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Heat challenges can enhance population tolerance to thermal stress in mussels: a potential mechanism by which ship transport can increase species invasiveness

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Abstract

It is unclear whether transport by human vectors can increase the robustness of translocated populations and thereby enhance their invasiveness. To test this concept, we investigated the effect of heat stress on the tolerance of mussel populations towards a second stress event of the same kind. The heat challenges we mimicked can be faced by marine invertebrates that are transported through regions with high sea surface temperatures on ship hulls or in ballast water tanks. The study included 5 mussel species that were collected at sites in Brazil, Chile, Finland, Germany (Baltic Sea) and Portugal. In parallel laboratory experiments, monospecific groups of individuals were exposed to heat challenges that caused 60–83% mortality in the experimental groups within 15–28 days. The surviving individuals were exposed to a second stress event of the same kind, while their survival was then compared to the robustness of conspecifics that had not been exposed to elevated temperatures before. We observed that thermal tolerance was significantly enhanced by previous heat stress experience in case of Semimytilus algosus from Chile and in case of Mytilus edulis from Germany. Our results suggest that heat challenges, which marine invertebrates experience during transport, can enhance stress tolerance in founder populations of these species in their non-native range by potentially increasing the frequency of genetically adapted genotypes. This points at the necessity to learn more about selection acting on organisms during human-mediated transport—in the aquatic but also in the terrestrial environment.

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Acknowledgements

The study was realized in the framework of the international research and student training programme GAME (Global Approach by Modular Experiments) that is coordinated by GEOMAR Helmholtz Centre for Ocean Research Kiel, Germany. It was generously funded by Lighthouse Foundation, mare Zeitschrift und Buch, HydroTechnik Lübeck, Okeanos Stiftung für das Meer, Hatlapa Marine Equipment, Terra Water, CONTROS Systems & Solutions GmbH, Oktopus GmbH, Hydro-Bios, KUM, Brunsbüttel Ports. J. Canning-Clode was supported by a starting grant in the framework of the 2014 FCT Investigator Programme (IF/01606/2014/CP1230/CT0001). We thank two anonymous reviewers for their valuable suggestions, which led to a substantial improvement of the manuscript. Furthermore, we thank Rainer Kiko for providing us the maximum water temperature data for the various study sites.

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Author notes

  1. Yasser Ahmed

    Present address: Department Utilization of Fisheries Resources, Satya Negara Indonesia University, Jl. Arteri Pondok Indah No 11, Kebayoran Lama, 12240, Jakarta, Indonesia

  2. Karen von Juterzenka

    Present address: Leibniz Centre for Tropical Marine Research (ZMT), Fahrenheitstraße 6, 28359, Bremen, Germany

  3. Daniel Wohlgemuth

    Present address: Ocean and Earth Science, University of Southampton, Waterfront Campus, European Way, Southampton, SO14 3ZH, UK

Authors and Affiliations

  1. Marine Ecology Department, GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Mark Lenz, Susanne Machura, Filipa Paiva & Martin Wahl

  2. Department of Marine Science and Technology, Bogor Agricultural University, Jalan Lingkar Akademi, Kampus IPB Darmaga, Bogor, 16680, West Java, Indonesia

    Yasser Ahmed, Karen von Juterzenka & Neviaty P. Zamani

  3. MARE – Marine and Environmental Sciences Centre, Quinta do Lorde Marina, Sítio da Piedade, 9200 – 044, Caniçal, Madeira Island, Portugal

    João Canning-Clode & Filipa Paiva

  4. Cais do Carvão, 9000-107, Funchal, Madeira, Portugal

    João Canning-Clode

  5. Department of Oceanography and Fisheries, Centre of IMAR of the University of the Azores, Rua Prof. Dr. Frederico Machado, 4, PT-9901-862, Horta, Azores, Portugal

    João Canning-Clode

  6. Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD, 21037, USA

    João Canning-Clode

  7. Department of Environmental Sciences, University of Helsinki, PO Box 65 (Viikinkaari 1), 0014, Helsinki, Finland

    Eliecer Díaz

  8. Department Marine Biology, University of Rostock, Albert-Einstein-Str. 3, 18059, Rostock, Germany

    Sandra Eichhorn

  9. Department of Ecology, Institute of Zoology, Johannes Gutenberg-University of Mainz, Johann-Joachim-Becher-Weg 13, 55099, Mainz, Germany

    Armin G. Fabritzek

  10. Departamento de Biologia Marinha, Universidade Federal Fluminense (UFF), Caixa Postal 100644, Niterói, Rio de Janeiro, CEP 24001-970, Brazil

    Bernardo A. P. da Gama & Felipe V. Ribeiro

  11. Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Hauptstrasse 1, 79104, Freiburg, Germany

    Marie Garcia

  12. Department of Aquatic Resources, Institute of Coastal Research, Swedish University of Agricultural Sciences, Skolgatan 6, 74242, Öregrund, Sweden

    Patrik Kraufvelin

  13. Mathematisch-Naturwissenschaftliche Fakultät, Fachbereich Geowissenschaften, Eberhard Karls Universität Tübingen, Geschwister-Scholl-Platz, 72074, Tübingen, Germany

    Lisa Oberschelp

  14. Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile

    Miguel A. Penna & Martin Thiel

  15. Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile

    Martin Thiel

  16. Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile

    Martin Thiel

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  1. Mark Lenz
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  2. Yasser Ahmed
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  3. João Canning-Clode
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  4. Eliecer Díaz
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  16. Martin Thiel
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  18. Neviaty P. Zamani
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  19. Martin Wahl
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Correspondence to Mark Lenz.

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Eliecer Díaz, Patrik Kraufvelin, Daniel Wohlgemuth: Tvärminne Zoological Station, J.A. Palménin tie 260, 10900 Hanko, Finland (address during field work).

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Lenz, M., Ahmed, Y., Canning-Clode, J. et al. Heat challenges can enhance population tolerance to thermal stress in mussels: a potential mechanism by which ship transport can increase species invasiveness. Biol Invasions 20, 3107–3122 (2018). https://doi.org/10.1007/s10530-018-1762-8

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