Impact of CO2 enrichment on organic matter dynamics during nutrient induced coastal phytoplankton blooms

Journal of Plankton Research

Volumn 36, Issue 3, 2014, Pages 641-657

  Engel, Anja ^a,b   Piontek, Judith ^a,b   Grossart, Hans Peter ^c,d   Riebesell, Ulf ^a   Schulz, Kai G ^a,e   Sperling, Martin ^a,b  

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

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

^c Department Experimental Limnology IGB Neuglobsow ^*  (Germany)

^d UNIVERSITY OF POTSDAM   (Germany)

^e SOUTHERN CROSS UNIVERSITY   (Australia)

Author keywords

mesocosm; ocean acidification; organic matter; phytoplankton; TEP

Indexed keywords

ABUNDANCE; ACIDIFICATION; ALGAL BLOOM; BACTERIUM; CARBON DIOXIDE ENRICHMENT; MARINE ECOSYSTEM; MESOCOSM; ORGANIC MATTER; PHYTOPLANKTON; SPATIOTEMPORAL ANALYSIS;

ATLANTIC OCEAN; BALTIC SEA;

EID: 84900512628     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbt125     Document Type: Article

References (72)

1. Alldredge, A. L., Passow, U. and Logan, B. E. (1993) The abundance and significance of a class of large. Transparent organic particles in the ocean. Deep-Sea Res., 40, 1131-1140.
2. Anderson, T. R. and Williams, P. J. L. (1998) Modelling the seasonal cycle of dissolved organic carbon at station E-1 in the English Channel. Estuarine Coastal Shelf Sci., 46, 93-109.
3. Arrigo, K. R. (2007) Carbon cycle. Marine manipulations. Nature, 450, 491-492.
4. Bellerby, R. G. J., Schulz, K. G., Riebesell, U. et al. (2008) Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences, 5, 1517-1527.
5. Benner, R. (2002) Chemical composition and reactivity. In Hansell, D. A. and Carlson, C. (eds), Biogeochemistry of Marine Dissolved Organic Matter. Academic Press, Elsevier Science, pp 59-90.
6. Blackford, J. C. and Gilbert, F. J. (2007) pH variability and CO2 induced acidification in the North Sea. J. Mar. Syst., 64, 229-241.
7. Borchard, C. and Engel, A. (2012) Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions. Biogeosciences, 9, 3405-3423.
8. Bronk, D. A. (2002) Dynamics of DON. In Hansell, D. A. and Carlson, C. (eds), Biogeochemistry of Marine Dissolved Organic Matter. Academic Press, Elsevier Science, pp 59-90.
9. Cai, W. J., Hu, X., Huang, W. J. et al. (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci., 4, 766-770.
10. Chrost, R. J., Hoppe, H., Grossart, H. P. et al. (1998) The significance of limnetic organic aggregates (lake snow) for the sinking flux of particulate organic matter in a large lake. Aquatic Microb. Ecol., 15, 115-125.
11. Dickson, A. G., Sabine, C. L. and Christian, J. R. (eds) (2007) Guide to Best Practices for Ocean CO2 Measurements. PICES Press, Special Publication 3.
12. Engel, A. (2000) The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (alpha) during the decline of a diatom bloom. J. Plankton Res., 22, 485-497.
13. Engel, A. (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. J. Plankton Res., 24, 49-53.
14. Engel, A. and Passow, U. (2001) Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Mar. Ecol. Prog. Ser., 219, 1-10.
15. Engel, A. and Händel, N. (2011) A novel protocol for determining the concentration and composition of sugars in particulate and in high molecular weight dissolved organic matter (HMW-DOM) in seawater. Mar. Chem., 127, 180-191.
16. Engel, A., Händel, N., Wohlers, J. et al. (2011) 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.
17. Engel, A., Harlay, J., Piontek, J. et al. (2012) Contribution of combined carbohydrates to dissolved and particulate organic carbon after the spring bloom in the northern Bay of Biscay (North-Eastern Atlantic Ocean). Cont. Shelf Res., 45, 42-53.
18. Engel, A., Zondervan, I., Aerts, K. et al. (2005) Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol. Oceanogr., 50, 493-507.
19. Feely, R. A., Doney, S. C. and Cooley, S. R. (2009) Ocean acidification. Present conditions and future changes in a high-CO2 world. Oceanography, 22, 36-47.
20. Gärdes, A., Iversen, M. H., Grossart, H.-P. et al. (2011) Diatomassociated bacteria are required for aggregation of Thalassiosira weissflogii. ISMEJ, 5, 436-445.
21. Gehlen, M., Gruber, N., Gangsto, R. et al. (2011) Biogeochemical consequences of ocean acidification and feedbacks to the earth system. In Gattuso, J. P. and Hansson, L. (eds), Ocean Acidification. Oxford University Press, Oxford, UK, pp 99-121.
22. Grossart, H. P., Simon, M. and Logan, B. E. (1997) Formation of macroscopic organic aggregates (lake snow) in a large lake: The significance of transparent exopolymer particles, phytoplankton, and zooplankton. Limnol. Oceanogr., 42, 1651-1659.
23. Hansen, H. P. and Koroleff, F. (1999) Determination of Nutrients. Methods of Seawater Analysis, 3rd edn. Grasshoff, K., Kremling, K. and Ehrhardt, M. (eds),Wiley,Weinheim.
24. Havenhand, J., Dupont, S. and Quinn, G. P. (2011) Design ocean acidification experiments to maximize inference. In Gattuso, J.-P. and Hansson, L. (eds), Ocean Acidification. OxfordUniversity Press, Oxford,UK.
25. Hofmann, G. E., Smith, J. E., Johnson, K. S. et al. (2011) High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE, 6, 12.
26. Hoppe, H.-G. (1983) Significance of exoenzymatic activities in the ecology of brackish water-measurements by means of methylumbelliferyl- substrates. Mar. Ecol. Prog. Ser., 11, 299-308.
27. Ittekkot, V., Brockmann, U., Michaelis, W. et al. (1981) Dissolved free and combined carbohydrates during a phytoplankton bloom in the northern North sea. Mar. Ecol. Prog. Ser., 4, 299-305.
28. Jackson, G. A. (1990) A model of the formation of marine algal flocs by physical coagulation processes. Deep-Sea Res. A, 37, 1197-1211.
29. Joint, I., Doney, S and Karl, D. (2011) Will ocean acidification affect marine microbes? ISMEJ, 5, 1-7.
30. Kahl, L. A., Vardi, A. and Schofield, O. (2008) Effects of phytoplankton physiology on export flux. Mar. Ecol. Prog. Ser., 354, 3-19.
31. Kaehler, P and Koeve, W. (2001) Marine dissolved organic matter: Can its C:N ratio explain carbon overconsumption? Deep-Sea Res. I, 48, 49-62.
32. Kim, J. M., Lee, K., Shin, K. et al. (2011) Shifts in biogenic carbon flow from particulate to dissolved forms under high carbon dioxide and warm ocean conditions. Geophys. Res. Lett., 38, doi:10.1029/2011GL047346
33. Kirchman, D. L., Meon, B., Ducklow, H. W. et al. (2001) Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone. Antarctica. Deep Sea Res, II, 48, 19-20.
34. Kroeker, K. J., Kordas, R. L., Crim, R. N. et al. (2010) Meta-Analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett., 13, 1419-1434.
35. Kulinski, K. and Pempkowiak, J. (2008) Dissolved organic carbon in the southern Baltic Sea: Quantification of factors affecting its distribution. Estuarine Coastal Shelf Sci., 78, 38-44.
36. Lewis, E. L. (1980) The practical salinity scale 1978 and its antecedents. IEEE J. Ocean Eng., 5, 3-8.
37. Leppäranta, M. and Myrberg, K. (2009) Physical Oceanography of the Baltic Sea. Springer-Praxis Books in Geophysical Sciences.
38. Lindroth, P. and Mopper, K. (1979) High performance liquid chromatography determination of subpicomole amounts of amino acids by precolumn fluorescence derivatisation with OPA. Anal. Chem., 51, 1667-1674.
39. Liu, J.W.,Weinbauer, M. G., Maier, C. et al. (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat. Microb. Ecol., 61, 291-305.
40. Lueker, T. J., Dickson, A. G. and Keeling, C. D. (2000) Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: Validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Mar. Chem., 70, 105-119.
41. Mari, X (2008) Does ocean acidification induce an upward flux of marine aggregates? Biogeosciences, 5, 1023-1031.
42. Mari, X. and Robert, M. (2008) Metal induced variations of TEP sticking properties in the southwestern lagoon of New Caledonia. Mar. Chem., 110, 98-108.
43. Mari, X., Migon, C. and Nicolas, E. (2009) Reactivity of transparent exopolymeric particles: A key parameter of trace metal cycling in the lagoon of Noumea, New Caledonia. Mar. Pollut. Bull., 58, 1874-1879.
44. Mari, X., Torreton, J. P., Claire, B. T. T. et al. (2012) Aggregation dynamics along a salinity gradient in the Bach Dang estuary, North Vietnam. Estuarine Coastal Shelf Sci., 96, 151-158.
45. Mehrbach, C., Culberson, C. H., Hawley, J. E. et al. (1973) Measurements of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr., 18, 897-907.
46. Melzner, F., Thomsen, J., Koeve, W. et al. (2012) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar. Biol., DOI:10.1007/s00227-012-1954-1.
47. Omstedt, A., Edman, M., Anderson, L. G. et al. (2010) Factors influencing the acid-base (pH) balance in the Baltic Sea: A sensitivity analysis. Tellus B, 62, 280-295.
48. Omstedt, A., Gustafsson, E. and Wesslander, K. (2009) Modelling the uptake and release of carbon dioxide in the Baltic Sea surface water. Cont. Shelf Res., 29, 870-885.
49. Oschlies, A., Schulz, K. G., Riebesell, U. et al. (2008) Simulated 21st century's increase in oceanic suboxia by CO2-enhanced biotic carbon export. Global Biogeochem. Cycles, 22, 1-10.
50. Passow, U. (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr., 55, 287-333.
51. Passow, U. (2011) The abiotic formation of TEP under ocean acidification scenarios. Mar. Chem., 129, 72-80.
52. Passow, U. and Alldredge, A. L. (1995) A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP) in the ocean. Limnol. Oceanogr., 40, 1326-1335.
53. Passow, U. and Alldredge, A. L. (1995) Agggregation of a diatom bloom in a mesocosms-The role of transparent exopolymer particles (TEP). Deep-Sea Res. II, 4, 99-109.
54. Passow, U., Shipe, R. F., Murray, A. et al. (2001) The origin of transparent exopolymer particles (TEP) and their role in the sedimentation of particulate matter. Cont. Shelf Res., 21, 327-346.
55. Piontek, J., Händel, N., de Bodt, C. et al. (2011) The utilization of polysaccharides by heterotrophic bacterioplankton in the Bay of Biscay (North Atlantic Ocean). J. Plankton Res., 33, 1719-1735.
56. Piontek, J., Lunau, M.,Händel, N. et al. (2010) Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences, 7, 1615-1624.
57. Qian, J. and Mopper, K. (1996) An automated, high performance, high temperature combustion dissolved organic carbon analyzer. Anal. Chem., 68, 3090-3097.
58. Riebesell, U., Czerny, J., von Bröckel, K. et al. (2013) Technical Note: A mobile sea-going mesocosm system-new opportunities for ocean change research. Biogeosciences, 10, 1835-1847.
59. Riebesell, U., Schulz, K. G., Bellerby, R. G. J. et al. (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature, 450, 545-U510.
60. Riebesell, U. and Tortell, P. D. (2011) Effects of ocean acidification on pelagic organisms and ecosystems. In Gattuso, J.-P. and Hansson, L. (eds), Ocean Acidification. Oxford University Press, Oxford, UK.
61. Sarmiento, J. L. and Gruber, N. (2006) Ocean Biogeochemical Dynamics. Princeton University press, Princeton, NJ, 526pp.
62. Schartau, M., Engel, A., Schröter, J. et al. (2007) Modelling carbon overconsumption and the formation of extracellular particulate organic carbon. Biogeosciences, 4, 433-454.
63. Schulz, K. G. and Riebesell, U. (2012) Diurnal changes in seawater carbonate chemistry speciation at increasing atmospheric carbon dioxide. Mar. Biol., doi:10.1007/s00227-012-1965-y.
64. Sharp, J. H. (1974) Improved analysis for 'particulate' organic carbon and nitrogen from seawater. Limnol. Oceanogr., 19, 984-989.
65. Simon, M., Grossart, H. P., Schweitzer, B. et al. (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat.Microb. Ecol., 28, 175-211.
66. Skoog, A. and Benner, R. (1997) Aldoses in various size fractions of marine organic matter. Implications for carbon cycling. Limnol. Oceanogr., 42, 1803-1813.
67. Smith, D. C., Simon, M., Alldredge, A. L. et al. (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature, 359, 139-142.
68. Stoderegger, K. E. and Herndl, G. J. (1999) Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar. Ecol. Prog. Ser., 189, 9-16.
69. Thingstad, T. F., Hagstrom, A. and Rassoulzadegan, F. (1997) Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop? Limnol. Oceanogr., 42, 398-404.
70. Thornton, D. C. O. (2009) Effect of low pH on carbohydrate production by a marine planktonic diatom (Chaetoceros muelleri). Res. Lett. Ecol., doi:10.1155/2009/105901.
71. Welschmeyer, N. A. (1994) Fluometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr., 39, 1985-1992.
72. Williams, P. J. le B. (1995) Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in comparison with changes in particulate material and the consequential effect on net C/N assimilation ratios. Mar. Chem., 51, 17-29.