Behavior-altering parasite

Parasite manipulations can be either direct or indirect. Indirect manipulation is the most frequent method used by behavior-altering parasites,{{cite journal |last1=Adamo |first1=S |year=2002 |title=Modulating the Modulators: Parasites, Neuromodulators and Host Behavioral Change |journal=Brain, Behavior and Evolution |volume=60 |issue=6 |pages=370–377 |pmid=12563169 |doi=10.1159/000067790 |s2cid=8702062}} 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.{{cite journal |last1=Thomas |first1=F. |last2=Adamo |first2=S. |last3=Moore |first3=J. |year=2005 |title=Parasitic manipulation: where are we and where should we go? |journal=Behavioural Processes |volume=68 |issue=3 |pages=185–199 |pmid=15792688 |doi=10.1016/j.beproc.2004.06.010 |s2cid=599951}} Affecting the host's neural system is complicated and manipulation includes initiating immune cascades in the host.{{cite journal |last1=Tomonaga |first1=K |year=2004 |title=Virus-induced neurobehavioral disorders: mechanisms and implications |journal=Trends in Molecular Medicine |volume=10 |issue=2 |pages=71–77 |pmid=15102360 |doi=10.1016/j.molmed.2003.12.001 |pmc=7128097}} 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. A direct approach to behavioral manipulation is often very costly for the parasite, 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 to create the necessary neuroactive compounds to induce a desired behavioral response. Parasites can also indirectly affect the behavior of their hosts by disturbing their metabolism, development, or immunity. Parasitic castrators drastically modify their hosts' metabolism and reproduction, sometimes by secreting castrating hormones, changing their behavior and physiology to benefit the parasite.{{cite book |last=Poulin |first=Robert |author-link=Robert Poulin (zoologist) |title=Evolutionary Ecology of Parasites - From individuals to communities |year=1997 |publisher=Springer |isbn=978-0-412-79370-7 |page=76 |url=https://books.google.com/books?id=QaDVuLXoUNIC}}

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);{{cite journal |last1=Thomas |first1=F. |last2=Schmidt-Rhaesa |first2=A. |last3=Martin |first3=G. |last4=Manu |first4=C. |last5=Durand |first5=P. |last6=Renaud |first6=F. |title=Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?: Parasites and host behaviour |journal=Journal of Evolutionary Biology |date=30 April 2002 |volume=15 |issue=3 |pages=356–361 |citeseerx=10.1.1.485.9002 |doi=10.1046/j.1420-9101.2002.00410.x |s2cid=86278524}} increase parasite survival or increase the host's likelihood of being infected with more parasites.

Viruses from the family Baculoviridae induce in their hosts changes to both feeding behavior and environment selection. They infect moth and butterfly caterpillars, which, sometime 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.{{cite news |last=Zimmer |first=Carl |title=Mindsuckers - Meet Nature's Nightmare |date=November 2014 |work=National Geographic |url=http://ngm.nationalgeographic.com/2014/11/mindsuckers/zimmer-text |url-status=dead |archive-url=https://web.archive.org/web/20141018031555/http://ngm.nationalgeographic.com/2014/11/mindsuckers/zimmer-text |archive-date=October 18, 2014}}

Rabies is a disease caused by viruses of the Lyssavirus genus, which are released into a host's saliva and transmitted when it comes in contact with an other animal's mucous membranes or open wounds. The disease causes the host to become aggressive and prone to attacking or biting others; this, along with increased salivation, increases the chances of it spreading to new hosts. At the same time, the host experiences hydrophobia (fear of water){{cite web |title=Rabies |date=2019-09-27 |website=World Health Organization |language=en |url=https://www.who.int/news-room/fact-sheets/detail/rabies |access-date=2020-03-18 |url-status=live |archive-url=https://web.archive.org/web/20190509201021/https://www.who.int/news-room/fact-sheets/detail/rabies |archive-date=2019-05-09}} and laryngeal spasms,{{cite journal |last1=Chacko |first1=Kadavil |last2=Parakadavathu |first2=Rakesh Theeyancheri |last3=Al-Maslamani |first3=Muna |last4=Nair |first4=Arun P |last5=Chekura |first5=Amrutha Puthalalth |last6=Madhavan |first6=Indira |title=Diagnostic difficulties in human rabies: A case report and review of the literature |journal=Qatar Medical Journal |date=21 April 2017 |volume=2016 |issue=2 |pages=15 |pmid=28534007 |doi=10.5339/qmj.2016.15 |pmc=5427514}} which prevent it from drinking, keeping the virus-laden saliva from being washed down into the stomach or out of the mouth.{{Citation needed|date=September 2022}}

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.{{cite journal |last1=Nyasembe |first1=Vincent O. |last2=Teal |first2=Peter E.A. |last3=Sawa |first3=Patrick |last4=Tumlinson |first4=James H. |last5=Borgemeister |first5=Christian |last6=Torto |first6=Baldwyn |title=Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake |journal=Current Biology |date=January 2014 |volume=24 |issue=2 |pages=217–221 |pmid=24412210 |doi=10.1016/j.cub.2013.12.022 |pmc=3935215}} It also decreases the host's attraction to human blood while gestating, only to increase it when it is ready to be transmitted to a human host.{{cite journal |last1=Wekesa |first1=Joseph W. |last2=Mwangi |first2=Richard W. |last3=Copeland |first3=Robert S. |title=Effect of Plasmodium Falciparum on Blood Feeding Behavior of Naturally Infected Anopheles Mosquitoes in Western Kenya |date=1992-10-01 |journal=The American Journal of Tropical Medicine and Hygiene |volume=47 |issue=4 |pages=484–488 |pmid=1443347 |doi=10.4269/ajtmh.1992.47.484}}

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.{{cite journal |last1=Berdoy |first1=M. |last2=Webster |first2=J. |last3=Macdonald |first3=D. |year=2000 |title=Fatal attraction in rats infected with Toxoplasma gondii |journal=Proceedings of the Royal Society B: Biological Sciences |volume=267 |issue=1452 |pages=1591–1594 |pmid=11007336 |doi=10.1098/rspb.2000.1182 |pmc=1690701}} 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.{{cite journal |title=Higher Extraversion and Lower Conscientiousness in Humans Infected with Toxoplasma |volume=26 |issue=3 |journal=European Journal of Personality |pages=285–291 |year=2012 |last1=Lindová |first1=Jitka |last2=Příplatová |first2=Lenka |last3=Flegr |first3=Jaroslav |doi=10.1002/per.838 |s2cid=3236799}}

Ants infected with the fungus Ophiocordyceps unilateralis exhibit intricate behaviors: irregularly timed body convulsions cause the ant to drop to the forest floor,{{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 |title=Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection |journal=BMC Ecology |date=2011 |volume=11 |issue=1 |pages=13–22 |pmid=21554670 |doi=10.1186/1472-6785-11-13 |doi-access=free |pmc=3118224}} from which it climbs a plant up to a certain height{{cite journal |author1=Andersen, S. B. |author2=Gerritsma, S. |author3=Yusah, K. M. |author4=Mayntz, D. |author5=Hywel-Jones, N. L. |author6=Billen, J. |author7=Boomsma, J. J. |author8=Hughes, D. P. |title=The life of a dead ant: The expression of an adaptive extended phenotype |date=September 2009 |journal=The American Naturalist |volume=174 |issue=3 |pages=424–433 |jstor=10.1086/603640 |pmid=19627240 |doi=10.1086/603640 |hdl=11370/e6374602-b2a0-496c-b78e-774b34fb152b |hdl-access=free |s2cid=31283817 |url=https://pure.rug.nl/ws/files/67295795/603640.pdf}} 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.{{cite news |last=Sample |first=Ian |title='Zombie ants' controlled by parasitic fungus for 48m years |date=18 August 2010 |newspaper=The Guardian |url=https://www.theguardian.com/science/2010/aug/18/zombie-carpenter-ant-fungus |access-date=2010-08-22 |url-status=live |archive-url=https://web.archive.org/web/20200705074241/https://www.theguardian.com/science/2010/aug/18/zombie-carpenter-ant-fungus |archive-date=2020-07-05}}

Extinct Allocordyceps was found in 50-million-year-old amber infecting an ant.

Multiple parasites increase their host's risk of predation to facilitate their transition from their intermediate host to their definitive host, including: Euhaplorchis californiensis,{{cite journal |last1=Otranto |first1=D. |last2=Traversa |first2=D. |year=2002 |title=A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment |journal=Veterinary Parasitology |volume=107 |issue=4 |pages=317–335 |pmid=12163243 |doi=10.1016/s0304-4017(02)00121-8}} Dicrocoelium dendriticum, Diplostomum pseudospathaceum,{{Cite journal |last=Enabulele |first=Egie Elisha |last2=Awharitoma |first2=Agnes Ogheneruemu |last3=Lawton |first3=Scott P. |last4=Kirk |first4=Ruth S. |date=2018-09-25 |title=First molecular identification of an agent of diplostomiasis, Diplostomum pseudospathaceum (Niewiadomska 1984) in the United Kingdom and its genetic relationship with populations in Europe |url=https://www.degruyter.com/doi/10.1515/ap-2018-0054 |journal=Acta Parasitologica |volume=63 |issue=3 |pages=444–453 |doi=10.1515/ap-2018-0054 |issn=1896-1851}} and Myrmeconema neotropicum.{{cite journal |last1=Yanoviak |first1=S. P. |last2=Kaspari |first2=M. |last3=Dudley |first3=R. |last4=Poinar |first4=G. |title=Parasite‐Induced Fruit Mimicry in a Tropical Canopy Ant |journal=The American Naturalist |date=April 2008 |volume=171 |issue=4 |pages=536–544 |pmid=18279076 |doi=10.1086/528968 |s2cid=23857167}}

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.File:Succinea mit Leucocholoridium.jpg]]

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.{{cite journal |last1=Robinson |first1=E |year=1947 |title=Notes on the Life History of Leucochloridium fuscostriatum n. sp. provis. (Trematoda: Brachylaemidae) |journal=The Journal of Parasitology |volume=33 |issue=6 |pages=467–475 |jstor=3273326 |pmid=18903602 |doi=10.2307/3273326}} 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.{{cite journal |author=Robinson, Edwin J. Jr. |title=Notes on the Life History of Leucochloridium fuscostriatum n. sp. provis. (Trematoda: Brachylaemidae) |date=December 1947 |journal=The Journal of Parasitology |volume=33 |issue=6 |pages=467–475 |jstor=3273326 |pmid=18903602 |doi=10.2307/3273326}}

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).{{cite journal |last1=Levri |first1=E |year=1998 |title=The Influence of Non-Host Predators on Parasite-Induced Behavioral Changes in a Freshwater Snail |journal=Oikos |volume=81 |issue=3 |pages=531–537 |jstor=3546773 |citeseerx=10.1.1.527.3484 |doi=10.2307/3546773}}File:Horsehair Worm (14629048952).jpg shortly after emerging from its cricket host, now drowned|left]]

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.{{cite journal |last1=Ponton |first1=Fleur |last2=Otálora-Luna |first2=Fernando |last3=Lefèvre |first3=Thierry |last4=Guerin |first4=Patrick M. |last5=Lebarbenchon |first5=Camille |last6=Duneau |first6=David |last7=Biron |first7=David G. |last8=Thomas |first8=Frédéric |title=Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation |journal=Behavioral Ecology |date=2011 |volume=22 |issue=2 |pages=392–400 |pmid=22476265 |doi=10.1093/beheco/arq215 |pmc=3071748}}

Schistocephalus solidus is a parasitic flatworm 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).{{cite journal |last1=Benesh |first1=D. |last2=Hafer |first2=N. |year=2012 |title=Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host |journal=Parasites & Vectors |volume=5 |issue=1 |page=90 |pmid=22564512 |doi=10.1186/1756-3305-5-90 |doi-access=free |pmc=3403952}} 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.{{cite journal |last1=Barber |first1=I. |last2=Walker |first2=P. |last3=Svensson |first3=P. |year=2004 |title=Behavioural Responses to Simulated Avian Predation in Female Three Spined Sticklebacks: The Effect of Experimental Schistocephalus Solidus Infections |journal=Behaviour |volume=141 |issue=11 |pages=1425–1440 |doi=10.1163/1568539042948231}} 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 and therefore effectively reduce its own mortality rate, due to premature transmission.{{Citation needed|date=September 2022}}

File:Vespa Joia arrastando barata (cropped).jpg "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 precise sting, directly into the cockroach's brain;{{cite journal |volume=56 |issue=3 |pages=287–292 |last1=Haspel |first1=Gal |last2=Rosenberg |first2=Lior Ann |last3=Libersat |first3=Frederic |title=Direct injection of venom by a predatory wasp into cockroach brain |journal=Journal of Neurobiology |date=2003-09-05 |citeseerx=10.1.1.585.5675 |pmid=12884267 |doi=10.1002/neu.10238}} 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".{{cite journal |last1=Banks |first1=Christopher N. |last2=Adams |first2=Michael E. |title=Biogenic amines in the nervous system of the cockroach, Periplaneta americana following envenomation by the jewel wasp, Ampulex compressa |journal=Toxicon |date=February 2012 |volume=59 |issue=2 |pages=320–328 |pmid=22085538 |doi=10.1016/j.toxicon.2011.10.011}} 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.{{cite web |last=Milstein |first=Mati |title="Zombie" Roaches Lose Free Will Due to Wasp Venom |work=National Geographic News |date=2007-12-06 |url=http://news.nationalgeographic.com/news/2007/12/071206-roach-zombie.html |access-date=2017-10-10 |url-status=dead |archive-url=https://web.archive.org/web/20071207135846/http://news.nationalgeographic.com/news/2007/12/071206-roach-zombie.html |archive-date=December 7, 2007}} The adult wasp emerges after 6 weeks, leaving behind nothing but an empty cockroach "shell".

File:Ladybird with a parasitoid cocoon (7211917770).jpg guarding a Dinocampus coccinellae cocoon. The ladybug will remain stationary until the adult wasp emerges from its cocoon, and die some time afterward]]

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. When a predator approaches, the beetle twitches its limbs, scaring the predator off. This use of the host as a protection has been termed bodyguard manipulation.{{cite journal |last1=Maure |first1=Fanny |last2=Brodeur |first2=Jacques |last3=Ponlet |first3=Nicolas |last4=Doyon |first4=Josée |last5=Firlej |first5=Annabelle |last6=Elguero |first6=Éric |last7=Thomas |first7=Frédéric |year=2011 |title=The cost of a bodyguard |journal=Biology Letters |volume=7 |issue=6 |pages=843–846 |pmid=21697162 |doi=10.1098/rsbl.2011.0415 |pmc=3210670}}{{cite journal |last1=Maure |first1=F. |last2=Doyon |first2=J. |last3=Thomas |first3=F. |last4=Brodeur |first4=J. |year=2014 |title=Host behaviour manipulation as an evolutionary route toward attenuation of parasitoid virulence |journal=Journal of Evolutionary Biology |volume=27 |issue=12 |pages=2871–2875 |pmid=25399504 |doi=10.1111/jeb.12530 |doi-access=free}} Similarly, several parasitic wasps induce their spider hosts to build stronger webs to protect the growing parasites.{{cite journal |last1=Maure |first1=F. |last2=Daoust |first2=S. P. |last3=Brodeur |first3=J. |last4=Mitta |first4=G. |last5=Thomas |first5=F. |year=2013 |title=Diversity and evolution of bodyguard manipulation |journal=Journal of Experimental Biology |volume=216 |issue=Pt 1 |pages=36–42 |pmid=23225865 |doi=10.1242/jeb.073130 |doi-access=free}}

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,{{cite web |last1=Bates |first1=Mary |title=Meet 5 "Zombie" Parasites That Mind-Control Their Hosts |work=National Geographic News |date=2014-11-02 |url=http://news.nationalgeographic.com/news/2014/10/141031-zombies-parasites-animals-science-halloween/ |access-date=2017-10-10 |url-status=dead |archive-url=https://web.archive.org/web/20141101114543/http://news.nationalgeographic.com/news/2014/10/141031-zombies-parasites-animals-science-halloween/ |archive-date=November 1, 2014}} causing it to weave a strong, cocoon-like structure. The larva then kills the spider and enters the cocoon to pupate.{{cite journal |last1=W.G. |first1=Ebenhard |title=Spider manipulation by a wasp larva |journal=Nature |date=2000 |volume=406 |issue=6793 |pages=255–256 |bibcode=2000Natur.406..255E |pmid=10917517 |doi=10.1038/35018636 |s2cid=4346139}}

Several species of fly in the genus Pseudacteon parasitize 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 toward a moist, leafy place where they can hatch safely.{{cite web |title="Zombie" Ants Controlled, Decapitated by Flies |date=2009-05-14 |work=National Geographic News |url=http://news.nationalgeographic.com/news/2009/05/photogalleries/zombie-ants/ |access-date=2017-10-10 |url-status=dead |archive-url=https://web.archive.org/web/20090517030309/http://news.nationalgeographic.com/news/2009/05/photogalleries/zombie-ants/ |archive-date=May 17, 2009}}{{cite episode |publisher=PBS |number=3 |title=Crowded Skies |date=2016-06-30 |series=SuperNature - Wild Flyers |url=http://www.pbs.org/video/2365791097/ |access-date=2017-10-10 |url-status=live |archive-url=https://web.archive.org/web/20161106185036/http://www.pbs.org/video/2365791097/ |archive-date=2016-11-06}} Eventually the larva completely devours the ant's brain, which often falls off (hence the species nickname: "decapitating fly").{{cite web |last=Malhotra |first=Richa |title=Phorid fly is the headhunter of the animal kingdom |date=2015-01-09 |work=BBC - Earth |url=http://www.bbc.com/earth/story/20150109-headhunters-of-the-animal-kingdom |access-date=2017-10-10 |archive-url=https://web.archive.org/web/20150720185856/https://www.bbc.com/earth/story/20150109-headhunters-of-the-animal-kingdom |archive-date=July 20, 2015}} The larva then pupates in the empty head capsule, emerging as an adult fly after two weeks.{{cite news |last=Hanna |first=Bill |title=Parasitic flies turn fire ants into zombies |date=May 12, 2009 |publisher=Fort Worth Star-Telegram |url=https://news.yahoo.com/s/mcclatchy/20090512/sc_mcclatchy/3231765 |access-date=2009-05-14 |url-status=dead |archive-url=https://web.archive.org/web/20090522005217/http://news.yahoo.com/s/mcclatchy/20090512/sc_mcclatchy/3231765 |archive-date=May 22, 2009}}File:Reclinervellus nielseni.jpg larva parasitizing Cyclosa argenteoalba in Japan]]

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.{{cite journal |last1=Takasuka |first1=Keizo |title=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 |journal=The Journal of Arachnology |date=16 September 2019 |volume=47 |issue=2 |pages=181 |doi=10.1636/joa-s-18-082 |s2cid=202579182}}

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).{{cite journal |volume=72 |issue=1 |pages=43–51 |last=Wojcik |first=Daniel P. |title=Behavioral Interactions between Ants and Their Parasites |journal=The Florida Entomologist |date=1989 |jstor=3494966 |doi=10.2307/3494966}}

Members of the order Rhizocephala such as Sacculina 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.{{Google books|d4GQlYzode8C|Rhizocephalan Host-Parasite Relationships|page=756}} in {{cite book |chapter=Other Zooparasites |title=General Parasitology |year=1986 |last1=Cheng |first1=Thomas C. |pages=706–787 |isbn=978-0-12-170755-2 |doi=10.1016/B978-0-12-170755-2.50025-X}}

The ways in which parasites induce behavioral changes in hosts have been compared to the way a neurobiologist would effect a similar change in a lab.{{cite book |title=Host Manipulation by Parasites |year=2012 |isbn=978-0-19-964223-6 |editor-last1=Hughes |editor-last2=Brodeur |editor-last3=Thomas |editor-first1=David P |editor-first2=Jacques |editor-first3=Frédéric |doi=10.1093/acprof:oso/9780199642236.001.0001}}{{page needed|date=December 2022}} 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.{{cite journal |last=Klein |first=Sabra L. |author-link1=Sabra Klein |title=Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates |date=August 2003 |journal=Physiology & Behavior |volume=79 |issue=3 |pages=441–449 |pmid=12954438 |doi=10.1016/S0031-9384(03)00163-X |s2cid=28547443}}

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.

File:Toxoplasma gondii (2).jpg

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.{{cite journal |volume=818 |issue=2 |pages=291–303 |last1=Lacosta |first1=S. |last2=Merali |first2=Z. |last3=Anisman |first3=H. |title=Behavioral and neurochemical consequences of lipopolysaccharide in mice: anxiogenic-like effects |journal=Brain Research |date=1999-02-13 |pmid=10082815 |doi=10.1016/s0006-8993(98)01288-8 |s2cid=5915083}} 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.

Parasites that induce behavioral changes in their hosts often exploit the regulation of social behavior in the brain. 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. 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.{{cite journal |volume=109 |pages=583–589 |last=Webster |first=J. P. |title=The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus |journal=Parasitology |date=Dec 1994 |issue=5 |pmid=7831094 |doi=10.1017/s0031182000076460 |s2cid=22689318}} 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. 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. The mechanistic details underlying the increase in dopamine levels and the way it affects the rat's behavioral change remain elusive.

The emerald cockroach wasp alters behavior through the injection of venom directly into the host's brain, causing hypokinesia. This is achieved by a reduction in dopamine and octopamine activity, which affects the transmission of interneurons involved in the escape response; 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.{{cite journal |last1=Kavaliers |first1=M |last2=Colwell |first2=D.D |last3=Choleris |first3=E |title=Parasites and behavior: an ethopharmacological analysis and biomedical implications |journal=Neuroscience & Biobehavioral Reviews |date=November 1999 |volume=23 |issue=7 |pages=1037–1045 |pmid=10580316 |doi=10.1016/s0149-7634(99)00035-4 |s2cid=29936892}} Other sources suggest a possible origin in molecular mimicry.{{cite journal |last1=Biron |first1=D.G |last2=Marché |first2=L |last3=Ponton |first3=F |last4=Loxdale |first4=H.D |last5=Galéotti |first5=N |last6=Renault |first6=L |last7=Joly |first7=C |last8=Thomas |first8=F |title=Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach |journal=Proceedings of the Royal Society B: Biological Sciences |date=22 October 2005 |volume=272 |issue=1577 |pages=2117–2126 |pmid=16191624 |doi=10.1098/rspb.2005.3213 |pmc=1559948}}

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.{{cite journal |last1=C.M. |first1=Williams |title=Increased haemolymph osmolality suggests a new route for behavioural manipulation of Talorchestia quoyana (Amphipoda: Talitridae) by its mermithid parasite |journal=Functional Ecology |date=2004 |volume=18 |issue=5 |pages=685–691 |doi=10.1111/j.0269-8463.2004.00910.x |doi-access=free |s2cid=3984423}}

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.{{cite journal |last1=Trail |first1=D |year=1980 |title=Behavioral Interactions between Parasites and Hosts: Host Suicide and the Evolution of Complex Life Cycles |journal=The American Naturalist |volume=116 |issue=1 |pages=77–91 |doi=10.1086/283612 |hdl=1808/17548 |hdl-access=free |s2cid=16777324}}{{cite journal |last1=Brown |first1=S. |last2=Renaud |first2=F. |last3=Guégan |first3=J. |last4=Thomas |first4=F. |year=2001 |title=Evolution of trophic transmission in parasites: the need to reach a mating place? |journal=Journal of Evolutionary Biology |volume=14 |issue=5 |pages=815–820 |doi=10.1046/j.1420-9101.2001.00318.x |doi-access=free |s2cid=62785069}} It is probable that most parasites with complex life cycles evolved from simple life cycles;{{cite journal |last1=Choisy |first1=M. |last2=Brown |first2=S. |last3=Lafferty |first3=K. |last4=Thomas |first4=F. |year=2003 |title=Evolution of Trophic Transmission in Parasites: Why Add Intermediate Hosts?. |journal=Am Nat |volume=162 |issue=2 |pages=172–181 |pmid=12858262 |doi=10.1086/375681 |s2cid=37774233 |url=https://hal.umontpellier.fr/hal-02502579/file/Thomas_04.pdf |access-date=2020-06-05 |url-status=live |archive-url=https://web.archive.org/web/20200506023158/https://hal.umontpellier.fr/hal-02502579/file/Thomas_04.pdf |archive-date=2020-05-06}} 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. Additional factors that catalyze this transfer are high predation rates, and a low natural mortality rate of the intermediate host.

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. 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.

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.{{cite journal |last1=Lagrue |first1=Clément |last2=Kaldonski |first2=Nicolas |last3=Perrot-Minnot |first3=Marie J. |last4=Motreuil |first4=Sébastien |last5=Bollache |first5=Loïc |title=Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation |date=Nov 2007 |journal=Ecology |volume=88 |issue=11 |pages=2839–2847 |pmid=18051653 |doi=10.1890/06-2105.1}} 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": The life cycle of the pathogen, its virulence and the host's immune response.

Conversely, evolved behaviors of the host may be a result of adaptations to parasitism.{{cite journal |last1=Del Giudice |first1=Marco |title=Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation |date=September 2019 |journal=The Quarterly Review of Biology |volume=94 |issue=3 |pages=249–282 |doi=10.1086/705038 |hdl=2318/1853346 |hdl-access=free |s2cid=199523717}}

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Category:Abnormal behaviour in animals

Category:Mind-altering parasitism

Category:Parasites of animals