Abstract
The response of Acropora digitifera to ocean acidification is determined using geochemical proxy measurements of the skeletal composition of A. digitifera cultured under a range of pH levels. We show that the chemical composition (δ11B, Sr/Ca, Mg/Ca, and Ba/Ca) of the coral skeletons can provide quantitative constraints on the effects of seawater pH on the pH in the calcification fluid (pHCF) and the mechanisms controlling the incorporation of trace elements into coral aragonite. With the decline of seawater pH, the skeletal δ11B value decreased, while the Sr/Ca ratio showed an increasing trend. The relationship between Mg/Ca and Ba/Ca versus seawater pH was not significant. Inter-colony variation of δ11B was insignificant, although inter-colony variation was observed for Ba/Ca. The decreasing trend of pHCF calculated from δ11B was from ~8.5, 8.4, and 8.3 for seawater pH of ~8.1, 7.8, and 7.4, respectively. Model calculations based on Sr/Ca and pHCF suggest that upregulation of pHCF occurs via exchange of H+ with Ca2+ with kinetic effects (Rayleigh fractionation), reducing Sr/Ca relative to inorganic deposition of aragonite from seawater. We show that it is possible to constrain the overall carbonate chemistry of the calcifying fluid with estimates of the carbonate saturation of the calcifying fluid (Ω CF) being derived from skeletal Sr/Ca and pHCF (from δ11B). These estimates suggest that the aragonite saturation state of the calcifying fluid Ω CF is elevated by a factor of 5–10 relative to ambient seawater under all treatment conditions.
References
Al-Horani F, Al-Moghrabi S, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426
Alibert C, Kinsley L, Fallon S, McCulloch M, Berkelmans R, McAllister F (2003) Source of trace element variability in Great Barrier Reef corals affected by the Burdekin flood plumes. Geochim Cosmochim Acta 67:231–246
Allemand D, Ferrier-Pages C, Furla P, Houlbreque F, Puverel S, Reynaud S, Tambutte E, Tambutte S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C R Palevol 3:453–467
Allison N, Finch A, Sutton S, Newville M (2001) Strontium heterogeneity and speciation in coral aragonite: Implications for the strontium paleothermometer. Geochim Cosmochim Acta 65:2669–2676
Allison N, Cohen I, Finch A, Erez J, EMIF (2011) Controls on Sr/Ca and Mg/Ca in scleractinian corals: the effects of Ca-ATPase and transcellular Ca channels on skeletal chemistry. Geochim Cosmochim Acta 75:6350–6360
Anthony K, Maynard J, Diaz-Pulido G, Mumby P, Marshall P, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Change Biol 17:1798–1808
Burton EA, Walter LM (1987) Relative precipitation rates of aragonite and Mg calcite from seawater: temperature or carbonate ion control? Geology 15:111–1114
Beck J, Recy J, Taylor F, Edwards R, Cabioch G (1997) Abrupt changes in early Holocene tropical sea surface temperature derived from coral records. Nature 385:705–707
Chalker B, Taylor D (1975) Light-enhanced calcification, and role of oxdative-phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc Ser B-Bio 190:323–331
Cohen A, Hart S (2004) Deglacial sea surface temperatures of the western tropical Pacific: a new look at old coral. Paleoceanography. doi:10.1029/2004PA001084
Correge T (2006) Sea surface temperature and salinity reconstruction from coral geochemical tracers. Palaeogeogr Palaeoclimatol Palaeoecol 232:408–428
De Carlo TM, Gaetani GA, Holcomb M, Cohen AL (2015) Experimental determination of factors controlling U/Ca of aragonite precipitated from seawater: Implications for interpreting coral skeleton. Geochim Cosmochim Acta 162:151–165
deVilliers S, Shen G, Nelson B (1994) The Sr/Ca-temperature relationship in coralline aragonite-Influence of variability in (Sr/Ca)seawater and skeletal growth-parameters. Geochim Cosmochim Acta 58:197–208
Dickson A (1990) Thermodynamics of the dissociation of boric-acid in synthetic seawater from 273.15 to 318.15 K. Deep Sea Res 37:755–766
Douville E, Paterne M, Cabioch G, Louvat P, Gaillardet J, Juillet-Leclerc A, Ayliffe L (2010) Abrupt sea surface pH change at the end of the Younger Dryas in the central sub-equatorial Pacific inferred from boron isotope abundance in corals (Porites). Biogeosciences 7:2445–2459
Elderfield H, Bertram C, Erez J (1996) Biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate. Earth Planet Sci Lett 142:409–423
Fallon S, McCulloch M, van Woesik R, Sinclair D (1999) Corals at their latitudinal limits: laser ablation trace element systematics in Porites from Shirigai Bay, Japan. Earth Planet Sci Lett 172:221–238
Finch A, Allison N (2003) Strontium in coral aragonite: 2. Sr coordination and the long-term stability of coral environmental records. Geochim Cosmochim Acta 67:4519–4527
Finch A, Allison N (2008) Mg structural state in coral aragonite and implications for the paleoenvironmental proxy. Geophys Res Lett. doi:10.1029/2008GL033543
Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457
Gaetani G, Cohen A (2006) Element partitioning during precipitation of aragonite from seawater: A framework for understanding paleoproxies. Geochim Cosmochim Acta 70:4617–4634
Gattuso J, Allemand D, Frankignoulle M (1999) 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
Gattuso J, Frankignoulle M, Bourge I, Romaine S, Buddemeier R (1998) Effect of calcium carbonate saturation of seawater on coral calcification. Glob Planet Change 18:37–46
Gladfelter E (2007) Skeletal development in Acropora palmata (Lamarck 1816): a scanning electron microscope (SEM) comparison demonstrating similar mechanisms of skeletal extension in axial versus encrusting growth. Coral Reefs 26:883–892
Grove C, Brummer G, Kasper S, Zinke J, Pfeiffer M, Garbe-Schonberg D (2013) Confounding effects of coral growth and high SST variability on skeletal Sr/Ca: implications for coral paleothermometry. Geochem Geophys Geosyst 14:1277–1293
Hemming N, Hanson G (1992) Boron isotopic composition and concentration in modern marine carbonate. Geochim Cosmochim Acta 56:537–543
Holcomb M, Venn AA, Tambutte E, Tambutte S, Allemand D, Trotter J, McCulloch M (2014) Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep 4:4
Holcomb M, DeCarlo TM, Schoepf V, Dissard D, Tanaka K, McCulloch M (2015) Cleaning and pre-treatment procedures for biogenic and synthetic calcium carbonate powders for determination of elemental and boron isotopic compositions. Chem Geol 398:11–21
Honisch B, Hemming N, Grottoli A, Amat A, Hanson G, Buma J (2004) Assessing scleractinian corals as recorders for paleo-pH: Empirical calibration and vital effects. Geochim Cosmochim Acta 68:3675–3685
Ishikawa T, Nagaishi K (2011) High-precision isotopic analysis of boron by positive thermal ionization mass spectrometry with sample preheating. J Anal At Spectrom 26:359–365
Kinsman D, Holland H (1969) Co-precipitation of cation with CaCO3 - IV. Co-precipitation of Sr2+ with aragonite between 16 and 96°C. Geochim Cosmochim Acta 33:1–17
Klochko K, Kaufman A, Yao W, Byrne R, Tossell J (2006) Experimental measurement of boron isotope fractionation in seawater. Earth Planet Sci Lett 248:276–285
Krief S, Hendy E, Fine M, Yam R, Meibom A, Foster G, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74:4988–5001
Kuffner I, Jokiel P, Rodgers K, Andersson A, Mackenzie F (2012) An apparent “vital effect” of calcification rate on the Sr/Ca temperature proxy in the reef coral Montipora capitata. Geochem Geophys Geosyst. doi:10.1029/2012GC004128
Langdon C, Atkinson MJ (2005) Effect of elevated pCO(2) on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res. doi:10.1029/2004JC002576
Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson M (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cy 14:639–654
Marshall JF, McCulloch M (2002) An assessment of the Sr/Ca ratio in shallow water hermatypic corals as a proxy for sea surface temperature. Geochim Cosmochim Acta 66:3263–3280
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
McConnaughey T, Burdett J, Whelan J, Paull C (1997) Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochim Cosmochim Acta 61:611–622
McCulloch M, Tudhope A, Esat T, Mortimer G, Chappell J, Pillans B, Chivas A, Omura A (1999) Coral record of equatorial sea-surface temperatures during the penultimate deglaciation at Huon Peninsula. Science 283:202–204
McCulloch M, Fallon S, Wyndham T, Hendy E, Lough J, Barnes D (2003) Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421:727–730
McCulloch M, Falter J, Trotter J, Montagna P (2012a) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change 2:623–633
McCulloch M, Trotter J, Montagna P, Falter J, Dunbar R, Freiwald A, Forsterra N, Lopez Correa M, Maier C, Ruggeberg A, Taviani M (2012b) Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation. Geochim Cosmochim Acta 87:21–34
McCulloch MT, Holcomb M, Rankenburg K, Trotter JA (2014) Rapid, high-precision measurements of boron isotopic compositions in marine carbonates. Rapid Commun Mass Sp 28:2704–2712
Meibom A, Cuif J, Hillion F, Constantz B, Juillet-Leclerc A, Dauphin Y, Watanabe T, Dunbar R (2004) Distribution of magnesium in coral skeleton. Geophys Res Lett. doi:10.1029/2004GL021313
Mitsuguchi T, Matsumoto E, Abe O, Uchida T, Isdale P (1996) Mg/Ca thermometry in coral-skeletons. Science 274:961–963
Moya A, Tambutte S, Tambutte E, Zoccola D, Caminiti N, Allemand D (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for ‘light-enhanced calcification’. J Exp Biol 209:3413–3419
Nagtegaal R, Grove C, Kasper S, Zinke J, Boer W, Brummer G (2012) Spectral luminescence and geochemistry of coral aragonite: Effects of whole-core treatment. Chem Geol 318:6–15
Pelejero C, Calvo E, McCulloch M, Marshall J, Gagan M, Lough J, Opdyke B (2005) Preindustrial to modern interdecadal variability in coral reef pH. Science 309:2204–2207
Reynaud S, Ferrier-Pages C, Boisson F, Allemand D, Fairbanks R (2004) Effect of light and temperature on calcification and strontium uptake in the scleractinian coral Acropora verweyi. Mar Ecol-Prog Ser 279:105–112
Reynaud S, Ferrier-Pages C, Meibom A, Mostefaoui S, Mortlock R, Fairbanks R, Allemand D (2007) Light and temperature effects on Sr/Ca and Mg/Ca ratios in the scleractinian coral Acropora sp. Geochim Cosmochim Acta 71:354–362
Ries J, Cohen A, McCorkle D (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674
Roche R, Abel R, Johnson K, Perry C (2011) Spatial variation in porosity and skeletal element characteristics in apical tips of the branching coral Acropora pulchra (Brook 1891). Coral Reefs 30:195–201
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
Shinjo R, Asami R, Huang K, You C, Iryu Y (2013) Ocean acidification trend in the tropical North Pacific since the mid-20th century reconstructed from a coral archive. Mar Geol 342:58–64
Shirai K, Kawashima T, Sowa K, Watanabe T, Nakaniori T, Takahata N, Arnakawa H, Sano Y (2008) Minor and trace element incorporation into branching coral Acropora nobilis skeleton. Geochim Cosmochim Acta 72:5386–5400
Sinclair D (2005) Non-river flood barium signals in the skeletons of corals from coastal Queensland, Australia. Earth Planet Sci Lett 237:354–369
Spivack AJ, Edmond JM (1986) Determination of boron isotope ratios by thermal ionization mass spectrometry of the dicesium metaborate cation. Anal Chem 58:31–35
Takahashi A, Kurihara H (2013) Ocean acidification does not affect the physiology of the tropical coral Acropora digitifera during a 5-week experiment. Coral Reefs 32:305–314
Trotter J, Montagna P, McCulloch M, Silenzi S, Reynaud S, Mortimer G, Martin S, Ferrier-Pagés C, Gattuso J, Rodolfo-Metalpa R (2011) Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: validation of the boron seawater pH proxy. Earth Planet Sci Lett 303:163–173
Venn A, Tambutte E, Holcomb M, Allemand D, Tambutte S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. Plos One 6
Venn A, Tambutte E, Holcomb M, Laurent J, Allemand D, Tambutte S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Natl Acad Sci USA 110:1634–1639
Wang B, You C, Huang K, Wu S, Aggarwal S, Chung C, Lin P (2010) Direct separation of boron from Na- and Ca-rich matrices by sublimation for stable isotope measurement by MC-ICP-MS. Talanta 82:1378–1384
Wei G, McCulloch M, Mortimer G, Deng W, Xie L (2009) Evidence for ocean acidification in the Great Barrier Reef of Australia. Geochim Cosmochim Acta 73:2332–2346
Zoccola D, Tambutte E, Kulhanek E, Puverel S, Scimeca J, Allemand D, Tambutte S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. BBA-Biomembranes 1663:117–126
Acknowledgments
We thank H. Osieriski for support of geochemical analyses. We also thank to J. Zinke, K. Shirai, M. Hori, and two anonymous reviewers for fruitful comments. We also thank International Research Hub Project for Climate Change, Coral Reef/Island Dynamics (the University of the Ryukyus), and Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation (G2301), and the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies. M. McCulloch and M. Holcomb were also supported by ARC Laureate Fellowship and Super Science funding, respectively.
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Tanaka, K., Holcomb, M., Takahashi, A. et al. Response of Acropora digitifera to ocean acidification: constraints from δ11B, Sr, Mg, and Ba compositions of aragonitic skeletons cultured under variable seawater pH. Coral Reefs 34, 1139–1149 (2015). https://doi.org/10.1007/s00338-015-1319-6
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DOI: https://doi.org/10.1007/s00338-015-1319-6