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Living coral tissue slows skeletal dissolution related to ocean acidification

Nature Ecology & Evolution volume 3, pages 1438–1444 (2019)Cite this article

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Abstract

Climate change is causing major changes to marine ecosystems globally, with ocean acidification of particular concern for coral reefs. Using a 200 d in situ carbon dioxide enrichment study on Heron Island, Australia, we simulated future ocean acidification conditions, and found reduced pH led to a drastic decline in net calcification of living corals to no net growth, and accelerated disintegration of dead corals. Net calcification declined more severely than in previous studies due to exposure to the natural community of bioeroding organisms in this in situ study and to a longer experimental duration. Our data suggest that reef flat corals reach net dissolution at an aragonite saturation state (ΩAR) of 2.3 (95% confidence interval: 1.8–2.8) with 100% living coral cover and at ΩAR > 3.5 with 30% living coral cover. This model suggests that areas of the reef with relatively low coral mortality, where living coral cover is high, are likely to be resistant to carbon dioxide-induced reef dissolution.

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Fig. 1: The CP-FOCE system deployed on the Heron Island reef flat.
Fig. 2: pH levels in the FOCE flumes and controls throughout the experiment and the changes in coral annual buoyant weights.
Fig. 3: Observed and estimated responses of changes in annual buoyant weight as a function of ΩAR and coral status (live versus dead).
Fig. 4: Illustration revealing the drivers of the dynamic balance between growth and dissolution on a coral reef.

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Data availability

All data generated or analysed during this study are included in this published article and its Supplementary information files.

Code availability

Script files and associated data for analysis can be found at https://github.com/dkokamoto.

References

  1. Pachauri, R. K. et al. in Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer, L. A.) 151 (IPCC, 2014).

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

    Article  CAS  PubMed  Google Scholar 

  3. 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 

  4. Cohen, A. L. & Holcomb, M. Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22, 118–127 (2009).

    Article  Google Scholar 

  5. Chan, N. C. & Connolly, S. R. Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob. Change Biol. 19, 282–290 (2013).

    Article  Google Scholar 

  6. Comeau, S., Edmunds, P., Lantz, C. & Carpenter, R. Water flow modulates the response of coral reef communities to ocean acidification. Sci. Rep. 4, 6681 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Page, H. N. et al. Spatiotemporal variability in seawater carbon chemistry for a coral reef flat in Kāne‘ohe Bay, Hawai‘i. Limnol. Oceanogr. 64, 913–934 (2018).

    Article  Google Scholar 

  8. Kroeker, K. J., Micheli, F. & Gambi, M. C. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Change 3, 156–159 (2013).

    Article  CAS  Google Scholar 

  9. Perry, C. T. et al. Changing dynamics of caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential. Proc. R. Soc. B 281, 20142018 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Albright, R. et al. Carbon dioxide addition to coral reef waters suppresses net community calcification. Nature 555, 516 (2018).

    Article  CAS  PubMed  Google Scholar 

  11. Eyre, B. D. et al. Coral reefs will transition to net dissolving before end of century. Science 359, 908–911 (2018).

    Article  CAS  PubMed  Google Scholar 

  12. Perry, C. T. et al. Loss of coral reef growth capacity to track future increases in sea level. Nature 558, 396 (2018).

    Article  CAS  PubMed  Google Scholar 

  13. Anthony, K. et al. Ocean acidification and warming will lower coral reef resilience. Glob. Change Biol. 17, 1798–1808 (2011).

    Article  Google Scholar 

  14. Albright, R. in Coral Bleaching: Patterns, Processes, Causes and Consequences (eds van Oppen, M. J. H. & Lough, J. M.) 295–323 (Springer, 2018).

  15. Cheng, L., Abraham, J., Hausfather, Z. & Trenberth, K. E. How fast are the oceans warming? Science 363, 128–129 (2019).

    Article  CAS  PubMed  Google Scholar 

  16. Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    Article  CAS  PubMed  Google Scholar 

  17. Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    Article  PubMed  Google Scholar 

  18. Andersson, A. J. et al. Understanding ocean acidification impacts on organismal to ecological scales. Oceanography 28, 16–27 (2015).

    Article  Google Scholar 

  19. Hoegh-Guldberg, O., Kennedy, E. V., Beyer, H. L., McClennen, C. & Possingham, H. P. Securing a long-term future for coral reefs. Trends Ecol. Evol. 33, 936–944 (2018).

    Article  PubMed  Google Scholar 

  20. Pendleton, L. et al. Coral reefs and people in a high-CO2 world: where can science make a difference to people? PLoS ONE 11, e0164699 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dove, S. G. et al. Future reef decalcification under a business-as-usual CO2 emission scenario. Proc. Natl Acad. Sci. USA 110, 15342–15347 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Yates, K. K. & Halley, R. B. Diurnal variation in rates of calcification and carbonate sediment dissolution in florida bay. Estuaries Coasts 29, 24–39 (2006).

    Article  CAS  Google Scholar 

  24. Albright, R. et al. Reversal of ocean acidification enhances net coral reef calcification. Nature 531, 362–365 (2016).

    Article  CAS  PubMed  Google Scholar 

  25. Marker, M. et al. The Coral Proto Free Ocean Carbon Enrichment system (CP-FOCE): engineering and development. In Proc. Oceans 2010 IEEE 1–10 (IEEE, 2010).

  26. Gattuso, J.-P. et al. Free Ocean CO2 Enrichment (FOCE) systems: present status and future developments. Biogeosciences 11, 4057–4075 (2014).

    Article  CAS  Google Scholar 

  27. Barry, J. P. et al. Use of a Free Ocean CO2 Enrichment (FOCE) system to evaluate the effects of ocean acidification on the foraging behavior of a deep-sea urchin. Environ. Sci. Technol. 48, 9890–9897 (2014).

    Article  CAS  PubMed  Google Scholar 

  28. Cox, T. E. et al. Effects of in situ CO2 enrichment on structural characteristics, photosynthesis and growth of the Mediterranean seagrass Posidonia oceanica. Biogeosciences 13, 2179–2194 (2016).

    Article  CAS  Google Scholar 

  29. Stark, J. S. et al. Free Ocean CO2 Enrichment (FOCE) experiments: scientific and technical recommendations for future in situ ocean acidification projects. Prog. Oceanogr. 172, 89–107 (2019).

    Article  Google Scholar 

  30. Kline, D. I. et al. A short-term in situ CO2 enrichment experiment on Heron Island (GBR). Sci. Rep. 2, 413 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu. Rev. Ecol. Evol. Syst. 42, 181–203 (2011).

    Article  Google Scholar 

  32. Kline, D. I. et al. Six month in situ high-resolution carbonate chemistry and temperature study on a coral reef flat reveals asynchronous pH and temperature anomalies. PLoS ONE 10, e0127648 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Jiang, L. Q. et al. Climatological distribution of aragonite saturation state in the global oceans. Glob. Biogeochem. Cycles 29, 1656–1673 (2015).

    Article  CAS  Google Scholar 

  34. Camp, E. F., Schoepf, V. & Suggett, D. J. How can `super corals’ facilitate global coral reef survival under rapid environmental and climatic change? Global Change Biol. 24, 2755–2757 (2018).

    Article  Google Scholar 

  35. Darling, E. S. & Côté, I. M. Seeking resilience in marine ecosystems. Science 359, 986–987 (2018).

    Article  CAS  PubMed  Google Scholar 

  36. Tribollet, A., Godinot, C., Atkinson, M. & Langdon, C. Effects of elevated \({\rm{p}}_{{\rm{CO}}_2}\) on dissolution of coral carbonates by microbial euendoliths. Glob. Biogeochem. Cycles 23, 1–7 (2009).

    Google Scholar 

  37. Hoegh-Guldberg, O. et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) 1655–1731 (IPCC, 2014).

  38. Silverman, J. et al. Carbon turnover rates in the One Tree Island reef: a 40-year perspective. J. Geophys. Res. Biogeosci. 117, 1–16 (2012).

    Article  Google Scholar 

  39. Hurd, C. L. Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J. Phycol. 51, 599–605 (2015).

    Article  CAS  PubMed  Google Scholar 

  40. Fantazzini, P. et al. Gains and losses of coral skeletal porosity changes with ocean acidification acclimation. Nat. Commun. 6, 7785 (2015).

    Article  CAS  PubMed  Google Scholar 

  41. Georgiou, L. et al. pH homeostasis during coral calcification in a free ocean CO2 enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef. Proc. Natl Acad. Sci. USA 112, 13219–13224 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Silverman, J., Lazar, B., Cao, L., Caldeira, K. & Erez, J. Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys. Res. Lett. 36, L05606 (2009).

  43. Muehllehner, N., Langdon, C., Venti, A. & Kadko, D. Dynamics of carbonate chemistry, production and calcification of the Florida Reef tract (2009-2010): evidence for seasonal dissolution. Glob. Biogeochem. Cycles 30, 661–688 (2016).

    Article  CAS  Google Scholar 

  44. Fang, J. K. et al. Sponge biomass and bioerosion rates increase under ocean warming and acidification. Glob. Change Biol. 19, 3581–3591 (2013).

    Article  Google Scholar 

  45. Chen, D. & Krol, A. in Geology and Hydrogeology of Carbonate Islands (eds Vacher, H. L. & Quinn, T. M.) 867–884 (Elsevier, 1997).

  46. Santos, I. R., Glud, R. N., Maher, D., Erler, D. & Eyre, B. D. Diel coral reef acidification driven by porewater advection in permeable carbonate sands, Heron Island, Great Barrier Reef. Geophys. Res. Lett. 38, L03604 (2011).

    Article  Google Scholar 

  47. Dickson, A. G., Afghan, J. D. & Anderson, G. C. Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity. Mar. Chem. 80, 185–197 (2003).

    Article  CAS  Google Scholar 

  48. van Heuven, S., Pierrot, D., Lewis, E. & Wallace, D. MATLAB Program Developed for CO 2 System Calculations ORNL/CDIAC-105b (Oak Ridge National Laboratory, 2009).

  49. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  50. Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. Preprint at https://arxiv.org/abs/1406.5823 (2018).

  51. Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).

    Article  Google Scholar 

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Acknowledgements

We acknowledge the Australian Research Council (ARC) Linkage Infrastructure, Equipment and Facilities (grant no. LE0989608 to O.H.-G., S.D. and D.I.K.); an ARC Linkage grant (no. LP0775303); an ARC Centre of Excellence grant (no. CE0561435); a Queensland Government Smart State Premier’s Fellowship to O.H.-G.; a Schmidt Marine Technology Partners grant (nos. G-1605-55984 and G-1802-57451 to D.I.K.); National Science Foundation grants (nos. OCE-0729236 to R.B.D. and ATM-0941760 to B.G.M.); and the Pacific Blue Foundation for supporting this research. We thank staff at the Heron Island Research Station, especially M. Roy, S. Venn, K. Hay and L. Perkins for their support throughout this project. We also thank staff at the University of Queensland Engineering Instrumentation Workshop, especially R. White, G. Manning, P. Blakely and M. James. Permits from the Department of Environment and Resource Management (no. CSCE00874010) and the GBR Marine Park Authority (no. G09/29996.1) were provided to conduct this research.

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Authors and Affiliations

  1. Smithsonian Tropical Research Institute, Ancón, Panama

    David I. Kline

  2. Scripps Institution of Oceanography, Integrative Oceanography Division, University of California San Diego, La Jolla, CA, USA

    David I. Kline & B. Greg Mitchell

  3. Global Change Institute and Coral Reef Ecosystems Laboratory, School of Biological Sciences, University of Queensland, St Lucia, Queensland, Australia

    David I. Kline, Thomas Miard, Aaron Chai, Sophie Dove & Ove Hoegh-Guldberg

  4. Australian Research Council Centre of Excellence for Coral Reef Studies, St Lucia, Queensland, Australia

    David I. Kline, Thomas Miard, Aaron Chai, Sophie Dove & Ove Hoegh-Guldberg

  5. Environmental Earth System Science, Stanford University, Stanford, CA, USA

    Lida Teneva & Robert B. Dunbar

  6. OceanX, New York, NY, USA

    Lida Teneva

  7. Department of Biological Science, Florida State University, Tallahassee, FL, USA

    Daniel K. Okamoto

  8. Department of Global Ecology, Carnegie Institution, Stanford, CA, USA

    Kenneth Schneider & Ken Caldeira

  9. Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

    Kenneth Schneider

  10. Faculty of Engineering, Architecture and Information Technology, University of Queensland, St Lucia, Australia

    Malcolm Marker

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Contributions

D.I.K., S.D. and O.H.-G. conceived of and designed the experiment. D.I.K, T.M., A.C. and M.M. designed and built the CP-FOCE experimental system. D.I.K., L.T., K.S., K.C., T.M., A.C., M.M., R.B.D., B.G.M., S.D. and O.H.-G. collected the data and conducted the field experiments. D.I.K., L.T. and D.K.O. analysed the data. D.I.K. and L.T. wrote the manuscript with input from all co-authors.

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Correspondence to David I. Kline.

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Supplementary information

Supplementary Information

Supplementary Fig. 1 and text summaries for Datasets 1–3.

Reporting Summary

Supplementary Dataset 1

Continuous pH, T, PAR, tides.

Supplementary Dataset 2

Discrete chem.

Supplementary Dataset 3

Buoyant weights.

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Kline, D.I., Teneva, L., Okamoto, D.K. et al. Living coral tissue slows skeletal dissolution related to ocean acidification. Nat Ecol Evol 3, 1438–1444 (2019). https://doi.org/10.1038/s41559-019-0988-x

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