Carbon isotopic fractionation during a mesocosm bloom experiment dominated by Emiliania huxleyi: Effects of CO2 concentration and primary production

Geochimica et Cosmochimica Acta

Volumn 71, Issue 6, 2007, Pages 1528-1541

  Benthien, Albert ^a   Zondervan, Ingrid ^a   Engel, Anja ^a   Hefter, Jens ^a   Terbrüggen, Anja ^a   Riebesell, Ulf ^b  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

ALKENONE; CARBON DIOXIDE; CARBON ISOTOPE; COCCOLITH; ISOTOPIC FRACTIONATION; MESOCOSM; PARTICULATE ORGANIC MATTER; PHYTOPLANKTON; PRIMARY PRODUCTION;

EMILIANIA HUXLEYI;

EID: 33847403988     PISSN: 00167037     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gca.2006.12.015     Document Type: Article

References (91)

1. 2 in surface waters: results from the Late Quaternary Angola Current. In: Fischer G., and Wefer G. (Eds). Use of Proxies in Paleoceanography: Examples from the South Atlantic (1999), Springer 469-488
2. 2-concentrating mechanisms in algae. Can. J. Bot. 76 (1998) 1052-1071
3. Bell M.V., and Pond D. Lipid composition during growth of motile and coccolith forms of Emiliania huxleyi. Phytochemistry 41 (1996) 465-471
4. Benner R., Pakulski J.D., McCarthy M., Hedges J.I., and Hatcher P. Bulk chemical characteristics of dissolved organic matter in the ocean. Science 255 (1992) 1561-1564
5. 2 and nutrient concentrations. Global Biogeochem. Cycles 16 (2002) 10.1029/2001GB001433
6. 37:2 alkenone in the South Atlantic: Last Glacial Maximum (LGM) vs. Holocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 221 (2005) 123-140
7. 13C in nature and in the laboratory: growth-rate effects in some haptophyte algae. Global Biogeochem. Cycles 11 (1997) 279-292
8. Brassell S.C. Applications of biomarkers for delineating marine paleoclimatic fluctuations during the Pleistocene. In: Engel M.H., and Macko S.A. (Eds). Org. Geochem. (1993), Plenum Press, New York 699-738
9. Brown C.W., and Yoder J.A. Coccolithophorid blooms in the global ocean. J. Geophys. Res. 99 (1994) 7467-7482
10. Brown M.R., Dunstan G.A., Norwood S.J., and Miller K.A. Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J. Phycol. 32 (1996) 64-73
11. 2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochim. Cosmochim. Acta 63 (1999) 3729-3741
12. Calvo E., Pelejero C., and Logan G.A. Pressurized liquid extraction of selected molecular biomarkers in deep sea sediments used as proxies in paleoceanography. J. Chromatogr. A 989 (2003) 197-205
13. Conte M.H., Thompson A., Eglinton G., and Green J.C. Lipid biomarker diversity in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) and the related species Gephyrocapsa oceanica. J. Phycol. 31 (1995) 272-282
14. Conte M.H., Thompson A., Lesley D., and Harris R.P. Genetic and physiological influences on the alkenone/alkenoate versus growth temperature relationship in Emiliania huxleyi and Gephyrocapsa oceanica. Geochim. Cosmochim. Acta 62 (1998) 51-68
15. 2+-binding polysaccharide associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner. Eur. J. Biochem. 70 (1976) 611-621
16. Deines P. The isotopic composition of reduced organic carbon. In: Fritz P., and Fontes J.C. (Eds). Handbook of environmental isotope geochemistry (1980), Elsevier 329-406
17. 2 during experimental blooms of the coccolithophorid Emiliania huxleyi. Global Biogeochem. Cycles 19 (2005) 10.1029/2004GB002318
18. Dunstan G.A., Volkman J.K., Barrett S.M., and Garland C.D. Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J. Appl. Phycol. 5 (1993) 71-83
19. Egge J.K., and Aksnes D.L. Silicate as regulating nutrient in phytoplankton competition. Mar. Ecol. Prog. Ser. 83 (1992) 281-289
20. Eltgroth M.L., Watwood R.L., and Wolfe G.V. Production and cellular localization of neutral long-chain lipids in the haptophyte algae Isochrysis galbana and Emiliania huxleyi. J. Phycol. 41 (2005) 1000-1009
21. Engel A. The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (α) during the decline of a diatom bloom. J. Plankton Res. 22 (2000) 485-497
22. Engel A., and Passow U. Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Mar. Ecol. Prog. Ser. 219 (2001) 1-10
23. Engel A., Thoms S., Riebesell U., Rochelle-Newall E., and Zondervan I. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. Nature 428 (2004) 929-932
24. 2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol. Oceanog. 50 (2005) 493-507
25. Epstein B.L., D'Hondt S., Quinn J.G., Zhang J., and Hargraves P.E. An effect of dissolved nutrient concentrations on alkenone-based temperature estimates. Paleoceanography 13 (1998) 122-126
26. 37 alkenones in Emiliania huxleyi. Org. Geochem. 32 (2001) 867-875
27. Fernández E., Balch W.M., Marañón E., and Holligan P.M. High rates of lipid biosynthesis in cultured, mesocosm and coastal populations of the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser. 114 (1994) 13-22
28. Fernández E., Marañón E., and Balch W.M. Intracellular carbon partitioning in the coccolithophorid Emiliania huxleyi. J. Mar. Syst. 9 (1996) 57-66
29. Fichtinger-Schepman A.M.J., Kamerling J.P., Vliegenhart J.F.G., De Jong E.W., Bosch L., and Westbroek P. Composition of a methylated, acidic polysaccharide associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner. Carbohydr. Res. 69 (1979) 181-189
30. 13C of surface water particulate organic matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem. Cycles 7 (1993) 627-644
31. 2 levels. Global Biogeochem. Cycles 6 (1992) 185-198
32. Goericke R., Montoya J.P., and Fry B. Physiology of isotopic fractionation in algae and cyanobacteria. In: Lajhta K., and Michener R.H. (Eds). Stable Isotopes in Ecology and Environmental Science (1994), Blackwell Science Publishers 187-221
33. Hayes J.M. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. In: Valley J.W., and Cole D.R. (Eds). Stable Isotope Geochemistry vol. 43 (2001), Mineralogical Society of America 225-277
34. Herbert T. D., 2001. Review of alkenone calibrations (culture, water column, and sediments). Geochem., Geophys., Geosyst. 2, Paper number 2000G000055.
35. 2 levels during the late Quaternary. Nature 347 (1990) 462-464
36. 2 in the central equatorial Pacific during the last 255,000 years. Paleoceanography 9 (1994) 781-798
37. Keller K., and Morel F.M.M. A model of carbon isotopic fractionation and active carbon uptake in phytoplankton. Mar. Ecol. Prog. Ser. 182 (1999) 295-298
38. Kepkay P.E., Niven S.E.H., and Milligan T.G. Low molecular weight and colloidal DOC production during a phytoplankton bloom. Mar. Ecol. Prog. Ser. 100 (1993) 233-244
39. Kerner M., Hohenberg H., Ertl S., Reckermann M., and Spitzy A. Self-organization of dissolved organic matter to micelle-like microparticles in river water. Nature 422 (2003) 150-154
40. Kienast M., Steinke S., Stattegger K., and Calvert S.E. Synchronous tropical South China Sea SST change and Greenland warming during deglaciation. Science 291 (2001) 2132-2134
41. Koroleff F., and Grasshof K. Determination of nutrients. In: Grasshof K., Erhardt M., and Kremling K. (Eds). Methods of Seawater Analyses vol. 2 (1983), Verlag Chemie 125-188
42. 2aq: theoretical considerations and experimental results. Geochim. Cosmochim. Acta 59 (1995) 1131-1138
43. Laws E. A., Popp B. N., Bidigare R. R., Riebesell U., Burkhardt S., and Wakeham S. G., 2001. Controls on the molecular distribution and carbon isotopic composition of alkenones in certain haptophyte algae. Geochem., Geophys., Geosyst. 2, Paper number 2000GC000057.
44. Lyle M.W., Prahl F.G., and Sparrow M.A. Upwelling and productivity changes inferred from a temperature record in the central equatorial pacific. Nature 355 (1992) 812-815
45. Mook W.G., Bommerson J.C., and Staverman W.H. Carbon isotope fractionation between dissolved bicarbonate and gaseous dioxide. Earth Planet. Sci. Lett. 22 (1974) 169-176
46. K′ based on core-tops from the eastern South Atlantic and the global ocean (60°N-60°S). Geochim. Cosmochim. Acta 62 (1998) 1757-1772
47. Myklestad S.M. Release of extracellular products by phytoplankton with special emphasis on polysaccharides. The Science of the Total Environment 165 (1995) 155-164
48. Nanninga H.J., Ringenaldus P., and Westbroek P. Immunological quantitation of a polysaccharide formed by Emiliania huxleyi. J. Mar. Syst. 9 (1996) 67-74
49. Paasche E. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40 6 (2002) 503-529
50. 2 proxy. Paleoceanography 17 (2002) 1069 10.1029/2002PA000756
51. Pagani M., Zachos J.C., Freeman K.H., Tipple B., and Bohaty S. Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309 (2005) 600-603
52. Pond D.W., and Harris R.P. The lipid composition of the coccolithophore Emiliania huxleyi and its possible ecophysiological significance. J. Mar. Biol. Assoc. U.K. 76 (1996) 579-594
53. Popp B.D., Kenig F., Wakeham S.G., Laws E.A., and Bidigare R.R. Does growth rate affect ketone unsaturation and intracellular carbon isotopic variability in Emiliania huxleyi?. Paleoceanography 13 (1998) 35-41
54. Popp B.N., Laws E.A., Bidigare R.R., Dore J.E., Hanson K.L., and Wakeham S.G. Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochim. Cosmochim. Acta 62 (1998) 69-77
55. Popp B.D., Prahl F.G., Wallsgrove R.J., and Tanimoto J. Seasonal patterns of alkenone production in the subtropical oligotrophic North Pacific. Paleoceanography 21 1 (2006) PA1004 10.1029/2005PA001165
56. Prahl F.G., and Wakeham S.G. Calibration of unsaturation patterns in long-chain ketone compositions for paleotemperature assessment. Nature 330 (1987) 367-369
57. Prahl F.G., Muehlhausen L.A., and Zahnle D.L. Further evaluation of long-chain alkenones as indicators of paleoceanographic conditions. Geochim. Cosmochim. Acta 52 (1988) 2303-2310
58. Prahl F. G., Herbert T. D., Brassell S. C., Ohkouchi N., Pagani M., Repeta D., Rosell-Melé A., and Sikes E., 2000. Status of alkenone paleothermometer calibration: report from Working Group 3. Geochem., Geophys., Geosyst. 1, Paper number 2000GC000058.
59. Prahl F.G., Wolfe G.V., and Sparrow M.A. Physiological impacts on alkenone paleothermometry. Paleoceanography 18 (2003) 1025 10.1029/2002PA000803
60. Prahl F.G., Popp B.N., Karl D.M., and Sparrow M.A. Ecology and biogeochemistry of alkenone production at Station ALOHA. Deep Sea Research Part I: Oceanographic Research Papers 52 5 (2005) 699-719
61. Purdie D.A., and Finch M.S. Impact of coccolithophorids on dissolved carbon dioxide in sea water enclosures in a Norwegian Fjord. Sarsia 79 (1994) 379-387
62. 2 uptake. Mar. Ecol. Prog. Ser. 133 (1996) 275-285
63. Raven J.A., and Johnston A.M. Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources. Limnol. Oceanog. 38 (1991) 1701-1714
64. 2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi. Geochim. Cosmochim. Acta 64 (2000) 4179-4192
65. Riegman R., Stolte W., Noordeloos A.A.M., and Slezak D. Nutrient uptake and alkaline phosphatase (EC 3:1:3:1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. J. Phycol. 36 (2000) 87-96
66. Robertson J.E., Robinson C., Turner D.R., Holligan P., Watson A.J., Boyd P., Fernández E., and Finch M. The impact of a coccolithophore bloom on oceanic carbon uptake in the northeast Atlantic during summer 1991. Deep-Sea Res. I 41 (1994) 297-314
67. 2 levels. Mar. Ecol. Progr. Ser. 272 (2004) 25-31
68. Rost B., Zondervan I., and Riebesell U. Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnol. Oceanog. 47 (2002) 120-128
69. Rost B., Riebesell U., Burkhardt S., and Sültemeyer D. Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanog. 48 (2003) 55-67
70. Rost B., and Riebesell U. Coccolithophores and the biological pump: responses to environmental changes. In: Thierstein H.R., and Young J.R. (Eds). Coccolithophores-From Molecular Process To Global Impact (2004), Springer 99-125
71. Rost B., Riebesell U., and Sültemeyer D. Carbon acquisition of marine phytoplankton: Effect of photoperiod length. Limnol. Oceanog. 51 1 (2006) 12-20
72. 18O and alkenone records. Nature 364 (1993) 319-321
73. Sachs J.P., and Lehman S.J. Subtropical North Atlantic temperatures 60,000 to 30,000 years ago. Science 286 (1999) 756-759
74. Sawada K., and Shiraiwa Y. Alkenone and alkenoic acid compositions of the membrane fractions of Emiliania huxleyi. Phytochemistry 65 9 (2004) 1299-1307
75. Schantz M.M., Nichols J.J., and Wise S.A. Evaluation of pressurized fluid extraction for the extraction of environmental matrix reference materials. Anal. Chem. 69 (1997) 4210-4219
76. Schouten S., Klein Breteler W.C.M., Blokker P., Schogt N., Rijpstra W.I.C., Grice K., Baas M., and Sinninghe Damsté J.S. Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: Implications for deciphering the carbon isotopic biomarker record. Geochim. Cosmochim. Acta 62 (1998) 1397-1406
77. 37 alkenones in deep-sea sediments: its potential as paleonutrient proxy. Paleoceanography 19 (2004) PA1011 10.1029/2002PA000811
78. 2 concentrating mechanism. In: Lucas W.J., and Berry J.A. (Eds). Inorganic Carbon Uptake By Aquatic Photosynthetic Organisms (1985), The American Society of Plant Physiologists 389-401
79. Shifrin N.S., and Chisholm S.W. Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J. Phycol. 17 (1981) 374-384
80. Trimborn S., Langer G., and Rost B., submitted for publication. Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi. Limnol. Oceanog.
81. Tyrrell T., and Mercio A. Emiliania huxleyi: bloom observations and the conditions that induce them. In: Thierstein H.R., and Young J.R. (Eds). Coccolithophores-From Molecular Processes To Global Impact (2004), Springer 75-97
82. Van Bleijswijk J.D.L., Kempers R.S., and Veldhuis M.J.W. Cell and growth characteristics of types A and B of Emiliania huxleyi (Prymnesiophyceae) as determined by flow cytometry and chemical analyses. J. Phycol. 30 (1994) 230-241
83. Van Dongen B.E., Schouten S., and Sinninghe Damsté J.S. Carbon isotope variability in monosaccharides and lipids of aquatic algae and terrestrial plants. Mar. Ecol. Prog. Ser. 232 (2002) 83-92
84. Van Emburg P.R., De Jong E.W., and Daems W.T. Immunochemical localization of a polysaccharide from biomineral structures (coccoliths) of Emiliania huxleyi. J. Ultrastruct. Mol. Struct. Res. 94 (1986) 246-259
85. Volkman J.K., Barrett S.M., Blackburn S.I., and Sikes E.L. Alkenones in Gephyrocapsa oceanica: implications for studies of paleoclimate. Geochim. Cosmochim. Acta 59 (1995) 513-520
86. Westbroek P., Brown C.W., Bleijswijk J.v., Brownlee C., Brummer G.J., Conte M., Egge J., Fernández E., Jordan R., Knappertsbusch M., Stefels J., Veldhuis M., Van der Wal P., and Young J. A model system approach to biological climate forcing. The example of Emiliania huxleyi. Glob. Planet. Change 8 (1993) 27-46
87. Williams P.J.l.B., and Egge J.K. The management and behaviour of the mesocosms. Est. Coast. Shelf Sci. 46 (1998) 3-14
88. Winter A., Jordan R.W., and Roth P.H. Biogeography of living coccolithophores in ocean waters. In: Winter A., and Siesser W.G. (Eds). Coccolithophores (1994), Cambridge University Press 161-177
89. Wong W., Sackett W.M., and Benedict C.R. Isotope fractionation in photosynthetic bacteria during carbon dioxide assimilation. Plant Physiol. 55 (1975) 475-479
90. 2 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 (2002) 55-70
91. Zondervan I., in press. Factors controlling the ratio of biogenic calcium carbonate to organic carbon production in coccolithophores. Deep-Sea Res. II.