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Parental environment mediates impacts of increased carbon dioxide on a coral reef fish

Nature Climate Change volume 2, pages 858–861 (2012)Cite this article

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Abstract

Carbon dioxide concentrations in the surface ocean are increasing owing to rising CO2 concentrations in the atmosphere1. Higher CO2 levels are predicted to affect essential physiological processes of many aquatic organisms2,3, leading to widespread impacts on marine diversity and ecosystem function, especially when combined with the effects of global warming4,5,6. Yet the ability for marine species to adjust to increasing CO2 levels over many generations is an unresolved issue. Here we show that ocean conditions projected for the end of the century (approximately 1,000 μatm CO2 and a temperature rise of 1.5–3.0 °C) cause an increase in metabolic rate and decreases in length, weight, condition and survival of juvenile fish. However, these effects are absent or reversed when parents also experience high CO2 concentrations. Our results show that non-genetic parental effects can dramatically alter the response of marine organisms to increasing CO2 and demonstrate that some species have more capacity to acclimate to ocean acidification than previously thought.

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Figure 1: The effect of parental environment on life history and metabolic traits of juvenile anemonefish exposed to high CO2.

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References

  1. Doney, S. C. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512–1516 (2010).

    Article  CAS  Google Scholar 

  2. 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 

  3. 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).

    Article  CAS  Google Scholar 

  4. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  6. Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414–432 (2008).

    Article  CAS  Google Scholar 

  7. Rosa, R. & Seibel, B. A. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc. Natl Acad. Sci. USA 105, 20776–20780 (2008).

    Article  CAS  Google Scholar 

  8. Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).

    Article  Google Scholar 

  9. Eliason, E. J. et al. Differences in thermal tolerance among sockeye salmon populations. Science 332, 109–112 (2011).

    Article  CAS  Google Scholar 

  10. Nilsson, G. E., Crawley, N., Lunde, I. G. & Munday, P. L. Elevated temperature reduces the respiratory scope of coral reef fishes. Glob. Change Biol. 15, 1405–1412 (2009).

    Article  Google Scholar 

  11. Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422 (2011).

    Article  CAS  Google Scholar 

  12. Pörtner, H. O. et al. in Ocean Acidification (eds Gattuso, J-P. & Hansson, L.) (Oxford Univ. Press, 2011).

    Google Scholar 

  13. Marshall, D. J. & Morgan, S. G. Ecological and evolutionary consequences of linked life-history stages in the sea. Curr. Biol. 21, R718-R725 (2011).

    Article  Google Scholar 

  14. 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 

  15. Donelson, J. M., Munday, P. L. & McCormick, M.I. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Clim. Change 2, 30–32 (2012).

    Article  Google Scholar 

  16. Salinas, S. & Munch, S.B. Thermal legacies: Transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15, 159–163 (2012).

    Article  Google Scholar 

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

    Google Scholar 

  18. Poloczanska, E. S. et al. Climate change and Australian marine life. Oceanogr. Mar. Biol. Annu. Rev. 45, 407–478 (2007).

    Google Scholar 

  19. Nowicki, J. P., Miller, G. M. & Munday, P. L. Interactive effects of elevated temperature and CO2 on foraging behavior of juvenile coral reef fish. J. Exp. Mar. Biol. Ecol. 412, 46–51 (2012).

    Article  Google Scholar 

  20. Bonduriansky, R. & Day, T. Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40, 103–125 (2009).

    Article  Google Scholar 

  21. Donelson, J. M., Munday, P. L. & McCormick, M. I. Parental effects on offspring life histories: when are they important? Biol. Lett. 5, 262–265 (2009).

    Article  Google Scholar 

  22. Bernardo, J. Maternal effects in animal ecology. Am. Zool. 36, 83–105 (1996).

    Article  Google Scholar 

  23. Kurihara, H. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Mar. Ecol. Prog. Ser. 373, 275–284 (2008).

    Article  CAS  Google Scholar 

  24. Hendriks, I. E., Duarte, C. M. & Alvarez, M. Vulnerability of marine biodiversity to ocean acidification: A meta-analysis. Estuar. Coast. Shelf Sci. 86, 157–164 (2010).

    Article  CAS  Google Scholar 

  25. Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

    Article  Google Scholar 

  26. Baumann, H., Talmage, S. C. & Gobler, C. J. Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nature Clim. Change 2, 38–41 (2012).

    Article  CAS  Google Scholar 

  27. Frommel, A. Y. et al. Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Clim. Change 2, 42–46 (2012).

    Article  CAS  Google Scholar 

  28. Jablonka, E. & Raz, G. Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131–176 (2009).

    Article  Google Scholar 

  29. Deigweiher, K., Koschnick, N., Pörtner, H. O. & Lucassen, M. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1660-R1670 (2008).

    Article  Google Scholar 

  30. Green, B. S. Maternal effects in fish populations. Adv. Mar. Biol. 54, 1–105 (2008).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Munday, P. L., Donelson, J. M., Dixson, D. L. & Endo, G. G. K. Effects of ocean acidification on the early life history of a tropical marine fish. Proc. R. Soc. B 276, 3275–3283 (2009).

    Article  CAS  Google Scholar 

  33. Munday, P.L., Hernaman, V., Dixson, D. L. & Thorrold, S.R. Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 8, 1631–1641 (2011).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank staff of James Cook University’s Marine Aquarium Facility, R. De Nys for logistical support and J. L. Rummer for comments on the manuscript. The project was financially supported by the Australian Research Council (P.L.M), ARC Centre of Excellence for Coral Reef Studies (P.L.M. and M.I.M.) and Sea World Research and Rescue Foundation (G.M.M.). This project was completed under JCU Ethics A1427.

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  1. ARC Centre of Excellence for Coral Reef Studies, and School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia

    Gabrielle M. Miller, Sue-Ann Watson, Jennifer M. Donelson, Mark I. McCormick & Philip L. Munday

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  1. Gabrielle M. Miller
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  2. Sue-Ann Watson
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  3. Jennifer M. Donelson
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  4. Mark I. McCormick
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  5. Philip L. Munday
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Contributions

G.M.M. and P.L.M. designed the experiments. G.M.M. carried out all experimentation and analysed raw data. S-A.W. and G.M.M. collected and analysed seawater chemistry parameters. P.L.M., G.M.M., J.M.D., S-A.W. and M.I.M. wrote the article. All authors contributed intellectual input, read and approved the manuscript.

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Correspondence to Gabrielle M. Miller.

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Miller, G., Watson, SA., Donelson, J. et al. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nature Clim Change 2, 858–861 (2012). https://doi.org/10.1038/nclimate1599

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