Skip to main content

Advertisement

Log in

A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Anthropogenic elevation of atmospheric pCO2 is predicted to cause the pH of surface seawater to decline by 0.3–0.4 units by 2100 AD, causing a 50% reduction in seawater [CO3 2−] and undersaturation with respect to aragonite in high-latitude surface waters. We investigated the impact of CO2-induced ocean acidification on the temperate scleractinian coral Oculina arbuscula by rearing colonies for 60 days in experimental seawaters bubbled with air-CO2 gas mixtures of 409, 606, 903, and 2,856 ppm pCO2, yielding average aragonite saturation states (ΩA) of 2.6, 2.3, 1.6, and 0.8. Measurement of calcification (via buoyant weighing) and linear extension (relative to a 137Ba/138Ba spike) revealed that skeletal accretion was only minimally impaired by reductions in ΩA from 2.6 to 1.6, although major reductions were observed at 0.8 (undersaturation). Notably, the corals continued accreting new skeletal material even in undersaturated conditions, although at reduced rates. Correlation between rates of linear extension and calcification suggests that reduced calcification under ΩA = 0.8 resulted from reduced aragonite accretion, rather than from localized dissolution. Accretion of pure aragonite under each ΩA discounts the possibility that these corals will begin producing calcite, a less soluble form of CaCO3, as the oceans acidify. The corals’ nonlinear response to reduced ΩA and their ability to accrete new skeletal material in undersaturated conditions suggest that they strongly control the biomineralization process. However, our data suggest that a threshold seawater [CO3 2−] exists, below which calcification within this species (and possibly others) becomes impaired. Indeed, the strong negative response of O. arbuscula to ΩA = 0.8 indicates that their response to future pCO2-induced ocean acidification could be both abrupt and severe once the critical ΩA is reached.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Al-Horani FA, Al-Moghrabi SM, DeBeer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Google Scholar 

  • Barry J, Tyrrell T, Hansson L, Gattuso J-P 2009, Section 2.1: Atmospheric CO2 targets for ocean acidification perturbation experiments. In: Riebesell U, Fabry VJ, Gattuso J-P (eds) Guide to best practices for ocean acidification research. http://www.epoca-project.eu/index.php/Home/Guide-to-OA-Research/

  • Brewer PG (1997) Ocean chemistry of the fossil fuel CO2 signal: The haline signal of “business as usual”. Geophys Res Lett 24:1367–1369

    Article  CAS  Google Scholar 

  • Cohen AL, Holcomb MC (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127

    Google Scholar 

  • Cohen AL, McConnaughey TA (2003) A geochemical perspective on coral mineralization. In: Dove PM, Weiner S, De Yoreo JJ (eds) Biomineralization. Reviews in Mineralogy and Geochemistry 54: 151–187

  • Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: Insights into the biomineralization response to ocean acidification. Geochem Geophys Geosys 10:Q07005

    Article  CAS  Google Scholar 

  • Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

    Article  Google Scholar 

  • Doney SC, Schimel DS (2007) Carbon and climate system coupling on timescales from the Precambrian to the Anthropocene. Annu Rev Environ Resour 32:31–66

    Article  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432

    Article  CAS  Google Scholar 

  • Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811

    Article  CAS  PubMed  Google Scholar 

  • Gaetani GA, Cohen AL (2006) Element partitioning during precipitation of aragonite from seawater: A framework for understanding paleoproxies. Geochim Cosmochim Acta 70:4617–4634

    Article  CAS  Google Scholar 

  • Hawkins CP (1986) Pseudo-understanding of pseudoreplication: A cautionary note. Bull Ecol Soc Am 67:184–185

    Google Scholar 

  • Heiri OO, Lotter AF, Lemcke G (2001) Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol 25:101–110

    Article  Google Scholar 

  • Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia. J Exp Mar Biol Ecol 386:27–33

    Article  Google Scholar 

  • Houghton JT, Ding Y, Griggs DJ, Noguer M, Van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: The scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 881

    Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Jury CP, Whitehead RF, Szmant AM (2009) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973): bicarbonate concentrations best predict calcification rates. Global Change Biol 16:1632–1644

    Article  Google Scholar 

  • Keeling CD (1960) The concentration and isotopic abundances of carbon dioxide in the atmosphere. Tellus 12:200–203

    Article  Google Scholar 

  • Keeling RF, Piper SC, Bollenbacher AF, Walker JS (2009) Atmospheric CO2 records from sites in the SIO air sampling network. Trends: A Compendium of Data on Global Change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee, U.S.A., http://cdiac.ornl.gov/trends/co2/sio-mlo.html

  • Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CS, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: A guide for future research. Report of a Workshop Held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological Survey, p 88

  • Langdon C (2000) Review of experimental evidence for effects of CO2 on calcification of reef-builders. Proc 9th Int Coral Reef Symp:1091-1098

  • Langdon C, Atkinson MJ (2005) 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

    Google Scholar 

  • Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639–654

    Article  CAS  Google Scholar 

  • Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. U.S Department of Energy, Oak Ridge, Tennessee

    Google Scholar 

  • Luthi D, Le Floch M, Bereiter B, Blunier T, Barnola JM, Siegenthaler U, Raynaud D, Jouzel J, Fischer H, Kawamura K (2008) High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Nature 453:379–382

    Article  PubMed  CAS  Google Scholar 

  • Maier C, Hegeman J, Weinbauer MG, Gattuso JP (2009) Calcification of the cold-water coral Lophelia pertusa under ambient and reduced pH. Biogeosciences Discussions 6:1875–1901

    Article  Google Scholar 

  • Marubini F, Atkinson MJ (1999) Effects of lowered pH and elevated nitrate on coral calcification. Mar Ecol Prog Ser 188:117–121

    Article  CAS  Google Scholar 

  • Marubini F, Thake B (1999) Bicarbonate addition promotes coral growth. Limnol Oceanogr 44:716–720

    Article  CAS  Google Scholar 

  • Marubini F, Barnett H, Langdon C, Atkinson MJ (2001) Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar Ecol Prog Ser 220:153–162

    Article  CAS  Google Scholar 

  • Marubini F, Ferrier-Pages C, Cuif JP (2003) Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison. Proc R Soc Lond Ser B 270:179–184

    Article  Google Scholar 

  • Marubini F, Ferrier-Pages C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27:491–499

    Article  Google Scholar 

  • McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117

    Article  CAS  Google Scholar 

  • Miller MW (1995) Growth of a temperate coral: effects of temperature, light, depth, and heterotrophy. Mar Ecol Prog Ser 122:217–225

    Article  Google Scholar 

  • Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Am J Sci 283:780–799

    CAS  Google Scholar 

  • Neftel A, Moor E, Oeschger H, Stauffer B (1985) Evidence from polar ice cores for the increase in atmospheric CO2 in the past two centuries. Nature 315:45–47

    Article  CAS  Google Scholar 

  • Piniak GA (2002) Effects of symbiotic status, flow speed, and prey type on prey capture by the facultatively symbiotic temperature coral Oculina arbuscula. Mar Biol 141:449–455

    Article  Google Scholar 

  • Rahmstorf S, Cazenave A, Church JA, Hansen JE, Keeling RF, Parker DE, Somerville RCJ (2007) Recent climate observations compared to projections. Science 316:709

    Article  CAS  PubMed  Google Scholar 

  • Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society, London, p 55

    Google Scholar 

  • Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagés C, Jaubert J, Gattuso JP (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biol 9:1660–1668

    Article  Google Scholar 

  • Ries JB, Stanley SM, Hardie LA (2006) Scleractinian corals produce calcite, and grow more slowly, in artificial Cretaceous seawater. Geology 34:525–528

    Article  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso JP (2010) Response of the temperate coral Cladocora caespitosa to mid-and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosci 7:289–300

    Article  CAS  Google Scholar 

  • Rogers WH (1993) Regression standard errors in clustered samples. Stata Tech Bull 13:19–23

    Google Scholar 

  • Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Mar Chem 44:249–267

    Article  CAS  Google Scholar 

  • Royer DL, Berner RA, Montañez IP, Tabor NJ, Beerling DJ (2004) CO2 as a primary driver of Phanerozoic climate. Geol Soc Am Today 14:4–10

    Google Scholar 

  • Ruppert EE, Fox RS (1988) Seashore animals of the Southeast: a guide to common shallow-water invertebrates of the southeastern Atlantic Coast. University of South Carolina Press, Columbia, p 429

    Google Scholar 

  • Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293

    Article  CAS  Google Scholar 

  • Schulz KG, Barcelos e Ramos J, Zeebe RE, Riebesell U (2009) CO2 perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations. Biogeosci 6:2145–2153

    Article  CAS  Google Scholar 

  • Scott RW (1995) Global environmental controls on Cretaceous reefal ecosystems. In: Philip J, Skelton PW (eds) Palaeoenvironmental models for the benthic associations of Cretaceous carbonate platforms in the Tethyan realm. Palaeogeogr Palaeoclimatol Palaeoecol 119: 187–199

  • Tyrrell T, Zeebe RE (2004) History of carbonate ion concentration over the last 100 million years. Geochim Cosmochim Acta 68:3521–3530

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Greg Piniak at NOAA in Beaufort, North Carolina, for generously collecting and supplying the coral specimens used in this study. We thank Wade McGillis for providing gas standards. Michael Holcomb provided critical input in the design and implementation of these experiments. This work was supported with funding from UNC—Chapel Hill (to JBR), the Ocean and Climate Change Institute at WHOI (to JBR), the Tropical Research Institute at WHOI (to ALC), and the National Science Foundation (to ALC and DCM).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. B. Ries.

Additional information

Communicated by Environment Editor Prof. Rob van Woesik

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ries, J.B., Cohen, A.L. & McCorkle, D.C. A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula . Coral Reefs 29, 661–674 (2010). https://doi.org/10.1007/s00338-010-0632-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-010-0632-3

Keywords

Navigation