Deep carbon export from a Southern Ocean iron-fertilized diatom bloom

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Fertilization of the ocean by adding iron compounds has induced diatom-dominated phytoplankton blooms accompanied by considerable carbon dioxide drawdown in the ocean surface layer. However, because the fate of bloom biomass could not be adequately resolved in these experiments, the timescales of carbon sequestration from the atmosphere are uncertain. Here we report the results of a five-week experiment carried out in the closed core of a vertically coherent, mesoscale eddy of the Antarctic Circumpolar Current, during which we tracked sinking particles from the surface to the deep-sea floor. A large diatom bloom peaked in the fourth week after fertilization. This was followed by mass mortality of several diatom species that formed rapidly sinking, mucilaginous aggregates of entangled cells and chains. Taken together, multiple lines of evidence—although each with important uncertainties—lead us to conclude that at least half the bloom biomass sank far below a depth of 1,000 metres and that a substantial portion is likely to have reached the sea floor. Thus, iron-fertilized diatom blooms may sequester carbon for timescales of centuries in ocean bottom water and for longer in the sediments.

At a glance


  1. Experimental eddy and the fertilized patch.
    Figure 1: Experimental eddy and the fertilized patch.

    a, The eddy core depicted with the stream function (Ψ; contours and colour scale) derived from currents measured using a vessel-mounted acoustic Doppler current profiler at a regular grid of stations between days1 and 7. The black spiral is the ship’s track (a Lagrangian circle) around the buoy drifting southwestward during fertilization. The white line is the superimposed track of the drifting buoy during its first rotation from days−1 to 11 (same as in b and c). b, Altimeter image of sea surface height anomaly (SSHA; contours and colour scale from CCAR, The rectangle in a and b is enlarged in cf. c, Area and location of the patch on days10 and 11 after fertilization, depicted on the basis of chlorophyll measurements. The yellow area is the hot spot. df, Location and area of the patch 17 days after fertilization, depicted in terms of photochemical efficiency (Fv/Fm; d), CO2 fugacity (fCO2; e) and chlorophyll concentration (f). The line is the track of the drifting buoy during its second rotation (days13–21). The red area in f is the hot spot. gi, Satellite-derived surface chlorophyll concentrations of the EIFEX eddy before fertilization (g), during the bloom peak (h) and in its demise phase (i). The eddy core is encircled in white; the EIFEX bloom is evident in h and i (green colour is >1μg Chl l−1). Note the natural bloom along the Antarctic polar front, which disappeared in this period. SeaWiFS images (gi) courtesy of the NASA SeaWiFS Project and GeoEye.

  2. Temporal evolution of chlorophyll and silicate concentrations.
    Figure 2: Temporal evolution of chlorophyll and silicate concentrations.

    a, Chlorophyll concentrations reflect the growth, peak and demise phases of the bloom in the patch. b, By comparison, the Chl concentration outside the patch is low. The slightly higher out-patch values soon after fertilization are due to local patchiness in outside water and not to interim accumulation. c, d, The declining trend of silicate in outside water (d) is interrupted by local patchiness, whereas within the patch the trend is smooth (c). Note the variations in mixed-layer depth below 100m. Black diamonds indicate depths of discrete samples.

  3. Temporal evolution of dissolved and particulate elements.
    Figure 3: Temporal evolution of dissolved and particulate elements.

    Values inside (filled circles) and outside (open circles) the fertilized patch are depth-integrated average concentrations for the upper 100m of the water column. All concentrations are in millimoles per cubic metre except that for Chl (k), which is expressed in milligrams per cubic metre. Lines represent the temporal evolution inside (solid line) and outside (broken line) the fertilized patch used in elemental budget calculations (Supplementary Methods) determined by linear regression. Inside the patch, the r2 values for the models are 0.64 (DIC; a), 0.88 (nitrate plus nitrite; b), 0.74 (phosphate; c), 0.97 (silicic acid; d), 0.33 (ammonium; e), 0.63 (DON; f), 0.84 (POC; g), 0.94 (PON; h), 0.93 (POP; i), 0.96 (BSi; j), 0.92 (Chl; k) and 0.05 (DOC; l). Outside the patch, the r2 values are 0.06 (DIC), 0.24 (nitrate plus nitrite), 0.13 (phosphate), 0.71 (silicic acid), 0.24 (ammonium), 0.58 (DON), 0.84 (POC), 0.64 (PON), 0.85 (POP), 0.008 (BSi) and 0.005 (DOC). All regressions are significant (P<0.005) with the exception of in-patch DOC (P = 0.4) and out-patch DIC (P = 0.5), nitrate plus nitrite (P = 0.011), phosphate (P = 0.1), ammonium (P = 0.02), DON (P = 0.046), PON (P = 0.03), BSi (P = 0.8) and DOC (P = 0.8).

  4. Temporal evolution of particulate organic carbon stocks in successive depth layers.
    Figure 4: Temporal evolution of particulate organic carbon stocks in successive depth layers.

    Stocks for the respective layers are derived from depth-integrated, vertical profiles of beam attenuation of a transmissometer calibrated using discrete POC measurements (black symbols). Filled and open symbols show data inside and outside the patch, respectively. Depth intervals of integrations are 0–100m (a, i), 100–200m (b, j), 200–300m (c, k), 300–400m (d, l), 400–500m (e, m), 500–1,000m (f, n), 1,000–2,000m (g, o) and 2,000–3,000m (h, p). Lines are derived from linear regression models. Variability in stocks and trends in the layers at 100–200m (b, j) is due to intermittent shoaling and deepening of the particle-rich, surface mixed layer between 100 and 120m, possibly as a result of the passage of internal waves. The high out-patch values on days5 and 34 are not included in the regressions. The layer below 3,000m is not included to avoid contamination by resuspended sediments in the nepheloid layer. Red diamonds show integrated stocks from measurements on discrete water samples. Variability in these values is due to low depth resolution, particularly below 500m.

  5. Depth-integrated particulate organic carbon stocks.
    Figure 5: Depth-integrated particulate organic carbon stocks.

    Stocks for the 0–500-m (triangles) and 0–3,000-m (circles) water columns are derived from vertical transmissometer profiles as in Fig. 4. Filled and open symbols show data inside and outside the patch, respectively. All profiles measured down to the sea floor during the study are depicted. Because the depth of the flux event was not anticipated and deep casts are time consuming, only six profiles to the sea floor were measured before the flux event: one before fertilization, one in the hot spot, two outside the patch (of which one was inside the core) and two in the meander of the Antarctic polar front (APF).


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Author information

  1. These authors contributed equally to this work.

    • Victor Smetacek &
    • Christine Klaas


  1. Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany

    • Victor Smetacek,
    • Christine Klaas,
    • Volker H. Strass,
    • Philipp Assmy,
    • Boris Cisewski,
    • Ulrich Bathmann,
    • Joachim Henjes,
    • Martin Losch,
    • Ilka Peeken,
    • Oliver Sachs,
    • Eberhard Sauter,
    • Jill Schwarz,
    • Anja Terbrüggen &
    • Dieter Wolf-Gladrow
  2. National Institute of Oceanography, Dona Paula, Goa 403 004, India

    • Victor Smetacek
  3. Norwegian Polar Institute, Fram Centre, Hjalmar Johansens Gate 14, 9296 Tromsø, Norway

    • Philipp Assmy
  4. Ecology and Evolution of Plankton, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121-Napoli, Italy

    • Marina Montresor
  5. Johann Heinrich von Thünen Institute, Institute of Sea Fisheries, Palmaille 9, 22767 Hamburg, Germany

    • Boris Cisewski
  6. Department of Analytical and Environmental Chemistry, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium

    • Nicolas Savoye
  7. Univ. Bordeaux/CNRS, EPOC, UMR 5805, Station Marine d’Arcachon, 2 rue du Professeur Jolyet, F-33120 Arcachon, France

    • Nicolas Savoye
  8. Oceanography Department, University of Cape Town, Private Bag X3, Rondebosch, 7701 Cape Town, South Africa

    • Adrian Webb
  9. LOCEAN-IPSL, CNRS/UPMC/IRD/MNHN, 4 Place Jussieu, 75252 Paris Cedex 5, France

    • Francesco d’Ovidio
  10. Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, The Netherlands

    • Jesús M. Arrieta,
    • Santiago Gonzalez &
    • Gerhard J. Herndl
  11. Department of Global Change Research, Instituto Mediterraneo de Estudios Avanzados, CSIC-UIB, Miquel Marques 21, 07190 Esporles, Mallorca, Spain

    • Jesús M. Arrieta
  12. Leibniz Institute for Baltic Sea Research Warnemünde, Seestraße 15, 18119 Rostock, Germany

    • Ulrich Bathmann
  13. Bjerknes Centre for Climate Research, University of Bergen, Allegaten 55, N-5007 Bergen, Norway

    • Richard Bellerby &
    • Craig Neill
  14. Norwegian Institute for Water Research, Thormøhlensgate 53 D, 5006 Bergen, Norway

    • Richard Bellerby
  15. Department of Environmental Earth System Science, Stanford University, Stanford, California 94305, USA

    • Gry Mine Berg &
    • Matthew M. Mills
  16. Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105 Kiel, Germany

    • Peter Croot &
    • Linn J. Hoffmann
  17. Earth and Ocean Sciences, School of Natural Sciences, National University of Ireland, Galway, Quadrangle Building, University Road, Galway, Ireland

    • Peter Croot
  18. Phytolutions GmbH, Campus Ring 1, 28759 Bremen, Germany

    • Joachim Henjes
  19. Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria

    • Gerhard J. Herndl
  20. School of Environmental Sciences, University of Liverpool, Room 209 Nicholson Building, 4 Brownlow Street, Liverpool L69 3GP, UK

    • Harry Leach
  21. Wealth from Oceans Flagship, Commonwealth Scientific and Industrial Research Organisation, Castray Esplanade, Hobart, Tasmania 7000, Australia

    • Craig Neill
  22. MARUM – Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, D-28359 Bremen, Germany

    • Ilka Peeken
  23. Institute for Coastal Research, Helmholtz-Zentrum Geesthacht, Center for Materials and Coastal Research, Max-Planck-Strasse 1, 21502 Geesthacht, Germany

    • Rüdiger Röttgers
  24. Eberhard & Partner AG, General Guisan Strasse 2, 5000 Arau, Switzerland

    • Oliver Sachs
  25. Centre for Biomolecular Interactions Bremen, FB 2, University of Bremen, Postfach 33 04 40, 28359 Bremen, Germany

    • Maike M. Schmidt
  26. School of Marine Science & Engineering, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK

    • Jill Schwarz


V.S. and C.K. wrote the manuscript. V.S. directed the experiment and C.K. carried out the budget calculations. V.H.S., P.A., M.M. and D.W.-G. contributed to the preparation of the manuscript. V.H.S., B.C., H.L. and M.L. contributed physical data on mixed-layer depth dynamics, eddy coherence, patch movement and transmissometer data. N.S. provided thorium data. A.W. provided nutrient data. P.A. and J.H. provided phytoplankton and BSi data. F.D. carried out the Lagrangian analysis based on delayed-time altimetry. J.M.A. and G.J.H. provided bacterial data. C.N. and R.B. provided inorganic carbon data. G.M.B., C.K. and M.M.M. provided POC and PON data. P.C. provided the iron data. S.G. and A.T. provided DOM data. I.P. and L.J.H. performed the 14C primary production measurements and provided high-pressure liquid chromatography data. R.R. provided data on photochemical efficiency (Fv/Fm). C.K., M.M.S. and A.T. provided Chl data. U.B., E.S., O.S. and J.S. provided data on the eddy core from a subsequent cruise and satellite Chl images.

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The authors declare no competing financial interests.

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Supplementary information

PDF files

  1. Supplementary Information 1 (13.8M)

    This file contains Supplementary Text and Data 1-5 (see contents). Each section also includes Supplementary Figures, Supplementary Tables and additional references.

  2. Supplementary Information 2 (6.1M)

    This file contains Supplementary Methods, additional references, Supplementary Figures 1-7 and Supplementary Tables 1-3. This file was replaced on 20 July 2012, as the figures that appeared in the original file were incorrect.


  1. Report this comment #51119

    Faye Fornasier said:

    To: The Editors of Nature
    From: Charles B. Miller,
    Prof. Emeritus, Oceanography
    College of Earth, Ocean and Atmospheric Sciences
    Oregon State University
    Corvallis, Oregon 97331-5503, USA

    29 August 2012

    Some points remain to be made concerning the report by Smetacek, V. et al. (Nature 487: 313-319, 19 July 2012) regarding carbon export from a 2004 ocean-iron-fertilization (OIF) experiment, termed EIFEX, in the Southern Ocean. (1) That iron fertilization resulted in a diatom bloom is supported, and typical of all other OIF studies (Boyd, P.W., et al. 2007. Mesoscale iron enrichment experiments 1993-2005: synthesis and future directions. Science 315 612-617). Results implying induced increase of carbon export to 500 m seem sound, but that only provides surface-return times of a few decades. The conclusion that organic matter from the bloom reached below 1000 and 2000 m is marginal. Iron was added to an eddy with low phytoplankton standing stock surrounded by an areally significant bloom (their Fig. 1g), and blooms without added iron were scattered within the eddy near the fertilized patch (Supplement Fig. S1.1e). Smetacek et al. admit that the out-of-patch stations were not an ideal control. Perhaps reflecting that, approximations of the increasing carbon in layers below 500 m after ~25 days (their Fig. 4) were roughly comparable beneath the OIF patch to those at the out-of-patch stations. Thus, the surrounding and spatially larger bloom was as likely responsible for the uptick in very deep particulate carbon as were iron-stimulated diatoms. In-patch species counts to 3700 m are provided for diatoms (Supplement Fig. 7), and the figure caption argues they imply export from the induced bloom. However, no data are shown from surrounding waters. It's an old rule: if the control data are like the treatment data, then sophisticated argument is required to claim a treatment effect.
    (2) Both the paper and the introductory comment by K.D. Buesseler (Nature 487: 305-306) enthuse about the stimulated production and the export. However, the amount of nitrate actually drawn down by the diatom bloom was only 1.6 μM from the initial concentration of ~25.2 μM (their Fig. 3b, both initial and final concentrations integrated over 100 m, the mixing depth during the experiment). Thus, a very small fraction of the usually considered potential (major nutrients unused because of iron limitation) of OIF in the Southern Ocean for geoengineering of carbon drawdown was realized. At the same time most of the dissolved silicic acid, the raw material of diatom tests, was utilized at both the patch and control stations, reduced from 20 μM to ~6 μM. Furthermore, the only area in the vicinity with initial silicate above 6 μM was in the eddy selected for fertilization (Fig. S1.1). Whether or not there was increase in very deep export due to diatoms responding to the EIFEX iron, the silicate drawdown was large. Possibly a little more iron would have allowed diatoms to exhaust it. The geoengineering implication from results for these two nutrients (fixed N and Si(OH)4) is that not only iron in low nM concentrations but silicic acid at 10s of μM would have to be supplied for OIF to produce significant sequestration of carbon from the atmosphere. Supplying sufficient iron annually for very long periods to substantial sectors of the Southern Ocean might theoretically be possible, if extremely difficult and costly; however, supplying enough silicic acid to make that useful is utterly impossible. OIF is not a viable geoengineering option, and further study by larger and longer OIF experiments motivated by its supposed potential, as advocated by Buesseler, cannot be justified on the basis that it might be.


  2. Report this comment #51624

    Faye Fornasier said:

    From: Victor Smetacek, Professor Emeritus, Bio-Oceanography Alfred Wegener Institute for Polar and Marine Research Bremerhaven, Germany

    Reply to the letter posted by Prof. Charlie Miller on August 29, 2012.
    In the following I comment on the points raised by Prof. Miller concerning deep export, the magnitude and composition of the EIFEX bloom, the need for more OIF experiments and their implications for geo-engineering. We have presented data in our paper and supplementary information showing that the particulate organic carbon (POC) in the deep water column and close to the sea floor under our bloom emanated from it. It requires more than a leap of faith to attribute the deep POC increase below 500 m under the patch to outside sources. The fact that there were also relatively high POC concentrations in outside deep water columns is not at all surprising given the fact that there were natural blooms in the area. The species compositions of diatoms inside and outside the patch were similar and the fact that fresh cells of some of these surface species were found close to the bottom at 3,700 m depth under the patch is clear evidence of extremely rapid sinking. We are not claiming that adding iron to natural HNLC waters is the only way to deliver fresh diatom cells to the deep sea floor. That fresh diatom aggregates were present not only under our patch but also in the surroundings wh ere natural blooms had occurred (data presented in Assmy et al in prep., see below) merely confirms what has been known for decades: diatom blooms, whether natural or artificially induced in mesocosms (CEPEX, MERL, etc), tend to aggregate and sink most of their biomass rapidly after peaking (Smetacek, V.S. 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol. 84, 239-251). Our only misfortune was that the last 3 deep casts in outside waters, aimed at water columns as far from the spreading patch as possible but still within the eddy core, happened to encounter water columns over which blooms had occurred previously. Since each deep cast takes 4 hours, and time was running short when the bloom started sinking, we had to restrict the number of control, outside stations. The deep water column under our patch prior to the sinking event had low POC levels: these levels are the crucial baselines for estimating POC input from the bloom and not the patchy levels found in outside water columns. (2) We were not boasting when we mentioned that the EIFEX bloom built up the highest chlorophyll stock (m-2) of any previous experiment. Nitrate decline from beginning to end of 1.6 -M (Table 1, NO2 + NO3, line 1) might seem low, but this concentration is for a 100 m water column, i.e. the reduction in the nitrate stock m-2 is equivalent to 1.6 millimole x 100 m = 160 mmol m-2. Translated to a mixed layer depth of 10 m such as reported from the SEEDS I experiment in the Subarctic Pacific, the reduction in nitrate concentration would be 16 -M. Similarly, the peak chlorophyll concentration of 2.8 mg m-3 recorded in EIFEX, when compressed into a 10 m water column, is equivalent to 28 mg Chl m-3, which is well above natural bloom concentrations attained in eutrophic coastal waters of 10m mixed layer depth. This confusion between concentrations and stocks has been made before (de Baar, H. J. W. et al., 2005. Synthesis of iron fertilization experi ments: From the iron age in the age of enlightenment. J. Geophys. Res. 110, C09S16, doi:10.1029/2004JC002601) and explained (Smetacek, V. and Naqvi, S.W.A., 2008. The next generation of iron fertilization experiments in the Southern Ocean. Phil Trans. R. Soc. A 366, 3947-3967). Furthermore, the measured nitrate concentrations read off the figures, need to be corrected for DON uptake and dilution of the patch by surrounding water as explained in the text and presented in Table 1 and the tables under supplementary information. There, total N uptake including vertical and horizontal dilution is calculated to be 0.5 moles m-2, equivalent to 5 -M (line 4, Table 1). This is equivalent to a chlorophyll concentration in the 100 m water column of about 9 mg m-3, or 90 mg m-3 in a 10 m deep mixed layer. It seems unlikely that such a large biomass could be built-up in a patch large enough to retain undiluted water in its centre over a period of 3 - 4 weeks. B ut it would really be interesting to explore when and if self-shading ultimately restricts biomass accumulation. This and other relevant hypotheses, also pertaining to the fate of phytoplankton biomass and its effect on grazers, higher pelagic trophic levels but also the underlying benthos could be tested in much larger experiments. The point raised regarding silicon and Si/N ratios was addressed in a companion manuscript -Antarctic grazer-protected diatoms decouple ocean carbon and silicon cycles- by Assmy, Smetacek et al. currently under revision. We state there: 'the upper limit of carbon sequestration will be determined by competition between C- and Si-sinkers for silicate, expressed in the Si/C ratios of the stimulated blooms'. The C- and Si-sinkers refer to different groups of diatom species whose accumulation rates relative to growth and mortality were studied during EIFEX in unprecedented detail. We call for more experiments not only because of the geoengineering implications but because in situ experiments are the only way to study and quantify processes in natural ecosystems with their full complement of pathogens, parasitoids and grazers together with their predators. Were it not for whole lake experiments, limnology would be where bio-oceanography is today, firmly entrenched in the bottom-up paradigm. It follows that bio-oceanography could be where limnology is today if more dedicated in situ experiments are carried out by the scientific community. It goes without saying that the technique of iron fertilization, whether applied at experimental or larger scales and for whatever purpose, must remain firmly in the hands of the international scientific community. This is a challenge that we have to rise to. The transition from use to abuse of OIF is a matter of dosage and duration, the limits of which must be explored and set by the scientific community. The London Co nvention is drawing up international policy guidelines with the intention of preventing commercialisation of OIF. The way for legitimate scientific experiments is open and should remain open. I too wish that geo-engineering were not an option, but wishful thinking will not bring back the Arctic summer sea ice.

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