Reviews and syntheses: Responses of coccolithophores to ocean acidification: A meta-analysis

Biogeosciences

Volumn 12, Issue 6, 2015, Pages 1671-1682

  Meyer, J ^a   Riebesell, U ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; ADAPTATION; CALCIFICATION; CARBON DIOXIDE; COCCOLITH; META-ANALYSIS; PHYTOPLANKTON; POLLUTION EFFECT; POLLUTION TOLERANCE; SPECIES DIVERSITY;

COCCOLITHUS; EMILIANIA HUXLEYI; GEPHYROCAPSA OCEANICA; HAPTOPHYCEAE;

EID: 84924943280     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-12-1671-2015     Document Type: Article

References (54)

1. Armstrong, R. A., Lee, C., Hedges, J. I., Honjo, S., and Wakeham, S. G.: A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals, Deep-Sea Res. Pt. II, 49, 219-236, 2002.
2. Bach, L. T., Riebesell, U., and Schulz, K.: Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi, Limnol. Oceanogr., 56, 2040-2050, 2011.
3. Barcelos e Ramos, J., Müller, M. N., and Riebesell, U.: Shortterm response of the coccolithophore Emiliania huxleyi to an abrupt change in seawater carbon dioxide concentrations, Biogeosciences, 7, 177-186, doi:10.5194/bg-7-177-2010, 2010.
4. Borenstein, M., Hedges, L. V., Higgins, J., and Rothstein, H. R.: A basic introduction to fixed-effect and random-effects models for meta-analysis, Res. Synth. Methods, 1, 97-111, 2010.
5. Brownlee, C. and Taylor, A.: Calcification in coccolithophores: A cellular perspective, in: Coccolithophores-From Molecular Processes to Global Impact, edited by: Thierstein, H. R. and Young, J. R., Springer, Germany, 31-49, 2004.
6. Cochran, W.: The contribution of estimates from different experiments, Biometrics, 10, 101-129, 1954.
7. Cubillos, J. C., Wright, S. W., Nash, G., de Salas, M. F., Griffiths, B., Tilbrook, B., Poisson, A., and Hallegraeff, G. M.: Calcification morphotypes of the coccolithophorid Emiliania huxleyi in the Southern Ocean: changes in 2001 to 2006 compared to historical data, Mar. Ecol.-Prog. Ser., 348, 47-54, 2007.
8. De Bodt, C., Van Oostende, N., Harlay, J., Sabbe, K., and Chou, L.: 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, doi:10.5194/bg-7-1401-2010, 2010.
9. Delille, B., Harlay, J., Zondervan, I., Jacquet, S., Chou, L., Wollast, R., Bellerby, R. G. J., Frankignoulle, M., Borges., A. V., Riebesell, U., and Gattuso, J. P.: Response of primary production and calcification to changes of pCO2 during experimental blooms of the coccolithophorid Emiliania huxleyi, Global Biogeochem. Cy., 19, 1-14, 2005.
10. Engel, A., Zondervan, I., Aerts, K., Beaufort, L., Benthien, A., Chou, L., Delille, B., Gattuso, J. P., Harlay, J., Heemann, C., Hoffmann, L., Jacquet, S., Nejstgaard, J., Pizay, M. D., Rochelle-Newall, E., Schneider, U., Terbrueggen, A., and Riebesell, U.:: Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments, Limnol. Oceanogr., 50, 493-507, 2005.
11. Feng, Y., Warner, M. E., Zhang, Y., Sun, J., Fu, F. X., Rose, J. M., and Hutchins, D. A.: Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae), Eur. J. Phycol., 43, 87-98, 2008.
12. Findlay, H. S., Calosi, P., and Crawfurd, K.: Determinants of the PIC:POC response in the coccolithophore Emiliania huxleyi under future ocean acidification scenarios, Limnol. Oceanogr., 56, 1168-1178, 2011.
13. Fiorini, S., Middelburg, J. J., and Gattuso, J. P.: Testing the effects of elevated pCO2 on coccolithophores (Prymnesiophyceae): comparison between haploid and diploid life stages, J. Phycol., 47, 1281-1291, 2011.
14. Gao, K., Ruan, Z., Villafañe, V. E., Gattuso, J. P., and Helbling, E. W.: Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi, Limnol. Oceanogr., 54, 1855-1862, 2009.
15. Hedges, L. V. and Olkin, I. (Eds.): Statistical Methods for Meta-Analysis, Academic Press, London, New York, 108-138, 1985.
16. Hedges, L. V., Gurevitch, J., and Curtis, P. S.: The meta-analysis of response ratios in experimental ecology, Ecology, 80, 1150-1156, 1999.
17. Hendriks, I. E., Duarte, C. M., and Álvarez, M.: Vulnerability of marine biodiversity to ocean acidification: A meta-analysis, Estuar. Coast. Shelf, 86, 157-164, 2010.
18. Hoppe, C. J. M., Langer, G., and Rost, B.: Emiliania huxleyi shows identical responses to elevated pCO2 in TA and DIC manipulations, J. Exp. Mar. Biol. Ecol., 406, 54-62, 2011.
19. Hoppe, C. J. M., Langer, G., Rokitta, S. D., Wolf-Gladrow, D. A., and Rost, B.: Implications of observed inconsistencies in carbonate chemistry measurements for ocean acidification studies, Biogeosciences, 9, 2401-2405, doi:10.5194/bg-9-2401-2012, 2012.
20. Iglesias-Rodriguez, M. D., Schofield, O. M., Batley, J., Medlin, L. K., and Hayes, P. K.: Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies, J. Phycol., 42, 526-536, 2006.
21. Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E., Hall, I. R., Colmenero-Hidalgo, E., Gittins, J. R., Green, D. R. H., Tyrrell, T., Gibbs, S. J., von Dassow, P., Rehm, E., Armbrust, E. V., and Boessenkool, K. P.: Phytoplankton Calcification in a High-CO2 World, Science, 320, 336-340, 2008.
22. Jones, B. M., Iglesias-Rodriguez, M. D., Skipp, P. J., Edwards, R. J., Greaves, M. J., Young, J. R., Elderfield, H., and O'Connor, C. D.: Responses of the Emiliania huxleyi Proteome to Ocean Acidification, PLoS ONE, 8, e61868, doi:10.1371/journal.pone.0061868, 1-13, 2013.
23. Klaas, C. and Archer, D. E.: Association of sinking organic matter with various types of mineral ballast in the deep sea: Implications for the rain ratio, Global Biogeochem. Cy., 16, 63-1-63-14, 2002.
24. Kroeker, K. J., Kordas, R. L., Crim, R. N., and Singh, G. G.: Metaanalysis reveals negative yet variable effects of ocean acidification on marine organisms, Ecol. Lett., 13, 1419-1434, 2010.
25. Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M., and Gattuso, J. P.: Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming, Glob. Change Biol., 19, 1884-1896, 2013.
26. Krug, S. A., Schulz, K. G., and Riebesell, U.: Effects of changes in carbonate chemistry speciation on Coccolithus braarudii: a discussion of coccolithophorid sensitivities, Biogeosciences, 8, 771-777, doi:10.5194/bg-8-771-2011, 2011.
27. Langer, G. and Bode, M.: CO2 mediation of adverse effects of seawater acidification in Calcidiscus leptoporus, Geochem. Geophy. Geosy., 12, 1-8, 2011.
28. Langer, G., Geisen, M., Baumann, K. H., Kläs, J., Riebesell, U., Thoms, S., and Young, J. R.: Species-specific responses of calcifying algae to changing seawater carbonate chemistry, Geochem. Geophy. Geosy., 7, 1-12, 2006.
29. Langer, G., Nehrke, G., Probert, I., Ly, J., and Ziveri, P.: Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry, Biogeosciences, 6, 2637-2646, doi:10.5194/bg-6-2637-2009, 2009.
30. Lefebvre, S. C., Benner, I., Stillman, J. H., Parker, A. E., Drake, M. K., Rossignol, P. E., Okimura, K. M., Komada, T., and Carpenter, E. J.: Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle, Glob. Change Biol., 18, 493-503, 2012.
31. Lohbeck, K. T., Riebesell, U., and Reusch, T. B.: Adaptive evolution of a key phytoplankton species to ocean acidification, Nat. Geosci., 5, 346-351, 2012.
32. Müller, M. N., Schulz, K. G., and Riebesell, U.: Effects of long-term high CO2 exposure on two species of coccolithophores, Biogeosciences, 7, 1109-1116, doi:10.5194/bg-7-1109-2010, 2010.
33. Nakicenovic, N., Alcamo, J., Davis, G., De Vries, B., Fenhann, J., Gaffin, S., Gregory, K., Griibler, A., Jung, T. Y., Kram, T., Lebre, E., Rovere, L., Michaelis, L., Mori, S., Morita, T., Smith, S., Swart, R., Van Rooijen, S., Victor, N., and Dadi, Z.: Emission scenarios, A special report of Working Group III of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom, 239-292, 2000.
34. Nimer, N. A. and Merrett, M. J.: The development of a CO2-concentrating mechanism in Emiliania huxleyi, New Phytol., 133, 383-389, 1996.
35. Richier, S., Fiorini, S., Kerros, M. E., Von Dassow, P., and Gattuso, J. P.: Response of the calcifying coccolithophore Emiliania huxleyi to low pH/high pCO2: from physiology to molecular level, Mar. Biol., 158, 551-560, 2011.
36. Rickaby, R. E. M., Henderiks, J., and Young, J. N.: Perturbing phytoplankton: response and isotopic fractionation with changing carbonate chemistry in two coccolithophore species, Clim. Past, 6, 771-785, doi:10.5194/cp-6-771-2010, 2010.
37. Ridgwell, A., Schmidt, D. N., Turley, C., Brownlee, C., Maldonado, M. T., Tortell, P., and Young, J. R.: From laboratory manipulations to Earth system models: scaling calcification impacts of ocean acidification, Biogeosciences, 6, 2611-2623, doi:10.5194/bg-6-2611-2009, 2009.
38. Riebesell, U.: Effects of CO2 Enrichment on Marine Phytoplankton, J. Oceanogr., 60, 719-729, 2004.
39. Riebesell, U. and Tortell, P. D.: Effects of ocean acidification on pelagic organisms and ecosystems, in: Ocean Acidification, edited by: Gattuso, J. P. and Hansson, L., Oxford University Press, 99-121, 2011.
40. Riebesell, U., Zondervan, I., Rost, B., Tortell, P. D., Zeebe, R. E., and Morel, F. M.: Reduced calcification of marine plankton in response to increased atmospheric CO2, Nature, 407, 364-367, 2000.
41. Riebesell, U., Bellerby, R. G., Engel, A., Fabry, V. J., Hutchins, D. A., Reusch, T. B. H., Schulz, K. G., and Morel, F. M. M.: Comment on Phytoplankton Calcification in a High-CO2 World, Science, 322, 1466b, 2008.
42. Riebesell, U., Körtzinger, A., and Oschlies, A.: Sensitivities of marine carbon fluxes to ocean change, P. Natl. Acad. Sci. USA, 106, 20602-20609, 2009.
43. Ries, J. B., Cohen, A. L., and McCorkle, D. C.: Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification, Geology, 37, 1131-1134, 2009.
44. Rokitta, S. D. and Rost, B.: Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi, Limnol. Oceanogr., 57, 607-618, 2012.
45. Rost, B., Riebesell, U., Burkhardt, S., and Sültemeyer, D.: Carbon acquisition of bloom-forming marine phytoplankton, Limnol. Oceanogr., 48, 55-67, 2003.
46. Rost, B., Zondervan, I., andWolf-Gladrow, D.: Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions, Mar. Ecol.-0Prog. Ser., 373, 227-237, 2008.
47. Sabine, C. L., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J. L., Wanninkhof, R., Wong, C. S., Wallace, D. W. R., Tilbrook, B., Millero, F. J., Peng, T. H., Kozyr, A., Ono, T., and Rios, A. F.: The oceanic sink for anthropogenic CO2, Science, 305, 367-371, 2004.
48. Sciandra, A., Harlay, J., Lefèvre, D., Lemeé, R., Rimmelin, P., Denis, M., and Gattuso, J. P.: Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation, Mar. Ecol.-Prog. Ser., 261, 111-122, 2003.
49. Sett, S., Bach, L. T., Schulz, K. G., Koch-Klavsen, S., Lebrato, M., and Riebesell, U.: Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcifi-cation to increasing seawater pCO2, PLoS ONE, 9, e88308, doi:10.1371/journal.pone.0088308, 2014.
50. Shi, D., Xu, Y., and Morel, F. M. M.: Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth, Biogeosciences, 6, 1199-1207, doi:10.5194/bg-6-1199-2009, 2009.
51. Shutler, J. D., Grant, M. G., Miller, P. I., Rushton, E., and Anderson, K.: Coccolithophore bloom detection in the northeast Atlantic using SeaWiFS: Algorithm description, application and sensitivity analysis, Remote Sens. Environ., 114, 1008-1016, 2010.
52. Wuori, T.: Effects of elevated pCO2 on the physiology of Emiliania huxleyi, M.Sc. Thesis, Western Washington University, USA, 97 pp., 2012.
53. Ziveri, P., de Bernardi, B., Baumann, K. H., Stoll, H. M., and Mortyn, P. G.: Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean, Deep-Sea Res. Pt. II, 54, 659-675, 2007.
54. Zondervan, I., Rost, B., and Riebesell, U.: Effect of CO2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths, J. Exp. Mar. Biol. Ecol. 272, 55-70,