Coral Reefs

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Coral calcification, mucus, and the origin of skeletal organic molecules

  • Sönke HohnEmail author
  • Claire E. Reymond


Biocalcification encompasses the kinetic and structural, abiotic and biologically mediated processes involved in the formation of calcium carbonate skeletons by marine organisms and represents a key process in the global carbon cycle. Throughout the geological record, this process has evolved repetitively and has altered global biogeochemical cycles. Besides the structural variability of calcium carbonate polymorphs laid down by different organisms, biogenic carbonate skeletons are characterized by the presence of organic molecules that are incorporated into the growing skeleton. Major advances have identified the macromolecules associated to the organic matrix within marine calcifiers, however, it has yet to be established the actual role these organic molecules play in the calcification process. In this study, we isolated the effect of skeletal organic molecules (SOM) on the precipitation of calcium carbonate on coral skeleton fragments by adding extracted SOM or coral mucus (CM) to oversaturated calcium carbonate solutions. We found that the precipitation rate did not change regardless if organic molecules were present or not. However, the primary polymorph did change between the treatments, suggesting that organic molecules influence the surface processes that lead to the formation of the crystal lattice but not the kinetic processes that transport ions to the crystal surface. Since SOM and CM both altered the crystal polymorph but not the crystallization rate, we argue that SOM may not represent a specialized biomineralization toolkit, but that SOM originate from CM and the requirement of the polyp to adhere to the substratum.


Coral Calcification Skeletal organic matrix Biomineralization 


Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

338_2019_1826_MOESM1_ESM.docx (67 kb)
Supplementary material 1 (DOCX 66 kb)


  1. Abe N (1938) Feeding behavior and the nematocyst of Fungia and 15 other species of corals. Palao Trop Biol Stn Stud 1:Google Scholar
  2. Abrams JF, Hohn S, Rixen T, Merico A (2018) Sundaland peat carbon dynamics and its contribution to the global Holocene climate. Global Biogeochem Cycles 1:1–23Google Scholar
  3. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003a) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426CrossRefGoogle Scholar
  4. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003b) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: Active internal carbon cycle. J Exp Mar Bio Ecol 288:1–15CrossRefGoogle Scholar
  5. Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté É, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: From molecular mechanisms to environmental control. Comptes Rendus - Palevol 3:453–467CrossRefGoogle Scholar
  6. Allemand D, Tambutte E, Girard J, Jaubert J, Tambutté E, Girard J, Jaubert J (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. J Exp Biol 201:2001–2009PubMedGoogle Scholar
  7. Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Bio Ecol 232:85–106CrossRefGoogle Scholar
  8. Arendt D, Benito-Gutierrez E, Brunet T, Marlow H (2015) Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution. Philos Trans R Soc B Biol Sci 370:20150286–20150286Google Scholar
  9. Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309CrossRefGoogle Scholar
  10. Cai W-J, Ma Y, Hopkinson BM, Grottoli AG, Warner ME, Ding Q, Hu X, Yuan X, Schoepf V, Xu H, Han C, Melman TF, Hoadley KD, Pettay DT, Matsui Y, Baumann JH, Levas S, Ying Y, Wang Y (2016) Microelectrode characterization of coral daytime interior pH and carbonate chemistry. Nat Commun 7:11144CrossRefPubMedPubMedCentralGoogle Scholar
  11. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  12. Carafoli E (1987) Intracellular Calcium Homeostasis. Ann Rev. Biochem 56:395–433CrossRefGoogle Scholar
  13. Carafoli E (2002) Calcium signaling: A tale for all seasons. Proc Natl Acad Sci 99:1115–1122CrossRefPubMedGoogle Scholar
  14. Carpenter FW (1910) Feeding Reactions of the Rose Coral (Isophyllia). Proc Am Acad Arts Sci 46:149–162CrossRefGoogle Scholar
  15. Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A (2007) Evolution of calcium homeostasis : From birth of the first cell to an omnipresent signalling system. 42:345–350CrossRefGoogle Scholar
  16. Chan K (1976) Control of colony formation in Coelastrum microporum (Chlorococcales, Chlorophyta). Phycologia 15:149–154CrossRefGoogle Scholar
  17. Cohen AL (2003) Geochemical Perspectives on Coral Mineralization. Rev Mineral Geochemistry 54:151–187CrossRefGoogle Scholar
  18. Crossland CJ (1987) In situ Release Of Mucus And Doc-Lipid From The Corals Acropora Variabilis And Stylophora-Pistillata In Different Light Regimes. Coral Reefs 6:35–42CrossRefGoogle Scholar
  19. Cuif J-P, Dauphin Y, Nehrke G, Nouet J, Perez-Huerta A (2012) Layered Growth and Crystallization in Calcareous Biominerals: Impact of Structural and Chemical Evidence on Two Major Concepts in Invertebrate Biomineralization Studies. Minerals 2:11–39CrossRefGoogle Scholar
  20. Cuif JP, Dauphin Y (2005) The two-step mode of growth in the scleractinian coral skeletons from the micrometre to the overall scale. J Struct Biol 150:319–331CrossRefPubMedGoogle Scholar
  21. Dahan D, Vago R, Golan Y (2003) Skeletal architecture and microstructure of the calcifying coral Fungia simplex. Mater Sci Eng C 23:473–477CrossRefGoogle Scholar
  22. DeCarlo TM, Comeau S, Cornwall CE, McCulloch MT (2018) Coral resistance to ocean acidification linked to increased calcium at the site of calcification. Proc R Soc B Biol Sci 285:20180564CrossRefGoogle Scholar
  23. Deman JJ, Bruyneel EA, Mareel MM (1974) A study on the mechanism of intercellular adhesion: Effects of neuraminidase, calcium, and trypsin on the aggregation of suspended hela cells. J Cell Biol 60:641–652CrossRefPubMedPubMedCentralGoogle Scholar
  24. Drake JL, Mass T, Haramaty L, Zelzion E, Bhattacharya D, Falkowski PG (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci 110:3788–3793CrossRefPubMedGoogle Scholar
  25. Edmunds PJ, Cumbo VR, Fan TY (2013) Metabolic costs of larval settlement and metamorphosis in the coral Seriatopora caliendrum under ambient and elevated pCO2. J Exp Mar Bio Ecol 443:33–38CrossRefGoogle Scholar
  26. Erez J (2003) The Source of Ions for Biomineralization in Foraminifera and Their Implications for Paleoceanographic Proxies. Rev Mineral Geochemistry 54:115–149CrossRefGoogle Scholar
  27. Fabricius KE, Genin A, Benayahu Y (1995) Flow-dependent herbivory and growth in zooxanthellae-free soft corals. Limnol Oceanogr 40:1290–1301CrossRefGoogle Scholar
  28. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169CrossRefGoogle Scholar
  29. Falini G, Fermani S, Goffredo S (2015) Coral biomineralization: A focus on intra-skeletal organic matrix and calcification. Semin Cell Dev Biol 46:17–26CrossRefPubMedGoogle Scholar
  30. Fine M, Tchernov D (2007) Scleractinian Coral Species Survive and Recover from Decalcification. Science (80- ) 315:1811CrossRefGoogle Scholar
  31. Freeman LA, Kleypas JA, Miller AJ (2013) Coral reef habitat response to climate change scenarios. PLoS One 8:1–14Google Scholar
  32. Galli G, Solidoro C (2018) ATP supply may contribute to light-enhanced calcification in corals more than abiotic mechanisms. Front Mar Sci 5:Google Scholar
  33. Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky Winters E, McLaughlin SM, Meteyer CU, Morado JF, Nicholson H, Parnell PG, Peters EC, Reynolds TL, Rotstein D, Sileo L, Woodley C (2007) Coral Disease and Health Workshop: Coral Histopathology II. NOAA Tech Memo NOS NCCOS 56 NOAA Tech Memo CRCP 4 84Google Scholar
  34. Gateño D, Israel A, Barki Y, Rinkevich B (1998) Gastrovascular circulation in an octocoral: Evidence of significant transport of coral and symbiont cells. Biol Bull 194:178–186CrossRefPubMedGoogle Scholar
  35. Gebauer D, Volkel A, Colfen H (2008) Stable Prenucleation Calcium Carbonate Clusters. Science (80- ) 322:1819–1822CrossRefGoogle Scholar
  36. Georgiou L, Falter J, Trotter J, Kline DI, Holcomb M, Dove SG, Hoegh-Guldberg O, McCulloch M (2015) pH homeostasis during coral calcification in a free ocean CO 2 enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef. Proc Natl Acad Sci 112:13219–13224CrossRefPubMedGoogle Scholar
  37. Gilis M, Meibom A, Domart-Coulon I, Grauby O, Stolarski J, Baronnet A (2014) Biomineralization in newly settled recruits of the scleractinian coral Pocillopora damicornis. J Morphol 275:1349–1365CrossRefPubMedGoogle Scholar
  38. Gleason DF, Hofmann DK (2011) Coral larvae: From gametes to recruits. J Exp Mar Bio Ecol 408:42–57CrossRefGoogle Scholar
  39. Goffredo S, Caroselli E, Mezzo F, Laiolo L, Vergni P, Pasquini L, Levy O, Zaccanti F, Tribollet A, Dubinsky Z, Falini G (2012) The puzzling presence of calcite in skeletons of modern solitary corals from the Mediterranean Sea. Geochim Cosmochim Acta 85:187–199CrossRefGoogle Scholar
  40. Goffredo S, Dubinsky Z (2016) The Cnidaria. The world of Medusa and her sisters. Springer International Publishing, Past, Present and FutureGoogle Scholar
  41. Goldberg WM (2002) Feeding behavior, epidermal structure and mucus cytochemistry of the scleractinian Mycetophyllia reesi, a coral without tentacles. Tissue Cell 34:232–245CrossRefPubMedGoogle Scholar
  42. Harii S, Kayanne H (1996) Larval Settlement of Corals in Flowing Water using a Racetrack Flume. MTS J 36:76–79CrossRefGoogle Scholar
  43. Harii S, Kayanne H (2003) Larval dispersal, recruitment, and adult distribution of the brooding stony octocoral Heliopora coerulea on Ishigaki Island, southwest Japan. Coral Reefs 22:188–196CrossRefGoogle Scholar
  44. Helman Y, Natale F, Sherrell RM, LaVigne M, Starovoytov V, Gorbunov MY, Falkowski PG (2008) Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro. Proc Natl Acad Sci 105:54–58CrossRefPubMedGoogle Scholar
  45. 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 (80- ) 318:1737–1742CrossRefGoogle Scholar
  46. Hohn S, Merico A (2012) Modelling coral polyp calcification in relation to ocean acidification. Biogeosciences 9:4441–4454CrossRefGoogle Scholar
  47. Hohn S, Merico A (2015) Quantifying the relative importance of transcellular and paracellular ion transports to coral polyp calcification. Front Earth Sci 2:37CrossRefGoogle Scholar
  48. Hottinger LC (2000) Functional Morphology of Benthic Foraminiferal Shells, Envelopes of Cells beyond Measure. Micropaleontology 46:57–86Google Scholar
  49. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17CrossRefPubMedGoogle Scholar
  50. Ipcc (2000) Summary for Policymakers: Emissions Scenarios. A Special Report of Working Group III of the Intergovernmental Panel on Climate Change. Group 20Google Scholar
  51. Jones NS, Ridgwell A, Hendy EJ (2015a) Evaluation of coral reef carbonate production models at a global scale. Biogeosciences 12:1339–1356CrossRefGoogle Scholar
  52. Jones R, Ricardo GF, Negri AP (2015b) Effects of sediments on the reproductive cycle of corals. Mar Pollut Bull 100:13–33CrossRefPubMedGoogle Scholar
  53. Kauffman SA (1992) The Origins of Order: Self-Organization and Selection in Evolution. Spin Glasses and Biology. pp 61–100Google Scholar
  54. Kaźmierczak J, Ittekkot V, Degens ET (1985) Biocalcification through time: environmental challenge and cellular response. Paläontologische Zeitschrift 59:15–33CrossRefGoogle Scholar
  55. Kaźmierczak J, Kempe S, Kremer B (2013) Calcium in the Early Evolution of Living Systems: A Biohistorical Approach. 1738–1750Google Scholar
  56. Kaźmierczak J, Kempe (2004) Calcium Build-up in the Precambrian Sea. Origins: Genesis, Evolution and Diversity of Life. Springer, pp 329–345Google Scholar
  57. Kleypas JA, Buddemeier RW, Gattuso JP (2001) The future of Coral reefs in an age of global change. Int J Earth Sci 90:426–437CrossRefGoogle Scholar
  58. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL, Allemand D, Balch WM, Berelson WM, Gattuso JP, Muller PH, Lough JM, Mackenzie FT, Muller-Karger F, Ridgwell AJ, Spero HJ, Swart PK (2006) Impacts of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Guide for Future Research. A Rep a Work held 18–20 April 2005, St Petersburg, FL, Spons by NSF, NOAA, US Geol Surv 88 pagesGoogle Scholar
  59. Knoll AH (2003) Biomineralization and Evolutionary History. Rev Mineral Geochemistry 54:329–356CrossRefGoogle Scholar
  60. Kralj D, Brecevic L, Nielsen AE (1990) VATERITE GROWTH AND DISSOLUTION IN AQUEOUS SOLUTION I. KINETICS OF CRYSTAL GROWTH. J Cryst Growth 104:793–800CrossRefGoogle Scholar
  61. Kralj D, Breevi L, Kontrec J (1997) Vaterite growth and dissolution in aqueous solution III. Kinetics of transformation. 177:248–257Google Scholar
  62. Kretsinger RH (1976) Calcium-Binding Proteins. Annu Rev Biochem 45:239–266CrossRefPubMedGoogle Scholar
  63. Kump LR, Brantley SL, Arthur MA (2000) Chemical Weathering, Atmospheric CO2, and Climate. Annu Rev Earth Planet Sci 28:611–667CrossRefGoogle Scholar
  64. Lasaga AC (2014) Kinetic theory in the earth sciences. Princeton university press,Google Scholar
  65. Lippmann F (1973) Sedimentary Carbonate Minerals. Springer,Google Scholar
  66. Lønborg C, Calleja ML, Fabricius KE, Smith JN, Achterberg EP (2019) The Great Barrier Reef: A source of CO2 to the atmosphere. Mar Chem 210:24–33CrossRefGoogle Scholar
  67. Mann S (2001) Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford University Press, OxfordGoogle Scholar
  68. Marin F, Smith M, Isa Y, Muyzer G, Westbroek P (1996) Skeletal matrices, muci, and the origin of invertebrate calcification. Proc Natl Acad Sci USA 93:1554–1559CrossRefPubMedGoogle Scholar
  69. Marshall AT (1996) Calcification in Hermatypic and Ahermatypic Corals. Science (80- ) 271:637–639CrossRefGoogle Scholar
  70. Marshall AT, Wright OP (1993) Confocal laser scanning light microscopy of the extra-thecal epithelia of undecalcified scleractinian corals. Cell Tissue Res 272:533–543CrossRefGoogle Scholar
  71. Mass T, Drake JL, Haramaty L, Kim JD, Zelzion E, Bhattacharya D, Falkowski PG (2013) Cloning and characterization of four novel coral acid-rich proteins that precipitate carbonates in vitro. Curr Biol 23:1126–1131CrossRefPubMedGoogle Scholar
  72. Mass T, Genin A, Shavit U, Grinstein M, Tchernov D (2010) Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. Proc Natl Acad Sci 107:2527–2531CrossRefPubMedGoogle Scholar
  73. Mayer G, Sarikaya M (2002) Rigid biological composite materials: Structural examples for biomimetic design. Exp Mech 42:395–403CrossRefGoogle Scholar
  74. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627CrossRefGoogle Scholar
  75. Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from six species of coral. Mar Biol 99:187–193CrossRefGoogle Scholar
  76. Menviel L, Joos F (2012) Toward explaining the Holocene carbon dioxide and carbon isotope records: Results from transient ocean carbon cycle-climate simulations. Paleoceanography 27:1–17CrossRefGoogle Scholar
  77. Meyers MA, Chen PY, Lin AYM, Seki Y (2008) Biological materials: Structure and mechanical properties. Prog Mater Sci 53:1–206CrossRefGoogle Scholar
  78. Morse JW, Wang Q, Tsio MY (1997) Influences of temperature and Mg : Ca ratio on CaCO 3 precipitates from seawater. Geology 25:85–87CrossRefGoogle Scholar
  79. Müller MN, Barcelos E, Ramos J, Schulz KG, Riebesell U, Kaźmierczak J, Gallo F, Mackinder L, Li Y, Nesterenko PN, Trull TW, Hallegraeff GM (2015) Phytoplankton calcification as an effective mechanism to alleviate cellular calcium poisoning. Biogeosciences 12:6493–6501CrossRefGoogle Scholar
  80. Nakamura T, Nadaoka K, Watanabe A (2013) A coral polyp model of photosynthesis, respiration and calcification incorporating a transcellular ion transport mechanism. Coral Reefs 32:779–794CrossRefGoogle Scholar
  81. Nehrke G, Reichart GJ, Van Cappellen P, Meile C, Bijma J (2007) Dependence of calcite growth rate and Sr partitioning on solution stoichiometry: Non-Kossel crystal growth. Geochim Cosmochim Acta 71:2240–2249CrossRefGoogle Scholar
  82. Nielsen C (2008) Six major steps in animal evolution: Are we derived sponge larvae? Evol Dev 10:241–257CrossRefPubMedGoogle Scholar
  83. Nystrom M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417CrossRefPubMedGoogle Scholar
  84. Ogino T, Suzuki T, Sawada K (1987) The formation and transformation mechanism of calcium carbonate in water. Geochemica Cosmochem Acta 51:2757–2767CrossRefGoogle Scholar
  85. Okumura K, De Gennes PG (2001) Why is nacre strong? Elastic theory and fracture mechanics for biocomposites with stratified structures. Eur Phys J E 4:121–127CrossRefGoogle Scholar
  86. Oliver WA Jr (1996) Origins and relationships of Paleozoic coral groups and the origin of the Scleractinia. Paleontol Soc Pap 1:107–134CrossRefGoogle Scholar
  87. Ostwald W (1897) Studien uber die Bildung und Umwandlung fester Korper. Zeitschrift für Phys Chemie 289–331Google Scholar
  88. Plummer LN, Busenberg E (1982) The solubilities of calcite, aragonite and vaterite in CO2-H2O solutions between 0 and 90°C, and an evaluation of the aqueous model for the system CaCO3-CO2-H2O. Geochim Cosmochim Acta 46:1011–1040CrossRefGoogle Scholar
  89. Puverel S, Tambutté E, Pereira-Mouries L, Zoccola D, Allemand D, Tambutté S (2005) Soluble organic matrix of two Scleractinian corals: Partial and comparative analysis. Comp Biochem Physiol - B Biochem Mol Biol 141:480–487CrossRefPubMedGoogle Scholar
  90. Pytkowicz R (1973) Calcium carbonate retention in supersaturated seawater. Am J Sci 273:515CrossRefGoogle Scholar
  91. Ramos-Silva P, Kaandorp J, Herbst F, Plasseraud L, Alcaraz G, Stern C, Corneillat M, Guichard N, Durlet C, Luquet G, Marin F (2014) The skeleton of the staghorn coral Acropora millepora: Molecular and structural characterization. PLoS One 9:Google Scholar
  92. Raybaud V, Tambutté S, Ferrier-Pagès C, Reynaud S, Venn AA, Tambutté É, Nival P, Allemand D (2017) Computing the carbonate chemistry of the coral calcifying medium and its response to ocean acidification. J Theor Biol 424:26–36CrossRefPubMedGoogle Scholar
  93. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie J-M, Frickenhaus S, Gonzalez K, Herman EK, Lin Y-C, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G, Allen AE, Bidle K, Borodovsky M, Bowler C, Brownlee C, Mark Cock J, Elias M, Gladyshev VN, Groth M, Guda C, Hadaegh A, Debora Iglesias-Rodriguez M, Jenkins J, Jones BM, Lawson T, Leese F, Lindquist E, Lobanov A, Lomsadze A, Malik S-B, Marsh ME, Mackinder L, Mock T, Mueller-Roeber B, Pagarete A, Parker M, Probert I, Quesneville H, Raines C, Rensing SA, Riaño-Pachón DM, Richier S, Rokitta S, Shiraiwa Y, Soanes DM, van der Giezen M, Wahlund TM, Williams B, Wilson W, Wolfe G, Wurch LL, Dacks JB, Delwiche CF, Dyhrman ST, Glöckner G, John U, Richards T, Worden AZ, Zhang X, Grigoriev IV (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213CrossRefPubMedGoogle Scholar
  94. Reymond CE, Lloyd A, Kline DI, Dove SG, Pandolfi JM (2013) Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios. Glob Chang Biol 19:291–302CrossRefPubMedGoogle Scholar
  95. Ridgwell AJ, Watson AJ, Maslin MA, Kaplan JO (2003) Implications of coral reef buildup for the controls on atmospheric CO2 since the Last Glacial Maximum. Paleoceanography 18:Google Scholar
  96. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064CrossRefGoogle Scholar
  97. Romano SL, Palumbi SR (1996) Evolution of Scleractinian Corals Inferred from Molecular Systematics. Science (80- ) 271:640–642CrossRefGoogle Scholar
  98. Sabine CL (2004) The Oceanic Sink for Anthropogenic CO2. Science (80- ) 305:367–371CrossRefGoogle Scholar
  99. Sancho-Tomás M, Fermani S, Gómez-Morales J, Falini G, García-Ruiz JM (2014) Calcium carbonate bio-precipitation in counter-diffusion systems using the soluble organic matrix from nacre and sea-urchin spine. Eur J Mineral 26:523–535CrossRefGoogle Scholar
  100. Sarmiento JL, Sundquist ET (1992) Revised budget for the oceanic uptake of anthropogenic carbon dioxide. Nature 356:589–593CrossRefGoogle Scholar
  101. Sebens KP (1984) Water Flow and Coral Colony Size: Interhabitat Comparisons of the Octocoral Alcyonium siderium. Proc Natl Acad Sci United States Am Biol Sci Ecol 81:5473–5477CrossRefGoogle Scholar
  102. Sebens KP, Grace SP, Helmuth B, Maney EJ, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites in a field enclosure. Mar Biol 131:347–360CrossRefGoogle Scholar
  103. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317CrossRefGoogle Scholar
  104. Sevilgen DS, Venn AA, Hu MY, Tambutté E, Beer D De (2019) Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci Adv 5:Google Scholar
  105. Shumway W (1932) The Recapitulation Theory. Q Rev Biol 7:93–99CrossRefGoogle Scholar
  106. Simkiss K (1977) Biomineralization and detoxification. Calcif Tissue Res 24:199–200CrossRefPubMedGoogle Scholar
  107. Stanley GD (2003) The evolution of modern corals and their early history. Earth-Science Rev 60:195–225CrossRefGoogle Scholar
  108. Stolarski J, Kitahara M V., Miller DJ, Cairns SD, Mazur M, Meibom A (2011) The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol Biol 11:Google Scholar
  109. Tambutté S, Holcomb M, Ferrier-Pagés C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: From the gene to the environment. J Exp Mar Bio Ecol 408:58–78CrossRefGoogle Scholar
  110. Vandermeulen JH, Watabe N (1973) Studies on reef corals. I. Skeleton formation by newly settled planula larva of Pocillopora damicornis. Mar Biol 23:47–57CrossRefGoogle Scholar
  111. Venn AA, Tambutté E, Holcomb M, Laurent J, Allemand D, Tambutté S (2013) Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. Proc Natl Acad Sci 110:1634–1639CrossRefPubMedGoogle Scholar
  112. Wall M, Nehrke G (2012) Reconstructing skeletal fiber arrangement and growth mode in the coral Porites lutea (Cnidaria, Scleractinia): A confocal Raman microscopy study. Biogeosciences 9:4885–4895CrossRefGoogle Scholar
  113. Watanabe T, Fukuda I, China K, Isa Y (2003) Molecular analyses of protein components of the organic matrix in the exoskeleton of two scleractinian coral species. Comp Biochem Physiol - B Biochem Mol Biol 136:767–774CrossRefPubMedGoogle Scholar
  114. Westbroek P, Marin F (1998) A marriage of bone and nacre. Nature 392:861–862CrossRefPubMedGoogle Scholar
  115. Wijgerde T, Diantari R, Lewaru MW, Verreth JAJ, Osinga R (2011) Extracoelenteric zooplankton feeding is a key mechanism of nutrient acquisition for the scleractinian coral Galaxea fascicularis. J Exp Biol 214:3351–3357CrossRefPubMedGoogle Scholar
  116. Williams RJP (1984) An Introduction to Biominerals and the Role of Organic Molecules in Their Formation. Philos Trans R Soc Lond B Biol Sci 304:411–424CrossRefGoogle Scholar
  117. Young SD (1973) Collagen and other mesoglea protein from the coral lbophyllia crymbosa (anthozoa, scleractinia). Int J Biochem 4:339–344CrossRefGoogle Scholar
  118. Zeebe RE, Wolf-Gladrow DA (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Gulf Professional Publishing,Google Scholar

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Authors and Affiliations

  1. 1.Leibniz Centre for Tropical Marine ResearchBremenGermany

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