Tongue Worms, The Reptilian Pentastomids.
The Phylum Pentastomida is composed of two orders, representing sixty species of endoparasites that usually reside in the lungs and respiratory tract of reptiles and carnivorous mammals (Drabick, 1987). These highly evolved bloodsucking helminths possess characters of both Annelida and Arthropoda, but a detailed study of the cuticle by Trainer, Self, and Richter (1975) showed that it was arthropodian in nature. There are, however, enough differences in the pentastome cuticle to warrant the independent phylum. The life cycles of the parasites and their relationships with the intermediate and definitive hosts will be studied.
The body of a pentastomid is elongate and either cylindrical or flattened. The bodies are annulated, but not truly segmented (Cheng, 1986). The name pentastomes may have come from the presence of two pairs of anterior hooks and a mouth, which give the appearance of five openings or stoma. The indistinct demarcations between the head, thorax and abdomen (Cheng, 1986), or the fore body and hind body (Schmidt and Roberts, 1981), may be why they received their common name of tongue worms. The adults lack legs, but have two pair of sharp, hollow, curved, retractile hooklets that may have been vestigial appendages (Cheng, 1986). The hooks are manipulated by powerful muscles and are used to embed the mouth into host tissue or tear directly through it (Schmidt, and Roberts, 1981). At the base of each hook are frontal glands, which secrete a lytic substance that dissolves tissue (Cheng, 1986). The mouth is permanently held open by a chitinous ring or cadre, which may be circular, oval, or U-shaped (Schmidt and Roberts, 1981). The mouth leads into a buccal cavity, then into the prepharynx and the pharynx, which leads into a cardiac valve lined with microvilli. The cardiac valve opens into the esophagus, which leads into a stomach-intestine that passes through the rest of the abdomen with the anus opening usually on the last body segment (Cheng, 1986). The digestive process appears to be mainly intraluminar (Rao and Jennings, 1959). The pentastomids are true coelomate animals with a peritoneum lining the body cavity. There is a "brain" connected to various organs and tissues by a double or, rarely, a single ventral nerve (Cheng, 1986). The only sensory structures are papillae, located especially at the most anterior portion, the cephalothorax (Schmidt and Roberts, 1981).
Pentastomids are dioecious and usually show little sexual dimorphism, except that males are often smaller than females. Males possess a single, tubular testis which can occupy anywhere from one third to one half of the body cavity. It gives rise to a pair of testiducts, which carry the spermatozoa to the vas deferens. The vas deferens open to a terminal cirrus that fits into the groove of a dilator organ, which acts as a guide for the cirrus during copulation. The testiducts also act as storage sites and are sometimes referred to as seminal vesicles (Cheng, 1986). The male genital pore is on the midventral side of the anterior abdominal segment, near the mouth (Schmidt and Roberts, 1981). In females, a single elongate ovary gives rise to two oviducts that reunite to form the uterus. The uterus may be short and simple, but the oviducts and uterus are usually extensively coiled within the body. The uterus leads into a short muscular vagina that opens through the female genital pore. One defining characteristic between the two orders of Pentastomida is the location of the female genital pore. The female gonopore opens ventrally at the anterior end of the abdomen in the order Cephalobaenida and at the posterior end in the order Porocephalida. The fertilization is internal, and the females are oviparous - their eggs hatch outside the body. The two testiducts in males and two oviducts in females suggest that each sex of the ancestral form had paired gonads (Cheng, 1986).
The adults generally parasitize the respiratory systems of reptiles with little if any pathological tissue response; whereas, in accidental hosts, the response may be highly inflammatory. Because there is no inflammatory response in the natural mammalian or reptilian intermediate hosts, nor in the primary hosts, there must be a high degree of adaptation between hosts and their parasites as a result of a long evolutionary association (Self and Kuntz, 1967). The frontal and subparietal glands produce a lamellar secretion, which covers the entire surface of the cuticle and may protect vital areas of the parasite from the host's immune system and antibody action (Schmidt and Roberts, 1981). The cuticle is an acellular, non-living secretion composed of three layers: an outer epicuticle, median exocuticle, and inner endocuticle (Trainer, Self, and Richter, 1975). As in Arthropoda, this cuticle also acts as an impermeable exoskeleton onto which muscles are inserted and attached (Trainer, Self, and Richter, 1975).
The Pentastomida is subdivided into two orders: Cephalobaenida and Porocephalida (Schmidt and Roberts, 1981; Noble and Noble, 1976). Cheng divides it into two classes instead of two orders (1986). The Cephalobaenida are more primitive, involving insects, fish, amphibia, and reptiles as secondary hosts. The Porocephalida often require mammals as secondary hosts and are generally more advanced (Noble and Noble, 1976). The members of Cephalobaenida are divided into two families. The family Cephalobaenidae (Raillietiellidae according to Schmidt and Roberts, 1981) are parasitic in the lungs of snakes, lizards, other reptiles, and amphibians. The family Reighardiidae are found in the air sacs of birds, and therefore will not be covered (Cheng, 1986). The members of Porocephalida are divided into four families. The family Porocephalidae parasitizes two vertebrate hosts. The adults are found in the lungs, trachea, and nasal passages of snakes and lizards, while the larva are found in small mammals. The family Sambonidae includes parasites of lacertilians. The family Sebekidae are parasitic in Crocodylia and Chelonia. The family Linguatulidae is usually parasitic in the nasal passages and frontal sinuses of canines, felines, and other mammals (and are not included in the scope of this paper). Some species of this family are of human importance because they will invade the nasopharyngeal spaces of humans, causing nasopharyngeal pentastomiosis (Cheng, 1986). Hunter and Higgins (1960) found a third-stage larval Linguata serrata in the anterior chamber of a young Virginian's eye.
The family Cephalobaenidae (Raillietiellidae) includes five genera: Cephalobaena, Gretillatia, Mahafaliella, Raillietiella, and Travassostulida (Schmidt and Roberts, 1981). Self and Kuntz (1957) propose a sixth genus: Megadrepanoides. Raillietiella contains approximately twenty species (Esslinger, 1968), and has been studied in the greatest detail. Because of this, its life cycle will represent the whole family in this paper. As stated previously, the Cephalobaenidae are parasitic in the lungs of snakes, lizards, and sometimes birds. There is evidence that Raillietiella may have a direct life cycle, and may use a lizard or cockroach, Periplaneta americana, as an intermediate host (Cheng, 1986). The adults live in the distal membranous regions of the lungs of reptiles, and therefore, the eggs are likely to pass to the exterior in the nasal mucus. Eggs can also be found in the feces of the host after traveling up the trachea of its host and swallowed. (Esslinger, 1968). The larvae of R. furcocerca of South America will hatch and migrate from the small intestine to the peritoneal cavity in albino laboratory mice within 45 minutes after inoculation; further development did not occur (Esslinger, 1968). A definitive host that eats the eggs can also become an intermediate host, but it is not known whether the larvae can migrate to the lung and mature (Schmidt and Roberts, 1981). This phenomenon may be the reason for the assumption of a direct life cycle. The eggs are covered by two distinct transparent and inelastic membranes, 115 X 88 microns, which resist desiccation (Esslinger, 1968). A general characteristic of the pentastomid egg is a permanent funnel-shaped opening through the inner membrane to the larva, called the facette (Schmidt and Roberts, 1981). A mucoid substance is secreted from the dorsal organ and ruptures the outer membrane to cover the inner membrane with its sticky secretion that allows many eggs to stick together (Schmidt, and Roberts, 1981). The larva have three pairs of fixed lateral cuticular spines and two stigmatas (Esslinger, 1968). The life cycle of the larva is not well known. If it is similar to the life cycle in other families, it will hatch inside the intermediate host, tear through the intestinal wall, and "wander" around in the body until becoming dormant and metamorphosing into an infective nymph (Schmidt and Roberts, 1981). The process of becoming a nymph may take upwards of several months, during which time the larva undergoes a number of molts, attaining greater size with each additional molt. The infective larvae are encapsulated within host tissue and are infective to the carnivorous animals that feed on the intermediate host (Noble and Noble, 1976). The ingested nymph may then penetrate the definitive host's intestine and migrate to the lung, where it matures (Schmidt and Roberts, 1981). There is evidence in Linguatula serrata that the nymphs may quickly leave their cysts and cling to the mucous membranes of the mouth of the definitive host (Noble and Noble, 1976). The same type of phenomenon may occur in Raillietiella. In members of Porocephalida, even the adult may leave the lung of a stressed host and escape through the mouth of the organism (Self and Kuntz, 1967). This may be an adaptation for the organism to avoid being digested by a carnivore and to establish residence inside a new host, if it is compatible.
The family Sebekidae is a member of the second, more advanced, order Porocephalida. It includes four genera: Sebeka, Alofia, Diesingia, and Leiperia. Very few studies have been done on this family, probably because it is of little human importance. Diesingia usually reside in turtles or tortoises as adults; the other genera parasitize animals of the order Crocodilylia. One species of Diesingia was noted in the lungs and large bronchi of the pacific boa, Engyrus carinatus (Self and Kuntz, 1957). The adult stage of Sebekia oxycephala is reached in the respiratory tracts of alligators, crocodiles, and apparently in turtles as well. The immature larva stage occurs in fish, lizards, snakes, and crocodiles. The first description of the larva was by Holl in 1928, and not much work has been done in this area since then. Dukes, Shealy, and Rogers (1971) recorded the immature stages of S. oxycephala in largemouth bass from Lake St. John, Louisiana. The high frequency of infection in the bass, coupled with the lake's low alligator population, led the researchers to suspect a different definitive host. Viable cysts in the bass tissue were force-fed to four species of snakes and one species of turtle, Chelydra serpentina. Only in the lungs of C. serpentina were parasites recovered one month later, which led them to suspect that the alligator snapping turtle may be the definitive host in the lake (Dukes, Shealy, and Rogers, 1971) . No additional information could be found on the other genera of Sebekidae.
The family Sambonidae is also a member of Porocephalida, including the genera Sambonia, Parasambonia, Waddycephalus, and Elenia. The adult stages are reached in the respiratory tracts of snakes and lizards. Self and Kuntz (1957) reported finding Sambonia lohrmanni in the lungs of a Nile monitor, Varanus nilotica, in the southwest part of the Sudan, and in a wart snake, Acrochordus granulatus, of Florida IslandWaddycephalus teretiusculus was found in the large bronchi of a painted bronze snake, Ahaetulla calligaster, in a grass-covered lowland of the British Solomon Islands (Self and Kuntz, 1957). A life cycle involving two vertebrate hosts seems most likely since these adults live in snakes or carnivorous lizard hosts. These definitive hosts regularly feed on smaller reptiles, amphibians, and mammals that are known to carry the nymphal stages.
Substantially more research has been done on the family Porocephalidae, probably because this is a family known to affect humans. This family of the Porocephalida includes the genera Armillifer, Cubirea, Gigliolella, Kiricephalus, Ligamifer, and Porocephalus. The adult parasites reside in the lungs, trachea, and nasal passages of snakes and lizards that feed on the intermediate mammalian host. The females oviposite eggs within the lungs, i.e. the bronchi, of their definitive host. The eggs contain fully-formed larva within the confines of their shell and are infective to the intermediate host upon deposition. The eggs are carried out of the host by the nasal mucus and adhere to surrounding vegetation or are deposited in standing water (Cheng, 1986). According to Esslinger (1962b), the eggs can take an alternate route from the lung to the pharynx, where they are swallowed and passed out of the body in the feces. When an appropriate intermediate host ingests the eggs, they hatch, and the larvae burrow through the intestinal wall to become lodged within one of the visceral organs. In this organ, the larvae increase in size and develop further through several successive molts until they reach the infective stage. The infective stage of the larvae then leave the organ to become encysted in the abdominal cavity. The intermediate hosts for Armillifer spp. include monkeys, antelope, hedgehogs, rats, cats, giraffe, and humans (Cheng, 1986). Armillifer armillatus have been found in the liver, spleen, and lungs of humans. These infections may have been contracted by drinking water contaminated with eggs, eating vegetables on which eggs are deposited, or by eating or handling snakes that serve as the definitive host (Cheng, 1986). The eggs of Porocephalus crotali in snake sputum are readily ingested by the intermediate hosts. These hosts include muskrats, opossums, armadillos, raccoons, and other mammals (Noble and Noble, 1976).
The life cycle of Porocephalus crotali living in crotaline snakes have been well studied; therefore, in this paper, it will be used as the representative life cycle of the whole family. Esslinger isolated eggs of P. crotali from adults living in the lung tissues of Louisiana cottonmouth water moccasins, Agkistrodon piscivorus, and performed tests on lab mice and rats. Seven stages of larval development were found to occur in inoculated albino lab rats (Esslinger, 1962a). The first stage was the "primary larva," which is the motile stage in the mature egg. The larva has two pairs of stumpy legs, each with a pair of clawlike hooks, an anterior penetration apparatus, and a short bifurcate tail. On the dorsal surface, there are two stigmata, a median dorsal organ, and a large, heavily chitinized, U-shaped mouth ring (Esslinger, 1962a). The dorsal organ may be a site of phosphatase activity during times of accelerated cellular activity (Hollis, 1979). On hatching, the larvae penetrate the duodenal mucosa and work their way to the abdominal cavity about one hour after inoculation (Schmidt and Roberts, 1981). The larvae will wander around the body cavity for seven or eight days, at which time they undergo their first molt and become lightly encapsulated in host tissue. Since Porocephalus remain immobile once encapsulated in the mesenteries, fat or viscera, the cast skins or exuviae remain in the capsule with the growing parasite (Esslinger, 1962a). Eight days after the larva molts, the first nymphal stage is seen, which is devoid of the larval structures. In this stage, the alimentary tract is clearly divided into a foregut, midgut, and a hindgut. Approximately nineteen days after the initial inoculation, the second nymphal stage is formed at twice the size of the first stage and with eighteen more stigmata than the previous stage. The mouth ring also doubles in size to 40 X 33 microns. The third nymphal stage occurs at 30 days and is again doubled in size. The stigmata have greatly increased in number, covering the dorsal and lateral surfaces. The first signs of mouth hooks appear as two pairs of cuticular papillae, just lateral to the mouth. After 40 days and the fourth molt, the fourth nymphal stage exhibits distinct segmentation and has yet again doubled in size. At 50 days, the fifth nymphal stage measures 6.5 X 1mm and is bent ventrally into an incomplete ring. The mouth hooks have increased in length to 50 microns. Sexual differentiation is noted at this stage. The cuticle-lined male genital opening can be seen just posterior to the mouth. The sixth and final molt occurs around 80 days, and the parasite is tightly encapsulated in the exuvia of the preceding molt. When the exuvia is split, the nymph is freed and becomes active. It measures about 12 mm in length and 1.5 mm in diameter. The sixth-stage nymphs are infectious and often penetrate the stomach and enter the body cavity within 24 hours of ingestion. They often pass directly into the lung tissue since the anatomy of the reptiles places the lung and the alimentary tract side-by-side (Esslinger, 1962a).
Cheng, T. C. 1986. General Parisitology, Second ed. Academic Press College Division, Orlando, p. 765 - 773.
Dukes, G. H., R. M. Shealy, and W. A. Rogers. 1971. Sebekia oxycephala (Pentastomida) in Largemouth Bass from Lake St. John, Concordia Parish Louisiana. Journal of Parasitology 57: 1028.
Drabick, J. J. 1987. Pentastomiasis. Review of Infectious Diseases 9: 1087 - 1094.
Esslinger, J. H. 1968. Morphology of the Egg and Larva of Rallietiella furcocerca (Pentastomida) From A Colombian Snake (Clelia clelia). Journal of Parasitology 54: 411 - 416.
---------. 1962a. Development of Porocephalus crotali (Humboldt, 1808) (Pentastomida) in Experimental Intermediate Hosts. Journal of Parasitology 48: 452 - 456.
---------. 1962b. Morphology of the Egg and Larva of Porocephalus crotali (Pentastomida). Journal of Parasitology 48: 457 - 462.
Hollis, P. D. 1979. The Histochemical Demonstration of Alkaline Phosphatase Activity in Porocephalus crotali Humboldt 1811 (Pentastomidia). Journal of Parasitology 65: 461 - 463.
Hunter, W. S., and R. P. Higgens. 1960. An Unusual Case Of Human Porocephaliasis. Journal of Parasitology 46: 68.
Noble, E. R., and G. A. Noble. 1976. Parasitology The Biology of Animal Parasites,
Fourth ed. Lea & Febiger, Philadelphia, p.407 - 410.
Rao, H., and J. B. Jennings. 1959. The Alimentary System of a Pentastomid from the Indian Water-Snake Natrix piscator Schneider. Journal of Parasitology 45: 299 - 300.
Schmidt, G. D., and L. S. Roberts. 1981. Foundations of Parasitology, Second ed. The C. V. Mosby Co., St. Louis, p. 559 - 566.
Self, J. T., and R. E. Kunts. 1957. Pentastomids From African Reptiles and Mammals and From Reptiles of Florida Island, British Solomon Islands (South Pacific). Journal of Parasitology 43: 194 - 199.
---------, and ---------. 1967. Host-Parasite Relations in Some Pentastomida. Journal of Parasitology 53: 202 - 206.
Trainer, J. E., J. T. Self, and K. M. Richter. 1975. Ultrastructure of Porocephalus crotali (Pentastomida) Cuticle With Phylogenetic Implications. Journal of Parasitology 61: 753 - 758.
Tongue Worms, The Reptilian Pentastomids.
Bryan H. Hummel
November 2, 1998.