Marine Biology

, 163:135 | Cite as

Annual response of two Mediterranean azooxanthellate temperate corals to low-pH and high-temperature conditions

  • Juancho Movilla
  • Eva Calvo
  • Rafel Coma
  • Eduard Serrano
  • Àngel López-Sanz
  • Carles Pelejero
Original paper


Ocean acidification (OA) and warming related to the anthropogenic increase in atmospheric CO2 have been shown to have detrimental effects on several marine organisms, especially those with calcium carbonate structures such as corals. In this study, we evaluate the response of two Mediterranean shallow-water azooxanthellate corals to the projected pH and seawater temperature (ST) scenarios for the end of this century. The colonial coral Astroides calycularis and the solitary Leptopsammia pruvoti were grown in aquaria over a year under two fixed pH conditions, control (8.05 pHT units) and low (7.72 pHT units), and simulating two annual ST cycles, natural and high (+3 °C). The organic matter (OM), lipid and protein content of the tissue and the skeletal microdensity of A. calycularis were not affected by the stress conditions (low pH, high ST), but the species exhibited a mean 25 % decrease in calcification rate at high-ST conditions at the end of the warm period and a mean 10 % increase in skeletal porosity under the acidified treatment after a full year cycle. Conversely, an absence of effects on calcification and skeletal microdensity of L. pruvoti exposed to low-pH and high-ST treatments contrasted with a significant decrease in the OM, lipid and protein content of the tissue at high-ST conditions and a 13 % mean increase in the skeletal porosity under low-pH conditions following a full year of exposure. This species-specific response suggests that different internal self-regulation strategies for energy reallocation may allow certain shallow-water azooxanthellate corals to cope more successfully than others with global environmental changes.


  1. Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Heidelberg, pp 119–150CrossRefGoogle Scholar
  2. Anthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, energetics, and coral mortality risk: effects of temperature, light, and sediment regime. Limnol Oceanogr 52:716–726CrossRefGoogle Scholar
  3. Anthony KRN, Kline DI, Diaz-Pulido G, Dove SG, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446CrossRefGoogle Scholar
  4. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195Google Scholar
  5. Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Glob Change Biol 13:2078–2088CrossRefGoogle Scholar
  6. Barnes H, Blackstock J (1973) Estimation of lipids in marine animals and tissues: detailed investigation of the sulphophosphovanillin method for total lipids. J Exp Biol 12:103–118CrossRefGoogle Scholar
  7. Bianchi CN (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580:7–21CrossRefGoogle Scholar
  8. Bianchi CN, Morri C (1994) Southern species in the Ligurian Sea (northern Mediterranean): new records and a review. Bollettino dei Musei e degli Istituti biologici dell’Università di Genova (1992–1993) 58–59:181–197Google Scholar
  9. Bramanti L, Movilla J, Guron M, Calvo E, Gori A, Dominguez-Carrió C, Grinyó J, López-Sanz A, Martínez-Quintana A, Pelejero C, Ziveri P, Rossi S (2013) Detrimental effects of Ocean Acidification on the economically important Mediterranean red coral (Corallium rubrum). Glob Change Biol 19:1897–1908CrossRefGoogle Scholar
  10. Brewer PG, Peltzer ET (2009) Limits to marine life. Science 324:347CrossRefGoogle Scholar
  11. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  12. Brown BE, Sya’Rani L, Le Tissier M (1985) Skeletal form and growth in Acropora aspera (Dana) from the Pulau Seribu, Indonesia. J Exp Mar Biol Ecol 86:139–150CrossRefGoogle Scholar
  13. Bucher D, Harriott VJ, Roberts LG (1998) Skeletal micro-density, porosity and bulk density of acroporid corals. J Exp Mar Biol Ecol 228:117–136CrossRefGoogle Scholar
  14. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol 49:1–42Google Scholar
  15. Calvo E, Simó R, Coma R, Ribes M, Pascual J, Sabatés A, Gili JM, Pelejero C (2011) Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Climate Res 50:1–29CrossRefGoogle Scholar
  16. Caroselli E, Prada F, Pasquini L, Marzano FN, Zaccanti F, Falini G, Levy O, Dubinsky Z, Goffredo S (2011) Environmental implications of skeletal micro-density and porosity variation in two scleractinian corals. Zoology 114:255–264CrossRefGoogle Scholar
  17. Caroselli E, Zaccanti F, Mattioli G, Falini G, Levy O, Dubinsky Z, Goffredo S (2012) Growth and demography of the solitary scleractinian coral Leptopsammia pruvoti along a sea surface temperature gradient in the Mediterranean Sea. PLoS ONE 7:e37848. doi:10.1371/journal.pone.0037848 CrossRefGoogle Scholar
  18. Casado-Amezúa P, Goffredo S, Templado J, Machordom A (2012) Genetic assessment of population structure and connectivity in the threatened Mediterranean coral Astroides calycularis (Scleractinia, Dendrophylliidae) at different spatial scales. Mol Ecol 21:3671–3685CrossRefGoogle Scholar
  19. Casellato S, Masiero L, Sichirollo E, Soresi S (2007) Hidden secrets of the Northern Adriatic: Tegnuè, peculiar reefs. Cent Eur J Biol 2:122–136Google Scholar
  20. Cebrian E, Ballesteros E (2004) Zonation patterns of benthic communities in an upwelling area from the western Mediterranean (La Herradura, Alboran Sea). Sci Mar 68:69–84CrossRefGoogle Scholar
  21. Chevin LM, Lande R (2010) When do adaptive plasticity and genetic evolution prevent extinction of a density-regulated population? Evolution 64:1143–1150CrossRefGoogle Scholar
  22. Clayton TD, Byrne RH (1993) Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep Sea Res 40:2115–2129CrossRefGoogle Scholar
  23. Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127CrossRefGoogle Scholar
  24. 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. doi:10.1029/2009GC002411 Google Scholar
  25. Coll M, Piroddi C, Steenbeek J et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE 5:e11842CrossRefGoogle Scholar
  26. Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215CrossRefGoogle Scholar
  27. Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol Oceanogr 47:324–331CrossRefGoogle Scholar
  28. Coma R, Ribes M, Gili JM, Zabala M (2002) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453CrossRefGoogle Scholar
  29. Coma R, Linares C, Ribes M, Diaz D, Garrabou J, Ballesteros J (2006) Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Mar Ecol Prog Ser 327:51–60CrossRefGoogle Scholar
  30. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Natl Acad Sci USA 106:6176–6181CrossRefGoogle Scholar
  31. Cooper TF, De’ath G, Fabricius KE, Lough JM (2008) Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Glob Change Biol 14:529–538CrossRefGoogle Scholar
  32. Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  33. De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119CrossRefGoogle Scholar
  34. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A Oceanogr Res Pap 34:1733–1743CrossRefGoogle Scholar
  35. Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172CrossRefGoogle Scholar
  36. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  37. Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37CrossRefGoogle Scholar
  38. Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea, French Polynesia. Mar Biol 159:2149–2160CrossRefGoogle Scholar
  39. 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 Change 1:165–169CrossRefGoogle Scholar
  40. Fantazzini P, Mengoli S, Pasquini L, Bortolotti V, Brizi L, Mariani M, Di Giosia M, Fermani S, Capaccioni B, Caroselli E, Prada F, Zaccanti F, Levy O, Dubinsky Z, Kaandorp JA, Konglerd P, Hammel JU, Dauphin Y, Cuif JP, Weaver JC, Fabricius KE, Wagermaier W, Fratzl P, Falini G, Goffredo S (2015) Gains and losses of coral skeletal porosity changes with ocean acidification acclimation. Nat Commun 6:7785. doi:10.1038/ncomms8785 CrossRefGoogle Scholar
  41. Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811CrossRefGoogle Scholar
  42. Gambi MC, Barbieri F, Signorelli S, Saggiomo V (2010) Mortality events along the Campania coast (Tyrrhenian Sea) in summers 2008 and 2009 and relation to thermal conditions. Biol Mar Mediterr 17:126–127Google Scholar
  43. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103CrossRefGoogle Scholar
  44. Gattuso JP, Hansson L (2011) Ocean acidification: background and history. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 1–20Google Scholar
  45. 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. Integr Comp Biol 39:160–183Google Scholar
  46. Goffredo S, Airi V, Radetic J, Zaccanti F (2006) Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia: Dendrophylliidae) in the Mediterranean. 2. Quantitative aspects of the annual reproductive cycle. Mar Biol 148:923–932CrossRefGoogle Scholar
  47. Goffredo S, Caroselli E, Pignotti E, Mattioli G, Zaccanti F (2007) Variation in biometry and population density of solitary corals with solar radiation and sea surface temperature in the Mediterranean Sea. Mar Biol 152:351–361CrossRefGoogle Scholar
  48. Grubelić I, Antolić B, Despalatović M, Grbec B, Paklar GB (2004) Effect of climatic fluctuations on the distribution of warm-water coral Astroides calycularis in the Adriatic Sea: new records and review. J Mar Biol Ass UK 84:599–602CrossRefGoogle Scholar
  49. Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann NY Acad Sci 1134:320–342CrossRefGoogle Scholar
  50. Herrmann M, Estournel C, Adloff F, Diaz F (2014) Impact of climate change on the northwestern Mediterranean Sea pelagic planktonic ecosystem and associated carbon cycle. J Geophys Res Oceans 119:5815–5836CrossRefGoogle Scholar
  51. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839CrossRefGoogle Scholar
  52. 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 318:1737–1742CrossRefGoogle Scholar
  53. Holcomb M, 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 Bio Ecol 386:27–33CrossRefGoogle Scholar
  54. Holcomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39CrossRefGoogle Scholar
  55. Holcomb M, Venn AA, Tambutté E, Tambutté S, Allemand D, Trotter J, McCulloch MT (2014) Coral calcifying fluid pH dictates response to ocean acidification. Sci Rep 4:5207CrossRefGoogle Scholar
  56. Ip YK, Lim ALL, Lim RWL (1991) Some properties of calcium-activated adenosine triphosphatase from the hermatypic coral Galaxea fascicularis. Mar Biol 1991:191–197CrossRefGoogle Scholar
  57. IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, New YorkGoogle Scholar
  58. Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: monographs on oceanographic methodology. UNESCO, Paris, pp 529–541Google Scholar
  59. Khatiwala S, Tanhua T, Mikaloff-Fletcher S, Gerber M, Doney SC, Graven HD, Gruber N, McKinley GA, Murata A, Ríos AF, Sabine CL, Sarmiento JL (2013) Global ocean storage of anthropogenic carbon. Biogeosciences 10:2169–2219CrossRefGoogle Scholar
  60. Kroeker KJ, Kordas RL, Crim R, Hendriks IE (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896CrossRefGoogle Scholar
  61. Kružić P, Zibrowius H, Pozar-Domac A (2002) Actiniaria and Scleractinia (Cnidaria, Anthozoa) from the Adriatic Sea: first records, confirmed occurrences and significant range extensions of certain species. Italian J Zool 69:345–353CrossRefGoogle Scholar
  62. Kushmaro A, Rosenberg E, Fine M, Ben Haim Y, Loya Y (1998) Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 171:131–137CrossRefGoogle Scholar
  63. Maier C, Schubert A, Berzunza Sánchez MM, Weinbauer MG, Watremez P, Gattuso J-P (2013) End of the century pCO2 levels do not impact calcification in Mediterranean Cold-water corals. PLoS ONE. doi:10.1371/journal.pone.0062655 Google Scholar
  64. Marbà N, Jorda G, Agusti S, Girard C, Duarte CM (2015) Footprints of climate change on Mediterranean Sea biota. Front Mar Sci 2:56. doi:10.3389/fmars.2015.00056 CrossRefGoogle Scholar
  65. Mass T, Drake JL, Haramaty L, Rosenthal Y, Schofield OME, Sherrell RM, Falkowski PG (2012) Aragonite precipitation by “proto-polyps” in coral cell cultures. PLoS ONE 7:4. doi:10.1371/journal.pone.0035049 CrossRefGoogle Scholar
  66. McCulloch MT, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change 2:623–627CrossRefGoogle Scholar
  67. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RN (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  68. Movilla J, Calvo E, Pelejero C, Coma R, Serrano E, Fernández-Vallejo P, Ribes M (2012) Calcification reduction and recovery in native and non-native Mediterranean corals in response to ocean acidification. J Exp Mar Biol Ecol 438:144–153CrossRefGoogle Scholar
  69. Movilla J, Orejas C, Calvo E, Gori A, López-Sanz À, Grinyó J, Domínguez-Carrió C, Pelejero C (2014) Differential response of two Mediterranean cold-water coral species to ocean acidification. Coral Reefs 33:675–686CrossRefGoogle Scholar
  70. Muehllehner N, Edmunds PJ (2008) Effects of ocean acidification and increased temperature on skeletal growth of two scleractinian corals, Pocillopora meandrina and Porites rus. In: Proceedings of 11th international coral reef symposium, pp 7–11Google Scholar
  71. Palmiéri J, Orr JC, Dutay J-C, Béranger K, Schneider A, Beuvier J, Somot S (2014) Simulated anthropogenic CO2 uptake and acidification of the Mediterranean Sea. Biogeosci Discuss 11:6461–6517CrossRefGoogle Scholar
  72. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422CrossRefGoogle Scholar
  73. Parker L, Ross P, Connor W, Pörtner H, Scanes E, Wright J (2013) Predicting the response of molluscs to the impact of ocean acidification. Biology 2:651–692CrossRefGoogle Scholar
  74. Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspectives on ocean acidification. Trends Ecol Evol 25:332–344CrossRefGoogle Scholar
  75. Pelletier F, Clutton-Brock T, Pemberton J, Tuljapurkar S, Coulson T (2007) The evolutionary demography of ecological change: linking trait variation and population growth. Science 315:1571–1574CrossRefGoogle Scholar
  76. Perez FF, Fraga F (1987) A precise and rapid analytical procedure for alkalinity determination. Mar Chem 21:169–182CrossRefGoogle Scholar
  77. Perez FF, Rios AF, Rellán T, Alvarez M (2000) Improvements in a fast potentiometric seawater alkalinity determination. Cienc Mar 26:463–478Google Scholar
  78. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692CrossRefGoogle Scholar
  79. Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagès C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Change Biol 9:1660–1668CrossRefGoogle Scholar
  80. Reynaud S, Ferrier-Pagès 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 71:354–362CrossRefGoogle Scholar
  81. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  82. Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674CrossRefGoogle Scholar
  83. Rodolfo-Metalpa R, Richard C, Allemand D, Ferrier-Pagès C (2006) Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures. J Exp Biol 209:4546–4556CrossRefGoogle Scholar
  84. Rodolfo-Metalpa R, Reynaud C, Allemand D, Ferrier-Pagès C (2008) Temporal and depth responses of two temperate corals, Cladocora caespitosa and Oculina patagonica, from the North Mediterranean Sea. Mar Ecol Prog Ser 369:103–114CrossRefGoogle Scholar
  85. Rodolfo-Metalpa R, Martin S, Ferrier-Pagès 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. Biogeosciences 7:289–300CrossRefGoogle Scholar
  86. Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Change 1:308–312CrossRefGoogle Scholar
  87. Rodolfo-Metalpa R, Hoogenboom MO, Rottier C, Ramos-Esplá A, Baker AC, Fine M, Ferrier-Pagès C (2014) Thermally tolerant corals have limited capacity to acclimatize to future warming. Glob Change Biol 20:3036–3049CrossRefGoogle Scholar
  88. Rossi L (1971) Cnidari e Ctenofori d’Italia. Quaderni della Civica Stazione Idrobiologica di Milano 2:77–86Google Scholar
  89. Slattery M, McClintock JB, Heine J (1995) Chemical defenses in Antarctic soft corals: evidence for antifouling compounds. J Exp Mar Biol Ecol 190:61–77CrossRefGoogle Scholar
  90. Sokolov AP, Stone PH, Forest CE, Prinn RG, Sarofim MC, Webster M, Paltsev S, Schlosser CA, Kicklighter D, Dutkiewicz S, Reilly J, Wang C, Felzer B, Melillo J, Jacoby HD (2009) Probabilistic forecast for 21st century climate based on uncertainties in emissions (without policy) and climate parameters. J Clim 22:5175–5204CrossRefGoogle Scholar
  91. Solomon S, Qin D, Manning MR, Marquis M, Averyt K, Tignor MMB, Miller HLJ, Zhenlin C (2007) Climate change 2007: the physical science basis: Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge Univ Press, CambridgeGoogle Scholar
  92. Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté E, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Bio Ecol 408:58–78CrossRefGoogle Scholar
  93. Tambutté E, Venn AA, Holcomb M, Segonds N, Techer N, Zoccola D, Allemand D, Tambutté S (2015) Morphological plasticity of the coral skeleton under CO2-driven seawater acidification. Nat Commun. doi:10.1038/ncomms8368 Google Scholar
  94. Templado J (2014) Future trends of Mediterranean biodiversity. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea: its history and present challenges. Springer, London, pp 479–498CrossRefGoogle Scholar
  95. Touratier F, Goyet C (2011) Impact of the Eastern Mediterranean transient on the distribution of anthropogenic CO2 and first estimate of acidification for the Mediterranean Sea. Deep Sea Res I: Oceanogr Res Pap 58:1–15CrossRefGoogle Scholar
  96. Touratier F, Guglielmi V, Goyet C, Prieur L, Pujo-Pay M, Conan P, Falco C (2012) Distributions of the carbonate system properties, anthropogenic CO2, and acidification during the 2008 BOUM cruise (Mediterranean Sea). Biogeosci Discuss 9:2709–2753CrossRefGoogle Scholar
  97. Trenberth K (2012) Framing the way to relate climate extremes to climate change. Clim Change 115:283–290CrossRefGoogle Scholar
  98. Vargas-Yáñez M, Moya F, García-Martínez MC, Tel E, Zunino P, Plaza F, Salat J, Pascual J, López-Jurado JL, Serra M (2010) Climate change in the Western Mediterranean Sea 1900–2008. J Mar Syst 82:171–176CrossRefGoogle Scholar
  99. Venn AA, Tambutté E, 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:e20013CrossRefGoogle Scholar
  100. 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 USA 110:1634–1639CrossRefGoogle Scholar
  101. Weinberg S (1979) Autecology of shallow-water Octocorallia from Mediterranean rocky substrata, I. The Banyuls area. Bijdragen tot de Dierkunde 49:1–15Google Scholar
  102. Wicks L, Roberts JM (2012) Benthic invertebrates in a high-CO2 world. Oceanogr Mar Biol Annu Rev 50:127–188CrossRefGoogle Scholar
  103. Zibrowius H (1980) Les scléractiniaires de la Méditerranée et de l’Atlantique nord-oriental. Mem Inst Oceanogr 11:1–284Google Scholar
  104. Zibrowius H (1995) The ‘‘southern’’ Astroides calycularis in the Pleistocene of the northern Mediterranean—an indicator of climatic changes (Cnidaria, Scleractinia). Geobios 28:9–16CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Juancho Movilla
    • 1
  • Eva Calvo
    • 1
  • Rafel Coma
    • 2
  • Eduard Serrano
    • 2
  • Àngel López-Sanz
    • 1
  • Carles Pelejero
    • 1
    • 3
  1. 1.Institut de Ciències del Mar, CSICBarcelonaSpain
  2. 2.Centre d’Estudis Avançats de Blanes, CSICGironaSpain
  3. 3.Institució Catalana de Recerca i Estudis AvançatsBarcelonaSpain

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