Parasitoid#Types of parasitoids

The term "parasitoid" was coined in 1913 by the Swedo-Finnish writer Odo Reuter,{{cite book |author=Reuter, Odo M. |author-link=Odo Reuter |year=1913 |title=Lebensgewohnheiten und Instinkte der Insekten |trans-title=Habits and instincts of the insects up to the awakening of social instincts |publisher=R. Friedländer und Sohn |language=de}} and adopted in English by his reviewer,{{cite journal | last=Wheeler | first=William Morton | title=Scientific Books {{!}} Lebensgewohnheiten und Instinkte der Insekten bis zum Erwachen der sozialen Instinkte | journal=Science | publisher=American Association for the Advancement of Science (AAAS) | volume=39 | issue=993 | date=9 January 1914 | doi=10.1126/science.39.993.69 | pages=69–71}} the entomologist William Morton Wheeler.{{cite book |author=Wheeler, William Morton |author-link=William Morton Wheeler |title=Social life among the insects: being a series of lectures delivered at the Lowell Institute in Boston in March 1922 |publisher=Harcourt, Brace |year=1923 |url=https://archive.org/details/sociallifeamongi00whee}} Previously published in Scientific Monthly, June 1922 to February 1923. 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.{{cite book |last=Godfray |first=H. C. J. |title=Parasitoids: Behavioral and Evolutionary Ecology |url=https://archive.org/details/parasitoidsbehav0000godf |url-access=registration |date=1994 |publisher=Princeton University Press |isbn=978-0-691-00047-3}}

A perspective on the evolutionary options can be gained by considering four questions: the effect on the reproductive fitness of 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.{{cite journal |last1=Lafferty |first1=K. D. |last2=Kuris |first2=A. M. |date=2002 |title=Trophic strategies, animal diversity and body size |journal=Trends Ecol. Evol. |volume=17 |issue=11 |pages=507–513 |doi=10.1016/s0169-5347(02)02615-0}}

Parasitoidism, in the view of R. Poulin and H. S. Randhawa, is one of six main 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.{{cite journal |last1=Poulin |first1=Robert |author1-link=Robert Poulin (zoologist) |last2=Randhawa |first2=Haseeb S. |title=Evolution of parasitism along convergent lines: from ecology to genomics |journal=Parasitology |date=February 2015 |volume=142 |issue=Supplement 1 |pages=S6–S15 |doi=10.1017/S0031182013001674 |pmc=4413784 |pmid=24229807}}{{cite book |author=Poulin, Robert |author-link=Robert Poulin (zoologist) |editor1=Rollinson, D. |editor2=Hay, S. I. |title=The Many Roads to Parasitism: A Tale of Convergence |journal=Advances in Parasitology |url=https://books.google.com/books?id=9y4AlXka7t0C&pg=PA28 |year=2011 |volume=74 |publisher=Academic Press |isbn=978-0-12-385897-9 |pages=27–28|doi=10.1016/B978-0-12-385897-9.00001-X |pmid=21295676 }}

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.{{cite journal |last1=Stevens |first1=Alison N. P. |title=Predation, Herbivory, and Parasitism |journal=Nature Education Knowledge |date=2010 |volume=3 |issue=10 |page=36 |url=https://www.nature.com/scitable/knowledge/library/predation-herbivory-and-parasitism-13261134 |access-date=12 February 2018 |quote=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.}}{{cite journal |last1=Møller |first1=A. P. |year=1990 |title=Effects of parasitism by a haematophagous mite on reproduction in the barn swallow |jstor=1938645 |journal=Ecology |volume=71 |issue=6 |pages=2345–2357 |doi=10.2307/1938645|bibcode=1990Ecol...71.2345M }}

{{anchor|Koinobiont}}

{{anchor|Idiobiont}}

File:Pteromalid hyperparasitoid.jpg chalcidoid wasp on the cocoons of its host, a braconid wasp, 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, 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 and moult. Most endoparasitoids are koinobionts, giving them the advantage of a host that continues to grow larger and avoid predators.{{cite book |author1=Gullan, P. J. |author2=Cranston, P. S. |date=2014 |title=The Insects: An Outline of Entomology |publisher=Wiley |edition=5th |isbn=978-1-118-84615-5 |pages=362–370}}

Primary parasitoids have the simplest parasitic relationship, involving two organisms, the host and the parasitoid. Hyperparasitoids are 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. In oak gall systems, there can be up to five levels of parasitism.{{cite journal |last=Askew |first=R. R. |date=1961 |title=On the biology of the inhabitants of oak galls of Cynipidae (Hymenoptera) in Britain |url=https://www.researchgate.net/publication/238289888 |journal=Transactions of the Society for British Entomology |volume=14 |pages=237–268}} 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 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.{{cite book |author1=Gullan, P. J. |author2=Cranston, P. S. |date=2014 |title=The Insects: An Outline of Entomology |publisher=Wiley |edition=5th |pages=365–369 |isbn=978-1-118-84615-5 }}{{cite journal |last=Fisher |first=R. C. |title=A Study in Insect Multiparasitism: I. Host Selection and Oviposition |journal=Journal of Experimental Biology |date=1 June 1961 |volume=38 |issue=2 |pages=267–275 |doi=10.1242/jeb.38.2.267 |url=http://jeb.biologists.org/cgi/reprint/38/2/267.pdf}}

File:Female Apocephalus borealis ovipositing into the abdomen of a worker honey bee.png Apocephalus borealis (centre left) ovipositing into the abdomen of a worker honey bee, altering its behaviour]]

{{further|Behavior-altering parasite}}

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, 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 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.{{cite journal |author=Wojcik, Daniel P. |title=Behavioral Interactions between Ants and Their Parasites |journal=The Florida Entomologist |volume=72 |issue=1 |date=March 1989 |pages=43–51 |doi=10.2307/3494966|jstor=3494966 }} 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.{{cite journal |author=Taylor, P. J. |title=A systematic and population genetic approach to the rabies problem in the yellow mongoose (Cynictis penicillata) |journal=Onderstepoort J. Vet. Res. |volume=60 |issue=4 |pages=379–87 |date=December 1993 |pmid=7777324}} Among the parasitic wasps, Glyptapanteles modifies the behaviour of its host caterpillar to defend the pupae of the wasps after they emerge from the caterpillar's body.{{cite journal |last1=Grosman |first1=Amir H. |last2=Janssen |first2=Arne |last3=Brito |first3=Elaine F. de |last4=Cordeiro |first4=Eduardo G. |last5=Colares |first5=Felipe |last6=Fonseca |first6=Juliana Oliveira |last7=Lima |first7=Eraldo R. |last8=Pallini |first8=Angelo |last9=Sabelis |first9=Maurice W. |date=4 June 2008 |title=Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators |journal=PLOS ONE |volume=3 |issue=6 |pages=e2276 |doi=10.1371/journal.pone.0002276 |pmc=2386968 |pmid=18523578|bibcode=2008PLoSO...3.2276G |doi-access=free }} 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.{{cite journal |last1=Core |first1=Andrew |last2=Runcke |first2=Charles |last3=Ivers |first3=Jonathan |last4=Quock |first4=Christopher |last5=Siapno |first5=Travis |last6=DeNault |first6=Seraphina |last7=Brown |first7=Brian |last8=DeRisi |first8=Joseph |last9=Smith |first9=Christopher D. |last10=Hafernik |first10=John |year=2012 |title=A new threat to honey bees, the parasitic phorid fly Apocephalus borealis |journal=PLoS ONE |volume=7 |issue=1 |pages=e29639 |doi=10.1371/journal.pone.0029639 |pmid=22235317 |pmc=3250467|bibcode=2012PLoSO...729639C |doi-access=free }}

About 10% of described insects are parasitoids, in the orders Hymenoptera, Diptera, Coleoptera, Neuroptera, Lepidoptera, Strepsiptera, and Trichoptera. The majority are wasps within the Hymenoptera; most of the others are Dipteran flies.{{cite journal |last1=Eggleton |first1=P. |last2=Belshaw |first2=R. |year=1992 |title=Insect parasitoids: an evolutionary overview |journal=Philosophical Transactions of the Royal Society B |volume=337 |issue=1279 |pages=1–20 |doi=10.1098/rstb.1992.0079|bibcode=1992RSPTB.337....1E }}{{cite book |last1=Foottit |first1=R. G. |last2=Adler |first2=P. H. |year=2009 |title=Insect Biodiversity: Science and Society, Volume 1 |page=656 |publisher=Wiley-Blackwell |isbn=978-1118945537}} Parasitoidism has evolved independently many 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 all holometabolous insects (Endopterygota, which form a single clade), and it is always the larvae that are parasitoidal. The metamorphosis from active larva to an adult with a different body structure permits the dual lifestyle of parasitic larva, freeliving adult in this group.{{cite web|title=Parasites (Parasitoids)|url=http://www.biology.ualberta.ca/courses.hp/ent207/lec31-32.htm|publisher=University of Alberta|access-date=10 March 2018|archive-date=2 March 2018|archive-url=https://web.archive.org/web/20180302202049/http://www.biology.ualberta.ca/courses.hp/ent207/lec31-32.htm|url-status=dead}} These relationships are shown on the phylogenetic tree;{{cite journal |author1=Niehuis, O. |author2=Hartig, G. |author3=Grath, S. |author4=Pohl, H. |author5=Lehmann, J. |author6=Tafer, H. |author7=Donath, A. |author8=Krauss, V. |author9=Eisenhardt, C. |author10=Hertel, J. |author11=Petersen, M. |author12=Mayer, C. |author13=Meusemann, K. |author14=Peters, R.S. |author15=Stadler, P.F. |author16=Beutel, R.G. |author17=Bornberg-Bauer, E. |author18=McKenna, D.D. |author19=Misof, B. | year=2012 |title=Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera | journal=Current Biology | volume=22 | issue=14 | pages=1309–1313 |doi=10.1016/j.cub.2012.05.018 | pmid=22704986|doi-access=free |bibcode=2012CBio...22.1309N }}{{cite journal |last1=Colgan |first1=Donald J. |last2=Zhao |first2=Chenjing |last3=Liu |first3=Xingyue |last4=Yang |first4=Ding |title=Wing Base Structural Data Support the Sister Relationship of Megaloptera and Neuroptera (Insecta: Neuropterida) |journal=PLOS ONE |volume=9 |issue=12 |year=2014 |pages=e114695 |doi=10.1371/journal.pone.0114695|pmid=25502404 |pmc=4263614 |bibcode=2014PLoSO...9k4695Z |doi-access=free }} 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 out of the total is shown in square brackets, e.g. [2,500 of 400,000].

{{clade

|label1=Endopterygota

|1={{clade

|1={{clade

|label1=Neuropterida

|1={{clade

|1=Raphidioptera

|2={{clade

|1=Megaloptera

|2=Neuroptera (net-winged insects) (1 clade) [c. 15 of 6,000]

}}

}}

|label2=Coleopterida

|2={{clade

|1=Coleoptera (beetles) (10 clades) [c. 2,500 of 400,000] File:Ripiphorid larva on wing of braconid wasp.jpg beetle triungulin larva on the wing of a braconid wasp|90px]]

|label2=(1 clade)

|2=Strepsiptera (twisted-wing parasites) [600 of 600] 90px

}}

}}

|2={{clade

|label1=Hymenoptera

|1={{clade

|1=Symphyta

|label2= (1 clade)

|2={{clade

|1=Orussoidea (parasitic wood wasps) [75 of 75] File:Orussus coronatus.jpg

|2=Apocrita (wasp-waisted insects) [c. 50,000 of 100,000] alt=The [[parasitoid wasp Megarhyssa macrurus ovipositing into host through wood. Her body is c. 50 mm long, her ovipositor c. 100 mm.|90px]]

}}

}}

|label2=Panorpida

|2={{clade

|1={{clade

|1=Diptera (true flies) (21 clades) [c. 17,000 of 125,000] alt=[[Stylogaster, a conopid fly, showing the long ovipositor|100px]]

|2={{clade

|1=Mecoptera

|2=Siphonaptera

}}

}}

|2={{clade

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

|2=Lepidoptera (butterflies, moths) (2 clades) [c. 40 of 180,000] alt=Moth Epiricania hagoromo ([[Epipyropidae) feeding on planthopper Euricania facialis|120px]]

}}

}}

}}

}}

}}

{{main|Parasitoid wasp}}

File:Potter Wasp building mud nest near completion.JPG, an idiobiont, building a mud nest; she will provision it with 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{{efn|There may be far more species of parasitoid wasp not yet described.}} species of parasitoid wasps{{cite book |title=Hymenoptera of the world : an identification guide to families |date=1993 |publisher=Centre for Land and Biological Resources Research |author1=Goulet, Henri |author2=Huber, John Theodore |isbn=978-0-660-14933-2 |oclc=28024976}} represent the great majority of species in the order, barring those like the ants, bees, and Vespidae wasps that have secondarily lost the parasitoid habit. The parasitoid wasps include some 25,000 Ichneumonoidea, 22,000 Chalcidoidea, 5,500 Vespoidea, 4,000 Platygastroidea, 3,000 Chrysidoidea, 2,300 Cynipoidea, and many smaller families. These often have remarkable life cycles.{{cite journal |last=Hochberg |first=M. |author2=Elmes, G. W. |author3=Thomas, J. A. |author4=Clarke, R. T. |title=Mechanisms of local persistence in coupled host-parasitoid associations: the case model of Maculinea rebeli and Ichneumon eumerus|year=1996 |volume=351 |issue=1348 |pages=1713–1724 |doi=10.1098/rstb.1996.0153 |journal=Philosophical Transactions of the Royal Society B: Biological Sciences|bibcode=1996RSPTB.351.1713H }}

They can be classified as either endoparasitic or ectoparasitic according to where they lay their eggs.{{cite journal |author1=Apostolos, Kapranas |author2=Tena, Alejandro |author3=Luck, Robert F. |title=Dynamic virulence in a parasitoid wasp: the influence of clutch size and sequential oviposition on egg encapsulation |journal=Animal Behaviour |volume=83 |issue=3 |year=2012 |pages=833–838 |doi=10.1016/j.anbehav.2012.01.004|s2cid=54275511 }} 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. Most species of wasps attack the eggs or larvae of their host, but some attack adults. Oviposition depends 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.{{cite book |author1=Gullan, P. J. |author2=Cranston, P. S. |date=2010 |title=The Insects: An Outline of Entomology |url=https://archive.org/details/insectsoutlineen00pjgu |url-access=limited |publisher=Wiley |edition=4th |pages=[https://archive.org/details/insectsoutlineen00pjgu/page/n388 364], 367 |isbn=978-1-118-84615-5}}{{cite journal | last1=Gomez | first1=Jose-Maria | last2=van Achterberg | first2=Cornelius | year=2011 | title=Oviposition behaviour of four ant parasitoids (Hymenoptera, Braconidae, Euphorinae, Neoneurini and Ichneumonidae, Hybrizontinae), with the description of three new European species | journal=ZooKeys | issue=125 | pages=59–106 | doi=10.3897/zookeys.125.1754| pmid=21998538 | pmc=3185369 | doi-access=free | bibcode=2011ZooK..125U..59V }}{{cite journal | last1=Quicke | first1=D. L. J. | last2=Fitton | first2=M. G. | title=Ovipositor Steering Mechanisms in Parasitic Wasps of the Families Gasteruptiidae and Aulacidae (Hymenoptera) | journal=Proceedings of the Royal Society B: Biological Sciences | publisher=The Royal Society | volume=261 | issue=1360 | date=22 July 1995 | doi=10.1098/rspb.1995.0122 | pages=99–103 | bibcode=1995RSPSB.261...99Q | s2cid=84043987 |quote=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).}} 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.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.

Parasitoid wasps face a range of obstacles to oviposition, including behavioural, morphological, physiological and immunological defences of their hosts.{{cite journal | last1=Schmidt | first1=O. | last2=Theopold | first2=U. | last3=Strand | first3=M.R. | year=2001 | title=Innate immunity and evasion by insect parasitoids | journal=BioEssays | volume=23 | issue=4| pages=344–351 | doi=10.1002/bies.1049| pmid=11268040 | s2cid=20850885 }} To thwart this, some wasps inundate their host with their eggs so as to overload its immune system's ability to encapsulate foreign bodies;{{cite journal |last1=Salt |first1=George | year=1968 | title=The resistance of insect parasitoids to the defense reactions of their hosts | journal=Biological Reviews of the Cambridge Philosophical Society | volume=43 | issue=2| pages=200–232 | doi=10.1111/j.1469-185x.1968.tb00959.x|pmid=4869949 |s2cid=21251615 }} others introduce a virus which interferes with the host's immune system.{{cite journal | last1=Summers | first1=M. D. | last2=Dib-Hajj | year=1995 | title=Polydnavirus-facilitated endoparasite protection against host immune defenses | journal=PNAS | volume=92 | issue=1 | pages=29–36 | doi=10.1073/pnas.92.1.29| pmid=7816835 | pmc=42812 | bibcode=1995PNAS...92...29S | doi-access=free }}

Some parasitoid wasps locate hosts by detecting the chemicals that plants release to defend against insect herbivores.{{cite journal | last1=Kessler | first1=Andre | last2=Baldwin | first2=Ian T. | year=2002 | title=Plant Responses to Insect Herbivory: The Emerging Molecular Analysis | journal= Annual Review of Plant Biology | volume=53 | pages=299–328 | doi=10.1146/annurev.arplant.53.100301.135207| pmid=12221978 }}

File:Odynerus spinipes^ Vespidae. See parasite note - Flickr - gailhampshire.jpgn protruding (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 the Tachinidae (some 9,200 species), followed by the Bombyliidae (some 4,500 species), along with the Pipunculidae and the Conopidae, which includes parasitoidal genera such as Stylogaster. Other families of flies include some protelean species.{{cite web |url=http://www.entomology.wisc.edu/mbcn/fea506.html |title=Midwest Biological Control News |publisher=Department of Entomology at the University of Wisconsin–Madison |access-date=19 February 2018 |archive-date=5 October 2017 |archive-url=https://web.archive.org/web/20171005235859/http://www.entomology.wisc.edu/mbcn/fea506.html |url-status=dead }} Some Phoridae are parasitoids of ants.{{cite journal |last1=Wuellner |first1=C. T.|display-authors=etal|title=Phorid Fly (Diptera: Phoridae) Oviposition Behavior and Fire Ant (Hymenoptera: Formicidae) Reaction to Attack Differ According to Phorid Species |journal=Annals of the Entomological Society of America |date=2002 |volume=95 |issue=2 |pages=257–266 |doi=10.1603/0013-8746(2002)095[0257:pfdpob]2.0.co;2 |doi-access=free}}{{Cite journal|last1=Feener |first1=Donald H. Jr.|last2=Jacobs |first2=Lucia F.|last3=Schmidt |first3=Justin O. |date=January 1996 |title=Specialized parasitoid attracted to a pheromone of ants |journal=Animal Behaviour |volume=51 |issue=1 |pages=61–66 |doi=10.1006/anbe.1996.0005|s2cid=16627717|issn=0003-3472}} Some flesh flies are parasitoids: for instance Emblemasoma auditrix is parasitoidal on cicadas, locating its host by sound.{{cite journal |author1=Köhler, U. |author2=Lakes-Harlan, R. |title=Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera) |journal=J Comp Physiol A |date=October 2001 |volume=187 |issue=8 |pages=581–587|doi=10.1007/s003590100230 |pmid=11763956 |s2cid=23343345 }}

The Strepsiptera (twisted-wing parasites) consist entirely of parasitoids; they usually sterilise their hosts.{{cite book |author=Whiting, M. F. |editor1=Resh, V. H. |editor2=Cardé, R. T. |year=2003 |title=Encyclopedia of Insects |url=https://archive.org/details/encyclopediainse00resh |url-access=limited |publisher=Academic Press |chapter=Strepsiptera |pages=[https://archive.org/details/encyclopediainse00resh/page/n1122 1094]–1096|isbn=9780125869904 }}

Two beetle families, Ripiphoridae (450 species){{cite book |author=Falin, Z. H. |year=2002 |chapter=102. Ripiphoridae. Gemminger and Harold 1870 (1853) |pages=431–444 |editor1=Arnett, R.H. Jr |editor2=Thomas, M. C. |editor3=Skelley, P. E. |editor4=Frank, J. H. |title=American beetles. Volume 2. Polyphaga: Scarabaeoidea through Curculionoidea |publisher=CRC Press |isbn=978-0-8493-0954-0 |doi=10.1201/9781420041231.ch6|doi-broken-date=12 November 2024 }}{{cite book |author1=Lawrence, J. F. |author2=Falin, Z. H. |author3=Ślipiński, A. |year=2010 |chapter=Ripiphoridae Gemminger and Harold, 1870 (Gerstaecker, 1855) |pages=538–548 |editor=Leschen, R. A. B. |editor2=Beutel, R. G. |editor3=Lawrence, J. F. |title=Coleoptera, beetles. Volume 2: Morphology and systematics (Elateroidea, Bostrichiformia, Cucujiformia partim) |place=New York |publisher=Walter de Gruyter |isbn=978-3-11-019075-5 |doi=10.1515/9783110911213.538}} and Rhipiceridae, are largely parasitoids, as are Aleochara Staphylinidae; in all, some 400 staphylinids are parasitoidal.{{cite journal |last1=Yamamoto |first1=Shûhei |last2=Maruyama |first2=Munetoshi |title=Revision of the subgenus Aleochara Gravenhorst of the parasitoid rove beetle genus Aleochara Gravenhorst of Japan (Coleoptera: Staphylinidae: Aleocharinae) |journal=Zootaxa |volume=4101 |issue=1 |pages=1–68 |year=2016 |doi=10.11646/zootaxa.4101.1.1|pmid=27394607 }} Some 1,600 species of the large and mainly freeliving family Carabidae are parasitoids.

A few Neuroptera are parasitoidal; they have larvae that actively search for hosts.{{cite book |last=Godfray |first=H. C. J. |title=Parasitoids: Behavioral and Evolutionary Ecology |url=https://archive.org/details/parasitoidsbehav0000godf |url-access=registration |year=1994|publisher=Princeton University Press|isbn=978-0-691-00047-3 |page=[https://archive.org/details/parasitoidsbehav0000godf/page/40 40]}} The larvae of some Mantispidae, subfamily Symphrasinae, are parasitoids of other arthropods including bees and wasps.{{cite encyclopedia |author=Mills, N. |date=2009 |edition=2nd |title=Parasitoids |encyclopedia=Encyclopedia of Insects |editor=V. H. Resh |editor2=R. T. Cardé |pages=748–750 |publisher=Elsevier |isbn=978-0123741448 |url=https://books.google.com/books?id=Jk0Hym1yF0cC&pg=PA749}}

Although nearly all Lepidoptera (butterflies and moths) are herbivorous, a few species are parasitic. The larvae of Epipyropidae feed on Homoptera such as leafhoppers and cicadas, and sometimes on other Lepidoptera. The larvae of Cyclotornidae parasitise first Homoptera and later ant brood.{{cite journal |last1=Pierce |first1=Naomi E. |title=Predatory and Parasitic Lepidoptera: Carnivores Living on Plants |journal=Journal of the Lepidopterists' Society |date=1995 |volume=49 |issue=4 |pages=412–453 |url=http://images.peabody.yale.edu/lepsoc/jls/1990s/1995/1995-49(4)412-Pierce.pdf}} The pyralid moth Chalcoela has been used in biological control of the wasp Polistes in the Galapagos Islands.{{cite book |last=Foottit |first=Robert G. |title=Insect Biodiversity: Science and Society |url=https://books.google.com/books?id=V3ItDwAAQBAJ&pg=PA606 |year=2017 |publisher=John Wiley & Sons |isbn=978-1-118-94553-7 |page=606}}

Parasitism is rare in the Trichoptera (caddisflies), but it is found among the Hydroptilidae (purse-case caddisflies), probably including all 10 species in the Orthotrichia aberrans group; they parasitise the pupae of other trichopterans.{{cite journal | last=Wells | first=Alice | title=Parasitism by hydroptilid caddisflies (Trichoptera) and seven new species of Hydroptilidae from northern Queensland | journal=Australian Journal of Entomology | volume=44 | issue=4 | year=2005 | doi=10.1111/j.1440-6055.2005.00492.x | pages=385–391}}

Mites of the family Acarophenacidae are 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.{{Citation |title=Acarophenacidae |date=2003-01-23 |work=Mites (Acari) for Pest Control |pages=74–77 |editor-last=Gerson |editor-first=Uri |url=https://onlinelibrary.wiley.com/doi/10.1002/9780470750995.ch5 |access-date=2024-08-28 |edition=1 |publisher=Wiley |language=en |doi=10.1002/9780470750995.ch5 |isbn=978-0-632-05658-3 |editor2-last=Smiley |editor2-first=Robert L. |editor3-last=Ochoa |editor3-first=Ronald}}

All known fungi in the genera Cordyceps and Ophiocordyceps are endoparasitic.{{Cite journal |last1=Qu |first1=Shuai-Ling |last2=Li |first2=Su-Su |last3=Li |first3=Dong |last4=Zhao |first4=Pei-Ji |date=2022-07-24 |title=Metabolites and Their Bioactivities from the Genus Cordyceps |journal=Microorganisms |volume=10 |issue=8 |pages=1489 |doi=10.3390/microorganisms10081489 |issn=2076-2607 |pmc=9330831 |pmid=35893547|doi-access=free }} One of the most notable fungal parasitoids is O. unilateralis which 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'.{{Cite journal |last1=Evans |first1=Harry C. |last2=Elliot |first2=Simon L. |last3=Hughes |first3=David P. |date=September 1, 2011 |title=Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? |journal= Communicative & Integrative Biology |volume=4 |issue=5 |pages=598–602 |doi=10.4161/cib.16721 |pmid=22046474 |pmc=3204140 }} This approach is so fine-tuned, it causes the ant to bite down on the adaxial leaf midrib, which is the part of the leaf most optimal for the fungus to fruit. In fact, it has been found that in specific circumstances, the time of the death bite is synchronised to solar noon.{{Cite journal |last1=Hughes |first1=David P |last2=Andersen |first2=Sandra B |last3=Hywel-Jones |first3=Nigel L |last4=Himaman |first4=Winanda |last5=Billen |first5=Johan |last6=Boomsma |first6=Jacobus J |date=2011 |title=Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection |journal= BMC Ecology |language=en |volume=11 |issue=1 |pages=13 |doi=10.1186/1472-6785-11-13 |issn=1472-6785 |pmc=3118224 |pmid=21554670 |doi-access=free |bibcode=2011BMCE...11...13H }} As much as 40% of the ant's biomass is fungal hyphae at the moment of the death bite.{{Cite book |last=Sheldrake |first=Merlin |title=Entangled Life |publisher=Vintage |year=2021 |isbn=9781784708276 |pages=107–119 |language=En}} After the ant dies, the fungus produces a large stalk, growing from the back of the ant's head{{Cite journal |last1=Pontoppidan |first1=Maj-Britt |last2=Himaman |first2=Winanda |last3=Hywel-Jones |first3=Nigel L. |last4=Boomsma |first4=Jacobus J. |last5=Hughes |first5=David P. |date=2009-03-12 |editor-last=Dornhaus |editor-first=Anna |title=Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants |journal= PLOS ONE |language=en |volume=4 |issue=3 |pages=e4835 |doi=10.1371/journal.pone.0004835 |issn=1932-6203 |pmc=2652714 |pmid=19279680|doi-access=free |bibcode=2009PLoSO...4.4835P }} 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.{{Cite journal |last1=Pontoppidan |first1=Maj-Britt |last2=Himaman |first2=Winanda |last3=Hywel-Jones |first3=Nigel L. |last4=Boomsma |first4=Jacobus J. |last5=Hughes |first5=David P. |date=2009-03-12 |editor-last=Dornhaus |editor-first=Anna |title=Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants |journal= PLOS ONE |language=en |volume=4 |issue=3 |pages=e4835 |doi=10.1371/journal.pone.0004835 |issn=1932-6203 |pmc=2652714 |pmid=19279680|doi-access=free |bibcode=2009PLoSO...4.4835P }} O. sinesis is a parasitoid as well, parasitising ghost moth larvae, killing them within 15-25 days, a similar process to that of O. unilateralis.{{Cite journal |last1=Zhang |first1=Yongjie |last2=Li |first2=Erwei |last3=Wang |first3=Chengshu |last4=Li |first4=Yuling |last5=Liu |first5=Xingzhong |date=2012-03-01 |title=Ophiocordyceps sinensis, the flagship fungus of China: terminology, life strategy and ecology |journal=Mycology |volume=3 |issue=1 |pages=2–10 |doi=10.1080/21501203.2011.654354 |issn=2150-1203|doi-access=free }}

Host location has been studied in Ormia ochracea, a parasitoid tachinid fly that locates their field cricket host acoustically (phonotaxis).{{Cite journal |last=Cade |first=W. |date=1975-12-26 |title=Acoustically Orienting Parasitoids: Fly Phonotaxis to Cricket Song |url=https://www.science.org/doi/10.1126/science.190.4221.1312 |journal=Science |language=en |volume=190 |issue=4221 |pages=1312–1313 |doi=10.1126/science.190.4221.1312 |issn=0036-8075}} 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.{{Cite journal |last1=Gray |first1=David A. |last2=Banuelos |first2=Christina |last3=Walker |first3=Sean E. |last4=Cade |first4=William H. |last5=Zuk |first5=Marlene |date=2007-01-01 |title=Behavioural specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts |url=https://www.sciencedirect.com/science/article/pii/S0003347206003939 |journal=Animal Behaviour |volume=73 |issue=1 |pages=99–104 |doi=10.1016/j.anbehav.2006.07.005 |issn=0003-3472|hdl=10211.3/195743 |hdl-access=free }} A captive population of lab-reared flies were raised on two different host songs (Gryllus integer or G. lineaticeps). Responsive adult females overwhelmingly chose their familiar song, indicating the use of a learned, auditory search image. This phenotypic plasticity allows 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.{{Cite journal |last1=Paur |first1=Jennifer |last2=Gray |first2=David A. |date=2011-10-01 |title=Individual consistency, learning and memory in a parasitoid fly, Ormia ochracea |url=https://www.sciencedirect.com/science/article/pii/S0003347211002971 |journal=Animal Behaviour |volume=82 |issue=4 |pages=825–830 |doi=10.1016/j.anbehav.2011.07.017 |issn=0003-3472}} 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 of O. ochracea, as well as the presence and power of learning in parasitoids.

{{Main|Biological pest control}}

File:Encarsia formosa, an endoparasitic wasp, is used for whitefly control.jpg, an endoparasitic aphelinid wasp, bred commercially to control whitefly in greenhouses]]

Parasitoids are among the most widely used biological control agents. Classic biological pest control using 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.{{cite journal | last1=Bale | first1=J.S | last2=van Lenteren | first2=J.C | last3=Bigler | first3=F | title=Biological control and sustainable food production | journal=Philosophical Transactions of the Royal Society B: Biological Sciences | publisher=The Royal Society | volume=363 | issue=1492 | date=February 2008 | doi=10.1098/rstb.2007.2182 | pmid=17827110 | pages=761–776| pmc=2610108 }}{{cite web |last1=Legner |first1=Erich F.|title=Economic Gains & Analysis Of Successes In Biological Pest Control |url=http://www.faculty.ucr.edu/~legneref/biotact/bc-5.htm |publisher=University of California, Riverside |access-date=13 February 2018 |archive-url=https://web.archive.org/web/20080623113302/http://www.faculty.ucr.edu/~legneref/biotact/bc-5.htm |archive-date=23 June 2008 |url-status=live}}

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; chalcidoid wasps, which parasitise eggs and larvae of greenfly, whitefly, cabbage caterpillars, and scale insects; and tachinid flies, which parasitise a wide range of insects including caterpillars, adult and larval beetles, and true bugs.{{cite web |title=Parasitoid Wasps (Hymenoptera) |url=https://extension.umd.edu/hgic/insects/parasitoid-wasps-hymenoptera |publisher=University of Maryland |access-date=6 June 2016 |archive-date=27 August 2016 |archive-url=https://web.archive.org/web/20160827072031/https://extension.umd.edu/hgic/insects/parasitoid-wasps-hymenoptera |url-status=dead }} 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.{{cite journal |author=Smith, S. M. |date=1996 |title=Biological control with Trichogramma: advances, successes, and potential of their use |journal=Annual Review of Entomology |volume=41 |pages=375–406 |pmid=15012334 |doi=10.1146/annurev.en.41.010196.002111}}{{cite book |author1=Wajnberg, E. |author2=Hassan, S.A. |title=Biological Control with Egg Parasitoids |publisher=CABI Publishing |year=1994}}{{-}}

File:Garden Tiger Moth Maria Sibylla Merian.pngs (centre right) with their garden tiger moth host, by Maria 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.{{cite journal |last=Todd |first=Kim |title=Maria Sibylla Merian (1647-1717): an early investigator of parasitoids and phenotypic plasticity |journal=Terrestrial Arthropod Reviews |volume=4 |issue=2 |year=2011 |pages=131–144 |doi=10.1163/187498311X567794}}

Parasitoids influenced the religious thinking of Charles Darwin,{{efn|Darwin mentions "parasitic" wasps in On the Origin of Species, Chapter 7, page 218.On the Origin of Species, Chapter 7, [http://darwin-online.org.uk/content/frameset?pageseq=236&itemID=F373&viewtype=side page 218.]}} who wrote in an 1860 letter to the American naturalist Asa 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."{{cite web |url=http://www.darwinproject.ac.uk/entry-2814 | title=Letter 2814 — Darwin, C. R. to Gray, Asa, 22 May [1860] |access-date=5 April 2011}} The palaeontologist Donald Prothero notes that religiously minded people of the Victorian era, including Darwin, were horrified by this instance of evident cruelty in nature, particularly noticeable in the ichneumonid wasps.{{cite book |last=Prothero |first=Donald R. |title=Evolution: What the Fossils Say and Why It Matters |url=https://books.google.com/books?id=-LIvDwAAQBAJ&pg=PT85 |year=2017 |publisher=Columbia University Press |isbn=978-0-231-54316-3| pages=84–86}}

{{further|Parasites in fiction|Alien (creature in Alien franchise)}}

File:Paisley Abbey "Xenomorph" Gargoyle (10317339143) (cropped).jpg at Paisley Abbey, Scotland, resembling a Xenomorph{{cite web |last1=Budanovic |first1=Nikola |title=An explanation emerges for how the 12th century Paisley Abbey in Scotland could feature a gargoyle out of the film "Alien" |url=https://www.thevintagenews.com/2018/03/10/alien-gargoyle/ |publisher=The Vintage News |access-date=17 June 2018 |date=10 March 2018}} parasitoid from the film Alien{{cite web |title='Alien' gargoyle on ancient Paisley Abbey |url=https://www.bbc.co.uk/news/uk-scotland-glasgow-west-23810979 |publisher=British Broadcasting Corporation |access-date=17 June 2018 |date=23 August 2013}}]]

Parasitoids have inspired science fiction authors and screenwriters to create terrifying parasitic alien species that kill their human hosts.{{cite book |last1=Moisseeff |first1=Marika |author-link=Marika Moisseeff |title=Aliens as an Invasive Reproductive Power in Science Fiction |url=https://hal.archives-ouvertes.fr/hal-00935705 |website=HAL Archives-Ouvertes |date=23 January 2014|pages=239–257 |publisher=Polis, Sofia }} One of the best-known is the Xenomorph in Ridley Scott's 1979 film Alien, which runs rapidly through its lifecycle from violently entering a human host's mouth to bursting fatally from the host's chest.{{cite web |last1=Pappas |first1=Stephanie |title=5 Alien Parasites and Their Real-World Counterparts |url=https://www.livescience.com/20624-5-alien-parasites-real-inspiration.html |publisher=Live Science |date=29 May 2012}}{{cite web |last1=Williams |first1=Robyn |last2=Field |first2=Scott |title=Behaviour, Evolutionary Games and .... Aliens |url=http://www.abc.net.au/science/kelvin/files/s223.htm |publisher=Australian Broadcasting Corporation |access-date=30 November 2017 |date=27 September 1997}}{{cite web |title=The Making of Alien's Chestburster Scene |date=13 October 2009 |work=The Guardian |url=https://www.theguardian.com/film/2009/oct/13/making-of-alien-chestburster |access-date=29 May 2010| archive-url=https://web.archive.org/web/20100430221033/http://www.guardian.co.uk/film/2009/oct/13/making-of-alien-chestburster| archive-date=30 April 2010 | url-status=live}} The molecular biologist Alex Sercel, writing in Signal to Noise Magazine, compares "the biology of the [Alien] Xenomorphs to parasitoid wasps and nematomorph worms from Earth to illustrate how close to reality the biology of these aliens is and to discuss this exceptional instance of science inspiring artists".{{cite web |last1=Sercel |first1=Alex |title=Parasitism in the Alien Movies |url=http://www.signaltonoisemag.com/allarticles/2017/5/19/parasitism-in-the-alien-movies |publisher=Signal to Noise Magazine |date=19 May 2017}} 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 nematomorph Paragordius tricuspidatus which grows to fill its host's body cavity before bursting out and killing it. Alistair Dove, on the science website Deep Sea News, writes that there are multiple parallels with parasitoids, although in his view, there are more disturbing life cycles in real biology. Dove stated that the parallels include the placing of an embryo in the host; its growth in the host; the resulting death of the host; and alternating generations, as in the Digenea (trematodes).{{cite web |last1=Dove |first1=Alistair |title=This is clearly an important species we're dealing with |url=http://www.deepseanews.com/2011/05/this-is-clearly-an-important-species-were-dealing-with/ |publisher=Deep Sea News |date=9 May 2011}} The social anthropologist Marika Moisseeff argues that "The parasitical and swarming aspects of insect reproduction make these animals favoured villains in Hollywood science 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." The Encyclopedia of Science Fiction lists many instances of "parasitism", often causing the host's death.{{cite encyclopedia|title=Parasitism and Symbiosis |url=http://www.sf-encyclopedia.com/entry/parasitism_and_symbiosis |encyclopedia=The Encyclopedia of Science Fiction |date=10 January 2016}}

{{notelist}}

{{reflist|30em}}

{{Biological interaction-footer}}

{{Use dmy dates|date=August 2018}}

Category:Parasitology

Category:Parasitism

Category:Biological pest control