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Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis

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Abstract

The manipulation of host behaviour by the not-fully-developed, immature larvae of trophically transmitted parasites is attracting growing interest. A theoretical model predicts that while facilitation of host predation risk is advantageous for fully developed parasite larvae, the immature ones should make hosts less vulnerable to the predators (predation suppression hypothesis). However, there is still little evidence of such manipulation by non-infective parasite stages. We tested whether immature trematode larvae of the eye fluke, Diplostomum pseudospathaceum, a common parasite of many freshwater fishes, enhance the anti-predatory responses of their host (Oncorhynchus mykiss). To test the predation suppression hypothesis, we experimentally infected young-of-the-year (YOY) rainbow trout and studied the influence of pre-infective metacercariae of the eye fluke on the anti-predator behaviour of the fish. Fish activity, depth preference and the ability to avoid simulated predation were evaluated in the experiments. Infected fish—harbouring a moderate number of immature metacercariae—were significantly less vulnerable to simulated predation (dip-net catch) and less active (horizontal move), but their swimming depth (vertical position) was not changed when compared with the control fish harbouring no larvae. Our findings suggest that immature larvae of D. pseudospathaceum induce changes in host behaviour that can protect them from predation, thereby supporting the predation suppression hypothesis and indicating that manipulations caused by immature parasites may play an important role in modulating predator–prey interactions.

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Acknowledgments

The work was funded by the Academy of Finland, grants no: 260704/2011 and 279220/2014 to JT and Russian Foundation for Basic Research (RFBR), grant no: 140400090a to VM.

We are grateful to Dale Edwards for reading and checking a draft of the manuscript, the entire Ecological Parasitology Group at the University of Jyväskylä (JYU) for fruitful discussion and especially Ines Klemme for her valuable comments on the manuscript. We also thank Matthew Wuethrich from the Language Centre of JYU for his highly professional and thorough editing of the manuscript. Finally, we thank two anonymous referees for their constructive comments and suggestions.

Conflict of interest

The authors declare that they have no competing interests.

Ethical standards

All experiments in the study were performed following the ethical standards of the National Animal Experiments Board in Finland according to legislation (licence ESAVI/6759/04.10.03/2011).

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Authors and Affiliations

  1. A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Laboratory for Behaviour of Lower Vertebrates, 33 Leninsky Prospekt, 119071, Moscow, Russia

    Mikhail Gopko & Victor N. Mikheev

  2. Department of Biological and Environmental Sciences, University of Jyväskylä, P.O. Box 35 (YAC-315.2), FI-40014, Jyväskylä, Finland

    Jouni Taskinen

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  1. Mikhail Gopko
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  2. Victor N. Mikheev
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  3. Jouni Taskinen
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Correspondence to Mikhail Gopko.

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Communicated by J. Lindström

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Gopko, M., Mikheev, V.N. & Taskinen, J. Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behav Ecol Sociobiol 69, 1723–1730 (2015). https://doi.org/10.1007/s00265-015-1984-z

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