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A parasitoidal wasp ovipositing into the body of a spotted alfalfa aphid

A parasitoid is an organism that spends a significant portion of its life history attached to or within a single host organism in a relationship where the host is ultimately killed. Parasitoidy is one of six major evolutionary strategies within parasitism, distinguished by the fatal prognosis for the host. Because the host is killed the strategy is close to predation.

There are parasitoids in a wide variety of taxa, including microbial diseases, plants, crustaceans, insects, and vertebrates. Among the Hymenoptera, the ichneumons and many wasps are highly specialised for a parasitoidal way of life. Some parasitoidal wasps are used in biological pest control. Parasitoids are found in some other insect groups, including the Diptera.

Parasitoidal alien species that kill their human hosts are widespread in science fiction, as for instance in Ridley Scott's 1979 film Alien.

Contents

HistoryEdit

The term "parasitoid" was coined in 1913 by the Swedo-Finnish writer Odo Morannal Reuter,[1] and adopted in English by his reviewer, William Morton Wheeler.[2] Reuter used it to describe the strategy where the parasite develops in or on the body of a single host individual, eventually killing that host, while the adult is free-living. Since that time, the concept has been generalised and widely applied.[3]

A spectrum of strategiesEdit

 
Parasitoid strategy compared with typical parasite (not killing its host) and predator (killing its prey immediately). There is a continuum between them.

DefinitionEdit

Parasitoidy is one of six major evolutionary strategies within parasitism, the others being parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite, and micropredator. These are adaptive peaks, with many possible intermediate strategies, but organisms in many different groups have consistently converged on these six.[4]

Parasitoids feed on a living host which is eventually killed, typically before it can produce offspring. While some conventional parasites kill their hosts under certain conditions, they usually do not. Many species of true parasites can cause the death of their host if they are present in overwhelming numbers, the host is in poor condition, or the host's health is compromised by secondary infections. For example, blood-sucking mites sometimes overwhelm nestlings of birds such as swallows to the point that the young birds cannot fledge.[5]

In their extreme forms, conventional parasitism and parasitoidy are distinct: there is no doubt that the larva of a Tarantula hawk wasp behaves more like a parasitoid, or even a predator, than a parasite; and similarly the biting midges that suck blood from large insects are plainly ectoparasites; but many intermediate forms exist. At the opposite extreme, parasitoidy grades into predation. Differences between various hunting wasps provide convenient illustrations. Predatory social wasps hunt flies, caterpillars and the like, kill, cut up, and carry them to a nest to feed to their young. Similarly, some solitary wasps such as beewolves, sting prey, sometimes fatally, before saving it, usually entire, in a nest or burrow for the young to feed on. In contrast, the best-known protelean solitary hunting wasps sting prey to paralyse it before storing it for the young in the nest.[6][7] Other wasps paralyse prey in the plant or other environment in which it feeds, before laying eggs nearby; the emerging young feed on the paralysed prey in its own home.[8]

Parasitoid strategiesEdit

 
A hyperparasitoid chalcid wasp (Pteromalidae) on the cocoons of its host, a braconid wasp (Microgastrinae), itself a koinobiont parasitoid of Lepidoptera.

Parasitoids can be classified as either endo- or ectoparasitoids with idiobiont or koinobiont developmental strategies. Endoparasitoids live within their host's body. Ectoparasitoids feed on the host from outside. Idiobiont parasitoids prevent further development of the host after initially immobilizing it. Koinobiont parasitoids allow the host to continue its development while feeding upon it. Most ectoparasitoids are idiobiont, as the host could damage or dislodge the external parasitoid if allowed to move and or molt. Most endoparasitoids are koinobionts, giving them the advantage of a host that continue to grow larger and avoid predators.[9]

Primary parasitoids have the simplest parasitic relationship with two organisms involved: the host and the parasitoid. Hyperparasitoids are parasitoids of parasitoids. Secondary parasitoids are hyperparasitoids which use a primary parasitoid as their host. In this case there are three organisms involved. Hyperparasitoids are either facultative (can be a primary parasitoid or hyperparasitoid depending on the situation) or obligate (always develop as a hyperparasitoid). Levels of parasitoids beyond secondary also occur, especially among facultative parasitoids. In oak gall systems, there can be up to five levels of parasitism.[10] Cases in which two or more species of parasitoids simultaneously attack the same host without parasitizing each other are called multi- or multiple parasitism. In many cases, multiple parasitism still leads to the death of one or more of the parasitoids involved. If multiple parasitoids of the same species coexist in a single host, it is called superparasitism. Gregarious species purposefully lay multiple eggs or polyembryonic eggs which lead to multiple larvae in a single host. The end result of gregarious superparasitism can be a single surviving parasitoid individual or multiple surviving individuals, depending on the species. If superparasitism occurs accidentally in normally solitary species the larvae often fight among themselves until only one is left.[11]

Influence on host behaviourEdit

 
Female Apocephalus borealis ovipositing into the abdomen of a worker honey bee, altering its behavior

In another strategy, some parasitoids influence the host's behaviour in ways that favour the propagation of the parasitoid, often at the cost of the host's life. A spectacular example is the lancet liver fluke that causes host ants to die clinging to grass stalks, where grazers or birds may be expected to eat them and complete the parasitoidal fluke's life cycle in its definitive host. Similarly, as strepsipteran parasitoids of ants mature, they cause the hosts to climb high on grass stalks, positions that are risky, but favour the emergence of the strepsipterans.[12] Among pathogens of mammals, the rabies virus affects the host's central nervous system, eventually killing it, but perhaps helping to disseminate the virus by modifying the host's behaviour.[13] Among the parasitic wasps, Glyptapanteles modifies the behavior of its host caterpillar to defend the pupae of the wasps after they emerge from the caterpillar's body.[14] The phorid fly Apocephalus borealis oviposits into the abdomen of its hosts, including honey bees, causing them to abandon their nest, flying from it at night and soon dying, allowing the next generation of flies to emerge outside the hive.[15]

In different taxaEdit

Microbial diseasesEdit

 
Fly fungus Entomophthora muscae, having killed its host, the dung fly Scathophaga stercoraria

Some microbial parasitoids waste most of the host's resources when it dies, but others exploit the host efficiently. Microbial pathogens of insects include microsporidiosis in the form of nosema in silkworms. This infection is highly virulent[16] and the tissues of the victims contain huge numbers of infectious spores. In effect the pathogen in its role of parasitoid has used up most of the resources of the host to propagate and spread its offspring. Similarly, many viruses propagate inside a host cell until it physically ruptures. Parasitoidal fungi such as Entomophthora species carry this principle as far as is possible. Having infected and killed an insect, they continue to grow on the carcass and release spores for as long as any resources remain. A nonlethal parasitic organism, especially if it is a fungus, is sometimes termed a biotroph, while a parasitoidal fungus may be called a necrotroph.[17][18]

PlantsEdit

 
The strangler fig Ficus watkinsiana slowly killing a rainforest tree, Syzygium hemilampra

Parasitoidal plants include various species of dodder, which indiscriminately parasitise wide ranges of host plants, and debilitate or kill the branches that they infect, and commonly the whole host plant as well.[4][19]

Mistletoes in families such as Santalaceae and Loranthaceae commonly accumulate on host trees until they stunt and eventually kill them, sometimes after many decades. Occasionally a freak condition can arise where the (strictly speaking "hemiparasitic") plant can supply sufficient photosynthetic power to support the root system of a small host tree for several years after the live host shoots have effectively disappeared.[20]

The parasitoid plant may strictly not be a parasite in the normal sense, but nonetheless exploits the host's resources of space, support and light. The best-known are the so-called strangler figs such as Ficus watkinsiana. Some of them grow on and around the trunk of the host tree and squeeze or starve it of light until, after perhaps decades, it dies. The strangler eventually replaces the host utterly as the original trunk rots within the stems of the strangler, leaving a hollow framework.[4][21]

CrustaceansEdit

The many parasitoidal Crustacea have a wide range of species and strategies. The killing of the host is often incidental. In the gill lice, most adult females live as parasites in the gills of fish, causing incidental harm that may kill the fish or weaken them so badly as to prevent breeding. Sacculina barnacles inject themselves into a crab, and convert themselves into egg-laying bags. This disrupts the crab's reproductive system in parasitic castration.[22]

NematodesEdit

While many nematodes are free-living, two species of parasitoid mermithid nematodes can be found in common aestivation sites of bogong moths: Amphimermis bogongae and Hexamermis cavicola.[23] The parasites are transmitted through water; the early instar larval nematodes reside in the debris of the cave floors of common aestivation sites, and crawl up to reach the moths through trickles of water coming down the walls. Bogong moths are infected upon their arrival within the caves once they drink the water. After a few months, the larval nematodes emerge from the moths, killing them.[24]

InsectsEdit

About 10% of described insects are parasitoids, in six orders: Hymenoptera, Diptera, Coleoptera, Neuroptera, Lepidoptera, and Trichoptera. The majority are within the Hymenoptera; most of the others are Dipteran flies.[3][25][26]

Parasitoid waspsEdit

 
Braconid wasp cocoons on giant leopard moth larva

The many species of parasitoid wasps in the Hymenopteran suborder Apocrita are mostly chalcidoid and ichneumon wasps, followed by the Proctotrupoidea and Platygastroidea. Outside these, many Hymenopteran lineages contain some parasitoids, such as most of the Chrysidoidea and Vespoidea, and the rare Symphytan (sawfly) family Orussidae.[27]

Hymenopteran parasitoids often have remarkable life cycles. In one family, the Trigonalidae, the female wasps deposit eggs into small pockets they cut into the edge of leaves with their ovipositor. A caterpillar chewing these leaves may unknowingly swallow some of the eggs, and when they get into the caterpillar's gut, they hatch and burrow through the gut wall and into the body cavity. Later they search the caterpillar's body cavity for other parasitoid larvae, and it is these they attack and feed on. Some trigonalids, once in a caterpillar or sawfly larva, need their vehicle to fall prey to a social wasp. The wasp carries the caterpillar back to its nest, and there it is butchered and fed to the wasp's young; they will serve as the host for the trigonalid, the eggs of which are in the butchered caterpillar.[28] The ichneumon wasp Ichneumon eumerus parasitises the butterfly Phengaris rebeli by directly seeking out, through smell, Myrmica ant nests that the butterfly larvae previously parasitised, and ovipositing into the P. rebeli larvae. Once the wasps' eggs hatch, they feast on the carcass of the dead caterpillar.[29]

 
Megarhyssa macrurus, a parasitoid, ovipositing into its host through the wood of a tree. The body of a female is c. 2 inches (51 mm) long, with an ovipositor c. 4 inches (100 mm) long.

Parasitoid wasps can be classified as either endoparasitic or ectoparasitic according to where they lay their eggs.[30] Endoparasitic wasps insert their eggs inside their host, while ectoparasitic wasps deposit theirs outside the host's body.[3] Most species of wasps attack during the egg or larval stage of their host, but some attack adult hosts. Oviposition is complex, as it depends on finding the host and on evading host defense mechanisms. The ovipositor is a long tube-like organ used to inject eggs into hosts. It consists of the genital structures from segments eight and nine of the wasp's body.[31]

Parasitoid wasps face a range of obstacles to oviposition,[3] including behavioral, morphological, physiological or immunological defenses of their hosts.[32] An example of immunological defense against endoparasitic wasps would be the encapsulation of their eggs.[33] To thwart this immunological protection system, some wasps inundate their host with their eggs so as to overload the encapsulation response.[34] Another way of hindering a host's defense is to introduce a virus which interferes with the immune system.[35]

Some parasitoid wasps locate hosts by detecting chemicals released as indirect plant defenses against insect herbivores.[36]

Parasitoid wasps have specialized behavior for ovipositing on their hosts. For example, those that attack ants either use a horizontal or vertical alighting approach from behind the host. In the horizontal method, the wasp maintains its body horizontally until it grabs on to the ant's metasoma (upper abdomen) with its tarsi (lower legs). After that, it places the rest of its legs on the ant's abdomen, folds its wings, and proceeds to inject its victim with the ovipositor. The vertical approach is more complicated, and requires more steps. The wasp attaches its front legs onto the ant's abdomen, then rotates 180 degrees so that it becomes upside down. After that, it rotates once more so that its head and legs switch places, before inserting its ovipositor.[37]

Ants are often aware of the wasps' presence, as they violently turn around, moving their mandibles and legs in order to defend against their attacker. This sometimes prevents the wasps from depositing their eggs successfully. To try to beat such behavioral diversions, the wasps close in very fast to inject their hosts. To prevent missing the target when making contact with the host, the wasp may wait for the ant to stop moving, and then attack suddenly.[38]

Other insectsEdit

 
The head of a strepsipteran, Odynerus spinipes, protruding from the abdomen of its wasp host

The true flies (Diptera) include several families of parasitoids, the largest of which is the Tachinidae, along with others such as the Pipunculidae and Conopidae. Other families of flies include some protelean species. For example, the Phoridae are parasitoidal on ants, and some flesh flies, such as Emblemasoma auditrix, are parasitoidal on cicadas, locating their hosts by sound.[39]

The "twisted-wing parasites" (Strepsiptera) consists entirely of parasitoids; they usually sterilise their hosts.[40]

Two beetle families, Ripiphoridae and Rhipiceridae, are largely parasitoids, as are Aleochara rove beetles. Other orders include a few parasitoids, such as epipyropid moths, which are ectoparasitoids of planthoppers and cicadas. More elaborately, the genus Cyclotorna begins its growth period parasitising plant bugs, and ends by feeding on ant larvae in their colonies.

VertebratesEdit

 
Sea lampreys, Petromyzon marinus, on a lake trout, (Salvelinus namaycush)

Lampreys can be either parasitic or parasitoidal.[41] The sea lamprey is hematophagous, inflicting deep rasping wounds, and the muscle damage and loss of blood commonly weaken the host severely, affecting its reproduction or killing it.[42]

The sabre-toothed blenny parasitises the cleaning symbiosis relationship between some cleaner fish and their client fishes. It attacks the client fish, approaching it in the guise of cleaner wrasse, and snatches a mouthful of scales or other convenient tissue. Clients often react violently, and thereafter trust neither wrasse nor the wrasse-mimicking blenny.[43][44][45]

 
Cape robin-chat (Cossypha caffra) feeding a juvenile red-chested cuckoo (Cuculus solitarius), its brood parasite

Another form of parasitism that can approach parasitoidy occurs in the Perissodini, cichlids from Lake Tanganyika. Seven species in the genus Perissodus are specialised in eating scales from other fish. Their teeth are variously suited to being able to grab bits of skin with the scales attached. At least some of the species also have behavioral adaptations to enable them to approach potential hosts.[46] They have an adaptation of the jaw that enables them to lash out sideways when passing a victim; the jaw is asymmetrical,[47] and there is continuous selection for the asymmetry that currently is less frequent in the population, because host fishes are more alert to defend themselves on the side on which they have been attacked in the past.[48]

Such a lifestyle is reminiscent of sharks of the genus Isistius, also known as the cookiecutter shark because of the circular wounds it leaves on the skin of whales and large fish that it has bitten in passing.[49] Isistius species have been referred to as partly ectoparasitic,[50] but they sometimes overwhelm their hosts and kill them.

Brood parasitism is found among birds such as cuckoos and cowbirds. They are parasitoids, as they often cause the starvation of the host's chicks by competing with them for food, while others either remove (and eat) host eggs when laying eggs in host nests, or the chick ejects or kills the eggs or chicks of the host when they hatch. Some hatchlings have hooked beaks adapted to attacking the host chicks and eggs; these hooks vanish before fledging. The hosts often have counter-adaptations such as the ability to recognise and eject the parasite's eggs.[51]

 
Encarsia formosa, an endoparasitic chalcid wasp, bred commercially to control whitefly in greenhouses

Biological controlEdit

Parasitoids are among the most widely used biological control agents. From the point of view of the farmer or horticulturalist, the most important groups are the Ichneumonid wasps, which prey mainly on caterpillars of butterflies and moths; Braconid wasps, which attack caterpillars and a wide range of other insects including greenfly; Chalcid wasps, which parasitise eggs and larvae of greenfly, whitefly, cabbage caterpillars, and scale insects; and Tachinid flies, which parasitize a wide range of insects including caterpillars, adult and larval beetles, and true bugs.[52] Commercially, there are two types of rearing systems: short-term daily output with high production of parasitoids per day, and long-term low daily output with a range in production of 4–1000 million female parasitoids per week.[53] Larger production facilities produce on a yearlong basis, whereas some facilities produce only seasonally. Rearing facilities are usually a significant distance from where the agents are to be used in the field, and transporting the parasitoids from the point of production to the point of use can pose problems.[54] Shipping conditions can be too hot, and even vibrations from planes or trucks can adversely affect parasitoids.[53]

 
Parasitic "facehugger" alien species in James Cameron's 1986 science fiction film Aliens

In science fictionEdit

Disgusting and terrifying parasitic alien species that kill their human hosts are widespread in science fiction, as for instance in Ridley Scott's 1979 film Alien.[55] In one scene of that film, an alien bursts out of the chest of a dead man, with blood squirting out under high pressure assisted by explosive squibs. Animal viscera were used to reinforce the shock effect. The scene was filmed in a single take, and the startled reaction of the actors was genuine.[56]

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