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Linguatula serratatongueworm

By Katie Behrmann

Geographic Range

Linguatula serrata can be found in several countries in Asia, Southeast Asia, the Middle East, Europe, North Africa, and the Americas. Although the distribution of this pentastomid is almost global, it is predominantly prevalent in warm subtropical and temperate regions. Most cases of linguatuliasis or pentastomiasis are recorded in the Middle East. (Gardiner, et al., 1984; Lazo, et al., 1999; Shakerian, et al., 2008)

Habitat

As an adult, Linguatula serrata lives in the nasal airways or frontal sinuses of dogs, wolves, foxes, felines or other carnivorous mammals. The parasite's eggs are transferred when coughed or sneezed out from the lungs to the external environment. If swallowed by the definitive host, the eggs are passed through the feces to the external environment. The intermediate host ingests the eggs off aquatic or wet vegetation in the external environment. In the larval stage, it is endoparasitic on herbivorous and domesticated mammals such as sheep, camels, goats, cattle, rabbits, rodents and pigs. During these sexually immature stages, it resides in the herbivorous mammal's mesenteric lymph nodes, lungs and liver. Humans are an accidental definitive host for Linguatula serrata. Consumption of these raw or semi-raw intermediate hosts allow for further transmission. Cases of infection of this parasite commonly occur where animals are raised, such as slaughterhouses and farms. Eggs survive well in aqueous environments, such as water or wet vegetation, where they are ingested. Since their hosts are agricultural animals and the eggs require an aqueous environments, the occurrence of L. serrata depends on the sanitation of water and food in the area. (Drabick, 1987; Lazo, et al., 1999; Shakerian, et al., 2008)

  • Aquatic Biomes
  • lakes and ponds
  • temporary pools

Physical Description

Lengths range from a few millimeters to 15 centimeters (cm). The adult male L. serrata is 1.8-2 cm, while an adult female is 8-13 cm. The worm is colorless and transparent. Larval L. serrata normaly measure 3-4 mm. Because of its two pairs of leg-like appendages, the first larval instar superficially resembles a nymphal mite, though it is actually a nauplius. During this stage, the parasite has a stylet to tunnel through gut walls, along with appendages for further propulsion. After a series of molts, the worm loses its leg-like appendages and tapers from its cone shaped head down to its posterior end. The ventral has four hook pits. The body is covered with about 70-100 annuli, or rings, with many pores and spines on each annulus arranged in rows. The first three abdominal annuli have three pairs of sensory papillae. After multiple instar stages, adult L. serrata have unaligned pores or stigmata along their bodies. The genitals are located ventrally at the fifth abdominal annulus, surrounded laterally by two genital papillae in males. Both adults and larvae are dorso-ventrally flattened. (Banaja, 1983; Drabick, 1987; Shakerian, et al., 2008)

  • Sexual Dimorphism
  • female larger

Development

After being ingested by an herbivorous intermediate host from an aqueous environment, eggs hatch into their first larval stage, looking superficially like a mite. Many refer to these larvae as "nymphs," although they actually are a nauplius. The larvae use leg-like appendages for movement through the intermediate host. The first larval stage of L. serrata tunnels through gut wall with a stylet, as the host elicits an immune response. The immature larvae are then encysted. Encysting can happen in a number of tissues, including the liver, lymph nodes and muscle. This stage of infection is typically asymptomatic. After a series of molts in these cysts, the third stage larvae lose the leg-like appendages and can travel in between the abdominal cavity and the abdominal wall. While the larvae are encysted, many of them die and calcify after about two years, but if the definitive, carnivorous host feeds upon the intermediate host when the larvae are in their third stage, the carnivore acquires the parasite. The larvae develop to their adult stage in the nasopharynx of the carnivorous mammals and mate. (Drabick, 1987)

Reproduction

Although sexually dimorphic, larger females attempt to find similarly sized males to mate. Linguatula serrata females mate once over the course of their lifetime, but due to huge spermathecal storage and oocytes continuously being ejected from the ovary, females can lay thousands or millions of eggs per year. (Riley, 1983)

Linguatula serrata reaches sexual maturity after several molts in a carnivorous host's repiratory tract. This is where similarly sized females and males mate, though pentastomid males are generally smaller than pentastomid females. Pentastomid females usually mate only once during their lifetime, but eggs develop inside females, who have already stored sperm in the spermathecae. Females can produce hundreds of thousands of eggs, which are expelled into the environment through nasal discharge, saliva or feces. (Drabick, 1987; Riley, 1983; Shakerian, et al., 2008)

Females can lay up to one million eggs in the definitive host per year. The eggs are about 70-90 micrometers and contain the fully-developed first stage of the larva. While many pentastomid males die directly after mating, Linguatula serrata males may live for a period of time after mating. (Hami, et al., 2009; Haugerud, 1989; Riley, 1983)

  • Parental Investment
  • no parental involvement
  • pre-fertilization

Lifespan/Longevity

Larvae can survive for up to two years encysted before they calcify and die in the intermediate host. There was little information on the longevity of adults, but other pentastomid species can live for around ten years. (Drabick, 1987; Hami, et al., 2009)

Behavior

Linguatula serrata is an opportunist and can infect humans and other omnivores in their immature or mature stages, depending on their diet. This worm has been found in the eye chambers and livers of humans, where humans have ingested the eggs from the external environment. When humans ingest eggs from vegetation in the external environment, the parasite develops in the infected person as an intermediate host. Carnivores can subsequently feed on infected human cadavers. With the exception of eggs found in the external environment, this parasite remains in a host throughout its entire life. (Lazo, et al., 1999)

Communication and Perception

Adult Linguatula serrata uses papillae on its annuli to sense its environment. (Banaja, 1983)

Food Habits

Adults ingest food in the final host's respiratory tract. Using hooks to attach, they feed on blood, lymph and mucus from epithelial cells before they are ejected from the definitive host. Larvae are primarily non-feeding, encysting in a variety of host tissues. (Drabick, 1987)

  • Animal Foods
  • body fluids

Predation

Although specific predators for this species are unknown, L. serrata depends on predator-prey relationships to reach its hosts. To become an adult, a carnivorous mammal must prey on herbivorous mammals which already have the parasitic larvae. This pentastomid has a relatively low host specificity, infecting many herbivorous mammals as juveniles and many carnivorous mammals as adults. This generalist approach helps the parasite evade a host defense. (Drabick, 1987; Lazo, et al., 1999)

Ecosystem Roles

This parasite uses domesticated and wild herbivores as intermediate hosts, including sheep, goats, camels, and many other small ruminants. The definitive hosts of L. serrata include carnivores such as dogs, wolves, and coyotes. Humans can serve both roles. They are always parasitic or paratenic, causing zoonotic disease in definitive hosts or remaining asymptomatic as larvae in the paratenic host. Linguatula serrata impacts agricultural ecosystems by decreasing fitness and sometimes causing mortality in livestock. Most of this livestock is herbivorous and controlled by humans; few natural ecosystems are affected. Similarly, the chief definitive hosts of L. serrata are dogs existing in urban areas, also leaving natural ecosystems relatively unaffected. (Drabick, 1987; Shakerian, et al., 2008; Tavassoli, et al., 2007)

Species Used as Host

Economic Importance for Humans: Positive

There is no known positive importance for this species.

Economic Importance for Humans: Negative

Many human infections arise in underdeveloped areas of the world like the Middle East, India, Africa, and Southeast Asia, where eating raw glands of cattle, sheep, and other herbivorous mammals is a part of a normal diet. Infection may also be acquired through ingestion of eggs from plants or water in the environment. Infestations of the worm are frequent in humans, and deaths have even been reported due to blocked nasal passages. Because humans are often the accidental intermediate or final host of L. serrata, the pentastomid is of medical and economic importance. Those who can afford medical help can direct their treatment either towards eliminating the nymphs in their system or relieving the symptoms of infestation through nasal sprays or antihistamines. (Tavassoli, et al., 2007)

Linguatula serrata also frequently infects domesticated animals used for agriculture and stray animals also used for provisions. Infection in liver, mesenteric lymph nodes, and other glands may cause weakening and death of the animals, thus weakening the agricultural economy. Infection rates of small ruminants in the Middle East are significant, as up to 50% of sheep may be infected within a region.

Conservation Status

Linguatula serrata is not endangered, nor does it typically affect endangered animals. (Tavassoli, et al., 2007)

Contributors

Katie Behrmann (author), University of Michigan-Ann Arbor, Heidi Liere (editor), University of Michigan-Ann Arbor, John Marino (editor), University of Michigan-Ann Arbor, Barry OConnor (editor), University of Michigan-Ann Arbor, Renee Mulcrone (editor), Special Projects.

Glossary

Nearctic

living in the Nearctic biogeographic province, the northern part of the New World. This includes Greenland, the Canadian Arctic islands, and all of the North American as far south as the highlands of central Mexico.

World Map

Neotropical

living in the southern part of the New World. In other words, Central and South America.

World Map

Palearctic

living in the northern part of the Old World. In otherwords, Europe and Asia and northern Africa.

World Map

agricultural

living in landscapes dominated by human agriculture.

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

bog

a wetland area rich in accumulated plant material and with acidic soils surrounding a body of open water. Bogs have a flora dominated by sedges, heaths, and sphagnum.

carnivore

an animal that mainly eats meat

causes disease in humans

an animal which directly causes disease in humans. For example, diseases caused by infection of filarial nematodes (elephantiasis and river blindness).

causes or carries domestic animal disease

either directly causes, or indirectly transmits, a disease to a domestic animal

chemical

uses smells or other chemicals to communicate

diapause

a period of time when growth or development is suspended in insects and other invertebrates, it can usually only be ended the appropriate environmental stimulus.

ectothermic

animals which must use heat acquired from the environment and behavioral adaptations to regulate body temperature

fertilization

union of egg and spermatozoan

heterothermic

having a body temperature that fluctuates with that of the immediate environment; having no mechanism or a poorly developed mechanism for regulating internal body temperature.

internal fertilization

fertilization takes place within the female's body

iteroparous

offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

marsh

marshes are wetland areas often dominated by grasses and reeds.

metamorphosis

A large change in the shape or structure of an animal that happens as the animal grows. In insects, "incomplete metamorphosis" is when young animals are similar to adults and change gradually into the adult form, and "complete metamorphosis" is when there is a profound change between larval and adult forms. Butterflies have complete metamorphosis, grasshoppers have incomplete metamorphosis.

motile

having the capacity to move from one place to another.

oriental

found in the oriental region of the world. In other words, India and southeast Asia.

World Map

oviparous

reproduction in which eggs are released by the female; development of offspring occurs outside the mother's body.

parasite

an organism that obtains nutrients from other organisms in a harmful way that doesn't cause immediate death

sanguivore

an animal that mainly eats blood

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

sperm-storing

mature spermatozoa are stored by females following copulation. Male sperm storage also occurs, as sperm are retained in the male epididymes (in mammals) for a period that can, in some cases, extend over several weeks or more, but here we use the term to refer only to sperm storage by females.

suburban

living in residential areas on the outskirts of large cities or towns.

swamp

a wetland area that may be permanently or intermittently covered in water, often dominated by woody vegetation.

tactile

uses touch to communicate

temperate

that region of the Earth between 23.5 degrees North and 60 degrees North (between the Tropic of Cancer and the Arctic Circle) and between 23.5 degrees South and 60 degrees South (between the Tropic of Capricorn and the Antarctic Circle).

terrestrial

Living on the ground.

tropical

the region of the earth that surrounds the equator, from 23.5 degrees north to 23.5 degrees south.

urban

living in cities and large towns, landscapes dominated by human structures and activity.

year-round breeding

breeding takes place throughout the year

References

Banaja, A. 1983. Scanning electron microscopy examintion of larval Linguatula serrata Frölich (Linguatulidae: Pentastomida). Parasitenkunde, 69: 271-277.

Drabick, J. 1987. Pentastomiasis. Reviews of Infectious Diseases, 9 (6): 1087-1095.

Gardiner, C., J. Dyke, S. Shirley. 1984. Hepatic granuloma due to a nymph of Linguatula serrata in a woman from Michigan: A case report and review of the literature. American Journal of Tropical Medicine, 33 (1): 187-189.

Hami, M., S. Naddaf, I. Mobedi, M. Zare-Bidaki, S. Athari, B. Hajimohammadi, G. Anaraki-Mohammed. 2009. Prevalence of Linguatula serrata infection in domestic bovids slaughtered in Tabriz Abattoir, Iran. Iranian Journal of Parasitology, 4 (3): 25-31.

Haugerud, R. 1989. Evolution in the pentastomids. Parsitology Today, 5 (4): 126-132.

Lazo, R., E. Hidalgo, J. Lazo, A. Bermeo, M. Llaguno, J. Murillo, V. Teixeira. 1999. Ocular linguatuliasis in Ecuador: Case report and morphometric study of the larva of Linguatula serrata. American Journal of Tropical Medicine, 60 (3): 405-409.

Riley, J. 1983. Recent advances in our understanding of pentastomid reproductive biology. Parasitology, 86: 59-83.

Shakerian, A., H. Ghafari Rad, S. Shekarforoush. 2008. Prevalence of Linguatula serrata nymphs in one-humped camel (Camelus dromedarius) in Najaf-Abad, Iran. Research in Veterinary Science, 84: 243-245.

Tavassoli, M., H. Tajic, B. Dalir-Naghadeh, F. Hairiri. 2007. Prevalence of Linguatula serrata nymphs and gross changes of infected mesenteric lymph nodes in sheep in Urmia, Iran. Small Ruminent Research, 72: 73-76.

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