Reversal of ocean acidification enhances net coral reef calcification

Abstract

Approximately one-quarter of the anthropogenic carbon dioxide released into the atmosphere each year is absorbed by the global oceans, causing measurable declines in surface ocean pH, carbonate ion concentration ([CO32−]), and saturation state of carbonate minerals (Ω)1. This process, referred to as ocean acidification, represents a major threat to marine ecosystems, in particular marine calcifiers such as oysters, crabs, and corals. Laboratory and field studies2,3 have shown that calcification rates of many organisms decrease with declining pH, [CO32−], and Ω. Coral reefs are widely regarded as one of the most vulnerable marine ecosystems to ocean acidification, in part because the very architecture of the ecosystem is reliant on carbonate-secreting organisms4. Acidification-induced reductions in calcification are projected to shift coral reefs from a state of net accretion to one of net dissolution this century5. While retrospective studies show large-scale declines in coral, and community, calcification over recent decades6,7,8,9,10,11,12, determining the contribution of ocean acidification to these changes is difficult, if not impossible, owing to the confounding effects of other environmental factors such as temperature. Here we quantify the net calcification response of a coral reef flat to alkalinity enrichment, and show that, when ocean chemistry is restored closer to pre-industrial conditions, net community calcification increases. In providing results from the first seawater chemistry manipulation experiment of a natural coral reef community, we provide evidence that net community calcification is depressed compared with values expected for pre-industrial conditions, indicating that ocean acidification may already be impairing coral reef growth.

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Figure 1: Study site and experimental design.
Figure 2: Chemical conditions for control (N = 7) and experiment (N = 15) days (mean ± 1 s.e.m.).
Figure 3: Relationships between alkalinity and dye for control (N = 7) and experiment (N = 15) days.
Figure 4: Alkalinity–dye slopes and percentage change in net calcification for control (N = 7) and experiment (N = 15) days (mean ± 1 s.e.m.).

References

  1. 1

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

    Google Scholar 

  2. 2

    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)

    CAS  Article  Google Scholar 

  3. 3

    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)

    ADS  Article  Google Scholar 

  4. 4

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

    Article  Google Scholar 

  5. 5

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

  6. 6

    Silverman, J. et al. Community calcification in Lizard Island, Great Barrier Reef: a 33 year perspective. Geochim. Cosmochim. Acta 144, 72–81 (2014)

    CAS  ADS  Article  Google Scholar 

  7. 7

    De’ath, G., Lough, J. M. & Fabricius, K. E. Declining coral calcification on the Great Barrier Reef. Science 323, 116–119 (2009)

    ADS  Article  Google Scholar 

  8. 8

    Cooper, T. F., De’Ath, G., Fabricius, K. E. & Lough, J. M. Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Glob. Change Biol. 14, 529–538 (2008)

    ADS  Article  Google Scholar 

  9. 9

    Manzello, D. P. Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29, 749–758 (2010)

    ADS  Article  Google Scholar 

  10. 10

    Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M. & McCorkle, D. C. Ocean warming slows coral growth in the central Red Sea. Science 329, 322–325 (2010)

    CAS  ADS  Article  Google Scholar 

  11. 11

    Tanzil, J. T. et al. Regional decline in growth rates of massive Porites corals in Southeast Asia. Glob. Change Biol. 19, 3011–3023 (2013)

    ADS  Article  Google Scholar 

  12. 12

    Silverman, J. et al. Carbon turnover rates in the One Tree Island reef: a 40-year perspective. J. Geophys. Res. 117, G03023 (2012)

  13. 13

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

  14. 14

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

    Article  Google Scholar 

  15. 15

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

    ADS  Article  Google Scholar 

  16. 16

    Langdon, C. & Atkinson, M. 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, C09S07 (2005)

  17. 17

    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 

  18. 18

    Cyronak, T., Schulz, K. G. & Jokiel, P. L. The Omega myth: what really drives lower calcification rates in an acidifying ocean. ICES J. Mar. Sci. http://dx.doi.org/10.1093/icesjms/fsv075 (2015)

  19. 19

    Shaw, E. C., Phinn, S. R., Tilbrook, B. & Steven, A. Natural in situ relationships suggest coral reef calcium carbonate production will decline with ocean acidification. Limnol. Oceanogr. 60, 777–788 (2015)

    CAS  ADS  Article  Google Scholar 

  20. 20

    Albright, R., Benthuysen, J., Cantin, N., Caldeira, K. & Anthony, K. Coral reef metabolism and carbon chemistry dynamics of a coral reef flat. Geophys. Res. Lett. 42, 3980–3988 (2015)

    CAS  ADS  Article  Google Scholar 

  21. 21

    Koweek, D. et al. Environmental and ecological controls of coral community metabolism on Palmyra Atoll. Coral Reefs 34, 339–351 (2014)

    ADS  Article  Google Scholar 

  22. 22

    Shaw, E. C., McNeil, B. I. & Tilbrook, B. Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J. Geophys. Res. 117, C03038 (2012)

  23. 23

    Albright, R., Langdon, C. & Anthony, K. R. N. Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, central Great Barrier Reef. Biogeosciences 10, 6747–6758 (2013)

    CAS  ADS  Article  Google Scholar 

  24. 24

    Falter, J. L., Lowe, R. J., Zhang, Z. & McCulloch, M. Physical and biological controls on the carbonate chemistry of coral reef waters: effects of metabolism, wave forcing, sea level, and geomorphology. PLoS ONE 8, e53303 (2013)

    CAS  ADS  Article  Google Scholar 

  25. 25

    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 

  26. 26

    Helmle, K. P., Dodge, R. E., Swart, P. K., Gledhill, D. K. & Eakin, C. M. Growth rates of Florida corals from 1937 to 1996 and their response to climate change. Nature Commun. 2, 215 (2011)

    ADS  Article  Google Scholar 

  27. 27

    Tierney, J. E. et al. Tropical sea surface temperatures for the past four centuries reconstructed from coral archives. Paleoceanography 30, 226–252 (2015)

    ADS  Article  Google Scholar 

  28. 28

    Lough, J. M. & Cooper, T. F. New insights from coral growth band studies in an era of rapid environmental change. Earth Sci. Rev. 108, 170–184 (2011)

    CAS  ADS  Article  Google Scholar 

  29. 29

    National Research Council. Climate Intervention: Carbon Dioxide Removal and Reliable Sequestration (National Academies Press, 2015)

  30. 30

    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 

  31. 31

    Friedlander, S. K., Turner, J. R. & Hering, S. V. A new method for estimating dry deposition velocities for atmospheric aerosols. J. Aerosol Sci. 17, 240–244 (1986)

    CAS  ADS  Article  Google Scholar 

  32. 32

    Andersson, A. J. & Mackenzie, F. T. Revisiting four scientific debates in ocean acidification research. Biogeosciences 9, 893–905 (2012)

    CAS  ADS  Article  Google Scholar 

  33. 33

    Anderson, L. G., Haraldsson, C. & Lindegren, R. Gran linearization of potentiometric Winkler titrations. Mar. Chem. 37, 179–190 (1992)

    CAS  Article  Google Scholar 

  34. 34

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

    CAS  ADS  Article  Google Scholar 

  35. 35

    Riebesell, U., Fabry, V. J., Hansson, L. & Gattuso, J. P. Guide to Best Practices for Ocean Acidification Research and Data Reporting (Publications Office of the European Union, 2010)

  36. 36

    Lewis, E. & Wallace, D. W. R. Program developed for CO2 system calculations (US Department of Energy Oak Ridge National Laboratory, 1998)

  37. 37

    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)

    CAS  ADS  Article  Google Scholar 

  38. 38

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

    CAS  ADS  Article  Google Scholar 

  39. 39

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

    CAS  ADS  Article  Google Scholar 

  40. 40

    Wilson, J. F. in Techniques for Water Resources Investigations of the U.S. Geological Survey, Book 3, Ch. A12 (U.S. Government Printing Office, 1968)

    Google Scholar 

  41. 41

    Dickson, A. G., Sabine, C. L. & Christian, J. R. Guide to Best Practices for Ocean CO2 Measurements (North Pacific Marine Science Organization, 2007)

  42. 42

    Holmes, R. M., Aminot, A., Kerouel, 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 

  43. 43

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

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Acknowledgements

We thank R. Dunbar for the use of his laboratory and D. Mucciarone for laboratory training and assistance; the Australian Institute of Marine Science for scientific and technical support; Y. Estrada for graphics assistance; and the following people for their support in the field and/or laboratory: M. Byrne, A. Chai, R. Graham, T. Hill, D. Kline, B. Kravitz, J. Reiffel, D. Ross, E. Shaw, and the staff of the One Tree Island Research Station. Expedition and staff support was provided by the Carnegie Institution for Science. Some additional support for staff, but not expedition expenses, was provided by 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.

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Authors

Contributions

R.A., J.K.M., K.Sc., J.S., and K.C. conceived and designed the project. J.K.M., K.Sc., J.S., J.P., K.L.R., and K.Sh. conducted pilot studies and collected preliminary data. R.A., L.K., L.C., B.M.M., Y.N., T.R., M.S., K.W., A.N., J.H., and K.C. performed the experiments. R.A. and K.C. performed the computational analyses. K.Z. assisted with statistical analyses. R.A. wrote the manuscript with input from K.C. All co-authors reviewed and approved the final manuscript.

Corresponding author

Correspondence to Rebecca Albright.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Theoretical representations of the null, H0, and alternative, H1, hypotheses.

a, In H0, the reef does not take up added alkalinity; here, the change in alkalinity between the upstream and downstream transects would not be systematically related to the dye concentration, and the ratio of the alkalinity–dye relationship, r, would not be expected to change between the upstream and downstream locations (that is, rup = rdown). b, In H1, reef uptake of added alkalinity occurs; here, areas with more alkalinity (and more dye) change at a different rate than areas with less alkalinity (and less dye), resulting in a change in the alkalinity–dye slope (that is, rup > rdown).

Extended Data Figure 2 Community composition of the reef flat study area.

Percentage cover by benthic type is as follows: crustose coralline algae (39%), live coral (17%), turf algae (16%), macroalgae (19%), sand/rubble (9%), and Halimeda (5%).

Extended Data Figure 3 Schematic of study area showing meter-spacing of station locations for the 9 upstream (U) stations and 15 downstream (D) transects.

Numbers indicate the metre-spacing from the centre of the study area, denoted as U0 for the upstream transect and D0 for the downstream transect. The outermost sampling locations for the upstream (−U16, U16) and downstream (−D16, D16) transects define the four outermost corners of the study area and were strategically positioned to lie outside the alkalinity–dye plume, rendering zero dye concentrations and added alkalinity.

Extended Data Figure 4 Mean chemical conditions for control (N = 7) and experiment (N = 15) days.

a, b, Carbonate ion concentrations ([CO32−]); c, d, p CO 2 ; e, f, dissolved inorganic carbon concentrations (CT) for upstream and downstream transects. Error bars, which represent standard errors, are indicative of day-to-day and hour-to-hour variability (not measurement error); estimates of measurement error are provided in the Methods. Total alkalinity (AT), dye concentration, aragonite saturation state (Ωarag), and total pH (pHT) are provided in Figs 2 and 3.

Extended Data Figure 5 Comparison of alkalinity values before and after ‘offset-corrections’ used in the multivariate regression analysis.

a, b, Measured (that is, ‘raw’) alkalinity values. c, d, ‘Offset-corrected’ alkalinity values. Bold lines represent average conditions; dashed lines show results by day. See Supplementary Information.

Extended Data Figure 6 Results of the multivariate regression analysis.

a, b, Unique offsets by station, xs, for the upstream and downstream transects. 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. Error bars represent standard errors. See Supplementary Information.

Extended Data Figure 7 Results of the multivariate regression were used to calculate the additional alkalinity uptake (that is, Gincrease) and background alkalinity uptake (that is, Gbackground) by day.

a, Fraction of added alkalinity taken up by the reef by day, given by (1 – (rdown/rup), equation (1) of main text). b, Background reef uptake by day, given by (âd, upâd, down). Error bars represent standard errors. See Supplementary Information.

Extended Data Table 1 Schedule for control and experiment days, including date, time, predicted height of low tide, and mean photosynthetically active radiation (PAR) for the 1 h study period
Extended Data Table 2 Mean (±1 s.e.m.) values for temperature (T), salinity (S), ammonium (NH4), nitrite and nitrate (NO2 + NO3), and dissolved oxygen (DO) during the 22-day study period

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Notes, Supplementary Equations | Mathematical explanation (and computer code) of multivariate regression approach used to calculate alkalinity-dye ratios (slopes) and mean background alkalinities (y-intercepts), Supplementary Equations for calculating calcification, the mathematical explanation of mixed effects model and Supplementary Notes regarding underlying hypotheses. (PDF 823 kb)

Supplementary Table 1

This table contains the 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 92 kb)

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Albright, R., Caldeira, L., Hosfelt, J. et al. Reversal of ocean acidification enhances net coral reef calcification. Nature 531, 362–365 (2016). https://doi.org/10.1038/nature17155

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