Abstract

Survival of marine fishes that are exposed to elevated near-future CO2 levels is threatened by their altered responses to sensory cues. Here we demonstrate a physiological and molecular mechanism in the olfactory system that helps to explain altered behaviour under elevated CO2. We combine electrophysiology measurements and transcriptomics with behavioural experiments to investigate how elevated CO2 affects the olfactory system of European sea bass (Dicentrarchus labrax). When exposed to elevated CO2 (approximately 1,000 µatm), fish must be up to 42% closer to an odour source for detection, compared with current CO2 levels (around 400 µatm), decreasing their chances of detecting food or predators. Compromised olfaction correlated with the suppression of the transcription of genes involved in synaptic strength, cell excitability and wiring of the olfactory system in response to sustained exposure to elevated CO2 levels. Our findings complement the previously proposed impairment of γ-aminobutyric acid receptors, and indicate that both the olfactory system and central brain function are compromised by elevated CO2 levels.

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Acknowledgements

We thank L. Hagey and A. Hofmann (UCSD) for their gift of cyprinol sulfate and scymnol sulfate, the Aquatic Research Centre (ARC) staff at the University of Exeter for their assistance with fish husbandry and experimental setup, B. Verbruggen for helpful bioinformatics advice and L. Salisbury for help with tissue sampling. This study was supported by grants from Association of European Marine Biology Laboratories (227799), the Natural Environment Research Council (R.W.W.; NE/H017402/1), the Biotechnology and Biological Sciences Research Council (R.W.W.; BB/D005108/1), Fundação para a Ciência e Tecnologia (Portuguese Science Ministry) (UID/Multi/04326/2013) and a Royal Society Newton International Fellowship to C.S.P. C.S.P. is also a beneficiary of a Starting Grant from AXA.

Author information

Affiliations

  1. Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK

    • Cosima S. Porteus
    • , Eduarda M. Santos
    •  & Rod W. Wilson
  2. Centro de Ciências do Mar, Campus de Gambelas, Universidade do Algarve, Faro, Portugal

    • Peter C. Hubbard
    •  & Adelino V. M. Canário
  3. Biosciences, College of Science, Swansea University, Swansea, UK

    • Tamsyn M. Uren Webster
  4. Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth, UK

    • Ronny van Aerle

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Contributions

C.S.P. and R.W.W. designed the behavioural experiments. C.S.P. performed the experiments and analysed those data; C.S.P., P.C.H., A.V.M.C. and R.W.W. designed the electrophysiology study, C.S.P. and P.C.H. performed the electrophysiology experiments. C.S.P., T.M.U.W., R.v.A. and E.M.S. designed the transcriptomics experiments, C.S.P. performed the experiments and constructed the libraries. C.S.P. performed the bioinformatics analysis and interpreted the results with help from T.M.U.W., R.v.A. and E.M.S. All authors contributed to and provided feedback on various drafts of the paper.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Cosima S. Porteus or Rod W. Wilson.

Supplementary information

  1. Supplementary Information

    Supplementary figures 1–8, Supplementary tables 1–13, Supplementary References

  2. Supplementary Data 1

    Lists of differentially expressed genes in the olfactory epithelium and olfactory bulb at 2 and 7 days of exposure to control and high CO2

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https://doi.org/10.1038/s41558-018-0224-8