Pentastomida

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Pentastomida
Temporal range: Wuliuan–Recent
Linguatula.jpg
Adult female Linguatula serrata
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Ichthyostraca
Subclass: Pentastomida
Diesing, 1836
Orders

see text

Synonyms
  • Pentastomata
  • Linguatulida

The Pentastomida are an enigmatic group of parasitic arthropods commonly known as tongue worms due to the resemblance of the species of the genus Linguatula to a vertebrate tongue; molecular studies point to them being highly-derived crustaceans. [1]

Contents

About 130 species of pentastomids are known; all are obligate parasites with correspondingly degenerate anatomy. Adult tongue worms vary from about 1 to 14 cm (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.

Taxonomy

Historically significant accounts of tongue worm biology and systematics include early work by Josef Aloys Frölich, [2] Alexander von Humboldt, [3] Karl Asmund Rudolphi, [4] Karl Moriz Diesing [5] and Rudolph Leuckart. [6]

Other important summaries have been published by Louis Westenra Sambon, [7] Richard Heymons [8] and John Riley, [9] and a review of their evolutionary relationships with a bibliography up to 1969 was published by J. T. Self. [10]

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, [11] 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[ citation needed ] drew comparisons with millipedes and centipedes (Myriapoda), with velvet worms (Onychophora) and water bears (Tardigrada). Some authors[ citation needed ] 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. [12] In general, the two current alternative interpretations are: 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 discovery that tongue worms are crustaceans can be traced back to the work of Pierre-Joseph Van Beneden, [13] who compared them to parasitic copepods. The modern form of this hypothesis dates from Karl Georg Wingstrand's study of sperm morphology, [14] which recognised similarities in sperm structure between tongue worms and fish lice (Argulidae) – a group of maxillopod 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. [15] The fish louse model received significant further support from the molecular work of Lawrence G. Abele and colleagues. [16] A number of subsequent molecular phylogenies have corroborated these results, [17] [18] [19] and the name Ichthyostraca has been proposed for a (Pentastomida + Branchiura) clade. [20] Thus a number of important standard works and databases on crustaceans now include the pentastomids as members of this group. [21]

Stem-arthropods

Critics of the Ichthyostraca classification 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. [22] A recent morphological analysis recovered Pentastomida outside the arthropods, as sister group to a clade including nematodes, priapulids and similar ecdysozoan 'worm' groups. [23] 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 [24] and the Cambrian/Ordovician boundary of Canada [25] have been identified as pentastomids. Also one from the Wuluian (middle Cambrian) of Greenland. [26] Four fossil genera have been identified from the Cambrian so far: Aengapentastomum , Boeckelericambria , Dietericambria , 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 (primitive fish) have sometimes been mentioned as possible hosts in this context. [25] A fifth genus, Invavita , is from Silurian-aged marine strata of England: fossil specimens of Invavita are found firmly attached to their ostracod hosts of the species Nymphatelina gravida. [27] [28] It possessed a head, a worm-like body, and two pairs of limbs. [29]

Classification

There are four extant orders recognised in the subclass Pentastomida:

Description

Pentastomids are worm-like animals ranging from 1 to 14 centimetres (0.39 to 5.51 in) in length. The female is larger than the male. 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, except from genus Linguatula which lives in the nasal cavity of carnivorous mammals where they feed mainly on mucus and dead cells, [30] [31] although the mouth is somewhat modified as a muscular pump. [32]

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, no circulatory, respiratory, or excretory organs are present. [32]

Behaviour and ecology

Armillifer armillatus from a python Pentastomum armillatum.png
Armillifer armillatus from a python

Pentastomids live in the upper respiratory tract of reptiles, birds, and mammals, where they lay eggs. They are gonochoric (having two 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. [32]

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. At least one species, Subtriquetra subtriquetra , has a free-living larva. [33] There is both indirect development with nymphal stages and direct development. 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. [32] [34]

Human infestation

Extraction of an Armillifer grandis nymph from a human eye

Tongue worms occasionally parasitise humans. [35] While a report exists of Sebekia inducing dermatitis, [36] [37] 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 . [38]

Armillifer armillatus Wyman, 1848, a 4 cm individual collected from the respiratory system of a python, Python sebae. Specimen deposited in the Natural History Museum of Berlin. Armillifer armillatus.jpg
Armillifer armillatus Wyman, 1848, a 4 cm individual collected from the respiratory system of a python, Python sebae . Specimen deposited in the Natural History Museum of Berlin.
Female (right) and male (left) Armillifer sp. Armillifer.jpg
Female (right) and male (left) Armillifer sp.

The terms associated with infections can vary:

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).

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<span class="mw-page-title-main">Acanthocephala</span> Group of parasitic thorny-headed worms

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<span class="mw-page-title-main">Lobopodia</span> Group of extinct worm-like animals with legs

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<span class="mw-page-title-main">Copepod</span> Subclass of crustaceans

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<span class="mw-page-title-main">Tantulocarida</span> Subclass of crustaceans

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<span class="mw-page-title-main">Rhizocephala</span> Superorder of barnacles

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<i>Porocephalus crotali</i> Species of crustacean

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<span class="mw-page-title-main">Ichthyostraca</span> Class of parasitic crustaceans

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References

  1. ↑ Lavrov, Dennis V.; Brown, Wesley M.; Boore, Jeffrey L. (7 March 2004). "Phylogenetic position of the Pentastomida and (pan)crustacean relationships". Proceedings of the Royal Society of London. Series B: Biological Sciences. 271 (1538): 537–544. doi:10.1098/rspb.2003.2631. PMC   1691615 . PMID   15129965.
  2. ↑ J. A. Frölich (1789). "Beschreibung einiger neuer Eingeweidewürmer". Der Naturforscher . 24: 101–162.
  3. ↑ A. von Humboldt (1811). "Sur un ver intestin trouvé dans les poumons du serpent à sonnettes, de Cumana". Voyage de Humboldt et Bonpand 2. Ptie. F. Schoell et G. Dufour, Paris. pp. 298–304.
  4. ↑ K. A. Rudolphi (1819). Entozoorum Synopsis. Augustus Rücker Berlin.
  5. ↑ K. M. Diesing (1835). "Versuch einer Monographie der Gattung Pentastoma". Annalen des Wiener Museums der Naturgeschichte. 1: 1–32.
  6. ↑ R. Leuckart (1860). "Bau und Entwicklungsgeschichte der Pentastomen nach Untersuchungen besonders von Pent. taenoides und P. denticulatum". C. F. Winter'sche Verlagshandlung, Leipzig: vi + 160.{{cite journal}}: Cite journal requires |journal= (help)
  7. ↑ L. W. Sambon (1922). "A synopsis of the family Linguatulidae". Journal of Tropical Medicine and Hygiene. 12: 188–206, 391–428.
  8. ↑ R. Heymons (1935). "Pentastomida". In H. G. Bronns (ed.). Klassen und Ordnungen des Tierreichs. Fünfter Band. IV Abteilung, 1. Buch. Leipzig: Akademische Verlagsgesellschaft m.b.H. pp. 1–268 pp.
  9. ↑ J. Riley (1986). "The biology of pentastomids". Advances in Parasitology . 25: 45–128. doi:10.1016/S0065-308X(08)60342-5. ISBN   9780120317257. PMID   3535437.
  10. ↑ J. T. Self (1969). "Biological relationships of the Pentastomida: a bibliography on the Pentastomida". Experimental Parasitology . 24 (1): 63–119. doi:10.1016/0014-4894(69)90222-7. PMID   4887218.
  11. ↑ T. D. Schubart (1853). "Ueber die Entwicklung des Pentastoma taenioides". Zeitschrift für Wissenschaftliche Zoologie. 4: 117–118.
  12. ↑ G. Osche (1959). ""Arthropodencharaktere" bei einem Pentastomiden Embryo (Reighhardia sernae)". Zoologischer Anzeiger . 163: 169–178.
  13. ↑ P. J. van Beneden (1849). "Recherches sur l'organisation et le développement des Lingatules (Pentastoma Rud.), suivies de la description d'une espèce nouvelle provenant d'un Mandrill". Annales des Sciences Naturelles Zoologie Series. 3 (11): 313–348.
  14. ↑ K. G. Wingstrand (1972). "Comparative spermatology of a pentastomid, Raillietiella hemidactyli, and a branchiuran crustacean, Argulus foliaceus, with a discussion of pentastomid relationships". Det Kongelige Danske Videnskabernes Selskab Biologiske Skrifter. 19 (4): 1–72.
  15. ↑ J. Riley, A. A. Banaja & J. L. James (1978). "The phylogenetic relationships of the Pentastomida: the case for their inclusion within the Crustacea". International Journal for Parasitology . 8 (4): 245–254. doi:10.1016/0020-7519(78)90087-5.
  16. ↑ L. G. Abele, W. Kim & B. E. Felgenhauer (1989). "Molecular evidence for inclusion of the Phylum Pentastomida in the Crustacea" (PDF). Molecular Biology and Evolution . 6 (6): 685–691.[ dead link ]
  17. ↑ D. V. Lavrov, W. M. Brown & J. L. Boore (2004). "Phylogenetic position of the Pentastomida and (pan)crustacean relationships" (PDF). Proceedings of the Royal Society of London B . 271 (1538): 537–544. doi:10.1098/rspb.2003.2631. PMC   1691615 . PMID   15129965. Archived from the original (PDF) on 2015-09-23. Retrieved 2009-12-20.
  18. ↑ O. S. Møller; J. Olesen; A. Avenant-Oldewage; P. F. Thomsen; H. Glenner (2008). "First maxillae suction discs in Branchiura (Crustacea): development and evolution in light of the first molecular phylogeny of Branchiura, Pentastomida, and other "Maxillopoda"". Arthropod Structure & Development. 37 (4): 333–346. Bibcode:2008ArtSD..37..333M. doi:10.1016/j.asd.2007.12.002. PMID   18394959.
  19. ↑ Todd H. Oakley; Joanna M. Wolfe; Annie R. Lindgren; Alexander K. Zaharoff (2013). "Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and Pancrustacean phylogeny". Molecular Biology and Evolution . 30 (1): 215–233. doi: 10.1093/molbev/mss216 . PMID   22977117.
  20. ↑ J. Zrzavý (2001). "The interrelationships of metazoan parasites: a review of phylum- and higher-level hypotheses from recent morphological and molecular phylogenetic analyses". Folia Parasitologica. 48 (2): 81–103. doi: 10.14411/fp.2001.013 . PMID   11437135.
  21. ↑ J. W. Martin & G. E. Davis (2001). An Updated Classification of the Recent Crustacea (PDF). Natural History Museum of Los Angeles County. pp. 132 pp. Archived from the original (PDF) on 2019-09-08. Retrieved 2009-12-20.
  22. ↑ Dieter Waloszek, John E. Repetski & Andreas Maas (2006). "A new Late Cambrian pentastomid and a review of the relationships of this parasitic group". Transactions of the Royal Society of Edinburgh: Earth Sciences. 96 (2): 163–176. doi:10.1017/S0263593300001280. S2CID   84859920.
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  24. ↑ D. Walossek & K. J. Müller (1994). "Pentastomid parasites from the Lower Palaeozoic of Sweden". Transactions of the Royal Society of Edinburgh: Earth Sciences. 85: 1–37. doi:10.1017/s0263593300006295. S2CID   86957051.
  25. 1 2 Dieter Walossek, John E. Repetski & Klaus J. Müller (1994). "An exceptionally preserved parasitic arthropod, Heymonsicambria taylori n. sp. (Arthropoda increate sedis: Pentastomida) from Cambrian – Ordovician boundary beds of Newfoundland". Canadian Journal of Earth Sciences . 31 (11): 1664–1671. doi:10.1139/e94-149.
  26. ↑ Peel, John S. (2022). "The oldest tongue worm: A stem-group pentastomid arthropod from the early middle Cambrian (Wuliuan Stage) of North Greenland (Laurentia)". GFF. 144 (2): 97–105. Bibcode:2022GFF...144...97P. doi: 10.1080/11035897.2022.2064543 . S2CID   249028918.
  27. ↑ Gill, Victoria (22 May 2015). "A 425-million-year-old parasite found attached to host". BBC Online . Retrieved 22 May 2015.
  28. ↑ Siveter, David J.; Briggs, Derek E.G.; Siveter, Derek J.; Sutton, Mark D. (2015). "A 425-Million-Year-Old Silurian Pentastomid Parasitic on Ostracods". Current Biology. 25 (12): 1632–1637. Bibcode:2015CBio...25.1632S. doi: 10.1016/j.cub.2015.04.035 . hdl: 10044/1/23597 . PMID   26004764.
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  32. 1 2 3 4 Barnes, Robert D. (1982). Invertebrate Zoology. Philadelphia, PA: Holt-Saunders International. pp. 880–881. ISBN   0-03-056747-5.
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  35. ↑ A. Fain (1975). "The Pentastomida parasitic in man". Annales de la Société Belge de Médecine Tropicale. 55 (1): 59–64. PMID   1231664.
  36. ↑ H. Solano Mairena & W. Venegas (1989). "Human dermatitis caused by a nymph of Sebekia". American Journal of Tropical Medicine and Hygiene . 41 (3): 352–354. doi:10.4269/ajtmh.1989.41.352. PMID   2802021.
  37. ↑ Correct spelling: Sebakia --> Sebekia, See "Sebekia Sambon, 1922". WoRMS. World Register of Marine Species.
  38. ↑ Dennis Tappe & Dietrich W. Büttner (2009). Bethony, Jeffrey M. (ed.). "Diagnosis of human visceral pentastomiasis". PLOS Neglected Tropical Diseases . 3 (2): e320. doi: 10.1371/journal.pntd.0000320 . PMC   2643528 . PMID   19238218.
  39. ↑ Esmond M. Mapp, Howard M. Pollack & Louis H. Goldman (May 1976). "Roentgen diagnosis of Armillifer armillatus infestation (porocephalosis) in man". Journal of the National Medical Association . 68 (3): 198–200, 191. PMC   2609651 . PMID   933188.
  40. ↑ Philip E. S. Palmer; Maurice Merrick Reeder (2001). Imaging of tropical diseases: with epidemiological, pathological, and clinical correlation. Birkhäuser. pp. 389–. ISBN   978-3-540-62471-4 . Retrieved 19 April 2010.
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