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Increased behavioural lateralization in parasitized coral reef fish

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Abstract

Preferential use of one side of the body for cognitive or behavioural tasks (lateralization) is common in many animals, including humans. However, few studies have demonstrated whether lateralization is phenotypically plastic, and varies depending on the ecological context. We studied lateralization (measured as a turning preference) in the bridled monocle bream (Scolopsis bilineatus). This coral reef fish is commonly infected by a large, ectoparasitic isopod (Anilocra nemipteri) that attaches to the left or right side of its host’s head. Fish that were parasitized showed no turning bias with respect to the side on which the parasite had attached. On average, however, parasitised fish were significantly more lateralized (i.e. had a strong side bias) than unparasitized fish. The extent of lateralization declined significantly when we experimentally removed the parasite. Our results indicate that lateralization can vary with the ecological context. One possible explanation is that lateralization shortens the response time until fish flee after encountering a predator. A stronger side bias might be advantageous for parasitized individuals to overcome their recently documented lower maximum swimming speed.

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References

  • Adlard R, Lester R (1994) Dynamics of the interaction between the parasitic isopod, Anilocra pomacentri, and the coral reef fish, Chromis nitida. Parasitology 109:311–324

    Article  PubMed  Google Scholar 

  • Binning SA, Roche DG, Layton C (2013) Ectoparasites increase swimming costs in a coral reef fish. Biol Lett 9:20120927

    Article  PubMed  Google Scholar 

  • Bisazza A, Dadda M (2005) Enhanced schooling performance in lateralized fishes. Proc R Soc Lond B 272:1677–1681

    Article  Google Scholar 

  • Bisazza A, Cantalupo C, Vallortigara G (1997a) Lateral asymmetries during escape behavior in a species of teleost fish (Jenynsia lineata). Physiol Behav 61:31–35

    Article  PubMed  CAS  Google Scholar 

  • Bisazza A, Pignatti R, Vallortigara G (1997b) Detour tests reveal task- and stimulus-specific behavioural lateralization in mosquitofish (Gambusia holbrooki). Behav Brain Res 89:237–242

    Article  PubMed  CAS  Google Scholar 

  • Bisazza A, Facchin L, Pignatti R, Vallortigara G (1998) Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav Brain Res 91:157–164

    Article  PubMed  CAS  Google Scholar 

  • Brown C, Gardner C, Braithwaite VA (2004) Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi. Proc R Soc Lond B 271:S455–S457

    Article  Google Scholar 

  • Dadda M, Bisazza A (2006a) Does brain asymmetry allow efficient performance of simultaneous tasks? Anim Behav 72:523–529

    Article  Google Scholar 

  • Dadda M, Bisazza A (2006b) Lateralized female topminnows can forage and attend to a harassing male simultaneously. Behav Ecol 17:358–363

    Article  Google Scholar 

  • Dadda M, Zandonà E, Agrillo C, Bisazza A (2009) The costs of hemispheric specialization in a fish. Proc R Soc Lond B 276:4399–4407

    Article  Google Scholar 

  • Dadda M, Koolhaas WH, Domenici P (2010) Behavioural asymmetry affects escape performance in a teleost fish. Biol Lett 6:414–417

    Article  PubMed  Google Scholar 

  • Domenici P (2002) The visually mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar Freshw Behav Physiol 35:87–110

    Article  Google Scholar 

  • Domenici P, Allan B, McCormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8:78–81

    Article  PubMed  CAS  Google Scholar 

  • Eaton RC, Lee RKK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63:467–485

    Article  PubMed  CAS  Google Scholar 

  • Farrell AP (2007) Cardiorespiratory performance during prolonged swimming tests with salmonids: a perspective on temperature effects and potential analytical pitfalls. Philos T Roy Soc B 362:2017–2030

    Article  CAS  Google Scholar 

  • Fogelman RM, Kuris AM, Grutter AS (2009) Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus. Int J Parasitol 39:577–583

    Article  PubMed  Google Scholar 

  • Geuze RH, Schaafsma SM, Lust JM, Bouma A, Schiefenhövel W, Groothuis TGG (2012) Plasticity of lateralization: schooling predicts hand preference but not hand skill asymmetry in a non-industrial society. Neuropsychologia 50:612–620

    Article  PubMed  Google Scholar 

  • Gotanda KM, Turgeon K, Kramer DL (2009) Body size and reserve protection affect flight initiation distance in parrotfishes. Behav Ecol Sociobiol 63:1563–1572

    Article  Google Scholar 

  • Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30

    Article  Google Scholar 

  • Heatwole SJ, Fulton CJ (2012) Behavioural flexibility in reef fishes responding to a rapidly changing wave environment. Mar Biol 160:677–689

    Article  Google Scholar 

  • Hori M (1993) Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216–219

    Article  PubMed  CAS  Google Scholar 

  • Jozet-Alves C, Viblanc VA, Romagny S, Dacher M, Healy SD, Dickel L (2012) Visual lateralization is task and age dependent in cuttlefish, Sepia officinalis. Anim Behav 83:1313–1318

    Article  Google Scholar 

  • Lee HJ, Kusche H, Meyer A (2012) Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry. PLoS One 7:e44670

    Article  PubMed  CAS  Google Scholar 

  • Mandel JT, Ratcliffe JM, Cerasale DJ, Winkler DW (2008) Laterality and flight: concurrent tests of side-bias and optimality in flying tree swallows. PLoS One 3:e1748

    Article  PubMed  Google Scholar 

  • Östlund-Nilsson S, Curtis L, Nilsson GE, Grutter AS (2005) Parasitic isopod Anilocra apogonae, a drag for the cardinal fish Cheilodipterus quinquelineatus. Mar Ecol Prog Ser 287:209–216

    Article  Google Scholar 

  • Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A Mol Integr Physiol 131:41–50

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2010) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. (http://www.R-project.org). Accessed 22 Apr 2010

  • Reddon AR, Balshine S (2010) Lateralization in response to social stimuli in a cooperatively breeding cichlid fish. Behav Process 85:68–71

    Article  Google Scholar 

  • Reddon AR, Hurd PL (2009) Individual differences in cerebral lateralization are associated with shy–bold variation in the convict cichlid. Anim Behav 77:189–193

    Article  Google Scholar 

  • Roche DG, Strong LE, Binning SA (2013a) Prevalence of the parasitic cymothoid isopod Anilocra nemipteri on its fish host at Lizard Island, Great Barrier Reef. Aust J Zool 60:330–333

    Article  Google Scholar 

  • Roche DG, Binning SA, Bosiger Y, Johansen JL, Rummer JL (2013b) Finding the best estimates of metabolic rates in a coral reef fish. J Exp Biol 216:2103–2110

    Article  PubMed  Google Scholar 

  • Rogers LJ, Andrew RJ (2002) Comparative vertebrate lateralization. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc Lond B 271:S420–S422

    Article  Google Scholar 

  • Schaafsma SM, Riedstra BJ, Pfannkuche KA, Bouma A, Groothuis TGG (2009) Epigenesis of behavioural lateralization in humans and other animals. Philos T Roy Soc B 364:915–927

    Article  CAS  Google Scholar 

  • Sovrano VA, Dadda M, Bisazza A (2005) Lateralized fish perform better than nonlateralized fish in spatial reorientation tasks. Behav Brain Res 163:122–127

    Article  PubMed  Google Scholar 

  • Stewart WJ, Cardenas GS, McHenry MJ (2013) Zebrafish larvae evade predators by sensing water flow. J Exp Biol 216:388–398

    Article  PubMed  Google Scholar 

  • Svendsen JC, Tudorache C, Jordan AD, Steffensen JF, Aarestrup K, Domenici P (2010) Partition of aerobic and anaerobic swimming costs related to gait transitions in a labriform swimmer. J Exp Biol 213:2177–2183

    Article  PubMed  Google Scholar 

  • Takeuchi Y, Hori M, Myint O, Kohda M (2010) Lateral bias of agonistic responses to mirror images and morphological asymmetry in the Siamese fighting fish (Betta splendens). Behav Brain Res 208:106–111

    Article  PubMed  Google Scholar 

  • Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633

    PubMed  Google Scholar 

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Acknowledgments

We thank the Lizard Island staff, C. Layton and C. Juan, for field assistance. The associate editor and two anonymous reviewers provided helpful comments on a previous version of the manuscript. DGR and SAB were supported by the Ian Potter Foundation Doctoral Fellowships at the Lizard Island Research Station (a facility of the Australian Museum), the Australian National University, the ARC Centre of Excellence for Coral Reef Studies, the Natural Sciences and Engineering Research Council of Canada and Total Diving Montreal.

Ethical standards

Research was conducted under the Australian National University animal ethics permit A2012/02 and the Great Barrier Reef Marine Parks Authority collection permit G12/34805.1. Animals were released at their site of capture at the end of the study and none were harmed as a result of the parasite removal.

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The authors declare that they have no conflict of interest.

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Correspondence to Dominique G. Roche.

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Communicated by A. Pilastro

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Roche, D.G., Binning, S.A., Strong, L.E. et al. Increased behavioural lateralization in parasitized coral reef fish. Behav Ecol Sociobiol 67, 1339–1344 (2013). https://doi.org/10.1007/s00265-013-1562-1

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  • DOI: https://doi.org/10.1007/s00265-013-1562-1

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