Acanthocephala

(Thorny headed worms)

Phylum Acanthocephala

Number of families 22

Thumbnail description
Parasitic thorny headed worms with complex life cycles; sexes separated; adults found in intestines of vertebrates (definitive host), larvae found in hemocoel (body cavity) of arthropods (intermediate hosts) and sometimes in body cavities of vertebrates (paratenic or transport hosts)

Evolution and systematics

As with most soft-bodied parasites, no fossil record of acanthocephalans is known. However, prehistoric human coprolites at archeological sites in the United States and Brazil have revealed infections by acanthocephalans. Additionally, some 9,000-year-old animal coprolites also from Brazil have been found to contain acanthocephalan eggs. The phylum Acanthocephala is divided into 3 major taxonomic groups: the Archiacanthocephala, Eoacanthocephala, and Palaeacanthocephala, which are considered by some to be classes and others to be orders. A fourth group, the Polyacanthocephala, has been proposed but its status is controversial. Taxonomic groups are based on morphological characters of the worms as well as their hosts' taxonomy and ecology, and such division is supported by molecular data. Molecular, morphological, and ultrastructural analysis of 18S ribosomal DNA sequences has revealed that acanthocephalans and their closest living relatives, members of the phylum Retifera, should be in one clade—referred to as the Syndermata. Acanthocephalans include 22 families and about 1,000 species.

Physical characteristics

Adults are cylindrical or slightly flattened worms that are usually white or colorless; however, some species may be yellow, brown, red, or orange. Acanthocephalans are never segmented, although some species exhibit superficial pseudosegmentation. As adults acanthocephalans measure from less than an inch (a few millimeters) to more than 24 in (60 cm) in length, with the archiacanthocephalans being the largest ones. These worms are sexually dimorphic with females usually larger than males. Structurally, the worms may be divided into three body regions: a proboscis, a neck, and a trunk. The proboscis harbors hooks that may be arranged either in rows or longitudinal lines depending upon the species. Some species harbor an apical organ at the tip of the proboscis that is presumably sensory. The proboscis invaginates into a proboscis receptacle hanging into the anterior part of the trunk. The neck is unarmed but may show lateral organs that may be involved in sensory perception. The trunk may or may not be armed with spines whose distribution is an important criterion for species identification. Acanthocephalans are pseudocoelomate with a syncitial tegument within which runs a lacunar system (an interconnected fluid-filled network of cavities). These worms also have hollow tubular muscles and lemnisci (sac-like structures hanging from the base of the neck into the pseudocoel) that are connected to the proboscis lacunar system. Unique features of acanthocephalan genitalia are a uterine bell in females and cement glands, the organ of Saefftigen, and the copulatory bursa in males. Both males and females have a cerebral ganglion in the proboscis receptacle, and males have genital ganglia and a bursal ganglion. All internal organs are derived from a ligament running down the center of the pseudocoel.

Distribution

Acanthocephalans are found throughout the world, including in fish at deep-sea hydrothermal vents.

Habitat

Adults are intestinal parasites of mammals, birds, fishes, amphibians, and reptiles. Larvae develop in the hemocoel of mandibulate arthropods (crustaceans, myriapods, and insects).

Behavior

Acanthocephalans usually occupy precise niches within the intestines of their definitive hosts. However, some species have been shown to migrate along the intestinal tract during the term of infection. Such migration is correlated with both host diet and sexual maturity of the worms. Nothing is known of acanthocephalan behavior and communication, and there is no evidence of chemical attractants being released to assist in mates finding each other within the hosts' digestive tract. However, acanthocephalans are known to modify the behavior of both their definitive host (e.g., to induce giddiness) and intermediate hosts (e.g., to induce positive phototropism or decrease/alter intermediate host evasive responsiveness). Further, some species also selectively alter the coloration of their intermediate hosts. Such alterations are known to favor transmission of acanthocephalan infective stages to their definitive hosts via increasing intermediate host susceptibility to predation. Disruption of definitive host behavior is speculated to affect transmission by altering host distribution and selection of habitat. Because acanthocephalans attach themselves to the intestinal wall of their host, they may induce pathology, such as inflammation of the surrounding tissues, perforation of the intestinal wall, peritonitis, enlargement of the intestine, and edema, in their host. Results of infection may be fatal while other cases may appear to be mild; oftentimes, more numerous the worms, the more serious the infection. Further, some acanthocephalans have been shown to disrupt host digestion and energy metabolism, which has been shown to have serious detrimental effects during periods of host stress.

Feeding ecology and diet

Acanthocephalans have no digestive tract but selectively absorb nutrients from the host's intestine across their tegument. However, knowledge in this area is limited and is based on only a few species whose feeding and metabolism have been studied (see below Moniliformis moniliformis). The major substrate for acanthocephalan metabolism is carbohydrate, with ethanol being the main end product. Uptake of monosaccharides appears to involve active transport mechanisms. Some species may store glucose in the proboscis receptacle muscle, and intense labeling of the cytoplasmic core of the hollow muscles following uptake of radiolabled glucose occurs. However, it has not been reported whether this latter area acts as a storage site, or whether it plays a role in distributing nutrients throughout the body. The plasma membrane at the surface of the tegument shows hydrolytic activity and tegumental surface crypts within which various enzymatic activities have been localized. These crypts increase the absorptive surface area and are considered to be extra-cytoplasmic digestive organelles. Various amino acids are known to be absorbed through the tegumental surface, but their role in metabolism is not clear. Routes of absorption also vary according to the amino acid studied. Lipids are absorbed and then stored in the lemnisci, although controversy exists as to whether the primary site of lipid absorption is the body wall or the neck/proboscis region. While large amounts of lipids may be deposited in acanthocephalans, they are not thought to be used in metabolism.

Reproductive biology

Female and male acanthocephalans copulate in the intestine of their vertebrate definitive hosts. Fertilization is internal and it is thought that males initiate copulation. The male bursa, the spines that both males and females may harbor at the very posterior end of their trunks, as well as the "cement" (mucilaginous and proteinaceous material) discharged from the male's cement gland(s), all appear to play a role in strengthening the copulatory union. Cement plugs/caps are often observed at the posterior extremities of females, although the role of these plugs is still under discussion. The favored hypothesis is that the cap, which lasts a few days, prevents the loss of injected sperm and further prevents sperm from competing males to enter the female. Cement plugs are also often observed on males, which may serve to prevent male competitors from copulating.

Not all acanthocephalans show seasonality in their life cycle, but there are many instances in which they do. When seasonal life cycles exist there is often a direct link to change in host diet, water temperature, and/or the presence of intermediate hosts in the environment. Maturation of acanthocephalans is sometimes correlated to the maturation of their definitive hosts. Females have ovaries that break up into ovarian balls, which in turn produce oocytes. Once fertilized oocytes become eggs, they float freely in the pseudocoel while the larvae within them develops into an acanthor. During larval maturation eggs are sorted via the uterine bell, which returns immature eggs to the pseudocoel while directing mature eggs containing acanthors to the uterus where they are stored until release. Mature eggs are released via a gonopore into the lumen of the host's intestine and are excreted with the feces. Once outside the host, the eggs must be consumed by the intermediate host to assure transmission. The eggs of acanthocephalans are the only free-living stages of the parasites. Eggs have four envelopes (exceptions exist) that are separated by interstices. Although all analyzed acanthocephalan eggs contain keratin in their second shell, other chemical structures exist and differences among palae-, archi-, and eoacanthocephalan shell structure probably reflect differences in the nature of the intermediate hosts among the three groups. Eggs contain the acanthor, which is the infective stage of the parasite for the intermediate hosts. Acanthors harbor at their anterior end a boring structure called the aclid organ, which consists of a pair of "blades." Acanthors of most species are covered with spines that decrease in size posteriorly. Acanthors of some species also exhibit hooks on their anterior part. Once the intermediate host ingests the egg, the acanthor hatches and uses the aclid organ to penetrate the intestinal wall and then develops, often first beneath the intestinal serosa and then in the hemocoel. Development generally lasts several weeks as the acanthor first transforms into the acanthella and then into a cystacanth, which is the infective stage for the definitive host.

With the exception of size and sexual maturity, cystacanths show all the morphological features of an adult. A thin membrane whose origin is still under discussion surrounds the cystacanths of most species and may serve to protect against the invertebrate host's immuno-defense system. Once intermediate hosts carrying cystacanths are ingested by the correct definitive host, the life cycle is completed. Some cycles include paratenic (transport) hosts, which are vertebrates that ingest infected intermediate hosts and within which the larvae do not develop further. Paratenic hosts oftentimes accumulate large numbers of infective cystacanths and may be required to assure that the parasites reach a definitive host that is higher in the food web. In paratenic hosts the cystacanths most often penetrate the intestinal wall and stay in the body cavity. Within these hosts, accumulated cystacanths are usually attached to the intestinal mesenteries, awaiting paratenic host ingestion by an appropriate definitive host. Postcyclic parasitism may also occur when predators of a definitive host ingest adult acanthocephalans and in turn become parasitized themselves. As such, acanthocephalans may be transferred via cannibalism within a definitive host population.

Conservation status

Little is known about the status of most acanthocephalans. Declines, occurrences, or commonality would all be linked directly to the status of the life cycle, i.e., to the presence of all hosts, and can thus be adversely affected by habitat loss/disruption.

Significance to humans

Very few species of acanthocephalans are known to induce acanthocephaliasis in humans. Symptoms such as giddiness, acute abdominal pain, tinnitus, edema, constipation, diarrhea, undernutrition, and underdevelopment have been reported. The disease is fairly rare (only several hundred cases reported) but may be fatal. Humans obtain the parasite by ingesting infected intermediate hosts either accidentally, as part of their regular diet, or for medicinal purposes. In the former case children are most often affected. Eating sashimi (or raw fish in general) may also be a way for humans to become infected with acanthocephalans. Acanthocephalans, particularly those parasitizing fish, are known to selectively accumulate toxic heavy metals, such as lead and cadmium, in extremely high proportion relative to their surrounding host tissues and host environment. Consequently, their potential use in monitoring polluted environments is an active avenue of research.

Species accounts

List of Species

No common name

Moniliformis moniliformis

order

Moniliformida

family

Moniliformidae

taxonomy

Moniliformis moniliformis (Bremser, 1811) Travassos, 1915.

other common names

None known.

physical characteristics

Worm filiform, often coiled, with distinct pseudosegmentation and bead-like appearance when mature. Females: 4–11 in (10–27 cm) long and 0.08 in (2 mm) maximum in width; males:1.6–2 in (4–5 cm) long. Trunk unarmed. Proboscis nearly cylindrical. Twelve longitudinal rows of 7–8 hooks. Eight cement glands.

distribution

Cosmopolitan.

habitat

Definitive hosts: numerous wild rodents, particularly rats, dogs, and cats. Intermediate hosts: beetles and cockroaches. Paratenic hosts: toads and lizards.

behavior

A few weeks post infection: migration of worms from posterior part to anterior half of intestine of definitive host. Optimal attachment site influenced by sugar gradient in host intestine. Several, but not all, species of roaches containing larvae exhibit altered behavior (e.g., decreased evasive responsivness). Altered intermediate host behavior likely increases probability of parasite transfer to definitive host.

feeding ecology and diet

Major sources of energy are host dietary carbohydrates. Man-nose, glucose, fructose, galactose, and starch all known to influence worm growth, longevity, and reproduction. Absorption across tegumental surface. Primary sites of absorption are extra-cytoplasmic crypts opening to the outside via narrow necks and pores. Pinocytotic and enzymatic activity observed within crypts. Cystacanths store large amounts of glycogen that likely act as an energy source during activation and establishment in the definitive host. Little known about lipid metabolism: available evidence indicates larval stages accumulate lipids. Adult dispersion

in host intestine influenced by nature of lipids in host diet. Specific amino acids readily taken up and catabolized; role in energy metabolism still unclear. Site of absorption of amino acids unknown. Both uridine and thymine transported from host lumen but nucleoside transport mechanism not known.

reproductive biology

Adults mature in 5–6 weeks in intestine of definitive host. Hatching of acanthor occurs between 15 minutes and 48 hours post ingestion by intermediate host. Larvae develop into cystacanth in adult roach in about two months at 81°F (27°C).

conservation status

Not threatened. Most likely flourishing because of widespread distribution and abundance of hosts.

significance to humans

Human pathogen. Symptoms include fatigue, tinnitus, and diarrhea.

Giant thorny-headed worm

Macracanthorhynchus hirudinaceus

order

Oligacanthorhynchida

family

Oligacanthorhynchidae

taxonomy

Macracanthorhynchus hirudinaceus (Pallas, 1781) Travassos, 1917.

other common names

None known.

physical characteristics

Very large worms. Females up to 26 in (65 cm) long, 0.32–0.36 in (8–9 mm) at their largest width and ventrally curved. Males up to 4 in (10 cm) long. Body unarmed, grayish brown, with deep grooves on surface. Globular proboscis with six spiral rows of six hooks each. Eight cement glands.

distribution

Cosmopolitan.

habitat

Adults in swine Sus scrofa and other mammals (e.g., fox squirrel [Sciurus niger], eastern mole [Scalopus aquaticus], hyena [Hyaena hyaena], and dog [Canis familiaris]). Thirty-three species of intermediate hosts reported (e.g., the cockroach Periplaneta americana and scarab [Polyphylla rugosa]).

behavior

Causes serious pathology in pigs.

feeding ecology and diet

Little known. Metabolism is likely to be carbohydrate based. Uptake of amino acids via undefined transport mechanisms.

reproductive biology

Immense number of eggs released by each female. Eggs remain viable for up to 3.5 years. Cold temperatures improve egg survival. Larval development in 4–5 months in the intermediate

host. Adult maturity reached in definitive hosts in 70–110 days. Life span: 10–23 months.

conservation status

Not listed by the IUCN.

significance to humans

Most frequent agent of human acanthocephaliasis (macracanthorhynchosis or macracanthorhynchiasis). Symptoms: constipation, abdominal pain, fever, perforation of the intestinal wall. Also economical effect in countries where macracanthorhynchosis causes heavy losses in pig farms.

No common name

Plagiorhynchus cylindraceus

order

Polymorphida

family

Plagiorhynchidae

taxonomy

Plagiorhynchus (Prosthorhynchus) cylindraceus (Goeze, 1782) Schmidt and Kuntz, 1966.

other common names

None known.

physical characteristics

Small worms with elliptical, unarmed, and milky-white body. Females: 0.35–0.60 in (9–15 mm) long. Males 0.32–0.51 in (8–13 mm) long. Cylindrical proboscis with 15–18 longitudinal rows of 11–15 hooks each. Six cement glands.

distribution

Cosmopolitan.

habitat

Definitive hosts: passerine birds such as robins (Turdus migratorius) and starlings (Sturnus vulgaris), although virtually any bird can be infected. Intermediate hosts: terrestrial isopods Armadillidium vulgare and Porcellio scaber. Paratenic hosts: crested anole (Anolis cristatellus) and short-tailed shrew (Blarina brevicauda).

behavior

Behavior of adult worms: not known. Detrimentally affects definitive host metabolism and digestive abilities. Behavior change of infected isopods: found more on white surfaces and low humidity areas than uninfected isopods. Evidence indicates such altered behavior makes them easier prey to bird definitive hosts.

feeding ecology and diet

Nothing is known.

reproductive biology

Development in isopods takes about 60–65 days. Maturity reached within several weeks following ingestion of cystacanths by definitive host.

conservation status

Not threatened. Based upon great diversity of definitive hosts, an unlikely candidate for extinction.

significance to humans

None known. Indirect effect by negatively affecting populations of passerine birds such as mountain bluebirds.

No common name

Pomphorhynchus laevis

order

Echinorhynchida

family

Pomphorhynchidae

taxonomy

Pomphorhynchus laevis (Zoega in O. F. Muller, 1776) Van Cleave, 1924 (nec laeve).

other common names

None known.

physical characteristics

Average-sized worms with a long and cylindrical neck. Neck dilated in its anterior part into the shape of a bulb. Females are 0.5–1.1 in (13–28 mm) long. Males: 0.24–0.63 in (6–16 mm) long. Body unarmed and most often orange. Cylindrical proboscis with 18–20 longitudinal rows of 12–13 hooks each. Short lemnisci. Two testes in tandem. Six cement glands.

distribution

Palaearctic.

habitat

Definitive hosts: numerous freshwater fishes (e.g., sharp-nosed eel (Anguilla vulgaris), common bream (Abramis brama), chub (Leuciscus cephalus), barbel (Barbus barbus), goldfish (Carassius auratus), etc. Intermediate hosts: amphipods: Corophium volutator, Gammarus bergi, G. fossarum, G. lacustris, G. pulex, and Pontagammarus robustoides. Fish for paratenic hosts (e.g., Phoxinus phoxinus).

behavior

Not known. Host dietary carbohydrates likely the major energy source. Adults perforate all layers of intestinal wall with their proboscis and thus never change position in intestine. Infected intermediate hosts exhibit photophilic behavior. Cystacanths bright orange, making infected amphipod intermediate hosts more visible to fish predators.

feeding ecology and diet

Little known. Lipid analysis indicates neck and lemnisci function in lipid absorption and storage.

reproductive biology

Larvae mature in intermediate hosts within several weeks. Gravid females in fish intestine carry immense numbers of eggs. Once released in water, spindle-shaped eggs appear to be diatom-like.

conservation status

Not listed by the IUCN.

significance to humans

Not pathological to humans. Possible economic effect by affecting fingerling development in aquaculture conditions.

Resources

Books

Crompton, D. W. T., and Brent B. Nickol. Biology of the Acanthocephala. Cambridge: Cambridge University Press, 1985.

Moore, Janice. Parasites and the Behavior of Animals. New York and Oxford: Oxford University Press, 2002

Muller, Ralph. Worms and Human Diseases. Cambridge, MA: CABI Publishing, 2002.

Neafie, Ronald C., and Aileen M. Marty. "Acanthocephaliasis." In Pathology of Infectious Diseases, vol.1, Helminthiases, edited by W. M. Meyers. Armed Forces Institute of Pathology, American Registry of Pathology, 2000.

Taraschewski, Horst. "Host-Parasite Interactions in Acanthocephala: A Morphological Approach." In Advances in Parasitology, vol. 46, edited by J. R. Baker, R. Muller, and D. Rollinson. San Diego: Academic Press, 2000.

Periodicals

Garcia-Varela, M., M. P. Cummings, G. Perez-Ponce de Leon, S. L. Gardner, and J. P. Laclette. "Phylogenetic Analysis Based on 18S Ribosomal RNA Gene Sequences Supports the Existence of Class Polyacanthocephala (Acanthocephala)." Molecular Phylogenetics and Evolution 23 (2002): 288–292.

Garcia-Varela, M., G. Perez-Ponce de Leon, P. de la Torre, M. P. Cummings, S. S. S. Sarma, and J. P. Laclette. "Phylogenetic Relationships of Acanthocephala Based on Analysis of 18S Ribosomal RNA Gene Sequences." Journal of Molecular Evolution 50: 532–540.

Golvan, Y. J. "Nomenclature of the Acanthocephala." Research and Reviews in Parasitology 54, no.3 (1994): 135–205.

Goncalves, M. L. C., A. Araujo, and L. F. Ferreira. "Human Intestinal Parasites in the Past: New Findings and a Review." Memorias do Instituto Oswaldo Cruz 98, suppl.1 (2003): 103–118.

Herlyn, H., O. Piskurek, J. Schmitz, U. Ehlers, and H. Zischler. "The Sundermatan Phylogeny and the Evolution of Acanthocephalan Endoparasitism as Inferred from 18S rDNA Sequences." Molecular Phylogenetics and Evolution 26 (2003): 155–164.

Isaure de Buron, PhD

Vincent A. Connors, PhD