Estuaries and Coasts

, Volume 38, Issue 6, pp 1986–1999 | Cite as

Extreme pH Conditions at a Natural CO2 Vent System (Italy) Affect Growth, and Survival of Juvenile Pen Shells (Pinna nobilis)

  • Lorena Basso
  • Iris E. Hendriks
  • Alejandro B. Rodríguez-Navarro
  • Maria C. Gambi
  • Carlos M. Duarte


Predicted pH decreases in ocean surface waters of ~0.3–0.5 and 0.7–0.8 pH units (for 2100 and 2300, respectively) are expected to negatively affect calcification processes and physiological performances of many marine organisms. Here we evaluated the response of important parameters such as growth, mortality, oxygen consumption, and mineralization of transplanted Pinna nobilis juveniles in the naturally acidified waters of a CO2 vent system. Our field experiments show a general decrease of physiological responses of juveniles for the studied parameters along a decreasing pH gradient, even if significant effects are only observed under pH values of 7.6 units (“extreme” pH). In particular, the mortality rate increased from 10–30 % over the study period at control conditions to 60–70 % at extreme pH values. We conclude that near-future decreases in pH (decreases of 0.3–0.5 pH units) may not have a significant effect on performance of P. nobilis juveniles, while predicted longer-term decreases (decreases of 0.7–0.8 pH units) could affect the survival of the species. The combination of laboratory experiments with the assessment of naturally acidified environments can provide further insights into the threshold pH affecting the performance of vulnerable marine species.


Pinna nobilis Ocean acidification Volcanic CO2 vents Bivalve Mineralization Growth 



This research was supported by the MedSeA project (, contract number 265103 of the Framework Program 7 of the European Union), and ESTRESX (ref. CTM2012-32603), funded by the Spanish Ministry of Economy and Competitiveness. L.B. was supported by JAE pre-DOC fellowship and I.E.H. by a JAE-DOC fellowship (CSIC, Spain). We thank the staff of the Benthic Ecology research unit (Villa Dorhn, Ischia) for advice and technical support. We particularly thank Captain Vincenzo Rando for his outstanding support with all boat operations and Asier Rodriguez for his help with analysis of the data.


  1. Addadi, L., and S. Weiner. 1992. Control and design principles in biological mineralization. Angewandte Chemie Int. Ed 31(2): 153–169.CrossRefGoogle Scholar
  2. Andersen, S., E.S. Grefsrud, and T. Harboe. 2013. Effect of increased pCO2 on early shell development in great scallop (Pecten maximus Lamark) larvae. Biogeosciences Discussions 10: 3281–3310.CrossRefGoogle Scholar
  3. Andersson, A.J., F.T. Mackenzie, and J.-P. Gattuso. 2011. Effects of ocean acidification on benthic processes, organisms, and ecosystems. In Ocean acidification, ed. J.-P. Gattuso and L. Hansson, 122–153. Oxford: Oxford University Press.Google Scholar
  4. Anthony, K.R.N., D.I. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America 105: 17442–17446.CrossRefGoogle Scholar
  5. Aufdenkampe, A.K., E. Mayorga, P.A. Raymond, J.M. Melack, S.C. Doney, S.R. Alin, R.E. Aalto, and K. Yoo. 2011. Riverine coupling of biogeochemical cycles between land, oceans, and atmosphere. Frontiers in Ecology and the Environment 9(1): 53e60.CrossRefGoogle Scholar
  6. Bosc, E., A Bricaud, D. Antoine. 2004. Seasonal and interannual variability in algal biomass and primary productionin the Mediterranean Sea, as derived from 4 years of Sea- WiFS observations. Global Biogeochemical Cy.18. GB1005. doi: 10.1029/2003GB002034.
  7. Brennand, H.S., N. Soars, S.A. Dworjanyn, A.R. Davis, and M. Byrne. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5: 7.Google Scholar
  8. Bressan, M., A. Chinellato, M. Munari, V. Matozzo, A. Manci, T. Marčeta, L. Finos, I. Moro, P. Pastore, D. Badocco, and M.G. Marin. 2014. Marine Environmental Research 99: 136–14.CrossRefGoogle Scholar
  9. Broecker, W.S., and T. Takahash. 1966. Calcium carbonate precipitation on bahama banks. Journal of Geophysical Research 71: 1575–1602.CrossRefGoogle Scholar
  10. Buapet, P., M. Gullström, and M. Björk. 2013. Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment. Marine and Freshwater Research 64: 1040–1048. doi: 10.1071/MF12124.
  11. Cabanellas-Reboredo, M., S. Deudero, J. Alos, J.M. Valencia, D. March, I.E. Hendriks, and E. Alvarez. 2009. Recruitment of Pinna nobilis (Mollusca: Bivalvia) on artificial structures. Marine Biodiversity Records. Marine Biological Association of the United Kingdom 2: 1–5.Google Scholar
  12. Caldeira, K., and M.E. Wickett. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research 110: C09S04.CrossRefGoogle Scholar
  13. Calosi, P., S.P.S. Rastrick, M. Graziano, S.C. Thomas, C. Baggini, H.A. Carter, J.M. Hall-Spencer, M. Milazzo, and J.I. Spicer. 2013. Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid–base and ion-regulatory abilities. Marine Pollution Bulletin 73: 470–484.CrossRefGoogle Scholar
  14. Carritt, D.E., and J.H. Carpenter. 1966. Comparison and evaluation of currently employed modifications of Winkler method for determining dissolved oxygen in seawater - a nasco report. Journal of Marine Research 24: 286–318.Google Scholar
  15. Centoducati, G., E. Tarsitano, A. Bottalico, M. Marvulli, O.R. Lai, and G. Crescenzo. 2007. Monitoring of the endangered Pinna nobilis Linnaeus, 1758 in the Mar Grande of Taranto (Ionian sea, Italy). Environmental Monitoring and Assessment 131: 339–347.CrossRefGoogle Scholar
  16. Chiarore, A., and F.P. Patti. 2013. Molluschi associati all’alga bruna Sargassum vulgare (C. Agardh, 1820) (Fucales Sargassaceae) rinvenuti lungo le coste dell’isola d’Ischia (Napoli): check-list preliminare. Notiziario SIM 31(2): 10–11.Google Scholar
  17. Cigliano, M., M.C. Gambi, R. Rodolfo-Metalpa, F.P. Patti, and J.M. Hall-Spencer. 2010. Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Marine Biology 157: 2489–2502.CrossRefGoogle Scholar
  18. Comeau, S., G. Gorsky, R. Jeffree, J.L. Teyssie, and J.P. Gattuso. 2009. Impact of ocean acidification on a key Arctic pelagic mollusc (Limacina helicina). Biogeosciences 6: 1877.CrossRefGoogle Scholar
  19. Crook, E.D., D. Potts, M. Rebolledo-Vieyra, L. Hernandez, and A. Paytan. 2012. Calcifying coral abundance near low-pH springs: implications for future ocean acidification. Coral Reefs 31: 239–245.CrossRefGoogle Scholar
  20. Cummings, V., J. Hewitt, A. Van Rooyen, K. Currie, S. Beard, S. Thrush, J. Norkko, N. Barr, P. Heath, N.J. Halliday, R. Sedcole, A. Gomez, C. McGraw, and V. Metcalf. 2011. Ocean acidification at high latitudes: potential effects on functioning of the antarctic bivalve Laternula elliptica. PLoS ONE 6: e16069.CrossRefGoogle Scholar
  21. De Bodt, C., N. Van Oostende, J. Harlay, K. Sabbe, and L. Chou. 2010. Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7: 1401–1412.CrossRefGoogle Scholar
  22. Dickson, A.G. 1990. Standard potential of the reaction - AgCl(S) + 1/2H2(g) = AG(S) + HCL(aq) and the standard acidity constant of the ion HSO4− in synthetic sea-water from 273.15 K to 318.15 K. Journal of Chemical Thermodynamics 22: 113–127.CrossRefGoogle Scholar
  23. Dickson, A.G., and F.J. Millero. 1987. Comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media. Deep Sea Res 34: 1733–1743.CrossRefGoogle Scholar
  24. Dickson, A.G., C.L. Sabine, and J.R. Christian. 2007. Guide to the best practices for ocean CO2 measurements. PICES Special Publication 3: 191.Google Scholar
  25. Donnarumma, L., C. Lombardi, S. Cocito, and M.C. Gambi. 2014. Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Mediterranean Marine Science 15: 498–509.Google Scholar
  26. Duarte, C.M., I.E. Hendriks, T.S. Moore, Y.S. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J.A. Trotter, and M. McCulloch. 2013. Is ocean acidification an open- ocean syndrome? Understanding anthropogenic impacts on Marine pH. Estuaries and Coast 36(2): 221e236. doi: 10.1007/s12237-013-9594-3.CrossRefGoogle Scholar
  27. Edmunds, P.J., D. Brown, and B. Moriarty. 2012. Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea French Polynesia. Global Change Biology 18: 2173–2183.CrossRefGoogle Scholar
  28. EEC, 1992. Council directive on the conservation of natural habitats and of wild fauna and flora (the habitats and species directive), ed. EEC. Official Journal of the European Communities.Google Scholar
  29. Fabricius, K.E., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. De’ath, R. Okazaki, N. Muehllehner, M.S. Glas, and J.M. Lough. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change 1(3): 165–169.CrossRefGoogle Scholar
  30. Falini, G., G. Sartor, D. Fabbri, P. Vergni, S. Fermani, A.M. Belcher, G.D. Stucky, and D.E. Morse. 2011. The interstitial crystal-nucleating sheet in molluscan Haliotis rufescens shell: a bio-polymeric composite. Journal of Structural Biology 173: 128–137.CrossRefGoogle Scholar
  31. Feely, R.A., C.L. Sabine, K. Lee, W. Berelson, J. Kleypas, V.J. Fabry, and F.J. Millero. 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305: 362–366.CrossRefGoogle Scholar
  32. Fernandez-Reiriz, M.J., P. Range, X.A. Alvarez-Salgado, J. Espinosa, and U. Labarta. 2012. Tolerance of juvenile Mytilus galloprovincialis to experimental seawater acidification. Marine Ecology Progress Series 454: 65–74.CrossRefGoogle Scholar
  33. Findlay, H.S., H.L. Wood, M.A. Kendall, J.I. Spicer, R.J. Twitchett, and S. Widdicombe. 2009. Calcification, a physiological process to be considered in the context of the whole organism. Biogeosciences Discussion 6: 2267–2284.CrossRefGoogle Scholar
  34. Garcia-March, J.R. 2003. Contribution to the knowledge of the status of Pinna nobilis (L.) 1758 in Spanish coasts. Memories de l’institut océanographique Paul Ricard 9: 29–41.Google Scholar
  35. Gazeau, F., C. Quiblier, J.M. Jansen, J.-P. Gattuso, J.J. Middelburg, and C.H.R. Heip. 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34, L07603.CrossRefGoogle Scholar
  36. Gazeau, F., L.M. Parker, S. Comeau, J.-P. Gattuso, W.A. O’ Connor, S. Martin, H.-O. Pörtner, and P.M. Ross. 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology 160: 2207–2245.CrossRefGoogle Scholar
  37. Gieskes, J.M. 1969. Effect of temperature on the pH of sea water. Limnology and Oceanography 14: 679–685.CrossRefGoogle Scholar
  38. Ginger, K.W.K., C.B.S. Vera, R. Dineshram, C.K.S. Dennis, L.J. Adela, Z. Yu, and V. Thiyagarajan. 2013. Larval and post-larval stages of Pacific oyster (Crassostrea gigas) are resistant to elevated CO2. PLoS ONE 8: e64147.CrossRefGoogle Scholar
  39. Hahn, S., R. Rodolfo-Metalpa, E. Griesshaber, W.W. Schmahl, D. Buhl, J.M. Hall-Spencer, C. Baggini, K.T. Fehr, and A. Immenhauser. 2012. Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: environmental effect versus experimental bias. Biogeosciences 9: 1897–1914. doi: 10.5194/bg-9-1897-2012.CrossRefGoogle Scholar
  40. Hall-Spencer, J.M., R. Rodolfo-Metalpa, S. Martin, E. Ransome, M. Fine, S.M. Turner, S.J. Rowley, D. Tedesco, and M.-C. Buia. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96–99.CrossRefGoogle Scholar
  41. Havenhand, J.N., and P. Schlegel. 2009. Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences 6: 3009–3015.CrossRefGoogle Scholar
  42. Heinemann, A. 2011. The suitability of Mytilus edulis as proxy archive and its response to ocean acidification. Doctoral thesis, Christian-Albrechts-Universität, Kiel, GermanyGoogle Scholar
  43. Hendriks, I.E., C.M. Duarte, and M. Alvarez. 2010. Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal and Shelf Science 86: 157–164.CrossRefGoogle Scholar
  44. Hendriks, I.E., L. Basso, S. Deudero, M. Cabanellas-Reboredo, and E. Alvarez. 2012. Relative growth rates of the noble pen shell Pinna nobilis throughout ontogeny around the Balearic Islands (Western Mediterranean, Spain). Journal of Shellfish Research 31: 749–756.CrossRefGoogle Scholar
  45. Hendriks, I.E., C.M. Duarte, Y.S. Olsen, A. Steckbauer, L. Ramajo, T.S. Moore, J.A. Trotter, and M. McCulloch. 2015. Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems. Estuarine, Coastal and Shelf Science 152: A1-A8. doi: 10.1016/j.ecss.2014.07.019.
  46. Hendriks, I.E., Y.S. Olsen, L. Ramajo, L. Basso, A. Steckbauer, T.S. Moore, J. Howard, and C.M. Duarte. 2014. Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11: 333–346.CrossRefGoogle Scholar
  47. Hoegh-Guldberg, O., P.J. Mumby, A.J. Hooten, R.S. Steneck, P. Greenfield, E. Gomez, C.D. Harvell, P.F. Sale, A.J. Edwards, K. Caldeira, N. Knowlton, C.M. Eakin, R. Iglesias-Prieto, N. Muthiga, R.H. Bradbury, A. Dubi, and M.E. Hatziolos. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318: 1737.CrossRefGoogle Scholar
  48. Hofmann, G.E., J.E. Smith, K.S. Johnson, U. Send, L.A. Levin, F. Micheli, A. Paytan, N.N. Price, B. Peterson, Y. Takeshita, P.G. Matson, E.D. Crook, K.J. Kroeker, M.C. Gambi, E.B. Rivest, C.A. Frieder, P.C. Yu, and T.R. Martz. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 6(12): e28983.CrossRefGoogle Scholar
  49. Hubbard, F., J. McManus and M. Al-Dabbas. 1981. Environmental influences on the shell mineralogy of Mytilus edulisGeo Marine Letter 1: 267–269.Google Scholar
  50. IPCC. 2013. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. T.F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P.M. Midgley. Cambridge: Cambridge University Press. doi: 10.1017/CBO9781107415324. 1535 pp.Google Scholar
  51. Joint, I., S.C. Doney, and D.M. Karl. 2011. Will ocean acidification affect marine microbes? The ISME Journal 5: 1–7.CrossRefGoogle Scholar
  52. Jokiel, P.L., J.E. Maragos, and L. Franzisket. 1978. Coral growth: buoyant weight technique. In Coral reefs: research methods, ed. D.R. Stoddart and R.E. Johannes, 529–542. Paris: UNESCO monographs on oceanographic methodology.Google Scholar
  53. Kamenos, N.A., P. Calosi, and P.G. Moore. 2006. Substratummediated heart rate responses of an invertebrate to predation threat. Animal Behaviour 71: 809–813.CrossRefGoogle Scholar
  54. Katsanevakis, S. 2007. Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): A generalized additive modelling approach. Marine Biology 152: 1319–1331.CrossRefGoogle Scholar
  55. Katsanevakis, S. 2009. Population dynamics of the endangered fan mussel Pinna nobilis in a marine lake: a metapopulation matrix modeling approach. Marine Biology 156: 1715–1732.CrossRefGoogle Scholar
  56. Kleypas, J.A., R.A. Feely, V.J. Fabry, C. Langdon, C.L. Sabine, and L.L. Robbins. 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 the U.S. Geological Survey.Google Scholar
  57. Kroeker, K.J., R.L. Kordas, R.N. Crim, and G.G. Singh. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13: 1419–1434.CrossRefGoogle Scholar
  58. Kroeker, K.J., F. Micheli, M.C. Gambi, and T.R. Martz. 2011. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proceedings of the National Academy of Sciences 108: 14515–14520. doi: 10.1073/pnas.1107789108.CrossRefGoogle Scholar
  59. Kroeker, K.J., R.L. Kordas, R. Crim, I.E. Hendriks, L. Ramajo, G.S. Singh, C.M. Duarte, and J.-P. Gattuso. 2013a. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896.CrossRefGoogle Scholar
  60. Kroeker, K.J., F. Micheli, and M.C. Gambi. 2013b. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nature Climate Change 3: 156–159.CrossRefGoogle Scholar
  61. Krom, M.D., B. Herut, and R.F.C. Mantoura. 2004. Nutrient budget for the eastern Mediterranean: implications for phosphorus limitation. Limnology Oceanography 49(5): 1582–1592.CrossRefGoogle Scholar
  62. Kurihara, H. 2008. Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series 373: 275–284.CrossRefGoogle Scholar
  63. Labasque, T. 2004. Spectrophotometric Winkler determination of dissolved oxygen: re-examination of critical factors and reliability. Marine Chemistry 88: 53–60.CrossRefGoogle Scholar
  64. Lannig, G., S. Eilers, H.O. Pörtner, I.M. Sokolova, and C. Bock. 2010. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas-changes in metabolic pathways and thermal response. Marine Drugs 8: 2318–2339.CrossRefGoogle Scholar
  65. Liu, W., and M. He. 2012. Effects of ocean acidification on the metabolic rates of three species of bivalve from southern coast of China. Chinese Journal Oceanololy and Limnology 30: 206–211.CrossRefGoogle Scholar
  66. Lombardi, C., M.C. Gambi, C. Vasapollo, P.D. Taylor, and S. Cocito. 2011a. Skeletal alteration and polymorphism in a Mediterranean bryozoan at natural CO2 vents. Zoomorphology 130: 135–145. doi: 10.1007/s00435-001-0127-y.CrossRefGoogle Scholar
  67. Lombardi, C., R. Rodolfo-Metalpa, S. Cocito, M.C. Gambi, and P.D. Taylor. 2011b. Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification. Marine Ecology 32(2): 211–221. doi: 10.1111/j.1439-0485.2010.00426.x.CrossRefGoogle Scholar
  68. Manzello, D.P., J.A. Kleypas, D.A. Budd, C.M. Eakin, P.W. Glynn, and C. Langdon. 2008. Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. Proceedings of the National Academy of Sciences 105: 10450–10455.CrossRefGoogle Scholar
  69. Mehrbach, C., C.H. Culberso, J.E. Hawley, and R.M. Pytkowic. 1973. Measurement of apparent dissociation-constants of carbonic-acid in seawater at atmospheric-pressure. Limnology and Oceanography 18: 897–907.CrossRefGoogle Scholar
  70. Melzner, F., S. Goebel, M. Langenbuch, M.A. Gutowska, H.-O. Pöertner, and M. Lucassen. 2009. Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater pCO2. Aquatic Toxicology 92: 30–37.CrossRefGoogle Scholar
  71. Melzner, F., P. Stange, K. Trübenbach, J. Thomsen, I. Casties, U. Panknin, S.N. Gorb, and M.A. Gutowska. 2011. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS ONE 6: e24223.CrossRefGoogle Scholar
  72. Michaelidis, B., C. Ouzounis, A. Paleras, and H.O. Pörtner. 2005. Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293: 109–118.CrossRefGoogle Scholar
  73. Miles, H., S. Widdicombe, J.I. Spicer, and J. Hall-Spencer. 2007. Effects of anthropogenic seawater acidification on acid–base balance in the sea urchin Psammechinus miliaris. Marine Pollution Bulletin 54: 89–96.CrossRefGoogle Scholar
  74. Miller, A.W., A.C. Reynolds, C. Sobrino, and F.G. Riedel. 2009. Shellfish face uncertain future in high CO2 world: influence of acidification on oyster larvae calcification and growth in estuaries. PLoS ONE 4: e5661.CrossRefGoogle Scholar
  75. Moy, A.D., W.R. Howard, S.G. Bray, and T.W. Trull. 2009. Reduced calcification in modern Southern Ocean planktonic Foraminifera. Nature Geoscience 2: 276–280.CrossRefGoogle Scholar
  76. Navarro, J.M., R. Torres, K. Acura, C. Duarte, P.H. Manriquez, M. Lardies, N.A. Lagos, C. Vargas, and V. Aguilera. 2013. Impact of medium-term exposure to elevated pCO2 levels on the physiological energetics of the mussel Mytilus chilensis. Chemosphere 90: 1242–1248.CrossRefGoogle Scholar
  77. Nienhuis, S., A.R. Palmer, and C.D.G. Harley. 2010. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proceedings of the Royal Society B: Biological Sciences 277: 2553–2558.CrossRefGoogle Scholar
  78. Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, R.M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfray, A. Mouchet, R.G. Najjar, G.K. Plattner, K.B. Rodgers, C.L. Sabine, J.L. Sarmiento, R. Schlitzer, R.D. Slater, I.J. Totterdell, M.F. Weirig, Y. Yamanaka, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.CrossRefGoogle Scholar
  79. Parker, L.M., P.M. Ross, W.A. O’Connor, L. Borysko, D.A. Raftos, and H.O. Pörtner. 2012. Adult exposure influences offspring response to ocean acidification in oysters. Global Change Biology 18: 82–92.CrossRefGoogle Scholar
  80. Pierrot, D., E. Lewis, and D.W.R. Wallace. 2006. MS Excel Program Developed for CO 2 System Calculations. ORNL/CDIAC-105a. Oak Ridge, Tennessee: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.Google Scholar
  81. Pörtner, H.O. 2008. Ecosystem effects of ocean acidification in times of ocean warming: A physiologist’s view. Marine Ecology Progress Series 373: 203–217.CrossRefGoogle Scholar
  82. Pörtner, H.O., M. Langenbuch, and A. Reipschläger. 2004. Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. Journal Oceanography 60: 705–718.CrossRefGoogle Scholar
  83. Rabaoui, L., S.T. Zouari, and O.K. Ben Hassine. 2008. Two species of Crustacea (Decapoda) associated with the fan mussel, Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia). Crustaceana 81: 433–446.CrossRefGoogle Scholar
  84. Range, P., M.A. Chicharo, R. Ben-Hamadou, D. Piló, D. Matias, S. Joaquim, A.P. Oliveira, and L. Chicharo. 2011. Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: variable responses to ocean acidification at local scales? Journal Experimental Marine Biology and Ecology 396: 177–184.CrossRefGoogle Scholar
  85. Raven, J., K. Caldeira, H. Elderfield, O. Hoegh-Guldberg, P. Liss, U. Riebesell, J. Shepherd, C. Turley, and A. Watson. 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/5Google Scholar
  86. Ricevuto, E., M. Lorenti, F.P. Patti, M.B. Scipione, and M.C. Gambi. 2012. Temporal trends of benthic invertebrate settlement along a gradient of ocean acidification at natural CO2 vents (Tyrrhenian Sea). Biologia Marina Mediterrana 19(1): 49–52.Google Scholar
  87. Richardson, C.A., M. Peharda, H. Kennedy, P. Kennedy, and V. Onofri. 2004. Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determined from Mg:Ca and Sr:Ca shell profiles. Journal of Experimental Marine Biology and Ecology 299: 1–16.CrossRefGoogle Scholar
  88. Ries, J.B. 2011. Skeletal mineralogy in a high-CO2 world. Journal of Experimental Marine Biology and Ecology 403: 54–64.CrossRefGoogle Scholar
  89. Ries, J.B., A.L. Cohen, and D.C. McCorkle. 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: 1131–1134.CrossRefGoogle Scholar
  90. Rodolfo-Metalpa, R., F. Houlbreque, E. Tambutte, F. Boisson, C. Baggini, F.P. Patti, R. Jeffree, M. Fine, A. Foggo, J.P. Gattuso, and J.M. Hall-Spencer. 2011. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1: 308–312.CrossRefGoogle Scholar
  91. Rodriguez-Navarro, A.B... 2006. XRD2D Scan a new software for polycrystalline materials characterization using two-dimensional X-ray diffraction. Journal of Applied Crystallography 39: 905–909.CrossRefGoogle Scholar
  92. Rodríguez-Navarro, A.B..., N. Dominguez-Gasca, A. Munoz, and M. Ortega-Huertas. 2013. Change in the chicken eggshell cuticle with hen age and egg freshness. Poultry Science 92(11): 3026–3035.CrossRefGoogle Scholar
  93. Sanders, M.B., T.P. Bean, T.H. Hutchinson, and W.J.F. Le Quesne. 2013. Juvenile king scallop, Pecten maximus, is potentially tolerant to low levels of ocean acidification when food is unrestricted. PLoS ONE 8: e74118.CrossRefGoogle Scholar
  94. Siletic, T., and M. Peharda. 2003. Population study of the fan shell Pinna nobilis L. in Malo and Veliko Jezero of the Mljet National park (Adriatic Sea). Scientia Marina 67: 91–98.CrossRefGoogle Scholar
  95. Silverman, J., B. Lazar, L. Cao, K. Caldeira, and J. Erez. 2009. Coral reefs may start dissolving when atmospheric CO2 doubles. Geophysical Research Letters 36, L05606.CrossRefGoogle Scholar
  96. Thomsen, J., and F. Melzner. 2010. Moderate seawater acidification does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Marine Biology 157: 2667–2676.CrossRefGoogle Scholar
  97. Thomsen, J., M.A. Gutowska, J. Saphoerster, A. Heinemann, K. Truebenbach, J. Fietzke, C. Hiebenthal, A. Eisenhauer, A. Koertzinger, M. Wahl, and F. Melzner. 2010. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7: 3879–3891.CrossRefGoogle Scholar
  98. Thomsen, J., I. Casties, C. Pansch, A. Körtzinger, and F. Melzner. 2013. Food availability outweighs ocean acidification effects in juvenile. Mytilus edulis: laboratory and field experiments. Global Change Biology 19(4): 1017–1027. doi: 10.1111/gcb.12109.CrossRefGoogle Scholar
  99. Tunnicliffe, V., K.T.A. Davies, D.A. Butterfield, R.W. Embley, J.M. Rose, and W.W. Chadwick Jr. 2009. Survival of mussels in extremely acidic waters on a submarine volcano. Nature Geoscience 2: 344–348. doi: 10.1038/NGEO500.CrossRefGoogle Scholar
  100. Widdicombe, S., and J.I. Spicer. 2008. Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? Journal of Experimental Marine Biology and Ecology 366: 187–197.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2015

Authors and Affiliations

  • Lorena Basso
    • 1
  • Iris E. Hendriks
    • 1
  • Alejandro B. Rodríguez-Navarro
    • 2
  • Maria C. Gambi
    • 3
  • Carlos M. Duarte
    • 1
    • 4
  1. 1.Global Change DepartmentIMEDEA, Instituto Mediterráneo de Estudios AvanzadosEsporlesSpain
  2. 2.Department of Mineralogy and Petrology, Faculty of ScienceUniversity of GranadaGranadaSpain
  3. 3.Functional and Evolutionary Ecology LaboratoryStazione Zoologica Anton DohrnNaplesItaly
  4. 4.The UWA Oceans Institute and School of Plant BiologyUniversity of Western AustraliaCrawleyAustralia

Personalised recommendations