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Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps

Abstract

Experiments have shown that the behaviour of reef fishes can be seriously affected by projected future carbon dioxide (CO2) concentrations in the ocean1,2,3,4. However, whether fish can acclimate to elevated CO2 over the longer term, and the consequences of altered behaviour on the structure of fish communities, are unknown. We used marine CO2 seeps in Papua New Guinea as a natural laboratory to test these questions. Here we show that juvenile reef fishes at CO2 seeps exhibit behavioural abnormalities similar to those seen in laboratory experiments. Fish from CO2 seeps were attracted to predator odour, did not distinguish between odours of different habitats, and exhibited bolder behaviour than fish from control reefs. High CO2 did not, however, have any effect on metabolic rate or aerobic performance. Contrary to expectations, fish diversity and community structure differed little between CO2 seeps and nearby control reefs. Differences in abundances of some fishes could be driven by the different coral community at CO2 seeps rather than by the direct effects of high CO2. Our results suggest that recruitment of juvenile fish from outside the seeps, along with fewer predators within the seeps, is currently sufficient to offset any negative effects of high CO2 within the seeps. However, continuous exposure does not reduce the effect of high CO2 on behaviour in natural reef habitat, and this could be a serious problem for fish communities in the future when ocean acidification becomes widespread as a result of continued uptake of anthropogenic CO2 emissions.

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Figure 1: Preference of juvenile fish for water streams containing different chemical cues presented in a two-channel flume chamber.
Figure 2: Activity level and boldness of fish from CO2 seep and control reefs.
Figure 3: Comparisons of fish community structure at CO2 seep and control locations.

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).

    Article  CAS  Google Scholar 

  2. 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 

  3. Nilsson, G. E. et al. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Clim. Change 2, 201–204 (2012).

    Article  CAS  Google Scholar 

  4. Briffa, M., de la Haye, K. & Munday, P. L. High CO2 and marine animal behaviour: Potential mechanisms and ecological consequences. Mar. Pollut. Bull. 64, 1519–1528 (2012).

    Article  CAS  Google Scholar 

  5. Wittmann, A. C. & Portner, H.-O. Sensitivities of extant animal taxa to ocean acidification. Nature Clim. Change 3, 995–1001 (2013).

    Article  CAS  Google Scholar 

  6. Russell, B. D. et al. Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems. Biol. Lett. 8, 164–166 (2012).

    Article  Google Scholar 

  7. Kroeker, K. J., Gambi, M. C. & Micheli, F. Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc. Natl Acad. Sci. USA 110, 12721–12726 (2013).

    Article  CAS  Google Scholar 

  8. Ries, J. B., Cohen, A. L. & McCorkle, D. C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131–1134 (2009).

    Article  CAS  Google Scholar 

  9. Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

    Article  Google Scholar 

  10. Form, A. U. & Riebesell, U. Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Glob. Change Biol. 18, 843–853 (2012).

    Article  Google Scholar 

  11. Miller, G. M., Watson, S. A., Donelson, J. M., McCormick, M. I. & Munday, P. L. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nature Clim. Change 2, 858–861 (2012).

    Article  CAS  Google Scholar 

  12. Parker, L. M. et al. Adult exposure influences offspring response to ocean acidification in oysters. Glob. Change Biol. 18, 82–92 (2012).

    Article  Google Scholar 

  13. Dupont, S., Dorey, N., Stumpp, M., Melzner, F. & Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 160, 1835–1843 (2013).

    Article  CAS  Google Scholar 

  14. Domenici, P., Allan, B., McCormick, M. I. & Munday, P. L. Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol. Lett. 8, 78–81 (2012).

    Article  CAS  Google Scholar 

  15. Ferrari, M. C. O. et al. Effects of ocean acidification on visual risk assessment in coral reef fishes. Funct. Ecol. 26, 553–558 (2012).

    Article  Google Scholar 

  16. Chivers, D. P. et al. Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference. Glob. Change Biol. 20, 512–522 (2014).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  18. Ferrari, M. C. O. et al. Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: Implications for climate change projections on marine communities. Glob. Change Biol. 17, 2980–2986 (2011).

    Article  Google Scholar 

  19. 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 

  20. Portner, H. O. & Farrell, A. P. Ecology: Physiology and climate change. Science 322, 690–692 (2008).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Esbaugh, A. J., Heuer, R. & Grosell, M. Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta. J. Comp. Physiol. B. 182, 921–934 (2012).

    Article  CAS  Google Scholar 

  23. Munday, P. L., Crawley, N. E. & Nilsson, G. E. Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Mar. Ecol.-Prog. Ser. 388, 235–242 (2009).

    Article  CAS  Google Scholar 

  24. Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim. Change 1, 165–169 (2011).

    Article  CAS  Google Scholar 

  25. Almany, G. R. & Webster, M. S. The predation gauntlet: Early post-settlement mortality in reef fishes. Coral Reefs 25, 19–22 (2006).

    Article  Google Scholar 

  26. Couturier, C. S., Stecyk, J. A. W., Rummer, J. L., Munday, P. L. & Nilsson, G. E. Species-specific effects of near-future CO2 on the respiratory performance of two tropical prey fish and their predator. Comp. Biochem. Physiol. A. 166, 482–489 (2013).

    Article  CAS  Google Scholar 

  27. Hixon, M. A. & Jones, G. P. Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86, 2847–2859 (2005).

    Article  Google Scholar 

  28. Wen, C. K. C., Pratchett, M. S., Almany, G. R. & Jones, G. P. Patterns of recruitment and microhabitat associations for three predatory coral reef fishes on the southern Great Barrier Reef, Australia. Coral Reefs 32, 389–398 (2013).

    Article  Google Scholar 

  29. Allan, B. J. M., Miller, G. M., McCormick, M. I., Domenici, P. & Munday, P. L. Parental effects improve escape performance of juvenile reef fish in a high-CO2 world. Proc. R. Soc. B. 281, 20132179 (2014).

    Article  Google Scholar 

  30. Clark, T. D., Sandblom, E. & Jutfelt, F. Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J. Exp. Biol. 216, 2771–2782 (2013).

    Article  Google Scholar 

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Acknowledgements

We thank the people at Upa Upasina (Illi Illi Bwa Bwa), Dobu and Esa’Ala reefs for allowing us to visit their reefs, and Rob van der Loos and the crew of MV Chertan for logistical support. Special thanks to S. Noonan for logistic support and assistance with experiments. The study was funded by the Australian Institute of Marine Science, a Grant for Research and Exploration by the National Geographic Society, and the ARC Centre of Excellence for Coral Reef Studies.

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All authors contributed to the designs of the study, collection and analysis of data, and writing the article.

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Correspondence to Philip L. Munday.

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Munday, P., Cheal, A., Dixson, D. et al. Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nature Clim Change 4, 487–492 (2014). https://doi.org/10.1038/nclimate2195

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