Jump to content

Parasitoid

This is a good article. Click here for more information.
From Wikipedia, the free encyclopedia
(Redirected fromEndoparasitoid)

Aparasitoid wasp(Trioxys complanatus,Aphidiinae)ovipositinginto the body of a spotted alfalfaaphid(Therioaphis maculata,Calaphidinae), a behaviour that is used inbiological pest control[a][2]

Inevolutionary ecology,aparasitoidis anorganismthat lives in close association with itshostat the host's expense, eventually resulting in the death of the host. Parasitoidism is one of six majorevolutionary strategieswithinparasitism,distinguished by the fatalprognosisfor the host, which makes the strategy close topredation.

Among parasitoids, strategies range from living inside the host (endoparasitism), allowing it to continue growing before emerging as an adult, toparalysingthe host and living outside it (ectoparasitism). Hosts can include other parasitoids, resulting inhyperparasitism;in the case ofoak galls,up to five levels of parasitism are possible. Some parasitoidsinfluence their host's behaviourin ways that favour the propagation of the parasitoid.

Parasitoids are found in a variety oftaxaacross theinsectsuperorderEndopterygota,whose completemetamorphosismay havepre-adaptedthem for a split lifestyle, with parasitoidlarvaeand free-living adults. Most are in theHymenoptera,where theichneumonsand many otherparasitoid waspsare highly specialised for a parasitoidal way of life. There are parasitoids, too, in theDiptera,Coleopteraand otherordersofendopterygote insects.Some of these, usually but not only wasps, are used inbiological pest control.

The 17th-century zoological artistMaria Sibylla Merianclosely observed parasitoids and their hosts in her paintings. The biology of parasitoidism influencedCharles Darwin's beliefs and has inspiredscience fictionauthors andscriptwritersto create numerous parasitoidal aliens that kill their human hosts, such as thealien speciesinRidley Scott's 1979 filmAlien.

Etymology

[edit]

The term "parasitoid" was coined in 1913 by theSwedo-FinnishwriterOdo Reuter,[3]and adopted in English by his reviewer,[4]the entomologistWilliam Morton Wheeler.[5]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.[6]

Strategies

[edit]

Evolutionary options

[edit]

A perspective on the evolutionary options can be gained by considering four questions: the effect on thereproductive fitnessof a parasite's hosts; the number of hosts they have per life stage; whether the host is prevented from reproducing; and whether the effect depends on intensity (number of parasites per host). From this analysis, proposed by K. D. Lafferty and A. M. Kunis, the major evolutionary strategies of parasitism emerge, alongside predation.[7]

Evolutionary strategies in parasitism and predation[7]
(intensity-dependent: green, roman;
intensity-independent: purple, italics)
Host fitness Single host, stays alive Single host, dies Multiple hosts
Able to
reproduce
(fitness > 0)		 Conventional parasite
Pathogen		 Trophically transmitted parasite[b]
Trophically transmitted pathogen		 Micropredator
Micropredator
Unable to
reproduce
(fitness = 0)		 —
Parasitic castrator		 Trophically transmitted parasitic castrator
Parasitoid		 Social predator[c]
Solitary predator

Parasitoidism, in the view ofR. Poulinand H. S. Randhawa, is one of six mainevolutionary strategieswithinparasitism,the others beingparasitic castrator,directly transmitted parasite,trophicallytransmitted parasite,vector-transmitted parasite, and micropredator. These areadaptive peaks,with many possible intermediate strategies, but organisms in many different groups have consistentlyconvergedon these six.[8][9]

Parasitoids feed on a living host which they eventually kill, typically before it can produce offspring, whereas conventional parasites usually do not kill their hosts, and predators typically kill their prey immediately.[10][11]

Basic concepts

[edit]
Ahyperparasitoidchalcidoid waspon the cocoons of its host, abraconid wasp,itself a koinobiont parasitoid ofLepidoptera

Parasitoids can be classified as either endo- or ectoparasitoids with idiobiont or koinobiont developmental strategies. Endoparasitoids live within their host's body, while ectoparasitoids feed on the host from outside. Idiobiont parasitoids prevent further development of the host after initially immobilising it, whereas 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 andmoult.Most endoparasitoids are koinobionts, giving them the advantage of a host that continues to grow larger and avoid predators.[12]

Primary parasitoids have the simplest parasitic relationship, involving two organisms, the host and the parasitoid.Hyperparasitoidsare parasitoids of parasitoids; secondary parasitoids have a primary parasitoid as their host, so there are three organisms involved. Hyperparasitoids are either facultative (can be a primary parasitoid or a hyperparasitoid depending on the situation) or obligate (always develop as a hyperparasitoid). Levels of parasitoids beyond secondary also occur, especially among facultative parasitoids. Inoak gallsystems, there can be up to five levels of parasitism.[13]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 calledsuperparasitism.Gregarious species 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.[14][15]

Influencing host behaviour

[edit]
Femalephorid flyApocephalus borealis(centre left)ovipositinginto the abdomen of a workerhoney bee,altering its behaviour
Further information:Behavior-altering parasite

In another strategy, some parasitoidsinfluence the host's behaviourin ways that favour the propagation of the parasitoid, often at the cost of the host's life. A spectacular example is thelancet liver fluke,which 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 itsdefinitive host.Similarly, asstrepsipteranparasitoids of ants mature, they cause the hosts to climb high on grass stalks, positions that are risky, but favour the emergence of the strepsipterans.[16]Among pathogens of mammals, therabies virusaffects the host'scentral nervous system,eventually killing it, but perhaps helping to disseminate the virus by modifying the host's behaviour.[17]Among the parasitic wasps,Glyptapantelesmodifies the behaviour of its host caterpillar to defend the pupae of the wasps after they emerge from the caterpillar's body.[18]Thephorid flyApocephalus borealisoviposits into the abdomen of its hosts, includinghoney 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.[19]

Taxonomic range

[edit]

About 10% of described insects are parasitoids, in the ordersHymenoptera,Diptera,Coleoptera,Neuroptera,Lepidoptera,Strepsiptera,andTrichoptera.The majority are wasps within the Hymenoptera; most of the others are Dipteran flies.[6][20][21]Parasitoidism hasevolved independentlymany times: once each in Hymenoptera, Strepsiptera, Neuroptera, and Trichoptera, twice in the Lepidoptera, 10 times or more in Coleoptera, and no less than 21 times among the Diptera. These are allholometabolousinsects (Endopterygota,which form a singleclade), and it is always the larvae that are parasitoidal.[22]The metamorphosis from active larva to an adult with a different body structurepermitsthe dual lifestyle of parasitic larva, freeliving adult in this group.[23]These relationships are shown on thephylogenetic tree;[24][25]groups containing parasitoids are shown in boldface, e.g.Coleoptera,with the number of times parasitoidism evolved in the group in parentheses, e.g.(10 clades).The approximate number (estimates can vary widely) of parasitoid species[26]out of the total is shown in square brackets, e.g. [2,500 of 400,000].

Endopterygota
Neuropterida

Raphidioptera

Megaloptera

Neuroptera(net-winged insects)(1 clade)[c. 15 of 6,000]

Coleopterida

Coleoptera(beetles)(10 clades)[c. 2,500 of 400,000]Ripiphorid beetle triungulin larva on the wing of a braconid wasp

(1 clade)

Strepsiptera(twisted-wing parasites) [600 of 600]

Hymenoptera

Symphyta

(1 clade)

Orussoidea(parasitic wood wasps) [75 of 75]Parasitic wood wasp

Apocrita(wasp-waisted insects) [c. 50,000 of 100,000]The parasitoid wasp Megarhyssa macrurus ovipositing into host through wood. Her body is c. 50 mm long, her ovipositor c. 100 mm.

Panorpida

Diptera(true flies)(21 clades)[c. 17,000 of 125,000]Stylogaster, a conopid fly, showing the long ovipositor

Trichoptera(caddis flies)(1 clade)[c. 10 of 14,500]

Lepidoptera(butterflies, moths)(2 clades)[c. 40 of 180,000]Moth Epiricania hagoromo (Epipyropidae) feeding on planthopper Euricania facialis

Hymenoptera

[edit]
Main article:Parasitoid wasp
Potter wasp,an idiobiont, building a mud nest; she willprovision itwith paralysed insects, on which she will lay her eggs; she will then seal the nest and provide no further care for her young

Within the Hymenoptera, parasitoidism evolved just once, and the many described[d]species ofparasitoid wasps[27]represent the great majority of species in the order, barring those like theants,bees,andVespidaewasps that have secondarily lost the parasitoid habit. The parasitoid wasps include some 25,000Ichneumonoidea,22,000Chalcidoidea,5,500Vespoidea,4,000Platygastroidea,3,000Chrysidoidea,2,300Cynipoidea,and many smaller families.[26]These often have remarkable life cycles.[28] They can be classified as either endoparasitic or ectoparasitic according to where they lay their eggs.[29]Endoparasitic wasps insert their eggs inside their host, usually as koinobionts, allowing the host to continue to grow (thus providing more food to the wasp larvae), moult, and evade predators. Ectoparasitic wasps deposit theirs outside the host's body, usually as idiobionts, immediately paralysing the host to prevent it from escaping or throwing off the parasite. They often carry the host to a nest where it will remain undisturbed for the wasp larva to feed on.[6]Most species of wasps attack the eggs or larvae of their host, but some attack adults.Ovipositiondepends on finding the host and on evading host defences; the ovipositor is a tube-like organ used to inject eggs into hosts, sometimes much longer than the wasp's body.[30][31][32]Hosts such as ants often behave as if aware of the wasps' presence, making violent movements to prevent oviposition. Wasps may wait for the host to stop moving, and then attack suddenly.[33]

Parasitoid wasps face a range of obstacles to oviposition,[6]including behavioural, morphological, physiological and immunological defences of their hosts.[29][34]To thwart this, some wasps inundate their host with their eggs so as to overload its immune system's ability to encapsulate foreign bodies;[35]others introduce aviruswhich interferes with the host's immune system.[36] Some parasitoid wasps locate hosts by detecting the chemicals that plants release to defend against insect herbivores.[37]

Other orders

[edit]
The head of a sessile femalestrepsipteranprotruding (lower right) from the abdomen of its wasp host; the male (not shown) has wings

The true flies (Diptera) include several families of parasitoids, the largest of which is theTachinidae(some 9,200 species[26]), followed by theBombyliidae(some 4,500 species[26]), along with thePipunculidaeand theConopidae,which includes parasitoidal genera such asStylogaster.Other families of flies include someproteleanspecies.[38]SomePhoridaeare parasitoids of ants.[39][40]Someflesh fliesare parasitoids: for instanceEmblemasoma auditrixis parasitoidal on cicadas, locating its host by sound.[41]

TheStrepsiptera(twisted-wing parasites) consist entirely of parasitoids; they usually sterilise their hosts.[42]

Twobeetlefamilies,Ripiphoridae(450 species[26])[43][44]andRhipiceridae,are largely parasitoids, as areAleocharaStaphylinidae;in all, some 400 staphylinids are parasitoidal.[26][38][45]Some 1,600 species of the large and mainly freeliving familyCarabidaeare parasitoids.[26]

A few Neuroptera are parasitoidal; they have larvae that actively search for hosts.[46]The larvae of someMantispidae,subfamily Symphrasinae, are parasitoids of other arthropods including bees and wasps.[26]

Although nearly all Lepidoptera (butterflies and moths) are herbivorous, a few species are parasitic. The larvae ofEpipyropidaefeed onHomopterasuch as leafhoppers and cicadas, and sometimes on other Lepidoptera. The larvae ofCyclotornidaeparasitise first Homoptera and laterantbrood.[47]Thepyralid mothChalcoelahas been used in biological control of the waspPolistesin theGalapagos Islands.[22]

Parasitism is rare in the Trichoptera (caddisflies), but it is found among theHydroptilidae(purse-case caddisflies), probably including all 10 species in theOrthotrichia aberransgroup; they parasitise the pupae of other trichopterans.[48]

Mites of the familyAcarophenacidaeare ectoparasitoids of insect eggs. Unlike the insect parasitoids, it is the adult stage in Acarophenacidae that acts as a parasitoid. Specifically, adult female mites feed on insect eggs and their body swells up with offspring, which eventually emerge as adults.[49]

Entomopathogenic fungi

[edit]

All known fungi in the generaCordycepsandOphiocordycepsare endoparasitic.[50]One of the most notable fungal parasitoids isO. unilateraliswhich infects carpenter ants by breaching the ant's exoskeletons via their spores and growing in the ant's hemocoel as free living yeast cells. Eventually the yeast cells progress to producing nerve toxins to alter the behaviour of the ant causing it to climb and bite onto vegetation, known as the 'death bite'.[51]This approach is so fine-tuned it causes the ant to bite down on the part of the leaf most optimal for the fungus to fruit; the adaxial leaf midrib. In fact, it has been found that in specific circumstances, the time of the death bite is synchronised to solar noon.[52]As much as 40% of the ant's biomass is fungal hyphae at the moment of the death bite.[53]After the ant dies, the fungus produces a large stalk, growing from the back of the ant's head[54]which subsequently releases ascospores. These spores are too large to be wind dispersed and instead fall directly to the ground where they produce secondary spores that infect ants as they walk over them.[55]O. sinesis,is a parasitoid as well, parasitising ghost moth larvae, killing them within 15-25 days, a similar process to that ofO. unilateralis.[56]

Learning in parasitoids

[edit]

Host location has been studied inOrmia ochracea,a parasitoid tachinid fly that locates their field cricket host acoustically (phonotaxis).[57]Preference for the dominant local host species was not explained by DNA analysis. In fact, populations across the southern U.S. were inexplicably closely related, considering rate of range expansion from a presumed Central American origin.[58]A captive population of lab-reared flies were raised on two different host songs (Gryllus integerorG. lineaticeps). Responsive adult females overwhelmingly chose their familiar song, indicating the use of a learned, auditory search image. Thisphenotypic plasticityallows such a highly specialized parasitoid to avoid overspecialization disasters. Interestingly, when receptive females only heard silence the night before testing for preference, they chose the host songs equally, 50/50.[59]This capacity for learning and use of search images paired with a highly specialized morphology and lifestyle (eg. tympana tuned to host sound cues, larviparous) supports the extraordinarily fast range expansion ofO. ochracea,as well as the presence and power of learning in parasitoids.

Interactions with humans

[edit]

In biological pest control

[edit]
Main article:Biological pest control
Encarsia formosa,an endoparasiticaphelinidwasp, bred commercially to control whitefly ingreenhouses

Parasitoids are among the most widely used biological control agents. Classicbiological pest controlusing natural enemies of pests (parasitoids or predators) is extremely cost effective, the cost/benefit ratio for classic control being 1:250, but the technique is more variable in its effects than pesticides; it reduces rather than eliminates pests. The cost/benefit ratio for screening natural enemies is similarly far higher than for screening chemicals: 1:30 against 1:5 respectively, since the search for suitable natural enemies can be guided accurately with ecological knowledge. Natural enemies are more difficult to produce and to distribute than chemicals, as they have a shelf life of weeks at most; and they face a commercial obstacle, namely that they cannot be patented.[60][61]

From the point of view of the farmer or horticulturalist, the most important groups are theichneumonid wasps,which prey mainly oncaterpillarsofbutterfliesandmoths;braconid wasps,which attack caterpillars and a wide range of other insects includinggreenfly;chalcidoid wasps,which parasitise eggs and larvae of greenfly,whitefly,cabbage caterpillars,andscale insects;andtachinid flies,which parasitise a wide range of insects including caterpillars, adult and larvalbeetles,andtrue bugs.[62]Commercially, there are two types of rearing systems: short-term seasonal daily output with high production of parasitoids per day, and long-term year-round low daily output with a range in production of 4–1000 million female parasitoids per week, to meet demand for suitable biological control agents for different crops.[63][64]

Maria Sibylla Merian

[edit]
Parasitic wasps(centre right) with theirgarden tiger mothhost, byMaria Sibylla Merian

Maria Sibylla Merian(1647–1717) was one of the first naturalists to study and depict parasitoids and their insect hosts in her closely-observed paintings.[65]

Charles Darwin

[edit]

Parasitoids influenced the religious thinking ofCharles Darwin,[e]who wrote in an 1860 letter to the American naturalistAsa Gray:"I cannot persuade myself that a beneficent and omnipotent God would have designedly created parasitic wasps with the express intention of their feeding within the living bodies of Caterpillars."[67]The palaeontologistDonald Protheronotes that religiously minded people of theVictorian era,including Darwin, were horrified by this instance of evident cruelty in nature, particularly noticeable in theichneumonidwasps.[68]

In science fiction

[edit]
Further information:Parasites in fictionandAlien (creature in Alien franchise)
A 1990sgargoyleatPaisley Abbey,Scotland, resembling aXenomorph[69]parasitoid from the filmAlien[70]

Parasitoids have inspiredscience fictionauthors and screenwriters to create terrifyingparasitic alien speciesthat kill their human hosts.[71]One of the best-known is theXenomorphinRidley Scott's 1979 filmAlien,which runs rapidly through its lifecycle from violently entering a human host's mouth to bursting fatally from the host's chest.[72][73][74]The molecular biologist Alex Sercel, writing inSignal to Noise Magazine,compares "the biology of the [Alien] Xenomorphs to parasitoid wasps andnematomorph wormsfrom Earth to illustrate how close to reality the biology of these aliens is and to discuss this exceptional instance of science inspiring artists ".[75]Sercel notes that the way the Xenomorph grasps a human's face to implant its embryo is comparable to the way a parasitoid wasp lays its eggs in a living host. He further compares the Xenomorph life cycle to that of the nematomorphParagordius tricuspidatuswhich grows to fill its host's body cavity before bursting out and killing it.[75]Alistair Dove, on the science websiteDeep Sea News,writes that there are multiple parallels with parasitoids, though there are in his view more disturbing life cycles in real biology. In his view, the parallels include the placing of an embryo in the host; its growth in the host; the resulting death of the host; andalternating generations,as in theDigenea(trematodes).[76]The social anthropologistMarika Moisseeffargues that "The parasitical and swarming aspects of insect reproduction make these animals favouredvillainsinHollywoodscience fiction. The battle of culture against nature is depicted as an unending combat between humanity and insect-like extraterrestrial species that tend to parasitise human beings in order to reproduce. "[71]The Encyclopedia of Science Fictionlists many instances of "parasitism", often causing the host's death.[77]

Notes

[edit]
  1. ^The species has been introduced to Australia to control the spotted alfalfa aphid.[1]
  2. ^Trophically transmitted parasites are transmitted to their definitive host, a predator, when their intermediate host is eaten. These parasites often modify the behaviour of their intermediate hosts, causing them to behave in a way that makes them likely to be eaten, such as by climbing to a conspicuous point: this gets the parasites transmitted at the cost of the intermediate host's life.
  3. ^Thewolfis a social predator, hunting in packs; thecheetahis a solitary predator, hunting alone. Neither strategy is conventionally considered parasitic.
  4. ^There may be far more species of parasitoid wasp not yet described.
  5. ^Darwin mentions "parasitic" wasps inOn the Origin of Species,Chapter 7, page 218.[66]

References

[edit]
  1. ^Wilson, C. G.; Swincer, D. E.; Walden, K. J. (1982). "The Introduction of Trioxys Complanatus Quilis (Hymenoptera: Aphidiidae), an Internal Parasite of the Spotted Alfalfa Aphid, into South Australia".Australian Journal of Entomology.21(1): 13–27.doi:10.1111/j.1440-6055.1982.tb01758.x.S2CID84996305.
  2. ^"Spotted Alfalfa Aphid / Alfalfa / Agriculture: Pest Management Guidelines / UC Statewide IPM Program (UC IPM)".ipm.ucanr.edu.Retrieved22 September2023.
  3. ^Reuter, Odo M.(1913).Lebensgewohnheiten und Instinkte der Insekten[Habits and instincts of the insects up to the awakening of social instincts] (in German). R. Friedländer und Sohn.
  4. ^Wheeler, William Morton (9 January 1914). "Scientific Books | Lebensgewohnheiten und Instinkte der Insekten bis zum Erwachen der sozialen Instinkte".Science.39(993). American Association for the Advancement of Science (AAAS): 69–71.doi:10.1126/science.39.993.69.
  5. ^Wheeler, William Morton(1923).Social life among the insects: being a series of lectures delivered at the Lowell Institute in Boston in March 1922.Harcourt, Brace.Previously published inScientific Monthly,June 1922 to February 1923.
  6. ^abcdGodfray, H. C. J. (1994).Parasitoids: Behavioral and Evolutionary Ecology.Princeton University Press.ISBN978-0-691-00047-3.
  7. ^abLafferty, K. D.; Kuris, A. M. (2002). "Trophic strategies, animal diversity and body size".Trends Ecol. Evol.17(11): 507–513.doi:10.1016/s0169-5347(02)02615-0.
  8. ^Poulin, Robert;Randhawa, Haseeb S. (February 2015)."Evolution of parasitism along convergent lines: from ecology to genomics".Parasitology.142(Supplement 1): S6–S15.doi:10.1017/S0031182013001674.PMC4413784.PMID24229807.
  9. ^Poulin, Robert(2011). Rollinson, D.; Hay, S. I. (eds.).The Many Roads to Parasitism: A Tale of Convergence.Vol. 74. Academic Press. pp. 27–28.doi:10.1016/B978-0-12-385897-9.00001-X.ISBN978-0-12-385897-9.PMID21295676.{{cite book}}:|journal=ignored (help)
  10. ^Stevens, Alison N. P. (2010)."Predation, Herbivory, and Parasitism".Nature Education Knowledge.3(10): 36.Retrieved12 February2018.Predation, herbivory, and parasitism exist along a continuum of severity in terms of the extent to which they negatively affect an organism's fitness.... In most situations, parasites do not kill their hosts. An exception, however, occurs with parasitoids, which blur the line between parasitism and predation.
  11. ^Møller, A. P. (1990). "Effects of parasitism by a haematophagous mite on reproduction in the barn swallow".Ecology.71(6): 2345–2357.Bibcode:1990Ecol...71.2345M.doi:10.2307/1938645.JSTOR1938645.
  12. ^Gullan, P. J.; Cranston, P. S. (2014).The Insects: An Outline of Entomology(5th ed.). Wiley. pp. 362–370.ISBN978-1-118-84615-5.
  13. ^Askew, R. R. (1961)."On the biology of the inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain".Transactions of the Society for British Entomology.14:237–268.
  14. ^Gullan, P. J.; Cranston, P. S. (2014).The Insects: An Outline of Entomology(5th ed.). Wiley. pp. 365–369.ISBN978-1-118-84615-5.
  15. ^Fisher, R. C. (1 June 1961)."A Study in Insect Multiparasitism: I. Host Selection and Oviposition"(PDF).Journal of Experimental Biology.38(2): 267–275.doi:10.1242/jeb.38.2.267.
  16. ^Wojcik, Daniel P. (March 1989). "Behavioral Interactions between Ants and Their Parasites".The Florida Entomologist.72(1): 43–51.doi:10.2307/3494966.JSTOR3494966.
  17. ^Taylor, P. J. (December 1993). "A systematic and population genetic approach to the rabies problem in the yellow mongoose (Cynictis penicillata)".Onderstepoort J. Vet. Res.60(4): 379–87.PMID7777324.
  18. ^Grosman, Amir H.; Janssen, Arne; Brito, Elaine F. de; Cordeiro, Eduardo G.; Colares, Felipe; Fonseca, Juliana Oliveira; Lima, Eraldo R.; Pallini, Angelo; Sabelis, Maurice W. (4 June 2008)."Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators".PLOS ONE.3(6): e2276.Bibcode:2008PLoSO...3.2276G.doi:10.1371/journal.pone.0002276.PMC2386968.PMID18523578.
  19. ^Core, Andrew; Runcke, Charles; Ivers, Jonathan; Quock, Christopher; Siapno, Travis; DeNault, Seraphina; Brown, Brian; DeRisi, Joseph; Smith, Christopher D.; Hafernik, John (2012)."A new threat to honey bees, the parasitic phorid flyApocephalus borealis".PLoS ONE.7(1): e29639.Bibcode:2012PLoSO...729639C.doi:10.1371/journal.pone.0029639.PMC3250467.PMID22235317.
  20. ^Eggleton, P.; Belshaw, R. (1992). "Insect parasitoids: an evolutionary overview".Philosophical Transactions of the Royal Society B.337(1279): 1–20.Bibcode:1992RSPTB.337....1E.doi:10.1098/rstb.1992.0079.
  21. ^Foottit, R. G.; Adler, P. H. (2009).Insect Biodiversity: Science and Society, Volume 1.Wiley-Blackwell. p. 656.ISBN978-1118945537.
  22. ^abFoottit, Robert G. (2017).Insect Biodiversity: Science and Society.John Wiley & Sons. p. 606.ISBN978-1-118-94553-7.
  23. ^"Parasites (Parasitoids)".University of Alberta. Archived fromthe originalon 2 March 2018.Retrieved10 March2018.
  24. ^Niehuis, O.; Hartig, G.; Grath, S.; Pohl, H.; Lehmann, J.; Tafer, H.; Donath, A.; Krauss, V.; Eisenhardt, C.; Hertel, J.; Petersen, M.; Mayer, C.; Meusemann, K.; Peters, R.S.; Stadler, P.F.; Beutel, R.G.; Bornberg-Bauer, E.; McKenna, D.D.; Misof, B. (2012)."Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera".Current Biology.22(14): 1309–1313.Bibcode:2012CBio...22.1309N.doi:10.1016/j.cub.2012.05.018.PMID22704986.
  25. ^Colgan, Donald J.; Zhao, Chenjing; Liu, Xingyue; Yang, Ding (2014)."Wing Base Structural Data Support the Sister Relationship of Megaloptera and Neuroptera (Insecta: Neuropterida)".PLOS ONE.9(12): e114695.Bibcode:2014PLoSO...9k4695Z.doi:10.1371/journal.pone.0114695.PMC4263614.PMID25502404.
  26. ^abcdefghMills, N. (2009)."Parasitoids".In V. H. Resh; R. T. Cardé (eds.).Encyclopedia of Insects(2nd ed.). Elsevier. pp. 748–750.ISBN978-0123741448.
  27. ^Goulet, Henri; Huber, John Theodore (1993).Hymenoptera of the world: an identification guide to families.Centre for Land and Biological Resources Research.ISBN978-0-660-14933-2.OCLC28024976.
  28. ^Hochberg, M.; Elmes, G. W.; Thomas, J. A.; Clarke, R. T. (1996). "Mechanisms of local persistence in coupled host-parasitoid associations: the case model of Maculinea rebeli and Ichneumon eumerus".Philosophical Transactions of the Royal Society B: Biological Sciences.351(1348): 1713–1724.Bibcode:1996RSPTB.351.1713H.doi:10.1098/rstb.1996.0153.
  29. ^abApostolos, Kapranas; Tena, Alejandro; Luck, Robert F. (2012). "Dynamic virulence in a parasitoid wasp: the influence of clutch size and sequential oviposition on egg encapsulation".Animal Behaviour.83(3): 833–838.doi:10.1016/j.anbehav.2012.01.004.S2CID54275511.
  30. ^Gullan, P. J.; Cranston, P. S. (2010).The Insects: An Outline of Entomology(4th ed.). Wiley. pp.364,367.ISBN978-1-118-84615-5.
  31. ^Gomez, Jose-Maria; van Achterberg, Cornelius (2011)."Oviposition behaviour of four ant parasitoids (Hymenoptera, Braconidae, Euphorinae, Neoneurini and Ichneumonidae, Hybrizontinae), with the description of three new European species".ZooKeys(125): 59–106.Bibcode:2011ZooK..125U..59V.doi:10.3897/zookeys.125.1754.PMC3185369.PMID21998538.
  32. ^Quicke, D. L. J.; Fitton, M. G. (22 July 1995). "Ovipositor Steering Mechanisms in Parasitic Wasps of the Families Gasteruptiidae and Aulacidae (Hymenoptera)".Proceedings of the Royal Society B: Biological Sciences.261(1360). The Royal Society: 99–103.Bibcode:1995RSPSB.261...99Q.doi:10.1098/rspb.1995.0122.S2CID84043987.The length of the ovipositor compared with the body of the parasitic wasp varies enormously between taxa, from being a fraction of the length of the metasoma to more than 14 times longer than the head and body. (Townes 1975; Achterberg 1986; Compton & Nefdt 1988).
  33. ^Van Achterberg Cornelius; Argaman Q. "Kollasmosoma gen. nov. and a key to the genera of the subfamily Neoneurinae (Hymenoptera: Braconidae)". Zoologische Mededelingen Leiden. 67. (1993):63-74.
  34. ^Schmidt, O.; Theopold, U.; Strand, M.R. (2001). "Innate immunity and evasion by insect parasitoids".BioEssays.23(4): 344–351.doi:10.1002/bies.1049.PMID11268040.S2CID20850885.
  35. ^Salt, George (1968). "The resistance of insect parasitoids to the defense reactions of their hosts".Biological Reviews of the Cambridge Philosophical Society.43(2): 200–232.doi:10.1111/j.1469-185x.1968.tb00959.x.PMID4869949.S2CID21251615.
  36. ^Summers, M. D.; Dib-Hajj (1995)."Polydnavirus-facilitated endoparasite protection against host immune defenses".PNAS.92(1): 29–36.Bibcode:1995PNAS...92...29S.doi:10.1073/pnas.92.1.29.PMC42812.PMID7816835.
  37. ^Kessler, Andre; Baldwin, Ian T. (2002). "Plant Responses to Insect Herbivory: The Emerging Molecular Analysis".Annual Review of Plant Biology.53:299–328.doi:10.1146/annurev.arplant.53.100301.135207.PMID12221978.
  38. ^ab"Midwest Biological Control News".Department of Entomology at the University of Wisconsin–Madison. Archived fromthe originalon 5 October 2017.Retrieved19 February2018.
  39. ^Wuellner, C. T.; et al. (2002)."Phorid Fly (Diptera: Phoridae) Oviposition Behavior and Fire Ant (Hymenoptera: Formicidae) Reaction to Attack Differ According to Phorid Species".Annals of the Entomological Society of America.95(2): 257–266.doi:10.1603/0013-8746(2002)095[0257:pfdpob]2.0.co;2.
  40. ^Feener, Donald H. Jr.; Jacobs, Lucia F.; Schmidt, Justin O. (January 1996). "Specialized parasitoid attracted to a pheromone of ants".Animal Behaviour.51(1): 61–66.doi:10.1006/anbe.1996.0005.ISSN0003-3472.S2CID16627717.
  41. ^Köhler, U.; Lakes-Harlan, R. (October 2001). "Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera)".J Comp Physiol A.187(8): 581–587.doi:10.1007/s003590100230.PMID11763956.S2CID23343345.
  42. ^Whiting, M. F. (2003). "Strepsiptera". In Resh, V. H.; Cardé, R. T. (eds.).Encyclopedia of Insects.Academic Press. pp.1094–1096.ISBN9780125869904.
  43. ^Falin, Z. H. (2002). "102. Ripiphoridae. Gemminger and Harold 1870 (1853)". In Arnett, R.H. Jr; Thomas, M. C.; Skelley, P. E.; Frank, J. H. (eds.).American beetles. Volume 2. Polyphaga: Scarabaeoidea through Curculionoidea.CRC Press. pp. 431–444.doi:10.1201/9781420041231.ch6.ISBN978-0-8493-0954-0.
  44. ^Lawrence, J. F.; Falin, Z. H.; Ślipiński, A. (2010). "Ripiphoridae Gemminger and Harold, 1870 (Gerstaecker, 1855)". In Leschen, R. A. B.; Beutel, R. G.; Lawrence, J. F. (eds.).Coleoptera, beetles. Volume 2: Morphology and systematics (Elateroidea, Bostrichiformia, Cucujiformia partim).New York: Walter de Gruyter. pp. 538–548.doi:10.1515/9783110911213.538.ISBN978-3-11-019075-5.
  45. ^Yamamoto, Shûhei; Maruyama, Munetoshi (2016). "Revision of the subgenusAleocharaGravenhorst of the parasitoid rove beetle genusAleocharaGravenhorst of Japan (Coleoptera: Staphylinidae: Aleocharinae) ".Zootaxa.4101(1): 1–68.doi:10.11646/zootaxa.4101.1.1.PMID27394607.
  46. ^Godfray, H. C. J. (1994).Parasitoids: Behavioral and Evolutionary Ecology.Princeton University Press. p.40.ISBN978-0-691-00047-3.
  47. ^Pierce, Naomi E. (1995)."Predatory and Parasitic Lepidoptera: Carnivores Living on Plants"(PDF).Journal of the Lepidopterists' Society.49(4): 412–453.
  48. ^Wells, Alice (2005). "Parasitism by hydroptilid caddisflies (Trichoptera) and seven new species of Hydroptilidae from northern Queensland".Australian Journal of Entomology.44(4): 385–391.doi:10.1111/j.1440-6055.2005.00492.x.
  49. ^Gerson, Uri; Smiley, Robert L.; Ochoa, Ronald, eds. (23 January 2003),"Acarophenacidae",Mites (Acari) for Pest Control(1 ed.), Wiley, pp. 74–77,doi:10.1002/9780470750995.ch5,ISBN978-0-632-05658-3,retrieved28 August2024
  50. ^Qu, Shuai-Ling; Li, Su-Su; Li, Dong; Zhao, Pei-Ji (24 July 2022)."Metabolites and Their Bioactivities from the Genus Cordyceps".Microorganisms.10(8): 1489.doi:10.3390/microorganisms10081489.ISSN2076-2607.PMC9330831.PMID35893547.
  51. ^Evans, Harry C.; Elliot, Simon L.; Hughes, David P. (1 September 2011)."Ophiocordyceps unilateralis:A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? ".Communicative & Integrative Biology.4(5): 598–602.doi:10.4161/cib.16721.PMC3204140.PMID22046474.
  52. ^Hughes, David P; Andersen, Sandra B; Hywel-Jones, Nigel L; Himaman, Winanda; Billen, Johan; Boomsma, Jacobus J (2011)."Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection".BMC Ecology.11(1): 13.Bibcode:2011BMCE...11...13H.doi:10.1186/1472-6785-11-13.ISSN1472-6785.PMC3118224.PMID21554670.
  53. ^Sheldrake, Merlin (2021).Entangled Life.Vintage. pp. 107–119.ISBN9781784708276.
  54. ^Pontoppidan, Maj-Britt; Himaman, Winanda; Hywel-Jones, Nigel L.; Boomsma, Jacobus J.; Hughes, David P. (12 March 2009). Dornhaus, Anna (ed.)."Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants".PLOS ONE.4(3): e4835.Bibcode:2009PLoSO...4.4835P.doi:10.1371/journal.pone.0004835.ISSN1932-6203.PMC2652714.PMID19279680.
  55. ^Pontoppidan, Maj-Britt; Himaman, Winanda; Hywel-Jones, Nigel L.; Boomsma, Jacobus J.; Hughes, David P. (12 March 2009). Dornhaus, Anna (ed.)."Graveyards on the Move: The Spatio-Temporal Distribution of DeadOphiocordyceps-Infected Ants ".PLOS ONE.4(3): e4835.Bibcode:2009PLoSO...4.4835P.doi:10.1371/journal.pone.0004835.ISSN1932-6203.PMC2652714.PMID19279680.
  56. ^Zhang, Yongjie; Li, Erwei; Wang, Chengshu; Li, Yuling; Liu, Xingzhong (1 March 2012)."Ophiocordyceps sinensis, the flagship fungus of China: terminology, life strategy and ecology".Mycology.3(1): 2–10.doi:10.1080/21501203.2011.654354.ISSN2150-1203.
  57. ^Cade, W. (26 December 1975)."Acoustically Orienting Parasitoids: Fly Phonotaxis to Cricket Song".Science.190(4221): 1312–1313.doi:10.1126/science.190.4221.1312.ISSN0036-8075.
  58. ^Gray, David A.; Banuelos, Christina; Walker, Sean E.; Cade, William H.; Zuk, Marlene (1 January 2007)."Behavioural specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts".Animal Behaviour.73(1): 99–104.doi:10.1016/j.anbehav.2006.07.005.hdl:10211.3/195743.ISSN0003-3472.
  59. ^Paur, Jennifer; Gray, David A. (1 October 2011)."Individual consistency, learning and memory in a parasitoid fly, Ormia ochracea".Animal Behaviour.82(4): 825–830.doi:10.1016/j.anbehav.2011.07.017.ISSN0003-3472.
  60. ^Bale, J.S; van Lenteren, J.C; Bigler, F (February 2008)."Biological control and sustainable food production".Philosophical Transactions of the Royal Society B: Biological Sciences.363(1492). The Royal Society: 761–776.doi:10.1098/rstb.2007.2182.PMC2610108.PMID17827110.
  61. ^Legner, Erich F."Economic Gains & Analysis Of Successes In Biological Pest Control".University of California, Riverside.Archivedfrom the original on 23 June 2008.Retrieved13 February2018.
  62. ^"Parasitoid Wasps (Hymenoptera)".University of Maryland. Archived fromthe originalon 27 August 2016.Retrieved6 June2016.
  63. ^Smith, S. M. (1996). "Biological control with Trichogramma: advances, successes, and potential of their use".Annual Review of Entomology.41:375–406.doi:10.1146/annurev.en.41.010196.002111.PMID15012334.
  64. ^Wajnberg, E.; Hassan, S.A. (1994).Biological Control with Egg Parasitoids.CABI Publishing.
  65. ^Todd, Kim (2011). "Maria Sibylla Merian (1647-1717): an early investigator of parasitoids and phenotypic plasticity".Terrestrial Arthropod Reviews.4(2): 131–144.doi:10.1163/187498311X567794.
  66. ^On the Origin of Species,Chapter 7,page 218.
  67. ^"Letter 2814 — Darwin, C. R. to Gray, Asa, 22 May [1860]".Retrieved5 April2011.
  68. ^Prothero, Donald R. (2017).Evolution: What the Fossils Say and Why It Matters.Columbia University Press. pp. 84–86.ISBN978-0-231-54316-3.
  69. ^Budanovic, Nikola (10 March 2018)."An explanation emerges for how the 12th century Paisley Abbey in Scotland could feature a gargoyle out of the film" Alien "".The Vintage News.Retrieved17 June2018.
  70. ^"'Alien' gargoyle on ancient Paisley Abbey ".British Broadcasting Corporation.23 August 2013.Retrieved17 June2018.
  71. ^abMoisseeff, Marika(23 January 2014).Aliens as an Invasive Reproductive Power in Science Fiction.Polis, Sofia. pp. 239–257.{{cite book}}:|website=ignored (help)
  72. ^Pappas, Stephanie (29 May 2012)."5 Alien Parasites and Their Real-World Counterparts".Live Science.
  73. ^Williams, Robyn; Field, Scott (27 September 1997)."Behaviour, Evolutionary Games and.... Aliens".Australian Broadcasting Corporation.Retrieved30 November2017.
  74. ^"The Making of Alien's Chestburster Scene".The Guardian.13 October 2009.Archivedfrom the original on 30 April 2010.Retrieved29 May2010.
  75. ^abSercel, Alex (19 May 2017)."Parasitism in the Alien Movies".Signal to Noise Magazine.
  76. ^Dove, Alistair (9 May 2011)."This is clearly an important species we're dealing with".Deep Sea News.
  77. ^"Parasitism and Symbiosis".The Encyclopedia of Science Fiction.10 January 2016.

Retrieved from "https://en.wikipedia.org/w/index.php?title=Parasitoid&oldid=1242727606#Definitions_and_distinctions"