Near-future CO2 levels impair the olfactory system of a marine fish

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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Fig. 1: Behaviour responses of European sea bass (D. labrax) to a 5-min exposure to a predator odour (monkfish bile).
Fig. 2: Elevated CO2 decreases the olfactory sensitivity of European sea bass to amino acids, bile acids and body fluids.
Fig. 3: Acute exposure of European seabass to elevated CO2 (around 1,000 µatm) decreases the amplitude of the olfactory response and increases the detection threshold of several odorants tested.
Fig. 4: Differential regulation of genes in the olfactory epithelium and olfactory lobe of European sea bass exposed to control and high CO2.
Fig. 5: Proposed mechanism of action of CO2-induced ocean acidification on fish behaviour via the olfactory pathway.

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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.

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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.

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

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

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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Porteus, C.S., Hubbard, P.C., Uren Webster, T.M. et al. Near-future CO2 levels impair the olfactory system of a marine fish. Nature Clim Change 8, 737–743 (2018). https://doi.org/10.1038/s41558-018-0224-8

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