Coral Calcification and Ocean Acidification

  • Paul L. JokielEmail author
  • Christopher P. Jury
  • Ilsa B. Kuffner
Part of the Coral Reefs of the World book series (CORW, volume 6)


Over 60 years ago, the discovery that light increased calcification in the coral plant-animal symbiosis triggered interest in explaining the phenomenon and understanding the mechanisms involved. Major findings along the way include the observation that carbon fixed by photosynthesis in the zooxanthellae is translocated to animal cells throughout the colony and that corals can therefore live as autotrophs in many situations. Recent research has focused on explaining the observed reduction in calcification rate with increasing ocean acidification (OA). Experiments have shown a direct correlation between declining ocean pH, declining aragonite saturation state (Ωarag), declining [CO3 2−] and coral calcification. Nearly all previous reports on OA identify Ωarag or its surrogate [CO3 2−] as the factor driving coral calcification. However, the alternate “Proton Flux Hypothesis” stated that coral calcification is controlled by diffusion limitation of net H+ transport through the boundary layer in relation to availability of dissolved inorganic carbon (DIC). The “Two Compartment Proton Flux Model” expanded this explanation and synthesized diverse observations into a universal model that explains many paradoxes of coral metabolism, morphology and plasticity of growth form in addition to observed coral skeletal growth response to OA. It is now clear that irradiance is the main driver of net photosynthesis (Pnet), which in turn drives net calcification (Gnet), and alters pH in the bulk water surrounding the coral. Pnet controls [CO3 2−] and thus Ωarag of the bulk water over the diel cycle. Changes in Ωarag and pH lag behind Gnet throughout the daily cycle by two or more hours. The flux rate Pnet, rather than concentration-based parameters (e.g., Ωarag, [CO3 2−], pH and [DIC]:[H+] ratio) is the primary driver of Gnet. Daytime coral metabolism rapidly removes DIC from the bulk seawater. Photosynthesis increases the bulk seawater pH while providing the energy that drives calcification and increases in Gnet. These relationships result in a correlation between Gnet and Ωarag, with both parameters being variables dependent on Pnet. Consequently the correlation between Gnet and Ωarag varies widely between different locations and times depending on the relative metabolic contributions of various calcifying and photosynthesizing organisms and local rates of carbonate dissolution. High rates of H+ efflux continue for several hours following the mid-day Gnet peak suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Model. DIC flux (uptake) tracks Pnet and Gnet and drops off rapidly after the photosynthesis-calcification maxima, indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H+. Predictive models of future global changes in coral and coral reef growth based on oceanic Ωarag must include the influence of future changes in localized Pnet on Gnet as well as changes in rates of reef carbonate dissolution. The correlation between Ωarag and Gnet over the diel cycle is simply the result of increasing pH due to photosynthesis that shifts the CO2-carbonate system equilibria to increase [CO3 2−] relative to the other DIC components of [HCO3 ] and [CO2]. Therefore Ωarag closely tracks pH as an effect of Pnet, which also drives changes in Gnet. Measurements of DIC flux and H+ flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.


Calcification Corals Ocean acidification Seawater CO2-carbonate system Aragonite saturation state Boundary layers Phase lag 



This work was supported in part by NOAA Grant “Research in Support of the NWHI Coral Reef Ecosystem Reserve”, the EPA Star Grant Program, the Pacific Island Climate Change Cooperative (PICCC), the USGS Cooperative Agreement G13AC00130, and the George Melendez Wright Climate Change Fellowship Program. IBK’s involvement was supported by the USGS Coastal and Marine Geology Program. Any use of trade names herein was for descriptive purposes only and does not imply endorsement by the U.S. Government.


  1. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003a) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15 [doi: 10.1016/S0022-0981(02)00578-6]CrossRefGoogle Scholar
  2. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003b) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426 [doi: 10.1007/s00227-002-0981-8]Google Scholar
  3. Al-Horani FA, Al-Rousan SA, Manasrah RS, Rasheed MY (2005a) Coral calcification : Use of radioactive isotopes and metabolic inhibitors to study the interactions with photosynthesis and respiration. Chem and Ecol 21(5): 325–335 [doi:  10.1080/02757540500258724]CrossRefGoogle Scholar
  4. Al-Horani FA, Ferdelman T, Al-Moghrabi SM, De Beer D (2005b) Spatial distribution of calcification and photosynthesis in the scleractinian coral Galaxea fascicularis. Coral Reefs 24:173–180 [doi: 10.1007/s00338-004-0461-3]CrossRefGoogle Scholar
  5. Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté E, Tambutté S, Zaccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467. [doi: 10.1016/j.crpv.2004.07.011 ] CrossRefGoogle Scholar
  6. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941 [doi:  10.1139/b98-086]Google Scholar
  7. Allemand D, Tambutté E, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds), Coral reefs: an ecosystem in transition. New York; Springer Press pp 119–150CrossRefGoogle Scholar
  8. Allison N, Cohen I, Finch AA, Erez J, Tudhope AW (2014) Corals concentrate dissolved inorganic carbon to facilitate calcification. Nature Communications 5:5741[doi:  10.1038/ncomms6741]CrossRefGoogle Scholar
  9. Allison N, Tudhope AW, Fallick AE (1996) Factors influencing the stable carbon and oxygen isotopic composition of Porites lutea coral skeletons from Phuket, South Thailand. Coral Reefs 15:43–57 [ 10.1007/BF01626076]Google Scholar
  10. Andersson AJ, Kuffner IB, Mackenzie FT, Jokiel PL, Rodgers KS, Tan A (2009) Net loss of CaCO3 from coral reef communities due to human induced seawater acidification. Biogeosci 6, 1811–1823 [doi:  10.5194/bg-6-1811-2009]CrossRefGoogle Scholar
  11. Andersson AJ, Mackenzie FT, Ver LM (2003) Solution of shallow-water carbonates: An insignificant buffer against rising atmospheric CO2. Geology 31:513–516 [doi:  10.1130/0091-7613(2003)031<0513:SOSCAI>2.0.CO;2]CrossRefGoogle Scholar
  12. Anlauf H, D’Croz L, O’Dea A (2011) A corrosive concoction: The combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J Exp Mar Biol Ecol 397:13–20 [doi: 10.1016/j.jembe.2010.11.009]CrossRefGoogle Scholar
  13. Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci 105:17442–17446 [doi:  10.1073/pnas.0804478105]CrossRefGoogle Scholar
  14. Atkinson MJ, Carlson B, Crow GL (1995) Coral growth in high-nutrient, low-pH seawater: a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14:215–223 [ 10.1007/BF00334344]CrossRefGoogle Scholar
  15. Australian Bureau of Meteorology and CSIRO (2011) Climate change in the Pacific: Scientific assessment and new research. Volume 1: Regional Overview (ISBN: 9781921826733 (pbk.) ISBN: 9781921826740 (ebook))Google Scholar
  16. Bach LT (2015) Reconsidering the role of carbonate ion concentration in calcification by marine organisms. Biogeosci Discuss 12:6689–6722. [doi: 10.5194/bgd-12-6689-2015]CrossRefGoogle Scholar
  17. Barnes DJ, Crossland CJ (1980) Diurnal and seasonal variations in the growth of a staghorn coral measured by time-lapse photography. Limnol Oceanog 35(6): 1113–1117 [doi:  10.4319/lo.1980.25.6.1113]CrossRefGoogle Scholar
  18. Barnes DJ, Lough JM (1993) On the nature and causes of density banding in massive coral skeletons. J Exp Mar Biol Ecol 167: 91–108 [doi: 10.1016/0022-0981(93)90186-R]CrossRefGoogle Scholar
  19. Brahmi C, Kopp C, Domart-Coulon I, Stolarski J, Meibom A (2012) Skeletal growth dynamics linked to trace-element composition in the scleractinian coral Pocillopora damicornis. Geochimica et Cosmochimica Acta 99:146–158CrossRefGoogle Scholar
  20. Brown BE, Hewit R, Le Tissier MAA (1983) The nature and construction of skeletal spines in Pocillopora damicornis (Linnaeus). Coral Reefs 2:81–89 [ 10.1007/BF02395278]CrossRefGoogle Scholar
  21. Caldera K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365 [doi: 10.1038/425365a]CrossRefGoogle Scholar
  22. Carpenter KE, Abrar M, Aeby GR, Aronson B, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563 [doi:  10.1126/science.1159196]CrossRefGoogle Scholar
  23. Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30:911–923 [ 10.1007/s00338-011-0786-7]CrossRefGoogle Scholar
  24. Chave KE (1984) Physics and chemistry of biomineralization. Ann Rev Earth Planet Sci 12: 293–305 [doi:  10.1146/annurev.ea.12.050184.001453]CrossRefGoogle Scholar
  25. Cohen AL, Holcomb M (2009) Why corals care about ocean acidification. Oceanography 22:118–127 [ 10.5670/oceanog.2009.102]Google Scholar
  26. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. In: Dove PM, Weiner S, deYoreo JJ (eds) Biomineralization. reviews in mineralogy and geochemistry vol 54, The Mineralogical Society of America, Washington DC, pp 151–187 [doi: 10.2113/0540151]Google Scholar
  27. 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 Geosyst 10:Q07005 [doi: 10.1029/2009GC002411]CrossRefGoogle Scholar
  28. Coles SL (1988) Limitations on reef coral development in the Arabian Gulf: temperature or algal competition? Proc 6th Int Coral Reef Symp 3:211–216Google Scholar
  29. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration rates of reef corals. Mar Biol 43:209–216 [doi: 10.1007/BF00402313]CrossRefGoogle Scholar
  30. Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907 [doi: 10.1007/s00338-010-0638-x]CrossRefGoogle Scholar
  31. Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ. (2014a) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc B 281: 20141339. [doi: 10.1098/rspb.2014.1339]CrossRefGoogle Scholar
  32. Comeau S, Carpenter RC, Edmunds PJ (2012) Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate. Proc R Soc B 280:20122374 [doi: 10.1098/rspb.2012.2374]CrossRefGoogle Scholar
  33. Comeau S, Carpenter RC, Edmunds PJ (2013) Response to coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc R Soc B 280:20131153. [doi: 10.1098/rspb.2013.1153]CrossRefGoogle Scholar
  34. Comeau S, Edmunds PJ, Lantz CA, Carpenter RC (2014c) Water flow modulates the response of coral reef communities to ocean acidification. Sci Reports 4:6681 [doi: 10.1038/srep06681]CrossRefGoogle Scholar
  35. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014b) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnol Oceanogr 59:1081–1091CrossRefGoogle Scholar
  36. Connolly SR, Lopez-Yglesias MA, Anthony KRN (2012) Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs 31:951–960. [doi:  10.1007/s00338-012-0925-9]CrossRefGoogle Scholar
  37. Crossland CJ, Barnes DJ (1974) The role of metabolic nitrogen in coral calcification. Mar Biol 28:325–332CrossRefGoogle Scholar
  38. Cyronak T, Santos IR, Erler DV, Eyre BD (2013a) Groundwater and porewater as major sources of alkalinity to a fringing coral reef lagoon (Muri Lagoon, Cook Islands), Biogeosci 10:2467–2480 [doi: 10.5194/bg-10-2467-2013]CrossRefGoogle Scholar
  39. Cyronak T, Santos IR, McMahon A, Eyre BD (2013b) Carbon cycling hysteresis in permeable carbonate sands over a diel cycle: Implications for ocean acidification. Limnol Oceanogr 58(1):131–143 [doi: 10.4319/lo.2013.58.1.0131]CrossRefGoogle Scholar
  40. Cyronak T, Schulz KG, Santos IR, Eyre BD (2014) Enhanced acidification of global coral reefs driven by regional biogeochemical feedbacks. Geophys Res Lett 41(15): 5538–5546 [doi: 10.1002/2014GL060849]CrossRefGoogle Scholar
  41. Cyronak T, Schulz KG, Jokiel PL (2015) The Omega myth: what really drives lower calcification rates in an acidifying ocean. ICES J Mar Sci [doi: 10.1093/icesjms/fsv075]Google Scholar
  42. de Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2010) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs. 30(2):321–328 [doi: 10.1007/s00338-010-0697-z]CrossRefGoogle Scholar
  43. Dore JE, Lukas R, Sadler DW, Church MJ, Karl DM (2009) Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc Natl Acad Sci USA 106:12235–12240 [doi:  10.1073/pnas.0906044106]CrossRefGoogle Scholar
  44. Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36:221–236 [doi: 10.1007/s12237-013-9594-3]CrossRefGoogle Scholar
  45. Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324Google Scholar
  46. Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410 [doi: 10.4319/lo.2011.56.6.2402]CrossRefGoogle Scholar
  47. Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Global Change Biology. 18:2173–2183 [doi:  10.1111/j.1365-2486.2012.02695.x]CrossRefGoogle Scholar
  48. Enns T (1967) Facilitation by carbonic anhydrase of carbon dioxide transport. Science 155:44–47 [doi: 10.1126/science.155.3758.44]CrossRefGoogle Scholar
  49. Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032 [doi:  10.1364/AO.49.005032]CrossRefGoogle Scholar
  50. Erez J, Reynaud S, Silverman J, Schneider K, Allemand D (2011) Coral calcification under ocean acidification and global change. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. New York, Springer Press, pp 151–176CrossRefGoogle Scholar
  51. Evenhuis C, Lenton A, Cantin NE, Lough JM (2015) Modelling coral calcification accounting for the impacts of coral bleaching and ocean acidification. Biogeosci 12:2607–2630 [doi: 10.5194/bg-12-2607-2015]CrossRefGoogle Scholar
  52. 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. Nature Climate Change 1:165–169 [doi: 10.1038/nclimate1122]CrossRefGoogle Scholar
  53. Fagan KE, Mackenzie FT (2007) Air–sea CO2 exchange in a subtropical estuarine-coral reef system, Kaneohe Bay, Oahu, Hawaii. Mar Chem 106:174–191 [doi: 10.1016/j.marchem.2007.01.016]CrossRefGoogle Scholar
  54. Falkowski PG, Dubinsky Z, Muscatine L, Porter J (1984) Light and the bioenergetics of a symbiotic coral. BioScience 34:705–709 [doi: 10.2307/1309663]CrossRefGoogle Scholar
  55. Falter JL, Lowe RJ, Atkinson MJ, Cuet P (2012) Seasonal coupling and de-coupling of net calcification rates from coral reef metabolism and carbonate chemistry at Ningaloo Reef, Western Australia. J Geophys Res 117:C05003 [doi: 10.1029/2011JC007268]CrossRefGoogle Scholar
  56. Fang L-s, Chen Y-wJ, Chen C-s (2004) Why does the white tip of stony coral grow so fast without zooxanthellae? Mar Biol 103:359–363 [doi: 10.1007/BF00397270]CrossRefGoogle Scholar
  57. Feely RA, Doney C, Cooley S (2009) Ocean acidification. Oceanography 22:36–47CrossRefGoogle Scholar
  58. Ferrier-Pagès C, Witting, J, Tambtutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240 [doi: 10.1007/s00338-003-0312-7]CrossRefGoogle Scholar
  59. Fine M, Oren U, Loya Y (2002) Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica. Mar Ecol Prog Ser 234:119–125 [doi: 10.3354/meps234119]CrossRefGoogle Scholar
  60. Furla P, Galgani I, Durand I, Allemand D (2000b) Sources and mechanisms of inorganic transport for coral calcification and photosynthesis. J Exp Mar Biol Ecol 203:3445–3457Google Scholar
  61. Furla P, Orsenigo MN, Allemand D (2000a) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon absorption for endosymbiont photosynthesis. Am J Physiol 278: R870–R881Google Scholar
  62. Gagnon AC, Adkins JF, Erez J (2012) Seawater transport during coral biomineralization. Earth and Planetary Science Letters 329–330:150–161 [doi: 10.1016/j.epsl.2012.03.005]CrossRefGoogle Scholar
  63. Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, McLaughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG, Peters EC, Reynolds T, Rotstein DS, Sileo L, Woodley CM (2007) Coral disease and health workshop: Coral histopathology II. NOAA Technical Memorandum NOS NCCOS 56 and NOAA Technical Memorandum CRCP 4. National Oceanic and Atmospheric Administration, Silver Spring, MD 84 ppGoogle Scholar
  64. Gattuso JP, 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 [doi:  10.1093/icb/39.1.160]CrossRefGoogle Scholar
  65. Gladfelter EH (1982) Skeletal development in Acropora cervicornis: I. Patterns of calcium carbonate accretion in the axial corallite. Coral Reefs 1:45–51 [doi: 10.1007/BF00286539]CrossRefGoogle Scholar
  66. Gladfelter EH (1983) Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol Bull 165:619–636CrossRefGoogle Scholar
  67. Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland C (ed.) Life and death of coral reefs. New York: Chapman and Hall. 68–95CrossRefGoogle Scholar
  68. Goiran C, Almoghrabi S, Allemand D, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association. 1. Photosynthetic performances of symbionts and dependence on sea water bicarbonate. J Exp Mar Biol Ecol 199:207–225 [doi:  10.1016/0022-0981(95)00201-4]CrossRefGoogle Scholar
  69. Golbuu Y, Wolanski E, Idechong JW, Victor S, Isechal AL, Oldiais NW, Idip Jr D, Richmond RH, van Woesik R (2012) Predicting Coral Recruitment in Palau’s Complex Reef Archipelago. PLoS ONE 7(11):e50998. [doi: 10.1371/journal.pone.0050998]CrossRefGoogle Scholar
  70. Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different light conditions. Biol Bull 116:59–75CrossRefGoogle Scholar
  71. Goreau TF (1963) Calcium carbonate deposition by coralline algae and corals in relation to their roles as reef-builders. Ann NY Acad Sci 109:127–167 [doi:  10.1111/j.1749-6632.1963.tb13465.x]CrossRefGoogle Scholar
  72. Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250CrossRefGoogle Scholar
  73. Goreau TJ (1977) Coral skeletal chemistry: physiological and environmental regulation of stable isotopes and trace metals in Montastrea annularis. Proc R Soc B 196:291–315 [doi:  10.1098/rspb.1977.0042]CrossRefGoogle Scholar
  74. Graham D, Smillie RM (1976) Carbonate dehydratase in marine organisms of the Great Barrier Reef. Aust J Plant Physiol 3:113–119 [doi:  10.1071/PP9760113]CrossRefGoogle Scholar
  75. Graus RR, Macintyre IG (1976) Light control of growth form in colonial reef corals: computer simulation. Science 193:895–897 [doi:  10.1126/science.193.4256.895]CrossRefGoogle Scholar
  76. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189 [doi: 10.1038/nature04565]CrossRefGoogle Scholar
  77. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7(3): e33353 [doi: 10.1371/journal.pone.0033353]CrossRefGoogle Scholar
  78. Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios 7:389–398 [doi: 10.2307/3514476]CrossRefGoogle Scholar
  79. Harriott VJ, Banks SA (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83–94 [doi:  10.1007/s00338-001-0201-x]CrossRefGoogle Scholar
  80. Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98 [ 10.1111/j.1529-8817.2007.00445.x]CrossRefGoogle Scholar
  81. 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 [doi:  10.1126/science.1152509]CrossRefGoogle Scholar
  82. Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6(12): e28983 [doi: 10.1371/journal.pone.0028983]CrossRefGoogle Scholar
  83. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–45 [doi:  10.1146/annurev-physiol-021909-135900]Google Scholar
  84. Holcomb MC, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386:27–33 [doi: 10.1016/j.jembe.2010.02.007]CrossRefGoogle Scholar
  85. Hönisch B, Ridgwel A, Schmidt DN, Thomas E, Gibbs SJ, Sluijs A, Zeebe R, Kump, L, Martindale RC, Greene SE, KiesslingW, Ries J, Zachos JC, Royer DL, Barker S, Marchitto TM Jr, Moyer R, Pelejero C, Ziveri P, Foster GL, Williams B (2012) The geological record of ocean acidification. Science 335:1058–1063 [doi:  10.1126/science.1208277]CrossRefGoogle Scholar
  86. Hunter CL, Evans CW (1995) Coral reefs in Kaneohe Bay, Hawaii: two centuries of western influence and two decades of data. Bull Mar Sci 57:501–515Google Scholar
  87. IPCC (2001) Climate Change 2001: The scientific basis. The contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Houghton JT, Ding Y, Griggs DJ et al. (eds) Cambridge University Press, New York pp 1–881Google Scholar
  88. IPCC (2007) Technical Summary. Climate Change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds). Cambridge University Press, New York pp 19–91Google Scholar
  89. Jaubert J (1977) Light metabolism and growth forms of the hermatypic scleractinian coral Synaraea convexa (Verrill) in the lagoon of Moorea (French Polynesia). Proc 3rd Int Coral Reef Symp 1:483–488Google Scholar
  90. Jimenez IM, Kühl M, Larkum AWD, Ralph PJ (2011) Effects of flow and colony morphology on the thermal boundary layer of corals. J R Soc Interface 8:1785–1795 [doi: 10.1098/rsif.2011.0144]CrossRefGoogle Scholar
  91. Jokiel PL (1978) Effects of water motion on reef corals. J Exp Mar Biol Ecol 35:87–97CrossRefGoogle Scholar
  92. Jokiel PL (2011a) Ocean acidification and control of reef coral calcification by boundary layer limitation of proton flux. Bull Mar Sci 87:639–657 [ 10.5343/bms.2010.1107]Google Scholar
  93. Jokiel PL (2011b) The reef coral two compartment proton flux model: A new approach relating tissue-level physiological processes to gross corallum morphology. J Exp Mar Biol Ecol 409:1–12 [doi: 10.1016/j.jembe.2011.10.008]Google Scholar
  94. Jokiel PL (2013) Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc R Soc B 20130031 [doi: 10.1098/rspb.2013.0031]Google Scholar
  95. Jokiel PL (2015) Predicting the impact of ocean acidification on coral reefs: evaluating the assumptions involved. ICES J Mar Sci [doi:  10.1093/icesjma/fsv091]Google Scholar
  96. Jokiel PL, Bahr KD, Rodgers KS (2014b) Low-cost, high-flow mesocosm system for simulating ocean acidification with CO2 gas. Limnol Oceanogr Methods 12:313–322 [doi: 10.4319/lom.2014.12.313]Google Scholar
  97. Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208CrossRefGoogle Scholar
  98. Jokiel PL, Jury CP, Rodgers KS (2014a) Coral-algae metabolism and diurnal changes in the CO2-carbonate system of bulk sea water. PeerJ 2:e378 [doi: 10.7717/peerj.378]CrossRefGoogle Scholar
  99. Jokiel PL, Morrissey JI (1986) Influence of size on primary production in the reef coral Pocillopora damicornis and the tropical macroalga Acanthophora spicifera. Mar Biol 91:15–26 [doi: 10.1007/BF00397566]CrossRefGoogle Scholar
  100. Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483 [doi: 10.1007/s00338-008-0380-9]CrossRefGoogle Scholar
  101. Jury CP, Thomas FI, Atkinson MJ, Toonen RJ (2013) Buffer capacity, ecosystem feedbacks, and seawater chemistry under global change. Water 5:1303–1325CrossRefGoogle Scholar
  102. Jury CP, Whitehead RF, Szmant A (2010) 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 [doi: 10.1111/j.1365-2486.2009.02057.x]CrossRefGoogle Scholar
  103. Kaandorp JA, Sloot PMA, Merks RMH, Bak RPM, Vermeij MJA, Maier C (2005) Morphogenesis of the branching reef coral Madracis mirabilis. Proc R Soc B 272:127–133 [doi: 10.1098/rspb.2004.2934]CrossRefGoogle Scholar
  104. Kaandorp, JA, Filatov M, Chindapol N (2011) Simulating and quantifying the environmental influence on coral colony growth form. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. New York; Springer Press, pp 177–185Google Scholar
  105. Kajiwara K, Yokoch H, Nagai A, Ueno S (1997) Growth patterns of white-tipped and brown-tipped branches of the reef building coral, Acropora pulchra from Amitori Bay, Iriomote Island. Bull Inst Ocean Res Dev, Tokai Univ 18: 1–10Google Scholar
  106. Kawaguti S, Sakumoto D (1948) The effects of light on the calcium deposition of corals. Bull Oceanogr Inst Taiwan 4:65–70Google Scholar
  107. Kinsey DW (1978) Alkalinity changes and coral reef calcification. Limnol Oceanog 23(5):989–991 [doi:  10.4319/lo.1978.23.5.0989]CrossRefGoogle Scholar
  108. Kinsey DW, Davies PJ (1979) Effect of elevated nitrogen and phosphorus on coral reef growth. Limnol Oceanogr 24:935–940 [ 10.4319/lo.1979.24.5.0935]CrossRefGoogle Scholar
  109. Kleypas JA, Buddemeier RW, Archer D, Gattuso JP, Langdon C, Opdyke BN (1999b) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120 [doi: 10.1126/science.284.5411.118]CrossRefGoogle Scholar
  110. Kleypas JA, Buddemeier RW, Eakin CM, Gattuso J-P, Guinotte J, Hoegh-Guldberg O, Iglesias-Prieto R, Jokiel PL, Langdon C, Skirving W, Strong AE (2005) Comment on “Coral reef calcification and climate change: The effect of ocean warming,” Geophys. Res. Lett., 32, L08601 [doi: 10.1029/2004GL022329]CrossRefGoogle Scholar
  111. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CI, 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 US Geological Survey. 88 ppGoogle Scholar
  112. Kleypas JA, McManus JW, Meñez LAB (1999a) Environmental limits to coral reef development: where do we draw the line? Amer Zool 39 (1): 146–159. [doi:  10.1093/icb/39.1.146]CrossRefGoogle Scholar
  113. Kline DI, Teneva L, Schneider K, Miard T, Chai A, Marker M, Headley K, Opdyke B, Nash M, Valetich M, Caves JK, Russell BD, Connell SD, Kirkwood BJ, Brewer P, Peltzer E, Silverman J, Caldeira K, Dunbar RB, Koseff JR, Monismith SG, Mitchell BG, Dove S, Hoegh-Guldberg O. (2012) A short-term in situ CO2 enrichment experiment on Heron Island (GBR). Sci Rep 2:413 [doi: 10.1038/srep00413]CrossRefGoogle Scholar
  114. Kuffner IB, Hickey TD, Morrison JM (2013) Calcification rates of the massive coral Siderastrea siderea and crustose coralline algae along the Florida Keys (USA) outer-reef tract. Coral Reefs 32:987–997 [doi: 10.1007/s00338-013-1047-8]CrossRefGoogle Scholar
  115. Kühl, M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  116. Lamberts AE (1974) Measurement of alizarin deposited by coral. Proc 2nd Int Coral Reef Symp 2:241–244Google Scholar
  117. 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 [doi:110 C09S07/ 10.1029/2004JC002576]
  118. Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H. (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639–654 [doi:  10.1029/1999GB001195]CrossRefGoogle Scholar
  119. Lantz C (2011) Spatiotemporal analysis of the carbonate system on a coral reef, Oahu, Hawaii. MS Thesis. Hawaii Pacific University, Honolulu. 103 ppGoogle Scholar
  120. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds). Coral reefs: an ecosystem in transition. New York, Springer Press. pp 405–419CrossRefGoogle Scholar
  121. Lesser MP, Weis VM, Patterson, MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus) – diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J Exp Mar Biol Ecol 178:153–179CrossRefGoogle Scholar
  122. Lowenstam HS (1974) Impact of life on chemical and physical processes. In: Goldberg ED (ed.), The Sea, vol. 5, Marine chemistry, pp 725–796. Wiley, New YorkGoogle Scholar
  123. Marcelino LA, Westneat MW, Stoyneva V, Henss J, Rogers JD, Radosevich A, Turzhitsky V, Siple M, Fang A, Swain TD, Fung J, Backman V (2013) Modulation of light-enhancement to symbiotic algae by light-scattering in corals and evolutionary trends in bleaching. PLoS ONE 8(4): e61492 [doi:  10.1371/journal.pone.0061492]CrossRefGoogle Scholar
  124. Marshall AT, Wright A (1998) Coral calcification: autoradiography of a scleractinian coral Galaxea fascicularis after incubation in 45Ca and 14C. Coral Reefs 17:37–47 [doi:  10.1007/s003380050092 Google Scholar
  125. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biol 15:2089–2100 [doi:  10.1111/j.1365-2486.2009.01874.x]CrossRefGoogle Scholar
  126. Martinez JA, Smith CM, Richmond RH (2012) Algal mats degrade coral reef physical habitat quality. Estuar Coast Shelf Sci 99:42–49 [doi: 10.1016/j.ecss.2011.12.022]CrossRefGoogle Scholar
  127. Marubini F, Atkinson MJ (1999) Effects of lowered pH and elevated nitrate on coral calcification. Mar Ecol Prog Ser 188:117–121 [doi: 10.3354/meps188117]CrossRefGoogle Scholar
  128. 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 220:153–162CrossRefGoogle Scholar
  129. 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 [doi: 10.1007/s00338-008-0375-6]CrossRefGoogle Scholar
  130. Marubini F, Ferrier-Pages C, Cuif J (2003) Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison. Proc R Soc B 270:179–184 [doi: 10.1098/rspb.2002.2212]CrossRefGoogle Scholar
  131. 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 USA 107:2527–2531[doi:  10.1073/pnas.0912348107]CrossRefGoogle Scholar
  132. McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117CrossRefGoogle Scholar
  133. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change [doi: 10.1038/nclimate1473]Google Scholar
  134. McMahon A. Santos IR, Cyronak T, Eyre BD (2013) Hysteresis between coral reef calcification and the seawater aragonite saturation state. Geophys Res Lett 40:4675–4679 [doi: 10.1002/grl.50802]CrossRefGoogle Scholar
  135. McNeil BI, Matear RJ, Barnes DJ (2004) Coral reef calcification and climate change: The effect of ocean warming, Geophys Res Lett 31, L22309 [doi: 10.1029/2004GL021541]CrossRefGoogle Scholar
  136. Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, location and role in biomineralization. J Biol Chem 283:25475–25484 [doi:  10.1074/jbc.M804726200]CrossRefGoogle Scholar
  137. Murillo LJ, Jokiel PL, Atkinson MJ (2014) Alkalinity to calcium flux ratios for corals and coral reef communities: variances between isolated and community conditions. PeerJ 2:e249 [doi: 10.7717/peerj.24]CrossRefGoogle Scholar
  138. Muscatine, L (1973) Nutrition in corals. In; Jones OA, Endean R (eds) Biology and geology of coral reefs, 2:271–324. New York: Academic PressGoogle Scholar
  139. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. pp 75–87 In: Dubinsky Z (ed) Coral reefs. Elsevier Science Publishers BV, Amsterdam.Google Scholar
  140. Muscatine L, Falkowski PG, Porter J, Dubinsky Z (1984) Fate of photosynthetically fixed carbon in light and shade adapted corals. Proc R Soc Lond B Biol Sci 222:181–202 [doi:  10.1098/rspb.1984.0058]CrossRefGoogle Scholar
  141. Muscatine L, Porter J (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27: 454–460 [doi:  10.2307/1297526]CrossRefGoogle Scholar
  142. Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320CrossRefGoogle Scholar
  143. Ohde S (1995) Calcium carbonate production and carbon dioxide flux on a coral reef, Okinawa. In: Sakai EH, Nozaki Y (eds) Biogeochemical processes and ocean flux in the Western Pacific. Terra Scientific Pub Co, TokyoGoogle Scholar
  144. Ohde S, Hossain MMM (2004) Effect of CaCO3 (aragonite) saturation state of seawater on calcification of Porites coral. Geochem J 38:613–621CrossRefGoogle Scholar
  145. Ohde S, van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65: 559–576Google Scholar
  146. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty first century and its impact on calcifying organisms. Nature 437:681–686 [doi: 10.1038/nature04095]CrossRefGoogle Scholar
  147. Pandolfi JM, Connolly RM, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422 [doi:  10.1126/science.1204794]CrossRefGoogle Scholar
  148. Pearse V, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Bio Bull (Woods Hole) 141: 350–363.CrossRefGoogle Scholar
  149. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel Program Developed for CO2 System Calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Dept of Energy, Oak Ridge, TennesseeGoogle Scholar
  150. Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. J Geophys Res 110:C09S10 [doi: 10.1029/2004JC002561]
  151. Price NN, Martz TR, Brainard RE, Smith JE (2012) Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS ONE 7(8):e43843 [doi: 10.1371/journal.pone.0043843]CrossRefGoogle Scholar
  152. Reef R, Kaniewska P, Hoegh-Guldberg O (2009) Coral skeletons defend against ultraviolet radiation. PLoS ONE 4(11): e7995 [doi: 10.1371/journal.pone.0007995]CrossRefGoogle Scholar
  153. Renegar DA, Riegl BM (2005) Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. Mar Ecol Prog Ser 293:69–76CrossRefGoogle Scholar
  154. Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pages C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biol 9:1660–1668 [doi:  10.1046/j.1365-2486.2003.00678.x]CrossRefGoogle Scholar
  155. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064 [doi: 10.1016/j.gca.2011.04.025]CrossRefGoogle Scholar
  156. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology. 37:1131–1134 [doi:  10.1130/G30210A.1]CrossRefGoogle Scholar
  157. Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674 [doi:  10.1007/s00338-010-0632-3]CrossRefGoogle Scholar
  158. Rinkevich B, Loya Y (1983) Short term fate of photosynthetic products in a hermatypic coral. J Exp Mar Biol Ecol 73:175–184 [doi: 10.1016/j.gca.2011.04.025]CrossRefGoogle Scholar
  159. Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso J-P (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 7:289–300CrossRefGoogle Scholar
  160. Roleda M, Boyd P, Hurd C (2012) Before ocean acidification: calcifier chemistry lessons. J Phycol 48:840–843 [doi:  10.1111/j.1529-8817.2012.01195.x]CrossRefGoogle Scholar
  161. Roos P (1967) Growth and occurrence of the reef coral Porites astreoides (Lamarck) on relation to submarine radiance distribution. Dissertation, Drukkerij Elinkwijk, Utrecht, NorwayGoogle Scholar
  162. Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05. ISBN 0 85403 617 2 Download available at
  163. Santos SR, Toyoshima J, Kin zie III RA (2009) Spatial and temporal dynamics of symbiotic dinoflagellates (Symbiodinium: Dinophyta) in the perforate coral Montipora capitata. Galaxea, Journal of Coral Reef Studies 11:139–147 [doi: 10.3755/galaxea.11.139]CrossRefGoogle Scholar
  164. 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 [doi: 10.4319/lo.2006.51.3.1284 Google Scholar
  165. Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Marine Chem 127:64–75 [doi: 10.1016/j.marchem.2011.08.003]CrossRefGoogle Scholar
  166. Shamberger, KEF, Cohen AL, Golbuu Y, McCorkle DC, Lentz SJ, Barkley HC (2014) Diverse coral communities in naturally acidified waters of a Western Pacific Reef. Geophys Res Lett 41 [doi: 10.1002/2013GL058489]Google Scholar
  167. Shapiro O, Fernandez VI, Garren M, Guasto JS, Debaillon-Vesque FP, Kramarsky-Winter E, Vardi A, Stocker R. (2014) Vortical ciliary flows actively enhance mass transport in reef corals. Proc Nat Acad Sci 111 (37): 13391–13396 [doi:  10.1073/pnas.1323094111]CrossRefGoogle Scholar
  168. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461[doi:  10.2307/1542485]CrossRefGoogle Scholar
  169. Shashar N, Kinane S, Jokiel PL, Patterson MR (1996) Hydromechanical boundary layers over a coral reef. J Exp Mar Biol Ecol 199:17–28 [doi: 10.1016/0022-0981(95)00156-5]CrossRefGoogle Scholar
  170. Silbiger NJ, Donahue MJ (2015) Secondary calcification and dissolution respond differently to future ocean conditions. Biogeosci 12:567–578 [doi: 10.5194/bg-12-567-2015]CrossRefGoogle Scholar
  171. Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009), Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36, L05606 [doi: 10.1029/2008GL036282]CrossRefGoogle Scholar
  172. Silverman J, Lazar B, Erez J (2007) Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochem [doi  10.1007/s10533-007-9075-5]Google Scholar
  173. Simkiss K (1964) Phosphates as crystal poisons of calcification. Biol Rev 39:487–504 [doi:  10.1111/j.1469-185X.1964.tb01166.x]CrossRefGoogle Scholar
  174. Smith SV, Buddemeier RW (1992) Global change and coral reef ecosystems. Ann Rev Ecol Syst 23:89–118CrossRefGoogle Scholar
  175. Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495 [doi:  10.4319/lo.1975.20.3.0493]CrossRefGoogle Scholar
  176. Smith SV, Kinsey DW, 1978. Calcification and organic carbon metabolism as indicated by carbon dioxide. In: Stoddart, DR, Johannes RE (eds) Coral reefs: research methods, pp 469–484Google Scholar
  177. Stambler N, Popper N, Dubinsky Z, Stimson J (1991) Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pac Sci 45:299–307Google Scholar
  178. Suzuki A, Nakamori T, Kayanne H (1995) The mechanism of production enhancement in coral reef carbonate systems: model and empirical results. Sediment Geol 99:259–280 [doi:  10.1016/0037-0738(95)00048-D]CrossRefGoogle Scholar
  179. Tambutté É, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041Google Scholar
  180. Tambutté É, Allemand D, Zoccola D, Meibom A, Lotto S, Caminiti N, Tambutté S (2007) Observations of the tissue-skeleton interface in the scleractinian coral Stylophora pistillata. Coral Reefs 26:517–529 [doi:  10.1007/s00338-007-0263-5]CrossRefGoogle Scholar
  181. Tambutté É, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D (2012) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. R Lond B 279:19–27 [doi: 10.1098/rspb.2011.0733]CrossRefGoogle Scholar
  182. Taylor DL (1977) Intra-clonal transport of organic compounds and calcium in some Atlantic reef corals. Proc 3rd Int Coral Reef Symp pp 431–436Google Scholar
  183. Thomsen J, Haynert K, Wegner KM, Melzner F (2015) Impact of seawater carbonate chemistry on the calcification of marine bivalves. Biogeosci Discuss 12:1543–1571 [doi:  10.5194/bgd-12-1543-2015]CrossRefGoogle Scholar
  184. Tourniaire F, Pulos S (1985) Proportional reasoning: A review of the literature. Educ Stud Math 16(2):181–204 [doi:  10.1007/BF02400937]CrossRefGoogle Scholar
  185. Vandermeulen JH, Davis ND, Muscatine L (1972) The effects of inhibitors of photosynthesis on zooxanthellae in corals and other marine invertebrates. Mar Biol 16:185–191 [doi: 10.1007/BF00346940]Google Scholar
  186. Venn AA, Tambutté É, Holcomb M, Allemand D, Tambutté S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6(5) e20013 [doi:  10.1371/journal.pone.0020013]CrossRefGoogle Scholar
  187. Venn AA, Tambutté É, 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(5):1634–1639 [doi/ 10.1073/pnas.1216153110]CrossRefGoogle Scholar
  188. Venn AA, Tambutté É, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Intracellular pH in Symbiotic Cnidarians. Proc Natl Acad Sci USA 106:16574–16579 [doi:  10.1073/pnas.0902894106]CrossRefGoogle Scholar
  189. Venti A, Andersson A, Langdon C (2014) Multiple driving factors explain spatial and temporal variability in coral calcification rates on the Bermuda platform. Coral Reefs 33(4):979–997 [doi: 10.1007/s00338-014-1191-9]CrossRefGoogle Scholar
  190. Veron JEN (2000) Corals of the world. Vol. 1–3. Aust Inst Mar Sci, Townsville MC, Qld, AustraliaGoogle Scholar
  191. Veron JEN (2008) Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27:459–472 [doi: 10.1007/s00338-008-0381-8]CrossRefGoogle Scholar
  192. Vicsek T (1989) Fractal growth phenomena. World Scientific, London.CrossRefGoogle Scholar
  193. Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202 [doi:  10.1007/BF00391958]CrossRefGoogle Scholar
  194. Wijgerde T, Jurriaans S, Hoofd M, Verreth JAJ, Osinga R (2012) Oxygen and heterotrophy affect calcification of the scleractinian coral Galaxea fascicularis. PLoS ONE 7(12): e52702. [doi: 10.1371/journal.pone.0052702]CrossRefGoogle Scholar
  195. Wilt FH (2005) Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol 280:15–25 [doi: 10.1016/j.ydbio.2005.01.019]CrossRefGoogle Scholar
  196. Wisshak M, Schönberg CHL, Form A, Freiwald A (2013) Effects of ocean acidification and global warming on reef bioerosion—lessons from a clionaid sponge. Aquat Biol 19:111–127 [doi:  10.3354/ab00527]CrossRefGoogle Scholar
  197. Wooldridge S (2013) A new conceptual model of coral biomineralisation: hypoxia as the physiological driver of skeletal extension. Biogeosci 10:2867–2884 [doi: 10.5194/bg-10-2867-2013]CrossRefGoogle Scholar
  198. Yates KK, Halley RB (2006) Carbonate concentration and pCO2 thresholds for calcification and dissolution on the Molokai reef flat, Hawaii. Biogeosci 3:357–369 [doi: 10.5194/bg-3-357-2006]CrossRefGoogle Scholar
  199. Yonge CM (1968) Living corals. Proc R Soc Lond B 169:329–344CrossRefGoogle Scholar
  200. Zoccola D, Tambutté É, Sénégas-Balas F, Michiels J-F, Failla JP, Jaubert J, Allemand D (1999) Cloning of a calcium channel α1 subunit from the reef-building coral, Stylophora pistillata. Gene 227(2):157–167 [doi: 10.1016/S0378-1119(98)00602-7]CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Paul L. Jokiel
    • 1
    Email author
  • Christopher P. Jury
    • 1
  • Ilsa B. Kuffner
    • 2
  1. 1.Hawaii Institute of Marine BiologyUniversity of HawaiiKaneoheUSA
  2. 2.U.S. Geological SurveySt. Petersburg Coastal and Marine Science CenterSt. PetersburgUSA

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