Pentastomida

(Tongue worms)

Phylum Arthropoda

Subphylum Crustacea

Class Pentastomida

Number of families 8

Thumbnail description
Parasitic tongue worms inhabit the respiratory systems of terrestrial vertebrates

Evolution and systematics

Pentastomida once was classified as a minor phylum, a fact reflected in most modern textbooks of parasitology. The classification is being changed, however. The evolutionary history of tongue worms is unique among parasites. The fossil record apparently extends to the late Cambrian period (500 million years ago [mya]), exceeding that of the next oldest parasites, certain copepods, by some 370 million years. Tiny fossil tongue worms have been etched from ancient fine-grained, deep-water limestone when the rock has been dissolved with dilute acid. In most respects these 0.04 to 0.08 in long (1–2 mm) larvae are indistinguishable from modern tongue worms. Therein lies a conundrum, because extant adult tongue worms are parasitic in terrestrial vertebrates, which do not appear in the fossil record until the late Devonian, approximately 350 mya. Nonetheless, fossil agnathan fishes are known from the Upper Cambrian, and it is noteworthy that all of the fossil tongue worms discovered so far have been collected from limestone containing diverse conodont fauna. Conodonts are primitive fish-like chordates. Although a marine ancestry for tongue worms seems assured, the exact nature of the ancestral host may never be known. In addition to having anterior pairs of claws, some of these ancient tongue worms have two pairs of vestigial nonsegmented trunk limbs. These structures are lacking in other fossil specimens and in all modern forms. A compounding problem is that the larvae of modern tongue worms are highly modified for tissue migration. Clawed limbs, together with other limb-like outgrowths evident in early larval development within the egg, have so far proved impossible to homologize with euarthropod head and trunk appendages.

A relation between tongue worms and branchiuran crustaceans (class Maxillopoda, subclass Branchiura) is supported by results of studies of sperm of other species and by comparison of ribosomal 18S recombinant RNA sequences in the two groups. In numerous extant parasitic maxillopods representative of several subclasses, the degree of cephalization together with the development of the trunk and anchoring devices is highly variable, to the extent that many adults bear no resemblance to their free-living counterparts. Always, however, the first larval instar, the nauplius, is easily recognized. The highly modified first instar of tongue worms, the so-called primary larva, is very different from its putative naupliar fore-bear because it has evolved to penetrate and traverse tissues in (mostly) terrestrial hosts. These larvae hatch with only two limb-bearing head somites and three trunk somites. Subsequent growth of the trunk is by a form of pseudometamerism, without the addition of further somites. The development of some copepods, relatives of branchiurans, also fits this pattern.

The present, still unresolved debate hinges heavily on the relative merits of the fossil evidence versus that of ribosomal RNA and sperm morphology. In this entry, tongue worms are considered a class of crustaceans. The class Pentastomida contains eight families and approximately 110 species assorted between two orders—the primitive Cephalobaenida and the advanced Porocephalida.

Cephalobaenida

• Cephalobaenidae. Three genera. Cephalobaena, one species found in snakes; Raillietiella, more than 35 species found in amphibians, snakes, lizards, amphisbaenans, and birds; Rileyiella, one species found in mammals.
• Reighardiidae. One genus. Reighardia, two species found in marine birds.

Porocephalida

• Sebekidae. Seven genera. Alofia, five species; Leiperia, two species; Selfia, one species; Agema, one species, all found in crocodiles; Sebekia, 12 species, found in crocodiles and chelonians (one species); Pelonia, one species; Diesingia, one species, found in chelonians.

• Subtriquetridae. One genus. Subtriquetra, three species, found in crocodilians.
• Sambonidae. Four genera. Sambonia, four species; Elenia, two species, found in monitor lizards; Waddycephalus, 10 species; Parasambonia, two species, found in snakes.
• Porocephalidae. Two genera. Porocephalus, eight species; Kiricephalus, five species, found in snakes.
• Armilliferidae. Three genera. Armillifer, seven species; Cubirea, two species; Gigliolella, one species, found in snakes.
• Linguatulidae. One genus. Linguatula, more than six species, found in mammals.

Physical characteristics

All tongue worms inhabit the respiratory systems of terrestrial vertebrates. As a consequence, all aspects of their structure and function have adapted to life in this unusual habitat. All are aerodynamic, possessing an elongated, worm-like, mostly cylindrical body, which is rounded both anteriorly and posteriorly. The body is differentiated into an anterior head region, bearing a small ventral mouth flanked by two pairs of retractile hooks, and a long posterior trunk, which carries numerous raised annuli that are not true segments. Sexual dimorphism is pronounced, females are invariably larger than males. Females may be as small as 0.06 × 0.01 in (1.5 × 0.3 mm) (Rileyiella) to 4.7 × 0.4 in (12 × 1 cm) (Armillifer), but males are much shorter and proportionately more slender. The chitinous cuticle is thin, flexible, and translucent, so that in living specimens the body organs, suspended in an extensive fluid-filled haemocoel, are clearly visible. Peristaltic contractions of the body wall musculature affect locomotion, which is comparable with that of soft-skinned dipteran maggots. The cuticle is shed periodically during growth, and simple metamorphosis occurs (developing nymphs resemble adults). Numerous, exceedingly fine, chitinlined ducts erupt over the entire surface of the cuticle, each connected to an extensive system of subparietal gland cells that abound in the haemocoel immediately beneath the tegumental epidermis. Secretion from these glands, composed largely of membranous secretory droplets, is critical to prolonged survival of these parasites in the delicate environment of the lung. Large numbers of distinctive, flask-shaped cells, analogous to those involved in ion transport in other invertebrates, are embedded in the cuticle. Additional gland systems, located mainly in the head (both orders), but also flanking the intestine in porocephalids, discharge copious enzymic secretions over the head and into hook pits. There are no respiratory or excretory systems.

The sucking mouth leads into a short esophagus, which is separated by a valve from a simple undifferentiated tubular intestine. The intestine terminates at a short rectum. The simple nervous system forms initially as separate ganglia that fuse progressively during development to varying degrees within the two orders. In Porocephalida, all ganglia fuse to form a compact "brain." In cephalobaenids only the most anterior ganglia do so. A variety of small sense organs, often visible as distinct papillae, are arranged over the head, but most are concentrated on the ventral surface around the mouth.

The reproductive system differs between the two orders. The uterus of cephalobaenids is saccate, and the vagina opens anteriorly close to the junction of the head and trunk. In porocephalids, the uterus is elongate and tubular. Because it is many times longer than the body, the uterus is irregularly coiled to occupy most of the available haemocoel. The vagina opens near the anus. In both orders, the dorsal ovary leads into a paired oviduct, which passes around the gut. Close to the junction between the oviduct and the uterus are paired spermathecae, which are responsible for long-term storage of sperm.

The lower reproductive tract of males comprises paired, elongate penises—basically thin, coiled tubes of chitin—close to elaborate chitinous spicules called dilators. Dilators may be extruded through the anterior genital pore by muscles and thereby carry the tip of the penis either to the entrance of the spermathecal ducts in cephalobaenids or into the vagina/uterus in porocephalids. Peristalsis within the uterus of porocephalids pulls the ornamented heads of the paired penises toward the spermathecal ducts. The testis is dorsal, and the paired vasa deferentia empty into a seminal vesicle, which functions as a sperm storage depot before intromission.

Distribution

Most tongue worms, approximately 96%, live in tetrapod definitive hosts that are widespread in the tropics and subtropics. Only a few species are found outside these regions. Porocephalus crotali is unique in that it is cold-adapted, infecting North American rattlesnakes, which hibernate each winter. Reighardia sternae is a cosmopolitan species in gulls and terns, which are widespread in both hemispheres. Another cosmopolitan species, Linguatula serrata, lives in the nasal sinuses of canines (dogs, foxes, wolves), whereas the reindeer host of Linguatula arctica, inhabits the arctic tundra.

Habitat

Most tongue worms live in the lungs of their definitive hosts, although two genera, Leiperia and Subtriquetra, inhabit the trachea and nasal sinuses respectively. At least one member of the genus Elenia infests the throats of monitor lizards. All Linguatula species live in the nasal sinuses of mammals, and Reighardia species are located in the body cavity and air sacs of their avian hosts. An intermediate host is usual in the life cycle of tongue worms. In these cases infective larvae encyst in the tissues of arthropods or vertebrates, depending on the species.

Behavior

Because tongue worms are endoparasites of the respiratory tracts of tetrapods, what little is known about behavior has been inferred mostly from findings at autopsy. In the case of direct life cycles, eggs containing primary larvae gain entry to the definitive host through the alimentary tract as contaminants of food or water. When there are intermediate hosts in the life cycle, larvae acquired by the same means escape from the egg but invade the viscera, where they molt several times to form infective nymphs. The nymphs excyst when intermediate hosts are eaten, and larvae penetrate the stomach or intestinal wall of the final host. This stage is followed by a period of growth in the body cavity before larvae penetrate the lung through the pleura. It is possible to culture in vitro the lung-stage worms of certain species in a blood-based medium under sterile conditions. For example, developing nymphs of Porocephalus crotali, normally resident in the lung of their rattlesnake host, ingest ad libitum the medium in which they are suspended and molt normally through several instars to the adult stage. Thus lung-dwelling species appear not to require specific cues for successful development.

Feeding ecology and diet

With the exception of species belonging to the genus Linguatula, which browse on cells and mucus lining the nasal sinuses, all tongue worms feed on blood. In most cases the blood is pumped from capillaries lining the respiratory surface of the lung by the sucking action of an oral papilla. In some genera (Alofia, Leiperia, Elenia, Waddycephalus, Kiricephalus, and Cuberia) the head of females is separated from the trunk by a distinct neck, which is permanently encapsulated by inflammatory tissue and thereby anchored to the lung wall. In the lung females may also feed on inflammatory cells, as is known to occur during the development of Porocephalus nymphs in rodent intermediate hosts.

Reproductive biology

As far as is known, all tongue worm females become sexually mature precociously. Copulation occurs when the uterus is undeveloped and when males and females are of similar size. Copulation is a lengthy and complex process, entailing docking of the paired penises in the narrow spermathecal duct and concomitant transfer of millions of filiform sperm. Stored sperm fertilize ova released continuously from the ovaries of mature females. Fertilized eggs mature as they descend the uterus of porocephalids, and gravid females of Armillifer and Linguatula species may contain millions of eggs. In contrast, the eggs of cephalobaenids are stored temporarily in a saccate uterus until 30–50% become infectious (i.e., they contain a fully mature primary larva). Then egg deposition begins. The vagina is equipped with a sieve-like mechanism that retains small, undeveloped eggs but allows mature eggs to escape. Thus in both orders, continuous egg production is usual. Eggs shed into lungs are wafted out by the hosts' ciliation and swallowed.

Conservation status

No species are listed by the IUCN.

Significance to humans

The eggs of five tongue worm species are infective to humans, and in four of these species (Armillifer grandis, A. armillatus, A. moniliformis, and A. agkistrodontis), humans are merely an accidental intermediate host. Nearly always, nymphal infections are acquired when eggs in undercooked meat, derived from tongue worm–infected snakes, are consumed. The epidemiology of the remaining species, Linguatula serrata from the nasal sinuses of dogs, is complicated, because both eggs and infective larvae can become established in humans. Ingested eggs hatch to produce infective nymphs. In contrast, if ingested in contaminated offal from sheep or goats, nymphs attempt to migrate from the stomach to the nasal passages, producing acute symptoms of nasopharyngeal linguatulosis.

Resources

Books

Kabata, Z. Parasitic Copepoda of British Fishes. London: Ray Society, 1979.

Mehlhorn, H. Parasitology in Focus. Berlin: Springer Verlag, 1988.

Riley, J. "Pentastomids." In Reproductive Biology of Invertebrates. Vol. VI, edited by K. G. Adiyodi and R. G. Adiyodi. Oxford: IBH Publishing, 1994.

Periodicals

Almeida, W. O., and M. L. Christoffersson. "A Cladistic Approach to Relationships in Pentastomida." Journal of Parasitology 85 (1999): 695–704.

Böckeler, W. "Embryogenese und ZNS-Differenzierung bei Reighardia sternae, Lichtund electronenmikroskopishe Untersuchungen zur Tagmosis und systematischen Stellung der Pentastomiden." Zoologische Jahrbucher (Anatomie) 11 (1984): 297–342.

Buckle, A. C., J. Riley, and G. F. Hill. "The in vitro Development of the Pentastomid Porocephalus crotali from the Infective Instar to the Adult Stage." Parasitology 115 (1997): 503–512.

Martin, J. W., and G. E. Davis. "An Updated Classification of the Recent Crustacea." Science Series, Natural History Museum of Los Angeles County 39 (2001): 1–124.

Riley, J. "The Biology of Pentastomids." Advances in Parasitology 25 (1986): 46–128.

Riley, J., and R. J. Henderson. "Pentastomids and the Tetrapod Lung." Parasitology 119, supplement (1999): S89–105.

Storch, V., and B.G.M. Jamieson. "Further Spermatological Evidence for Including the Pentastomida (Tongue Worms) in the Crustacea." International Journal of Parasitology 22 (1992): 95–108.

Walossek, D., and K. J. Müller. "Pentastomid Parasites from the Lower Palaeozoic of Sweden." Transactions of the Royal Society of Edinburgh, Earth Sciences 85 (1994): 1–37.

Wingstrand K. G. "Comparative Spermatology of a Pentastomid Raillietiella hemidactyli and a Branchiuran Crustacean Argulus foliaceus with a Discussion of Pentastomid Relationships. Biologiske Skrifter 19 (1972): 1–72.

John Riley, PhD