Monogenea

(Monogeneans)

Phylum Platyhelminthes

Class Monogenea

Number of families 53

Thumbnail description
Flatworm parasites that live mainly on fish skin and gills, with a haptor (posterior attachment organ) containing hooks, and a direct (single host) life cycle

Evolution and systematics

The origins of the monogeneans are obscure, but it is assumed that they evolved from free-living ancestors similar to modern turbellarians (aquatic flatworms). Their nearest relatives are the cestodes (tapeworms). The naming of their upper-level taxa (biological categories) is controversial. "Monogenea" is widely accepted as the name of the class itself, as is the subdivision of the class into two orders, namely the Monopisthocotylea and the Polyopisthocotylea. More recently, the name "Monogenoidea" has been proposed for the class, with the class being subdivided in turn into three subclasses. The first-mentioned, older, and more widely supported scheme is followed here. Some believe that the Monopisthocotylea and the Polyopisthocotylea have separate origins; that is, they think that Monogenea is not a monophyletic (descended from a common ancestor) class. As of 2003, 53 families of monogeneans are recognized.

Physical characteristics

Like other platyhelminths, monogeneans are acoelomate animals; that is, they do not have a body cavity lying between the body wall and the digestive tract. Their bodies are covered by a living syncytial tegument. The digestive system consists of a pharynx, which is a muscular tube used to suck in food, and a saclike or branched intestine with no anus. The pharynx may or may not be glandular. Monogeneans range in length from about 0.04–0.08 in (1–2 mm), as in some gyrodactylids, to more than 0.75 in (2 cm), as in some capsalids. Large monogeneans tend to be flat and leaf-shaped, but the smaller parasites are usually cylindrical. In general, these flatworms are colorless and semitransparent. When on fish skin some may be virtually invisible to the human eye, either by virtue of their glass-like transparency or because they contain scattered pigment that matches pigment in the host's skin. These features may protect the parasites from being eaten by predatory fishes or crustaceans ("cleaner" organisms). The brown/black coloration of the polyopisthocotyleans is associated with their digestive system and derived from their blood meals.

The most significant anatomical feature of monogeneans is their possession of a posterior attachment organ or haptor armed with hooks. The hooks usually fall into two groups: small hooklets, which are often called marginal hooklets, and larger hooks called hamuli or anchors. The hooklets are essentially found in larvae although they often persist, usually without further growth, in adult monogeneans. The hooklets are specialized for attachment to the upper layer of cells (epidermal cells or Malpighian cells) in the host's skin; they fasten themselves in the web of filaments made of keratin known as the terminal web, which lies beneath the apimal membrane of the host epidermal cell. A basic and maximum number of 16 hooklets occurs in monopisthocotyleans and in polyopisthocotyleans, although they may be reduced to 14, 10, or lost altogether. In many but not in all monogeneans, the hooklets are supplemented as the parasite grows by one or two pairs of hamuli, which are usually large enough to penetrate through the epidermis (the outer layer of the host's skin) into the dermis, which is the thicker layer of skin just below the epidermis. Some monopisthocotyleans have haptors that become more elaborate during their development, either by acquiring glands or by subdividing into separate small compartments that function as suckers. As typical polyopisthocotyleans grow, they develop three or four pairs of muscular suckers or clamps; each one is at the site of a hook-let. Many monopisthyocotyleans are able to move like leeches since they have suckers or glands that secrete sticky material on the lateral borders of the head.

The ovary consists of a germarium, which produces egg cells, and an extensive vitellarium that produces vitelline cells. The vitelline cells do not contain genetic material; they secret substances that form a chemically and physically resistant eggshell of tanned protein (sclerotin) and provide food for the growing embryo. Gyrodactylids are exceptional viviparous. Monogeneans are hermaphrodites; many have hard structures (sclerites) supporting the penis, while others have an eversible cirrus. There may be one or more vaginae, often with supporting sclerites, but hypodermic impregnation (through the skin) also takes place.

Distribution

Monogeneans are found worldwide in freshwater and marine environments.

Habitat

Many monogeneans are strictly host-specific; that is, they are limited to a single or a few closely related hosts. Skin parasites may be widespread on the surface of the host's skin or concentrated in specific areas. Many monopisthocotyleans use two pairs of counter-rotating hamuli, one pair on their ventral surface and one pair on the dorsal surface, to attach themselves between two adjacent secondary gill lamellae on one of the fish's primary lamellae. The monocotylid monopisthocotyleans are parasites of elasmobranch fishes, and must occupy internal sites such as their nasal fossae (cavities), body cavity, and cloaca. Another monopisthocotylean, Amphibdella, spends its early life inside the heart of an electric ray, moving to the gills when it is an adult and releasing its eggs into the ray's gill cavity. Many polyopisthocotyleans use their clamps to grip one or two secondary gill lamellae. Other polyopisthocotyleans (polystomatids) use suckers to attach themselves inside the bladders of frogs and toads, or the bladders or mouths of freshwater turtles. Oculotrema hippopotami is the only monogenean that infests a mammal; it is a polystomatid that lives beneath the eyelids of the hippopotamus. The gyrodactylid Isancistrum lives on the skin of squids and is the only monogenean parasite that infests an invertebrate.

Behavior

Many monogeneans migrate, moving like leeches from their site of initial attachment to the host to the site where they mate and lay their eggs. How they find their way within the host is mostly unknown as of 2003. Many monopisthocotyleans retain the ability to change their location on the host throughout their lives. Most adult polyopisthocotyleans, however, are sedentary. Some skin parasites ventilate their bodies by undulating while some juvenile and adult parasites are able to swim.

Feeding ecology and diet

Most monopisthocotyleans feed on the epidermis of their host, which is eroded by a protrusible glandular pharynx. Polyopisthocotyleans are blood feeders. These parasites accumulate indigestible residues of brown/black hematin (a pigment found in blood) from their blood meals in their digestive tract, which they eject at intervals through their mouths.

Reproductive biology

Monogeneans are hermaphrodites, with the male reproductive system usually first to mature. This characteristic is known as protandry. Mutual or unilateral insemination may occur, although self-insemination also takes place. The tanned eggs are assembled in an egg mold or ootype; the vitelline cells provide the raw material for the shell and resources for the developing embryo. With the exception of the viviparous gyrodactylids, the eggs are released into the environment and produce infective larvae (oncomiracidia) which are able to swim freely with the help of cilia. The larvae of many monogeneans hatch spontaneously at a particular time of day, which often coincides with times when the host is particularly vulnerable to invasion. Hatching may also be triggered by such host-derived cues as chemicals, mechanical disturbance, or shadows. The oncomiracidia do not feed until they reach the host, which means that their survival as free-living organisms and their potential for host infection are limited, usually to a period of several hours. The oncomiracidia throw aside their ciliated cells when they reach the host. Entobdella soleae can infect new hosts by direct transfer of adults or juveniles, as well as by eggs and oncomiracidia. The juveniles of a related parasite can swim and may reach new hosts in this way.

The gyrodactylids are unique among monogeneans. They have abandoned freely deposited eggs and free-swimming oncomiracidia; they are viviparous, producing offspring that are usually full size at birth. They increase their reproductive rate by telescoping generations; their offspring already contain a partly developed embryo at birth and sometimes a second smaller embryo within the first. The appearance of the male reproductive system is delayed until after the female reproductive system is operational. This characteristic, which is known as protogyny, helps to concentrate the organism's resources on embryo development. The first two offspring are probably produced asexually. Gyrodactylids usually spread to new hosts by direct transfer when infected hosts make contact with one another. In addition, however, the hosts may be infected by gyrodactylids drifting freely in the water column or by making contact with parasites attached to the substrate. There is also one record of a gyrodactylid that can swim.

Conservation status

No species of monogeneans are listed by the IUCN.

Significance to humans

In the wild, the number of monogeneans living on an individual host is generally low, and infestations of these parasites do not usually cause disease. In crowded fish farms, however, parasite populations often increase uncontrollably and the hosts may be damaged or killed.

Species accounts

List of Species

No common name

Entobdella soleae

order

Monopisthocotylea

family

Capsalidae

taxonomy

Entobdella soleae van Beneden & Hesse, 1864; Johnston, 1929.

other common names

None known.

physical characteristics

Adults 0.07–0.23 in (2 –6 mm) long. Body white or yellowish, flattened with disc-shaped haptor. Embedded in haptor: two pairs of hamuli; one pair of central accessory sclerites that may represent a modified central pair of hooklets; and 14 tiny peripherally located hooklets. Mouth on ventral surface. Conspicuous glandular pharynx. Four eyespots. Adhesive pad on each side of head. Two testes and a large muscular unarmed "penis."

distribution

Not systematically mapped. Parasite of common sole, Solea solea, sand sole, Pegusa lascaris and Senegalese sole, Solea senegalensis on eastern Atlantic seaboard of Europe.

habitat

Adult parasites on lower surface of sole. Fifty percent of common soles off English coast carry 1–6 adult parasites.

behavior

Body muscles generate haptor suction by lifting anterior pair of hamuli relative to accessory sclerites. Edge of haptor sealed by valve. Soles partly bury themselves in sediments with low levels of oxygen; parasites respond to this condition by undulating their bodies. Their flat bodies also spread and become thinner. These responses increase the availability of oxygen to the organism and enhance its uptake. Adults and juveniles orientate themselves with respect to the host's scales, most probably using their sense of touch. May use scales as clues when moving forward along the upper surface of the host. Movement achieved by alternately attaching the haptor and the sticky pads.

feeding ecology and diet

Feed on host's epidermis, which is eroded by the parasite's protrusible pharynx.

reproductive biology

Mutual exchange of spermatophores occurs. Parasite lays tetrahedral eggs, each with long stalk. Two eggs laid per hour at 53°F (12°C). Eggs attach to sand grains— not to fish— by sticky droplets on stalks. After incubation for 4 weeks at 53°F (12°C), eggs hatch soon after dawn in absence of host. Host is

nocturnal and rests during daylight; hence freshly hatched larvae have a stationary target. There is, however, an unknown ingredient in the mucus of the sole's skin that stimulates hatching at any time of day or night. Oncomiracidia usually attach to sole's upper surface and migrate forward, moving from the head to the host's lower surface where they reach sexual maturity. When two fishes make contact, adult and juvenile parasites may move from the lower surface of one fish to upper surface of the other. Parasites arriving on the recipient host find their way forward and move onto its lower surface.

conservation status

Not threatened.

significance to humans

None known as of 2003. Entobdella, however, has the potential to kill soles by superinfection in captive situations. Its close relative Neobenedenia melleni poses an especially serious threat to fish farms and aquaria, because it combines the potential for massive superinfections with a remarkably low specificity. Neobenedenia melleni is capable of infecting over a hundred wild and captive fish species belonging to more than 30 families from 5 different orders.

No common name

Dactylogyrus vastator

order

Monopisthocotylea

family

Dactylogyridae

taxonomy

Dactylogyrus vastator Nybelin, 1924. Dactylogyrus is the largest helminth genus with more than 900 species. They live mostly on the gills of cypriniform fishes.

other common names

None known.

physical characteristics

About .045 in (1.25 mm) long. Two pairs of hamuli, with ventral hamuli reduced to spicules. One or two supporting bars. Fourteen hooklets, each with an enlarged handle. Three pairs of eversible adhesive sacs. Four eyespots. Male copulatory organ has hardened penis tube with accessory sclerite. Single testis.

distribution

Widespread in Palearctic region on common carp (Cyprinus carpio), Crucian carp (Carassius carassius), and goldfish (Carassius auratus).

habitat

Haptor lodges between two secondary gill lamellae.

behavior

Little is known about behavior. Parasite secures itself to host principally by dorsal hamuli.

feeding ecology and diet

Feeds on gill epithelium.

reproductive biology

Ovoid eggs are washed out of host's gill cavity and sink to bottom. Ciliated oncomiracidium emerges in 3–5 days, depending on water temperature. Larvae drawn into gill cavity by current attach themselves to host's gills. Some larvae may first attach to host's skin and then migrate to gills. Eggs are thought to spend the winter in a state of diapause, or period of inactivity.

conservation status

Not threatened.

significance to humans

Causes mass mortality among fingerling carp in fish-rearing ponds. Abnormal multiplication of cells in the gill epithelium interferes with carp's respiratory function. Parasite is especially significant in the former Soviet Union and eastern and northern Europe where carp are bred for food.

No common name

Gyrodactylus pungitii

order

Monopisthocotylea

family

Gyrodactylidae

taxonomy

Gyrodactylus pungitii Malmberg, 1964. About 400 species attributed to Gyrodactylus. Morphologial and anatomical differences between the many species of Gyrodactylus are relatively small, making their taxonomy difficult.

other common names

None known.

physical characteristics

Length 0.023–0.03 in (0.6–0.9 mm). May contain developing embryo. Haptor fan-shaped with one pair of hamuli linked by two bars; sixteen hooklets arranged around periphery. Single pair of eversible adhesive sacs on head. No eyespots. Vitellarium absent or possibly reduced. Germarium reduced. Single testis; penis armed with hooks. Penis absent in young specimens.

distribution

Not systematically mapped, but likely to occur wherever Pungitius pungitius, its specific host, occurs.

habitat

Skin, fins (pharynx) of stickleback, Pungitius pungitius.

behavior

Gyrodactylids rely on hamuli and hooklets for attachment. They move like leeches.

feeding ecology and diet

Feeds on fishes' epidermis.

reproductive biology

Unique among monogeneans. New hosts usually infected by transfer of parasites when hosts make contact with one another. Population growth of many gyrodactylids is limited by host reaction. Mechanism of limitation largely unknown as of 2003.

conservation status

Not threatened.

significance to humans

None known for G. pungitius. There are, however, strains of Norwegian salmon (Salmo salar) unable to control population growth of G. salaris. Young salmon (salmon parr), rarely exceeding 6 in (15 cm) in length, may support more than 10,000 parasites. The parasites' heavy grazing on the fishes' outer layer of skin, both in farms and in the wild, leads to loss of osmotic integrity, invasion by secondary disease agents, and death. Parasite probably introduced to Norway by Baltic salmon that have some resistance to it.

No common name

Tetraonchus monenteron

order

Monopisthocotylea

family

Tetraonchidae

taxonomy

Tetraonchus monenteron Wagener, 1857; Diesing, 1858.

other common names

None known.

physical characteristics

Body elongated, about 0.04 in (1 mm) in length. Haptor with four similar hamuli, arranged in lateral pairs, each pair comprising one dorsally orientated and one ventrally orientated hamulus. Transverse supporting bar between hamulus pairs. Sixteen hooklets present; one pair central on ventral surface, two pairs dorsally orientated. Haptor glands present. Head region with four eyespots and three pairs of adhesive sacs that can be turned inside out. Male copulatory organ is a hardened tube with associated accessory sclerite. Single testis.

distribution

Recorded in Europe, North America and Russia on its specific host, the freshwater pike, Esox lucius. Not systematically mapped.

habitat

Abundant on gills of Esox lucius. Haptor lodges between two secondary gill lamellae.

behavior

The parasite secures itself to the host by counter-rotating its ventral and dorsal hamuli until they push through the secondary gill lamellae. Each laterally situated pair of hamuli is operated by a single muscle. This muscle gives rise to a long tendon, which is threaded through loops attached to the hamuli. The arrangement resembles a pulley system and is likely to confer mechanical advantage. The hamuli are assisted by hooklets and possibly by glands. Sticky eversible sacs on head permit leech-like movement along the gill.

feeding ecology and diet

Feeds on gill epithelium; may take blood when the secondary gill lamella is ruptured.

reproductive biology

Mating not recorded. Ovoid eggs presumably leave the gill chamber and settle to the bottom. Ciliated oncomiracidium hatches after 3–4 days. Immature parasites have been found on host skin.

conservation status

Not threatened.

significance to humans

None known.

No common name

Diclidophora merlangi

order

Polyopisthocotylea

family

Diclidophoridae

taxonomy

Diclidophora merlangi Nordmann, 1832; Kroyer, 1838.

other common names

None known.

physical characteristics

Length may exceed 0.27 in (7 mm). Haptor has four pairs of clamps on stalks (peduncles); no hooks in adult. Mouth terminal (anterior) located at one end; buccal cavity contains two buccal suckers. No sticky pads or eversible sacs. No eyes. Small pharynx. Numerous testes. Penis bulb armed with spines.

distribution

Likely to be present wherever specific host whiting, Merlangius merlangus, is found, but not systematically mapped.

habitat

Gill parasite, strictly host-specific to Merlangius merlangus; 1–12 parasites per fish. Adults prefer first gill arch.

behavior

Parasite attaches itself to secondary gill lamellae using clamps. No evidence that adult is able to change location on gill. Each clamp has two jaws supported by sclerites. Jaws drawn together by suction generated by lifting a diaphragm near hinge line of clamp. Clamp peduncles enable parasite to span as many as five primary gill lamellae. Parasite's body lies between two hemibranchs of a gill. Gill-ventilating current washes both sides of parasite equally; consequently parasite has symmetrical shape.

feeding ecology and diet

Feeds on blood.

reproductive biology

Juveniles probably migrate mainly to first gill, where adults settle near one another. Insemination is unilateral in detached adults. Sperms enter recipient via breaches in tegument made by genital spines.

conservation status

Not threatened.

significance to humans

None known.

No common name

Gastrocotyle trachuri

order

Polyopisthocotylea

family

Gastrocotylidae

taxonomy

Gastrocotyle trachuri van Beneden and Hesse, 1863.

other common names

None known.

physical characteristics

Oncomiracidia and early post-larvae are symmetrical; however, 25–35 clamps develop on one side of body, producing a strongly asymmetrical adult that may exceed 0.15 in (4 mm) in length. Small terminal (posterior) flap bearing hamuli and hooklets. Mouth terminal located at one end; buccal cavity encloses two buccal suckers. No sticky pads or eversible sacs. No eyes. Small pharynx. Testis follicular. Muscular penis bulb with penis tube and ring of spines.

distribution

Likely to be present wherever its specific host the scad Trachurus trachurus occurs, but not systematically mapped.

habitat

Attaches to secondary gill lamellae of Trachurus trachurus by clamps. Single row of clamps attaches to the upstream, outer (efferent) region of secondary lamellae; body then drifts downstream between hemibranchs. Gill ventilating current washes only one side of parasite, promoting asymmetrical development. Asymmetry may be on either the right or left side, depending on which side of primary lamella the parasite attaches itself.

behavior

Clamps close, not by suction, but by relatively simple mechanical arrangement. Tendon from single muscle threads through hole in supporting sclerite of one jaw and attaches to other jaw. When muscle contracts, jaws are drawn together. Adult parasite probably unable to change its site on the gill.

feeding ecology and diet

Feeds on blood.

reproductive biology

Male copulatory organ probably serves for hypodermic (through the skin) impregnation. Infection of scad takes place on sea bottom; in summer at Plymouth, U.K., however, scad become planktonic. Parasites appear to anticipate this change either by ceasing to lay eggs or by laying eggs that enter diapause. Reproductive behavior of parasites may be controlled by hormonal changes in the host. The parasite has access to these hormonal changes via its blood meals.

conservation status

Not threatened.

significance to humans

None known.

No common name

Polystoma integerrimum

order

Polyopisthocotylea

family

Polystomatidae

taxonomy

Polystoma integerrimum Froelich, 1791; Rudolphi, 1808.

other common names

None known.

physical characteristics

Adult about 0.39 in (10 mm) in length. Haptor has six muscular suckers, one pair of hamuli and 16 hooklets, each sucker containing one hooklet. Oral sucker around mouth. Testis follicular.

distribution

Likely to be present wherever its specific host, the brown frog, Rana temporaria, occurs, but not systematically mapped.

habitat

Bladder of Rana temporaria.

behavior

Nothing is known for adult.

feeding ecology and diet

Feeds on blood.

reproductive biology

Adult parasite accumulates reserves, but assembles no eggs while frog is living on land during most of year. When frogs enter water to spawn in spring, the parasite assembles and lays its eggs. Hormonal changes in the host may control parasite reproduction; parasites feed on blood and would have access to hormones circulating in the blood. Ciliated oncomiracidia invade frog tadpole gills. If attached to young tadpole, parasites become precociously sexually mature and lay a few eggs. Oncomiracidia infecting older tadpoles remain immature; when the host undergoes metamorphosis, they migrate via the digestive tract and possibly the skin to the host's bladder where they mature. Single egg retained in uterus of adult develops and hatches; larva remains in host of its parent, increasing the host's parasite burden by autoinfection. In Polystoma nearcticum, which infests North American tree frogs, the parasite's egg assembly switches on and off abruptly as sexual activity of host switches on and off during nocturnal spawning episodes on successive nights.

conservation status

Not threatened.

significance to humans

None known.

No common name

Pseudodiplorchis americanus

order

Polyopisthocotylea

family

Polystomatidae

taxonomy

Pseudodiplorchis americanus Rodgers and Kuntz, 1940; Yamaguti, 1963.

other common names

None known.

physical characteristics

Length of adult about 0.31–0.39 in (8–10 mm). Haptor with six muscular suckers, each with an embedded hooklet. Sixteen hooklets. Fully developed, encapsulated oncomiracidia accumulate in huge uterus. Vitellarium greatly reduced. Pair of compact testes, positioned laterally in the anterior region of the body. Oral sucker present.

distribution

Deserts of Arizona, United States.

habitat

Bladder of spadefoot toad, Scaphiopus couchii.

behavior

No information available for adult.

feeding ecology and diet

Feeds on blood.

reproductive biology

Desert toad spends most of year buried about 3 ft (1 m) below surface of sand. Parasite in toad's bladder accumulates large numbers of eggs in uterus. Toads emerge following torrential annual rains; they spawn in temporary rain pools over a period of two or three nights. As toad enters pool, eggs of parasite are released and hatch immediately. Eggshell is reduced to thin membranous sac. Ciliated oncomiracidia are exceptionally large: 0.0236 in (600 µm) in length, compared to 0.00984 in (250 µm) for the oncomiracidia of Entobdella soleae. Larvae survive for 48 hours at 77–81°F (25–27°C). They attach to the toad, migrating over its skin to the nostrils. Larvae likely to be subjected to dehydration and high temperatures, but survive drying for up to one hour at 90°F (32°C) and 45% relative humidity. Period of development spent in lungs; then juveniles migrate through gut to bladder. Tegumental secretion probably protects migrating juvenile.

conservation status

Not threatened.

significance to humans

None known.

Resources

Books

Boeger, W. A., and D. C. Kritsky. "Phylogenetic Relationships of the Monogenoidea." In Interrelationships of the Platyhelminths, edited by D. T. J. Littlewood and R. A. Bray. London: Taylor & Francis, 2001.

Kearn, G. C. Parasitism and the Platyhelminths. London: Chapman & Hall, 1998.

Periodicals

Bakke, T. A., P. D. Harris, and J. Cable. "Host Specificity Dynamics: Observations on Gyrodactylid Monogeneans." International Journal for Parasitology 32 (2002): 281–308.

Kearn, G. C. "Evolutionary Expansion of the Monogenea." International Journal for Parasitology 24 (1994): 1227–1271.

——. "The Survival of Monogenean (Platyhelminth) Parasites on Fish Skin." Parasitology 119 (1999): S57–S88.

Tinsley, R. C. "Parasite Adaptation to Extreme Conditions in a Desert Environment." Parasitology 119 (1999): S31–S56.

Whittington, I. D., L. A. Chisholm, and K. Rohde. "The Larvae of Monogenea (Platyhelminthes)." Advances in Parasitology 44 (2000): 139–232.

Graham Clive Kearn, DSc