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Evolutionary and immediate effects of crude-oil pollution: depression of exploratory behaviour across populations of Trinidadian guppies

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Abstract

Human-induced perturbations such as crude-oil pollution can pose serious threats to aquatic ecosystems. To understand these threats fully it is important to establish both the immediate and evolutionary effects of pollutants on behaviour and cognition. Addressing such questions requires comparative and experimental study of populations that have evolved under different levels of pollution. Here, we compared the exploratory, activity and social behaviour of four populations of Trinidadian guppies (Poecilia reticulata) raised in common garden conditions for up to three generations. Two of these populations originated from tributaries with a long history of human-induced chronic crude-oil pollution with polycyclic aromatic hydrocarbons due to oil exploitation in Trinidad, the two others originating from non-polluted control sites. Laboratory-raised guppies from the oil-polluted sites were less exploratory in an experimental maze than guppies from the non-polluted sites and in a similar manner for the two independent rivers. We then compared the plastic behavioural responses of the different populations after an acute short-term experimental exposure to crude oil and found a decrease in exploration (but not in activity or shoaling) in the oil-exposed fish compared to the control subjects over all four populations. Taken together, these results suggest that both an evolutionary history with oil and an acute exposure to oil depressed guppy exploratory behaviour. We discuss whether the behavioural divergence observed represents adaptation to human-induced pollutants, the implications for conservation and the possible knock-on effects for information discovery and population persistence in fish groups.

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Acknowledgments

We thank G. Daggupati, C. LeBlond, L. Ljungberg, J Mateluna and PQ Sims for help at different stages of the study. We thank two anonymous referees for their helpful comments. L. Jacquin was supported by a postdoctoral grant from the Fyssen fellowship and an ATER fellowship from the Pau University UPPA, INRA Ecobiop. SM Reader thanks CFI and NSERC, and A Hendry thanks NSERC for funding.

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Authors and Affiliations

  1. Laboratoire Évolution et Diversité Biologique EDB UMR5174, UPS, CNRS, ENFA, Université de Toulouse, 118 route de Narbonne, 31062, Toulouse, France

    L. Jacquin

  2. McGill University, Redpath Museum, 859 Sherbrooke Street West, Montreal, QC, Canada

    L. Jacquin, C. Dybwad, G. Rolshausen & A. P. Hendry

  3. Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, QC, Canada

    L. Jacquin & S. M. Reader

  4. Laboratoire ECOBIOP, INRA, UPPA, Université de Pau et des Pays de l’Adour, 64310, Saint-Pée-Sur-Nivelle, France

    L. Jacquin

  5. Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, 9037, Tromsø, Norway

    C. Dybwad

  6. Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    G. Rolshausen

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  1. L. Jacquin
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Correspondence to L. Jacquin.

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This article is part of the Special Issue Animal cognition in a human dominated world.

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Jacquin, L., Dybwad, C., Rolshausen, G. et al. Evolutionary and immediate effects of crude-oil pollution: depression of exploratory behaviour across populations of Trinidadian guppies. Anim Cogn 20, 97–108 (2017). https://doi.org/10.1007/s10071-016-1027-9

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