Abstract

In mid- and high-latitude oceans, winter surface cooling and strong winds drive turbulent mixing that carries phytoplankton to depths of several hundred metres, well below the sunlit layer. This downward mixing, in combination with low solar radiation, drastically limits phytoplankton growth during the winter, especially that of the diatoms and other species that are involved in seeding the spring bloom. Here we present observational evidence for widespread winter phytoplankton blooms in a large part of the North Atlantic subpolar gyre from autonomous profiling floats equipped with biogeochemical sensors. These blooms were triggered by intermittent restratification of the mixed layer when mixed-layer eddies led to a horizontal transport of lighter water over denser layers. Combining a bio-optical index with complementary chemotaxonomic and modelling approaches, we show that these restratification events increase phytoplankton residence time in the sunlight zone, resulting in greater light interception and the emergence of winter blooms. Restratification also caused a phytoplankton community shift from pico- and nanophytoplankton to phototrophic diatoms. We conclude that transient winter blooms can maintain active diatom populations throughout the winter months, directly seeding the spring bloom and potentially making a significant contribution to over-winter carbon export.

  • Subscribe to Nature Geoscience for full access:

    $59

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    On conditions for the vernal blooming of phytoplankton. J. Cons. Int. pour l’exploitation la mer 18, 287–295 (1953).

  2. 2.

    et al. Convecion and primary production in winter. Mar. Ecol. Progr. Ser. 251, 1–14 (2003).

  3. 3.

    , & Seasonal development of phytoplankton at a high latitude oceanic site. Sarsia 84, 419–435 (1999).

  4. 4.

    , , & The influence of winter convection on primary production: a parameterisation using a hydrostatic three-dimensional biogeochemical model. J. Mar. Syst. 147, 138–152 (2015).

  5. 5.

    Abandoning Sverdrup’s critical depth hypothesis on phytoplankton blooms. Ecology 91, 977–989 (2010).

  6. 6.

    , , , & Annual cycles of ecological disturbance and recovery underlying the subarctic Atlantic spring plankton bloom. Glob. Biogeochem. Cycles 27, 526–540 (2013).

  7. 7.

    , & Mixed layer instabilities and restratification. J. Phys. Oceanogr. 37, 2228–2250 (2007).

  8. 8.

    , & Parameterization of mixed layer eddies. Part I: theory and diagnosis. J. Phys. Oceanogr. 38, 1145–1165 (2008).

  9. 9.

    , , & Eddy-driven stratification initiates North Atlantic spring phytoplankton blooms. Science 337, 54–58 (2012).

  10. 10.

    , , & Seasonality in submesoscale turbulence. Nat. Commun. 6, 6862 (2015).

  11. 11.

    & Biodiversity of plankton by species oscillations and chaos. Nature 402, 407–410 (1999).

  12. 12.

    & Shutdown of turbulent convection as a new criterion for the onset of spring phytoplankton blooms. Limnol. Ocean. 56, 2293–2307 (2011).

  13. 13.

    , & Shutdown of convection triggers increase of surface chlorophyll. J. Mar. Syst. 147, 116–122 (2015).

  14. 14.

    & Surface mixed and mixing layer depths. Deep-Sea Res. I 42, 1521–1543 (1995).

  15. 15.

    Has Sverdrup’s critical depth hypothesis been tested? Mixed layers vs. turbulent layers. ICES J. Mar. Sci. 72, 1897–1907 (2015).

  16. 16.

    & Changes in dominant mixing length scales as a driver of subpolar phytoplankton bloom initiation in the North Atlantic. Geophys. Res. Lett. 41, 3197–3203 (2014).

  17. 17.

    & Resurrecting the ecological underpinnings of ocean plankton blooms. Annu. Rev. Mar. Sci. 6, 167–194 (2014).

  18. 18.

    & A seasonal diary of phytoplankton in the North Atlantic. Front. Mar. Sci. 1, 37 (2014).

  19. 19.

    , & Global estimates of lateral springtime restratification. J. Phys. Oceanogr. 46, 1555–1573 (2016).

  20. 20.

    Growth rates of phytoplankton under fluctuating light. Freshwat. Biol. 44, 223–235 (2000).

  21. 21.

    , , & Interactive effects of temperature and light during deep convection: a case study on growth and condition of the diatom Thalassiosira weissflogii. ICES J. Mar. Sci. 72, 2061–2071 (2015).

  22. 22.

    et al. A simple optical index shows spatial and temporal heterogeneity in phytoplankton community composition during the 2008 North Atlantic Bloom Experiment. Biogeosciences 12, 2179–2194 (2015).

  23. 23.

    Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol. 84, 239–251 (1985).

  24. 24.

    & Diatom resting stages. J. Phycol. 32, 889–902 (1996).

  25. 25.

    Mixotrophy stirs up our understanding of marine food webs. Proc. Natl Acad. Sci. USA 113, 2806–2808 (2016).

  26. 26.

    & Dark survival of autotrophic, planktonic marine diatoms. Mar. Biol. 25, 195–202 (1974).

  27. 27.

    , & Physical controls of variability in North Atlantic phytoplankton communities. Limnol. Oceanogr. 60, 181–197 (2014).

  28. 28.

    , , & The oceanic mixed-layer pump. Deep-Sea Res. II 42, 757–775 (1995).

  29. 29.

    & Carbon export by small particles in the Norwegian Sea. Geophys. Res. Lett. 41, 2921–2927 (2014).

  30. 30.

    , , & Storm-induced convective export of organic matter during spring in the northeast Atlantic Ocean. Deep-Sea Res. I 49, 1431–1444 (2002).

Download references

Acknowledgements

We thank N. Briggs, M. J. Perry, E. D’Asaro, B. Gentili, E. Boss and F. Benedetti for fruitful discussions, C. Schmechtig for BGC-Argo float data management and J. Ras for proofreading the manuscript. We also thank S. Wright for sharing the CHEMTAX software v.1.95, and C. de Boyer Montégut for providing the MLD climatology. This work represents a contribution to the remOcean project (REMotely sensed biogeochemical cycles in the OCEAN, GA 246777) funded by the European Research Council, the ATLANTOS EU project (grant agreement 2014-633211) funded by H2020 program and the Italian Flagship Program RITMARE.

Author information

Affiliations

  1. Sorbonne Universités, UPMC Univ Paris 06, CNRS, Laboratoire d’Océanographie de Villefranche (LOV), Observatoire Océanologique, 06230 Villefranche-sur-Mer, France

    • L. Lacour
    • , M. Ardyna
    • , H. Claustre
    • , L. Prieur
    •  & A. Poteau
  2. Laboratory of Ecology and Evolution of Plankton, Stazione Zoologica Anton Dohrn, 80121 Naples, Italy

    • K. F. Stec
    • , M. Ribera D’Alcala
    •  & D. Iudicone

Authors

  1. Search for L. Lacour in:

  2. Search for M. Ardyna in:

  3. Search for K. F. Stec in:

  4. Search for H. Claustre in:

  5. Search for L. Prieur in:

  6. Search for A. Poteau in:

  7. Search for M. Ribera D’Alcala in:

  8. Search for D. Iudicone in:

Contributions

D.I. and L.L. designed the study. L.L., M.A., K.F.S., H.C., A.P., M.R.D’A. and D.I. conducted the data analysis. L.L. and M.A. wrote the manuscript. All authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to L. Lacour.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Information

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/ngeo3035

Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.