Behavior-altering parasite

Behavior-altering parasites are parasites with two or more hosts, capable of causing changes in the behavior of one of their hosts to enhance their transmission, sometimes directly affecting the hosts' decision-making and behavior control mechanisms. They do this by making the intermediate host, where they may reproduce asexually, more likely to be eaten by a predator at a higher trophic level[1][2] which becomes the definitive host where the parasite reproduces sexually; the mechanism is therefore sometimes called parasite increased trophic facilitation[3] or parasite increased trophic transmission.[4] Examples can be found in bacteria, protozoa, viruses, and animals. Parasites may also alter the host behaviour to increase protection of the parasites or their offspring; the term bodyguard manipulation is used for such mechanisms.[5]

Among the behavioral changes caused by parasites is carelessness, making their hosts easier prey.[6][4] The protozoan Toxoplasma gondii, for example, infects small rodents and causes them to become careless and may even cause them to become attracted to the smell of feline urine, both of which increase their risk of predation and the parasite's chance of infecting a cat, its definitive host.

Parasites may alter the host's behavior by infecting the host's central nervous system, or by altering its neurochemical communication (studied in neuroparasitology).[7]

Examples

Parasite manipulations can be either direct or indirect. Indirect manipulation is the most frequent method used by behavior-altering parasites,[8] while the direct approach is far less common. Direct manipulation is when the parasite itself affects the host and induces a behavioral response, for example by creating neuroactive compounds that stimulate a response in the host's central nervous system (CNS), a method mostly practiced by parasites that reside within the CNS.[9] Affecting the host's neural system is complicated and manipulation includes initiating immune cascades in the host.[10] However, determination of the causative factor is difficult, especially whether the behavioral change is the result of direct manipulation from the parasite, or an indirect response of the host's immune system.[9] A direct approach to behavioral manipulation is often very costly for the parasite,[9] which results in a trade-off between the benefits of the manipulation (e.g., fitness increase) and the energy it costs. The more common approach for parasites is to indirectly induce behavioral responses by interacting with the host's immune system[8] to create the necessary neuroactive compounds to induce a desired behavioral response.[9] Parasites can also indirectly affect the behavior of their hosts by disturbing their metabolism, development, or immunity.[9] Parasitic castrators drastically modify their hosts' metabolism and reproduction, sometimes by secreting castrating hormones, changing their behavior and physiology to benefit the parasite.[11]

Parasites may alter hosts' behaviors in ways that increase their likelihood of transmission (e.g. by the host being ingested by a predator); result in the parasite's release at appropriate sites (e.g. by changes in the host's preferences for habitats);[12] increase parasite survival or increase the host's likelihood of being infected with more parasites.

Viruses

Baculoviridae

Viruses from the family Baculoviridae induce in their hosts changes to both feeding behavior and environment selection. They infect moth and butterfly caterpillars, who some time following infection begin to eat incessantly, providing nutrients for the virus's replication. When the virions (virus "units") are ready to leave the host, the caterpillar climbs higher and higher, until its cells are made to secrete enzymes that "dissolve the animal into goo", raining down clumps of tissue and viral material for ingestion by future hosts.[13]

Lyssavirus

Rabies (a disease caused by viruses of the Lyssavirus genus) causes the host to become aggressive and prone to biting others. This, along with increased salivation (virus particles are released into and spread via saliva), increases the chances of it spreading to new hosts. At the same time, the disease causes hydrophobia (fear of water),[14] preventing the host from drinking so that the virus-laden saliva is not washed down into the stomach and made unavailable for infection by biting.

Protozoal parasites

Plasmodium falciparum

The malaria parasite Plasmodium falciparum, carried by the Anopheles gambiae mosquito, changes its host's attraction to sources of nectar in order to increase its sugar intake and enhance the parasite's chance of survival.[15] It also decreases the host's attraction to human blood while gestating,[13] only to increase it when it is ready to be transmitted to a human host.[13][16]

Toxoplasma gondii

The protozoan Toxoplasma gondii infects animals from the family Felidae (its definitive host), and its oocysts are shed with the host's feces. When a rodent consumes the fecal matter it gets infected with the parasite (becoming its intermediate host). The rodent subsequently becomes more extroverted and less fearful of cats, increasing its chance of predation and the parasite's chance of completing its lifecycle.[17] There is some evidence that T. gondii, when infecting humans, alters their behavior in similar ways to rodents; it has also been linked to cases of schizophrenia.[18]

Parasitic helminths

Multiple parasites increase their host's risk of predation to facilitate their transition from their intermediate host to their definitive host, including: Euhaplorchis californiensis,[19] Dicrocoelium dendriticum,[19] Diplostomum pseudospathaceum, Euhaplorchis californiensis,[19] and Myrmeconema neotropicum.[20]

Dicrocoelium dendriticum

The lancet liver fluke (Dicrocoelium dendriticum) is a parasitic trematode with a complex life cycle. In its adult state it occurs in the liver of its definitive host (ruminants), where it reproduces. The parasite eggs are passed with the feces of the host, which then are eaten by a terrestrial snail (first intermediate host). The fluke matures into a juvenile stage in the snail, which in an attempt to protect itself excretes the parasites in "slime-balls". The "slime-balls" are then consumed by ants (second intermediate hosts). The fluke manipulates the ant to move up to the top of grass, where they have a higher chance of being eaten by grazing ruminants.[19]

Snail with its left eye stalk parasitized by Leucochloridium paradoxum

Leucochloridium paradoxum

The trematode Leucochloridium paradoxum matures inside snails of the genus Succinea. When ready to switch to its definitive host, a bird, the parasite travels to the eye stalks of its host and begins to pulsate, attracting birds with its striking resemblance to an insect larva.[21] It also influences the normally nocturnal snail to climb out into the open during the day for an increased chance of being consumed by a bird.[22]

A long horsehair worm shortly after emerging from its cricket host, now drowned

Microphallus

The parasitic trematodes of the genus Microphallus parasitise the snail Potamopyrgus antipodarum as an intermediate host. The parasites manipulate the snail's foraging behavior to increase the chance of it being preyed upon by the parasite's definitive hosts (waterfowl). The infected snail forages on the upper side of rocks during the period of the day when waterfowl feed most intensely. During the rest of the day, the snail forages at the bottom of rocks to reduce the risk of being eaten by fish (non-host predators).[23]

Myrmeconema neotropicum

The parasitic nematode Myrmeconema neotropicum infects the intermediate ant host Cephalotes atratus. The nematode then induces a morphological change in the ant, which turns the gaster color from black to red, making it resemble fruit. This color transition makes the ant susceptible to predation by frugivorous birds, which act as the parasite's definitive hosts. The parasitic eggs are deposited in the bird's feces and are eaten by ants, which complete the cycle.[20]

Nematomorpha

Crickets infected by horsehair worms (Nematomorpha) exhibit light-seeking behavior and increased walking speed, leading them to open spaces and ponds (the surface of which reflects moonlight); the crickets will eventually find and enter a body of water, where the worm will wiggle out of the cricket's abdomen and swim away. While crickets often drown in the process, those who survive exhibit a partial recovery and return to normal activities in as little as 20 hours.[24]

Schistocephalus solidus

Schistocephalus solidus is a parasitic tapeworm with three different hosts, two intermediate and one definitive. In its adult stage the tapeworm resides in the intestine of piscivorous birds, where they reproduce and release eggs through the bird's feces. Free-swimming larvae hatch from the eggs, which are in turn ingested by copepods (the first intermediate host). The parasite grows and develops in the crustacean into a stage that can infect the second intermediate host, the three-spined stickleback (Gasterosteus aculeatus).[25] The parasite's definitive host, a bird, then consumes the infected three-spined stickleback and the cycle is complete. It has been observed that S. solidus alters the behavior of the fish in a manner that impedes its escape response when faced with a predatorial bird.[26] This parasite-induced behavioral manipulation effectively increases the chance of it being consumed by its definitive bird host. It has also been observed that the parasite does not induce this behavior until it has reached a developed stage that can survive in the host bird[26] and therefore effectively reduce its own mortality rate, due to premature transmission.

Parasitic insects

Ampulex compressa

Emerald cockroach wasp "walking" a paralyzed cockroach to its burrow

The emerald cockroach wasp (Ampulex compressa) parasitises its host, the American cockroach (Periplaneta americana) as a food source and for its growing larvae. The wasp stings the cockroach twice: First in the thoracic ganglion, paralyzing its front legs and enabling the wasp to deliver a second, more difficult sting, directly into the cockroach's brain;[27] this second sting makes the cockroach groom itself excessively before sinking into a state of hypokinesia – "a... lethargy characterized by lack of spontaneous movement or response to external stimuli".[28] The wasp then pulls the idle cockroach into its burrow, where it deposits an egg onto its abdomen and buries it for the growing larva to feed on. Keeping the cockroach in a hypokinetic state at this stage, rather than simply killing it, allows it to stay "fresh" for longer for the larva to feed on.[29] The adult wasp emerges after 6 weeks, leaving behind nothing but an empty cockroach "shell".[28]

Dinocampus coccinellae

Ladybug guarding a Dinocampus coccinellae cocoon. The ladybug will remain stationary until the adult wasp emerges from its cocoon, and die some time afterwards

The wasp Dinocampus coccinellae is both an endoparasite and ectoparasite of ladybugs. The wasp injects an egg into the beetle's abdomen, where the larva feeds on its haemolymph. When grown and ready to pupate the larva exits its host, which remains immobile, and weaves a cocoon on its underside, where it pupates. Were a predator to approach, the beetle would twitch its limbs, scaring the predator off. This use of the host as a protection has been termed as bodyguard manipulation.[30][31] Similarly, several parasitic wasps induce their spider hosts to build stronger webs to protect the growing parasites.[32]

Hymenoepimecis argyraphaga

The parasitic wasp Hymenoepimecis argyraphaga grows its larvae on spiders of the species Leucauge argyra. Shortly before killing its host the larva injects it with a chemical that changes its weaving behavior,[33] causing it to weave a strong, cocoon-like structure. The larva then kills the spider and enters the cocoon to pupate.[34]

Ophiocordyceps unilateralis

A similar, but much more intricate behavior is exhibited by ants infected with the fungus Ophiocordyceps unilateralis: irregularly-timed body convulsions cause the ant to drop to the forest floor,[35] from which it climbs a plant up to a certain height[36] before locking its jaws into the vein of one of its leaves answering certain criteria of direction, temperature and humidity. After several days the fruiting body of the fungus grows from the ant's head and ruptures, releasing the fungus's spores.[37]

Phoridae

A larva of Reclinervellus nielseni parasitizing Cyclosa argenteoalba in Japan

Several species of fly in the family Phoridae parasitise fire ants. The fly injects an egg into the ant's thorax; upon hatching, the larva migrates into the ant's head, where it feeds on the ant's haemolymph, muscle and nerve tissue. During this period some larvae direct the ant up to 50 meters away from the nest and towards a moist, leafy place where they can hatch safely.[38][39] Eventually the larva completely devours the ant's brain, which often falls off (hence the species nickname: "decapitating fly").[40] The larva then pupates in the empty head capsule, emerging as an adult fly after two weeks.[41]

Reclinervellus nielseni

The parasitic wasp larvae Reclinervellus nielseni attach to the spider Cyclosa argenteoalba, releasing substances that modify the spider's web-building behavior so that it weaves a cocoon-like structure for the larvae to pupate in. This manipulated behavior was longer lasting and more prominent the longer the larvae were attached to the spider.[42]

Strepsiptera

Strepsiptera of the family Myrmecolacidae can cause their ant host to linger on the tips of grass leaves, increasing the chance of being found by the parasite's males (in case of females) and putting them in a good position for male emergence (in case of males).[43]

Parasitic crustaceans

Rhizocephala

Members of the order Rhizocephala such as S. carcini alter male hosts' hormonal balance, to encourage nurturing behavior similar to that seen in females. The parasite usually spends its entire life within the host; however, if it is removed from the host in a laboratory setting, male hosts will subsequently grow partial or complete female gonads.[44]

Mechanisms

The way in which parasites induce behavioral changes in hosts has been compared to the way a neurobiologist would effect a similar change in a lab.[45] A scientist may stimulate a certain pathway in order to produce a specific behavior, such as increased appetite or lowered anxiety; parasites also produce specific behavioral changes in their hosts, but rather than stimulate specific neurological pathways, they appear to target broader areas of the central nervous system. While the proximate mechanisms underlying this broad targeting have not been fully characterized, two mechanisms used by parasites to alter behavior in vertebrate hosts have been identified: infection of the central nervous system and altered neurochemical communication.[46]

Central nervous system infection

Some parasites alter host behavior by infecting neurons in the host's central nervous system. The host's central nervous system responds to the parasite as it would to any other infection. The hallmarks of such response include local inflammation and the release of chemicals such as cytokines. The immune response itself is responsible for induced behavioral changes in many cases of parasitic infection. Parasites that are known to induce behavioral changes through central nervous system inflammation in their hosts include Toxoplasma gondii in rats, Trypanosoma cruzi in mice and Plasmodium mexicanum in the Mexican lizard.[46]

Immune response
Toxoplasma gondii induces behavioural changes in rats by infecting central nervous system neurons.

While some parasites exploit their hosts' typical immune responses, others seem to alter the immune response itself. For example, the typical immune response in rodents is characterized by heightened anxiety.[47] Infection with Toxoplasma gondii inhibits this response, increasing the risk of predation by T. gondii's subsequent hosts. Research suggests that the inhibited anxiety-response could be the result of immunological damage to the limbic system.[45]

Altered neurotransmission

Parasites that induce behavioral changes in their hosts often exploit the regulation of social behavior in the brain.[46] Social behavior is regulated by neurotransmitters, such as dopamine and serotonin, in the emotional centers of the brain – primarily the amygdala and the hypothalamus, and although parasites may be capable of stimulating specific neurochemical pathways to induce behavioral changes, evidence suggests that they alter neurochemical communication through broad rather than specific targeting.[45] For example, Toxoplasma gondii attaches to the hypothalamus rather than target a specific cellular pathway; this broad targeting leads to a widespread increase in host dopamine levels, which may in turn account for the loss of aversion to cat odor.[48] In some cases, T. gondii is believed to cause increases in dopamine levels by secreting another compound, L-Dopa, which may trigger a rise in dopamine levels, though concrete evidence for this mechanism has not yet been demonstrated.[48] This rise in dopamine levels induces a loss of aversion to cat odor in the rats, increasing the risk of predation by cats, T. gondii's definitive host.[48] The mechanistic details underlying the increase in dopamine levels and the way it affects the rat's behavioral change remain elusive.[45]

The emerald cockroach wasp alters behavior through the injection of venom directly into the host's brain, causing hypokinesia.[27][46] This is achieved by a reduction in dopamine and octopamine activity, which affects the transmission of interneurons involved in the escape response;[28] so while the host's brain circuitry responsible for movement control is still functional – and indeed it will slog along when pulled by the wasp – the nervous system is in a depressed state. Put differently: the wasp's toxin affects not the host's ability to move, but its motivation to do so.

The original function of such secretions may have been to suppress the immune system of the host, as described above. The trematode Schistosoma mansoni secretes opioid peptides into the host's bloodstream, influencing both its immune response and neural function.[49] Other sources suggest a possible origin in molecular mimicry.[50]

Other mechanisms

Mermithid nematodes infect arthropods, residing in their haemocoel (circulatory cavity) and manipulating their hemolymph osmolality to trigger water-seeking behavior. The means by which they do so are unknown.[51]

Evolutionary perspective

Addition of intermediate hosts

For complex life cycles to emerge in parasites, the addition of an intermediate host species must be beneficial, i.e. result in a higher fitness.[52][53] It is probable that most parasites with complex life cycles evolved from simple life cycles;[54] the evolution from simple to complex life cycles has been analyzed theoretically, and it has been shown that trophically transmitted parasites (parasites that transmit from a prey host to a predator host during predation) can be favored by the addition of an intermediate prey host if the population density of the intermediate host is higher than that of the definitive host.[54] Additional factors that catalyze this transfer are high predation rates, and a low natural mortality rate of the intermediate host.[54]

Parasites with a single host species are faced with the problem of not being able to survive in higher trophic levels and therefore dying with their prey host. The development of complex life cycles is most likely an adaptation of the parasite to survive in the predator.[4] The development of parasite increased trophic transmission is a further adaptation in relation to a complex life cycle, where the parasite increases its transmission to a definitive host by manipulating its intermediate host.[52]

Evolution of induced behaviors

The adaptive manipulation hypothesis posits that specific behavioral alterations induced in a host can be used by parasites to increase their fitness. Under this hypothesis, induced behaviors are the result of natural selection acting upon the parasite's extended phenotype (in this case its host's behavior). Many behaviors induced by obligate parasites to complete their lifecycles are examples of adaptive manipulation because of their clear relationship to parasite fitness. For example, evidence has shown that infection by the parasitic worm Pomphorhynchus laevis leads to altered drifting behavior in its intermediate host, the amphipod Gammarus pulex; this altered behavior increases its host's predation risk by fish which are P. laevis's definitive hosts. The induced behavioral change in the host thus leads to the parasite's increased success in completing its life cycle.[55] In general, whether a specific behavioral change serves an adaptive purpose for the parasite, the host, or both, depends on the entire "host-parasite system":[46] The life cycle of the pathogen, its virulence and the host's immune response.[46]

Conversely, evolved behaviors of the host may be a result of adaptations to parasitism.[56]

References
  1. Seppala, O.; Valtonen, E.; Benesh, D. (2008). "Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission?". Proceedings of the Royal Society B: Biological Sciences. 275 (1643): 1611–1615. doi:10.1098/rspb.2008.0152. PMC 2602814. PMID 18430644.
  2. Luong, L.; Grear, D.; Hudson, P. (2014). "Manipulation of host-resource dynamics impacts transmission of trophic parasites". International Journal for Parasitology. 44 (10): 737–742. doi:10.1016/j.ijpara.2014.05.004. PMID 24929136.
  3. Mouritsen, K.; Poulin, R. (2003). "Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare" (PDF). International Journal for Parasitology. 33 (10): 1043–1050. doi:10.1016/s0020-7519(03)00178-4. PMID 13129526.
  4. Lafferty, K.D. (1999). "The Evolution of Trophic Transmission". Parasitology Today. 15 (3): 111–115. doi:10.1016/s0169-4758(99)01397-6. PMID 10322324.
  5. Maure, Fanny; Brodeur, Jacques; Droit, Anaïs; Doyon, Josée; Thomas, Frédéric (2013). "Bodyguard manipulation in a multipredator context: Different processes, same effect". Behavioural Processes. 99: 81–86. doi:10.1016/j.beproc.2013.06.003. PMID 23791577. S2CID 13154407.
  6. Moore, J. (2002). Parasites and the behavior of animals. Oxford: Oxford University Press.
  7. Libersat, Frederic (1 May 2018). "Mind Control: How Parasites Manipulate Cognitive Functions in Their Insect Hosts". Frontiers in Psychology. 9: 572. doi:10.3389/fpsyg.2018.00572. PMC 5938628. PMID 29765342.
  8. Adamo, S (2002). "Modulating the Modulators: Parasites, Neuromodulators and Host Behavioral Change". Brain, Behavior and Evolution. 60 (6): 370–377. doi:10.1159/000067790. PMID 12563169. S2CID 8702062.
  9. Thomas, F.; Adamo, S.; Moore, J. (2005). "Parasitic manipulation: where are we and where should we go?". Behavioural Processes. 68 (3): 185–199. doi:10.1016/j.beproc.2004.06.010. PMID 15792688. S2CID 599951.
  10. Tomonaga, K (2004). "Virus-induced neurobehavioral disorders: mechanisms and implications". Trends in Molecular Medicine. 10 (2): 71–77. doi:10.1016/j.molmed.2003.12.001. PMC 7128097. PMID 15102360.
  11. Poulin, Robert (1997). Evolutionary Ecology of Parasites - From individuals to communities. Springer. p. 76. ISBN 978-0-412-79370-7.
  12. Thomas, F.; Schmidt-Rhaesa, A.; Martin, G.; Manu, C.; Durand, P.; Renaud, F. (May 2002). "Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?" (PDF). J. Evol. Biol. 15 (3): 356–361. CiteSeerX 10.1.1.485.9002. doi:10.1046/j.1420-9101.2002.00410.x. S2CID 86278524. Archived from the original (PDF) on 2015-09-24.
  13. Zimmer, Carl (November 2014). "Mindsuckers - Meet Nature's Nightmare". National Geographic.
  14. "Rabies". World Health Organization. 2019-09-27. Retrieved 2020-03-18.
  15. Nyasembe, V.O.; et al. (2014). "Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake". Current Biology. 24 (2): 217–21. doi:10.1016/j.cub.2013.12.022. PMC 3935215. PMID 24412210.
  16. Wekesa, Joseph W.; Mwangi, Richard W.; Copeland, Robert S. (1992-10-01). "Effect of Plasmodium Falciparum on Blood Feeding Behavior of Naturally Infected Anopheles Mosquitoes in Western Kenya". The American Journal of Tropical Medicine and Hygiene. 47 (4): 484–488. doi:10.4269/ajtmh.1992.47.484. PMID 1443347.
  17. Berdoy, M.; Webster, J.; Macdonald, D. (2000). "Fatal attraction in rats infected with Toxoplasma gondii". Proceedings of the Royal Society B: Biological Sciences. 267 (1452): 1591–1594. doi:10.1098/rspb.2000.1182. PMC 1690701. PMID 11007336.
  18. Lindová, Jitka; Příplatová, Lenka; Flegr, Jaroslav (2012). "Higher Extraversion and Lower Conscientiousness in Humans Infected with Toxoplasma". European Journal of Personality. 26 (3): 285–291. doi:10.1002/per.838. S2CID 3236799.
  19. Otranto, D.; Traversa, D. (2002). "A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment". Veterinary Parasitology. 107 (4): 317–335. doi:10.1016/s0304-4017(02)00121-8. PMID 12163243.
  20. Yanoviak, S.; Kaspari, M.; Dudley, R.; Poinar, G. (2008). "Parasite-Induced Fruit Mimicry in a Tropical Canopy Ant". Am Nat. 171 (4): 536–544. doi:10.1086/528968. PMID 18279076. S2CID 23857167.
  21. Robinson, E (1947). "Notes on the Life History of Leucochloridium fuscostriatum n. sp. provis. (Trematoda: Brachylaemidae)". The Journal of Parasitology. 33 (6): 467–475. doi:10.2307/3273326. JSTOR 3273326. PMID 18903602.
  22. Robinson, Edwin J., Jr. (December 1947). "Notes on the Life History of Leucochloridium fuscostriatum n. sp. provis. (Trematoda: Brachylaemidae)". The Journal of Parasitology. 33 (6): 467–475. doi:10.2307/3273326. JSTOR 3273326. PMID 18903602.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  23. Levri, E (1998). "The Influence of Non-Host Predators on Parasite-Induced Behavioral Changes in a Freshwater Snail". Oikos. 81 (3): 531–537. doi:10.2307/3546773. JSTOR 3546773.
  24. Ponton, Fleur; Otálora-Luna, Fernando; Lefèvre, Thierry; Guerin, Patrick M.; Lebarbenchon, Camille; Duneau, David; Biron, David G.; Thomas, Frédéric (2011-03-01). "Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation". Behavioral Ecology. 22 (2): 392–400. doi:10.1093/beheco/arq215. PMC 3071748. PMID 22476265.
  25. Benesh, D.; Hafer, N. (2012). "Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host". Parasites & Vectors. 5 (1): 90. doi:10.1186/1756-3305-5-90. PMC 3403952. PMID 22564512.
  26. Barber, I.; Walker, P.; Svensson, P. (2004). "Behavioural Responses to Simulated Avian Predation in Female Three Spined Sticklebacks: The Effect of Experimental Schistocephalus Solidus Infections". Behaviour. 141 (11): 1425–1440. doi:10.1163/1568539042948231.
  27. Haspel, Gal; Rosenberg, Lior Ann; Libersat, Frederic (2003-09-05). "Direct injection of venom by a predatory wasp into cockroach brain". Journal of Neurobiology. 56 (3): 287–292. CiteSeerX 10.1.1.585.5675. doi:10.1002/neu.10238. PMID 12884267.
  28. Banks, Christopher N.; Adams, Michael E. (2012). "Biogenic amines in the nervous system of the cockroach, Periplaneta americana following envenomation by the jewel wasp, Ampulex compressa". Toxicon. 59 (2): 320–328. doi:10.1016/j.toxicon.2011.10.011. PMID 22085538..
  29. Milstein, Mati (2007-12-06). ""Zombie" Roaches Lose Free Will Due to Wasp Venom". National Geographic News. Retrieved 2017-10-10.
  30. Maure, Fanny; Brodeur, Jacques; Ponlet, Nicolas; Doyon, Josée; Firlej, Annabelle; Elguero, Éric; Thomas, Frédéric (2011). "The cost of a bodyguard". Biology Letters. 7 (6): 843–846. doi:10.1098/rsbl.2011.0415. PMC 3210670. PMID 21697162.
  31. Maure, F.; Doyon, J.; Thomas, F.; Brodeur, J. (2014). "Host behaviour manipulation as an evolutionary route towards attenuation of parasitoid virulence". Journal of Evolutionary Biology. 27 (12): 2871–2875. doi:10.1111/jeb.12530. PMID 25399504.
  32. Maure, F.; Daoust, S. P.; Brodeur, J.; Mitta, G.; Thomas, F. (2013). "Diversity and evolution of bodyguard manipulation". Journal of Experimental Biology. 216 (Pt 1): 36–42. doi:10.1242/jeb.073130. PMID 23225865.
  33. Bates, Mary (2014-11-02). "Meet 5 "Zombie" Parasites That Mind-Control Their Hosts". National Geographic News. Retrieved 2017-10-10.
  34. W.G., Ebenhard (2000). "Spider manipulation by a wasp larva". Nature. 406 (6793): 255–256. Bibcode:2000Natur.406..255E. doi:10.1038/35018636. PMID 10917517. S2CID 4346139.
  35. Hughes, D. P.; Andersen, S. B.; Hywel-Jones, N. L.; Himaman, W.; Billen, J.; Boomsma, J. J. (May 2011). "Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection". BMC Ecology. 11 (1): 13–22. doi:10.1186/1472-6785-11-13. PMC 3118224. PMID 21554670.
  36. Andersen, S. B.; Gerritsma, S.; Yusah, K. M.; Mayntz, D.; Hywel-Jones, N. L.; Billen, J.; Boomsma, J. J.; Hughes, D. P. (September 2009). "The life of a dead ant: The expression of an adaptive extended phenotype" (PDF). The American Naturalist. 174 (3): 424–433. doi:10.1086/603640. hdl:11370/e6374602-b2a0-496c-b78e-774b34fb152b. JSTOR 10.1086/603640. PMID 19627240. S2CID 31283817.
  37. Sample, Ian (18 August 2010). "'Zombie ants' controlled by parasitic fungus for 48m years". The Guardian. Retrieved 2010-08-22.
  38. ""Zombie" Ants Controlled, Decapitated by Flies". National Geographic News. 2009-05-14. Retrieved 2017-10-10.
  39. "Crowded Skies". SuperNature - Wild Flyers. Episode 3. PBS. 2016-06-30. Retrieved 2017-10-10.
  40. Malhotra, Richa (2015-01-09). "Phorid fly is the headhunter of the animal kingdom". BBC - Earth. Retrieved 2017-10-10.
  41. Hanna, Bill (May 12, 2009). "Parasitic flies turn fire ants into zombies". Fort Worth Star-Telegram. Archived from the original on May 22, 2009. Retrieved 2009-05-14.
  42. Takasuka, Keizo (2019-09-16). "Evaluation of manipulative effects by an ichneumonid spider-ectoparasitoid larva upon an orb-weaving spider host (Araneidae: Cyclosa argenteoalba) by means of surgical removal and transplantation". The Journal of Arachnology. 47 (2): 181. doi:10.1636/joa-s-18-082. ISSN 0161-8202. S2CID 202579182.
  43. Wojcik, Daniel P. (1989). "Behavioral Interactions between Ants and Their Parasites". The Florida Entomologist. 72 (1): 43–51. doi:10.2307/3494966. JSTOR 3494966.
  44. Cheng, Thomas C. (2012). General Parasitology. Elsevier Science. pp. 756–757. ISBN 978-0-323-14010-2. Archived from the original on 2018-02-08.
  45. Thomas, edited by David P. Hughes, Jacques Brodeur, Frédéric; Brodeur, J.; Thomas, F. (2012). Host manipulation by parasites. Oxford University Press. ISBN 978-0-19-964224-3. {{cite book}}: |first1= has generic name (help)
  46. Klein, Sabra L. (August 2003). "Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates". Physiology & Behavior. 79 (3): 441–449. doi:10.1016/S0031-9384(03)00163-X. PMID 12954438. S2CID 28547443.
  47. Lacosta, S.; Merali, Z.; Anisman, H. (1999-02-13). "Behavioral and neurochemical consequences of lipopolysaccharide in mice: anxiogenic-like effects". Brain Research. 818 (2): 291–303. doi:10.1016/s0006-8993(98)01288-8. PMID 10082815. S2CID 5915083.
  48. Webster, J. P. (Dec 1994). "The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus". Parasitology. 109 (5): 583–589. doi:10.1017/s0031182000076460. PMID 7831094.
  49. M., Kavaliers; et al. (1999). "Parasites and behavior: an ethopharmacological analysis and biomedical implications". Neuroscience and Biobehavioral Reviews. 23 (7): 1037–1045. doi:10.1016/s0149-7634(99)00035-4. PMID 10580316. S2CID 29936892.
  50. Biron, D. G.; et al. (2005). "Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach" (PDF). Proceedings of the Royal Society B. 272 (1577): 2117–21126. doi:10.1098/rspb.2005.3213. PMC 1559948. PMID 16191624. Archived from the original (PDF) on 2013-08-05.
  51. C.M., Williams (2004). "Increased haemolymph osmolality suggests a new route for behavioural manipulation of Talorchestia quoyana (Amphipoda: Talitridae) by its mermithid parasite". Functional Ecology. 18 (5): 685–691. doi:10.1111/j.0269-8463.2004.00910.x. S2CID 3984423.
  52. Trail, D (1980). "Behavioral Interactions between Parasites and Hosts: Host Suicide and the Evolution of Complex Life Cycles". The American Naturalist. 116 (1): 77–91. doi:10.1086/283612. hdl:1808/17548. S2CID 16777324.
  53. Brown, S.; Renaud, F.; Guégan, J.; Thomas, F. (2001). "Evolution of trophic transmission in parasites: the need to reach a mating place?". Journal of Evolutionary Biology. 14 (5): 815–820. doi:10.1046/j.1420-9101.2001.00318.x. S2CID 62785069.
  54. Choisy, M.; Brown, S.; Lafferty, K.; Thomas, F. (2003). "Evolution of Trophic Transmission in Parasites: Why Add Intermediate Hosts?" (PDF). Am Nat. 162 (2): 172–181. doi:10.1086/375681. PMID 12858262. S2CID 37774233.
  55. Lagrue, Clément; Kaldonski, Nicolas; Perrot-Minnot, Marie J.; Motreuil, Sébastien; Bollache, Loïc (Nov 2007). "Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation". Ecology. 88 (11): 2839–2847. doi:10.1890/06-2105.1. PMID 18051653.
  56. Del Giudice, Marco (September 2019). "Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation". The Quarterly Review of Biology. 94 (3): 249–282. doi:10.1086/705038. hdl:2318/1853346. S2CID 199523717.
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