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Definition: ACANTHOCEPHALA from A Dictionary of Entomology

Noun. (Greek, akantha = spine + kephale = head. Acanthocephalae.) Spiny-Headed Worms; Thorny-Headed Worms. A Phylum of parasitic worms with taxonomic affinities not clear and whose members demonstrate a complicated life cycle. Adults live in intestinal tract of vertebrate predators; immatures develop within arthropods as intermediate hosts. (Conway & Crompton 1982, Biol. Rev. 57: 85–115.)


Summary Article: Acanthocephala (Thorny-Headed Worms) from Encyclopedia of Life Sciences
Abstract

The Acanthocephala or thorny-headed worms constitute a group of about 1100 species of endoparasites. Sexual maturity occurs in the gut of a vertebrate and development in the body cavity of an arthropod.

keywords

helminths

endoparasitism

Acanthocephala

phylogeny

reproduction

Introduction

Acanthocephalans usually measure a few millimetres in length. Sizes range from Octospiniferoides chandleri at 2 mm to Nephridiacanthus longissimus at 800 mm. There is often sexual dimorphism with females being longer than males and living longer. Usually acanthocephalans are cream or white in colour when alive.

Acanthocephalans rarely infect humans, but occasionally infection with Macracanthorhynchus hirudinaceus, a parasite of swine, is reported from China.

Basic Design

Van Cleave considered that their body plan justified phylum status for the Acanthocephala (see Hyman in the Further Reading for anatomical details). See also Parasitism: Variety of Parasites, and Invertebrate Body Plans

The diagnostic feature is the hook-bearing, retractile proboscis (Figures 1, 2 and 3) which anchors the worm to the intestinal wall of the vertebrate host. The number, arrangement and shape of the proboscis hooks serve to distinguish one species from another. The proboscis, the sac into which it is withdrawn and the paired lemnisci constitute the praesoma while the portion of the body exposed to the host's intestinal lumen is known as the metasoma. Trunk spines, embedded in the metasomal body wall, aid in gripping the gut wall and may assist locomotion.

Proboscis of Macracanthorhynchus ingens from a skunk. Length c.0.6 mm.

Proboscis of Acanthocephalus lucii from a perch. Length 0.7 mm. (Electron micrograph by O. L. Lassiere.)

Proboscis of Neoechinorhynchus rutili from a brown trout. Length c.0.15 mm. (Electron micrograph by O. L. Lassiere.)

Although acanthocephalans have a body cavity (pseudocoelom), they do not possess a gut at any stage of development and are dependent on the host's digestive processes to supply nutrient molecules for absorption across the body surface. Stages in the arthropod host obtain nutrients by tegumental absorption of molecules from the host's body fluid. In the fully developed worm, the body wall contains a network of cavities called the lacunar system which serves as a transport system.

Acanthocephalans are dioecious. Reproductive organs are located in the body cavity supported by the ligament sac or sacs. Male worms possess paired testes and a cement gland or glands. On copulation, the male extrudes a bursa which grips the posterior of the female, spermatozoa are transferred and a copulatory cap of secretions from the cement glands is deposited over the genital area of the female.

In the female, ovarian tissue grows and divides so that by maturity the body cavity contains numerous free-floating ovarian balls. Each ovarian ball consists of an oogonial syncytium giving rise to mature oocytes and a supporting syncytium providing nutritional and mechanical underpinning for the germ cells and zygotes. Fertilization occurs in the ovarian ball, zygotes develop there until they are shed into the body cavity where embryogenesis is completed. Female acanthocephalans possess a uterine bell which sorts the varying stages of developing eggs. Fully formed eggs pass down the uterus to the host's intestine while immature eggs are returned to the body cavity. Spermatozoa reach oocytes via the uterus and uterine bell.

The nervous system consists mainly of a cerebral ganglion located in the proboscis sac. In Moniliformis moniliformis, a parasite of rats, this ganglion measures about 160 × 130 × 100 μm and contains 88 cells. Nerves extend from the cerebral ganglion to the proboscis and the ventral and dorsal sides of the metasomal body wall. Males contain a genital ganglion of from 15 to 40 cells, assumed to be associated with copulatory behaviour. See also Invertebrate Nervous Systems

Distinct excretory organs are usually lacking and excretion occurs across the body wall. A few species possess protonephridia or nephridia which are assumed to have an excretory function.

Three major taxa are recognized in the Acanthocephala:

  • Archiacanthocephala (Figure 1) - trunk spines absent, usually eight cement glands, usually single muscle layer in the proboscis sheath, dorsal and ventral ligament sacs, thick egg shells, some species possess nephridia, large body size, infect terrestrial vertebrates and insects (occasionally millipedes).

  • Palaeacanthocephala (Figure 2) - trunk spines present or absent, two to eight cement glands, usually two muscle layers in the proboscis sheath, single ligament sac which ruptures, thin egg shells, nephridia absent, variable body size, infect mainly aquatic and some terrestrial vertebrates and crustaceans.

  • Eoacanthocephala (Figure 3) - trunk spines present or absent, usually one cement gland, single muscle layer in the proboscis sheath, initially dorsal and ventral ligament sacs, thin egg shells, small, infect aquatic vertebrates and crustaceans.

Diversity and Lifestyles

The life cycle begins with the discharge of eggs (Figures 4 and 5) from the definitive host into the environment of the intermediate host. On ingestion by an arthropod, an acanthor larva (Figure 6) emerges from the egg shell, crosses the gut wall and enters the body cavity. During development, the rate of which is determined by ambient temperature, the acanthor is transformed through acanthella stages to the cystacanth stage, which is infective to a definitive host. Inside the intermediate host, the parasite becomes enclosed in an envelope which protects it from the host's cellular defence responses. In the case of Polymorphus minutus, waterfowl acquire the parasite by eating Gammarus pulex (Crustacea, Amphipoda) containing cystacanths which take from 60 to 150 days to develop at 17°C and 10°C respectively. In the duck, with a body temperature of 41-42°C, the prepatent period (maturation, copulation, first egg release) lasts for 17 days and the patent period (egg production) lasts for 22 days. A female Polymorphus minutus produces about 13 000 infective eggs during its life. Moniliformis moniliformis has a fecundity of about 600 000 eggs per female and Macracanthorhynchus hirudinaceus releases over 20 million eggs per female during a year. See also Reproduction and Life Cycles in Invertebrates, Evolutionary Developmental Biology: Environmental Regulation of Normal Development, Immunity to Parasitic Worms, and Coevolution: Parasite-Host

Infective egg (shelled acanthor) of Moniliformis moniliformis from a rat. Length c.100 μm. (Photomicrograph by J. R. Georgi.)

Infective egg (shelled acanthor) of Polymorphus minutus from a duck. Length c.120 μm. (Photomicrograph by J. R. Georgi.)

Many acanthocephalans require a paratenic or transport host which bridges the trophic gap between an arthropod and a predatory vertebrate. In the Baltic Sea, Corynosoma semerme reproduces in ringed seals (Pusa hispida) and develops in amphipods (Pontoporeia affinis). Seals acquire the infection by eating a fish, four-horn sculpin (Myoxocephalus quadricornis), in which the parasites have encysted as a result of its eating the amphipods. Mature acanthocephalans can be transferred from fish to fish through cannibalism and predation. See also Predation (Including Parasites and Disease) and Herbivory

The behaviour of infected arthropods changes significantly once cystacanths are present. Infected arthropods respond differently from uninfected counterparts to various stimuli; their appearance, spatial distribution and community role may change and their chances of being eaten by the next host may be significantly increased.

Fossil History and Phylogeny

Fossilized worms are uncommon and those related to endoparasites are even rarer. There is in the mid-Cambrian deposits of the Burgess Shale from British Columbia, an exquisitely preserved group of fossil priapulid worms. Some of these have the anatomy that had been predicted for the free-living ancestor of an acanthocephalan worm. It is possible to speculate how such a free-living burrowing, scavenging worm could first invade moribund and later lively arthropods and then incorporate fish into its life history. See also Fossil Record, Fossil Record: Quality, and Burgess Shale

Acanthor of Moniliformis moniliformis. Length c.250 μm. (Photomicrograph by R. H. F. Holt.)

However, recent molecular evidence does not support a close link between Acanthocephala and Priapulida. Analysis of 18S rRNA databases suggests instead that the Acanthocephala are a sister group of the Rotifera. Morphological similarities between acanthocephalans and rotifers include the structure of the tegumentary pores, the form of muscle cells and the retractile proboscis. The evolutionary commitment of the Acanthocephala to endoparasitism at all stages of their life history complicates attempts to unravel their origins and phylogeny. See also Molecular Phylogeny Reconstruction, Priapulida, and Rotifera

Further Reading
  • Bryam, JE and Fisher, FM (1974) The absorptive surface of Moniliformis dubius (Acanthocephala) II. Functional aspects. Tissue and Cell 6: 21-42.
  • Conway, Morris S and Crompton, DWT (1982) The origins and evolution of the Acanthocephala. Biological Reviews of the Cambridge Philosophical Society 57: 85-115.
  • Crompton, DWT and Nickol, BB (eds) (1985) Biology of the Acanthocephala. Cambridge: Cambridge University Press.
  • Garey, JR, Near, TJ Nonnemacher, MR and Nadler, SA (1996) Molecular evidence for Acanthocephala as a subtaxon of Rotifera. Journal of Molecular Evolution 43: 287-292.
  • Hyman, LH (1951) The Invertebrates, vol. III. New York: McGraw-Hill.
  • Moore, J (1995) The behaviour of parasitised animals. BioScience 45: 89-96.
  • Uznanski, RL and Nickol, BB (1976) Structure and function of the fibrillar coat of Leptorhynchoides thecatus eggs. Journal of Parasitology 62: 569-573.
  • Van Cleave, HJ (1948) Expanding horizons in the recognition of a phylum. Journal of Parasitology 34: 1-20.
  • Van Cleave, HJ (1953) Acanthocephala of North American Mammals. Illinois Biological Monographs 23: 1-179.
  • Willmer, P (1990) Invertebrate Relationships. Cambridge: Cambridge University Press.
  • DWT Crompton
    University of Glasgow Glasgow, UK
    Wiley ©2007

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