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Parazitlerin konak davranışlarına etkileri

Year 2024, , 164 - 173, 15.06.2024
https://doi.org/10.33188/vetheder.1353693

Abstract

Parazitler ve konakları evrimsel süreçte uzun yıllardır birlikte var olmuş ve birbirlerine karşı çeşitli savunma mekanizmaları geliştirmişlerdir. Parazitin yerleştiği yere göre konakta davranış değişikliği meydana gelebilmektedir. Davranış değişiklikleri, parazitin yaşam döngüsünü tamamlamasını kolaylaştırarak enfeksiyon oluşma şansını ve konağa adaptasyonunu artırır. Bu durum konaklarda davranış, renk, morfoloji ve fizyoloji gibi pek çok değişikliğe sebep olur. Ayrıca saldırganlık, çiftleşme ve üreme, ebeveyn davranışı üzerine etkileri olmaktadır. Bu değişikliklerde nöral, endokrin, nöromodülatör, immunomodülatör gibi fizyolojik sistemlerin rolü büyüktür. Davranış manipülasyonları, genellikle indirekt yaşam döngüsüne sahip parazitlerde gözlenmektedir ve bu parazitlerin en önemlileri arasında Dicrocoelium dendriticum ve Toxoplasma gondii örnek olarak gösterilebilir. Son yıllarda parazitle enfekte hayvanlardaki davranış değişiklikleri, bilim dünyasınında da oldukça ilgi çekici bir hal almış ve bu konuda birçok çalışma yapılmıştır. Bu derlemede, konuyla ilişkin yapılan çalışmalar bir araya getirilmiş ve örnekler ile parazitlerin bu davranış değişikliklerine sebep olma mekanizmaları açıklanmaya çalışılmıştır.

References

  • Poulin R. “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 1995; 25: 1371-1383.
  • Dobson A. The population biology of parasite-induced changes in host behavior. Q Rev Biol 1988; 63: 139-165.
  • Moore J. Parasites and the behavior of animals: Oxford University Press on Demand, Oxford; 2002.
  • Klein SL. Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 2003; 79: 441-449.
  • Bakker TC, Frommen JG, Thünken T. Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology 2017; 123: 779-784.
  • Kavaliers M, Colwell D, Ossenkopp K-P, Perrot-Sinal T. Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav Ecol Sociobiol 1997; 40: 373-384.
  • Edwards J. The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Anim Behav 1988; 36: 529-540.
  • Pittella JEH. Central nervous system involvement in experimental trypanosomiasis cruzi. Mem Inst Oswaldo Cruz 1991; 86: 141-145.
  • Kavaliers M, Colwell D, Choleris E. Analgesic responses of male mice exposed to the odors of parasitized females: effects of male sexual experience and infection status. Behav Neurosci 1998; 112: 1001.
  • Isseroff H, Sylvester PW, Held WA. Effects of Schistosoma mansoni on androgen regulated gene expression in the mouse. Mol Biochem Parasitol 1986; 18: 401-412.
  • Larralde C, Morales J, Terrazas I, Govezensky T, Romano M. Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol 1995; 52: 575-580.
  • Cox D, Holland C. The relationship between numbers of larvae recovered from the brain of Toxocara canis-infected mice and social behaviour and anxiety in the host. Parasitology 1998; 116: 579-594.
  • Berdoy M, Webster J, MacDonald D. The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 1995; 59: 605-614.
  • Willis C, Poulin R. Effects of the tapeworm Hymenolepis diminuta on maternal investment in rats. Can J Zool 1999; 77: 1001-1005.
  • Lin YC, Rikihisa Y, Kono H, Gu Y. Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Exp Parasitol 1990; 70: 344-352.
  • Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S. Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 2004; 15(6): 930-937.
  • Henderson D, Bird DM, Rau ME, Negro JJ. Mate choice in captive American kestrels, Falco sparverius, parasitized by a nematode, Trichinella pseudospiralis. Ethology 1995; 101: 112-120.
  • Korpimaki E, Tolonen P, Bennett GF. Blood parasites, sexual selection and reproductive success of European kestrels. Ecoscience 1995; 2(4): 335-343.
  • Johnson LL, Boyce MS. Female choice of males with low parasite loads in sage grouse. Bird parasite interactions Oxford University Press, Oxford. 1991: 377-388.
  • Richner H, Christe P, Oppliger A. Paternal investment affects prevalence of malaria. Proc Natl Acad Sci 1995; 92: 1192-1194.
  • Rätti O, Dufva R, Alatalo RV. Blood parasites and male fitness in the pied flycatcher. Oecologia 1993; 96: 410-414.
  • Buchanan KL, Catchpole C, Lewis J, Lodge A. Song as an indicator of parasitism in the sedge warbler. Anim Behav 1999; 57: 307-314.
  • Zuk M, Thornhill R, Ligon JD, Johnson K. Parasites and mate choice in red jungle fowl. Am Zool 1990; 30: 235-244.
  • Møller AP. Parasite load reduces song output in a passerine bird. Anim Behav 1991; 41: 723-730.
  • Dunlap KD, Schall JJ. Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 1995; 68: 608-621.
  • Dunlap KD, Church DR. Interleukin-1β reduces daily activity level in male lizards, Sceloporus occidentalis. Brain Behav Immun 1996; 10(1): 68-73.
  • Gill DE, Mock BA. Ecological and evolutionary dynamics of parasites: the case of Trypanosoma diemyctyli in the red-spotted newt Notophthalmus viridescens. In: Rollinson D, Anderson RM, editors. Ecology and genetics of host–parasite interactions. London: Academic Press 1985; 157–183.
  • Kennedy C, Endler J, Poynton S, McMinn H. Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 1987; 21: 291-295.
  • Bakker TC, Mundwiler B. Pectoral fin size in a fish species with paternal care: a condition‐dependent sexual trait revealing infection status. Freshw Biol 1999; 41: 543-551.
  • Barber I, Huntingford FA. The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 1995; 132(15-16): 1223-1240.
  • Berger CS, Laroche J, Maaroufi H, Martin, H, Moon KM, Landry CR, Aubin-Horth N. The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions. Parasit Vectors 2021; 14(1): 1-20.
  • Baer J, Gugele SM, Roch S, Brinker A. Stickleback mass occurrence driven by spatially uneven parasite pressure? Insights into infection dynamics, host mortality, and epizootic variability. Parasitol Res 2022; 121(6): 1607-1619.
  • Mulvey M, Aho J. Parasitism and mate competition: liver flukes in white-tailed deer. Oikos 1993: 187-192.
  • Cox DM, Holland CV. The relationship between numbers of larvae recovered from the brain of Toxocara canis-infected mice and social behaviour and anxiety in the host. Parasitol 1998; 116(6): 579-594.
  • Poulin R. Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav. 41: Elsevier 2010; 151-186.
  • Aeby G. Trade-offs for the butterflyfish, Chaetodon multicinctus, when feeding on coral prey infected with trematode metacercariae. Behav Ecol Sociobiol 2002; 52: 158-165.
  • Lafferty KD, Shaw JC. Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 2013; 216: 56-66.
  • Joly DO, Messier F. The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves? Oecologia 2004; 140: 586-590.
  • Giles N. Predation risk and reduced foraging activity in fish: experiments with parasitized and non‐parasitized three‐spined sticklebacks, Gasterosteus aculeatus L. J Fish Biol 1987; 31(1): 37-44.
  • Heil M. Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts. Front Ecol Evol 2016: 4: 80.
  • Lyholt H, Buchmann K. Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Dis Aquat Organ 1996; 25: 169-173.
  • Gopko M, Mikheev VN, Taskinen J. Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behav Ecol Sociobiol 2017; 71: 68.
  • Lefevre T, Adamo SA, Biron DG, Misse D, Hughes D, Thomas F. Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host–parasite interactions. Adv Parasitol 2009; 68: 45-83.
  • Koçak OM, Atmaca HT, Terzi OS, Büyükkayaer S, Özdemir H, Uzunalioğlu T, ve ark. Deneysel kronik Toksoplazmoz fare modeli: beyin lezyonlarının davranış değişiklikleri ile ilişkilendirilmesi. Noro Psikiyatr Ars 2012; 49: 139-144.
  • Kristensson K, Mhlanga J, Bentivoglio M. Parasites and the brain: neuroinvasion, immunopathogenesis and neuronal dysfunctions. Curr Topics Microbiol Immunol 2002; 265: 227-257.
  • Morales J, Larralde C, Arteaga M, Govezensky T, Romano M, Morali G. Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 1996: 689-693.
  • Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology 1982; 85: 411-426.
  • Romig T, Lucius R, Frank W. Cerebral larvae in the second intermediate host of Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium hospes looss, 1907 (Trematodes, Dicrocoeliidae). Z Parasitenkd 1980; 63: 277-286.
  • Adamo SA. Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav Evol 2002; 60: 370-377.
  • Menigoz A, Hanelt B, Joly C, Ponton F, Thomas F, Biron DG. Water-seeking behavior in insects harboring hairworms: should the host collaborate? Behav Ecol 2005; 16: 656-660.
  • Lefevre T, Thomas F. Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol 2008; 8: 504-519.
  • Lefevre T, Thomas F, Schwartz A, Levashina E, Blandin S, Brizard JP ve ark. Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host. Proteomics 2007; 7: 1908-1915.
  • Lefevre T, Thomas F, Ravel S, Patrel D, Renault L, Le Bourligu L ve ark. Trypanosoma brucei brucei induces alteration in the head proteome of the tsetse fly vector Glossina palpalis gambiensis. Insect Mol Biol 2007; 16: 651-660.
  • Haine ER, Boucansaud K, Rigaud T. Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society B: Biological Sciences 2005; 272: 2505-2510.

Effects of parasites on host behavior

Year 2024, , 164 - 173, 15.06.2024
https://doi.org/10.33188/vetheder.1353693

Abstract

Parasites and their hosts have co-existed for many years in the evolutionary process and have developed various defence mechanisms against each other. Behaviour changes may occur in the host depending on where the parasite settles. Behaviour changes make it easier for the parasite to complete its life cycle, increasing the chance of infection and adaptation to the host. This causes many changes in the host, such as behaviour, colour, morphology, and physiology. It also affects aggression, mating and reproduction, and parental behaviour. Physiological systems such as neural, endocrine, neuromodulator, and immunomodulatory systems play a significant role in these changes. Behavioural manipulations are generally observed in parasites with indirect life cycles, and the most important of these parasites are Dicrocoelium dendriticum and Toxoplasma gondii. In recent years, behavioural changes in parasite-infected animals have become very interesting in the scientific world, and many studies have been conducted on this subject. In this review, the studies on the subject are brought together, and the mechanisms of parasites causing these behavioural changes are tried to be explained with examples.

References

  • Poulin R. “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 1995; 25: 1371-1383.
  • Dobson A. The population biology of parasite-induced changes in host behavior. Q Rev Biol 1988; 63: 139-165.
  • Moore J. Parasites and the behavior of animals: Oxford University Press on Demand, Oxford; 2002.
  • Klein SL. Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 2003; 79: 441-449.
  • Bakker TC, Frommen JG, Thünken T. Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology 2017; 123: 779-784.
  • Kavaliers M, Colwell D, Ossenkopp K-P, Perrot-Sinal T. Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav Ecol Sociobiol 1997; 40: 373-384.
  • Edwards J. The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice. Anim Behav 1988; 36: 529-540.
  • Pittella JEH. Central nervous system involvement in experimental trypanosomiasis cruzi. Mem Inst Oswaldo Cruz 1991; 86: 141-145.
  • Kavaliers M, Colwell D, Choleris E. Analgesic responses of male mice exposed to the odors of parasitized females: effects of male sexual experience and infection status. Behav Neurosci 1998; 112: 1001.
  • Isseroff H, Sylvester PW, Held WA. Effects of Schistosoma mansoni on androgen regulated gene expression in the mouse. Mol Biochem Parasitol 1986; 18: 401-412.
  • Larralde C, Morales J, Terrazas I, Govezensky T, Romano M. Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol 1995; 52: 575-580.
  • Cox D, Holland C. The relationship between numbers of larvae recovered from the brain of Toxocara canis-infected mice and social behaviour and anxiety in the host. Parasitology 1998; 116: 579-594.
  • Berdoy M, Webster J, MacDonald D. The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 1995; 59: 605-614.
  • Willis C, Poulin R. Effects of the tapeworm Hymenolepis diminuta on maternal investment in rats. Can J Zool 1999; 77: 1001-1005.
  • Lin YC, Rikihisa Y, Kono H, Gu Y. Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Exp Parasitol 1990; 70: 344-352.
  • Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S. Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 2004; 15(6): 930-937.
  • Henderson D, Bird DM, Rau ME, Negro JJ. Mate choice in captive American kestrels, Falco sparverius, parasitized by a nematode, Trichinella pseudospiralis. Ethology 1995; 101: 112-120.
  • Korpimaki E, Tolonen P, Bennett GF. Blood parasites, sexual selection and reproductive success of European kestrels. Ecoscience 1995; 2(4): 335-343.
  • Johnson LL, Boyce MS. Female choice of males with low parasite loads in sage grouse. Bird parasite interactions Oxford University Press, Oxford. 1991: 377-388.
  • Richner H, Christe P, Oppliger A. Paternal investment affects prevalence of malaria. Proc Natl Acad Sci 1995; 92: 1192-1194.
  • Rätti O, Dufva R, Alatalo RV. Blood parasites and male fitness in the pied flycatcher. Oecologia 1993; 96: 410-414.
  • Buchanan KL, Catchpole C, Lewis J, Lodge A. Song as an indicator of parasitism in the sedge warbler. Anim Behav 1999; 57: 307-314.
  • Zuk M, Thornhill R, Ligon JD, Johnson K. Parasites and mate choice in red jungle fowl. Am Zool 1990; 30: 235-244.
  • Møller AP. Parasite load reduces song output in a passerine bird. Anim Behav 1991; 41: 723-730.
  • Dunlap KD, Schall JJ. Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 1995; 68: 608-621.
  • Dunlap KD, Church DR. Interleukin-1β reduces daily activity level in male lizards, Sceloporus occidentalis. Brain Behav Immun 1996; 10(1): 68-73.
  • Gill DE, Mock BA. Ecological and evolutionary dynamics of parasites: the case of Trypanosoma diemyctyli in the red-spotted newt Notophthalmus viridescens. In: Rollinson D, Anderson RM, editors. Ecology and genetics of host–parasite interactions. London: Academic Press 1985; 157–183.
  • Kennedy C, Endler J, Poynton S, McMinn H. Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 1987; 21: 291-295.
  • Bakker TC, Mundwiler B. Pectoral fin size in a fish species with paternal care: a condition‐dependent sexual trait revealing infection status. Freshw Biol 1999; 41: 543-551.
  • Barber I, Huntingford FA. The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 1995; 132(15-16): 1223-1240.
  • Berger CS, Laroche J, Maaroufi H, Martin, H, Moon KM, Landry CR, Aubin-Horth N. The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions. Parasit Vectors 2021; 14(1): 1-20.
  • Baer J, Gugele SM, Roch S, Brinker A. Stickleback mass occurrence driven by spatially uneven parasite pressure? Insights into infection dynamics, host mortality, and epizootic variability. Parasitol Res 2022; 121(6): 1607-1619.
  • Mulvey M, Aho J. Parasitism and mate competition: liver flukes in white-tailed deer. Oikos 1993: 187-192.
  • Cox DM, Holland CV. The relationship between numbers of larvae recovered from the brain of Toxocara canis-infected mice and social behaviour and anxiety in the host. Parasitol 1998; 116(6): 579-594.
  • Poulin R. Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav. 41: Elsevier 2010; 151-186.
  • Aeby G. Trade-offs for the butterflyfish, Chaetodon multicinctus, when feeding on coral prey infected with trematode metacercariae. Behav Ecol Sociobiol 2002; 52: 158-165.
  • Lafferty KD, Shaw JC. Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 2013; 216: 56-66.
  • Joly DO, Messier F. The distribution of Echinococcus granulosus in moose: evidence for parasite-induced vulnerability to predation by wolves? Oecologia 2004; 140: 586-590.
  • Giles N. Predation risk and reduced foraging activity in fish: experiments with parasitized and non‐parasitized three‐spined sticklebacks, Gasterosteus aculeatus L. J Fish Biol 1987; 31(1): 37-44.
  • Heil M. Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts. Front Ecol Evol 2016: 4: 80.
  • Lyholt H, Buchmann K. Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Dis Aquat Organ 1996; 25: 169-173.
  • Gopko M, Mikheev VN, Taskinen J. Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behav Ecol Sociobiol 2017; 71: 68.
  • Lefevre T, Adamo SA, Biron DG, Misse D, Hughes D, Thomas F. Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host–parasite interactions. Adv Parasitol 2009; 68: 45-83.
  • Koçak OM, Atmaca HT, Terzi OS, Büyükkayaer S, Özdemir H, Uzunalioğlu T, ve ark. Deneysel kronik Toksoplazmoz fare modeli: beyin lezyonlarının davranış değişiklikleri ile ilişkilendirilmesi. Noro Psikiyatr Ars 2012; 49: 139-144.
  • Kristensson K, Mhlanga J, Bentivoglio M. Parasites and the brain: neuroinvasion, immunopathogenesis and neuronal dysfunctions. Curr Topics Microbiol Immunol 2002; 265: 227-257.
  • Morales J, Larralde C, Arteaga M, Govezensky T, Romano M, Morali G. Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 1996: 689-693.
  • Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology 1982; 85: 411-426.
  • Romig T, Lucius R, Frank W. Cerebral larvae in the second intermediate host of Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium hospes looss, 1907 (Trematodes, Dicrocoeliidae). Z Parasitenkd 1980; 63: 277-286.
  • Adamo SA. Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav Evol 2002; 60: 370-377.
  • Menigoz A, Hanelt B, Joly C, Ponton F, Thomas F, Biron DG. Water-seeking behavior in insects harboring hairworms: should the host collaborate? Behav Ecol 2005; 16: 656-660.
  • Lefevre T, Thomas F. Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol 2008; 8: 504-519.
  • Lefevre T, Thomas F, Schwartz A, Levashina E, Blandin S, Brizard JP ve ark. Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host. Proteomics 2007; 7: 1908-1915.
  • Lefevre T, Thomas F, Ravel S, Patrel D, Renault L, Le Bourligu L ve ark. Trypanosoma brucei brucei induces alteration in the head proteome of the tsetse fly vector Glossina palpalis gambiensis. Insect Mol Biol 2007; 16: 651-660.
  • Haine ER, Boucansaud K, Rigaud T. Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society B: Biological Sciences 2005; 272: 2505-2510.
There are 54 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Parasitology
Journal Section INVITED PAPER / REVIEW
Authors

Elif Burcu Gençay 0000-0002-0621-3125

Cenk Soner Bölükbaş 0000-0002-4863-696X

Early Pub Date June 12, 2024
Publication Date June 15, 2024
Submission Date September 1, 2023
Acceptance Date December 19, 2023
Published in Issue Year 2024

Cite

Vancouver Gençay EB, Bölükbaş CS. Parazitlerin konak davranışlarına etkileri. Vet Hekim Der Derg. 2024;95(2):164-73.

Veteriner Hekimler Derneği Dergisi açık erişimli bir dergi olup, derginin yayın modeli Budapeşte Erişim Girişimi (BOAI) bildirisine dayanmaktadır. Yayınlanan tüm içerik, çevrimiçi ve ücretsiz olarak sunulan Creative Commons CC BY-NC 4.0 lisansı altında lisanslanmıştır. Yazarlar, Veteriner Hekimler Derneği Dergisi'nde yayınlanan eserlerinin telif haklarını saklı tutarlar.


Veteriner Hekimler Derneği / Turkish Veterinary Medical Society