Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function

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Abstract

Predicted future CO2 levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function1,2,3,4,5. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats1,3. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function2,6. However, the underlying mechanism linking high CO2 to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO2 can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO2 interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO2 levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid–base balance through regulatory changes in HCO3 and Cl levels.

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Figure 1: Proposed response of GABA-A receptor function to elevated sea water pCO2.
Figure 2: Olfactory ability of larval clownfish (Amphiprion percula) is impaired by high CO2 and restored by a GABA-A receptor antagonist.
Figure 3: Behavioural lateralization of larval damselfish (Neopomacentrus azysron) is impaired by high CO2 and restored by a GABA-A receptor antagonist.

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Acknowledgements

We thank B. M. Devine, J. M. Donelson, G. M. Miller and the staff at Lizard Island Research Station for invaluable help with this study. The study was financially supported by The Australian Research Council and The University of Oslo.

Author information

G.E.N. and P.L.M. devised the study. G.E.N., P.L.M. and P.D. designed the experiments. G.E.N., P.D., D.L.D., P.L.M., M.I.M. and C.S. conducted the experiments. S-A.W. developed equipment and conducted the chemical analyses. P.L.M. and P.D. conducted the statistical analyses. All authors contributed to writing the paper.

Correspondence to Göran E. Nilsson.

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The authors declare no competing financial interests.

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