Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Carbon dioxide addition to coral reef waters suppresses net community calcification


Coral reefs feed millions of people worldwide, provide coastal protection and generate billions of dollars annually in tourism revenue1. The underlying architecture of a reef is a biogenic carbonate structure that accretes over many years of active biomineralization by calcifying organisms, including corals and algae2. Ocean acidification poses a chronic threat to coral reefs by reducing the saturation state of the aragonite mineral of which coral skeletons are primarily composed, and lowering the concentration of carbonate ions required to maintain the carbonate reef. Reduced calcification, coupled with increased bioerosion and dissolution3, may drive reefs into a state of net loss this century4. Our ability to predict changes in ecosystem function and associated services ultimately hinges on our understanding of community- and ecosystem-scale responses. Past research has primarily focused on the responses of individual species rather than evaluating more complex, community-level responses. Here we use an in situ carbon dioxide enrichment experiment to quantify the net calcification response of a coral reef flat to acidification. We present an estimate of community-scale calcification sensitivity to ocean acidification that is, to our knowledge, the first to be based on a controlled experiment in the natural environment. This estimate provides evidence that near-future reductions in the aragonite saturation state will compromise the ecosystem function of coral reefs.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Study site.
Figure 2: Mean change in Ωarag and NCC.
Figure 3: Change in Ωarag and NCC by day.


  1. 1

    Spalding, M. et al. Mapping the global value and distribution of coral reef tourism. Mar. Policy 82, 104–113 (2017)

    Article  Google Scholar 

  2. 2

    Andersson, A. J. & Gledhill, D. Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann. Rev. Mar. Sci. 5, 321–348 (2013)

    Article  Google Scholar 

  3. 3

    Eyre, B. D., Andersson, A. J. & Cyronak, T. Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat. Clim. Chang. 4, 969–976 (2014)

    ADS  CAS  Article  Google Scholar 

  4. 4

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

  5. 5

    Bates, N. et al. A time-series view of changing ocean chemistry due to ocean uptake of anthropogenic CO2 and ocean acidification. Oceanography (Wash. D.C.) 27, 126–141 (2014)

    Article  Google Scholar 

  6. 6

    Le Quéré, C. et al. Global carbon budget 2014. Earth Syst. Sci. Data 7, 47–85 (2015)

    Google Scholar 

  7. 7

    Cao, L. & Caldeira, K. Atmospheric CO2 stabilization and ocean acidification. Geophys. Res. Lett. 35, (2008)

  8. 8

    Ricke, K. L., Orr, J. C., Schneider, K. & Caldeira, K. Risks to coral reefs from ocean carbonate chemistry changes in recent earth system model projections. Environ. Res. Lett. 8, 034003 (2013)

    ADS  Article  Google Scholar 

  9. 9

    Feely, R. A., Doney, S. C. & Cooley, S. R. Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography (Wash. D.C.) 22, 36–47 (2009)

    Article  Google Scholar 

  10. 10

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

    ADS  CAS  Article  Google Scholar 

  11. 11

    Smith, S. V. & Key, G. S. Carbon dioxide and metabolism in marine environments. Limnol. Oceanogr. 20, 493–495 (1975)

    ADS  CAS  Article  Google Scholar 

  12. 12

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

    ADS  Article  Google Scholar 

  13. 13

    Langdon, C. & Atkinson, M. J. Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J. Geophys. Res. 110, (2005)

  14. 14

    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 

  15. 15

    Arnold, T. et al. Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE 7, e35107 (2012)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Koop, K. et al. ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull. 42, 91–120 (2001)

    CAS  Article  Google Scholar 

  17. 17

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

    Article  Google Scholar 

  18. 18

    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)

    ADS  CAS  Article  Google Scholar 

  19. 19

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

    Article  Google Scholar 

  20. 20

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

    ADS  CAS  Article  Google Scholar 

  21. 21

    Enochs, I. C. et al. Shift from coral to macroalgae dominance on a volcanically acidified reef. Nat. Clim. Chang. 5, 1083–1088 (2015)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Chang. 3, 683–687 (2013)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Price, N. N., Martz, T. R., Brainard, R. E. & Smith, J. E. Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS ONE 7, e43843 (2012)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017)

    ADS  CAS  Article  Google Scholar 

  25. 25

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

    ADS  CAS  Article  Google Scholar 

  26. 26

    Anthony, K. R. N. Coral reefs under climate change and ocean acidification: challenges and opportunities for management and policy. Annu. Rev. Environ. Resour. 41, 59–81 (2016)

    Article  Google Scholar 

  27. 27

    Cooley, S. R., Kite-Powell, H. L. & Doney, S. C. Ocean acidification’s potential to alter global marine ecosystem services. Oceanography (Wash. D.C.) 22, 172–181 (2009)

    Article  Google Scholar 

  28. 28

    Pascal, N. et al. Economic valuation of coral reef ecosystem service of coastal protection: a pragmatic approach. Ecosyst. Serv. 21, 72–80 (2016)

    Article  Google Scholar 

  29. 29

    Pendleton, L. H. Valuing coral reef protection. Ocean Coast. Manage. 26, 119–131 (1995)

    Article  Google Scholar 

  30. 30

    Spalding, M. D. & Brown, B. E. Warm-water coral reefs and climate change. Science 350, 769–771 (2015)

    ADS  CAS  Article  Google Scholar 

  31. 31

    Bresnahan, P. J., Martz, T. R., Takeshita, Y., Johnson, K. S. & LaShomb, M. Best practices for autonomous measurement of seawater pH with the Honeywell Durafet. Methods Oceanogr. 9, 44–60 (2014)

    Article  Google Scholar 

  32. 32

    Brewer, P. G. & Goldman, J. C. Alkalinity changes generated by phytoplankton growth. Limnol. Oceanogr. 21, 108–117 (1976)

    ADS  CAS  Article  Google Scholar 

  33. 33

    Berner, R. A., Scott, M. R. & Thomlinson, C. Carbonate alkalinity in the pore waters of anoxic marine sediments. Limnol. Oceanogr. 15, 544–549 (1970)

    ADS  CAS  Article  Google Scholar 

  34. 34

    Gaines, A. G. & Pilson, M. E. Q. Anoxic water in the Pettaquamscutt River. Limnol. Oceanogr. 17, 42–50 (1972)

    ADS  CAS  Article  Google Scholar 

  35. 35

    Kinsey, D. W. Alkalinity changes and coral reef calcification. Limnol. Oceanogr. 23, 989–991 (1978)

    ADS  CAS  Article  Google Scholar 

  36. 36

    Gattuso, J. P., Allemand, D. & Frankignoulle, M. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am. Zool. 39, 160–183 (1999)

    CAS  Article  Google Scholar 

  37. 37

    Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to Best Practices for Ocean CO2 Measurements 191 (PICES Special Publication, 2007)

  38. 38

    Mehrbach, C., Culberson, C. H., Hawley, J. E. & Pytkowicz, R. M. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897–907 (1973)

    ADS  CAS  Article  Google Scholar 

  39. 39

    Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res. A 34, 1733–1743 (1987)

    ADS  CAS  Article  Google Scholar 

  40. 40

    Dickson, A. G. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Res. A 37, 755–766 (1990)

    ADS  CAS  Article  Google Scholar 

  41. 41

    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)

    CAS  Article  Google Scholar 

  42. 42

    Carter, B. R., Radich, J. A., Doyle, H. L. & Dickson, A. G. An automated system for spectrophotometric seawater pH measurements. Limnol. Oceanogr. Methods 11, 16–27 (2013)

    Article  Google Scholar 

  43. 43

    Liu, X., Patsavas, M. C. & Byrne, R. H. Purification and characterization of meta-cresol purple for spectrophotometric seawater pH measurements. Environ. Sci. Technol. 45, 4862–4868 (2011)

    ADS  CAS  Article  Google Scholar 

  44. 44

    Wilson, J. F. in Techniques for Water Resources Investigations of the U.S. Geological Survey, Book 3 (U.S. Government Printing Office, 1968)

  45. 45

    Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A. & Peterson, B. J. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56, 1801–1808 (1999)

    CAS  Article  Google Scholar 

  46. 46

    Grasshoff, K., Kremling, K. & Ehrhardt, M. Methods of Seawater Analysis (Wiley-VCH, 1999)

Download references


We thank R. Dunbar for the use of his laboratory and D. Mucciarone for laboratory assistance; the Australian Institute of Marine Science for scientific and technical support; and the following people for their support in the field and/or laboratory: M. Byrne, T. Hill, L. Caldeira, R. Johnson, D. Ross and the staff of the One Tree Island Research Station. Expedition and staff support was provided by the Carnegie Institution for Science. Additional support for staff, but not expedition expenses, was provided by the California Academy of Sciences and the Fund for Innovative Climate and Energy Research. This work was permitted by the Great Barrier Reef Marine Park Authority under permit G14/36863.1.

Author information




R.A., Y.T. and K.C. conceived and designed the project, conducted pilot studies, and collected preliminary data. R.A., Y.T., D.A.K., A.N., K.W., T.R., Y.N., J.Y. and K.C. performed the experiments. R.A. and K.C. performed computational analyses. R.A. wrote the manuscript with input from Y.T., D.A.K. and K.C. All co-authors reviewed and approved the final manuscript.

Corresponding author

Correspondence to Rebecca Albright.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks H. Kayanne, J. Lough and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Figure 1 Relationships between alkalinity and dye for experiment and control days.

af, Relationships between alkalinity and dye for a representative experiment day (n = 20 independent experiments, 29 September 2016 shown here) and control day (n = 10 independent experiments, 30 October 2016 shown here). a, b, Dye concentrations; c, d, alkalinities; e, f, alkalinity anomalies versus dye concentrations. Linear regressions were fit to alkalinity–dye data using least-squares residuals. d, On control days, the observed (measured) alkalinities closely agree with predicted values for each station. Comparing the upstream and downstream alkalinity–dye ratios provides an estimate of the effect of CO2 enrichment on NCC, as described in the Methods. e, On experiment days (n = 20 independent experiments), if CO2 suppresses NCC, the drawdown in alkalinity is smaller in areas with more CO2 (and more dye) than in areas with less CO2 (and less dye). This effect yields a positive correlation between dye and alkalinity (that is, a positive alkalinity–dye slope) that increases as the water mass moves across the reef—in other words, the alkalinity–dye slope at the downstream transect is greater than that of the upstream transect. f, On control days (n = 10 independent experiments), when dye but no CO2 was added, alkalinity and dye were not correlated, and the mean alkalinity–dye slopes for the upstream and downstream transects did not differ from zero.

Extended Data Figure 2 Time series of pH inside the header tank during the 60-min pumping period.

Solid lines represent control days, and dashed lines represent experiment days.

Extended Data Figure 3 Results of the multivariate regression analysis.

a, b, Unique offsets by station (xs) for the upstream and downstream transects (mean ± s.e.m., n = 10). c, d, Magnitude of offsets by day (yd) for upstream and downstream transects. e, f, Alkalinity–dye ratios by day (rd), for upstream and downstream transects. g, h, Mean background alkalinities by day (âd) for upstream and downstream transects. In ch, bars represent central values as calculated by the multivariate regression described in the ‘Mathematical explanation’ section of the Methods, and error bars represent s.e.m. (for c, e and h, n = 11; for d, f and h, n = 15).

Extended Data Figure 4 Mean Ωarag and NCC rates for experiment and control days.

Background and in-plume Ωarag and NCC values (mean ± s.e.m.) for experiment (n = 20 independent experiments) and control (n = 10 independent experiments) days. Error bars reflect underlying natural variability (that is, day-to-day, hour-to-hour), because Ωarag and NCC varied based on time of day and light availability.

Extended Data Figure 5 Relationship between the change in NCC and background NCC across all experiment days.

Linear regression using least-squares residuals (n = 20 independent experiments).

Extended Data Figure 6 Change in NCC by day.

Change in NCC inside of the plume compared to background conditions (mean ± s.e.m.) for experiment (n = 20 independent experiments) and control (n = 10 independent experiments) days. On all 20 experiment days, we detected a statistically significant reduction in calcification within the plume (paired t-tests). On control days, in-plume NCC was higher than background NCC on five days, and lower than background NCC on five days.

Extended Data Figure 7 Physical and chemical conditions of the study site.

Time series of environmental data from SeapHOx and SAMI sensors. Instruments logged at 10-min intervals over the duration of the study. Gaps in the data correspond to when the instruments were removed from the reef for maintenance. a, PAR; b, temperature; c, pressure; d, salinity; e, dissolved oxygen; f, pH.

Extended Data Table 1 Dates, times, predicted heights of low tide and mean PAR for all days
Extended Data Table 2 Mean ± s.e.m. values for salinity, NH4+ and NO2 + NO3 during and control days

Supplementary information

Supplementary Information

This file contains the Computer Code. (PDF 754 kb)

Life Sciences Reporting Summary (PDF 86 kb)

Supplementary Table 1

Raw data for chemical and physical parameters across all days and station locations (measured and calculated). Details regarding measurements and associated errors are provided in the Methods. (XLSX 139 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Albright, R., Takeshita, Y., Koweek, D. et al. Carbon dioxide addition to coral reef waters suppresses net community calcification. Nature 555, 516–519 (2018).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing