Trematoda

(Flukes)

Phylum Platyhelminthes

Class Trematoda

Number of families Approximately 176

Thumbnail description
Parasitic flatworms ranging from less than 0.04 in (1 mm) to 23 ft (7 m) long, but usually 0.2–2 in (0.5–5 cm)

Evolution and systematics

The class Trematoda has about 6,000 species, although the number given varies considerably among different researchers. The class is commonly divided into two subclasses, Aspidogastrea and Digenea. Both are sometimes elevated to class level or dropped to order status; however, they will be treated in this text as subclasses of the class Trematoda. At one time, the class Monogenea was considered a subclass or order of the class Trematoda.

Recent studies of the evolution of trematodes indicate that the class may be paraphyletic—that is, it may represent only some of the descendants of a common ancestor; and that most of the species actually should be grouped together with the mollusks and annelids in the taxon Lophotrochozoa. Part of the difficulty in defining the placement of trematodes is that their fossil record is so sparse. Other than some fossil eggs dating from the Pleistocene epoch (1.8 million–8,000 years ago), historical evidence of trematodes consists mostly of trace fossils. Trace fossils are signs thought to have been left by an organism. For example, a trace fossil from a trematode might be a slight indentation on a fossil snail shell.

Despite the poor fossil record, scientists believe that Aspidogastrea is an ancient group, because many of its species, including those in the families Multicalycidae, Rugogastridae, and Stichocotylidae, use cartilaginous fishes as hosts. These fishes, which are in the class Chondrichthyes, evolved at an earlier point in time than the mammals and teleosts (bony fishes) generally used as hosts by digenetic trematodes. Species within the digenetic genera Nagmia and Probolitrema are exceptions to the rule, and will invade cartilaginous fishes.

A particularly noticeable synapomorphy of the two subclasses is the presence of a posterior sucker, which is manifested as the large, ventral disk in the subclass Aspidogastrea. In addition, both subclasses have life cycles that involve mollusks and vertebrates. Scientists still disagree about whether the former or the latter were the original hosts evolutionarily.

The subclass Aspidogastrea has four families with about 80 species and is often split into four orders. The subclass Digenea has about 6,000 species that are generally split into 10 major orders and numerous smaller orders. Frequently, taxa are switched from family to order status, so a total number of families and orders in this large subclass is difficult to ascertain.

Physical characteristics

Trematodes are parasitic flatworms, usually leaflike in appearance, with holdfast organs that they use to adhere to their hosts. Digenetic species typically use muscular, oral and/or

ventral suckers to attach to their hosts. Members of the subclass Aspidogastrea have a large ventral disk that they use for adhesion. This disk is covered with many small suckers known as alveoli.

Ventral suckers are generally about the same size as the oral suckers, and located centrally on the anterior, ventral surface. Often, the ventral suckers are quite close behind the oral sucker. Trematodes generally have one or two large, sometimes branched, testes, a comparatively small ovary, an often long and looping uterus, and a single common genital pore. They typically have a bifurcated intestine and blind caeca that exit the body through an anus or via an excretory vesicle. The integument lacks a cuticle.

Distribution

Trematodes are found around the world. The presence of their host species is often the limiting factor in their geographic distribution. For example, a flatworm that uses a mollusk as its host occurs only where that mollusk lives. Nonetheless, the distribution of a particular trematode can span large areas, particularly if their host species live in a broad range of habitats; or if members of the host species, like birds, are able to run or fly over vast regions.

In many cases, the species' distributions follow their hosts. For example, hosts of Uvulifer ambloplitis include snails, fishes, and birds. With such a complex life cycle, the trematode's distribution is a combination of the ranges of all three animals. As another example, the aspidogastrids infect mollusks, teleost fishes, and turtles, presenting another complex distribution pattern.

Habitat

The habitat of trematodes frequently varies over the course of their lives. Members of the subclass Digenea are endoparasites with indirect life cycles, which means that they infect different hosts during the various stages of their life cycles. Digenetic trematodes typically have two larval stages and at least two hosts. Several, including Halipegus occidualis, have four hosts, ending up at the base of the tongue of a green frog (Rana clamitans), which is the definitive host of H. occidualis. The life cycles of members of the subclass Aspidogastrea, which sometimes take a shorter path with only one host and no asexually reproducing larvae, are described as direct.

A typical digenetic individual begins its life as an egg in its so-called definitive host, and then passes with the host's feces either into water or onto land. After hatching, the larva takes up residence in a first intermediate host, which is often a mollusk. It then exits and moves to a second intermediate host, which is frequently either another mollusk, a fish, or an amphibian. The characteristic digenetic life cycle continues when the definitive host eats the secondary host, at which point the trematode infects the definitive host. Definitive hosts often include predatory mammals or birds.

Among species of Aspidogastrea, the life cycle is a bit simpler with usually only one host. After birth, the ectoparasitic species generally latch immediately onto the outside of a host organism, usually the skin or gills of bivalves or fishes. Endoparasitic species of Aspidogastrea infect such taxa as mollusks and fishes, but also the shark-like holocephalans and elasmobranchs.

Behavior

As described, the life cycle pattern of the digenetic trematodes is quite complex, involving first- and second-stage larvae as well as adults that are dependent on a host species for survival. Upon hatching, the first-stage larvae, known as miracidia, infect the first intermediate host, usually a mollusk. Many miracidia take advantage of light and gravitational cues to reach an area suitable to their hosts, then hone in on an individual host by following its chemical signature, which may be fatty acids or amino acids specific to the organism. Other miracidia, however, seem to stumble upon rather than track their host. In still other trematode species, the egg does not develop until it is eaten by the host species.

Once in the first intermediate host, the miracidium sheds the ciliated epidermal cells that the aquatic forms typically use to navigate the water. In the first intermediate host, the miracidia travel to a specific site, depending on the species of the trematode and of the host. Once there, the miracidium may develop into a saclike sporocyst and/or redia before generating cercariae. Cercariae are the larvae that finally exit from the mollusk and begin actively seeking the second intermediate host. Cercariae are generally propelled by a variety of different types of tails, although a few species, like Maritrema arenaria, have small or no tails and move by crawling rather than swimming. Cercariae use environmental cues, like light or water turbulence (in aquatic species), to seek out their secondary host. A few species, like Schistosoma mansoni and Trichobilharzia ocellata, also follow a chemical trail laid by the secondary host. Because cercariae are nonfeeding organisms, they must find a host quickly. The strong-swimming species generally need to locate a host more rapidly than slow-crawling species, with swimmers surviving only about 24 hours without a host, while crawlers can continue living without a host for several days.

Among digenetic trematodes, the species of several families of blood flukes, including the Schistosomatidae, Spirorchiidae, and Sanguinicolidae, skip the second intermediate host; their cercariae invade the definitive hosts directly. A few, like those of the families Azygiidae and Faciolidae, encyst on vegetation rather than in a secondary host. The definitive host then becomes infected by eating the trematode-infested vegetation. Other trematodes, such as Alaria species, add a larval stage that

forms after the cercaria and develops into the metacercaria. This stage is called the mesocercaria. Plagioporus sinitsini is an atypical trematode that can apparently take any of three paths from egg to adult. In the most intriguing of the three, these trematodes are able to bypass their usual second intermediate and definitive hosts, and develop into adults while still in the sporocysts of the first intermediate host. As a result, they can produce and hatch eggs, and release already-developed miracidia through the feces of their first intermediate hosts.

Cercariae enter the secondary host, drop their tails, and develop into metacercariae. Metacercaria look like the adults, except they lack reproductive organs. Often, the host can survive, ostensibly ignoring even heavy infestations with metacercariae. Young bluegills (Lepomis macrochirus ), on the other hand, die if they are infected with too many metacercaria of the species Uvulifer ambloplitis. In some cases, metacercariae can cause behavioral or morphological changes in the second intermediate host species that have the effect of making it more susceptible to predation by the definitive host. Trematodes in the genus Ribeiroia, for example, can trigger a frog to produce additional or fewer hind limbs. Such deformities effectively cripple the host, making it an easier target for birds, the definitive host.

Transmission to the definitive host usually results from the host's inadvertent ingestion of the metacercariae. From the digestive system, the metacercariae migrate to the target site, which varies by species, and reach their sexual maturity in that location.

Studies of trematode communities in the first intermediate host indicate that a single host carries no more than four different species of trematodes. The reason for this low number is under some debate. One hypothesis suggests that interspecific predation by redia keeps the number in check. Other researchers believe that temporal and/or spatial separation of trematode species accounts for the limit of four trematode species per host. There may also be limitations on space or other resources.

Members of the subclass Aspidogastrea have a simpler lifestyle than the digenetic trematodes. It usually involves just one host, often freshwater mussels or snails, in which development from egg to adult occurs. The larvae (cotylocidia) generally lack cilia, but some, like the larvae of Lophotaspis vallei, have cilia and are good swimmers. Nonciliated larvae, in contrast, creep rather than swim.

Feeding ecology and diet

Trematodes are obligate parasites, which means that they require nourishment from a host organism. Adult digenetic trematodes die soon after removal from the host, while members of Aspidogastrea may survive independently for a month or more.

Digenetic trematode first-stage larvae, or miracidia, do not feed. For this reason, they must find a first intermediate host very quickly, usually within one or two days of hatching. The eggs of some species don't even hatch until they are eaten by the first intermediate host. Miracidia develop into sporocysts, which also do not feed. The redia stage that often develops from the mother sporocyst in some taxa use their mouths to rip away and eat bits of host tissue. In fact, rediae will eat just about anything, including sporocysts of other species.

Adult trematodes attach to the host organism using suckers. They will eat blood cells, mucus, and loose cells; in some cases, they secrete enzymes that begin to digest tissue before consumption. Some genera, such as Schistosoma and Faciola species, adhere to the host in the blood vessels, liver, and other sensitive areas, inflicting damage to the host by releasing toxic materials through their excretory pores. In some cases, high numbers of trematodes can even plug small body passages or openings, like the host's ureter or bile duct; or interfere with digestion or respiration. Occasionally, mollusk hosts are so irritated by these tiny invaders that they begin coating them with layers of nacreous material, turning the trematodes into pearls.

Reproductive biology

Digenetic flukes engage in both asexual and sexual reproduction. When the first-stage larvae reach their destination within the first intermediate host, a polyembryonic asexual reproductive phase begins. After the larvae develop into sporocysts, the sporocysts of some species produce a second generation of sporocysts, while others produce rediae. Trichobilharzia physellae and Diplostomum flexicaudum take the two-generations-of sporocysts route. Metorchis conjunctus and Proterometra dickermani develop from miracidium to sporocyst to redia. A few species, including Stichorchis subtriquetres, go directly from miracidium to redia, bypassing the sporocyst stage altogether. The rediae are also capable of asexual reproduction to produce a second generation of rediae. Via sporocysts and rediae, the number of invading trematodes can multiply very quickly within the first intermediate host.

Both sporocysts and rediae produce the next stage, the cercariae and metacercariae. Cercariae are free-living and swim to the second intermediate host, which is typically a prey for the definitive host. Once on or in the second intermediate host, the cercariae transform themselves into metacercariae. Neither the cercariae nor metacercariae reproduce. The metacercariae finally enter the definitive host and become adults, which participate in sexual reproduction either by mating with a second fluke or by self-fertilization. Almost all trematodes are hermaphrodites. Some of these species, including members of the family Hemiuridae, even have fused male and female reproductive ducts. Members of the family Schistosomatidae are the exception. The schistosomatids have separate sexes with the adult females usually found coupled with adult males.

The eggs of both subclasses of trematodes are typically light-colored oval structures. The eggs of some species are embryonated (Heterophyes heterophyes) while others are not (Paragonimus westermani). Several species, including Metagonimus yokogawai and Opisthorchis felineus, have eggs that contain mature miracidia in addition to embryos. In digenetic trematodes, the eggs develop in a large loop-shaped uterus. The number of eggs varies by species, but production of several hundred per day is not unusual. The common digenetic marine trematode Cryptocotyle lingua can produce thousands of eggs over a 24-hour period. Trematode eggs exit the host through the feces. In some species, miracidia form in the egg before it is shed; more typically, however, the miracidia develop two or three weeks after oviposition. In a few digenetic species, the miracidium forms only after the egg is taken into the first intermediate host.

The life cycle of the subclass Aspidogastrea is simpler; it has no asexual phase of reproduction. The entire life cycle typically occurs in one host, usually a mollusk. Predators of the host species have been known to eat infected mollusks and temporarily harbor the flatworms. Flatworms can survive in the predator's digestive tract for a short period, but cannot reproduce or develop there. There are other exceptions. Mulicalyx cristata is thought to use marine crustaceans as intermediate hosts. After the crustaceans are eaten by sharks or rays, M. cristata matures in the gall bladder of the shark or ray.

Conservation status

No species of trematodes are listed by the IUCN as threatened.

Significance to humans

Trematodes pose a significant health threat to humans, particularly those living in developing countries. A common illness in developing countries is schistosomiasis. This condition, caused by three species of Schistosoma, affects more than 40 million individuals who live in tropical and subtropical countries, causing weakness, diarrhea, hemorrhage, fever, enlargement of the spleen, and other severe symptoms.

Other trematodes also infect humans, including the trematode Opisthorchis, which is transmitted to humans through eating infected fishes. Prevalent in parts of Russia, the fluke currently infects 1.2 million people, which is more than 4 percent of the region's population.

The cost for treatment of human fluke infections ranges into billions of dollars, in part because these conditions are frequently misdiagnosed. Treatment for infection by such organisms as Paragonimus species costs about $1, but the patient's illness is often misinterpreted as tuberculosis, which calls for years of expensive treatment.

Trematodes that infect such household pets as rabbits, dogs, and cats may cause gastrointestinal symptoms requiring veterinary treatment. In the case of dogs, the trematode Nanophyetus salmincola or so-called salmon-poisoning fluke, may cause a fatal disease resembling distemper because it carries a rickettsia (a type of bacterium) to which dogs are susceptible. The rickettsia, however, does not produce clinical disease in either humans or cats.

Trematodes can also infect livestock, sport and commercial fishes, and game mammals, which can have negative economic impacts on agriculture, sport fishing, and commercial fishing.

Species accounts

List of Species

No common name

Rugogaster hydrolagi

subclass

Aspidogastrea

family

Rugogastridae

taxonomy

Rugogaster hydrolagi Schell, 1973, vicinity of San Juan Island, Washington, United States.

other common names

None known.

physical characteristics

Adults have an elongated body 0.27–0.59 in (7–15 mm) long and 0.039–0.078 in (1–2 mm) wide without spines, but with a row of 17–25 transverse ridges or rugae on a small ventral sucker. It also has numerous testes and two caeca (large intestine) rather than the one caecum and one or two testes characteristic of other members of its subclass.

distribution

Southeastern coast of Australia; northwestern coast of United States and British Columbia.

habitat

Hosts include the ratfish (Hydrolagus colliei). The parasite inhabits the coecal glands, sometimes protruding into the rectum.

behavior

Adult flatworms infect the rectal glands of holocephalan fishes. (chimaeras).

feeding ecology and diet

These parasites rely for their nutritional needs on their host fishes, but little else is known about their feeding ecology.

reproductive biology

A large uterus contains numerous amber-colored eggs, which are oval and operculate, ranging from 0.006–0.0066 in (154–168 µm) long and 0.0036–0.004 in (92–102 µm) wide. The larvae, which do not reproduce, are 0.0104–0.011 in (265–288 µm) by 0.0027–0.0032 in (70–82 µm), and leaf-shaped with a rounded anterior end and a pointed posterior end. They have no cilia, but do have a posterior sucker.

conservation status

Not listed by IUCN

significance to humans

None known.

No common name

Aspidogaster conchicola

order

Aspidogastrida

family

Aspidogastridae

taxonomy

Aspidogaster conchicola von Baer, 1826, Anodonta, Unio Prussia.

other common names

None known.

physical characteristics

Adults are about 0.08 in (2.5–2.7 mm) long and 0.04 in (1.1–1.2 mm) wide, with a large sucker that covers almost the entire ventral surface of the organism. The body narrows to a neck-like region with a mouth at the front tip. The large ventral sucker has a windowpane pattern of sucking grooves. A lone testis is located in the middle of the posterior half of the body, and the ovary sits in the center and to one side of the animal. A common genital pore opens anteriorly about a quarter of the body length behind the mouth sucker.

distribution

Europe, North America, China, and Egypt.

habitat

Hosts are snails, including Viviparus malleatus and Goniobasis livescens; and such mussels as Anadonta grandis. Aspidogaster species use only one host. Sometimes, other species, like turtles, will eat infected mussels. The flukes can survive temporarily in the turtle's stomach.

behavior

Aspidogaster larvae use snails and mollusks as their hosts. Larvae apparently infect the host mollusk by entering its siphon. Various reports indicate that the flatworms enter the host either as larvae or as eggs containing larvae. Aspidogaster eggs hatch after they are eaten by freshwater snails or mussels. Eggs that are not eaten can survive for about two weeks. In snails, the newly hatched worms lack cilia and move about by creeping. The larvae migrate to the snail's intestines and then to the hepatopancreas, where they mature and lay eggs.

feeding ecology and diet

Parasites feed on host epithelium and mucus using the anteriroly located mouth.

reproductive biology

The entire life cycle of Aspidogaster from egg to adult to production of the next generation of eggs takes about 270 days at 68°F (20°C). Unlike digenetic trematodes, the life cycle of this species and other members of the subclass Aspidogastrea occurs in just one host and does not involve asexual reproduction. The eggs are oblong, operculate (having a small covering structure), and about 0.005 in (128–130 µm) long and 0.0019 in (48–50 µm) wide. Juveniles, which have a shape similar to the adults, grow from about 0.02 in (0.5 mm) in length to 0.05–0.06 in (1.25–1.5 mm).

conservation status

Not listed by IUCN.

significance to humans

None known.

No common name

Nematobothrium texomensis

order

Azygiida

family

Didymozoidae

taxonomy

Nematobothrium texomensis McIntosh and Self, 1955, entangled among buffalo fish ovaries, Lake Texoma, Willis, Oklahoma, United States.

other common names

None known.

physical characteristics

One of a group of worms that are generally long and thin, the adults of this species can reach 8.2 ft (2.5 m) in length. A ventral sucker is not evident and may be lacking in most specimens. It has little musculature, even in its oral sucker, which is completely enclosed in its integument (covering). It is transparent to slightly opaque.

distribution

Arizona, Arkansas, Kentucky, and Oklahoma.

habitat

This species is generally found in the gravid (pregnant) ovaries and occasionally in mature testes of the buffalo fish (Ictiobus species). In some cases, the worm can extend several inches outside the host organism through the fish's genital opening. Including this flatworm species, only a few other didymozoids infect freshwater fishes. Its snail host is unknown as of 2003.

behavior

The hermaphroditic adult worms live only as long as the fish remains gravid, and the worms probably shed their eggs as the adults perish and disintegrate into fragments.

feeding ecology and diet

Like other parasitic flatworms, this species is dependent on its host, the buffalo fish, to fulfill its nutritional needs.

reproductive biology

N. texomensis reproduces in the spring, shedding its eggs according to the reproductive cycle of its host. Eggs of this species are round and thin-shelled structures ranging from 0.0005–0.001 in (13–30 µm) in diameter. Usually within a few days of being shed, miracidia develop. The miracidia resemble amebas in shape, lack cilia, and move slowly. They are armed with small spines.

conservation status

Not listed by the IUCN

significance to humans

None known.

Echinostome

Echinostoma revolutum

order

Echinostomida

family

Echinostomidae

taxonomy

Echinostoma revolutum Froelich, 1802.

other common names

French: Échinostome.

physical characteristics

Adult echinostomes range from 0.24–1.3 in (6–30 mm) long and 0.02–0.06 in (0.6–1.6 mm) wide. Echinostomes have a tegument (outer surface) carrying spines or papillae (small rounded projections) and an anterior collar consisting of 37 spines arranged in a characteristic pattern. The ventral sucker is slightly behind the oral sucker. The uterus takes up much of the front half of the body and two testes follow, one after another, in the posterior half. The comparatively small ovary is located in the center of the animal.

distribution

Europe and Asia.

habitat

Echinostome eggs hatch in freshwater. The first intermediate hosts are lymnaeid snails. Common snail hosts in the United States and Europe belong to the genus Lymnaea. Second intermediate hosts include frogs, mussels, turtles, and snails; definitive hosts include various waterfowl, chickens, and other birds. Flukes attach to the mucosa or the ileum.

behavior

Echinostome eggs hatch in nine to 12 days in freshwater habitats. The miracidia can survive for only six to eight hours, so these fast swimmers must find snail hosts quickly. Penetration typically occurs along the mantle edge or foot of the snail. After developing into sporocysts, the eggs then undergo two or three generations of asexual reproduction as rediae, finally resulting in the development and release of cercariae. The progress from miracidia to cercariae takes about a month. The cercariae then swim and/or crawl to a second snail, a fingernail clam, a tadpole, or a silurid fish. The larval forms of this fluke use chemotaxis (orientation toward or away from a chemical stimulus) to detect snail slime trails and find their first intermediate hosts. They also engage in a searching method that uses such environmental stimuli as light and gravity. The cercariae burrow into snails and clams, where they encyst in soft tissue; but enter tadpoles and fish through the cloaca, eventually encysting in the kidneys.

Birds then devour the infected snails, clams, tadpoles, or fishes, and become the definitive hosts of echinostomes. Humans who eat raw or undercooked frogs also become definitive hosts. The metacercariae migrate to the cecum, small intestine, or rectum, and attach themselves to these organs with oral and ventral suckers. The hermaphrodites mature in the host's digestive tract, engage in self-fertilization, and lay eggs. In the laboratory, adult echinostomes live four to eight weeks. The eggs are transmitted to the environment via the feces.

feeding ecology and diet

As with other trematodes, these parasitic flukes depend on host species to supply their nutrition. These species include Lymnea or Planorbis snails as first intermediate hosts; snails or tadpoles as second intermediate hosts; and ducks, geese, chickens, partridge, pigeons, or humans as definitive hosts.

reproductive biology

Echinostomes reproduce asexually as larvae, and sexually as adults. The yellowish eggs range from 0.0034–0.0044 in (88–113 µm) in length and about 0.024 in (61 µm) in width; the flukes may produce as many as 3000 per day. The miracidia have four rows of epidermal plates and papillae on the body. The cercariae have a 37-spined anterior collar like that of the adults, and a robust unforked tail. Mature flukes are hermaphrodites and self-fertilize.

conservation status

Not listed by IUCN.

significance to humans

People who eat raw snails or frogs may become infected with this parasite. Symptoms appear about two to three weeks later. Hemorrhagic enteritis (inflammation of the intestines) may result from severe infections. Milder infections typically cause weakness and weight loss.

Liver fluke

Fasciola hepatica

order

Echinostomida

family

Fasciolidae

taxonomy

Fasciola hepatica Linnaeus, 1758, "in aquis dulcibus ad radices lapidum, inque hepate pecorum. Diss. de Ovibus;" Europe.

other common names

English: Sheep liver fluke; French: Grande douve du foie, douve du foie de mouton; German: Großer Leberegel.

physical characteristics

Adult liver flukes may reach 1.7–2.2 in (4–5 cm) in length and 0.6 in (1.5 cm) wide. They are typically about 1.3 in (3 cm) long, 0.4 in (1 cm) wide, and have a spiny tegument. They taper toward the rear. The front end bears an oral sucker and a cone-shaped tip. The sucker on the fluke's ventral (lower) surface is larger than the oral sucker. The ventral sucker is about a third of the body length behind the oral sucker. The branched ovary is situated behind and to the side of the ventral sucker about a third of the way back in the body. The testes are also branched and extend throughout the body behind the ovary.

distribution

Worldwide, but found most often in Europe and Latin America in habitats congenial to their freshwater snail and definitive hosts.

habitat

Liver flukes are found in swampy, generally wet freshwater areas inhabited by snails, especially of the species Lymnaea truncatula, Stagnicola bulimoides, and Fossaria modicella. Snails are their sole intermediate host. The definitive hosts of this fluke include grazing herbivores (in the bile ducts) primarily, including sheep and cattle, but also dogs, cats, rabbits, and humans.

behavior

The eggs, deposited in the environment in the definitive host's feces, hatch in freshwater areas, usually within about 10 days, longer if temperatures are cool. They have been known to survive in particularly cold water for several years. The embryos develop into miracidia, which quickly swim to and penetrate the soft tissue of snails. Miracidia can survive only 24 hours in the free-living state. Sporocysts form and produce first-generation rediae, which in turn produce second-generation rediae and eventually numerous cercariae. The cercariae live in the snail for 4–8 weeks, then exit and swim to vegetation lying just below the water line. There, they drop their tails and encyst. Passing herbivores become infected when they eat the vegetation, often grass. Humans typically become infected by drinking water containing flukes or by eating vegetation such as watercress. The flukes travel to the abdominal cavity in the first 24 hours, then to the liver over the next few days. Research indicates that immature flukes are able to orient during their migration from the duodenum (the first section of the small intestine) toward the liver. Within six to eight weeks, they reach the bile ducts, sometimes spreading to the lungs, where they mature and lay eggs. The eggs are then carried to the duodenum and pass into the feces.

feeding ecology and diet

This parasitic digenetic fluke has two hosts: Lymnaea species as the intermediate host, and wild or domesticated ruminants as the definitive host. Humans may become secondary hosts. The fluke feeds on bile duct lining, causing calcification of the duct.

reproductive biology

The tan or yellow eggs are about 0.0048–0.006 in (120–150 µm) long and 0.0025–0.0035 in (65–90 µm) wide. In warm water (78.8°F or 26°C), they develop into miracidia in less than two weeks. The miracidia are ciliated, and somewhat triangular in shape with the front end being broader than the rear. The front end also has a noticeable slender outgrowth with two eyespots behind it. The cercariae, which range from 0.0098–0.013 in (250–350 µm) long, resemble tadpoles in shape with a bulbous anterior end and long tail making up about two-thirds of the overall length. In artificial laboratory conditions, adult flukes have been known to survive as long as 11 years.

conservation status

Not listed by IUCN.

significance to humans

Infected humans may develop symptoms ranging from skin inflammation to pneumonia. Fluke infection can result in massive hemorrhages in horses, a reduction of milk production in dairy cattle, and mortality in sheep. Sheep mortality is often caused by bacterium Clostridium novyi, which thrives on the infected livers of sheep.

Oriental liver fluke

Clonorchis sinensis

order

Opisthorchiida

family

Opisthorchiidae

taxonomy

Clonorchis sinensis Cobbold, 1875. Some scientists now use the genus designation Opisthorchis for this fluke.

other common names

English: Chinese liver fluke; French: Douve du foie chinoise, douve du foie orientale; German: Chinesischer Leberegel.

physical characteristics

The adults are flattened cigar-shaped flatworms 0.4–1.0 in (10–25 mm) long and 0.1–0.2 in (3–5 mm) wide. The pointed front end has an oral sucker at its tip. Much of the anterior half of the animal is filled with a looping uterus. A small, slightly lobed ovary follows with two large branching testes located in the posterior half of the body. The genital pore opens about a fifth of the body length behind the oral sucker. The ventral sucker is circular and located slightly behind the oral sucker.

distribution

East Asia, including Japan, much of China, and Korea.

habitat

This organism begins its life as an egg passed in the feces of a human or other mammal. It then infects snails, followed by one of more than 100 species of fish, and finally humans or other fish-eating mammals.

behavior

After the eggs are passed into the water, they are eaten by the first intermediate host, which is a snail (Bulimus species or Parafossarulus manchouricus). The miracidia hatch in the intestine, form a sporocyte, generate rediae, and finally cercariae. Individual rediae can produce as many as 50 cercariae, which exit the snail into the water and begin the search for a second intermediate host. Clonorchis sinensis has an unusual method of searching; its cercariae sink until they hit either the bottom or some other structure, then swim to the surface to sink again. While bouncing back and forth between the surface and the bottom, cercariae that encounter a fish burrow through the skin and encyst in its muscle tissue. These second intermediate hosts are usually freshwater fishes of the Cyprinidae family, in addition to at least nine species of fishes from eight other families and possibly a few freshwater shrimp. The cercariae remain in the second intermediate host until the definitive host, which may be a human or other mammal, eats the fish. The flukes, now metacercariae, encyst in the host's small intestine and transform themselves into immature flukes, which then migrate to the bile ducts in the host's liver. There, the fluke matures in about three weeks and lays eggs that exit the host in the feces.

feeding ecology and diet

As a parasitic organism, Clonorchis sinensis relies on hosts to meet its dietary needs. Snails serve as hosts for its miracidia, fishes for its cercariae and metacercariae, and humans or other fish-eating predators for the adult flukes. Sporocysts form in snails. Metacercarial encyst in fishes. Adults live in the small bile ducts of the liver of definitive hosts and dine on their blood.

reproductive biology

Adults are hermaphroditic. Adult liver flukes can lay as many as 4000 eggs per day. The operculate eggs are shaped like light bulbs, yellowish brown in color, and range from 0.0009–0.001 in (25–35 µm) long and 0.0004–0.0007 in (11–20 µm) wide. The miracidia are ciliated and ovate with a short anterior protrusion. The cercariae resemble tadpoles with long tails. The life span of Clonorchis sinensis is at least 10 years, reportedly reaching 30–40 years.

conservation status

Not listed by IUCN.

significance to humans

Clonorchiasis is a disease that commonly affects people in parts of Asia, where people may eat uncooked infected fishes. Infections in other parts of the world result from eating imported infected fishes. Transmission of Clonorchis sinensis via infected dried, salted, smoked, or pickled fish has also been reported.

Lancet fluke

Dicrocoelium dendriticum

order

Plagiorchiida

family

Dicrocoeliidae

taxonomy

Dicrocoelium dendriticum Rudolphi, 1819, intestine of Xiphias gladius, a swordfish (probably in error).

other common names

English: Lancet liver fluke; French: Petite douve du foie; German: Kleiner Leberegel, Lanzettegel.

physical characteristics

Adult lancet flukes have translucent bodies shaped like long, thin leaves. Both oral and ventral suckers are located toward the front of the body, with the foremost oral sucker a bit smaller than the others. This species averages about 0.02–0.06 in (5–15 mm) long and 0.04–0.08 in (1–2.5 mm) wide.

distribution

Northeastern United States; Australia; northern and central Europe; Asia; and Africa.

habitat

Dicrocoelium dendriticum prefers dry habitats. It begins its life as an egg in the feces of its definitive hosts. Its first intermediate hosts are terrestrial snails, including Helicella species and Cionella lubrica; its second intermediate hosts are ants (Formica fusca); and its definitive hosts include various mammals, including sheep, cattle, and pigs, as well as cottontail rabbits, deer, and woodchucks. In snails the miracidia hatch in the intestine, then migrate through the intestinal wall. In ants, metacercariae encyst in the gaster. In the definitive hosts, immature flukes leave the metacercaria cysts and migrate to the common bile duct.

behavior

The eggs of lancet flukes are found on dry land, where they are eaten by snails, including Cionella lubrica in the United States. Hatched miracidia develop into sporocysts that in turn produce a second generation of sporocysts. The sporocysts transform into cercariae and migrate to the snail's lung cavity. The snail encases as many as 400 cercariae in mucus, then ejects the slime balls thus formed through its respiratory pore. Ants (Formica fusca) become the second intermediate host by ingesting the slime balls. While most of the infection in ants occurs in the hemocoel (spaces between the cells and tissues), some still-immature flukes make their way into the subesophageal ganglion (cluster of nerve cells underneath the eosphagus), which causes the ants' behavior to change. The ants are impelled to climb to the tips of grass blades. When the temperature drops at night, the ants' jaws clamp onto the grass, and keep them attached to the grass until temperatures rise the next morning. Herbivores grazing early in the morning inadvertently eat the ants with the foliage and become infected with the flukes. The metacercariae travel to the new host's bile duct, gall bladder, and pancreatic ducts, where they mature and lay their eggs. The mammals eliminate the eggs in their feces, and the life cycle repeats.

feeding ecology and diet

Lancet flukes meet their nutritional needs through various hosts, including snails, ants, and plant-eating mammals. In snails, mother sporocysts form, giving rise to daughter sporocysts and finally cercariae.

reproductive biology

Adults are hermaphroditic. The dark brown, ovate eggs are operculate, about 0.0014–0.0019 in (36–48 µm) long and 0.0008–0.0012 in (22–30 µm) wide. The cercariae are long with nipped-in "waists." The fluke's anterior portion is ovate and the posterior portion tapered.

conservation status

Not listed by the IUCN.

significance to humans

When left untreated, infected livestock may develop progressive hepatic cirrhosis. In sheep, the condition can reduce reproductive capacity and wool production.

Salmon-poisoning fluke

Nanophyetus salmincola

order

Plagiorchiida

family

Troglotrematidae

taxonomy

Nanophyetus salmincola Chapin, 1927, dogs, Canis lestes, Procyon psora pacifica, Lynx fasciatu.

other common names

None known.

physical characteristics

The ovate adult form of N. salmincola is about 0.03–0.08 in (0.8–2.5 mm) long and about 0.011–0.3 in (0.3–0.8 mm) wide. Two similar-sized suckers are present, one located at the anterior edge, and the other about a third of the way back on the body. The tegument is spiny. The pair of testes are large oval structures that extend from the central to the posterior body. In contrast, a small round ovary is located near the ventral sucker. A genital pore opens just behind the ventral sucker.

distribution

North Pacific basin, stretching from the Columbia River basin through British Columbia to Alaska.

habitat

N. salmincola is a fluke of freshwater streams when it is not infesting other animals. The eggs hatch in fast-moving streams, the miracidia infect snails (commonly Oxytrema silicula), and the cercariae penetrate the skin of frogs and fish, especially salmon and trout. The definitive hosts include birds and mammals, particularly skunks and raccoons, and occasionally humans. Immature and adult flukes inhabit the wall of the small intestine. Cercariae live free (not embedded) in the snail's tissues and enter the muscular tissue of fishes.

behavior

The eggs of this parasitic flatworm incubate in freshwater streams for a period of about three to seven months. The newly hatched miracidia randomly find and then burrow into snails, where they develop into cercariae. The cercariae exit the snails and move in random patterns through the water. They can survive in this free-living form for as long as two days. When they encounter a frog or fish, they quickly penetrate its tissue—a process that takes 30–120 seconds—and migrate to the muscles, kidneys and fins. The host sometimes dies from heavy infestations. Migratory fishes like salmon may carry N. salmincola many miles. Predatory birds and mammals ingest infected fish and frogs, and the flatworms encyst in the small intestine, where they mature within seven days and lay eggs. The eggs pass from the definitive host in the feces, and the life cycle begins again.

Salmon poisoning in dogs and other canids is often blamed on N. salmincola. The actual poisoning agent is a rickettsia bacteria known as Neorickettsia helminthoeca, which infects all life stages of N. salmincola. If untreated, infection by N. helminthoeca causes distemper-like symptoms and may be fatal in dogs. It does not, however, affect humans or cats. Dogs should never be fed raw salmonids.

feeding ecology and diet

N. salmincola is dependent on hosts to meet its nutritional needs. Its hosts include the snail Oxytrema silicula as the first intermediate host, salmonid fish as the second intermediate host, and a variety of fish-eating mammals, including dogs, cats, and humans, as definitive hosts. Metacercarial encyst in fishes. Immature flukes in dogs attach to the intestinal wall.

reproductive biology

The unembryonated eggs of N. salmincola are yellowish brown in color, and about 0.003–0.0039 in (80–100 µm) long and 0.0015–0.0019 in (40–50 µm) wide. Incubation may take from 87–200 days at room temperature. The rediae are elongated with birth pores located toward the front. The cercariae are also elongated, but have a ventral sucker and short tail. Thousands of cercariae may be deposited at a time in long strings of mucus.

conservation status

Not listed by IUCN.

significance to humans

Humans who eat raw or underprocessed infected fish are susceptible to the disease called nanophyetiasis or "fish flu," but such cases are rare. The symptoms of fish flu, which arise 5–8 days after eating infected fish, may include diarrhea or abdominal discomfort. Humans are unaffected by N. ricksettia, which is carried by N. salmincola, but such an infection can be fatal to dogs if left untreated. Heavy infestations in salmon and trout may cause some losses in populations of these sport fishes.

Black-spot flatworm

Uvulifer ambloplitis

order

Strigeatida

family

Diplostomatidae

taxonomy

Uvulifer ambloplitis (Hughes 1927) Ceryle alcyon, Helisoma trivolvis, H. campanulatum, Ambloplitis rupestris, Micropterus dolomieu, Aplites salmoides, Eupomotis gibbosus, Apomotis cyanellus, Enneacanthus obesus.

other common names

English: Black grub.

physical characteristics

Adults are spoon-shaped with a broad body, thinner "neck," and a slightly broader cocked "head." The oral sucker is small and foremost on the fluke, with a small ventral sucker about halfway back on the head, and a holdfast organ just behind the central sucker. Adults range from 0.08–0.09 in (1.8–2.3 mm) long. Two testes are present, one in front of the other in the posterior half of the animal. The comparatively small ovary is located in front of the anterior testis. A common genital pore opens at the posterior tip of the animal.

distribution

Northern tip of South America, Central America, and much of North America.

habitat

The first intermediate hosts are snails, including Helisoma trivolvis. Second intermediate hosts are commonly green sunfish (Lepomis cyanellus) and bluegill (L. macrochirus). The most common definitive host is the bird known as the belted kingfisher (Megaceryle alcyon). Sporocysts migrate to the digestive gland and liver of snails. Cercarial bore through the skin of fish, and cysts appear.

behavior

Eggs of this species hatch into miracidia within a month. The ciliated miricidia burrow into their snail intermediate hosts, and develop into first-generation sporocysts. Second-generation sporocysts spread to the snail's digestive gland and liver, where they produce cercariae about six weeks after the initial infection. The cercariae leave the first intermediate host, swim to, and penetrate the skin of sunfish, bass, perch, and other fishes. They drop their tails and develop into metacercariae that encyst and are surrounded by host melanocytes that appear as hard black spots in the fish's skin. (Other species of Diplostomatidae and Strigeidae also produce black spots in fishes.) When kingfishers eat the infected fish, the worms mature within the host's intestine in about a month. Eggs deposited are passed by the bird through its feces into the snail's environment.

feeding ecology and diet

The black-spot flatworm depends for its nutrition on host species, including the ram's horn snail (Helisoma species); percid fishes; and birds, especially belted kingfishers.

reproductive biology

Eggs are about 0.00004 in (1 µm) long and 0.00002 in (0.5 µm) wide; the miracidia are ovate and broader at the anterior end. The life cycle of the black-spot flatworm follows the prevalence and activity of its two host species. Cercariae begin appearing in the fish hosts in late spring following a 21-day development period. The snails continue to shed cercariae throughout the summer. The cercariae resemble tadpoles with a forked tail.

conservation status

Not listed by IUCN.

significance to humans

Infections with metacercariae appear as black spots in several species of game fish. Their appearance sometimes discourages humans from eating them, even though there is no danger, especially when cooked. "Blackspot disease" is sometimes fatal to fish fry.

Human blood fluke

Schistosoma mansoni

order

Strigeatida

family

Schistosomatidae

taxonomy

Schistosoma mansoni Sambon, 1907, Africa.

other common names

French: Schistosome intestinal; German: Pärchenegel

physical characteristics

A sexually dimorphic species, the female is thin and cylindrical, reaching between 0.5–1 in (1.2–2.5 cm) in length. The male is elongated but thicker, and reaches 0.39–0.78 in (1–2 cm) in length. He also has small spiny oral and ventral suckers, and a wrinkled dorsal surface dotted with tubercles (small nodules). A female typically exists in the male's gynecophoric canal, absorbing nutrients by diffusion from the male.

distribution

The human blood fluke is found in warm regions around the world, particularly in developing countries in South America, Africa, the Caribbean, and the Middle East.

habitat

Larvae of this digenetic parasitic flatworm infect the hepatic pancreas of freshwater snails of the genus Biomphilaria. Adult worms infect mesenteric veins of mammals ranging from rodents, dogs, cattle, and baboons to humans.

behavior

Eggs, which have spines, lodge in the intestinal mucosa and cause ulceration as well as the formation of granulomata (lesions that result from a chronic inflammation). The eggs hatch in freshwater areas and develop into miracidia, which follow chemical, light and gravitational cues to find and then penetrate the soft tissues of the snails. A sporocyst then forms. Cercariae develop within the sporocyst. The cercariae leave the snail by swimming and actively seek out their next host, apparently targeting certain fatty acids of the skin. They then penetrate the skin of a secondary host, which may be a human being or other mammal. Once in the host, they become immature flukes called schistosomules, migrate to the circulatory system, and travel to a site (specifically the superior and inferior mesenteric veins and related smaller veins) near the large intestine. Once in the mesenteric veins, they mature, mate, and lay eggs, many of which leave the host's body with the feces. The cycle begins again when the eggs make their way into the freshwater habitat of the snail.

feeding ecology and diet

The hosts of the human blood fluke include Biomphilaria snails and mammals, including humans. They enter both snails and mammals by burrowing into the skin and other soft tissue. They feed on blood from the hepatic and mesenteric veins.

reproductive biology

Adult males are typically found conjoined with the females, with the female remaining in the male's spine-covered gynecophoric canal, a groove that runs along the lower surface of the body. Larger spines cover the lateral margins of the canal, which suggests that they may play a role in mating. The eggs, which bear a lateral spine, range from 0.0045–0.0068 in (115–175 µm) long and 0.0017–0.0027 in (45–70 µm) wide. The free-swimming miracidia are tadpole-like in appearance with a tail slightly smaller than the body. The cercariae are about 0.019–0.039 in (0.5–1 mm) long, with constricted waists and forked tails.

conservation status

Not listed by IUCN.

significance to humans

Infection with this species results in schistosomiasis, also known as bilharziasis, in humans. The condition causes abdominal pain, dysentery, lethargy, and anemia, leaving the victim weak and susceptible to other diseases.

Resources

Books

Doss, Mildred A. Index Catalogue of Medical and Veterinary Zoology: Trematoda, Parts 1–8. Washington, DC: U. S. Government Printing Office, 1966.

Olsen, O. Wilford. Animal Parasites: Their Biology and Life Cycles. Minneapolis: Burgess Publishing Co., 1967.

Schell, Stewart C. How to Know the Trematodes. Dubuque, IA: William C. Brown Co., Publishers, 1970.

Periodicals

Combes, C., A. Fournier, H. Moné, and A. Théron. "Behaviours in Trematode Cercariae That Enhance Parasite Transmission: Patterns and Processes." Parasitology 109 (1994): S3–S13.

Esch, G. W., M. A. Barger, and K. Joel Fellis. The Transmission of Digenetic Trematodes: Style, Elegance, Complexity." Integrative and Comparative Biology 42, no. 2 (2002): 304–312.

Esch, G. W., E. J. Wetzel, D. A. Zelmer, and A. M. Schotthoeffer. "Long-Term Changes in Parasite Population and Community Structures: A Case History." American Midland Naturalist 137 (1997): 369–387.

Kanev, I. "Life-Cycle, Delimitation, and Redescription of Echinostoma revolutum (Froelich, 1802) (Trematoda: Echinostomatidae)." Systemic Parasitology 28 (1994): 125–144.

Machado-Silva, J. R., R. M. Lanfredi, and D. C. Gomes. "Morphological Study of Adult Male Worms of Schistosoma mansoni Sambon, 1907 by Scanning Electron Microscopy." Memorias do Instituto Oswaldo Cruz Online 92, no. 5 (1997): 647–653.

Maurice, J. "Beware the Flukes of Nature." World Press Review 41 (June 1994): 41.

McCarthy, H. O., S. Fitzpatrick, and S. W. B. Irwin. "Life History and Life Cycles: Production and Behavior of Trematode Cercariae in Relation to Host Exploitation and Next-Host Characteristics." Journal of Parasitology 88, no. 5 (2002): 910–918.

Self, J. T., L. E. Peters, and E. D. Davis. "The Egg, Miracidium and Adult of Nematobothrium texomensis." Journal of Parasitology 49, no. 5 (1963): 731–736.

Yoshimura, H. "The Life Cycle of Clonorchis sinensis: A Comment on the Presentation in the Seventh Edition of Craig and Faust's Clinical Parasitology." Journal of Parasitology 51, no. 6 (1965): 961–966.

Organizations

American Society of Parasitologists. Web site: <http://asp.unl.edu>

Helminthological Society of Washington. c/o Allen Richards, Ricksettsial Disease Department, Naval Medical Research Center, 503 Robert Grant Ave., Silver Spring, MD 20910-7500 United States.

Leslie Ann Mertz, PhD