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Carbon dioxide addition to coral reef waters suppresses net community calcification
- Rebecca Albright1,2,
- Yuichiro Takeshita1,3,
- David A. Koweek1,
- Aaron Ninokawa4,
- Kennedy Wolfe5,
- Tanya Rivlin6,7,
- Yana Nebuchina1,
- Jordan Young4 &
- …
- Ken Caldeira1
Naturevolume 555, pages516–519 (2018)Cite this article
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138Citations
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Abstract
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 anin 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.
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References
Spalding, M. et al. Mapping the global value and distribution of coral reef tourism.Mar. Policy82, 104–113 (2017)
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)
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)
Silverman, J., Lazar, B., Cao, L., Caldeira, K. & Erez, J. Coral reefs may start dissolving when atmospheric CO2 doubles.Geophys. Res. Lett.36, (2009)
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)
Le Quéré, C. et al. Global carbon budget 2014.Earth Syst.Sci. Data7, 47–85 (2015)
Cao, L. & Caldeira, K. Atmospheric CO2 stabilization and ocean acidification.Geophys. Res. Lett.35, (2008)
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)
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)
Albright, R. et al. Reversal of ocean acidification enhances net coral reef calcification.Nature531, 362–365 (2016)
Smith, S. V. & Key, G. S. Carbon dioxide and metabolism in marine environments.Limnol. Oceanogr.20, 493–495 (1975)
Chan, N. C. & Connolly, S. R. Sensitivity of coral calcification to ocean acidification: a meta-analysis.Glob. Chang. Biol.19, 282–290 (2013)
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)
Norby, R. J. & Zak, D. R. Ecological lessons from free-air CO2 enrichment (FACE) experiments.Annu. Rev. Ecol. Evol. Syst.42, 181–203 (2011)
Arnold, T. et al. Ocean acidification and the loss of phenolic substances in marine plants.PLoS ONE7, e35107 (2012)
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)
Andersson, A. et al. Understanding ocean acidification impacts on organismal to ecological scales.Oceanography (Wash. D.C.)28, 16–27 (2015)
Dove, S. G. et al. Future reef decalcification under a business-as-usual CO2 emission scenario.Proc. Natl Acad. Sci. USA110, 15342–15347 (2013)
Kline, D. I. et al. A short-termin situ CO2 enrichment experiment on Heron Island (GBR).Sci. Rep.2, 413 (2012)
Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations.Nat. Clim. Chang.1, 165–169 (2011)
Enochs, I. C. et al. Shift from coral to macroalgae dominance on a volcanically acidified reef.Nat. Clim. Chang.5, 1083–1088 (2015)
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)
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 ONE7, e43843 (2012)
Hughes, T. P. et al. Coral reefs in the Anthropocene.Nature546, 82–90 (2017)
Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals.Nature543, 373–377 (2017)
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)
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)
Pascal, N. et al. Economic valuation of coral reef ecosystem service of coastal protection: a pragmatic approach.Ecosyst. Serv.21, 72–80 (2016)
Pendleton, L. H. Valuing coral reef protection.Ocean Coast. Manage.26, 119–131 (1995)
Spalding, M. D. & Brown, B. E. Warm-water coral reefs and climate change.Science350, 769–771 (2015)
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)
Brewer, P. G. & Goldman, J. C. Alkalinity changes generated by phytoplankton growth.Limnol. Oceanogr.21, 108–117 (1976)
Berner, R. A., Scott, M. R. & Thomlinson, C. Carbonate alkalinity in the pore waters of anoxic marine sediments.Limnol. Oceanogr.15, 544–549 (1970)
Gaines, A. G. & Pilson, M. E. Q. Anoxic water in the Pettaquamscutt River.Limnol. Oceanogr.17, 42–50 (1972)
Kinsey, D. W. Alkalinity changes and coral reef calcification.Limnol. Oceanogr.23, 989–991 (1978)
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)
Dickson, A. G., Sabine, C. L. & Christian, J. R.Guide to Best Practices for Ocean CO2 Measurements191 (PICES Special Publication, 2007)
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)
Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media.Deep-Sea Res. A34, 1733–1743 (1987)
Dickson, A. G. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K.Deep-Sea Res. A37, 755–766 (1990)
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)
Carter, B. R., Radich, J. A., Doyle, H. L. & Dickson, A. G. An automated system for spectrophotometric seawater pH measurements.Limnol. Oceanogr. Methods11, 16–27 (2013)
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)
Wilson, J. F. inTechniques for Water Resources Investigations of the U.S. Geological Survey, Book 3 (U.S. Government Printing Office, 1968)
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)
Grasshoff, K., Kremling, K. & Ehrhardt, M.Methods of Seawater Analysis (Wiley-VCH, 1999)
Acknowledgements
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
Authors and Affiliations
Department of Global Ecology, Carnegie Institution for Science, Stanford, 94305, California, USA
Rebecca Albright, Yuichiro Takeshita, David A. Koweek, Yana Nebuchina & Ken Caldeira
California Academy of Sciences, San Francisco, 94118, California, USA
Rebecca Albright
Monterey Bay Aquarium Research Institute, Moss Landing, 95039, California, USA
Yuichiro Takeshita
UC Davis Bodega Marine Lab, Bodega Bay, 94923, California, USA
Aaron Ninokawa & Jordan Young
School of Medical Sciences, The University of Sydney, Sydney, 2006, New South Wales, Australia
Kennedy Wolfe
The Interuniversity Institute for Marine Sciences, The H. Steinitz Marine Biology Laboratory, The Hebrew University of Jerusalem, Coral Beach, Eilat, 8810300, Israel
Tanya Rivlin
The Fredy and Nadine Herrman Institute of Earth Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Jerusalem, 9190401, Israel
Tanya Rivlin
- Rebecca Albright
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- Yuichiro Takeshita
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- David A. Koweek
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- Aaron Ninokawa
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- Tanya Rivlin
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- Yana Nebuchina
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- Jordan Young
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Contributions
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 toRebecca Albright.
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Extended data figures and tables
Extended Data Figure 1 Relationships between alkalinity and dye for experiment and control days.
a–f, 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. Inc–h, 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. (forc,e andh,n = 11; ford,f andh,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 (pairedt-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.
Supplementary information
Supplementary Information
This file contains the Computer Code. (PDF 754 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)
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Albright, R., Takeshita, Y., Koweek, D.et al. Carbon dioxide addition to coral reef waters suppresses net community calcification.Nature555, 516–519 (2018). https://doi.org/10.1038/nature25968
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