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Reversal of ocean acidification enhances net coral reef calcification

Nature volume 531, pages 362–365 (2016)Cite this article

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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.).

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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.

Author information

Authors and Affiliations

  1. Department of Global Ecology, Carnegie Institution for Science, Stanford, 94305, California, USA

    Rebecca Albright, Lilian Caldeira, Lester Kwiatkowski, Jana K. Maclaren, Yana Nebuchina, Julia Pongratz, Katharine L. Ricke, Kenneth Schneider, Marine Sesboüé, Kai Zhu & Ken Caldeira

  2. Bodega Marine Laboratory, University of California, Davis, Bodega Bay, California, 94923, USA

    Jessica Hosfelt & Aaron Ninokawa

  3. Stanford Nano Shared Facilities, Stanford University, Stanford, 94305, California, USA

    Jana K. Maclaren

  4. Department of Genetics, Stanford University School of Medicine, Stanford, 94305, California, USA

    Benjamin M. Mason

  5. Max Planck Institute for Meteorology, Bundesstraße 53, Hamburg, 20146, Germany

    Julia Pongratz

  6. Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, 14853, New York, USA

    Katharine L. Ricke

  7. The Interuniversity Institute for Marine Sciences, The H. Steinitz Marine Biology Laboratory, The Hebrew University of Jerusalem, Eilat, Israel

    Tanya Rivlin

  8. The Fredy and Nadine Herrman Institute of Earth Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Jerusalem, Israel

    Tanya Rivlin

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

    Kenneth Schneider

  10. Woods Hole Oceanographic Institution, Woods Hole, 02543, Massachusetts, USA

    Kathryn Shamberger

  11. Texas A&M University, College Station, Texas, 77843, USA

    Kathryn Shamberger

  12. Institute for Oceanographic and Limnological Research, Haifa, Israel

    Jacob Silverman

  13. School of Medical Sciences, The University of Sydney, Sydney, 2006, New South Wales, Australia

    Kennedy Wolfe

  14. Department of Biology, Stanford University, Stanford, 94305, California, USA

    Kai Zhu

  15. Department of BioSciences, Rice University, Houston, 77005, Texas, USA

    Kai Zhu

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  1. Rebecca Albright
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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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Competing interests

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, up − âd, 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
Full size table
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
Full size table

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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