Advertisement

Behavioral Ecology and Sociobiology

, Volume 68, Issue 2, pp 197–204 | Cite as

Do brain parasites alter host personality? — Experimental study in minnows

  • Jukka Kekäläinen
  • Yi-Te Lai
  • Anssi Vainikka
  • Ilkka Sirkka
  • Raine Kortet
Original Paper

Abstract

Despite that the existence of animal personalities is widely recognized, no consensus has been reached on the relative importance of different ecological factors behind their expression. Recently, it has been suggested that parasites may have a crucial role in shaping animal personalities, but only a very few studies have experimentally tested the idea. We infected Eurasian minnows (Phoxinus phoxinus) with the brain-encysted trematode parasite, Diplostomum phoxini, and studied whether infection could modify the personality of their hosts. Our results show that D. phoxini infection did not affect the mean levels of boldness, activity or exploration, but infected minnows showed higher repeatability in boldness and activity, and reduced repeatability in exploration. We also found that D. phoxini may be able to break the associations (behavioral syndromes) between behavioral traits, but that this effect may be dependent on parasite intensity. Furthermore, the effect of D. phoxini infection on personality of the hosts was found to be nonlinearly dependent on infection intensity. Taken together, our results suggest that D. phoxini parasites may shape the personality of their hosts, but that behavioral consequences of ecologically relevant infection levels may be rather subtle and easily remain undetected if only the mean trait expressions are compared.

Keywords

Activity Boldness Exploration Parasite Personality Phoxinus phoxinus 

Notes

Acknowledgments

We thank Prof. Ann Hedrick and three anonymous reviewers for comments on earlier version of the manuscript, Leena Koponen and Leena Pääkkönen for their help in the maintenance of minnows and Matti Heep for collecting the snails.

Ethical standards

All the experiments comply with current relevant Finnish legislations.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Barber I, Crompton DWT (1997a) The distribution of the metacercariae of Diplostomum phoxini in the brain of minnows, Phoxinus phoxinus. Folia Parasit 44:9–25Google Scholar
  2. Barber I, Crompton DWT (1997b) The ecology of Diplostomum phoxini infections in two minnow (Phoxinus phoxinus) populations in Scotland. J Helminthol 71:189–196PubMedCrossRefGoogle Scholar
  3. Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philos T Roy Soc B 365:4077–4088CrossRefGoogle Scholar
  4. Barber I, Hoare D, Krause J (2004) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165CrossRefGoogle Scholar
  5. Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc Lond B 274:755–761CrossRefGoogle Scholar
  6. Bell AM, Sih A (2007) Exposure to predation generates personality in three-spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834PubMedCrossRefGoogle Scholar
  7. Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B 267:1591–1594CrossRefGoogle Scholar
  8. Butler MW, Toomey MB, McGraw KJ, Rowe M (2012) Ontogenetic immune challenges shape adult personality in mallard ducks. Proc R Soc Lond B 279:326–333CrossRefGoogle Scholar
  9. Cézilly F, Favrat A, Perrot-Minnot M-J (2013) Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. J Exp Biol 216:27–35PubMedCrossRefGoogle Scholar
  10. Coats J, Poulin R, Nakagawa S (2010) The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147:367–382CrossRefGoogle Scholar
  11. Cote J, Dreiss A, Clobert J (2008) Social personality trait and fitness. Proc R Soc Lond B 275:2851–2858CrossRefGoogle Scholar
  12. Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739CrossRefGoogle Scholar
  13. Dezfuli BS, Capuano S, Simoni E, Giari L, Shinn AP (2007) Histopathological and ultrastructural observations of metacercarial infections of Diplostomum phoxini (Digenea) in the brain of minnows Phoxinus phoxinus. Dis Aquat Organ 75:51–59PubMedCrossRefGoogle Scholar
  14. Dingemanse NJ, Both C, Drent PJ, Tingbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852CrossRefGoogle Scholar
  15. Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of stickleback. J Anim Ecol 76:1128–1138PubMedCrossRefGoogle Scholar
  16. Dönges J (1969) Entwicklungs- und Lebensdauer von Metacercariaen. Z Parasitenkd 31:340–366PubMedCrossRefGoogle Scholar
  17. Eberhard WG (2000) Spider manipulation by a wasp larva. Nature 406:255–256PubMedCrossRefGoogle Scholar
  18. Fleurance G, Duncan P, Fritz H, Cabaret J, Cortet J, Gordon IJ (2007) Selection of feeding sites by horses at pasture: testing the anti-parasite theory. Appl Anim Behav Sci 108:288–301CrossRefGoogle Scholar
  19. Goodman BA, Johnson PTJ (2011) Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PLoS One 6:e20193PubMedCentralPubMedCrossRefGoogle Scholar
  20. Hammond-Tooke CA, Nakagawa S, Poulin R (2012) Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. Behaviour 149:601–622CrossRefGoogle Scholar
  21. Hart BL (1997) Behavioral defence. In: Clayton DH, Moore J (eds) Host–parasite evolution: General principles and avian models. Oxford University Press, Oxford, pp 57–77Google Scholar
  22. Jog M, Watve M (2005) Role of parasites and commensals in shaping host behaviour. Curr Sci 8:1184–1191Google Scholar
  23. Kavaliers M, Coldwell DD, Choleris E (2000) Parasites and behaviour: an ethnopharmacological perspective. Parasitol Today 16:464–468PubMedCrossRefGoogle Scholar
  24. Koprivnikar J, Gibson CH, Redfern JC (2012) Infectious personalities: behavioural syndromes and disease risk in larval amphibians. Proc R Soc Lond B 279:1544–1550CrossRefGoogle Scholar
  25. Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458PubMedCrossRefGoogle Scholar
  26. Lafferty KD, Morris AK (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397CrossRefGoogle Scholar
  27. Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66PubMedCrossRefGoogle Scholar
  28. Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav R 26:91–104CrossRefGoogle Scholar
  29. Lennartz RC (2008) The role of extramaze cues in spontaneous alternation in a plus-maze. Learn Behav 36:138–144PubMedCrossRefGoogle Scholar
  30. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  31. Lozano GA (1991) Optimal foraging theory: a possible role for parasites. Oikos 60:391–395CrossRefGoogle Scholar
  32. Maure F, Brodeur J, Hughes D, Thomas F (2013) How much energy should manipulative parasites leave to their hosts to ensure altered behaviours? J Exp Biol 216:43–46PubMedCrossRefGoogle Scholar
  33. Maximino C, de Brito TM, de Mattos Dias CAG, Gouveia A Jr, Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5:221–228CrossRefGoogle Scholar
  34. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456CrossRefGoogle Scholar
  35. Niemelä PT, Vainikka A, Forsman JT, Loukola OJ, Kortet R (2013) How does variation in the environment and individual cognition explain the existence of consistent behavioural differences? Ecol Evol 3:457–464PubMedCentralPubMedCrossRefGoogle Scholar
  36. Niezgoda M, Hanlon CA, Rupprecht CE (2002) Animal rabies. In: Jackson AC, Wunner WH (eds) Rabies. Academic Press, New York, pp 163–218Google Scholar
  37. Poulin R (2000) Manipulation of host behavior by parasites: a weakening paradigm? Proc R Soc B Lond 267:787–792CrossRefGoogle Scholar
  38. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, PrincetonGoogle Scholar
  39. Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav 41:151–186Google Scholar
  40. Poulin R (2013) Parasite manipulation of host personality and behavioural syndromes. J Exp Biol 216:18–26PubMedCrossRefGoogle Scholar
  41. Poulin R, Thomas F (1999) Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitol Today 15:28–32PubMedCrossRefGoogle Scholar
  42. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318PubMedCrossRefGoogle Scholar
  43. Rees G (1955) The adult and Diplostomulum stage (Diplostomulum phoxini (Faust)) of Diplostomum pelmatoides Dubois and an experimental demonstration of part of the life cycle. Parasitology 45:295–312PubMedCrossRefGoogle Scholar
  44. Rohr JR, Swan A, Raffel TR, Hudson PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159:447–454PubMedCrossRefGoogle Scholar
  45. Schmid-Hempel P (2009) Parasites – the new frontier: celebrating Darwin 200. Biol Lett 5:625–627PubMedCentralPubMedCrossRefGoogle Scholar
  46. Seppälä O, Karvonen A, Valtonen ET (2005) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim Behav 70:889–894CrossRefGoogle Scholar
  47. Shaw JC, Korzan WJ, Carpenter RE, Kuris AM, Lafferty KD, Summers CH, Øverli Ø (2009) Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc R Soc Lond B 276:1137–1146CrossRefGoogle Scholar
  48. Shirakashi S, Goater CP (2001) Brain-encysting parasites affect visually-mediated behaviours of fathead minnows. Ecoscience 8:289–293Google Scholar
  49. Shirakashi S, Goater CP (2002) Intensity-dependent alteration of minnow (Pimephales promelas) behavior by a brain-encysting trematode. J Parasitol 88:1071–1074PubMedGoogle Scholar
  50. Shirakashi S, Goater CP (2005) Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology 130:177–183PubMedCrossRefGoogle Scholar
  51. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277PubMedCrossRefGoogle Scholar
  52. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289PubMedCrossRefGoogle Scholar
  53. Smith KL, Miner JG, Wiegmann DD, Newman SP (2009) Individual differences in exploratory and antipredator behaviour in juvenile smallmouth bass (Micropterus dolomieu). Behaviour 146:283–294CrossRefGoogle Scholar
  54. Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325PubMedCrossRefGoogle Scholar
  55. Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn & Bacon, BostonGoogle Scholar
  56. Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199CrossRefGoogle Scholar
  57. van Houte S, Ros VID, van Oers MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol 22:3458–3475PubMedCrossRefGoogle Scholar
  58. Vance SA (1996) Morphological and behavioural sex reversal in mermithid-infected mayflies. Proc R Soc Lond B 263:907–912CrossRefGoogle Scholar
  59. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137CrossRefGoogle Scholar
  60. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–585PubMedCrossRefGoogle Scholar
  61. Yanoviak SP, Kaspari M, Dudley R, Poinar G Jr (2008) Parasite-induced fruit mimicry in a tropical canopy ant. Am Nat 171:536–544PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jukka Kekäläinen
    • 1
  • Yi-Te Lai
    • 1
  • Anssi Vainikka
    • 1
    • 2
  • Ilkka Sirkka
    • 1
  • Raine Kortet
    • 1
  1. 1.Department of BiologyUniversity of Eastern FinlandJoensuuFinland
  2. 2.Department of BiologyUniversity of OuluUniversity of Oulu, OuluFinland

Personalised recommendations