Spring bloom community change modifies carbon pathways and C:N:P: Chl a stoichiometry of coastal material fluxes

Biogeosciences

Volumn 11, Issue 24, 2014, Pages 7275-7289

  Spilling, K ^a,b   Kremp, A ^a   Klais, R ^c   Olli, K ^c   Tamminen, T ^a  

^a FINNISH ENVIRONMENT INSTITUTE   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF TARTU   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL BLOOM; CHLOROPHYLL A; CLIMATE CHANGE; COMMUNITY COMPOSITION; COMMUNITY DYNAMICS; DIATOM; DISSOLVED ORGANIC CARBON; PARTICULATE ORGANIC CARBON; PHYTOPLANKTON; STOICHIOMETRY;

BACILLARIOPHYTA; DINOPHYCEAE;

EID: 84919792987     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-11-7275-2014     Document Type: Article

References (69)

1. Baird, M. E., Ralph, P. J., Rizwi, F., Wild-Allen, K., and Steven, A. D.: A dynamic model of the cellular carbon to chlorophyll ratio applied to a batch culture and a continental shelf ecosystem, Limnol. Oceanogr., 58, 1215-1226, 2013.
2. Banse, K.: Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in marine pelagial, Limnol. Oceanogr., 27, 1059-1071, 1982.
3. Behrenfeld, M. J. and Falkowski, P. G.: A consumer's guide to phy-toplankton primary productivity models, Limnol. Oceanogr., 42, 1479-1491, 1997.
4. Breton, E., Rousseau, V., Parent, J.-Y., Ozer, J., and Lancelot, C.: Hydroclimatic modulation of diatom/Phaeocystis blooms in nutrient-enriched Belgian coastal waters(North Sea), Limnol. Oceanogr., 51, 1401-1409, 2006.
5. Chan, A. T.: Comparative physiological study of marine diatoms and dinoflagellates in relation to irradiance and cell size, II, Relationship between photosynthesis, growth, and carbon/chlorophyll a ratio, J. Phycol., 16, 428-432, 1980.
6. Cloern, J. E., Grenz, C., and Vidergar-Lucas, L.: An empirical model of the phytoplankton chlorophyll: carbon ratio-the conversion factor between productivity and growth rate, Limnol. Oceanogr., 40, 1313-1321, 1995.
7. Collos, Y., Gagne, C., Laabir, M., Vaquer, A., Cecchi, P., and Souchu, P.: Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau Lagoon, Southern France, J. Phycol., 40, 96-103, 2004.
8. De La Rocha, C., Terbrueggen, A., Völker, C., and Hohn, S.: Response and recovery of Thalassiosira weissflogii to nitrogen and silicon starvation: growth rates, nutrient uptake, and C, Si, and N per cell, Mar. Ecol. Prog. Ser., 412, 57-68, 2010.
9. Dugdale, R. C. and Goering, J. J.: Uptake of new and regenerated forms of nitrogen in primary productivity, Limnol. Oceanogr., 12, 196-206, 1967.
10. Dunne, J. P., Sarmiento, J. L., and Gnanadesikan, A.: A synthesis of global particle export from the surface ocean and cycling through the ocean interior and on the seafloor, Global. Biogeochem. Cy., 21, GB4006, doi:10.1029/2006GB002907, 2007.
11. Eggers, S. L., Lewandowska, A. M., Barcelos e Ramos, J., Blanco-Ameijeiras, S., Gallo, F., and Matthiessen, B.: Community composition has greater impact on the functioning of marine phyto-plankton communities than ocean acidification, Global Change Biol., 20, 713-723, 2014.
12. 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.
13. Falkowski, P. G.: Rationalizing elemental ratios in unicellular algae, J. Phycol., 36, 3-6, 2000.
14. Falkowski, P. G. and Owens, T. G.: Effects of light intensity on photosynthesis and dark respiration in six species of marine phyto-plankton, Mar. Biol., 45, 289-295, 1978.
15. Field, C. B., Behrenfeld, M. J., Randerson, J. T., and Falkowski, P.: Primary production of the biosphere: integrating terrestrial and oceanic components, Science, 281, 237-240, 1998.
16. Geider, R. J., MacIntyre, H. L., and Kana, T. M.: A dynamic regulatory model of phytoplankton acclimation to light, nutrients and temperature, Limnol. Oceanogr., 43, 679-694, 1998.
17. Goldman, J., Hansell, D., and Dennett, M.: Chemical characterization of three large oceanic diatoms: potential impact on water column chemistry, Mar. Ecol. Prog. Ser., 88, 257-270, 1992.
18. Grasshoff, K., Ehrhardt, M., and Kremling, K.: Methods of seawater analysis, Verlag Chemie, Weinheim, 419 pp., 1983.
19. Hallegraeff, G. M.: Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge, J. Phycol., 46, 220-235, 2010.
20. Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., D'Agrosa, C., Bruno, J. F., Casey, K. S., Ebert, C., and Fox, H. E.: A global map of human impact on marine ecosystems, Science, 319, 948-952, 2008.
21. Harley, C. D., Randall Hughes, A., Hultgren, K. M., Miner, B. G., Sorte, C. J., Thornber, C. S., Rodriguez, L. F., Tomanek, L., and Williams, S. L.: The impacts of climate change in coastal marine systems, Ecol. Lett., 9, 228-241, 2006.
22. Heiskanen, A. S.: Factors governing sedimentation and pelagic nutrient cycles in the northern Baltic Sea, Monogr. Boreal. Env. Res., 8, 1-80, 1998.
23. Hinder, S. L., Hays, G. C., Edwards, M., Roberts, E. C., Walne, A. W., and Gravenor, M. B.: Changes in marine dinoflagellate and diatom abundance under climate change, Nature Climate Change, 2, 271-275, 2012.
24. Hoikkala, L.: Dynamics of dissolved organic matter and its bioavail-ability to heterotrophic bacteria in the Gulf of Finland, Northern Baltic Sea, University of Helsinki, 62 pp., 2012.
25. Kiørboe, T., Andersen, K. P., and Dam, H. G.: Coagulation efficiency and aggregate formation in marine phytoplankton, Mar. Biol., 107, 235-245, doi:10.1007/BF01319822, 1990.
26. Klais, R., Tamminen, T., Kremp, A., Spilling, K., and Olli, K.: Decadal-scale changes of dinoflagellates and diatoms in the anomalous Baltic Sea spring bloom, PLoS ONE, 6, e21567, doi:10.1371/journal.pone.0021567, 2011.
27. Klais, R., Tamminen, T., Kremp, A., Spilling, K., An, B. W., Hajdu, S., and Olli, K.: Spring phytoplankton communities shaped by interannual weather variability and dispersal limitation: Mechanisms of climate change effects on key coastal primary producers, Limnol. Oceanogr., 58, 753-762, 2013.
28. Kremp, A., Tamminen, T., and Spilling, K.: Dinoflagellate bloom formation in natural assemblages with diatoms: nutrient competition and growth strategies in Baltic spring phytoplankton, Aquat. Microb. Ecol., 50, 181-196, 2008.
29. Legrand, C. and Carlsson, P.: Uptake of high molecular weight dex-tran by the dinoflagellate Alexandrium catenella, Aquat. Microb. Ecol., 16, 81-86, 1998.
30. Leterme, S. C., Edwards, M., Seuront, L., Attrill, M., Reid, P., and John, A.: Decadal basin-scale changes in diatoms, dinoflagel-lates, and phytoplankton color across the North Atlantic, Limnol. Oceanogr., 50, 1244-1253, 2005.
31. Lignell, R., Heiskanen, A. S., Kuosa, H., Gundersen, K., Kuuppo-Leinikki, P., Pajuniemi, R., and Uitto, A.: Fate of a phytoplankton spring bloom-sedimentation and carbon flow in the planktonic food web in the northern Baltic, Mar. Ecol. Prog. Ser., 94, 239-252, 1993.
32. Litchman, E. and Klausmeier, C. A.: Trait-based community ecology of phytoplankton, Annu. Rev. Ecol. Evo. S., 39, 615-639, 2008.
33. Litchman, E., de Tezanos Pinto, P., Klausmeier, C. A., Thomas, M. K., and Yoshiyama, K.: Linking traits to species diversity and community structure in phytoplankton, Hydrobiol., 653, 15-28, 2010.
34. Marchal, O., Monfray, P., and Bates, N. R.: Spring-summer imbalance of dissolved inorganic carbon in the mixed layer of the north-western Sargasso Sea, Tellus B, 48, 115-134, 1996.
35. Mateus, M., Leitão, P., de Pablo, H., and Neves, R.: Is it relevant to explicitly parameterize chlorophyll synthesis in marine ecological models?, J. Mar. Sys., 94, S23-S33, 2012.
36. Menden-Deuer, S. and Lessard, E. J.: Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton, Limnol. Oceanogr., 45, 569-579, 2000.
37. Michaels, A. F., Bates, N. R., Buesseler, K. O., Carlson, C. A., and Knap, A. H.: Carbon-cycle imbalances in the Sargasso Sea, Nature, 372, 537-540, 1994.
38. Myklestad, S., Holm-Hansen, O., Vårum, K. M., and Volcani, B. E.: Rate of release of extracellular amino acids and carbohydrates from the marine diatom Chaetoceros affinis, J. Plankton. Res., 11, 763-773, 1989.
39. Niemi, Å.: Ecology of phytoplankton in the Tvärminne area, SW coast of Finland. II. Primary production and environmental conditions in the archipelago and the sea zone, Acta Botanica Fen-nica, 105, 1-73, 1975.
40. Niiranen, S., Yletyinen, J., Tomczak, M. T., Blenckner, T., Hjerne, O., MacKenzie, B. R., Müller-Karulis, B., Neumann, T., and Meier, H.: Combined effects of global climate change and regional ecosystem drivers on an exploited marine food web, Global Change Biol., 19, 3327-3342, 2013.
41. Pahlow, M.: Linking chlorophyll-nutrient dynamics to the Redfield N: C ratio with a model of optimal phytoplankton growth, Mar. Ecol. Prog. Ser., 287, 33-43, 2005.
42. Ptacnik, R., Solimini, A. G., Andersen, T., Tamminen, T., Brettum, P., Lepistö, L., Willén, E., and Rekolainen, S.: Diversity predicts stability and resource use efficiency in natural phytoplank-ton communities, P. Natl. Acad. Sci., 105, 5134-5138, 2008.
43. Quigg, A., Finkel, Z. V., Irwin, A. J., Rosenthal, Y., Ho, T.-Y., Reinfelder, J. R., Schofield, O., Morel, F. M., and Falkowski, P. G.: The evolutionary inheritance of elemental stoichiometry in marine phytoplankton, Nature, 425, 291-294, 2003.
44. Reid, P. C., Edwards, M., Hunt, H. G., and Warner, A. J.: Phyto-plankton change in the North Atlantic, Nature, 391, 546-546, 1998.
45. Ross, O. N. and Geider, R. J.: New cell-based model of photosynthesis and photo-acclimation: accumulation and mobilisation of energy reserves in phytoplankton, Mar. Ecol. Prog. Ser., 383, 53-71, 2009.
46. Rynearson, T., Richardson, K., Lampitt, R., Sieracki, M., Poulton, A., Lyngsgaard, M., and Perry, M.: Major contribution of diatom resting spores to vertical flux in the sub-polar North Atlantic, Deep Sea Res.-Pt I, 82, 60-71, 2013.
47. Sakshaug, E., Bricaud, A., Dandonneau, Y., Falkowski, P. G., Kiefer, D. A., Legendre, L., Morel, A., Parslow, J., and Taka-hashi, M.: Parameters of photosynthesis: definitions, theory and interpretation of results, J. Plankton. Res., 19, 1637-1670, 1997.
48. Sambrotto, R. N., Savidge, G., Robinson, C., Boyd, P., Takahashi, T., Karl, D. M., Langdon, C., Chipman, D., Marra, J., and Codis-poti, L.: Elevated consumption of carbon relative to nitrogen in the surface ocean, Nature, 363, 248-250, doi:10.1038/363248a0, 1993.
49. Sarthou, G., Timmermans, K. R., Blain, S., and Tréguer, P.: Growth physiology and fate of diatoms in the ocean: a review, J. Sea Res., 53, 25-42, 2005.
50. Sathyendranath, S., Stuart, V., Nair, A., Oka, K., Nakane, T., Bouman, H., Forget, M.-H., Maass, H., and Platt, T.: Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea, Mar. Ecol. Prog. Ser., 383, 73-84, 2009.
51. Schartau, M., Engel, A., Schröter, J., Thoms, S., Völker, C., and Wolf-Gladrow, D.: Modelling carbon overconsumption and the formation of extracellular particulate organic carbon, Biogeo-sciences, 4, 433-454, doi:10.5194/bg-4-433-2007, 2007.
52. Sharp, J. H., Benner, R., Bennett, L., Carlson, C. A., Dow, R., and Fitzwater, S. E.: Re-evaluation of high temperature combustion and chemical oxidation measurements of dissolved organic carbon in seawater, Limnol. Oceanogr., 38, 1774-1782, 1993.
53. Smayda, T. J. and Reynolds, C. S.: Community assembly in marine phytoplankton: application of recent models to harmful dinoflag-ellate blooms, J. Plankton. Res., 23, 447-461, 2001.
54. Solórzano, L. and Sharp, J. H.: Determination of total dissolved phosphorus and particulate phosphorus in natural waters, Lim-nol. Oceanogr., 25, 754-758, 1980.
55. Spilling, K. and Lindström, M.: Phytoplankton life cycle transformation lead to species-specific effects on sediment processes in the Baltic Sea, Cont. Shelf Res., 28, 2488-2495, 2008.
56. Spilling, K. and Markager, S.: Ecophysiological growth characteristics and modeling of the onset of the spring bloom in the Baltic Sea, J. Mar. Sys., 73, 323-337, 2008.
57. Staats, N., Stal, L. J., and Mur, L. R.: Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions, J. Exp. Mar. Biol. Ecol., 249, 13-27, 2000.
58. Stockenreiter, M., Haupt, F., Graber, A. K., Seppälä, J., Spilling, K., Tamminen, T., and Stibor, H.: Functional group richness: implications of biodiversity for light use and lipid yield in microalgae, J. Phycol., 49, 838-847, 2013.
59. Striebel, M., Behl, S., and Stibor, H.: The coupling of biodiversity and productivity in phytoplankton communities: consequences for biomass stoichiometry, Ecology, 90, 2025-2031, 2009.
60. Suikkanen, S., Hakanen, P., Spilling, K., and Kremp, A.: Allelo-pathic effects of Baltic Sea spring bloom dinoflagellates on co-occurring phytoplankton, Mar. Ecol. Prog. Ser., 439, 45-55, 2011.
61. Sun, J. and Liu, D.: Geometric models for calculating cell biovolume and surface area for phytoplankton, J. Plankton. Res., 25, 1331-1346, 2003.
62. Tamminen, T.: Nitrate and ammonium depletion rates and preferences during a Baltic spring bloom, Mar. Ecol. Prog. Ser., 120, 123-133, 1995.
63. Tamminen, T. and Andersen, T.: Seasonal phytoplankton nutrient limitation patterns as revealed by bioassays over Baltic Sea gradients of salinity and eutrophication, Mar. Ecol. Prog. Ser., 340, 121-138, 2007.
64. Taylor, A. H., Geider, R. J., and Gilbert, F. J. H.: Seasonal and latitudinal dependencies of phytoplankton carbon-to-chlorophyll a ratios: results of a modelling study, Mar. Ecol. Prog. Ser., 152, 51-66, 1997.
65. Tillmann, U., Alpermann, T., John, U., and Cembella, A.: Allelo-chemical interactions and short-term effects of the dinoflagel-late Alexandrium on selected photoautotrophic and heterotrophic protists, Harmful Algae, 7, 52-64, 2008.
66. Toggweiler, J.: Vanishing in Bermuda, Nature, 372, 505-506, 1994.
67. Underwood, G. J. C., Boulcott, M., Raines, C. A., and Waldron, K.: Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production, J. Phycol., 40, 293-304, doi:10.1111/j.1529-8817.2004.03076.x, 2004.
68. Vehmaa, A., Kremp, A., Tamminen, T., Hogfors, H., Spilling, K., and Engström-Öst, J.: Copepod reproductive success in spring-bloom communities with modified diatom and di-noflagellate dominance, ICES J. Mar. Sci., 69, 351-357, doi:10.1093/icesjms/fsr138, 2011.
69. Worm, B., Barbier, E. B., Beaumont, N., Duffy, J. E., Folke, C., Halpern, B. S., Jackson, J. B., Lotze, H. K., Micheli, F., and Palumbi, S. R.: Impacts of biodiversity loss on ocean ecosystem services, Science, 314, 787-790, 2006.