Pentastomida

Pentastomida Temporal range: Cambrian Stage 3–Recent PreЄ Є O S D C P T J K Pg N
Adult female Linguatula serrata
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Subphylum:	Crustacea
Class:	Maxillopoda
Subclass:	Pentastomida Diesing, 1836
Orders
Cephalobaenida Porocephalida Raillietiellida Reighardiida

Pentastomida are an enigmatic group of parasitic invertebrates commonly known as tongue worms due to the resemblance of the species of the genus Linguatula to a vertebrate tongue.

There are about 130 extant species of pentastomids; all are obligate parasites with correspondingly degenerate anatomy. Adult tongue worms vary from about 1 to 14 centimetres (0.4 to 5.5 in) in length, and parasitise the respiratory tracts of vertebrates. They have five anterior appendages. One is the mouth; the others are two pairs of hooks which they use to attach to the host. This arrangement led to their scientific name, meaning "five openings", but although the appendages are similar in some species, only one is a mouth.

Alternative names for the Pentastomida include Pentastoma (strictly a genus name), Linguatulida, and Acanthotheca.

Biology

Historically significant accounts of tongue worm biology and systematics include early work by Josef Aloys Frölich,^[1] Alexander von Humboldt,^[2] Karl Asmund Rudolphi,^[3] Karl Moriz Diesing^[4] and Rudolph Leuckart.^[5]

Other important summaries have been published by Louis Westenra Sambon,^[6] Richard Heymons^[7] and John Riley,^[8] and a review of their evolutionary relationships with a bibliography up to 1969 was published by J. T. Self.^[9]

Anatomy

Pentastomids are worm-like animals ranging from 2 to 13 centimetres (0.79 to 5.12 in) in length. The anterior end of the body bears five protuberances, four of which are clawed legs, while the fifth bears the mouth. The body is segmented and covered in a chitinous cuticle. The digestive tract is simple and tubular, since the animal feeds entirely on blood, although the mouth is somewhat modified as a muscular pump.^[10]

The nervous system is similar to that of other arthropods, including a ventral nerve cord with ganglia in each segment. Although the body contains a haemocoel, there are no circulatory, respiratory, or excretory organs.^[10]

Life cycle

Pentastomids live in the upper respiratory tract of reptiles, birds, and mammals, where they lay eggs. They are gonochoric (having 2 sexes), and employ internal fertilisation. The eggs are either coughed out by the host or leave the host body through the digestive system. The eggs are then ingested by an intermediate host, which is commonly either a fish or a small herbivorous mammal.^[10]

The larva hatches in the intermediate host and breaks through the wall of the intestine. It then forms a cyst in the intermediate host's body. The larva is initially rounded in form, with four or six short legs, but moults several times to achieve the adult form. The pentastomid reaches the main host when the intermediate host is eaten by the main host, and crawls into the respiratory tract from the oesophagus.^[10]

Human infestation

Extraction of an Armillifer grandis nymph from a human eye.

Tongue worms occasionally parasitise humans.^[11] While there is a report of Sebekia inducing dermatitis,^[12][13] the two genera responsible for most internal human infestation are Linguatula and Armillifer. Visceral pentastomiasis can be caused by Linguatula serrata, Armillifer armillatus, Armillifer moniliformis, Armillifer grandis, and Porocephalus crotali.^[14]

The terms associated with infections can vary:

• Linguatula disease can be called linguatuliasis or linguatulosis.
• Porocephalus disease can be called porocephaliasis or porocephalosis.
• Armillifer disease can also be called porocephalosis.^[15] (An alternate name for Armillifer moniliformis is Porocephalus moniliformis.)^[16]
• "Pentastomiasis" can refer to any infection of Pentastomida.

Porocephalus and Armillifer (which are all cylindrical and all inhabit snakes) have much more in common with each other than they do with Linguatula (which is flat and inhabits dogs and wolves.)

Affinities

The affinities of tongue worms have long proved controversial. Historically, they were initially compared to various groups of parasitic worms. Once the arthropod-like nature of their cuticle was recognised, similarities were drawn with mites,^[17] particularly gall mites (Eriophyidae). Although gall mites are much smaller than tongue worms they also have a long, segmented body and only two pairs of legs. Later work drew comparisons with millipedes and centipedes (Myriapoda), with velvet worms (Onychophora) and water bears (Tardigrada). Some authors interpreted tongue worms as essentially intermediate between annelids and arthropods, while others suggested that they deserved a phylum of their own. Tongue worms grow by moulting, which suggests they belong to Ecdysozoa, while other work has identified the arthropod-like nature of their larvae,^[18] In general, there are two current alternative interpretations: pentastomids are highly modified and parasitic crustaceans, probably related to fish lice, or they are an ancient group of stem-arthropods, close to the origins of Arthropoda.

Crustaceans

The possibility that tongue worms are crustaceans can be traced back to the work of Pierre-Joseph Van Beneden,^[19] who compared them to parasitic copepods. The modern form of this hypothesis dates from Karl Georg Wingstrand's study of sperm morphology,^[20] which recognised similarities in sperm structure between tongue worms and fish lice (Argulidae) – a group of maxillipod crustaceans which live as parasites on fish and occasionally amphibians. John Riley and colleagues also offered a detailed justification for the inclusion of the tongue worms among the crustaceans.^[21] The fish louse model received significant further support from the molecular work of Lawrence G. Abele and colleagues.^[22] A number of subsequent molecular phylogenies have corroborated these results,^[23][24][25] and the name Ichthyostraca has been proposed for a (Pentastomida + Branchiura) clade.^[26] Thus a number of important standard works and databases on crustaceans now include the pentastomids as members of this group.^[27]

Stem-arthropods

Critics of the Ichthyostraca hypothesis have pointed out that even parasitic crustaceans can still be recognised as crustaceans based on their larvae; but that tongue worms and their larvae do not express typical characters for Crustacea or even Euarthropoda. An alternative model notes the extremely ancient Cambrian origins of these animals and interprets tongue worms as stem-group arthropods.^[28] A recent morphological analysis recovered Pentastomida outside the arthropods, as sister group to a clade including nematodes, priapulids and similar ecdyzoan 'worm' groups.^[29] Adding fossils, they suggested an extinct animal called Facivermis could be closely related to tongue worms. However it should be stressed that these authors did not explicitly test pentastomid/crustacean relationships.

Fossil record

Exceptionally preserved, three-dimensional and phosphatised fossils from the Upper Cambrian Orsten of Sweden^[30] and the Cambrian/Ordovician boundary of Canada^[31] have been identified as pentastomids. Four fossil genera have been identified so far: Aengapentastomum, Bockelericambria, Haffnericambria and Heymonsicambria. These fossils suggest that pentastomids evolved very early and raise questions about whether these animals were parasites at this time, and if so, on which hosts. Conodonts have sometimes been mentioned as possible hosts in this context.^[31]

Classification

This article follows Martin and Davis^[27] in placing Pentastomida in the class Maxillopoda within the subphylum Crustacea. The subclass contains the following extant orders, superfamilies, families, genera and species:^[32]

Armillifer armillatus Wyman, 1848, a 4 cm individual collected from the respiratory system of a python, Python sebae. Specimen deposited in the Museum für Naturkunde Berlin

Female (right) and male (left) Armillifer sp.

• Cephalobaenida Heymons, 1935

• Cephalobaenidae Heymons, 1922

• Cephalobaena Heymons, 1922

• Cephalobaena tetrapoda Heymons, 1922

• Porocephalida

• Linguatuloidea

• Linguatulidae Haldeman, 1851

• Linguatula Frölich, 1789

• Linguatula arctica Riley, Haugerud & Nilssen, 1987
• Linguatula multiannulata Haffner & Rack in Haffner, Rack & Sachs, 1969
• Linguatula recurvata (Diesing, 1850)
• Linguatula serrata Frölich, 1789

• Neolinguatula Haffner & Rack in Haffner, Rack & Sachs, 1969

• Neolinguatula nuttalli (Sambon, 1922)

• Subtriquetridae Fain, 1961

• Subtriquetra Sambon, 1922

• Subtriquetra megacephalum (Baird, 1853)
• Subtriquetra rileyi Junker, Boomker & Booyse, 1998
• Subtriquetra shipleyi Hett, 1924
• Subtriquetra subtriquetra (Diesing, 1836)

• Porocephaloidea

• Porocephalidae Sambon, 1922

• Armillifer Sambon, 1922

• Armillifer aborealis Riley & Self, 1981
• Armillifer agkistrodontis Self & Kuntz, 1966
• Armillifer armillatus (Wyman, 1845)
• Armillifer australis Heymons, 1935
• Armillifer grandis (Hett, 1915)
• Armillifer mazzai (Sambon, 1922)
• Armillifer moniliformis (Diesing, 1836)
• Armillifer yoshidai Kishida, 1928

• Cubirea Kishida, 1928

• Cubirea annulata (Baird, 1853)
• Cubirea pomeroyi (Woodland, 1921)

• Elenia Heymons, 1932

• Elenia australis Heymons, 1932

• Gigliolella Chabaud & Choquet, 1954

• Gigliolella brumpti (Giglioli, 1922)

• Kiricephalus Sambon, 1922

• Kiricephalus clelii Riley & Self, 1980
• Kiricephalus coarctatus (Diesing, 1850)
• Kiricephalus constrictor Riley & Self, 1980
• Kiricephalus gabonensis Riley & Self, 1980
• Kiricephalus pattoni (Stephens, 1908)
• Kiricephalus tortus (Shipley, 1898)

• Parasambonia Stunkard & Gandal, 1968

• Parasambonia bridgesi Stunkard & Gandal, 1968
• Parasambonia minor Riley & Self, 1982

• Porocephalus Humboldt, 1812

• Porocephalus basiliscus Riley & Self, 1979
• Porocephalus benoiti Fain, 1960
• Porocephalus bifurcatus
• Porocephalus clavatus (Wyman, 1845)
• Porocephalus crotali Humboldt, 1812
• Porocephalus dominicana Riley & Walters, 1980
• Porocephalus stilesi Sambon in Vaney & Sambon, 1910
• Porocephalus subuliferum (Leuckart, 1860)
• Porocephalus taiwana Qiu, Ma, Fan & Lu, 2005
• Porocephalus tortugensis Riley & Self, 1979

• Waddycephalus Sambon, 1922

• Waddycephalus calligaster Riley & Self, 1981
• Waddycephalus komodoensis Riley & Self, 1981
• Waddycephalus longicauda Riley & Self, 1981
• Waddycephalus porphyriacus Riley & Self, 1981
• Waddycephalus punctulatus Riley & Self, 1981
• Waddycephalus radiata Riley & Self, 1981
• Waddycephalus scutata Riley & Self, 1981
• Waddycephalus superbus Riley & Self, 1981
• Waddycephalus teretiusculus (Baird, 1862)
• Waddycephalus vitiensis Heymons, 1932

• Sebekidae Sambon, 1922

• Alofia Giglioli in Sambon, 1922

• Alofia ginae Giglioli in Sambon, 1922
• Alofia indica (von Linstow, 1906)
• Alofia merki Giglioli 'in Sambon, 1922
• Alofia nilotici Riley & Huchzermeyer, 1995
• Alofia parva Riley & Huchzermeyer, 1995
• Alofia platycephalum (Lohrmann, 1889)
• Alofia simpsoni Riley, 1994
• Alofia travassosi (Heymons, 1932)

• Diesingia Sambon, 1922

• Diesingia kachugensis (Shipley, 1910)
• Diesingia megastomum (Diesing, 1836)

• Selfia Riley, 1994

• Selfia porosus Riley, 1994

• Leiperia Sambon, 1922

• Leiperia australiensis Riley & Huchzermeyer, 1996
• Leiperia cincinnalis (Sambon in Vaney & Sambon, 1910)
• Leiperia gracilis (Diesing, 1836)

• Sambonia Noc & Giglioli, 1922

• Sambonia clavata (Lohrmann, 1889)
• Sambonia parapodum Self & Kuntz, 1966
• Sambonia solomenensis (Self & Kuntz, 1957)
• Sambonia varani (Self & Kuntz, 1957)
• Sambonia wardi (Sambon in Vaney & Sambon, 1910)

• Agema Riley et al., 1997

• Agema silvaepalustris Riley et al., 1997

• Pelonia Junker & Boomker, 2002

• Pelonia africana Junker & Boomker, 2002

• Sebekia Sambon, 1922

• Sebekia cesarisi Giglioli in Sambon, 1922
• Sebekia divestei Giglioli in Sambon, 1922
• Sebekia johnstoni Riley, Spratt & Winch, 1990
• Sebekia microhamus Self & Rego, 1985
• Sebekia minor (Wedl, 1861)
• Sebekia mississippiensis Overstreet, Self & Vliet, 1985
• Sebekia multiannulata Riley, Spratt & Winch, 1990
• Sebekia novaeguineae Riley, Spratt & Winch, 1990
• Sebekia okavangoensis Riley & Huchzermeyer, 1995
• Sebekia oxycephalum (Diesing, 1836)
• Sebekia purdieae Riley, Spratt & Winch, 1990
• Sebekia trinitatis Riley, Spratt & Winch, 1990

• Raillietiellida Almeida & Christoffersen, 1999

• Raillietiellidae Sambon, 1922

• Raillietiella Sambon, 1910

• Raillietiella aegypti Ali, Riley & Self, 1982
• Raillietiella affinis Bovien, 1927
• Raillietiella agcoi Tubangui & Masiluñgan, 1936
• Raillietiella ampanihyensis Gretillat, Brygoo & Domergue, 1962
• Raillietiella amphiboluri Mahon, 1954
• Raillietiella belohaensis McAllister, Riley, Freed & Freed, 1993
• Raillietiella bicaudata Heymons & Vitzthum, 1935
• Raillietiella boulengeri (Vaney & Sambon, 1910)
• Raillietiella bufonis Ali, Riley & Self, 1982
• Raillietiella cartagenensis Ali, Riley & Self, 1985
• Raillietiella chamaeleonis Gretillat & Brygoo, 1959
• Raillietiella colubrilineati (Leuckart, 1860)
• Raillietiella congolensis Fain, 1961
• Raillietiella crotali Ali, Riley & Self, 1984
• Raillietiella freitasi (Motta & Gomes, 1968)
• Raillietiella furcocercum (Diesing, 1836)
• Raillietiella gehyrae Bovien, 1927
• Raillietiella gigliolii Hett, 1924
• Raillietiella gowrii Rajalu & Rajendran, 1970
• Raillietiella hebitihamata Self & Kuntz, 1960
• Raillietiella hemidactyli Hett, 1934
• Raillietiella indica Gedoelst, 1921
• Raillietiella kochi Heymons, 1926
• Raillietiella mabuiae Heymons, 1922
• Raillietiella maculatus Rao & Hiregaudar, 1962
• Raillietiella maculilabris Ali, Riley & Self, 1984
• Raillietiella madagascariensis McAllister et al., 1993
• Raillietiella mediterranea (Hett, 1915)
• Raillietiella monarchus Ali, Riley & Self, 1984
• Raillietiella morenoi Abreu-Acosta et al., 2006
• Raillietiella mottae Almeida, Freire & Lopes, 2008
• Raillietiella namibiensis Riley & Heideman 1998
• Raillietiella orientalis (Hett, 1915)
• Raillietiella piscator Nair, 1967
• Raillietiella rileyi Krishnasamy et al., 1995
• Raillietiella schoutedeni Fain, 1960
• Raillietiella scincoides Ali, Riley & Self, 1984
• Raillietiella spiralis Hett, 1924
• Raillietiella teagueselfi Riley, McAllister & Freed, 1988
• Raillietiella tetrapoda (Gretillat, Brygoo & Domergue, 1962)
• Raillietiella trachea Riley, Oaks & Gilbert, 2003
• Raillietiella venteli (Motta, 1965)

• Yelirella Spratt, 2010

• Yelirella petauri (Spratt, 2010)

• Reighardiida Almeida & Christoffersen, 1999

• Reighardiidae Heymons, 1926

• Hispania Martínez et al., 2004

• Hispania vulturis Martínez et al., 2004

• Reighardia Ward, 1899

• Reighardia lomviae Dyck, 1975
• Reighardia sternae (Diesing, 1864)

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• M.L. Christoffersen 1, J.E. De Assis, A systematic monograph of the Recent Pentastomida, with a compilation of their host; Zoologische Mededelingen, 87 (March 2013)