Subclass PENTASTOMIDA Shipley, 1905

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Subclass PENTASTOMIDA Shipley, 1905

Tongue Worm

Compiler and date details

14 March 2012 - Gary C. B. Poore (Museum Victoria) & David M. Spratt (CSIRO Ecosystem Sciences)

Pentastomida Shipley, A.E. 1905. Notes on ento-parasites from the Zoological Gardens, London, and elsewhere. Proceedings of the Zoological Society of London 17: 248-253.
Linguatulida Claus, C.F.W. 1872. Grundzüge der Zoologie. Marburg und Leipzig : Elwert.

Introduction

Pentastomids, tongue worms, are as adults obligatory parasites of amphibians, various reptiles — such as turtles, snakes, lizards and crocodiles, birds, and mammals — such as dogs, antelopes, reindeer calves and marsupials. These hosts and some fish and at least one insect species may serve as host of larvae. Adults inhabit the respiratory tracts (lungs, nasal passages and tracheae) of their hosts. The adult body is wormlike, 2–13 cm in length. Appendages are restricted to two pairs of lobe-like head limbs, each with chitinous claws used to cling to the host. The cuticle of the body is nonchitinous and highly porous. The musculature is sheet-like but clearly segmental and cross-striated. The mouth lacks any ancillary appendages; it is on the end of a snout-like projection and connected to a muscular pharynx that is used to pump blood from the host. The combination of the snout and two pairs of legs gives rise to the name ‘Pentastomida’, meaning five mouths. In many species the appendages are reduced to only the terminal claws. The animals lack dedicated respiratory, circulatory and excretory organs. The primary larva hatches from the egg as a mite-like form with two pairs of legs, a penetrating apparatus around the mouth and a terminal forked appendage. The primary larvamoults several times through nymphal stages, gradually transforming to the adult. Pentastomids are dioecious (the sexes separate); the females are larger than the males. Among the mammal species infected by pentastomids are humans, the resultant disease known as pentastomiasis or porocephalosis (in humans — Drabick 1987; pets — Paré 2008). For this reason and because they are frequently encountered parasites, the biology and life cycles are well understood. The literature is rich and diverse; for the most recent review see Riley (1986).

Much of our understanding of the biology of Pentastomida can be attributed to the studies of Berlin zoologist Richard Heymons (1867–1943) whose work was reviewed by Röhlig et al. (2010). An early bibliography of pentastomid literature (Hill 1948) was superseded by another by Self (1969). Self’s publications in the 1960s–1980s and those of John Riley (1970s–2004) also contributed significantly to pentastomid systematics and biology. David Spratt’s papers from the 1980s to 2010 improved knowledge of the Australian fauna. AQIS (2000) recognised the potential of pentastomes to cause pentostomiasis, a respiratory disease, in farmed Australian crocodiles. Such farms have been a source of recent new species records.

Systematics
The systematic position of pentastomids was for a long time enigmatic (Waloszek et al. 2006; Jenner & Littlewood 2008; Sanders & Lee 2010), the group having a mixture of annelid and arthropod features (Nicoli 1963; Self 1969; von Haffner 1977; Haugerud 1989). They were long recognised as a separate phylum variously related to platyhelminthes, nematodes, onychophorans or arthropods. Among arthropods, pentastomids have been related erroneously to mites or myriapods. Van Beneden (1849) was the first to propose that they are crustaceans but his views were not widely accepted until studies of the structure of the spermatozoa provided support, more specifically that they are related to Branchiura (Wingstrand 1972; Riley et al. 1978; Storch & Jamieson 1992; Zrzavý 2001). This relationship was supported by ribosomal and mitochondrial DNA molecular analyses (Abele et al. 1989; Spears & Abele 1998; Lavrov et al. 2004; Møller et al. 2008; Sanders & Lee 2010) and by larval morphology and cuticular ultrastructure (Karuppaswamy 1977). The position of the Branchiopoda-Pentastomida clade (called by some, Ichthyostraca), currently within Maxillopoda, may be more removed from core Crustacea than the present classification suggests (Giribet et al. 2005; Sanders & Lee 2010) and the question of their exact position remains open.

Alternative phylogenetic analyses, of morphology, seem to indicate that Pentastomida is a transitional group between the Arthropoda and groups such as Nematoda and Nematomorpha, a view supported by some palaeontologists. Upper Cambrian fossils have been discovered that are similar to modern pentastomid adults and larvae (Walossek & Müller 1994; Walossek et al. 1994; Waloszek et al. 2006; Castellani et al. 2011). These authors argued on the basis of the fossils and modern external morphology, internal anatomy, and ontogenetic development that the evidence does not support a relationship between crustaceans and pentastomids. They were supported by morphological analyses of modern taxa by Almeida and co-authors (Almeida & Christoffersen 1999; Almeida et al. 2008). The value of relying strictly on morphology of animals that are entirely endoparasitic and somewhat reduced as a consequence is limited. The fossils predate the origin of land vertebrates, raising the question of what groups they may have parasitised. The AFD includes Pentastomida in Crustacea Maxillopoda following a general but not universal consensus and Martin & Davis (2001).

Classification, nomenclature, taxon authorities and literature
The subclass Pentastomida is commonly attributed to Diesing (1836). Diesing published a widely cited paper in 1835 (none in 1836) discussing the genus Pentastoma Rudolphi but not a higher taxon based on this name. He included the genus in Acanthotheca, a group of the Nematoidea. Later, Diesing (1850: 609) placed the genus in the ‘Subordo II Proctucha’ and ‘Tribus I Taxobothria’. Later still, Diesing (1863: 324) included the genus in the ‘Ordo Cephalocotylea, Sectio I Paramecocotylea, Tribus I Aprocta, Subtribus II Trypanorhyncha’, and ‘Familia Hypobothria’. Leuckart (1860), whose early work is commonly referred to, used like many others, only the common German plural ‘Pentastomen’. Haldeman (1851), responsible for the family Linguatulidae, included them in the Helminthes. The first record of the name Pentastomida as such is by Shipley (1905: 249) who introduced the name without comment. In a later revisionary chapter on the group, Shipley (1909: 488) added a footnote stating ‘The animals included in this group are usually called Linguatulidae or Pentastomidae after the two genera … The familiar name Pentastoma may, however, be preserved by incorporporating it in the designation of the group.’

An older name for the taxon, Linguatulida, has fallen out of use. Claus (1872: 519) treated the Linguatulida as an Order of the Arachnoidea and the term was in common use in the nineteenth Century and even as late as Hill’s (1948) bibliography. Vogt’s (1851) use of Linguatulida as a family name may be viewed as an earlier mention, in the same year as Haldeman’s family Linguatulidae of Helminthes.

In most classifications, two orders are recognised: Cephalobaenida Heymons, 1935 and Porocephalida Heymons, 1935. In an alternative treatment, the taxon is divided into four with two additional orders, Reighardiida and Raillietellida (Almeida & Christoffersen 1999). Neither has wide acceptance except by Röhlig et al. (2010). Waloszek et al. (2006) proposed the taxon name Eupentastomida for the ‘crown’ pentastomids, excluding fossil taxa. Self (1969) provided a key to genera but not families; few genera have been added since. About 120 species are known, and lists of species names, both fossil and extant, can be found at http://en.wikipedia.org/wiki/Pentastomida and http://zipcodezoo.com/Key/Animalia/Pentastomida_Subclass.asp although the arrangement of families and genera, and the taxon authorities given there, are not followed here.

This work follows the classification of Riley (1986) and Martin & Davis (2001). Self’s (1969) catalogue of species and Martin & Davis’s list of families contain numerous errors in the attribution and spelling of family names. Martin & Davis attributed to Fain (1961) seven of the nine families they recognised and their list has been followed by several web-based lists (WoRMS, EoL, ZipcodeZoo, Wikipedia, etc.) and other authors. In fact, all except one of the families were erected much earlier and these authorities are acknowledged here. Many, but not all, authors have misspelled two family names (Sambonidae for Samboniidae, Sebekidae for Sebekiidae). ICZN (1999) Article 29.5 does not now require these to be corrected if the misspelling is in current use. The shorter form is used in both cases here, largely because that was how they were erected and followed by most authors. Self (1969) gave incorrect type species for some genera and allocated genera differently among families.

A literature database in Endnote format with many accompanying pdfs and web links is available on request from G.C.B. Poore.

The Australian fauna: history, sources and hosts
Pentastomes were first recognised in an Australian species of snake at Regent’s Park Zoo, London, by Baird (1862), and in New South Wales, Australia, in another snake, by Krefft (1871). These records and others by Spencer (1889, 1893) from Victoria and Tasmania were listed by Sweet (1908). The Australian fauna was next reviewed by Riley et al. (1985) and others taxa have been added since. This work records all species known to occur in Australia and notes the presence of other unidentified specimens from the literature. The literature is imprecise on the distribution of many species. Many are known only from types and few other specimens were listed in the original descriptive papers. The ‘type locality’ of these is often extremely vague, for example, just an Australian state. Some were retrieved during autopsies of zoo specimens, in some cases Australian animals in zoos overseas. The distributions of the host species are often widespread, more so than the records of the parasites themselves. Several species appear not to be host specific. For these reasons, distributions of species are given only by state name but this does not indicate the species is widespread throughout that state. IBRA regions are not given because these could be misleading given the disparities between parasite records and those of their known hosts. Previously unpublished records compiled by D.M. Spratt are incorporated here. In this catalogue scientific and common names of hosts are given in the modern combinations used by AFD with the stated host name in parentheses if significantly different. Minor spelling mistakes are corrected.

Diagnoses
Diagnoses of orders were taken from Riley (1986). Families have not been recently diagnosed. Two sets of diagnoses are given here. The first were generated from the data matrix used by Almeida and Christoffersen (1999) for their cladistic analysis by completing a DELTA matrix and deriving 'natural language' descriptions. The second are loose translations from French of Fain’s (1961) diagnoses and are not strictly comparable. A third set could be derived from Nicoli's (1963) tables.

Citation
Poore, G.C.B. & Spratt, D.M. (2012). Pentastomida. Australian Faunal Directory. Australian Biological Resources Study, Canberra. http://www.environment.gov.au/biodiversity/abrs/online-resources/fauna/afd/taxa/Pentastomida

General References

Abele, L., Kim, W. & Felgenhauer, B.E. 1989. Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. Molecular Biology and Evolution 6: 68-691

Almeida, W.O., Christoffersen, M.L., Amorim, D.S. & Eloy, E.C.C. 2008. Morphological support for the phylogenetic positioning of Pentastomida and related fossils. Revista Biotemas 21: 81-90

Almeida, W.O. & Christoffersen, M.L. 1999. A cladistic approach to relationships in Pentastomida. Journal of Parasitology 85: 695-704

AQIS 2000. Import risk analysis paper for live crocodilians and their eggs. Australian Quarantine & Inspection Service Canberra. http://www.aqis.gov.au. 70 pp.

Baird, W. 1862. Description of some new species of Entozoa. Proceedings of the Zoological Society of London 1862: 113-115

Castellani, C., Maas, A., Waloszek, D. & Haug, J.D. 2011. New pentastomids from the Late Cambrian of Sweden - deeper insight of the ontogeny of fossil tongue worms. Palaeontographica Beitrage zur Naturgeschichte der Vorzeit. Abteilung A: Paläozoologie - Stratigraphie 293: 95-145

Claus, C.F.W. 1872. Grundzüge der Zoologie. Marburg und Leipzig : Elwert.

Diesing, C.M. 1850. Systema Helminthum. Vindobonae : W. Braumüller Vol. 1 679 pp.

Diesing, K.M 1863. Revision der Cephalocotyleen. Abteilung Paramecotyleen. Sitzungsberichte der Akademie der Wissenschaften in Wien. Mathematisch-Naturwissenschaftliche Klasse 48: 200-345

Diesing, K.M. 1836. Versuch einer Monographie der Gattung Pentastoma. Annalen des Wiener Museums der Naturgeschichte 1: 1-38

Drabick, J.J. 1987. Pentastomiasis. Reviews of Infectious Diseases 9: 1087-1094

Fain, A. 1961. Les pentastomides de l'Afrique centrale. Annales du Musée Royal de l'Afrique Centrale Tervuren Belgique sér. 8, Zool. 92: 1-115

Giribet, G., Richter, S., Edgecombe, G.D. & Wheeler, W.C. 2005. The position of crustaceans within Arthropoda – evidence from nine molecular loci and morphology. pp. 307-352 in Koenemann, S. & Jenner, R.A. (eds). Crustacea and Arthropoda relations. Crustacean Issues 16: 1-423

Haldeman, S.S. 1851. Invertebrates. pp. 220-400 in Baird, S.F. Outlines of General Zoology. New York : Rudolph Garrigue. [reprinted from the Zoological portion of the work entitled "Iconographic Encyclopedia of Sciences, Literature and Art. Systematically arranged by J.G. Heck, translated from the German with additions, and edited by Spencer F. Baird, A.M., M.D., Professor of Natural Sciences in Dickinson College, Carlisle, Pa. ...]

Haugerud, R.E. 1989. Evolution in the pentastomids. Parasitology Today 5: 126-132

Heymons, R. 1935. Pentastomida. In, Bronns, H.G. (ed.). Klassen und Ordnungen des Tierreichs. Fünfter Band. IV Abteilung, 1. Buch. Leipzig : Akademische Verlagsgesellschaft m.b.H. pp. 1–268.

Hill, H.R. 1948. Annotated bibliography of the Linguatulida. Bulletin of the Southern California Academy of Sciences 47: 56-73

Jenner, R.A. & Littlewood, T.J. 2008. Problematica old and new. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 363: 1503-1512

Karuppaswamy, S.A. 1977. Occurrence of b-chitin in the cuticle of a pentastomid Railletiella gowrii. Experientia 33: 735-736

Krefft, G 1871. On Australian Entozoa, with descriptions of new species. Transactions of the Entomological Society of New South Wales 2: 206-232

Lavrov, D.V., Brown, W.M. & Boore, J.L. 2004. Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proceedings of the Royal Society of London (B) 271: 537-544

Martin, J.W. & Davis, G.E. 2001. An updated classification of the recent Crustacea. Natural History Museum of Los Angeles County. Science Series 39: 1-124

Møller, O.S., Olesen, J., Avenant-Oldewage, A., Thomsen, P.F. & Glenner, H. 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: 333-346

Nicoli, R.M. 1963. Phylogenèse et systèmatique de phylum des Pentastomida. Annales de Parasitologie Humaine et Comparée 38: 483-516

Paré, J.A. 2008. An overview of pentastomiasis in reptiles and other vertebrates. Journal of Exotic Pet Medicine 17: 285-294

Riley, J. 1986. The biology of pentastomids. Advances in Parasitology 25: 45-128