Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Climate-mediated dance of the plankton

Abstract

Climate change will unquestionably influence global ocean plankton because it directly impacts both the availability of growth-limiting resources and the ecological processes governing biomass distributions and annual cycles. Forecasting this change demands recognition of the vital, yet counterintuitive, attributes of the plankton world. The biomass of photosynthetic phytoplankton, for example, is not proportional to their division rate. Perhaps more surprising, physical processes (such as deep vertical mixing) can actually trigger an accumulation in phytoplankton while simultaneously decreasing their division rates. These behaviours emerge because changes in phytoplankton division rates are paralleled by proportional changes in grazing, viral attack and other loss rates. Here I discuss this trophic dance between predators and prey, how it dictates when phytoplankton biomass remains constant or achieves massive blooms, and how it can determine even the sign of change in ocean ecosystems under a warming climate.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Global dynamics of the phytoplankton biomass.
Figure 2: Phytoplankton chlorophyll and winter mixed-layer depth in the subarctic Atlantic.
Figure 3: Controls on phytoplankton accumulation rates.
Figure 4: A decade of variability in subarctic Atlantic phytoplankton concentrations.
Figure 5: Working framework for repeating cycles of phytoplankton biomass concentration.

References

  1. Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997).

    CAS  Article  Google Scholar 

  2. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. G. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    CAS  Article  Google Scholar 

  3. Antoine, D., André, J. M. & Morel, A. Oceanic primary production: II. Estimation at global scale from satellite (Coastal Zone Color Scanner) chlorophyll. Glob. Biogeochem. Cycles 10, 57–69 (1996).

    CAS  Article  Google Scholar 

  4. Chassot, E. et al. Global marine primary production constrains fisheries catches. Ecol. Lett. 13, 495–505 (2010).

    Article  Google Scholar 

  5. Takahashi, T. et al. Climatological mean and decadal change in surface ocean pCO2 and net sea–air CO2 flux over the global oceans. Deep-Sea Res. II 56, 554–577 (2009).

    CAS  Article  Google Scholar 

  6. Alkire, M. B. et al. Estimates of net community production and export using high-resolution, Lagrangian measurements of O2, NO3, and POC through the evolution of a spring diatom bloom in the North Atlantic. Deep-Sea Res. I 64, 157–74 (2012).

    CAS  Article  Google Scholar 

  7. Siegel, D. A. et al. Global assessment of ocean carbon export by combining satellite observations and food-web models. Glob. Biogeochem. Cycles 28, 181–196 (2014).

    CAS  Article  Google Scholar 

  8. Behrenfeld, M. J. Abandoning Sverdrup's critical depth hypothesis on phytoplankton blooms. Ecology 91, 977–989 (2010).

    Article  Google Scholar 

  9. Boss, E. & Behrenfeld, M. J. In situ evaluation of the initiation of the North Atlantic phytoplankton bloom. Geophys. Res. Lett. 37, L18603 (2010).

    Article  Google Scholar 

  10. Behrenfeld, M. J., Doney, S. C., Lima, I., Boss, E. S. & Siegel, D. A. Annual cycles of ecological disturbance and recovery underlying the subarctic Atlantic spring plankton bloom. Glob. Biogeochem. Cycles 27, 526–540 (2013).

    CAS  Article  Google Scholar 

  11. Behrenfeld, M. J. & Boss, E. S. Resurrecting the ecological underpinnings of ocean plankton blooms. Annu. Rev. Mar. Sci. 6, 167–194 (2014).

    Article  Google Scholar 

  12. Taylor, J. R. & Ferrari, R. Ocean fronts trigger high latitude phytoplankton blooms. Geophys. Res. Lett. 38, L23601 (2011).

    Article  Google Scholar 

  13. Taylor, J. R. & Ferrari, R. Shutdown of turbulent convection as a new criterion for the onset of spring phytoplankton blooms. Limnol. Oceanogr. 56, 2293–2307 (2011).

    Article  Google Scholar 

  14. Mahadevan, A., D'Asaro, E., Lee, C. & Perry, M. J. Eddy-driven stratification initiates North Atlantic spring phytoplankton blooms. Science 337, 54–58 (2012).

    CAS  Article  Google Scholar 

  15. Banse, K. Reflections about chance in my career, and on the top-down regulated world. Annu. Rev. Mar. Sci. 5, 1–19 (2013).

    Article  Google Scholar 

  16. Sverdrup, H. U. The place of physical oceanography in oceanographic research. J. Mar. Res. 14, 287–294 (1955).

    Google Scholar 

  17. McClain, C. R. A decade of satellite ocean color observations. Annu. Rev. Mar. Sci. 1, 19–42 (2009).

    Article  Google Scholar 

  18. Behrenfeld, M. J. et al. Climate-driven trends in contemporary ocean productivity. Nature 444, 752–755 (2006).

    CAS  Article  Google Scholar 

  19. Siegel, D. A. et al. Regional to global assessments of phytoplankton dynamics from the SeaWiFS mission. Remote Sens. Environ. 135, 77–91 (2013).

    Article  Google Scholar 

  20. Banse, K. Rates of phytoplankton cell division in the field and in iron enrichment experiments. Limnol. Oceanogr. 36, 1886–1898 (1991).

    CAS  Article  Google Scholar 

  21. Riley, G. A. Factors controlling phytoplankton populations on Georges Bank. J. Mar. Res. 6, 54–73 (1946).

    Google Scholar 

  22. Riley, G. A. & Bumpus, D. F. Phytoplankton–zooplankton relationships on Georges Bank. J. Mar. Res. 6, 33–47 (1946).

    Google Scholar 

  23. Cushing, D. H. The seasonal variation in oceanic production as a problem in population dynamics. J. Cons. Int. Explor. Mer. 24, 455–464 (1959).

    Article  Google Scholar 

  24. Banse, K. in Primary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. G. & Woodhead, A. D.) 409–440 (Plenum, 1992).

    Book  Google Scholar 

  25. Vaulot, D., Marie, D., Olson, R. J. & Chisholm, S. W. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science 268, 1480–1482 (1995).

    CAS  Article  Google Scholar 

  26. Vaulot, D. & Marie, D. Diel variability of photosynthetic picoplankton in the equatorial Pacific. J. Geophys. Res. 104, 3297–3310 (1999).

    CAS  Article  Google Scholar 

  27. Martinez, E., Antoine, D., D'Ortenzio, F. & Gentili, B. Climate-driven basin-scale decadal oscillations of oceanic phytoplankton. Science 326, 1253–1256 (2009).

    CAS  Article  Google Scholar 

  28. Sverdrup, H. U. On conditions for the vernal blooming of phytoplankton. J. Cons. Int. Explor. Mer. 18, 287–295 (1953).

    Article  Google Scholar 

  29. Chiswell, S. M. Annual cycles and spring blooms in phytoplankton: Don't abandon Sverdrup completely. Mar. Ecol. Prog. Ser. 443, 39–50 (2011).

    Article  Google Scholar 

  30. Landry, M. R. & Hassett, R. P. Estimating the grazing impact of marine micro-zooplankton. Mar. Biol. 67, 283–288 (1982).

    Article  Google Scholar 

  31. Evans, G. T. & Parslow, J. S. A model of annual plankton cycles. Biol. Oceanogr. 3, 327–347 (1985).

    Google Scholar 

  32. Levin, S. A. & Paine, R. T. Disturbance, patch formation and community structure. Proc. Natl Acad. Sci. USA 71, 2744–2747 (1974).

    CAS  Article  Google Scholar 

  33. Menge, B. A. & Sutherland, J. P. Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am. Nat. 130, 730–757 (1987).

    Article  Google Scholar 

  34. Carpenter, S. R. & Kitchell, J. F. The Trophic Cascade in Lakes (Cambridge Univ. Press, 1993).

    Book  Google Scholar 

  35. Terborgh, J., Feeley, K., Silman, M., Nuñez, P. & Balukjian, B. Vegetation dynamics of predator-free land-bridge islands. J. Ecol. 94, 253–263 (2006).

    Article  Google Scholar 

  36. de Baar, H. J. W. et al. Synthesis of iron fertilization experiments: from the Iron Age in the Age of Enlightenment. J. Geophys. Res. 110, C09S16 (2005).

    Article  Google Scholar 

  37. Boyd, P. W. et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science 315, 612–617 (2007).

    CAS  Article  Google Scholar 

  38. Cavender-Bares, K. K., Mann, E. L., Chisholm, S. W., Ondrusek, M. E. & Bidigare, R. R. Differential response of equatorial Pacific phytoplankton to iron fertilization. Limnol. Oceanogr. 44, 237–246 (1999).

    CAS  Article  Google Scholar 

  39. Landry, M. R. et al. Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II). III. Dynamics of phytoplankton growth and microzooplankton grazing. Mar. Ecol. Prog. Ser. 201, 57–72 (2000).

    CAS  Article  Google Scholar 

  40. Banse, K. Steemann Nielsen and the zooplankton. Hydrobiologia 480, 15–28 (2002).

    Article  Google Scholar 

  41. Bopp, L. et al. Potential impact of climate change on marine export production. Glob. Biogeochem. Cycles 15, 81–99 (2001).

    CAS  Article  Google Scholar 

  42. Boyd, P. W. & Doney, S. C. Modelling regional responses by marine pelagic ecosystems to global climate change. Geophys. Res. Lett. 29, 53-1–53-4 (2002).

    Article  Google Scholar 

  43. Sarmiento, J. L. et al. Response of ocean ecosystems to climate warming. Glob. Biogeochem. Cycles 18, GB3003 (2004).

    Article  Google Scholar 

  44. Henson, S. A., Dunne, J. P. & Sarmiento, J. L. Decadal variability in North Atlantic phytoplankton blooms. J. Geophys. Res. Oceans 114, C04013 (2009).

    Article  Google Scholar 

  45. Platt, T., Fuentes-Yaco, C. & Frank, K. Spring algal bloom and larval fish survival. Nature 423, 398–399 (2003).

    CAS  Article  Google Scholar 

  46. Edwards, M. & Richardson, J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881–884 (2004).

    CAS  Article  Google Scholar 

  47. Koeller, P. et al. Basin-scale coherence in phenology of shrimps and phytoplankton in the North Atlantic Ocean. Science 324, 791–793 (2009).

    CAS  Article  Google Scholar 

  48. Lochte, K., Ducklow, H. W., Fasham, M. J. R. & Stienen, C. Plankton succession and carbon cycling at 47°N 20°W during the JGOFS North Atlantic Bloom Experiment. Deep-Sea Res. II 40, 91–114 (1993).

    Article  Google Scholar 

  49. Martin, P. et al. Export and mesopelagic particle flux during a North Atlantic spring diatom bloom. Deep-Sea Res. I 58, 338–49 (2011).

    Article  Google Scholar 

  50. Steele, J. H. The Structure of Marine Ecosystems (Harvard Univ. Press, 1974).

    Book  Google Scholar 

  51. Teeling, H. et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611 (2012).

    CAS  Article  Google Scholar 

  52. Vergin, K. L., Done, B., Carlson, C. A. & Giovannoni, S. J. Spatiotemporal distributions of rare bacterioplankton populations indicate adaptive strategies in the oligotrophic ocean. Aquat. Microb. Ecol. 71, 1–13 (2013).

    Article  Google Scholar 

  53. Olson, R. J. & Sosik, H. M. A submersible imaging-in-flow instrument to analyze nano- and microplankton: imaging FlowCytobot. Limnol. Oceanogr. Meth. 5, 195–203 (2007).

    Article  Google Scholar 

  54. Picheral, M. et al. The Underwater Vision Profiler 5: an advanced instrument for high spatial resolution studies of particle size spectra and zooplankton. Limnol. Oceanogr. Meth. 8, 462–473 (2010).

    Article  Google Scholar 

  55. Landry, M. R. Switching between herbivory and carnivory by the planktonic marine copepod Calanus pacificus. Mar. Biol. 65, 77–82 (1981).

    Article  Google Scholar 

  56. Verity, P. G., Smetacek, V. & Smayda, T. J. Status, trends and the future of the marine pelagic ecosystem. Environ. Conserv. 29, 207–237 (2002).

    Article  Google Scholar 

  57. Mariani, P., Andersen, K. H., Visser, A. W., Barton, A. D. & Kiørboe, T. Control of plankton seasonal succession by adaptive grazing. Limnol. Oceanogr. 58, 173–184 (2013).

    Article  Google Scholar 

  58. Suttle, C. A., Chan, A. M. & Cottrell, M. T. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347, 467–469 (1990).

    Article  Google Scholar 

  59. Vardi, A. et al. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326, 861–865 (2009).

    CAS  Article  Google Scholar 

  60. Bidle, K. D. & Vardi, A. A chemical arms race at sea mediates algal host-virus interactions. Curr. Opin. Microbiol. 14, 449–457 (2011).

    Article  Google Scholar 

  61. Berman-Frank, I., Bidle, K. D., Haramaty, L. & Falkowski, P. G. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49, 997–1005 (2004).

    Article  Google Scholar 

  62. Bidle, K. D. & Falkowski, P. G. Cell death in planktonic, photosynthetic microorganisms. Nature Rev. Microbiol. 2, 643–655 (2004).

    CAS  Article  Google Scholar 

  63. Giovannoni, S. J. & Vergin, K. L. Seasonality in ocean microbial communities. Science 335, 671–676 (2012).

    CAS  Article  Google Scholar 

  64. Baird, M. E. Limits to prediction in a size-resolved pelagic ecosystem model. J. Plankton Res. 32, 1131–1146 (2010).

    Article  Google Scholar 

  65. Prowe, A. E. F., Pahlow, M., Dutkiewicz, S., Follows, M. & Oschlies, A. Top-down control of marine phytoplankton diversity in a global ecosystem model. Prog. Oceanogr. 101, 1–13 (2012).

    Article  Google Scholar 

  66. Behrenfeld, M. J., Boss, E., Siegel, D. A. & Shea, D. M. Carbon-based ocean productivity and phytoplankton physiology from space. Glob. Biogeochem. Cycles 19, GB1006 (2005).

    Article  Google Scholar 

  67. Ducklow, H. W. & Harris, R. P. Introduction to the JGOFS North Atlantic Bloom Experiment. Deep-Sea Res. II 40, 1–8 (1993).

    Article  Google Scholar 

  68. Blain, S. et al. Availability of iron and major nutrients for phytoplankton in the northeast Atlantic Ocean. Limnol. Oceanogr. 49, 2095–2104 (2004).

    CAS  Article  Google Scholar 

  69. Moore, C. M. et al. Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol. Oceanogr. 51, 936–949 (2006).

    Article  Google Scholar 

  70. Nielsdottir, M. C., Moore, C. M., Sanders, R., Hinz, D. J. & Achterberg, E. P. Iron limitation of the postbloom phytoplankton communities in the Iceland Basin. Glob. Biogeochem. Cycles 23, GB3001 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Aeronautics and Space Administration's Ocean Biology and Biogeochemistry Program. I thank R. O'Malley for assistance with satellite data and analyses, and E. Boss, J. Graff, K. Halsey, B. Jones, A. Milligan and T. Westberry for helpful comments and discussions during the development of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael J. Behrenfeld.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Supplementary information

Supplementary information

Supplementary Text and Figures (PDF 377 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Behrenfeld, M. Climate-mediated dance of the plankton. Nature Clim Change 4, 880–887 (2014). https://doi.org/10.1038/nclimate2349

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2349

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing