Parasitoid

SEM image of endoparasitoid ciliates of the genus Collinia, which can cause mass mortality in affected krill populations

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 that is in essence parasitic; unlike a true parasite, however, it ultimately sterilises or kills, and sometimes consumes, the host. Thus parasitoids are similar to typical parasites except in the more dire prognosis for the host.

Definitions and distinctions

The term parasitoid was coined in 1913 by the German writer O. M. Reuter^[1] (and adopted in English by his reviewer, William Morton Wheeler) to describe the strategy in which, during its development, the parasite lives in or on the body of a single host individual, eventually killing that host, the adult parasitoid being free-living. Since that time however, the concept has been variously generalised and widely applied.

In practice it is not always necessary to distinguish parasitoidy from parasitism, nor is it always even possible to do so cleanly. However, when it is appropriate to do so, a typically parasitic relationship is one in which parasite and host interact without lethal harm to the host, and without dramatically reducing the host's reproductive success. In most such relationships, the parasite arrogates enough nutrients or other resources to thrive without preventing the host from reproducing. In contrast, in a parasitoidal relationship the exploiting organism kills or sterilises the host, typically before it can produce offspring. A non-lethal parasite sometimes is termed a biotroph. In contrast, when a parasitoidal relationship is regarded as a form of parasitism, the parasitoid may be called a necrotroph.

When an organism sterilises its host without directly killing it, then whether to term it a parasitoid or a parasite, is a matter of context and preference. Often for a parasite to prevent reproduction of the host is incidental, but various forms of systematic parasitic castration occur among parasitoids, and many such biological strategies are highly sophisticated. Crustacean parasites or parasitoids include several impressive examples.

Protelean is a term that various authors use to denote organisms that live as parasites only during the early, growing, phases of their lives; typically they then begin by behaving as internal parasites; also typically they end that phase of their lives parasitoidally by killing or consuming the host. Finally they emerge as free-living adults, with or without an intervening phase of diapause or metamorphosis.

Protelean organisms are widely regarded as a special class of parasites, or more usually parasitoids. The most typical examples of proteleans are the parasitoidal Hymenoptera, Diptera, Strepsiptera, and some other insects. Usually such insects are holometabolous. It is reasonable to regard holometaboly as preadaptation for the protelean life history because it implies that their larval stage of life differs drastically from the adult stage, both functionally and morphologically.

Idiobiont parasitoids are those that prevent further development of the host after initial parasitization; typically they attack a host life stage that is immobile (e.g., an egg or pupa), and almost without exception idiobiont parasitoids live outside the host. Koinobiont parasitoids allow the host to continue its development and often do not kill or consume the host until the host either is about to pupate or become an adult; this therefore typically involves living within an active, mobile host. In turn, koinobionts can be subdivided further into endoparasitoids, which develop inside body of the host, and ectoparasitoids, which develop outside the host body, though the parasitoids frequently are attached or embedded in the host's tissues.

It is fairly common for a parasitoid itself to serve as the host for another parasitoid's offspring. The latter is commonly termed a hyperparasite, but in most cases this term is slightly misleading, as both the host and the primary parasitoid are killed. A better term might be secondary parasitoid, or hyperparasitoid.

Most known specialist hyperparasite and hyperparasitoid species are in the insect order Hymenoptera, but a fair amount of incidental hyperparasitoidy results when a single host or a single food stash happens to house multiple guests and rations run short. Some members of the flesh fly family, Sarcophagidae, subfamily Miltogramminae, for example members of the genus Craticulina, are kleptoparasites of wasps in the subfamilies Bembicinae and Philanthinae (both currently believed to be in the family Crabronidae). Both those subfamilies tend to build nests by digging tunnels in sand, which they then stock piecemeal with prey such as flies or bees, depending on the species. Kleptoparasitic flies such as Craticulina are much smaller than the host wasp and lay their eggs on the prey as the wasp returns to the nest on a victualing flight. The fly larvae are small, though faster-growing than the wasp larva, and if there is only one, the wasp is likely to complete its metamorphosis successfully, but when there are several it might suffer from malnutrition or even get eaten itself, which amounts to incidental kleptoparasitoidy.

In contrast though, as described in the following section, some insects, such as some members of the Trigonalidae, not only are specialist hyperparasitoids, but have advanced behavioural adaptations to support their speciality.

Note once again that there is no clear separation between the concepts of parasitism and parasitoidy. Many species of true parasites can cause the death of their host if for example they are present in overwhelming numbers or the host is in poor condition, or other compromising circumstances develop, such as secondary infections. For example, blood-sucking mites sometimes overwhelm nestlings of birds such as swallows to the point that the young birds cannot fledge successfully,.^[2]

Infestations of other mites cause various kinds of mange in mammals. Mange mites are generally in the families Demodicidae that cause Demodicosis or demodectic mange, Sarcoptidae that cause scabies or sarcoptic mange, and Psoroptidae that cause scab in sheep and rabbits. Severe mange can debilitate animals to the point that they cannot feed themselves adequately, so that in unfavourable circumstances they may die.

Again, various species of paralytic ticks sometimes kill dogs if the owners are insufficiently alert, and soft ticks can fatally poison a host such as a horse that might rest in an infested shady spot because it does not know the local hazards.^[3] Conversely, some parasitoids do somewhat shorten the lives of their hosts or constrain their reproduction, but without necessarily killing them as a part of their interaction. Almost any microbial disease could be defined as a parasitic condition, and some could be argued to amount to clear examples of parasitoidy. One converse argument is that when the death of the host is neither a logical nor necessarily even a desirable consequence from the point of view of the parasite, the relationship should be regarded as parasitic rather than parasitoidal. This certainly would apply to examples such as mange, and diseases in which the living victim acts as a natural reservoir or even a vector.

In their extreme forms the categories of parasitism and parasitoidy patently are distinct; one is in no doubt whether 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 plainly are simply ectoparasites. However, there is a continuum of intermediate and contingent conditions that bridge those categories in practically every respect. This should not be taken too seriously as a material problem in terminology; the terms are useful in particular contexts and should not be abused by inappropriate application in contexts in which they create confusion rather than clarity. Many examples of species that are technically parasitoidal, at least facultatively, are not generally referred to as parasitoidal. Many microbial diseases and the aforementioned soft ticks constitute instructive examples.

Nor do those complete the list of examples that constitute the requirement for fuzzy distinctions in such matters; at the opposite extreme from parasitism, parasitoidy in turn grades into predation. Differences between various kinds of hunting wasps provide convenient illustrations. Predatory social wasps hunt flies, caterpillars and the like, grab them, butcher them, carry them home and feed them to their young. That is patent predation. Some solitary wasps, such as bee pirates, sting prey, sometimes fatally, before saving it, usually entire, in a nest or burrow for the young to feed on. That too is predation, fairly clearly.

In contrast, the best-known protelean solitary hunting wasps sting prey to paralyse it before storing it for the young in the nest.^[4][5] The larvae then proceed to eat the stored prey alive, sometimes according to very sophisticated schedules that delay killing the victim sooner than necessary, thereby avoiding having their rations rot before they could be consumed.^[6][7][8] Some authorities regard such larval behaviour as having a strong element of parasitoidy. That view is based largely on the view that the young larvae begin with small exactions like any parasite, then proceed to the point where they eat at such a rate that they might as well be predators.

Other wasps paralyse prey in the plant or other environment in which it feeds, before laying eggs nearby. The emerging young attack and feed on the paralysed prey organism in its own home.^[9] Some solitary parasitoids among insects lay their eggs on or in their live prey and any of a wide range of consumption schedules might follow. Some parasitoids even lay their eggs where the larvae must locate the prey for themselves when they hatch from the eggs.^[10] Examples include flies in the families Tachinidae and Bombyliidae. The physiological and strategic sophistication of such relationships, whether parasitoidal or parasitic, often are impressive.

Patently there is no point to trying to draw arbitrary lines of distinction between such vague, and often variable, life histories. In each ecological or ethological study the terms applied should reflect the facts in the contexts relevant to the matter in question. Such studies need not in all cases use the identical terminology, and there is no reason they should. All that is necessary is that the terminology in each study should be clear, useful and relevant.

Types of parasitoids

The parasitoidal type of relationship seems to occur largely in organisms that have fast reproduction rates, such as insects or (perhaps more rarely) mites or nematodes. Workers in this field have pointed out that parasitoids often are closely coevolved with their hosts, which is inarguably true. To maintain a sound perspective of the matter though, one must remember that coevolution might reasonably be expected to develop to even higher degrees of sophistication in the more intimate classes of parasitic relationships. In fact advanced degrees of coevolution occur in the arms races of predator-prey relationships as well.

In using the term parasitoid it is common to think in terms of parasitoidal insects such as Tachinidae and Pompilidae. Some writers recognise or discuss no other classes of parasitoidy. More realistically however, the life histories of several other groups of organisms are equally parasitoidal. In general there is no logical basis for excluding wider use of the term. For example, among the so-called worms, many Nematoda are important parasitoids of insects, snails and similar commercially important pest organisms. Under favourable circumstances they commonly multiply in the host until the carcase is a shell overflowing with a pullulating mass of worms.

Other organisms that might merit the term include certain Pteromalid gall wasps that abort host plant inflorescences,^[11] seed weevils, certain plants largely regarded as parasitic, and certain bacteria and viruses (e.g., bacteriophages), in relationships where the beneficiaries obligately destroy their hosts.

Not all such organisms regularly behave quite so parasitoidally of course; for example some bacteriophages establish complex life cycles in which phage particles do get released catastrophically, but only at intervals of many generations of the host, whereas other bacterial viruses emerge intermittently but fairly harmlessly in small numbers at a time.^[12]

The clearest cases of fully functional parasitoidy are the likes of many parasitoidal wasps and flies that consume their hosts as completely as any spider or hawk that summarily eats its prey. However, there also are many species of parasitoid that frequently or even routinely kill their "host" or "prey" without consuming much of it. This apparently wasteful strategy sometimes might have the effect of reducing the risk that the prey could escape or offer resistance. In other cases the residue of the victim simply might be difficult to eat or not very nutritious. For example various Phorid flies such as Apocephalus species, are parasitoids of particular species of ants. Various species attack ant genera such as "big-headed ants", "Fire ants" or Solenopsis, Paraponera, and leaf-cutter ants. However, the larvae of most such Phoridae eat mainly the contents of the ants' "head capsules" abandoning the rest of the carcases when pupating. In laying her eggs, the parent fly selects the largest ant workers, which have just the size of head to produce an adequate adult phorid. Presumably the large head-capsule contains the most concentrated nutritious muscle and brain tissue.^[13] One also could think of the Rabies virus in similar terms, or the aforementioned soft ticks. Both commonly or invariably cause the death of the host, after consuming at most a trivial fraction of the host's resources.

Influence on host behaviour

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 own life. A spectular example is the endoparasitoid Dicrocoelium dendriticum, 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 dawdle high on grass stalks, positions that are risky, but favour the emergence of the Strepsipterans.^[13] Other species of endoparasitoids cause infected woodlice and land Amphipoda such as Talitroidesto run about in the open by day, where predators such as birds can catch them and continue the cycle.

Returning to the case of the rabies virus and the disease, one could rationalise the death of the host similarly. The virus affects the host's central nervous system with eventually fatal effects. That could be seen as a consequence of the strategy for dissemination of the virus by affecting the host behaviour.^[14] Similar principles might apply to, for example, Vibrio cholerae, the cholera bacterium and other, often fatal, enteric pathogens that induce diarrhoea and spread by contagion.

For the soft ticks the benefit of the paralysis they inflict might be seen as influencing behaviour in that it prevents the host from wandering away while they feed, which they do very quickly and in large numbers, some species emerging from their hiding places at night. Other species hide in sandy patches in the shade of trees in semi-desert such as the Kalahari, and emerge to feed as soon as any large animal settles down in the shade during the heat of the day.^[3]

In parasitic birds such as cuckoos, the young often are adapted to act as "super solicitors", with loud, persistent voices and with large, vividly coloured gapes and behaviour that stimulate the feeding instincts of the foster parents to the utmost. Consequently the legitimate chicks, even if they are not evicted, often starve because they are less well-equipped for soliciting for food.

Parasitoidal microbial diseases

As mentioned, some microbial parasitoids waste most of the host's resources when it dies, but there are other parasitoidal strategies among microbes as well. One more conceptually economical form of parasitoidy is exemplified by microbial pathogens of various invertebrates such as many insects. The most notorious might well be Microsporidiosis in the form of nosema in silkworms. This infection is highly virulent^[15] 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, bacterial and other, continue to propagate inside a host cell until it physically ruptures. In doing so they too consume effectively the whole of the host's resources.

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 carcase and release spores for as long as any resources remain. In this such microbes resemble the aforementioned propagation of some Nematoda in snails and insects.

Parasitoidal plants

There are parasitoidal plants as well. Various species of dodder indiscriminately parasitise wide ranges of host plants, and debilitate or kill the branches that they infect, and commonly the whole host plant as well.

Mistletoes in families such as Santalaceae and Loranthaceae commonly accumulate on host trees till 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.^[16]

A related example is where the parasitoid plant is not strictly a parasite in the normal sense, but none the less exploits the host's resources of space, support and light. The best-known are the so-called "strangler figs". Some of them will grow on and round the trunk of the host tree and squeeze it or starve it of light until, after perhaps decades, it dies. The strangler eventually replaces the host utterly as the original trunk rots from within the stems of the strangler, leaving a hollow framework.

Parasitoidal crustaceans

The subphylum Crustacea includes a surprising range of parasitoidal species and strategies. As with many other parasitoids, the killing of the host often is incidental. For example, in the family Ergasilidae, the "gill lice", most adult females live as parasites in the gills of fish. The harm they do the host is incidental to the parasitism, but it often is fatal or at least debilitates the fish so badly as to prevent breeding.

A particularly startling genus of Cirripedia, or barnacles is Sacculina. It literally injects itself into a crab of a suitable species and by complex processes converts itself into an egg-laying bag. In the process it disrupts the reproductive system of the host, an act of parasitic castration that qualifies it for classification as a parasitoid rather than just a parasite.

Those examples are just a few of many among the Crustacea.^[17]

Parasitoidal insects

Braconid Wasp Cocoons On Giant Leopard Larva.

About 10% of described insect species are entomophagous parasitoids.^[18] There are four insect orders that are particularly renowned for this type of life history. By far the majority are in the order Hymenoptera.

The largest and best-known group comprises the so-called "Parasitica" within the Hymenopteran suborder Apocrita: the largest subgroups of these are the chalcidoid wasps (superfamily Chalcidoidea) and the ichneumon wasps (superfamily Ichneumonoidea), followed by the Proctotrupoidea and Platygastroidea. Outside of the Parasitica, many other Hymenopteran lineages that include parasitoids, such as most of the Chrysidoidea and Vespoidea, and the rare Symphytan family Orussidae.

The flies (order Diptera) include several families of parasitoids, the largest of which is the family Tachinidae, and also smaller families such as Pipunculidae, Conopidae, and others. Other families of flies that are not primarily parasitoids or parasites, or at least not primarily protelean, do nonetheless include protelean species. For example Phoridae have already been mentioned as parasitoidal on ants, and at least some flesh fly species, such as Emblemasoma auditrix, are parasitoidal on cicadas, and have raised great interest because they locate their hosts by sound.^[19] The kleptoparasitic flesh fly genus Craticulina has already been mentioned and logically qualifies as a protelean fly genus.

Two other orders with parasitoidal members are the "twisted-wing parasites" (order Strepsiptera), which is a small group consisting entirely of parasitoids, and the beetles (order Coleoptera), which includes at least two families, Ripiphoridae and Rhipiceridae, that are largely parasitoids, and rove beetles (family Staphylinidae) of the genus Aleochara. Occasional members of other orders can be parasitoids; one of the more remarkable is the moth family Epipyropidae, which are ectoparasitoids of planthoppers and Cicadas. The genus Cyclotorna has even more elaborate habits, beginning its growth period parasitising plant bugs, and concluding by feeding on ant larvae in their colonies.

Koinobiont parasitoid on moth larva.

Hymenopteran parasitoids often have unique 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.^[20]

Parasitoidal and Parasitic Vertebrates

Perhaps because they are less specialised and their relationships with their hosts are less intimate than is the case with many invertebrates, it often is more difficult to distinguish parasitism from parasitoidy in vertebrates. In fact many of their relationships of such types do not immediately suggest parasitism to most people at all. However, the very concept is so open to interpretation that it emerges frequently in vertebrate biology.

Kleptoparasitism for example is ubiquitous, and is a major constraint on reproduction or even survival among vertebrate predators, especially in times of famine. Male lions in a pride for example, largely leave hunting for non-threatening prey to females. However, prides that specialise in very large prey such as giraffes, elephants,^[21][1] or buffalo, may behave differently.

Other predators such as cheetah, leopard, and even lions sometimes may be chased from their kills by hyaenas. Hyaena may sometimes follow such predators so routinely in the hope of confiscating their kills, that the hunters spend more effort on avoiding hyaena than on hunting.

Ethologists could multiply examples of kleptoparasitism many-fold; it may be intraspecific or interspecific; it ranges from the smallest foragers and predators to the largest, and may combine with predation, where the robber is happy to eat both hunter and prey. Curiously though, interspecific robbers often show at least some constraint as though they were robbing conspecifics, and do not necessarily attack the host as directly as they would have done had there not been a "robbery" situation. Interpretation and speculation about the nature of such behaviour is beyond the scope of this article however.

It is not easy to classify such relationships, because many of them involve degrees of payment in terms of protection and other benefits; for example the male lions who preempt the females' kills do at least offer protection from hyaenas and rival males.

Kleptoparasitism occurs in many other forms among vertebrates (see here for example), but for it to lead to the death of the host is not so common, and this would seem to disqualify it from the category of parasitoidy. Still, when the hosts are hard pressed in hard circumstances, the resulting injury and famine could cause reduced reproduction and even death.

Lampreys present both parasitic and parasitoidal examples. Most species are not parasitic, but among the North American species for example, there are several species ectoparasitic on freshwater fishes. They rasp away the skin of the host and suck the blood, but most do only superficial damage. In contrast the most notorious species is the sea lamprey, Petromyzon marinus. Its rasping wounds can extend deep into the host's flesh, and the muscle damage and loss of blood commonly weaken the host severely, affecting its reproduction unfavourably. Often the harm is severe enough to kill the host, which is about as clear an example of parasitoidy as one could ask.

Hagfish, are distant relatives of lampreys. They are largely carrion feeders and predators of large worms and similar small creatures, but various species also attack weakened fishes much as some lampreys do, and accordingly rank as opportunistic parasitoids under at least some conditions.

The sabre-toothed blenny presents a curiously difficult example of parasitism to classify. It parasitises the relationship between some cleaner fish and their client fishes, more than it parasitises either party to the relationship; 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. In its violence and the pernicious effect on a valuable relationship, it suggests parasitoidy as well as parasitism.

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, and such bits of skin and scale formed major components of the stomach contents. At least some of the species also have adaptations in their behavior to enable them to approach potential hosts^[22] They also have an adaptation of the jaw that enables them to lash out sideways in passing a victim; the jaw is asymmetrical,^[23] 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.^[24]

Such a lifestyle is reminiscent of sharks of the genus Isistius, which is known as the Cookiecutter shark because of the circular wounds it leaves in the skins of whales and large fish that it has bitten in passing.^[25] Isistius species have been referred to as partly ectoparasitic,^[26] but they sometimes overwhelm their hosts and kill them, which by definition amounts to parasitoidy.

Candiru and related fishes in the Family Trichomycteridae, subfamilies Vandelliinae and Stegophilinae, present unusual examples of vertebrate parasitism, and occasionally parasitoidy. Most popular accounts are obsessed with the idea of candiru entering the human urethra and other orifices, but they are very varied in their habits. Some burrow partway into the skin of larger fish, apparently largely for purposes of protection and transport rather than food. Several at least are haematophagous, commonly entering the gill cavities of larger fishes and feeding on blood drawn from the gill filaments. At least when large fishes are tethered by fishermen where large numbers of the parasites occur, the hosts may die. Possibly this effect is analogous to the effect of soft ticks on hosts that do not avoid the sand patches where they assemble.

Among birds the best-known forms of parasitism are brood parasitism by various species of cuckoos, honey-guides, cowbirds, and several more. They qualify as parasitoids because many of them will cause the starvation of the host's chicks by competing with them for food, and many others either will remove host eggs when laying eggs in host nests, (sometimes eating the eggs removed), or the chick will eject or kill the eggs or chicks of the host when they hatch. Some hatchlings actually have hooked beaks adapted to attacking the host chicks and eggs, hooks that vanish before fledging.

See also

• Parasitoid wasp

References

1. ^ Reuter, Reuter, O.M. (1913). Lebensgewohnheiten und Instinkte der Insekten (Berlin: Friendlander).
2. ^ Møller, A. P. (1990). Effects of parasitism by a haematophagous mite on reproduction in the barn swallow. Ecology, 71(6), 2345-2357. Retrieved from http://www.jstor.org/stable/pdfplus/1938645.pdf?acceptTC=true
3. ^ ^{a b} Holm, Erik, Dippenaar-Schoeman, Ansie; Goggo Guide; LAPA publishers (URL: WWW.LAPA.co.za). 2010
4. ^ Elizabeth G. Peckham; Peckham, George A. (2010). On the Instincts and Habits of the Solitary Wasps, Issue 2. Nabu Press. ISBN 1-143-02120-7. 
5. ^ Burroughs, John; Peckham, George A.; Elizabeth G. Peckham (2007). Wasps: Social And Solitary (1905). Kessinger Publishing, LLC. ISBN 0-548-63589-7. 
6. ^ Fabre, Jean-Henri; Translated by Alexander Teixeira de Mattos; The hunting wasps.; Pub: Hodder and Stoughton, London 1916
7. ^ Fabre, Jean-Henri; Translated by Alexander Teixeira de Mattos; More hunting wasps; Pub: Dodd, Mead, New York, 1921
8. ^ Fabre, Jean-Henri; Translated by Alexander Teixeira de Mattos; The mason-wasps; Pub: Dodd, Mead, New York,1919
9. ^ Li, Jian & Seal, Dakshina R; "Parasitoids of Dipteran leafminers, Diglyphus spp. (Insecta: Hymenoptera: Eulophidae)"; EENY-484 (IN877), Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. December 2010.
10. ^ Thomas Bugnyar; Emilie A. Weber; Lara H. Krause; Olaf Boebel (2009). Animal Behavior: New Research. Commack, N.Y: Nova Science Publishers. ISBN 1-60456-782-1. 
11. ^ Prinsloo G. L., Neser O. C.; Revision of the pteromalid wasp genus Trichilogaster Mayr (Hymenoptera: Chalcidoidea): gall-inducers on Australian acacias.; African Entomology Mar 2007 : Vol. 15, Issue 1, pg(s) 161-184 doi: 10.4001/1021-3589-15.1.161
12. ^ Levy, Jay A.; Fraenkel-Conrat, Heinz; Kimball, Paul C. (1988). Virology. London: Prentice-Hall International. ISBN 0-13-942822-4. 
13. ^ ^{a b} Wojcik, Daniel P.; Behavioral Interactions between Ants and Their Parasites.; The Florida Entomologist Vol. 72, No. 1 (Mar., 1989), pp. 43-51
14. ^ Taylor PJ (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. PMID 7777324. 
15. ^ Shabir Ahmad Bhat, Ifat Bashir, Afifa S. Kamili. Microsporidiosis of silkworm, Bombyx mori L. (Lepidoptera- bombycidae): A review. African Journal of Agricultural Research Vol. 4 (13), pp. 1519-1523, December, 2009 Special Review.
16. ^ Visser, Johann (1981). South African parasitic flowering plants. Cape Town: Juta. ISBN 0-7021-1228-3. 
17. ^ Janovy, John; Schmidt, Gerald D.; Roberts, Larry S. (1996). Gerald D. Schmidt & Larry S. Roberts' Foundations of parasitology. Dubuque, Iowa: Wm. C. Brown. ISBN 0-697-26071-2. 
18. ^ Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey, ISBN 0691033250
19. ^ Köhler U, Lakes-Harlan R.; Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). J Comp Physiol A. 2001 Oct;187(8):581-7.
20. ^ Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals, Greenwood Press.
21. ^ Whitworth Damian; “The killing fields” The Times October 4, 2006
22. ^ Rieko Takahashi, Katsutoshi Watanabe, Mutsumi Nishida, and Michio Hori. ; Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach.  ; BMC Evol Biol. 2007; 7: 195. Published online 2007 October 18. doi: 10.1186/1471-2148-7-195. PMCID: PMC2212659
23. ^ Evolution of a unique predatory feeding apparatus: functional anatomy, development and a genetic locus for jaw laterality in Lake Tanganyika scale-eating cichlids. BMC Biol. 2010 Jan 26 ;8:8.
24. ^ Hori, M. 1993. Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216-219.
25. ^ LastName, FirstName (2000). Cetacean societies : field studies of dolphins and whales. Chicago: University of Chicago Press. ISBN 0226503410. 
26. ^ Papastamatiou Yannis P., Wetherbee, Brad M., O'Sullivan, John, Goodmanlowe Gwen D. Lowe, Christopher G.; Foraging ecology of Cookiecutter Sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds.; Environmental Biology of Fishes, Volume 88, Number 4, 361-368, DOI: 10.1007/s10641-010-9649-2

External links

• On the UF / IFAS Featured Creatures website:
  • Ageniaspis citricola, a citrus leafminer parasitoid (Insecta: Hymenoptera: Encyrtidae)
  • Amitus hesperidum, a citrus blackfly parasitoid (Insecta: Hymenoptera: Platygastridae)
  • Cirrospilus ingenuus, a citrus leafminer parasitoid (Insecta: Hymenoptera: Eulophidae)
  • Encarsia lahorensis, a citrus whitefly parasitoid (Insecta: Hymenoptera: Aphelinidae)
  • Encarsia opulenta, a citrus blackfly parasitoid (Insecta: Hymenoptera: Aphelinidae)
  • Lipolexis scutellaris, brown citrus aphid parasitoid (Insecta: Hymenoptera: Aphidiidae)
  • Semielacher petiolatus, a citrus leafminer parasitoid (Insecta: Hymenoptera: Eulophidae)
  • Steinernema scapterisci, mole cricket nematode (Nematoda: Rhabditida: Steinernematidae)
• Parasitic and Parasitoid Alien Species in Science Fiction Movies