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

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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.

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References

  • Barber I, Crompton DWT (1997a) The distribution of the metacercariae of Diplostomum phoxini in the brain of minnows, Phoxinus phoxinus. Folia Parasit 44:9–25

    Google Scholar 

  • Barber I, Crompton DWT (1997b) The ecology of Diplostomum phoxini infections in two minnow (Phoxinus phoxinus) populations in Scotland. J Helminthol 71:189–196

    Article  CAS  PubMed  Google Scholar 

  • Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philos T Roy Soc B 365:4077–4088

    Article  Google Scholar 

  • Barber I, Hoare D, Krause J (2004) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165

    Article  Google Scholar 

  • Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc Lond B 274:755–761

    Article  Google Scholar 

  • Bell AM, Sih A (2007) Exposure to predation generates personality in three-spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834

    Article  PubMed  Google Scholar 

  • Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B 267:1591–1594

    Article  CAS  Google Scholar 

  • Butler MW, Toomey MB, McGraw KJ, Rowe M (2012) Ontogenetic immune challenges shape adult personality in mallard ducks. Proc R Soc Lond B 279:326–333

    Article  Google Scholar 

  • Cézilly F, Favrat A, Perrot-Minnot M-J (2013) Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. J Exp Biol 216:27–35

    Article  PubMed  Google Scholar 

  • Coats J, Poulin R, Nakagawa S (2010) The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147:367–382

    Article  Google Scholar 

  • Cote J, Dreiss A, Clobert J (2008) Social personality trait and fitness. Proc R Soc Lond B 275:2851–2858

    Article  CAS  Google Scholar 

  • Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739

    Article  Google Scholar 

  • 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 75:51–59

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, Tingbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852

    Article  Google Scholar 

  • 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 76:1128–1138

    Article  PubMed  Google Scholar 

  • Dönges J (1969) Entwicklungs- und Lebensdauer von Metacercariaen. Z Parasitenkd 31:340–366

    Article  PubMed  Google Scholar 

  • Eberhard WG (2000) Spider manipulation by a wasp larva. Nature 406:255–256

    Article  CAS  PubMed  Google Scholar 

  • 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 108:288–301

    Article  Google Scholar 

  • 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:e20193

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hammond-Tooke CA, Nakagawa S, Poulin R (2012) Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. Behaviour 149:601–622

    Article  Google Scholar 

  • Hart BL (1997) Behavioral defence. In: Clayton DH, Moore J (eds) Host–parasite evolution: General principles and avian models. Oxford University Press, Oxford, pp 57–77

    Google Scholar 

  • Jog M, Watve M (2005) Role of parasites and commensals in shaping host behaviour. Curr Sci 8:1184–1191

    Google Scholar 

  • Kavaliers M, Coldwell DD, Choleris E (2000) Parasites and behaviour: an ethnopharmacological perspective. Parasitol Today 16:464–468

    Article  CAS  PubMed  Google Scholar 

  • Koprivnikar J, Gibson CH, Redfern JC (2012) Infectious personalities: behavioural syndromes and disease risk in larval amphibians. Proc R Soc Lond B 279:1544–1550

    Article  Google Scholar 

  • Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458

    Article  PubMed  Google Scholar 

  • Lafferty KD, Morris AK (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397

    Article  Google Scholar 

  • Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66

    Article  PubMed  Google Scholar 

  • Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav R 26:91–104

    Article  CAS  Google Scholar 

  • Lennartz RC (2008) The role of extramaze cues in spontaneous alternation in a plus-maze. Learn Behav 36:138–144

    Article  PubMed  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Lozano GA (1991) Optimal foraging theory: a possible role for parasites. Oikos 60:391–395

    Article  Google Scholar 

  • 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 216:43–46

    Article  PubMed  Google Scholar 

  • Maximino C, de Brito TM, de Mattos Dias CAG, Gouveia A Jr, Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5:221–228

    Article  Google Scholar 

  • 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 26:450–456

    Article  Google Scholar 

  • 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 3:457–464

    Article  PubMed Central  PubMed  Google Scholar 

  • Niezgoda M, Hanlon CA, Rupprecht CE (2002) Animal rabies. In: Jackson AC, Wunner WH (eds) Rabies. Academic Press, New York, pp 163–218

    Google Scholar 

  • Poulin R (2000) Manipulation of host behavior by parasites: a weakening paradigm? Proc R Soc B Lond 267:787–792

    Article  CAS  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

    Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav 41:151–186

    Google Scholar 

  • Poulin R (2013) Parasite manipulation of host personality and behavioural syndromes. J Exp Biol 216:18–26

    Article  PubMed  Google Scholar 

  • Poulin R, Thomas F (1999) Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitol Today 15:28–32

    Article  CAS  PubMed  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • 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 45:295–312

    Article  CAS  PubMed  Google Scholar 

  • Rohr JR, Swan A, Raffel TR, Hudson PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159:447–454

    Article  PubMed  Google Scholar 

  • Schmid-Hempel P (2009) Parasites – the new frontier: celebrating Darwin 200. Biol Lett 5:625–627

    Article  PubMed Central  PubMed  Google Scholar 

  • Seppälä O, Karvonen A, Valtonen ET (2005) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Anim Behav 70:889–894

    Article  Google Scholar 

  • 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 276:1137–1146

    Article  CAS  Google Scholar 

  • Shirakashi S, Goater CP (2001) Brain-encysting parasites affect visually-mediated behaviours of fathead minnows. Ecoscience 8:289–293

    Google Scholar 

  • Shirakashi S, Goater CP (2002) Intensity-dependent alteration of minnow (Pimephales promelas) behavior by a brain-encysting trematode. J Parasitol 88:1071–1074

    PubMed  Google Scholar 

  • Shirakashi S, Goater CP (2005) Chronology of parasite-induced alteration of fish behaviour: effects of parasite maturation and host experience. Parasitology 130:177–183

    Article  CAS  PubMed  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Smith KL, Miner JG, Wiegmann DD, Newman SP (2009) Individual differences in exploratory and antipredator behaviour in juvenile smallmouth bass (Micropterus dolomieu). Behaviour 146:283–294

    Article  Google Scholar 

  • Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  PubMed  Google Scholar 

  • Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn & Bacon, Boston

    Google Scholar 

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199

    Article  Google Scholar 

  • van Houte S, Ros VID, van Oers MM (2013) Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Mol Ecol 22:3458–3475

    Article  PubMed  Google Scholar 

  • Vance SA (1996) Morphological and behavioural sex reversal in mermithid-infected mayflies. Proc R Soc Lond B 263:907–912

    Article  Google Scholar 

  • Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137

    Article  Google Scholar 

  • Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–585

    Article  CAS  PubMed  Google Scholar 

  • Yanoviak SP, Kaspari M, Dudley R, Poinar G Jr (2008) Parasite-induced fruit mimicry in a tropical canopy ant. Am Nat 171:536–544

    Article  CAS  PubMed  Google Scholar 

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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.

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Authors and Affiliations

  1. Department of Biology, University of Eastern Finland, P.O. Box 111, Joensuu, 80101, Finland

    Jukka Kekäläinen, Yi-Te Lai, Anssi Vainikka, Ilkka Sirkka & Raine Kortet

  2. Department of Biology, University of Oulu, P.O. Box 3000, 90014, University of Oulu, Oulu, Finland

    Anssi Vainikka

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  1. Jukka Kekäläinen
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  2. Yi-Te Lai
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Correspondence to Jukka Kekäläinen.

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Communicated by J. Lindström

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Kekäläinen, J., Lai, YT., Vainikka, A. et al. Do brain parasites alter host personality? — Experimental study in minnows. Behav Ecol Sociobiol 68, 197–204 (2014). https://doi.org/10.1007/s00265-013-1634-2

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  • DOI: https://doi.org/10.1007/s00265-013-1634-2

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