Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 119–150

    Chapter  Google Scholar 

  • Anthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, energetics, and coral mortality risk: effects of temperature, light, and sediment regime. Limnol Oceanogr 52:716–726

    Article  Google Scholar 

  • 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 105:17442–17446

    Article  CAS  Google Scholar 

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol 44:123–195

    Google Scholar 

  • 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 13:2078–2088

    Article  Google Scholar 

  • 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 12:103–118

    Article  CAS  Google Scholar 

  • Bianchi CN (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580:7–21

    Article  Google Scholar 

  • 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) 58–59:181–197

    Google Scholar 

  • 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 19:1897–1908

    Article  CAS  Google Scholar 

  • Brewer PG, Peltzer ET (2009) Limits to marine life. Science 324:347

    Article  CAS  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • 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 86:139–150

    Article  Google Scholar 

  • Bucher D, Harriott VJ, Roberts LG (1998) Skeletal micro-density, porosity and bulk density of acroporid corals. J Exp Mar Biol Ecol 228:117–136

    Article  Google Scholar 

  • 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 49:1–42

    Google Scholar 

  • 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 50:1–29

    Article  Google Scholar 

  • 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 114:255–264

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 21:3671–3685

    Article  Google Scholar 

  • Casellato S, Masiero L, Sichirollo E, Soresi S (2007) Hidden secrets of the Northern Adriatic: Tegnuè, peculiar reefs. Cent Eur J Biol 2:122–136

    Google Scholar 

  • Cebrian E, Ballesteros E (2004) Zonation patterns of benthic communities in an upwelling area from the western Mediterranean (La Herradura, Alboran Sea). Sci Mar 68:69–84

    Article  Google Scholar 

  • Chevin LM, Lande R (2010) When do adaptive plasticity and genetic evolution prevent extinction of a density-regulated population? Evolution 64:1143–1150

    Article  Google Scholar 

  • 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 40:2115–2129

    Article  CAS  Google Scholar 

  • Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127

    Article  Google Scholar 

  • 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 

  • Coll M, Piroddi C, Steenbeek J et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE 5:e11842

    Article  CAS  Google Scholar 

  • Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215

    Article  Google Scholar 

  • Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol Oceanogr 47:324–331

    Article  Google Scholar 

  • Coma R, Ribes M, Gili JM, Zabala M (2002) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453

    Article  Google Scholar 

  • 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 327:51–60

    Article  Google Scholar 

  • 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 106:6176–6181

    Article  CAS  Google Scholar 

  • 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 14:529–538

    Article  Google Scholar 

  • Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

    Article  Google Scholar 

  • De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119

    Article  CAS  Google Scholar 

  • 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 34:1733–1743

    Article  CAS  Google Scholar 

  • Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172

    Article  CAS  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • 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 4:11–37

    Article  Google Scholar 

  • Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea, French Polynesia. Mar Biol 159:2149–2160

    Article  CAS  Google Scholar 

  • 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 1:165–169

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811

    Article  CAS  Google Scholar 

  • 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 17:126–127

    Google Scholar 

  • 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 15:1090–1103

    Article  Google Scholar 

  • Gattuso JP, Hansson L (2011) Ocean acidification: background and history. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 1–20

    Google Scholar 

  • 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 39:160–183

    CAS  Google Scholar 

  • 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 148:923–932

    Article  Google Scholar 

  • 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 152:351–361

    Article  Google Scholar 

  • 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 84:599–602

    Article  Google Scholar 

  • Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann NY Acad Sci 1134:320–342

    Article  CAS  Google Scholar 

  • 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 119:5815–5836

    Article  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 386:27–33

    Article  Google Scholar 

  • 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 9:29–39

    Article  CAS  Google Scholar 

  • 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 4:5207

    Article  CAS  Google Scholar 

  • Ip YK, Lim ALL, Lim RWL (1991) Some properties of calcium-activated adenosine triphosphatase from the hermatypic coral Galaxea fascicularis. Mar Biol 1991:191–197

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • 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 529–541

    Google Scholar 

  • 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 10:2169–2219

    Article  CAS  Google Scholar 

  • 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 19:1884–1896

    Article  Google Scholar 

  • 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 69:345–353

    Article  Google Scholar 

  • 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 171:131–137

    Article  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McCulloch MT, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change 2:623–627

    Article  CAS  Google Scholar 

  • 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 18:897–907

    Article  CAS  Google Scholar 

  • 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 438:144–153

    Article  CAS  Google Scholar 

  • 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 33:675–686

    Article  Google Scholar 

  • 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 7–11

  • 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 11:6461–6517

    Article  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  Google Scholar 

  • 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 2:651–692

    Article  CAS  Google Scholar 

  • Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspectives on ocean acidification. Trends Ecol Evol 25:332–344

    Article  Google Scholar 

  • 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 315:1571–1574

    Article  CAS  Google Scholar 

  • Perez FF, Fraga F (1987) A precise and rapid analytical procedure for alkalinity determination. Mar Chem 21:169–182

    Article  CAS  Google Scholar 

  • Perez FF, Rios AF, Rellán T, Alvarez M (2000) Improvements in a fast potentiometric seawater alkalinity determination. Cienc Mar 26:463–478

    CAS  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692

    Article  Google Scholar 

  • 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 9:1660–1668

    Article  Google Scholar 

  • 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 71:354–362

    Article  CAS  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 209:4546–4556

    Article  Google Scholar 

  • 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 369:103–114

    Article  Google Scholar 

  • 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 7:289–300

    Article  CAS  Google Scholar 

  • 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 1:308–312

    Article  CAS  Google Scholar 

  • 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 20:3036–3049

    Article  Google Scholar 

  • Rossi L (1971) Cnidari e Ctenofori d’Italia. Quaderni della Civica Stazione Idrobiologica di Milano 2:77–86

    Google Scholar 

  • Slattery M, McClintock JB, Heine J (1995) Chemical defenses in Antarctic soft corals: evidence for antifouling compounds. J Exp Mar Biol Ecol 190:61–77

    Article  CAS  Google Scholar 

  • 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 22:5175–5204

    Article  Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • 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 408:58–78

    Article  Google Scholar 

  • 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 

  • 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 479–498

    Chapter  Google Scholar 

  • 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 58:1–15

    Article  CAS  Google Scholar 

  • 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 9:2709–2753

    Article  Google Scholar 

  • Trenberth K (2012) Framing the way to relate climate extremes to climate change. Clim Change 115:283–290

    Article  Google Scholar 

  • 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 82:171–176

    Article  Google Scholar 

  • 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:e20013

    Article  CAS  Google Scholar 

  • 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 110:1634–1639

    Article  CAS  Google Scholar 

  • Weinberg S (1979) Autecology of shallow-water Octocorallia from Mediterranean rocky substrata, I. The Banyuls area. Bijdragen tot de Dierkunde 49:1–15

    Google Scholar 

  • Wicks L, Roberts JM (2012) Benthic invertebrates in a high-CO2 world. Oceanogr Mar Biol Annu Rev 50:127–188

    Article  Google Scholar 

  • Zibrowius H (1980) Les scléractiniaires de la Méditerranée et de l’Atlantique nord-oriental. Mem Inst Oceanogr 11:1–284

    Google Scholar 

  • Zibrowius H (1995) The ‘‘southern’’ Astroides calycularis in the Pleistocene of the northern Mediterranean—an indicator of climatic changes (Cnidaria, Scleractinia). Geobios 28:9–16

    Article  Google Scholar 

Download references

Acknowledgments

Thanks are due to A. Olariaga (ICM) for technical help in the aquaria design and to M. Delgado (ZAE staff at the ICM) for technical assistance. The authors are also grateful to R. Sherrell and A. Williams for their insightful comments and help with the English. This work was supported by projects CTM2012-32017, CGL2013-43106-R and a FPI fellowship (BES-2007-16537) to JM from the Spanish Government. This is a contribution from the Marine Biogeochemistry and Global Change research group (Grant 2014SGR1029, Generalitat de Catalunya).

Author information

Authors and Affiliations

  1. Institut de Ciències del Mar, CSIC, Passeig Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain

    Juancho Movilla, Eva Calvo, Àngel López-Sanz & Carles Pelejero

  2. Centre d’Estudis Avançats de Blanes, CSIC, Accés Cala Sant Francesc 14, Blanes, 17300, Girona, Spain

    Rafel Coma & Eduard Serrano

  3. Institució Catalana de Recerca i Estudis Avançats, 08010, Barcelona, Spain

    Carles Pelejero

Authors
  1. Juancho Movilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Calvo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafel Coma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eduard Serrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Àngel López-Sanz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carles Pelejero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juancho Movilla.

Additional information

Responsible Editor: D. Gochfeld.

Reviewed by Undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Movilla, J., Calvo, E., Coma, R. et al. Annual response of two Mediterranean azooxanthellate temperate corals to low-pH and high-temperature conditions. Mar Biol 163, 135 (2016). https://doi.org/10.1007/s00227-016-2908-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2908-9

Keywords

Search

Navigation