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

An Author Correction to this article was published on 16 June 2020

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.

References

  1. Munday, P. L. et al. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl Acad. Sci. USA 106, 1848–1852 (2009).

    CAS  Article  Google Scholar 

  2. Munday, P. L. et al. Replenishment of fish populations is threatened by ocean acidification. Proc. Natl Acad. Sci. USA 107, 12930–12934 (2010).

    CAS  Article  Google Scholar 

  3. Dixson, D. L., Munday, P. L. & Jones, G. P. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13, 68–75 (2010).

    Article  Google Scholar 

  4. Simpson, S. D. et al. Ocean acidification erodes crucial auditory behaviour in a marine fish. Biol. Lett. 7, 917–920 (2011).

    CAS  Article  Google Scholar 

  5. Domenici, P., Allan, B., McCormick, M. I. & Munday, P. L. Elevated CO2 affects behavioural lateralization in a coral reef fish. Biol. Lett. http://dx.doi.org/10.1098/rsbl.2011.0591 (2011).

  6. Ferrari, M. C. O. et al. Putting prey and predator into the CO2 equation: Qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecol. Lett. 14, 1143–1148 (2011).

    Article  Google Scholar 

  7. Meehl, G. A. et al. in IPCC Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) 747–845 (Cambridge Univ. Press, 2007).

    Google Scholar 

  8. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192 (2009).

    Article  Google Scholar 

  9. Bormann, J., Hamill, O. P. & Sakmann, B. Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385, 243–286 (1987).

    CAS  Article  Google Scholar 

  10. Lambert, N. & Grover, L. The mechanism of biphasic GABA responses. Science 269, 928–929 (1995).

    CAS  Article  Google Scholar 

  11. Kahle, K. T. & Staley, K. Altered neuronal chloride homeostasis and excitatory GABAergic signaling in human temporal lobe epilepsy. Epilepsy Curr. 8, 51–53 (2008).

    Article  Google Scholar 

  12. Kim, D. Y., Fenoglio, K. A., Kerrigan, J. F. & Rho, J. M. Bicarbonate contributes to GABA-A receptor mediated excitation in surgically resected human hypothalamic hamartomas. Epilepsy Res. 83, 89–93 (2009).

    CAS  Article  Google Scholar 

  13. Ishimatsu, A., Hayashi, M. & Kikkawa, T. Fishes in high CO2 acidified oceans. Mar. Ecol. Prog. Ser. 373, 295–302 (2008).

    CAS  Article  Google Scholar 

  14. Brauner, C. J. & Baker, D. W. in Cardio-Respiratory Control in Vertebrates (eds Glass, M. L. & Wood, S. C.) 43–63 (Springer, 2009).

    Book  Google Scholar 

  15. Heaulme, M. et al. Biochemical characterization of the interaction of three pyridazinyl-GABA derivatives with the GABA A receptor site. Brain Res. 384, 224–231 (1986).

    CAS  Article  Google Scholar 

  16. Fu, C., Wilson, J. M., Rombough, P. J. & Brauner, C. J. Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss. Proc. R. Soc. B 277, 1553–1560 (2010).

    CAS  Article  Google Scholar 

  17. Akerman, C. J. & Cline, H. T. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 30, 382–389 (2007).

    CAS  Article  Google Scholar 

  18. Tsang, S. Y., Ng, S. K., Xu, Z. & Xue, H. The evolution of GABAA receptor-like genes. Mol. Biol. Evol. 24, 599–610 (2007).

    CAS  Article  Google Scholar 

  19. Heisler, N. in Acid–Base Regulation in Animals (ed. Heisler, N.) 3–47 (Elsevier, 1986).

    Google Scholar 

  20. Pörtner, H. O., Langenbuch, M. & Reipschlager, A. Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. J. Oceanogr. 60, 705–718 (2004).

    Article  Google Scholar 

  21. Melzner, F. et al. Physiological basis for high CO2 tolerance in marine ectothermic animals: Pre-adaptation through lifestyle and ontogeny? Biogeoscience 6, 2313–2331 (2009).

    CAS  Article  Google Scholar 

  22. Ohde, S. & Van Woesik, R. Carbon Dioxide flux and metabolic processes of a coral reef (Okinawa, Japan). Bull. Mar. Sci. 65, 559–576 (1999).

    Google Scholar 

  23. Kuffner, I. B., Andersson, A. J., Jokiel, P. L., Rodgers, K. S. & Mackenzie, F. T. Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geosci. 1, 114–117 (2008).

    CAS  Article  Google Scholar 

  24. Nilsson, G. E., Östlund-Nilsson, S., Penfold, R. & Grutter, A. S. From record performance to hypoxia tolerance—respiratory transition in damselfish larvae settling on a coral reef. Proc. R. Soc. B 274, 79–85 (2007).

    CAS  Article  Google Scholar 

  25. Boutilier, R. G., Aughton, P. & Shelton, G. O2 and CO2 transport in relation to ventilation in Atlantic mackerel, Scomber scombrus. Can. J. Zool. 62, 546–554 (1984).

    Article  Google Scholar 

  26. Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007).

    CAS  Article  Google Scholar 

  27. Thresher, R. E., Colin, P. L. & Bell, L. J. Planktonic duration, distribution and population structure of Western and Central Pacific Damselfishes (Pomacentridae). Copeia 1989, 420–434 (1989).

    Article  Google Scholar 

  28. Meekan, M. G. A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar. Biol. 139, 373–381 (2001).

    Article  Google Scholar 

  29. Bisazza, A. et al. Lateralization of detour behaviour in poeciliid fish: The effect of species, gender and sexual motivation. Behav. Brain Res. 91, 157–164 (1998).

    CAS  Article  Google Scholar 

  30. Dadda, M., Koolhaas, W. H. & Domenici, P. Behavioural asymmetry affects escape performance in a teleost fish. Biol. Lett. 6, 414–417 (2010).

    Article  Google Scholar 

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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.

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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.

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Correspondence to Göran E. Nilsson.

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The authors declare no competing financial interests.

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Nilsson, G., Dixson, D., Domenici, P. et al. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Clim Change 2, 201–204 (2012). https://doi.org/10.1038/nclimate1352

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