Extreme pH Conditions at a Natural CO2 Vent System (Italy) Affect Growth, and Survival of Juvenile Pen Shells (Pinna nobilis)
- 508 Downloads
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.
KeywordsPinna nobilis Ocean acidification Volcanic CO2 vents Bivalve Mineralization Growth
This research was supported by the MedSeA project (www.medsea-project.eu, 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.
- 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
- 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.
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- Hubbard, F., J. McManus and M. Al-Dabbas. 1981. Environmental influences on the shell mineralogy of Mytilus edulis. Geo Marine Letter 1: 267–269.Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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