the host tissue. In this area, digestive enzymes are believed to be membrane-bound, allowing products of digestion to be absorbed at the host-parasite interface.

Acanthocephalans contain large quantities of glycogen and in general have a pronounced carbohydrate metabolism. Glycogen is localized in the proboscis, body wall, and muscles. They appear to utilize the

Embden-Meyerhoff scheme of phosphorylating glycolysis. Chief waste products of carbohydrate metabolism in

Moniliformis dubius are succinic, lactic, formic, and acetic acids, along with large quantities of ethanol. It has been suggested that the end products of carbohydrate metabolism excreted by acanthocephalans may be metabolized by the host or may be effective in preventing other helminths from establishing in that area of the host’s intestine. See also: CARBOHYDRATE METABOLISM ; GLYCOGEN .

A significant Krebs cycle has not been demonstrated in acanthocephalans, but evidence indicates that it may be partially operative in some species. Pyruvate or phosphoenolpyruvate formed from glucose by glycolysis may be carboxylated to form malate, which is reduced via fumarate to form succinate. The reduction of fumarate could AccessScience from McGraw-Hill Education Page 10 of 10 www.accessscience.com

result in reoxidation of hydrogenated nicotinamide adenine dinucleotide (NADH) under anaerobic conditions, allowing glycolysis and synthesis of adenosine triphosphate (ATP) to be maintained. See also: CITRIC ACID CYCLE .

Donald V. Moore

Bibliography

T. Dunagan and D. Miller, Acanthocephala, pp. 299–332, in F. W. Harrison (ed.), Microscopic Anatomy of

Invertebrates , vol. 4, Wiley-Liss, New York, 1991

G. L. Hoffman,

C. R. Kennedy,

T. J. Near, Acanthocephalan phylogeny and the evolution of parasitism, Integr. Comp. Biol. , 42:668–677, 2002

DOI: http://doi.org/10.1093/icb/42.3.668

D. W. Thomasson Crompton and B. B. Nickol (eds.),

Additional Readings

C. T. Atkinson, N. J. Thomas, and D. B. Hunter, Parasitic Diseases of Wild Birds , Wiley-Blackwell, Hoboken, NJ,

2012

L. Margulis and M. J. Chapman, Kingdoms and Domains: An Illustrated Guide to the Phyla of Life on Earth , 4th ed., Elsevier - Academic Press, Boston, 2010