Biological Invasions

, Volume 20, Issue 11, pp 3107–3122 | Cite as

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

  • Mark LenzEmail author
  • Yasser Ahmed
  • João Canning-Clode
  • Eliecer Díaz
  • Sandra Eichhorn
  • Armin G. Fabritzek
  • Bernardo A. P. da Gama
  • Marie Garcia
  • Karen von Juterzenka
  • Patrik Kraufvelin
  • Susanne Machura
  • Lisa Oberschelp
  • Filipa Paiva
  • Miguel A. Penna
  • Felipe V. Ribeiro
  • Martin Thiel
  • Daniel Wohlgemuth
  • Neviaty P. Zamani
  • Martin Wahl
Original Paper


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.


Heat Mytilids Selection Stress tolerance Survival Transport 



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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


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Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Mark Lenz
    • 1
    Email author
  • Yasser Ahmed
    • 2
    • 17
  • João Canning-Clode
    • 3
    • 4
    • 5
    • 6
  • Eliecer Díaz
    • 7
  • Sandra Eichhorn
    • 8
  • Armin G. Fabritzek
    • 9
  • Bernardo A. P. da Gama
    • 10
  • Marie Garcia
    • 11
  • Karen von Juterzenka
    • 2
    • 18
  • Patrik Kraufvelin
    • 12
  • Susanne Machura
    • 1
  • Lisa Oberschelp
    • 13
  • Filipa Paiva
    • 1
    • 3
  • Miguel A. Penna
    • 14
  • Felipe V. Ribeiro
    • 10
  • Martin Thiel
    • 14
    • 15
    • 16
  • Daniel Wohlgemuth
    • 19
  • Neviaty P. Zamani
    • 2
  • Martin Wahl
    • 1
  1. 1.Marine Ecology DepartmentGEOMAR Helmholtz Centre for Ocean Research KielKielGermany
  2. 2.Department of Marine Science and TechnologyBogor Agricultural UniversityBogorIndonesia
  3. 3.MARE – Marine and Environmental Sciences CentreCaniçalPortugal
  4. 4.Cais do CarvãoFunchalPortugal
  5. 5.Department of Oceanography and FisheriesCentre of IMAR of the University of the AzoresHortaPortugal
  6. 6.Smithsonian Environmental Research CenterEdgewaterUSA
  7. 7.Department of Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  8. 8.Department Marine BiologyUniversity of RostockRostockGermany
  9. 9.Department of Ecology, Institute of ZoologyJohannes Gutenberg-University of MainzMainzGermany
  10. 10.Departamento de Biologia MarinhaUniversidade Federal Fluminense (UFF)NiteróiBrazil
  11. 11.Department of Evolutionary Biology and Animal Ecology, Faculty of BiologyUniversity of FreiburgFreiburgGermany
  12. 12.Department of Aquatic Resources, Institute of Coastal ResearchSwedish University of Agricultural SciencesÖregrundSweden
  13. 13.Mathematisch-Naturwissenschaftliche Fakultät, Fachbereich GeowissenschaftenEberhard Karls Universität TübingenTübingenGermany
  14. 14.Facultad de Ciencias del MarUniversidad Católica del NorteCoquimboChile
  15. 15.Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI)CoquimboChile
  16. 16.Centro de Estudios Avanzados en Zonas Áridas (CEAZA)CoquimboChile
  17. 17.Department Utilization of Fisheries ResourcesSatya Negara Indonesia UniversityKebayoran LamaIndonesia
  18. 18.Leibniz Centre for Tropical Marine Research (ZMT)BremenGermany
  19. 19.Ocean and Earth ScienceUniversity of SouthamptonSouthamptonUK

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