Pentastomes

The phylum Pentastomida (some consider it a class) includes four orders, seven families, and about 144 species, including eight extinct species from the Paleozoic Era. They are wormlike obligate parasites, meaning that they cannot complete their life cycle without a host. As adults, they inhabit the respiratory tract (lungs and nasal passages) of vertebrates. Four species are known from intermediate host insects (three coprophagus cockroaches and one coleopteran). In addition, fishes are common intermediate hosts for pentastomes occurring in crocodilians and piscivorous chelonians, and rarely for some species of snakes. Definitive hosts include amphibians (few hosts) but mainly reptiles (lizards, snakes, freshwater turtles, and crocodilians), the latter making up about seventy percent of hosts. The most common genera of reptilian pentastomes are Armillifer, Kiricephalus, Porocephalus, Raillietiella, and Sebekia, with the majority found as adults in lungs of snakes, lizards, and crocodilians. There are two species found in the air sacs of sea birds (gulls, terns, skuas, guillemots, and puffins) and another in the trachea of white-backed vultures. One species infects the nasopharynx of canines and felids. They infect humans, but rarely; therefore, pentastomids are of some medical importance. The only reported case of pentastomes in Arkansas was P. crotali in the liver of a raccoon from Van Buren County. However, there is a scarcity of published reports on pentastomes in Arkansas, and more research is needed to determine the diversity of pentastomid species within the state.

Evolutionarily speaking, relationships of pentastomids are in a state of flux as they share characters with the phylum Annelida, but most evidence suggests that members of the phylum Arthropoda are more closely related. Some researchers have even suggested that the Pentastomida be regarded as an order of the crustacean class Branchiura, while others essentially agree that pentastomids be deemed a subclass of Crustacea (Pancrustacea), closely allied with the Branchiura. Using morphological characters as well as molecular techniques (18S rRNA sequences) suggests retaining the Pentastomida as a separate phylum, although some recommend supporting their inclusion in the Crustacea. Therefore, pentastomids may be most closely related to branchiuran lice, which are ectoparasites on fish.

Apparently, the first to report a pentastomid was the eminent French veterinarian Philibert Chabert (1737–1814). In 1787, he discovered a “worm” in the nasal cavities of dogs and horses, which he mistook for the tapeworm Ténia lancéolé. Pioneer descriptions and further efforts to understand the pentastomids were made during the next century by Josef Aloys von Frölich (1789), Alexander von Humboldt (1812), Pierre-Joseph van Beneden (1849), and Karl Moritz Diesing (1850), culminating with the 1860 account of the Linguatula by C. G. F. Rudolph Leuckart. More recent significant works were written by Richard Heymons (1867–1943) of the Berlin Museum, J. Teague Self (1906–1995) of the University of Oklahoma, and John Riley of the University of Dundee, Scotland.

Pentastomids possess an elongate-tapered cuticular (chitinous) body showing distinct segmentation, forming numerous annuli (ring-shaped structures). The body is divided into an anterior forebody and posterior hindbody, which is bifurcated at its tip in some species. One prominent characteristic of pentastomids is the presence of two pairs of sclerotized hooks in the mouth region, which can be withdrawn into cuticular pockets. In some species, the hook articulates against a basal fulcrum and is manipulated by strong muscles to tear and embed its mouth into host tissues. The digestive system is simple and complete, with the anus opening at the posterior end of the abdomen. Adult pentastomids feed on tissue fluids and blood cells of their host. The nervous system is similar to that of arthropods.

Pentastomids are dioecious (having distinct males and females) and exhibit sexual dimorphism, as females are usually larger than males; they range in size from a few millimeters to fifteen centimeters in length. Males have a single, tubular testis; however, there are two in the genus Linguatula. The testis is continual with a seminal vesicle, which, in turn, connects to a pair of ejaculatory organs. The genital pore of the male is mid-ventral on the anterior abdominal segment, approaching the mouth.

Female pentastomids possess a single ovary that extends almost the entire length of the body cavity and may bifurcate at its distal end to become two oviducts that unite to form the uterus. The uterus terminates as a short vagina that opens through the female gonopore. Females mate only once, while the males may be polygamous. Females are capable of producing several million fully embryonated eggs, which pass up from the lungs to the trachea of the host and are then swallowed and passed out with the feces.

In a typical pentastomid life cycle, eggs are ingested by a suitable intermediate host and develop into nymphs that penetrate the intestinal tract and migrate casually to multiple tissues. If the definitive host is a reptile, it ingests the intermediate host containing nymphs that then infect the definitive host by penetrating the stomach or intestine using their hooks. The nymphs end up in the lungs, where they mature. In addition, pentastomid adults containing mature eggs may be expelled from the trachea and eliminated from the definitive host through oral expulsion. These adults may also be swallowed, resulting in shed eggs in the feces. Autoinfection can also occur in some species.

In the most common hosts (reptiles), pentastomes are hematophagous (meaning that they feed on blood), but even in heavily infected lizards or snakes, anemia has not yet been documented. Host death is often associated with larval and nymphal migration and molting, and by pathological damage caused to the pulmonary lining by the hooks and mouths of feeding adults, which often leads to secondary bacterial infection or fungal pneumonia. Mortality associated with progressive pneumonia from infection with adult Raillietiella has been reported in wild gecko lizards located in Nigeria, suggesting that pentastomes may act as regulators of wild reptile populations. Imported wild-caught reptiles in private collections and zoos may also develop overt disease from pentastome infection.

Adult Linguatula serrata is an unusual type of pentastome, as it lives in the nasal passages of mammals, such as dogs, cats, foxes, and other carnivores (rather than in amphibians or reptiles). It also uses other mammals as intermediate hosts. In humans, some pentastomids are zoonotic (meaning that they can be passed between humans and animals). Nasopharyngeal pentastomiasis results when nymphs of L. serrata are eaten by people, with the parasite attempting to attach to the human throat or nasopharynx. In the Old World, it is linked to eating undercooked goat or sheep liver and mesenteric lymph nodes or the visceral organs of sheep, goats, cattle, and camels. Visceral pentastomiasis results when eggs are eaten and nymphs develop in visceral organs, causing pathology such as hepatic granuloma (as was reported in a patient from Michigan). Other complications include abscesses in the auditory canals, facial swelling, paralysis, and even asphyxiation and death. Another unusual infection in humans occurs if Armillifer sp. are found in the liver.

Several pentastomids have been reported from states surrounding Arkansas, including Leiperia gracilis in American alligators (Alligator mississippiensis) from Texas; Porocephalus crotali from Louisiana and Oklahoma viperid snakes; Sebekia mississippiensis in Louisiana, Mississippi, and Texas A. mississippiensis; Sebekia oxycephalum from Louisiana fishes and common snapping turtle (Chelydra serpentina); Linguatula serrata from Oklahoma rabbits; and Raillietiella frenatus and R. teagueselfi in Texas Mediterranean geckos (Hemidactylus turcicus). The only report of pentastomes in Arkansas was a report of a nymphal P. crotali in the liver of a raccoon, Procyon lotor, from Van Buren County. The scarcity of published reports of pentastomes from Arkansas is likely due to a lack of relevant surveys on these parasites of the state. Furthermore, compared to surrounding states, particularly Oklahoma and Texas, it is not known whether Arkansas supports an equal diversity of pentastomid species.

Descriptions of new species of pentastomids have been based on various morphological features of the adult worm, with emphasis placed on body size, number of body annuli, and morphology of the two pairs of retractile hooks, buccal cadre, and the male copulatory spicules. However, due to the small numbers of specimens generally recovered, method of fixation used on those specimens, state of the preserved type or voucher specimens, and intraspecific variation in the previously mentioned morphological traits, there are many misidentifications. Some species erroneously described as new were eventually categorized as species inquirenda. Interestingly, morphological features used in pentastomid taxonomy vary as the parasite goes through different developmental stages in the definitive host, especially the morphology of the hooks, which can transition strikingly and progressively. Indeed, data on hooks can be meaningful only when compared between fully mature specimens. In addition, type specimens in museum collections are usually fixed as permanent mounts in formalin and/or without using DNA-grade ethanol as a preservative. In this regard, specimens cannot be characterized by using molecular techniques, a major issue in resolving the taxonomic status of already described pentastomid species. In the future, taxonomic work may involve a combination of morphological techniques, incorporating a consideration of body size and a quantitative measurement of hook bluntness with complementary molecular techniques to assist in the validation of descriptions of new pentastome species.

For additional information:
Able, Lawrence G., W. Kim, and B. E. Felgenhauer. “Molecular Evidence for Inclusion of the Phylum Pentastomida in the Crustacea.” Molecular Biology and Evolution 6 (1989): 685–691.

Ali, J. H., John Riley, and J. Teague Self. “Amphibians as Definitive Hosts for Pentastomids: Raillietiella bufonis n. sp. from Bufo lemur in Puerto Rico and a Reassessment of Raillietiella indica Gedoelst, 1921.” Systematic Parasitology 4 (1982): 279–284.

———. “Further Observations of Blunt-Hooked Raillietiellids (Pentastomida: Cephalobaenida) from Lizards with Descriptions of Three New Species.” Systematic Parasitology 6 (1984): 147–160.

———. “A Review of the Taxonomy and Systematics of the Pentastomid Genus Raillietiella Sambon, 1910 with a Description of a New Species.” Systematic Parasitology 7 (1985): 111–123.

Boyce, Walter M., and Evelyn A. Kazacos. “Histopathology of Nymphal Pentastomid Infections (Sebekia mississippiensis) in Paratenic Hosts.” Journal of Parasitology 77 (1991): 104–110.

Brookins, M. D., Jim F. X. Welleran Jr., J. F. Roberts, K. Allison, Stephen S. Curran, A. L. Childress, and Ellis C. Greiner. “Massive Visceral Pentastomiasis Caused by Porocephalus crotali in a Dog.” Veterinary Pathology 46 (2009): 460–463.

Christofferson, M. L., and J. E. De Assis. “A Systematic Monograph of the Recent Pentastomida, with a Compilation of Their Hosts.” Zoologiche Mededelingen Leiden 87 (2013): 1–206.

Junker, Kersten, John Riley, and J. Boomker. “Redescription of Diesingia megastoma (Diesing, 1836) Sambon, 1922, a Pentastomid Parasite from the South American Terrapin Hydromedusa tectifera Cope.” Systematic Parasitology 56 (2003): 211–218.

Kelehear, Crystal, David M. Spratt, Sylvain Dubey, Gregory Brown, and Richard Shine. “Using Combined Morphological, Allometric and Molecular Approaches to Identify Species of the Genus Raillietiella (Pentastomida).” PLoS ONE 6 (2011): e24936.

Lavoipierre, M. M. J., and Michéle Lavoipierre. “An Arthropod Intermediate Host of a Pentastomid.” Nature 210 (1966): 845–846.

McAllister, Chris T., Charles R. Bursey, and Paul S. Freed. “Endoparasites (Cestoidea, Nematoda, Pentastomida) of Reptiles (Sauria, Ophidia) from the Republic of Namibia.” Comparative Parasitology 78 (2011): 140–151.

———. “Helminth Parasites (Cestoidea, Nematoda, Pentastomida) of Selected Herpetofauna from Cameroon, West Africa.” Acta Parasitologica 55 (2012): 90–93.

McAllister, Chris T., John Riley, Paul S. Freed, and Deborah A. Freed. “Endoparasites of Some Malagasy Colubrids (Reptilia: Serpentes) with Descriptions of Two New Species of Raillietiella (Pentastomida: Cephalobaenidae).” Transactions of the American Microsopical Society 112 (1993): 35–42.

———. “Raillietiella (Pentastomida: Cephalobaenida) from a Malagasy Chamaeleon, Chamaeleo verrucosus (Sauria: Chamaeleonidae) from Madagascar.” Texas Journal of Science 44 (1992): 492–493.

Poore, G. C. B. “The Nomenclature of the Recent Pentastomida (Crustacea), with a List of Species and Available Names.” Systematic Parasitology 82 (2012): 211–240.

Richardson, Dennis J., Wilber B. Owen, and Daniel E. Snyder. “Helminth Parasites of the Raccoon (Procyon lotor) from North-Central Arkansas.” Journal of Parasitology 78 (1992): 163–166.

Riley, John. “The Biology of Pentastomids.” Advances in Parasitology 25 (1986): 45–128.

———. “An Experimental Investigation of the Development of Porocephalus crotali (Pentastomida: Porocephalida) in the Western Diamond Back Rattlesnake (Crotalus atrox).” International Journal of Parasitology 11 (1981): 127–131.

Riley, John A., A. Banaja, and J. L. James. “The Phylogenetic Relationships of the Pentastomida: The Case for their Inclusion within the Crustacea.” International Journal for Parasitology 8 (1978): 245–254.

Riley, John, Chris T. McAllister, and Paul S. Freed. “Raillietiella teagueselfi n. sp. (Pentastomida: Cephalobaenida) from the Mediterranean Gecko, Hemidactylus turcicus (Sauria: Gekkonidae), in Texas.” Journal of Parasitology 74 (1988): 481–486.

Riley, John, David M. Spratt, and P. J. A. Presidente. “Pentastomids (Arthropoda) Parasitic in Australian Reptiles and Mammals.” Australian Journal of Zoology 33 (1985): 39–53.

Roberts, Larry S., and John Janovy Jr. Foundations of Parasitology. 9th ed. Boston: McGraw-Hill Higher Education, 2012.

Self, J. Teague. “Biological Relationships of the Pentastomida: A Bibliography on the Pentastomida.” Experimental Parasitology 24 (1969): 63–119.

Self, J. Teague, and Robert E. Kuntz. “Host-Parasite Relations in Some Pentastomida.” Journal of Parasitology 53 (1967): 202–206.

Chris T. McAllister
Eastern Oklahoma State College