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

Estuaries and Coasts

Volumn 38, Issue 6, 2015, Pages 1976-1985

  Basso, Lorena ^a   Hendriks, Iris E ^a   Duarte, Carlos M ^a,b  

^a INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Growth; Metabolism rate; Ocean acidification; Pinna nobilis; Survival; Warming

Indexed keywords

ACIDIFICATION; ANTHROPOGENIC SOURCE; BIVALVE; CARBON DIOXIDE; GROWTH RATE; JUVENILE; METABOLISM; MORTALITY; OXYGEN; SURVIVAL; SYNERGISM; TEMPERATURE EFFECT; TOLERANCE; VULNERABILITY; WARMING; WATER TEMPERATURE;

INVERTEBRATA; PINNA NOBILIS;

EID: 84943348614     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-015-9948-0     Document Type: Article

References (90)

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.
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.
3. 2 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.
5. 2-induced seawater acidification on the health of Mytilus edulis. Climate Research 37: 215–225.
6. 2-induced seawater acidification on the health of Mytilus edulis. Climate Research 37: 215–225.
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.
8. Broecker, W.S., and T. Takahash. 1966. Calcium carbonate precipitation on Bahama banks. Journal of Geophysical Research 71: 1575–1602.
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.
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.
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.
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.
13. Caldeira, K., and M.E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425: 365–365.
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.
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.
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.
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.
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.
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.
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.
21. 2 levels on juvenile eastern oysters, Crassostrea virginica. Journal of Experimental Biology 215: 29–43.
22. − in synthetic seawater from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22: 113–127.
23. Dickson, A.G. 1993. The measurement of sea water pH. Marine Chemistry 44: 131–142.
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.
25. 2 measurements. PICES Special Publication 3: 191.
26. Diffenbaugh, N.S., and F. Giorgi. 2012. Climate change hotspots in the CMIP5 global climate model ensemble. Climatic Change 114: 813–822.
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.
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.
29. 3 system in the oceans. Science 305: 362–366.
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.
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.
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.
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.
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.
35. 2 on shellfish calcification. Geophysical Research Letters 34.
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.
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.
38. Giorgi, F. 2006. Climate change hot-spots. Geophysical Research Letters 33: L08707.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
49. Jordá, G., N. Marba, and C.M. Duarte. 2012. Mediterranean seagrass vulnerable to regional climate warming. Nature Climate Change 2: 821–824.
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.
51. Katsanevakis, S. 2005. Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research 1: 1–9.
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.
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.
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.
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.
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.
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.
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.
59. Labasque, T. 2004. Spectrophotometric Winkler determination of dissolved oxygen: Re-examination of critical factors and reliability. Marine Chemistry 88: 53–60.
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.
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.
62. Marbá, N., and C.M. Duarte. 2010. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology 16: 2366–2375.
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.
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.
65. 2. Aquatic Toxicology 92: 30–37.
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.
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.
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.
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.
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.
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.
72. 2system calculations. ORNL/CDIAC-105a. Oak Ridge: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.
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.
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.
75. 2 and reduced pH: Variable responses to ocean acidification at local scales? Journal of Experimental Marine Biology and Ecology 396: 177–184.
76. 2 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.
77. 2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressor. Regional Environmental Change 14: 19–30.
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.
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.
80. 2-induced ocean acidification. Geology 37: 1131–1134.
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.
82. 2 on shallow water marine benthos. Journal of Geophysical Research-Oceans 110.
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.
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.
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.
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.
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.
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.
89. 2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Marine Ecology Progress Series 379: 59–75.
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.