Biogeosciences
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2009
10.5194/bg-6-3131-2009
http://www.biogeosciences.net/6/3131/2009/
http://www.biogeosciences.net/6/3131/2009/bg-6-3131-2009.html
http://www.biogeosciences.net/6/3131/2009/bg-6-3131-2009.pdf
3131
3147
2009-12-21
Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages
J. M. Rose
Y. Feng
G. R. DiTullio
R. B. Dunbar
C. E. Hare
P. A. Lee
M. Lohan
M. Long
W. O. Smith Jr.
B. Sohst
S. Tozzi
Y. Zhang
D. A. Hutchins
dahutch@usc.edu
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
Biology Department, University of Southern California, Los Angeles, CA 90089-0371, USA
Hollings Marine Laboratory, College of Charleston, Charleston, SC 29412, USA
Department of Environmental Earth Systems Science, Stanford University, Stanford, CA 94305-2115, USA
College of Marine Studies, University of Delaware, Lewes, DE 19958, USA
School of Earth, Ocean and Environmental Sciences, University of Plymouth, Plymouth PL4 8AA, UK
Virginia Institute of Marine Science, College of William and Mary, Gloucester Pt, VA 23602, USA
Department of Ocean, Earth and Atmospheric Sciences, Old Dominion University, Norfolk, VA 23529, USA
Iron availability and temperature are important limiting factors for the
biota in many areas of the world ocean, and both have been predicted to
change in future climate scenarios. However, the impacts of combined changes
in these two key factors on microbial trophic dynamics and nutrient cycling
are unknown. We examined the relative effects of iron addition (+1 nM) and
increased temperature (+4°C) on plankton assemblages of the Ross Sea,
Antarctica, a region characterized by annual algal blooms and an active
microbial community. Increased iron and temperature individually had
consistently significant but relatively minor positive effects on total
phytoplankton abundance, phytoplankton and microzooplankton community
composition, as well as photosynthetic parameters and nutrient drawdown.
Unexpectedly, increased iron had a consistently negative impact on
microzooplankton abundance, most likely a secondary response to changes in
phytoplankton community composition. When iron and temperature were
increased in concert, the resulting interactive effects were greatly
magnified. This synergy between iron and temperature increases would not
have been predictable by examining the effects of each variable
individually. Our results suggest the possibility that if iron availability
increases under future climate regimes, the impacts of predicted temperature
increases on plankton assemblages in polar regions could be significantly
enhanced. Such synergistic and antagonistic interactions between individual
climate change variables highlight the importance of multivariate studies
for marine global change experiments.
Allen, A. E., LaRoche, J., Maheswari, U., Lommer, M., Schauer, N., Lopez, P. J., Finazzi, G., Fernie, A. R., and Bowler, C.: Whole-cell response of the pennate diatom \textitPhaeodactylum tricornutum to iron starvation, Proc Natl Acad Sci USA, 105, 10438–10443, 2008.
Alley, R., Berntsen, T., Bindoff, N. L., Chen, Z., Chidthaisong, A., Friedlingstein, P., Gregory, J., Hegerl, G., Heimann, M., Hewitson, B., Hoskins, B., Joos, F., Jouzel, J., Kattsov, V., Lohmann, U., Manning, M., Matsuno, T., Molina, M., Nicholls, N., Overpeck, J., Qin, D., Raga, G., Ramaswamy, V., Ren, J., Rusticucci, M., Solomon, S., Somerville, R., Stocker, T. F., Stott, P., Stouffer, R. J., Whetton, P., Wood, R. A., and Wratt, D.: Climate change 2007: The physical science basis. Summary for policymakers, Intergovernmental Panel on Climate Change, Geneva, 2007.
Arrigo, K. R., Robinson, D. H., Worthen, D. L., Dunbar, R. B., DiTullio, G. R., VanWoert, M., and Lizotte, M. P.: Phytoplankton community structure and the drawdown of nutrients and CO<sub>2</sub> in the Southern Ocean, Science, 283, 365–367, 1999.
Arrigo, K. R., Ditullio, G. R., Dunbar, R. B., Robinson, D. H., VanWoert, M., Worthen, D. L., and Lizotte, M. P.: Phytoplankton taxonomic variability in nutrient utilization and primary production in the Ross Sea, J. Geophys Res., 105, 8827–8846, 2000.
Bertrand, E. M., Saito, M. A., Rose, J. M., Riesselman, C. R., Lohan, M. C., Noble, A. E., Lee, P. A., and DiTullio, G. R.: Vitamin B$_12$ and iron colimitation of phytoplankton growth in the Ross Sea, Limnol. Oceanogr., 52, 1079–1093, 2007.
Blank, G. S., Robinson, D. H., and Sullivan, C. W.: Diatom mineralization of silicic acid VIII. metabolic requirements and the timing of protein synthesis, J. Phycol., 22, 382–389, 1986.
Boyd, P. W., LaRoche, J., Gall, M., Frew, R. D., and McKay, R.: Role of iron, light and silicate in controlling algal biomass in subantarctic waters SE of New Zealand, J. Geophys Res., 104, 13391–13404, 1999.
Boyd, P. W., Watson, A. J., Law, C. S., Abraham, E. R., Trull, T., Murdoch, R., Bakker, D. C. E., Bowie, A. R., Buesseler, K. O., Chang, H., Charette, M., Croot, P., Downing, K., Frew, R., Gall, M., Hadfield, M., Hall, J., Harvey, M., Jameson, G., LaRoche, J., Liddicoat, M., Ling, R., Maldonado, M. T., McDay, R. M., Nodder, S., Pickmere, S., Pridmore, R., Rintoul, S., Safi, K., Sutton, P., Strzepek, R., Tanneberger, K., Turner, S., Waite, A., and Zeldis, J.: A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization, Nature, 407, 695–702, 2000.
Boyd, P. W., Crossley, C., DiTullio, G. R., Griffiths, F. B., Hutchins, D. A., Queguiner, B., Sedwick, P. N., and Trull, T. W.: Control of phytoplankton growth by iron supply and irradiance in the subantarctic Southern Ocean: experimental results from the SAZ project, J. Geophys Res., 106, 31573–31583, 2001.
Boyd, P. W. and Doney, S. C.: Modelling regional responses by marine pelagic ecosystems to global climate change, Geophys. Res. Lett., 29, 1806, doi:10.1029/2001GL014130, 2002.
Bruland, K. W., Rue, E. L., Smith, G. J., and DiTullio, G. R.: Iron, macronutrients and diatom blooms in the Peru upwelling regime: brown and blue waters of Peru, Mar. Chem., 93, 81–103, 2005.
Brzezinski, M. A. and Nelson, D. M.: The annual silica cycle in the Sargasso Sea near Bermuda, Deep-Sea Res. I, 42, 1215–1237, 1995.
Bucciarelli, E., Pondaven, P., and Sarthou, G.: Effects of an iron-light co-limitation on the elemental composition (Si, C, N) of the marine diatoms \textitThalassiosira oceanica and \textitDitylum brightwellii, Biogeosciences Discuss., 6, 7175–7205, 2009.
Buck, K. N., Lohan, M. C., Berger, C. J. M., and Bruland, K. W.: Dissolved iron speciation in two distinct river plumes and an estuary: Implications for riverine iron supply, Limnol. Oceanogr., 52, 843–855, 2007.
Campbell, L.: Flow cytometric analysis of autotrophic picoplankton, in: Methods in Microbiology, Academic Press, 317–341, 2001.
Caron, D. A., Dennett, M. R., Lonsdale, D. J., Moran, D. M., and Shalapyonok, L.: Microzooplankton herbivory in the Ross Sea, Antarctica, Deep-Sea Res. II, 47, 3249–3272, 2000.
Clarke, K. R. and Green, R. H.: Statistical design and analysis for a 'biological effects' study, Mar. Ecol-Prog. Ser., 46, 213–226, 1988.
Clarke, K. R.: Non-parametric multivariate analyses of changes in community structure, Aust. J. Ecol., 18, 117–143, 1993.
Clarke, K. R. and Warwick, R. M.: Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition, Plymouth Marine Laboratory, Plymouth, UK, 2001.
Clarke, K. R. and Gorley, R. N.: Primer v6: user manual/tutorial, Primer-E Ltd, Plymouth, 190~pp., 2006.
Coale, K. H., Wang, X., Tanner, S. J., and Johnson, K. S.: Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170° W, Deep-Sea Res. II, 50, 635–653, 2003.
Coale, K. H., Johnson, K. S., Chavez, F. P., Buesseler, K. O., Barber, R. T., Brzezinski, M. A., Cochlan, W. P., Millero, F. J., Falkowski, P. G., Bauer, J. E., Wanninkhof, R. H., Kudela, R. M., Altabet, M. A., Hales, B. E., Takahashi, T., Landry, M. R., Bidigare, R. R., Wang, X., Chase, Z., Strutton, P. G., Friederich, G. E., Gorbunov, M. Y., Lance, V. P., Hilting, A. K., Hiscock, M. R., Demarest, M., Hiscock, W. T., Sullivan, K. F., Tanner, S. J., Gordon, R. M., Hunter, C. N., Elrod, V. A., Fitzwater, S. E., Jones, J. L., Tozzi, S., Koblizek, M., Roberts, A. E., Herndon, J., Brewster, J., Ladizinsky, N., Smith, G., Cooper, D., Timothy, D., Brown, S. L., Selph, K. E., Sheridan, C. C., Twining, B. S., and Johnson, Z. I.: Southern Ocean iron enrichment experiment: carbon cycling in high- and low-Si waters, Science, 304, 408–414, 2004.
De Baar, H. J. W., Buma, A. G. J., Nolting, R. F., Cadee, G. C., Jacques, G., and Treguer, P. J.: On iron limitation of the Southern Ocean: experimental observations in the Weddell and Scotia Seas, Mar. Ecol-Prog. Ser., 65, 105–122, 1990.
del Valle, D. A., Kieber, D. J., Toole, D. A., Bisgrove, J., and Kiene, R. P.: Dissolved DMSO production via biological and photochemical oxidation of dissolved DMS in the Ross Sea, Antarctica, Deep-Sea Res. I, 56, 166–177, 2009.
Dennett, M. R., Mathot, S., Caron, D. A., Smith Jr., W. O., and Lonsdale, D. J.: Abundance and distribution of phototrophic and heterotrophic nano- and microplankton in the southern Ross Sea, Deep-Sea Res. II, 48, 4019–4037, 2001.
DiTullio, G. R. and Smith Jr., W. O.: Relationship between dimethylsulfide and phytoplankton pigment concentrations in the Ross Sea, Antarctica, Deep-Sea Res. I, 42, 873–892, 1995.
DiTullio, G. R. and Smith Jr., W. O.: Spatial patterns in phytoplankton biomass and pigment distributions in the Ross Sea, J. Geophys. Res., 101, 18467–18478, 1996.
Donat, J. R. and Bruland, K. W.: Direct determination of dissolved cobalt and nickel in seawater by differential pulse cathodic stripping voltammetry preceded by adsorptive collection of cyclohexane-1, 2-dione dioxime complexes, Anal. Chem., 60, 240–244, 1988.
Ellwood, M. and Van den Berg, C. M. G.: Zinc speciation in the Northeastern Atlantic Ocean, Mar. Chem., 68, 295–306, 2000.
Eppley, R. W.: Temperature and phytoplankton growth in the sea, Fish. Bull., 70, 1063–1085, 1972.
Feng, Y., Hare, C. E., Leblanc, K., DiTullio, G. R., Lee, P. A., Wilhelm, S. W., Sun, J., Rose, J. M., Nemcek, N., Benner, I., and Hutchins, D. A.: The effects of increased pCO<sub>2</sub> and temperature on the North Atlantic Spring Bloom: I. The phytoplankton community and biogeochemical response, Mar. Ecol-Prog. Ser., 388, 13–25, 2009.
Firme, G. F., Rue, E. L., Weeks, D. A., Bruland, K. W., and Hutchins, D. A.: Spatial and temporal variability in phytoplankton iron limitation along the California coast and consequences for Si, N, and C biogeochemistry, Global Biogeochem. Cy., 17, 1016, doi:10.1029/2001GB001824, 2003.
Fitzwater, S. E., Johnson, K. S., Gordon, R. M., Coale, K. M., and Smith, W. O., Jr: Trace metal concentrations in the Ross Sea and their relationship with nutrients and phytoplankton growth, Deep-Sea Res. II, 47, 3159–3179, 2000.
Garrison, D. L.: An overview of the abundance and role of protozooplankton in Antarctic waters, J. Marine Syst., 2, 317–331, 1991.
Garrison, D. L. and Gowing, M. M.: Protozooplankton, in: Antarctic Microbiology, edited by: Friedmann, E. I., Wiley-Liss, New York, 123–166, 1993.
Garrison, D. L., Gibson, A., Kunze, H., Gowing, M. M., Vickers, C. L., Mathot, S., and Bayre, R. C.: The Ross Sea Polynya Project: diatom- and \textitPhaeocystis-dominated phytoplankton assemblages in the Ross Sea, Antarctica, 1994 and 1995, in: Biogeochemistry of the Ross Sea, edited by: DiTullio, G. R. and Dunbar, R. B., American Geophysical Union, Washington, DC, 53–76, 2003.
Genty, B., Briantais, J. M., and Baker, N. R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 990, 87–92, 1989.
Gervais, F., Riebesell, U., and Gorbunov, M. Y.: Changes in primary productivity and chlorophyll $a$ in response to iron fertilization in the Southern Polar Frontal Zone, Limnol. Oceanogr., 47, 1324–1335, 2002.
Goldman, J. C. and Carpenter, E. J.: A kinetic approach to the effect of temperature on algal growth, Limnol. Oceanogr., 19, 756–766, 1974.
Goldman, J. C.: Temperature effects on steady-state growth, phosphorus uptake, and the chemical composition of a marine phytoplankter, Microb. Ecol., 5, 153–166, 1979.
Green, R. M., Kolber, Z. S., Swift, D. G., Tindale, N. W., and Falkowski, P. G.: Physiological limitation of phytoplankton photosynthesis in the Eastern Equatorial Pacific determined from variability in the quantum yield of fluorescence, Limnol. Oceanogr., 39, 1061–1074, 1994.
Haberman, K. L., Quetin, L. B., and Ross, R. M.: Diet of the Antarctic krill (\textitEuphausia superba, Dana): I. Comparisons of grazing on \textitPhaeocystis antarctica (Karsten) and \textitThalassiosira antarctica (Comber), J. Exp. Mar. Biol. Ecol., 283, 79–95, 2003.
Haberman, K. L., Ross, R. M., and Quetin, L. B.: Diet of the Antarctic krill (\textitEuphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages, J. Exp. Mar. Biol. Ecol., 283, 97–113, 2003.
Hare, C. E., DiTullio, G. R., Trick, C. G., Wilhelm, S. W., Bruland, K. W., Rue, E. L., and Hutchins, D. A.: Phytoplankton community structure changes following simulated upwelled iron inputs in the Peru upwelling region, Aquat. Microb. Ecol., 38, 269–282, 2005.
Hare, C. E., Leblanc, K., DiTullio, G. R., Kudela, R. M., Zhang, Y., Lee, P. A., Riseman, S. F., and Hutchins, D. A.: Consequences of increased temperature and CO<sub>2</sub> for phytoplankton community structure in the Bering Sea, Mar. Ecol-Prog. Ser., 352, 9–16, doi:10.3354/meps07182, 2007.
Henjes, J., Assmy, P., Klaas, C., Verity, P. G., and Smetacek, V.: Response of microzooplankton (protists and small copepods) to an iron-induced phytoplankton bloom in the Southern Ocean (EisenEx), Deep-Sea Res. I, 54, 363–384, 2007.
Hutchins, D. A. and Bruland, K. W.: Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime, Nature, 393, 561–564, 1998.
Hutchins, D. A., Campbell, B. J., Cottrell, M. T., Takeda, S., and Cary, S. C.: Response of marine bacterial community composition to iron additions in three iron-limited regimes, Limnol. Oceanogr., 46, 1535–1545, 2001.
Hutchins, D. A., Hare, C. E., Weaver, R. S., Zhang, Y., Firme, G. F., DiTullio, G. R., Alm, M. B., Riseman, S. F., Maucher, J. M., Geesey, M. E., Trick, C. G., Smith, G. J., Rue, E. L., Conn, J., and Bruland, K. W.: Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling, Limnol. Oceanogr., 47, 997–1011, 2002.
Jacobs, S. S., Giulivi, C. F., and Mele, P. A.: Freshening of the Ross Sea during the late 20th century, Science, 297, 386–389, 2002.
Jacobson, D. M. and Anderson, D. M.: Thecate heterotrophic dinoflagellates: feeding behaviors and mechanisms, J. Phycol., 22, 249–258, 1986.
Kiene, R. P. and Slezak, D.: Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling, Limnol. Oceanogr-Meth., 4, 80–95, 2006.
Kiene, R. P., Kieber, D. J., Slezak, D., Toole, D. A., del Valle, D. A., Bisgrove, J., Brinkley, J., and Rellinger, A.: Distribution of cycling of dimethylsulfide, dimethylsulfoniopropionate, and dimethylsulfoxide during spring and early summer in the Southern Ocean south of New Zealand, Aquat. Sci., 69, 305–319, 2007.
Kolber, Z. S., Barber, R. T., Coale, K. H., Fitzwater, S. E., Greene, R. M., Johnson, K. S., Lindley, S., and Falkowski, G. P.: Iron limitation of the phytoplankton photosynthesis in the equatorial Pacific Ocean, Nature, 371, 145–149, 1994.
Leblanc, K., Hare, C. E., Boyd, P. W., Bruland, K. W., Sohst, B., Pickmere, S., Lohan, M. C., Buck, K., Ellwood, M., and Hutchins, D. A.: Fe and Zn effects on the Si cycle and diatom community structure in two contrasting high and low-silicate HNLC areas, Deep-Sea Res. I, 52, 1842–1864, 2005.
Leventer, A. R. and Dunbar, R. B.: Factors affecting the distribution of diatoms and other algae in the Ross Sea, J. Geophys. Res., 101, 18489–18500, 1996.
Lomas, M. W. and Glibert, P. M.: Interactions between NH$_4^+$ and NO$_3^-$ uptake and assimilation: comparison of diatoms and dinoflagellates at several growth temperatures, Mar. Biol., 133, 541–551, 1999.
Martin-Jezequel, V., Hildebrand, M., and Brzezinski, M. A.: Silicon metabolism in diatoms: implications for growth, J. Phycol., 36, 821–840, 2000.
Martin, J. H., Gordon, R. M., and Fitzwater, S. E.: Iron in Antarctic waters, Nature, 345, 156–158, 1990.
Maucher, J. M. and DiTullio, G. R.: Chronic iron limitation in the Ross Sea: Flavodoxin:Ferredoxin ratios in the Ross Sea, in: Biogeochemistry of the Ross Sea, edited by: DiTullio, G. R., and Dunbar, R. B., Antarctic Research Series, AGU Antarctic Research Series, Washington DC, 209–220, 2003.
Montes-Hugo, M. A., Doney, S. C., Ducklow, H. W., Fraser, W., Martinson, D., Stammerjohn, S. E., and Schofiield, O.: Recent changes in phytoplankton communities associated with rapid regional climate change along the Western Antarctic Peninsula, Science, 323, 1470–1473, 2009.
Noiri, Y., Kudo, I., Kiyosawa, H., Nishioka, J., and Tsuda, A.: Influence of iron and temperature on growth, nutrient utilization ratios and phytoplankton species composition in the western subarctic Pacific Ocean during the SEEDS experiment, Prog. Oceanogr., 64, 149–166, 2005.
Olson, R. J., Sosik, H. M., Chekalyuk, A. M., and Shalapyonok, A.: Effects of iron enrichment on phytoplankon in the Southern Ocean during late summer: active fluorescence and flow cytometric analyses, Deep-Sea Res. II, 47, 3181–3200, 2000.
Overpeck, J. T., Otto-Bliesner, B. L., and Miller, G. H.: Paleoclimatic evidence for future ice-sheet instability and rapid sea-level rise, Science, 311, 1747–1750, 2006.
Paasche, E.: Silicon, in: The physiological ecology of phytoplankton, edited by: Morris, I., Studies in Ecology, University of California Press, Berkeley, CA, 259–284, 1980.
Pondaven, P., Gallinari, M., Chollet, S., Bucciarelli, E., Sarthou, G., Schultes, S., and Jean, F.: Grazing-induced changes in cell wall silicification in a marine diatom, Protist, 158, 21–28, 2007.
Raiswell, R., Tranter, M., Benning, L. G., Siegert, M., De'ath, R., Huybrechts, P., and Payne, T.: Contributions from glacially derived sediment to the global iron (oxyhydr)oxide cycle: implications for iron delivery to the oceans, Geochim. Cosmochim. Ac., 70, 2765–2780, 2006.
Raiswell, R., Benning, L., Tranter, M., and Tulaczyk, S.: Bioavailable iron in the Southern Ocean: the significance of the iceberg conveyor belt, Geochem. T., 9, 7, doi:10.1186/1467-4866-9-7, 2008.
Raven, J. A. and Geider, R. J.: Temperature and algal growth, New Phytol., 110, 441–461, 1988.
Rellinger, A. N., Kiene, R. P., del Valle, D. A., Kieber, D. J., Slezak, D., Harada, H., Bisgrove, J., and Brinkley, J.: Occurrence and turnover of DMSP and DMS in deep waters of the Ross Sea, Antarctica, Deep-Sea Res. I, 56, 686–702, 2009.
Revel-Rolland, M., De Deckker, P., Delmonte, B., Hesse, P. P., Magee, J. W., Basile-Doelsch, I., Grousset, F., and Bosch, D.: Eastern Australia: a possible source of dust in East Antarctica interglacial ice, Earth Planet. Sc. Lett., 249, 1–13, 2006.
Rose, J. M. and Caron, D. A.: Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters, Limnol. Oceanogr., 52, 886–895, 2007.
Rose, J. M., Feng, Y., Gobler, C. J., Gutierrez, R., Hare, C. E., Leblanc, K., and Hutchins, D. A.: The effects of increased pCO<sub>2</sub> and temperature on the North Atlantic Spring Bloom. II. Microzooplankton abundance and grazing, Mar. Ecol-Prog. Ser., 388, 27–40, 2009.
Sarmiento, J. L., Hughes, T. M. C., Stouffer, R. J., and Manabe, S.: Simulated response of the ocean carbon cycle to anthropogenic climate warming, Nature, 393, 245–249, 1998.
Scharek, R., van Leeuwe, M. A., and de Baar, H. J. W.: Responses of Southern Ocean phytoplankton to the addition of trace metals, Deep-Sea Res. II, 44, 209–227, 1997.
Sedwick, P. N. and DiTullio, G. R.: Regulation of algal blooms in Antarctic shelf waters by the release of iron from melting sea ice, Geophys. Res. Lett., 24, 2515–2518, 1997.
Sedwick, P. N., DiTullio, G. R., and Mackey, D. J.: Iron and manganese in the Ross Sea, Antarctica: seasonal iron limitation in Antarctic shelf waters, J. Geophys. Res., 105, 11321–11332, 2000.
Smith Jr., W. O., Marra, J., Hiscock, M. R., and Barber, R. T.: The seasonal cycle of phytoplankton biomass and primary productivity in the Ross Sea, Antarctica, Deep-Sea Res. II, 47, 3119–3140, 2000.
Smith Jr., W. O., Dennett, M. R., Mathot, S., and Caron, D. A.: The temporal dynamics of the flagellated and colonial stages of \textitPhaeocystis antarctica in the Ross Sea, Deep-Sea Res. II, 50, 605–617, 2003.
Solorzano, L. and Sharp, J. H.: Determination of total dissolved phosphorus and particulate phosphorus in natural waters, Limnol. Oceanogr., 25, 756–760, 1980.
Strom, S., Wolfe, G., Holmes, J., Stecher, H., Shimeneck, C., Lambert, S., and Moreno, E.: Chemical defense in the microplankton I. Feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter \textitEmiliana huxleyi, Limnol. Oceanogr., 48, 217–229, 2003.
Sunda, W. G. and Huntsman, S. A.: Interrelated influence of iron, light, and cell size on growth of marine phytoplankton, Nature, 390, 389–392, 1997.
Sunda, W. G., Kieber, D. J., Kiene, R. P., and Huntsman, S. A.: An antioxidant function for DMSP and DMS in marine algae, Nature, 418, 317–320, 2002.
Takeda, S.: Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters, Nature, 393, 774–777, 1998.
Thamatrakoln, K. and Hildebrand, M.: Silicon uptake in diatoms revisited: a model for saturable and nonsaturable uptake kinetics and the role of silicon transporters, Plant Physiol., 146, 1397–1407, 2008.
Throndsen, J.: Preservation and storage, in: Phytoplankton manual, edited by: Sournia, A., UNESCO, Paris, 69–74, 1978.
Twining, B. S., Baines, S. B., Fisher, N. S., and Landry, M. R.: Cellular iron contents of plankton during the Southern Ocean Iron Experiment (SOFeX), Deep-Sea Res. I, 51, 1827–1850, 2004.
Twining, B. S., Baines, S. B., Vogt, S., and De Jonge, M.: Exploring ocean biogeochemistry by single-cell microprobe analysis of protist elemental composition, J. Eukaryot. Microbiol., 55, 151–162, 2008.
Utermöhl, H.: Zur Vervollkommung der quantitativen phytoplankton-methodik, Mitt. Int. Ver. Limnol., 9, 1–38, 1958.
Vaughan, D. G., Marshall, G. J., Connolley, W. M., Parkinson, C., Mulvaney, R., Hodgson, D. A., King, J. C., Pudsey, C. J., and Turner, J.: Recent rapid regional climate warming on the Antarctic Peninsula, Clim. Change, 60, 243–274, 2003.
Vogt, M., Steinke, M., Turner, S., Paulino, A., Meyerhöfer, M., Riebesell, U., LeQuéré, C., and Liss, P.: Dynamics of dimethylsulphoniopropionate and dimethylsulphide under different CO<sub>2</sub> concentrations during a mesocosm experiment, Biogeosciences, 5, 407–419, 2008.
Welschmeyer, N. A.: Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments, Limnol. Oceanogr., 39, 1985–1992, 1994.
Wilcox, R. R.: Applying contemporary statistical techniques, Academic Press, New York, 608~pp., 2003.
Wingenter, O. W., Haase, K. B., Zeigler, M., Blake, D. R., Rowland, F. S., Sive, B. C., Paulino, A., Thyrhaug, R., Larsen, A., Schulz, K., Meyerhofer, M., and Riebesell, U.: Unexpected consequences of increasing CO<sub>2</sub> and ocean acidity on marine production of DMS and CH<sub>2</sub>Cl 1. Potential climate impacts, Geophys. Res. Lett., 34, L05710, doi:10.1029/2006GL028139, 2007.
Wolfe, G. V. and Steinke, M.: Grazing-activated production of dimethylsulfide (DMS) by two clones of \textitEmiliania huxleyi, Limnol. Oceanogr., 41, 1151–1160, 1996.
Wolfe, G. V., Steinke, M., and Kirst, G. O.: Grazing-activated chemical defence in a unicellular marine alga, Nature, 387, 894–897, 1997.