Mapping coral calcification strategies from in situ boron isotope and trace element measurements of the tropical coral Siderastrea siderea
1.
Cesar, H. J. S., Burke, L. & Pet-Soede, L. The Economics of Worldwide Coral Reef Degradation. 23 (Cesar Environmental Economics Consulting: The Netherlands). https://www.icran.org/pdf/cesardegradationreport.pdf (2003).
2.
Tambutté, E. et al. Observations of the tissue-skeleton interface in the scleractinian coral Stylophora pistillata. Coral Reefs 26, 517–529 (2007).
ADS Article Google Scholar
3.
Mollica, N. R. et al. Ocean acidification affects coral growth by reducing skeletal density. Proc. Natl. Acad. Sci. 115, 1754–1759 (2018).
ADS CAS Article Google Scholar
4.
Mass, T. et al. Cloning and characterization of four novel coral acid-rich proteins that precipitate carbonates in vitro. Curr. Biol. 23, 1126–1131. https://doi.org/10.1016/j.cub.2013.05.007 (2013).
CAS Article PubMed Google Scholar
5.
Guo, W. Seawater temperature and buffering capacity modulate coral calcifying pH. Sci. Rep. 9, 1–13 (2019).
Article Google Scholar
6.
McCulloch, M. et al. 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 (2012).
ADS CAS Article Google Scholar
7.
Guo, W. et al. Ocean acidification has impacted coral growth on the great barrier reef. Geophys. Res. Lett. https://doi.org/10.1029/2019gl086761 (2020).
Article PubMed PubMed Central Google Scholar
8.
Sevilgen, D. S. et al. Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci. Adv. https://doi.org/10.1126/sciadv.aau7447 (2019).
Article PubMed PubMed Central Google Scholar
9.
Venn, A., Tambutté, E., Holcomb, M., Allemand, D. & Tambutté, S. Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6, e20013 (2011).
ADS CAS Article Google Scholar
10.
Cai, W.-J. et al. Microelectrode characterization of coral daytime interior pH and carbonate chemistry. Nat. Commun. 7, 1–8 (2016).
Google Scholar
11.
Holcomb, M. et al. Coral calcifying fluid pH dictates response to ocean acidification. Sci. Rep. 4, 5207. https://doi.org/10.1038/srep05207 (2014).
CAS Article PubMed PubMed Central Google Scholar
12.
DeCarlo, T. M., Holcomb, M. & McCulloch, M. T. Reviews and syntheses: revisiting the boron systematics of aragonite and their application to coral calcification. Biogeosciences 15, 2819–2834. https://doi.org/10.5194/bg-15-2819-2018 (2018).
ADS CAS Article Google Scholar
13.
McCulloch, M. T., D’Olivo, J. P., Falter, J., Holcomb, M. & Trotter, J. A. Coral calcification in a changing world and the interactive dynamics of pH and DIC upregulation. Nat. Commun. 8, 15686. https://doi.org/10.1038/ncomms15686 (2017).
ADS CAS Article PubMed PubMed Central Google Scholar
14.
Horvath, K. M. et al. Next-century ocean acidification and warming both reduce calcification rate, but only acidification alters skeletal morphology of reef-building coral Siderastrea siderea. Sci. Rep. 6, 29613. https://doi.org/10.1038/srep29613 (2016).
ADS CAS Article PubMed PubMed Central Google Scholar
15.
Tambutté, E. et al. Morphological plasticity of the coral skeleton under CO2-driven seawater acidification. Nat. Commun. 6, 7368. https://doi.org/10.1038/ncomms8368 (2015).
ADS CAS Article PubMed PubMed Central Google Scholar
16.
Stewart, J. A., Anagnostou, E. & Foster, G. L. An improved boron isotope pH proxy calibration for the deep-sea coral Desmophyllum dianthus through sub-sampling of fibrous aragonite. Chem. Geol. 447, 148–160. https://doi.org/10.1016/j.chemgeo.2016.10.029 (2016).
ADS CAS Article Google Scholar
17.
Allison, N., Finch, A. A. & EIMF. δ11B, Sr, Mg and B in a modern Porites coral: the relationship between calcification site pH and skeletal chemistry. Geochim. Cosmochim. Acta 74, 1790–1800 (2010).
ADS CAS Article Google Scholar
18.
Rollion-Bard, C. & Blamart, D. SIMS method and examples of applications in coral biomineralization. In Biomineralization Sourcebook: Characterization of Biominerals and Biomimetic Materials (eds DiMasi, E. & Gower, L. B.) 249–261 (CRC Press, Boca Raton, 2014).
Google Scholar
19.
Trotter, J. et al. 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. https://doi.org/10.1016/j.epsl.2011.01.030 (2011).
ADS CAS Article Google Scholar
20.
Krief, S. et al. Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim. Cosmochim. Acta 74, 4988–5001 (2010).
ADS CAS Article Google Scholar
21.
Hönisch, B. et al. Assessing scleractinian corals as recorders for paleo-pH: empirical calibration and vital effects. Geochim. Cosmochim. Acta 68, 3675–3685. https://doi.org/10.1016/j.gca.2004.03.002 (2004).
ADS CAS Article Google Scholar
22.
Tanaka, K. 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).
ADS Article Google Scholar
23.
Reynaud, S., Hemming, N. G., Juillet-Leclerc, A. & Gattuso, J.-P. Effect of pCO2 and temperature on the boron isotopic composition of the zooxanthellate coral Acropora sp. Coral Reefs 23, 539–546 (2004).
Google Scholar
24.
Anagnostou, E., Huang, K.-F., You, C.-F., Sikes, E. & Sherrell, R. Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: evidence of physiological pH adjustment. Earth Planet. Sci. Lett. 349, 251–260 (2012).
ADS Article Google Scholar
25.
Jurikova, H. et al. Boron isotope composition of the cold-water coral Lophelia pertusa along the Norwegian margin: zooming into a potential pH-proxy by combining bulk and high-resolution approaches. Chem. Geol. 513, 143–152. https://doi.org/10.1016/j.chemgeo.2019.01.005 (2019).
ADS CAS Article Google Scholar
26.
Kasemann, S. A., Schmidt, D. N., Bijma, J. & Foster, G. L. In situ boron isotope analysis in marine carbonates and its application for foraminifera and palaeo-pH. Chem. Geol. https://doi.org/10.1016/j.chemgeo.2008.12.015 (2009).
Article Google Scholar
27.
Rollion-Bard, C., Chaussidon, M. & France-Lanord, C. pH control on oxygen isotopic composition of symbiotic corals. Earth Planet. Sci. Lett. 215, 275–288. https://doi.org/10.1016/S0012-821X(03)00391-1 (2003).
ADS CAS Article Google Scholar
28.
Standish, C. D. et al. The effect of matrix interferences on in situ boron isotope analysis by laser ablation multi-collector inductively coupled plasma mass spectrometry. Rapid Commun. Mass Spectrom. 33, 959–968 (2019).
ADS CAS Article Google Scholar
29.
Sadekov, A. et al. Accurate and precise microscale measurements of boron isotope ratios in calcium carbonates using laser ablation multicollector-ICPMS. J. Anal. At. Spectrom. 34, 550–560 (2019).
CAS Article Google Scholar
30.
Fietzke, J. et al. Boron isotope ratio determination in carbonates via LA-MC-ICP-MS using soda-lime glass standards as reference material. J. Anal. At. Spectrom. 25, 1953–1957 (2010).
CAS Article Google Scholar
31.
Oppelt, A., López, M. & Rocha, C. Biogeochemical analysis of the calcification patterns of cold-water corals Madrepora oculata and Lophelia pertusa along contact surfaces with calcified tubes of the symbiotic polychaete Eunice norvegica: evaluation of a ‘mucus’ calcification hypothesis. Deep Sea Res. I Oceanogr. Res. Pap. 127, 90–104. https://doi.org/10.1016/j.dsr.2017.08.006 (2017).
ADS CAS Article Google Scholar
32.
Fowell, S. et al. Historical trends in pH and carbonate biogeochemistry on the Belize Mesoamerican Barrier Reef System. Geophys. Res. Lett. 45, 3228–3237 (2018).
ADS CAS Article Google Scholar
33.
Runcorn, S. K. Corals as paleontological clocks. Sci. Am. 215, 26–33 (1966).
Article Google Scholar
34.
DeCarlo, T. M. & Cohen, A. L. Dissepiments, density bands and signatures of thermal stress in Porites skeletons. Coral Reefs 36, 749–761. https://doi.org/10.1007/s00338-017-1566-9 (2017).
ADS Article Google Scholar
35.
Barnes, D. & Lough, J. On the nature and causes of density banding in massive coral skeletons. J. Exp. Mar. Biol. Ecol. 167, 91–108 (1993).
Article Google Scholar
36.
DeCarlo, T. M. et al. Coral Sr-U thermometry. Paleoceanography 31, 626–638 (2016).
ADS Article Google Scholar
37.
Gagnon, A. C., Adkins, J. F., Fernandez, D. P. & Robinson, L. F. Sr/Ca and Mg/Ca vital effects correlated with skeletal architecture in a scleractinian deep-sea coral and the role of Rayleigh fractionation. Earth Planet. Sci. Lett. 261, 280–295. https://doi.org/10.1016/j.epsl.2007.07.013 (2007).
ADS CAS Article Google Scholar
38.
Blamart, D. et al. Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa: implications for biomineralization and paleo-pH. Geochem. Geophys. Geosyst. https://doi.org/10.1029/2007GC001686 (2007).
Article Google Scholar
39.
Jokiel, P. L. Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc. Biol. Sci. 280, 20130031–20130031. https://doi.org/10.1098/rspb.2013.0031 (2013).
CAS Article PubMed PubMed Central Google Scholar
40.
Galli, G. & Solidoro, C. ATP supply may contribute to light-enhanced calcification in corals more than abiotic mechanisms. Front. Mar. Sci. https://doi.org/10.3389/fmars.2018.00068 (2018).
Article Google Scholar
41.
Barott, K. L., Venn, A. A., Perez, S. O., Tambutté, S. & Tresguerres, M. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc. Natl. Acad. Sci. 112, 607–612. https://doi.org/10.1073/pnas.1413483112 (2015).
ADS CAS Article PubMed Google Scholar
42.
Bernardet, C., Tambutté, E., Techer, N., Tambutté, S. & Venn, A. Ion transporter gene expression is linked to the thermal sensitivity of calcification in the reef coral Stylophora pistillata. Sci. Rep. 9, 1–13 (2019).
Article Google Scholar
43.
Le Goff, C. et al. In vivo pH measurement at the site of calcification in an octocoral. Sci. Rep. 7, 11210. https://doi.org/10.1038/s41598-017-10348-4 (2017).
ADS CAS Article PubMed PubMed Central Google Scholar
44.
Zoccola, D. et al. Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification. Sci. Rep. 5, 9983. https://doi.org/10.1038/srep09983 (2015).
CAS Article PubMed PubMed Central Google Scholar
45.
Furla, P., Galgani, I., Durand, I. & Allemand, D. Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203, 3445–3457 (2000).
CAS PubMed Google Scholar
46.
DeLong, K. L., Maupin, C. R., Flannery, J. A., Quinn, T. M. & Shen, C.-C. Refining temperature reconstructions with the Atlantic coral Siderastrea siderea. Palaeogeogr. Palaeoclimatol. Palaeoecol. 462, 1–15. https://doi.org/10.1016/j.palaeo.2016.08.028 (2016).
Article Google Scholar
47.
Castillo, K. D., Ries, J. B. & Weiss, J. M. Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System Southern Belize. PLoS ONE 6, e14615 (2011).
ADS CAS Article Google Scholar
48.
Castillo, K. D., Ries, J. B., Weiss, J. M. & Lima, F. P. Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat. Clim. Change 2, 756–760. https://doi.org/10.1038/nclimate1577 (2012).
Article Google Scholar
49.
Foster, G. L. Seawater pH, pCO2 and CO32− variations in the Caribbean Sea over the last 130 kyr: a boron isotope and B/Ca study of planktic forminifera. Earth Planet. Sci. Lett. 271, 254–266. https://doi.org/10.1016/j.epsl.2008.04.015 (2008).
ADS CAS Article Google Scholar
50.
Foster, G. L. et al. Interlaboratory comparison of boron isotope analyses of boric acid, seawater and marine CaCO3 by MC-ICPMS and NTIMS. Chem. Geol. 358, 1–14. https://doi.org/10.1016/j.chemgeo.2013.08.027 (2013).
ADS CAS Article Google Scholar
51.
le Roux P. J. et al. In situ, multiplemultiplier, laser ablation ICP‐MS measurement of boron isotopic composition (δ11B) at the nanogram level. Chem. Geol. 203(1–2), 123–138. https://doi.org/10.1016/j.chemgeo.2003.09.006 (2004).
ADS CAS Article Google Scholar
52.
Inoue, M., Nohara, M., Okai, T., Suzuki, A. & Kawahata, H. Concentrations of trace elements in carbonate reference materials coral JCp-1 and Giant Clam JCt-1 by inductively coupled plasma-mass spectrometry. Geostand. Geoanal. Res. 28, 411–416. https://doi.org/10.1111/j.1751-908X.2004.tb00759.x (2004).
CAS Article Google Scholar
53.
Thil, F. et al. Development of laser ablation multi-collector inductively coupled plasma mass spectrometry for boron isotopic measurement in marine biocarbonates: new improvements and application to a modern Porites coral. Rapid Commun. Mass Spectrom. 30, 359–371 (2016).
CAS Article Google Scholar
54.
Hathorne, E. C. et al. Interlaboratory study for coral Sr/Ca and other element/Ca ratio measurements. Geochem. Geophys. Geosyst. 14, 3730–3750. https://doi.org/10.1002/ggge.20230 (2013).
ADS CAS Article Google Scholar
55.
Hijmans, R. & Van Etten, J. Geographic analysis and modeling with raster data. R Package Version 2, 1–25 (2012).
Google Scholar
56.
R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2010).
57.
Foster, G. L., von Strandmann, P. & Rae, J. W. B. Boron and magnesium isotopic composition of seawater. Geochem. Geophys. Geosyst. https://doi.org/10.1029/2010gc003201 (2010).
Article Google Scholar
58.
Klochko, K., Kaufman, A. J., Yao, W. S., Byrne, R. H. & Tossell, J. A. Experimental measurement of boron isotope fractionation in seawater. Earth Planet. Sci. Lett. https://doi.org/10.1016/j.epsl.2006.05.034 (2006).
Article Google Scholar
59.
Holcomb, M., DeCarlo, T., Gaetani, G. & McCulloch, M. Factors affecting B/Ca ratios in synthetic aragonite. Chem. Geol. 437, 67–76 (2016).
ADS CAS Article Google Scholar
60.
Dickson, A. G. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep Sea Res. Oceanogr. Res. Pap. 37, 755–766. https://doi.org/10.1016/0198-0149(90)90004-F (1990).
ADS CAS Article Google Scholar
61.
Lee, K. et al. The universal ratio of boron to chlorinity for the North Pacific and North Atlantic oceans. Geochim. Cosmochim. Acta 74, 1801–1811 (2010).
ADS CAS Article Google Scholar
62.
Zeebe, R. E. & Wolf-Gladrow, D. A. CO2in Seawater: Equilibrium, Kinetics, Isotopes in Seawater: Equilibrium, Kinetics, Isotopes Vol. 65 (Elsevier, Amsterdam, 2001).
Google Scholar
63.
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675. https://doi.org/10.1038/nmeth.2089 (2012).
CAS Article PubMed PubMed Central Google Scholar More