Journal of Exotic Pet Medicine
Volume 18, Issue 4 , Pages 254-265 , October 2009

Behavioral Effects of Parasitism in Animals

  • Kristel-Marie Nerissa Ramnath, BSc (Hons), MSc

      Affiliations

    • Corresponding Author InformationAddress correspondence to: Kristel-Marie Nerissa Ramnath, BSc (Hons), MSc, Animal Behaviourist and Welfarist, c/o Best Pets Animal Behaviour Service, 48 Third Street, Sun Valley, Lower Santa Cruz, Trinidad and Tobago, West Indies

References 

  1. Price PW. Evolutionary Biology of Parasites. New Jersey: Princeton University Press; 1980;
  2. Zimmer C. Parasite Rex. New York: The Free Press; 2000;
  3. Beckage NE. Parasites and Pathogens—Effects on Host Hormones and Behaviour. London: Springer; 1997;
  4. Moore J. Parasites and the Behaviour of Animals. Oxford: Oxford University Press; 2002;
  5. Chapman JL, Reiss MJ. Ecology Principles and Applications. Cambridge: Cambridge University Press; 1999;
  6. Barnard CJ, Behnke JM. Parasitism and Host Behaviour. London: Taylor and Francis; 1990;
  7. Jog M, Watve M. Role of parasites and commensals in shaping host behavior. Curr Sci. 2005;89(7):1184–1191
  8. Van Valen L. A new evolutionary law. Evol Theory. 1973;1:1–30
  9. Windsor DA. Most of the species on earth are parasites. Int J Parasitol. 1998;28:1939–1941
  10. Seppala O. Host manipulation by parasites: adaptation to enhance transmission? (Jyvaskyla Studies in Biological and Environmental Science). Jyväskylä, Finland: Jyväskylä University Printing House; 2005;
  11. Poulin R. Evolutionary Ecology of Parasites: From Individuals to Communities. London: Chapman and Hall; 1998;
  12. Combes C. Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago: The University of Chicago Press; 2001;
  13. Sapolsky R. Bugs in the brain. Sci Amer. 2003;288:94–97
  14. Lafferty KD. The evolution of trophic transmission. Parasitol Today. 1999;15:111–115
  15. Moore J, Gotelli NJ. Phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In:  Barnard CJ,  Behnke JM editor. Parasitism and Host Behaviour. London: Taylor & Francis; 1990;p. 193–233
  16. Holmes JC, Bethel WM. In:  Canning EV,  Wright CA editor. Behavioural Aspects of Parasite Transmission. London: Linnean Society of London; 1972;p. 123–143
  17. Webster JP. Rats, cats, people and parasites: the impact of latent toxoplasmosis on behavior. Microbes Infect. 2001;3:1037–1045
  18. Hay J, Aitken PP, Hutchinson WM, et al. The effect of congenital and adult-acquired Toxoplasma infections on the motor-performance of mice. Ann Trop Med Parasitol. 1983;77:261–277
  19. Hay J, Aitken PP, Hair DM, et al. The effect of congenital Toxoplasma infection of mouse activity and relative preference for exposed areas over a series of trials. Ann Trop Med Parasitol. 1984;78:611–618
  20. Webster JP, Brunton CFA, Macdonald DW. Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology. 1994;109:37–43
  21. Berdoy M, Webster JP, Macdonald DW. Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B Biol Soc. 2000;267:1591–1594
  22. Mehlhorn H, Aspock H, Behr C, et al. Encyclopedia of Parasitology: N-Z. (ed) In: London: Springer; 2008;p. 1573
  23. Stibbs HH. Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol. 1985;79:153–157
  24. Benjamin J, Li L, Patterson C, et al. Population and familial association between the D4 dopamine receptor gene and measures of novelty seeking. Nat Genet. 1996;12:81–84
  25. Lee IH, Cheng CC, Yang YK, et al. Correlation between striatal dopamine D2 receptor density and neuroticism in community volunteers. Psychiatry Res. 2005;138:259–264
  26. Lafferty KD. Can the common brain parasite, Toxoplasma gondii, influence human culture?. Proc R Soc Lond B Biol Sci. 2006;273:2749–2755
  27. Combes C, Fournier A, Mone H, et al. Behaviors in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology. 1994;109:S3–S13
  28. Lafferty KD, Morris AK. Altered behavior of parasitised killifish increases susceptibility to predation by bird final hosts. Ecology. 1996;77:1390–1397
  29. Lafferty KD. Ecosystem consequences of fish parasites. J Fish Biol. 2008;73:2083–2093
  30. Crowden AE, Broom DM. Effects of the eye fluke Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav. 1980;28:287–294
  31. Seppala O, Karvonen A, Valtonen ET. Impaired crypsis of fish infected with a trophically transmitted parasite. Anim Behav. 2005;70:895–900
  32. Giles N. Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Anim Behav. 1983;31:1192–1194
  33. Barber I, Huntingford FA, Crompton DWT. The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. J Fish Biol. 1995;47:524–536
  34. Moss J, Vaughn M. Activation of adenylate cyclase by choleragen. Annu Rev Biochem. 1979;48:581–600
  35. Hudson PJ, Dobson AP, Newborn D. Do parasites make prey vulnerable to predation? (Red grouse and parasites). J Anim Ecol. 1992;61:681–692
  36. Zuk M, Rotenberry JT, Simmons LW. Calling songs of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evol. 1998;52:166–171
  37. Couzens D. How cruel is the cuckoo?. BBC Wildl. 2008;26(12):54–59
  38. Lafferty KD, Dobson AP, Kuris AM. Parasites dominate food web links. Ecology. 2006;103(3):11211–11216
  39. Wakelin D. Immunity to Parasites: How Parasitic Infections Are Controlled. Cambridge: Cambridge University Press; 1996;
  40. Read A. The evolution of virulence. Trends Microbiol. 1994;2(3):73–76
  41. Hutchings MR, Athanasiadou S, Kyriazakis I, et al. Can animals use foraging behavior to combat parasites?. Proc Nutr Soc. 2003;62(2):361–370
  42. Poulin R, Fitzgerald GJ. Risk of parasitism and microhabitat selection in juvenile sticklebacks. Can J Zool. 1989;67:14–18
  43. Dugatkin LA, Fitzgerald GJ, Lavoie J. Juvenile three-spined sticklebacks avoid parasitised conspecifics. Environ Biol Fishes. 1994;39:215–218
  44. Möller AP. Flight distance and blood parasites in birds. Behav Ecol. 2008;19:1305–1313
  45. Piersma T. Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure?. Oikos. 1997;80(3):623–631
  46. Lozano GA. Optimal foraging theory: a possible route for parasites. Oikos. 1991;60:391–395
  47. Freeland WJ. Mangabey (Cercocebus albegina) movement patterns in relation to food availability and fecal contamination. Ecology. 1980;61:1297–1303
  48. Watve MG. Ecology of host-parasite interactions in a wild mammalian host community in Mudumalai, Southern India. Ph.D. Thesis Bangalore: Indian Institute of Science; 1992;
  49. Dickman CR, Doncaster CP. Responses of small mammals to red fox (Vulpes vulpes) odour. J Zool Lond. 1984;204:521–531
  50. Murray MD. Influence of host behaviour on some ectoparasites of birds and mammals. In:  Barnard CJ,  Behnke JM editor. Parasitism and Host Behaviour. London: Taylor & Francis; 1990;p. 290–315
  51. Hart BL. Behavioural defense. In:  Clayton DH,  Moore J editor. Host-parasite evolution: general principles and avian models. Oxford: Oxford University Press; 1997;p. 59–77
  52. Hart BL, Hart LA. Fly switching by Asian elephants: tool use to control parasites. Anim Behav. 1994;48:35–45
  53. Dunbar R. Functional significance of social grooming in primates. Folia Primatol. 1991;57:121
  54. Hawlena H, Bashary D, Abramsky Z, et al. Benefits, costs and constraints of anti-parasitic grooming in adult and juvenile rodents. Ethol. 2007;113(4):394–402
  55. Barber I, Hoare D, Krause J. Effects of parasites on fish behavior: a review and evolutionary perspective. Rev Fish Biol Fisheries. 2000;10:131–165
  56. Lawrence K. Snakes. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 179–185
  57. Webb RA. Chinchillas. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 19–23
  58. Brancker MW. Primates. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 99–105
  59. Gregory MW. Hedgehogs. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 54–58
  60. Jackson OF, Lawrence K. Chelonians. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 142–160
  61. Turner T. Cagebirds. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 106–123
  62. Keymer IF. Pigeons. In:  Cooper JE,  Hutchison MF,  Jackson OF, et al. editor. Manual of Exotic Pets. Cheltenham: British Small Animal Veterinary Association; 1985;p. 124–135
  63. Humphreys PN. Wet feather in a duck associated with Holomenopon leucoxanthum. Vet Rec. 1975;88:417
  64. Butler JM, Roper TJ. Ectoparasites and sett use in European badgers. Anim Behav. 1996;52(3):621–629
  65. Tripet F, Glaser M, Richner H. Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas. Ibis. 2002;144(3):461–469
  66. Taylor MI, Turner GF, Robinson RL, et al. Sexual selection, parasites and bower height skew in a bower-building cichlid fish. Anim Behav. 1998;56:379–384
  67. Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites?. Science. 1982;218:384–386
  68. Zahavi A. Mate selection: a selection for a handicap. J Theor Biol. 1975;53:205–214
  69. Ezenwa VO, Jolles AE. Horns honestly advertise parasite infection in male and female African buffalo. Anim Behav. 2008;75:2013–2021
  70. Milinski M, Bakker TCM. Female sticklebacks use male colouration in mate choice and hence avoid parasitised males. Nature. 1990;344:330–333
  71. Houde AE, Torio AJ. Effect of parasitic infection on male colour pattern and female choice in guppies. Behav Ecol. 1992;3:346–351
  72. Hart BJ, Korinek E, Brennan P. Post-copulatory genital grooming in male rats: prevention of sexually transmitted infections. Physiol Behav. 1987;41:321–325
  73. Nunn CL. Behavioural defences against sexually transmitted diseases in primates. Anim Behav. 2003;66:37–48
  74. Newton PN, Nishida T. Possible buccal administration of herbal drugs by wild chimpanzees. Anim Behav. 1990;39:798–801
  75. Sack DA, Shamsul ATM, Huq A. Is protection against shigellosis induced by natural infection with Plesiomonas shigelloides?. Lancet. 1994;343:1413–1415
  76. Waage JK. How the zebra got its stripes—biting flies as selective agents in the evolution of zebra colouration. J Entomol Soc S Afr. 1981;44:351–358
  77. Kruuk H. A Study of Predation and Social Behavior in the Spotted Hyena. Chicago: University of Chicago Press; 1972;
  78. Rozsa L. Spite, xenophobia and collaboration between hosts and parasites. Oikos. 2000;91:396–400
  79. Hochberg ME. Viruses as costs to gregarious feeding behavior in the Lepidoptera. Oikos. 1991;61:291–296
  80. Loehle C. Social barriers to pathogen transmission in wild animal populations. Ecology. 1995;76:326–335
  81. Nunn CL, Dokey AT. Ranging patterns and parasitism in primates. Proc R Soc Lond B Biol Sci. 2006;2:351–354
  82. Mooring MS, Hart BL. Animal grouping for protection from parasites; selfish herd and encounter dilution effects. Behaviour. 1992;123:173–193
  83. Freeland WJ. Blood-sucking flies and primate polyspecific associations. Nature. 1977;269:801–802
  84. Wilson K, Knell R, Boots M, et al. Group living and investment in immune defence: an interspecific analysis. J Anim Ecol. 2003;72:133–143
  85. Cote IM, Poulin R. Parasitism and group size in social animals: a meta-analysis. Behav Ecol. 1995;6(2):159–165
  86. Pagel M, Bodmer W. A naked ape would have fewer parasites. Proc R Soc Lond B Biol Sci. 2003;270(Suppl):S117–S119
  87. Monaghan P, Wood-Gush DGM. Managing the behaviour of animals. In: London: Chapman and Hall; 1990;p. 257
  88. Smith LA, White PCL, Marion G, et al. Livestock grazing behaviour and inter- versus intra-specific disease risk via the faecal-oral route. Behav Ecol. 2009;20(2):426–432
  89. Dailey MD. Parasitic diseases. In:  Dierauf LA,  Gulland FMD editor. CRC Handbook of Marine Mammal Medicine. (ed 2). Boca Raton, Florida: CRC Press LLC; 2001;p. 357–383
  90. Norval RAI. Host susceptibility to infestation with Amblyomma hebraeum. Insect Sci Applic. 1992;13:489–494
  91. Nunn CL, Thrall PH, Stewart K, et al. Emerging infectious diseases and animal social systems. Evol Ecol. 2008;22:519–543
  92. Kavaliers M, Colwell DD, Choleris E. Parasites and behavior: an ethnopharmacological analysis and biomedical implications. Neurosci Biobehav Rev. 1999;23(7):1037–1045
  93. Hernandez-Divers SJ. Clinical aspects of reptile behavior. Vet Clin North Am Exotic Anim Pract. 2001;4(3):599–612

PII: S1557-5063(09)00157-8

doi: 10.1053/j.jepm.2009.10.004

Journal of Exotic Pet Medicine
Volume 18, Issue 4 , Pages 254-265 , October 2009