Enhanced carbon overconsumption in response to increasing temperatures during a mesocosm experiment

Biogeosciences

Volumn 9, Issue 9, 2012, Pages 3531-3545

  Taucher, J ^a   Schulz, K G ^a   Dittmar, T ^b   Sommer, U ^a   Oschlies, A ^a   Riebesell, U ^a  

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

^b UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBON CYCLE; COMMUNITY STRUCTURE; DISSOLVED MATTER; EXPERIMENTAL STUDY; MESOCOSM; NITROGEN; PLANKTON; SEA SURFACE TEMPERATURE; TEMPERATURE EFFECT;

ATLANTIC OCEAN; BALTIC SEA;

EID: 84870800198     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-9-3531-2012     Document Type: Article

References (64)

1. Banse, K.: Uptake of inorganic carbon and nitrate by marine plankton and the Redfield ratio, Global Biogeochem. Cy., 8, 81-84, 1994. (Pubitemid 24402984)
2. Behrends, G.: Long-term investigations of seasonal mesozooplankton dynamics in Kiel Bight, Germany, Jurmala, Latvia (1993), Proc. 13th BMB Symp., 1996.
3. Berges, J. A., Varela, D. E., and Harrison, P. J.: Effects of temperature on growth rate, cell composition and nitrogen metabolism in the marine diatom Thalassiosira pseudonana (Bacillariophyceae), Mar. Ecol.-Prog. Ser., 225, 139-146, doi:10.3354/meps225139, 2002. (Pubitemid 34161492)
4. Biddanda, B. and Benner, R.: Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton, Limnol. Oceanogr., 42, 506-518, 1997. (Pubitemid 27422594)
5. Brock, T. D.: Calculating solar radiation for ecological studies, Ecol. Model., 14, 1-19, doi:10.1016/0304-3800(81)90011-9, 1981. (Pubitemid 12260653)
6. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B.: Toward a metabolic theory of ecology, Ecology, 85, 1771-1789, 2004. (Pubitemid 39188101)
7. Burd, A. B. and Jackson, G. A.: Particle Aggregation, in: Annual Review of Marine Science, Annual Review of Marine Science, Annual Reviews, Palo Alto, 1, 65-90, 2009.
8. Carlson, C. A.: Production and Removal Processes, in: Biogeochemistry of Marine Dissolved Organic Matter, edited by: Dennis, A. H. and Craig, A. C., Academic Press, San Diego, 91-151, 2002.
9. Carstensen, J., Conley, D. J., and Henriksen, P.: Frequency, composition, and causes of summer phytoplankton blooms in a shallow coastal ecosystem, the Kattegat, Limnol. Oceanogr., 49, 191-201, 2004. (Pubitemid 38154300)
10. Claquin, P., Probert, I., Lefebvre, S., and Veron, B.: Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae, Aquat. Microb. Ecol., 51, 1-11, doi:10.3354/ame01187, 2008. (Pubitemid 351785223)
11. Daufresne, M., Lengfellner, K., and Sommer, U.: Global warming benefits the small in aquatic ecosystems, P. Natl. Acad. Sci. USA, 106, 12788-12793, doi:10.1073/pnas.0902080106, 2009.
12. Delille, B., Harlay, J., Zondervan, I., Jacquet, S., Chou, L., Wollast, R., Bellerby, R. G. J., Frankignoulle, M., Borges, A. V., Riebe sell, 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, Gb2023, doi:10.1029/2004gb002318, 2005. (Pubitemid 41576422)
13. Dickson, A. G. and Millero, F. J.: A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media, Deep-Sea Res., 34, 1733-1743, doi:10.1016/0198-0149(87)90021-5, 1987.
14. Dittmar, T. and Paeng, J.: A heat-induced molecular signature in marine dissolved organic matter, Nat. Geosci., 2, 175-179, doi:10.1038/ngeo440, 2009.
15. Engel, A., Goldthwait, S., Passow, U., and Alldredge, A.: Temporal decoupling of carbon and nitrogen dynamics in a mesocosm diatom bloom, Limnol. Oceanogr., 47, 753-761, 2002. (Pubitemid 34527281)
16. Engel, A., Delille, B., Jacquet, S., Riebesell, U., Rochelle-Newall, E., Terbruggen, A., and Zondervan, I.: Transparent exopolymer particles and dissolved organic carbon production by Emiliania huxleyi exposed to different CO2 concentrations: a mesocosm experiment, Aquat. Microb. Ecol., 34, 93-104, 2004. (Pubitemid 39098358)
17. Engel, A., Handel, N.,Wohlers, J., Lunau, M., Grossart, H. P., Sommer, U., and Riebesell, U.: Effects of sea surface warming on the production and composition of dissolved organic matter during phytoplankton blooms: results from a mesocosm study, J. Plankton Res., 33, 357-372, doi:10.1093/plankt/fbq122, 2011.
18. Eppley, R. W.: Temperature and phytoplankton growth in sea, Fish. B.-NOAA, 70, 1063-1085, 1972.
19. Feng, Y. Y., Hare, C. E., Leblanc, K., Rose, J. M., Zhang, Y. H., DiTullio, G. R., Lee, P. A., Wilhelm, S. W., Rowe, J. M., Sun, J., Nemcek, N., Gueguen, C., Passow, U., Benner, I., Brown, C., and Hutchins, D. A.: Effects of increased pCO2 and temperature on the North Atlantic spring bloom, I. The phytoplankton community and biogeochemical response, Mar. Ecol.-Prog. Ser., 388, 13-25, doi:10.3354/meps08133, 2009.
20. Fileman, E., Petropavlovsky, A., and Harris, R.: Grazing by the copepods Calanus helgolandicus and Acartia clausi on the protozooplankton community at station L4 in the Western English Channel, J. Plankton Res., 32, 709-724, doi:10.1093/plankt/fbp142, 2010.
21. Finkel, Z. V., Beardall, J., Flynn, K. J., Quigg, A., Rees, T. A. V., and Raven, J. A.: Phytoplankton in a changing world: cell size and elemental stoichiometry, J. Plankton Res., 32, 119-137, doi:10.1093/plankt/fbp098, 2010.
22. Fry, B., Hopkinson, C. S., and Nolin, A.: Long-term decomposition of DOC from experimental diatom blooms, Limnol. Oceanogr., 41, 1344-1347, 1996.
23. Geider, R. J. and La Roche, J.: Redfield revisited: variability of C : N : P in marine microalgae and its biochemical basis, Eur. J. Phycol., 37, 1-17, doi:10.1017/s0967026201003456, 2002. (Pubitemid 34264641)
24. Goldman, J. C., Hansell, D. A., Dennett, M. R.: Chemical characterization of three large oceanic diatoms: potential impact on water column chemistry, Mar. Ecol.-Prog. Ser., 88, 257-270, 1992. (Pubitemid 24406320)
25. Hansell, D. A., Carlson, C. A., Repeta, D. J., and Schlitzer, R.: Dissolved organic matter in the ocean-A controversy stimulates new insights, Oceanography, 22, 202-211, 2009.
26. Hansen, H. P. and Koroleff, F.: Determination of nutrients, Methods of Seawater Analysis, Wiley-VCH Verlag GmbH, 159-228, 2007.
27. Hare, C. E., Leblanc, K., DiTullio, G. R., Kudela, R. M., Zhang, Y., Lee, P. A., Riseman, S., and Hutchins, D. A.: Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea, Mar. Ecol.-Prog. Ser., 352, 9-16, doi:10.3354/meps07182, 2007. (Pubitemid 351211770)
28. Harrison, P. J., Conway, H. L., Holmes, R. W., and Davis, C. O.: Marine diatoms grown in chemostats under silicate or ammonium limitation, 3. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida, Mar. Biol., 43, 19-31, 1977.
29. Hoppe, H. G., Breithaupt, P., Walther, K., Koppe, R., Bleck, S., Sommer, U., and Jurgens, K.: Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study, Aquat. Microb. Ecol., 51, 105-115, doi:10.3354/ame01198, 2008. (Pubitemid 351959710)
30. Hutchins, D. A., Fu, F. X., Zhang, Y., Warner, M. E., Feng, Y., Portune, K., Bernhardt, P. W., and Mulholland, M. R.: CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry, Limnol. Oceanogr., 52, 1293-1304, doi:10.4319/lo.2007.52.4.1293, 2007. (Pubitemid 47121544)
31. IPCC: Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, edited by: Parry, M. L., Canziani, O. F., Palutikof, J. P., van der Linden, P. J. and Hanson, C. E., Cambridge University Press, Cambridge, UK, 976 pp., 2007a.
32. IPCC: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change., edited by: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M. and Miller, H. L., Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 996 pp., 2007b.
33. J̈ahne, B., Heinz, G., and Dietrich, W.: Measurement of the Diffusion Coefficients of Sparingly Soluble Gases in Water, J. Geophys. Res., 92, 10767-10776, doi:10.1029/JC092iC10p10767, 1987.
34. K̈ahler, P. and Koeve, W.: Marine dissolved organic matter: can its C : N ratio explain carbon overconsumption?, Deep-Sea Res. Pt. I, 48, 49-62, 2001.
35. Keller, A. A., Oviatt, C. A., Walker, H. A., and Hawk, J. D.: Predicted impacts of elevated temperature on the magnitude of the winter-spring phytoplankton bloom in temperate coastal waters: A mesocosm study, Limnol. Oceanogr., 44, 344-356, 1999. (Pubitemid 29150783)
36. Kim, J. M., Lee, K., Shin, K., Yang, E. J., Engel, A., Karl, D. M., and Kim, H. C.: Shifts in biogenic carbon flow from particulate to dissolved forms under high carbon dioxide and warm ocean conditions, Geophys. Res. Lett., 38, L08612, doi:10.1029/2011gl047346, 2011.
37. Kuss, J., and Schneider, B.: Chemical enhancement of the CO2 gas exchange at a smooth seawater surface, Mar. Chem., 91, 165-174, doi:10.1016/j.marchem. 2004.06.007, 2004. (Pubitemid 39444368)
38. Lassen, M. K., Nielsen, K. D., Richardson, K., Garde, K., and Schluter, L.: The effects of temperature increases on a temperate phytoplankton community-A mesocosm climate change scenario, J. Exp. Mar. Biol. Ecol., 383, 79-88, doi:10.1016/j.jembe.2009.10.014, 2010.
39. Lewis, E. and Wallace, D. W. R.: Program developed for CO2 system calculations (Internet), ORNL/CDIAC-105, Oak Ridge (Tennessee): Carbon Dioxide Information Analysis Center, US Department of Energy, available at: http://cdiac.ornl.gov/ftp/co2sys (last access: October 2011), 1998.
40. Menden-Deuer, S. and Lessard, E. J.: Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton, Limnol. Oceanogr., 45, 569-579, 2000. (Pubitemid 30247467)
41. Montagnes, D. J. S. and Franklin, D. J.: Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: Reconsidering some paradigms, Limnol. Oceanogr., 46, 2008-2018, 2001.
42. Mopper, K., Zhou, J. A., Ramana, K. S., Passow, U., Dam, H. G., and Drapeau, D. T.: The role of surface-active carbohydrates in the flocculation of a diatom bloom in a mesocosm, Deep-Sea Res. Pt. II, 42, 47-73, 1995.
43. Moran, X. A. G., Sebastian, M., Pedros-Alio, C., and Estrada, M.: Response of Southern Ocean phytoplankton and bacterioplankton production to short-term experimental warming, Limnol. Oceanogr., 51, 1791-1800, 2006. (Pubitemid 44185730)
44. Moran, X. A. G., Lopez-Urrutia, A., Calvo-D́Iaz, A., and Li, W. K. W.: Increasing importance of small phytoplankton in a warmer ocean, Global Change Biol., 16, 1137-1144, doi:10.1111/j.1365-2486.2009.01960.x, 2010.
45. Muren, U., Berglund, J., Samuelsson, K., and Andersson, A.: Potential effects of elevated sea-water temperature on pelagic food webs, Hydrobiologia, 545, 153-166, doi:10.1007/s10750-005-2742-4, 2005. (Pubitemid 40938263)
46. Myklestad, S.: Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture, J. Exp. Mar. Biol. Ecol., 15, 261-274, doi:10.1016/0022-0981(74)90049-5, 1974.
47. O'Connor, M. I., Piehler, M. F., Leech, D. M., Anton, A., and Bruno, J. F.: Warming and Resource Availability Shift Food Web Structure and Metabolism, Plos Biol., 7, e1000178, doi:10.1371/journal.pbio.1000178, 2009.
48. Passow, U.: Transparent exopolymer particles (TEP) in aquatic environments, Prog. Oceanogr., 55, 287-333, 2002. (Pubitemid 35464708)
49. Riebesell, U., Schulz, K. G., Bellerby, R. G. J., Botros, M., Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J., and Zollner, E.: Enhanced biological carbon consumption in a high CO2 ocean, Nature, 450, 545-548, doi:10.1038/Nature06267, 2007. (Pubitemid 350190242)
50. Riebesell, U., Kortzinger, A., and Oschlies, A.: Sensitivities of marine carbon fluxes to ocean change, P. Natl. Acad. Sci. USA, 106, 20602-20609, doi:10.1073/pnas.0813291106, 2009.
51. Sharp, J. H.: Improved Analysis for "Particulate" Organic Carbon and Nitrogen from Seawater, Limnol. Oceanogr., 19, 984-989, 1974.
52. Smith, S. V.: Physical, chemical and biological characteristics of CO2 gas flux across the air-water interface, Plant Cell Environ., 8, 387-398, doi:10.1111/j.1365-3040.1985.tb01674.x, 1985.
53. Sommer, U. and Lengfellner, K.: Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom, Global Change Biol., 14, 1199-1208, doi:10.1111/j.1365-2486.2008.01571.x, 2008. (Pubitemid 351659545)
54. Sommer, U., Aberle, N., Engel, A., Hansen, T., Lengfellner, K., Sandow, M., Wohlers, J., Zollner, E., and Riebesell, U.: An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phytoand zooplankton, Oecologia, 150, 655-667, doi:10.1007/s00442- 006-0539-4, 2007. (Pubitemid 46005322)
55. Stoll, M. H. C., Bakker, K., Nobbe, G. H., and Haese, R. R.: Continuous-Flow Analysis of Dissolved Inorganic Carbon Content in Seawater, Anal. Chem., 73, 4111-4116, doi:10.1021/ac010303r, 2001. (Pubitemid 32830850)
56. Taucher, J. and Oschlies, A.: Can we predict the direction of marine primary production change under global warming?, Geophys. Res. Lett., 38, L02603, doi:10.1029/2010gl045934, 2011.
57. Thingstad, T. F., Hagstrom, A., and Rassoulzadegan, F.: Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop?, Limnol. Oceanogr., 42, 398-404, 1997. (Pubitemid 27422914)
58. Thompson, P. A., Guo, M.-X., and Harrison, P. J.: Effects of variation in temperature. I. On the biochemical compostion of eight species of marine phytoplankton, J. Phycol., 28, 481-488, doi:10.1111/j.0022-3646.1992.00481.x, 1992.
59. Toggweiler, J. R.: Carbon overconsumption, Nature, 363, 210-211, 1993.
60. Verity, P. G.: Effects of temperature, irradiance, and daylength on the marine diatom Leptocylindrus danicus Cleve. II. Excretion, J. Exp. Mar. Biol. Ecol., 55, 159-169, doi:10.1016/0022-0981(81)90109-x, 1981.
61. Wetz, M. S. and Wheeler, P. A.: Production and partitioning of organic matter during simulated phytoplankton blooms, Limnol. Oceanogr., 48, 1808-1817, 2003. (Pubitemid 37207587)
62. Wetz, M. S. and Wheeler, P. A.: Release of dissolved organic matter by coastal diatoms, Limnol. Oceanogr., 52, 798-807, 2007. (Pubitemid 46972314)
63. Wohlers, J., Engel, A., Zollner, E., Breithaupt, P., Jurgens, K., Hoppe, H. G., Sommer, U., and Riebesell, U.: Changes in biogenic carbon flow in response to sea surface warming, P. Natl. Acad. Sci. USA, 106, 7067-7072, doi:10.1073/pnas.0812743106, 2009.
64. Zlotnik, I. and Dubinsky, Z.: The effect of light and temperature on DOC excretion by phytoplankton, Limnol. Oceanogr., 34, 831-839, 1989.