Estuaries and Coasts

, Volume 38, Issue 6, pp 1976–1985 | Cite as

Juvenile Pen Shells (Pinna nobilis) Tolerate Acidification but Are Vulnerable to Warming

  • Lorena Basso
  • Iris E. Hendriks
  • Carlos M. Duarte


In the course of this century, rising anthropogenic CO2 emissions will likely cause a decrease in ocean pH, know as ocean acidification, together with an increase of water temperature. Only in the last years, studies have focused on synergetic effects of both stressors on marine invertebrates, particularly on early life stages considered more vulnerable. Disparate responses of their singular and combined effects were reported, highlighting the importance of extending the studies to different species and populations of marine invertebrates. Here, we observed the response of important parameters such as growth, mortality and oxygen consumption of juvenile pen shell Pinna nobilis at supplied pCO2 gas levels of 400 ppm (ambient) and 1000 ppm and at three temperatures (20, 23 and 26 °C) during 36 days. To our knowledge, this is the first study on ocean acidification and temperature effects on juveniles of this species. We show that the two stressors play roles at distinct levels, with pCO2 influencing growth and partially mortality, and temperature increasing mortality rates and oxygen consumption strongly. Therefore, juveniles of P. nobilis are more likely affected by increasing temperature than the pCO2 levels expected by the end of the twenty-first century.


Ocean acidification Warming Growth Metabolism rate Survival Pinna nobilis 



This is a contribution to projects MEDEICG funded by the Spanish Ministry of Economy and Competitiveness (CTM2009-07013), and MedSEA of the FP7 of the EU (contract # FP7-ENV-2010-265103). IEH received funding from the JAE-Doc program “Junta para la Ampliación de Estudios” of CSIC, co-financed by the European Social Fund (ESF). LB was funded by a JAE pre-DOC fellowship from the Spanish Government. We thank the Palma Aquarium for making its structures available to support the laboratory work and colleagues of Department of Global Change, in particular Inés Mazarrasa, Laura Ramajo, Alice Chaplin and Asier Rodriguez, for their help.

Supplementary material

12237_2015_9948_MOESM1_ESM.doc (37 kb)
ESM 1 (DOC 35 kb)


  1. Andersen, S., E.S. Grefsrud, and T. Harboe. 2013. Effect of increased pCO(2) level on early shell development in great scallop (Pecten maximus Lamarck) larvae. Biogeosciences 10: 6161–6184.CrossRefGoogle Scholar
  2. 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
  3. Basso, L., I.E. Hendriks, A.B. Rodríguez-Navarro, C.M. Gambi, and C.M. Duarte. 2015. Extreme pH conditions at a natural CO2 vent system (Italy). Affect growth, and survival of juvenile pen shells (Pinna nobilis). Estuaries and Coasts. doi: 10.1007/s12237-014-9936-9.
  4. Bechmann, R.K., I.C. Taban, S. Westerlund, B.F. Godal, M. Arnberg, S. Vingen, A. Ingvarsdottir, and T. Baussant. 2011. Effects of ocean acidification on early life stages of shrimp (Pandalus borealis) and mussel (Mytilus edulis). Journal of Toxicology and Environmental Health-Part a-Current Issues 74: 424–438.CrossRefGoogle Scholar
  5. Beesley, A., D.M. Lowe, C.K. Pascoe, and S. Widdicombe. 2008. Effects of CO2-induced seawater acidification on the health of Mytilus edulis. Climate Research 37: 215–225.CrossRefGoogle Scholar
  6. Berge, J.A., B. Bjerkeng, O. Pettersen, M.T. Schaanning, and S. Øxnevad. 2006. Effects of CO2-induced seawater acidification on the health of Mytilus edulis. Climate Research 37: 215–225.Google Scholar
  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. Broecker, W.S., and T. Takahash. 1966. Calcium carbonate precipitation on Bahama banks. Journal of Geophysical Research 71: 1575–1602.CrossRefGoogle Scholar
  9. Butler, A., N. Vicente, and B. Gaulejac. 1993. Ecology of the pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Marine Life (Marseille) 3: 37–45.Google Scholar
  10. Byrne, M. 2012. Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research 76: 3–15.CrossRefGoogle Scholar
  11. Byrne, M., and R. Przeslawski. 2013. Multistressor impacts of warming and acidification of the ocean on marine invertebrates' life histories. Integrative and Comparative Biology 53: 582–596.CrossRefGoogle Scholar
  12. 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 2: e126.CrossRefGoogle Scholar
  13. Caldeira, K., and M.E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425: 365–365.CrossRefGoogle Scholar
  14. Carritt, D.E., and J.H. Carpente. 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 Linne, 1758 in the Mar Grande of Taranto (Ionian sea, Italy). Environmental Monitoring and Assessment 131: 339–347.CrossRefGoogle Scholar
  16. Comeau, S., G. Gorsky, S. Alliouane, and J.P. Gattuso. 2010. Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Marine Biology 157: 2341–2345.CrossRefGoogle Scholar
  17. Coppa, S., G.A. de Lucia, P. Magni, P. Domenici, P. Antognarelli, F. Satta, and A. Cucco. 2013. The effect of hydrodynamics on shell orientation and population density of Pinna nobilis in the Gulf of Oristano (Sardinia, Italy). Journal of Sea Research 76: 201–210.CrossRefGoogle Scholar
  18. Coutteau, P., and P. Sorgeloos. 1992. The use of algal substitutes and the requirement for live algae in the hatchery and nursery rearing of bivalve molluscs: an international survey. Journal of Shellfish Research 11: 467–476.Google Scholar
  19. 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.Google Scholar
  20. De Gaulejac, B., and N. Vicente. 1990. Ecologie de Pinna nobilis (L.) mollusque bivalve sur les côtes de Corse. Essais de Transplantation et Experiences en Milieu Contrôlé 10: 83–100.Google Scholar
  21. Dickinson, G.H., A.V. Ivanina, O.B. Matoo, H.O. Poertner, G. Lannig, C. Bock, E. Beniash, and I.M. Sokolova. 2012. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. Journal of Experimental Biology 215: 29–43.CrossRefGoogle Scholar
  22. Dickson, A.G. 1990. Standard potential of the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic seawater from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22: 113–127.CrossRefGoogle Scholar
  23. Dickson, A.G. 1993. The measurement of sea water pH. Marine Chemistry 44: 131–142.CrossRefGoogle Scholar
  24. Dickson, A.G., and F.J. Millero. 1987. Comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawatermedia. Deep Sea Research 34: 1773–1743.Google Scholar
  25. 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
  26. Diffenbaugh, N.S., and F. Giorgi. 2012. Climate change hotspots in the CMIP5 global climate model ensemble. Climatic Change 114: 813–822.CrossRefGoogle Scholar
  27. 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
  28. Fabry, V.J., B.A. Seibel, R.A. Feely, and J.C. Orr. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marin Sciences 65: 414–432.CrossRefGoogle Scholar
  29. 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
  30. Feely, R.A., C.L. Sabine, J.M. Hernandez-Ayon, D. Ianson, and B. Hales. 2008. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320: 1490–1492.CrossRefGoogle Scholar
  31. 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
  32. Folt, C.L., C.Y. Chen, M.V. Moore, and J. Burnaford. 1999. Synergism and antagonism among multiple stressors. Limnology and Oceanography 44: 864–877.CrossRefGoogle Scholar
  33. Garcia-March, J.R., A.M. Garcia-Carrascosa, A.L.P. Cantero, and Y.G. Wang. 2007. Population structure, mortality and growth of Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia) at different depths in Moraira bay (Alicante, Western Mediterranean). Marine Biology 150: 861–871.CrossRefGoogle Scholar
  34. Gaylord, B., T.M. Hill, E. Sanford, E.A. Lenz, L.A. Jacobs, K.N. Sato, A.D. Russell, and A. Hettinger. 2011. Functional impacts of ocean acidification in an ecologically critical foundation species. Journal of Experimental Biology 214: 2586–2594.CrossRefGoogle 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.Google Scholar
  36. Gazeau, F., L.M. Parker, S. Comeau, J.-P. Gattuso, W.A. O'Connor, S. Martin, H.-O. Poertner, and P.M. Ross. 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology 160: 2207–2245.CrossRefGoogle Scholar
  37. Gazeau, F., M. Levy, and C. Wilhelm. 2011. Intracellular confinement of magnetic nanoparticles by living cells: Impact for imaging and therapeutic applications. In eds. P. Fantazzini, V. Bortolotti, J. Karger, and P. Galvosas, Pages 19–22. Magnetic Resonance in Porous Media.Google Scholar
  38. Giorgi, F. 2006. Climate change hot-spots. Geophysical Research Letters 33: L08707.CrossRefGoogle Scholar
  39. Green, M.A., G. Waldbusser, S. Reilly, K. Emerson, and S. O’Donnell. 2009. Death by dissolution: sediment saturation state as a mortality factor for juvenile bivalve. Limnology and Oceanography 54(4): 1037–47.CrossRefGoogle Scholar
  40. Hale, R., P. Calosi, L. McNeill, N. Mieszkowska, and S. Widdicombe. 2011. Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120: 661–674.CrossRefGoogle Scholar
  41. 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
  42. Hansen, H.P., H.C. Giesenhagen, and G. Behrends. 1999. Seasonal and long-term control of bottom-water oxygen deficiency in a stratified shallow-water coastal system. ICES Journal of Marine Science 56: 65–71.CrossRefGoogle 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. Álvarez. 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., S. Tenan, G. Tavecchia, N. Marbà, G. Jordà, S. Deudero, E. Álvarez, and C.M. Duarte. 2013. Boat anchoring impacts coastal populations of the pen shell, the largest bivalve in the Mediterranean. Biological Conservation 160: 105–13.CrossRefGoogle Scholar
  46. Hiebenthal, C., E.E.R. Philipp, A. Eisenhauer, and M. Wahl. 2013. Effects of seawater pCO(2) and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Marine Biology 160: 2073–2087.CrossRefGoogle Scholar
  47. Hofmann, G.E., and A.E. Todgham. 2010. Living in the now: Physiological mechanisms to tolerate a rapidly changing environment. Annual Review of Physiology 72: 127–145.CrossRefGoogle Scholar
  48. IPCC, J.-P. Gattuso, P. Brewer, O. Hoegh-Guldberg, J.A. Kleypas, H.-O. Pörtner, and D. Schmidt. 2014. Ocean acidification. In Climate change 2014: Impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, ed. C.B. Field, V.R. Barros, D.J. Dokken, K.J. Mach, M.D. Mastrandrea, T.E. Bilir, M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova, B. Girma, E.S. Kissel, A.N. Levy, S. MacCracken, P.R. Mastrandrea, and L.L. White, 129–131. Cambridge: Cambridge University Press.Google Scholar
  49. Jordá, G., N. Marba, and C.M. Duarte. 2012. Mediterranean seagrass vulnerable to regional climate warming. Nature Climate Change 2: 821–824.CrossRefGoogle Scholar
  50. Jury, C.P., R.F. Whitehead, and A.M. Szmant. 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 Biology 16: 1632–1644.CrossRefGoogle Scholar
  51. Katsanevakis, S. 2005. Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research 1: 1–9.Google Scholar
  52. Katsanevakis, S. 2007a. Density surface modelling with line transect sampling as a tool for abundance estimation of marine benthic species: The Pinna nobilis example in a marine lake. Marine Biology 152: 77–85.CrossRefGoogle Scholar
  53. Katsanevakis, S. 2007b. 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
  54. 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
  55. 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
  56. Kroeker, K.J., R.L. Kordas, R. Crim, I.E. Hendriks, L. Ramajo, G.S. Singh, C.M. Duarte, and J.-P. Gattuso. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896.CrossRefGoogle Scholar
  57. Kurihara, H., S. Kato, and A. Ishimatsu. 2007. Effects of increased seawater pCO(2) on early development of the oyster Crassostrea gigas. Aquatic Biology 1: 91–98.CrossRefGoogle Scholar
  58. Kurihara, H., T. Asai, S. Kato, and A. Ishimatsu. 2009. Effects of elevated pCO(2) on early development in the mussel Mytilus galloprovincialis. Aquatic Biology 4: 225–233.CrossRefGoogle Scholar
  59. Labasque, T. 2004. Spectrophotometric Winkler determination of dissolved oxygen: Re-examination of critical factors and reliability. Marine Chemistry 88: 53–60.CrossRefGoogle Scholar
  60. Lannig, G., S. Eilers, H.O. Poertner, 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
  61. 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 of Oceanology and Limnology 30: 206–211.CrossRefGoogle Scholar
  62. Marbá, N., and C.M. Duarte. 2010. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology 16: 2366–2375.CrossRefGoogle Scholar
  63. Meehl, G.A., T.F. Stocker, W.D. Collins, P. Friedlingstein, A.T. Gaye, J.M. Gregory, A. Kitoh, R. Knutti, J.M. Murphy, A. Noda, S.C.B. Raper, I.G. Watterson, A.J. Weaver, and Z.-C. Zhao. 2007. Global climate projections. In Climate change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, ed. S. Solomon et al., 747–845. Cambridge: Cambridge University Press.Google Scholar
  64. 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
  65. Melzner, F., S. Goebel, M. Langenbuch, M.A. Gutowska, H.-O. Poertner, 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
  66. Michaelidis, B., C. Ouzounis, A. Paleras, and H.O. Portner. 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
  67. 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
  68. 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
  69. Parker, L.M., P.M. Ross, and W.A. O'Connor. 2010. Comparing the effect of elevated pCO(2) and temperature on the fertilization and early development of two species of oysters. Marine Biology 157: 2435–2452.CrossRefGoogle Scholar
  70. Parker, L.M., P.M. Ross, W.A. O'Connor, L. Borysko, D.A. Raftos, and H.O. Poertner. 2012. Adult exposure influences offspring response to ocean acidification in oysters. Global Change Biology 18: 82–92.CrossRefGoogle Scholar
  71. Parker, L.M., P.M. Ross, W.A. O’Connor, H.O. Pörtner, E. Scanes, and J.M. Wright. 2013. Predicting the Response of Molluscs to the Impact of Ocean Acidification. Biology 2: 651–692. doi: 10.3390/biology202065.CrossRefGoogle Scholar
  72. Pierrot, D., E. Lewis, and D.W.R. Wallace. 2006. MS excel program developed for CO 2 system calculations. ORNL/CDIAC-105a. Oak Ridge: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.Google Scholar
  73. Poloczanska, E.S., C.J. Brown, W.J. Sydeman, W. Kiessling, D.S. Schoeman, P.J. Moore, K. Brander, J.F. Bruno, L.B. Buckley, M.T. Burrows, C.M. Duarte, B.S. Halpern, J. Holding, C.V. Kappel, M.I. O'Connor, J.M. Pandolfi, C. Parmesan, F. Schwing, S.A. Thompson, and A.J. Richardson. 2013. Global imprint of climate change on marine life. Nature Climate Change 3: 919–925.CrossRefGoogle Scholar
  74. Rabaoui, L., S.T. Zouari, S. Katsanevakis, and O.K. Ben Hassine. 2007. Comparison of absolute and relative growth patterns among five Pinna nobilis populations along the Tunisian coastline: an information theory approach. Marine Biology 152: 537–548.CrossRefGoogle Scholar
  75. Range, P., M.A. Chícharo, R. Ben-Hamadou, D. Piló, D. Matias, S. Joaquim, A.P. Oliveira, and L. Chícharo. 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 of Experimental Marine Biology and Ecology 396: 177–184.CrossRefGoogle Scholar
  76. Range, P., D. Pilo, R. Ben-Hamadou, M.A. Chicharo, D. Matias, S. Joaquim, A.P. Oliveira, and L. Chicharo. 2012. Seawater acidification by CO2 in a coastal lagoon environment: Effects on life history traits of juvenile mussels Mytilus galloprovincialis. Journal of Experimental Marine Biology and Ecology 424: 89–98.CrossRefGoogle Scholar
  77. Range, P., M.A. Chícharo, P. Ben-Hamadou, D. Piló, M.J. Fernandez-Reiriz, U. Labarta, M.G. Marin, M. Bressan, V. Matozzo, A. Chinellato, M. Munari, N.T.E. Menif, M. Dellali, and L. Chícharo. 2013. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressor. Regional Environmental Change 14: 19–30.CrossRefGoogle Scholar
  78. Richardson, C.A., H. Kennedy, C.M. Duarte, D.P. Kennedy, and S.V. Proud. 1999. Age and growth of the fan mussel Pinna nobilis from south-east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Marine Biology 133: 205–212.CrossRefGoogle Scholar
  79. 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
  80. 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
  81. Rodolfo-Metalpa, R., S. Martin, C. Ferrier-Pages, and J.P. Gattuso. 2010. Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO(2) and temperature levels projected for the year 2100. Biogeosciences 7: 481–481.CrossRefGoogle Scholar
  82. Shirayama, Y. and H. Thornton. 2005. Effect of increased atmospheric CO2 on shallow water marine benthos. Journal of Geophysical Research-Oceans 110.Google Scholar
  83. Sunday, J.M., R.N. Crim, C.D.G. Harley, and M.W. Hart. 2011. Quantifying Rates of Evolutionary Adaptation in Response to Ocean Acidification. PloS ONE 6.Google Scholar
  84. Talmage, S.C., and C.J. Gobler. 2011. Effects of elevated temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of northwest Atlantic bivalves. PLoS ONE 6(10): e26941. doi: 10.1371/journal.pone.002694.CrossRefGoogle Scholar
  85. Thomas, M.K., C.T. Kremer, C.A. Klausmeier, and E. Litchman. 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338: 1085–1088.CrossRefGoogle Scholar
  86. Waldbusser, G.G., H. Bergschneider, and M.A. Green. 2010. Size-dependent pH effect on calcification in post-larval hard clam Mercenaria spp. Marine Ecology Progress Series 417: 171–182.CrossRefGoogle Scholar
  87. Weigelt, M., and H. Rumohr. 1986. Effects of wide-range oxygen depletion on benthic fauna and demersal fish in Kiel bay 1981–1983. Meeresforschung-Reports on Marine Research 31: 124–136.Google Scholar
  88. Welladsen, H.M., P.C. Southgate, and K. Heimann. 2010. The effects of exposure to near-future levels of ocean acidification on shell characteristics of Pinctada fucata (Bivalvia: Pteriidae). Molluscan Research 30: 125–130.Google Scholar
  89. Widdicombe, S., S.L. Dashfield, C.L. McNeill, H.R. Needham, A. Beesley, A. McEvoy, S. Oxnevad, K.R. Clarke, and J.A. Berge. 2009. Effects of CO2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Marine Ecology Progress Series 379: 59–75.CrossRefGoogle Scholar
  90. Zavodnik, D., M. Hrs-Brenko, and M. Legac. 1991. Synopsis on the fan shell Pinna nobilis L. in the Eastern Adriatic sea. 169–178.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2015

Authors and Affiliations

  • Lorena Basso
    • 1
  • Iris E. Hendriks
    • 1
  • Carlos M. Duarte
    • 1
    • 2
  1. 1.Global Change DepartmentInstituto Mediterráneo de Estudios Avanzados (IMEDEA)EsporlesSpain
  2. 2.King Abdullah University of Science and TechnologyThuwalKingdom of Saudi Arabia

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