Article | Published:

Revaluating ocean warming impacts on global phytoplankton

Nature Climate Change volume 6, pages 323330 (2016) | Download Citation

Abstract

Global satellite observations document expansions of the low-chlorophyll central ocean gyres and an overall inverse relationship between anomalies in sea surface temperature and phytoplankton chlorophyll concentrations. These findings can provide an invaluable glimpse into potential future ocean changes, but only if the story they tell is accurately interpreted. Chlorophyll is not simply a measure of phytoplankton biomass, but also registers changes in intracellular pigmentation arising from light-driven (photoacclimation) and nutrient-driven physiological responses. Here, we show that the photoacclimation response is an important component of temporal chlorophyll variability across the global ocean. This attribution implies that contemporary relationships between chlorophyll changes and ocean warming are not indicative of proportional changes in productivity, as light-driven decreases in chlorophyll can be associated with constant or even increased photosynthesis. Extension of these results to future change, however, requires further evaluation of how the multifaceted stressors of a warmer, higher-CO2 world will impact plankton communities.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Are ocean deserts getting larger? Geophys. Res. Lett. 36, L18609 (2009).

  2. 2.

    , & Subtropical gyre variability observed by ocean-color satellites. Deep-Sea Res. II 51, 281–301 (2004).

  3. 3.

    , & Ocean’s least productive waters are expanding. Geophys. Res. Lett. 35, 3618 (2008).

  4. 4.

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

  5. 5.

    , & Evolved physiological responses of phytoplankton to their integrated growth environment. Phil. Trans. R. Soc. B 363, 2687–2703 (2008).

  6. 6.

    , , & Climate-driven basin-scale decadal oscillations of oceanic phytoplankton. Science 326, 1253–1256 (2009).

  7. 7.

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

  8. 8.

    , & Recent trends in global ocean chlorophyll. Geophys. Res. Lett. 32, L03606 (2005).

  9. 9.

    , , & Trends in primary production in the California Current detected with satellite data. J. Geophys. Res. 114, C02004, 10340 (2009).

  10. 10.

    , & Global phytoplankton decline over the past century. Nature 466, 591–596 (2010).

  11. 11.

    & Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnol. Oceanogr. 25, 457–473 (1980).

  12. 12.

    Light and temperature dependence of the carbon to chlorophyll ratio in microalgae and cyanobacteria: Implications for physiology and growth of phytoplankton. New Phytol. 106, 1–34 (1987).

  13. 13.

    , , & Carbon-based ocean productivity and phytoplankton physiology from space. Glob. Biogeochem. Cycles 19, GB1006 (2005).

  14. 14.

    & Phytoplankton strategies for photosynthetic energy allocation. Annu. Rev. Mar. Sci. 7, 265–297 (2015).

  15. 15.

    et al. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl Acad. Sci. USA 92, 10237–10241 (1995).

  16. 16.

    & Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth. Res. 53, 229–241 (1997).

  17. 17.

    , & Redox regulation and overreduction control in the photosynthesizing cell: Complexity in redox networks. Biochim. Biophys. 1780, 1261–1272 (2008).

  18. 18.

    & The hidden function of photosynthesis: A sensing system for environmental conditions that regulates plant acclimation responses. Protoplasma 249, S125–S136 (2012).

  19. 19.

    , & Succinate: Quinol oxidoreductases in the cyanobacterium Synechocystis sp. strain PCC 6803: Presence and function in metabolism and electron transport. J. Bacteriol. 182, 714–722 (2000).

  20. 20.

    et al. Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442, 1025–1028 (2006).

  21. 21.

    & Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5, 217–246 (2013).

  22. 22.

    , , , & In situ observations of phytoplankton productivity by an underwater profiling buoy system: Use of fast repetition rate fluorometry. Mar. Ecol. Prog. Ser. 353, 81–88 (2008).

  23. 23.

    & Chlororespiration. Ann. Rev. Plant Biol. 53, 523–550 (2002).

  24. 24.

    Encyclopedia of Life Sciences (John Wiley, 2001).

  25. 25.

    , , & A photoacclimation and nutrient based model of light-saturated photosynthesis for quantifying oceanic primary production. Mar. Ecol. Prog. Ser. 228, 103–117 (2002).

  26. 26.

    , , & Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J. Phycol. 38, 17–38 (2002).

  27. 27.

    , , & Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22, GB2024 (2008).

  28. 28.

    & Estimators of primary production for interpretation of remotely sensed data on ocean color. J. Geophys. Res. 98, 14561–14567 (1993).

  29. 29.

    & A consumer’s guide to phytoplankton primary productivity models. Limnol. Oceanogr. 42, 1479–1491 (1997).

  30. 30.

    & In situ phytoplankton absorption, fluorescence emission, and particulate backscattering spectra determined from reflectance. J. Geophys. Res. 100, 13279–13294 (1995).

  31. 31.

    , & Optimization of a semianalytical ocean color model for global-scale applications. Appl. Opt. 41, 2705–2714 (2002).

  32. 32.

    , & Deriving inherent optical properties from water color: A multi-band quasi-analytical algorithm for optically deep waters. Appl. Opt. 41, 5755–5772 (2002).

  33. 33.

    , , , & Particle optical backscattering along a chlorophyll gradient in the upper layer of the eastern South Pacific Ocean. Biogeoscience 5, 495–507 (2008).

  34. 34.

    , , , & Optical backscattering is correlated with phytoplankton carbon across the Atlantic Ocean. Geophys. Res. Lett. 40, 1154–1158 (2013).

  35. 35.

    , & The measurement of phytoplankton biomass using flow-cytometric sorting and elemental analysis of carbon. Limnol. Oceanogr. Method 10, 910–920 (2012).

  36. 36.

    et al. Analytical phytoplankton carbon measurements spanning diverse ecosystems. Deep-Sea Res. I 102, 16–25 (2015).

  37. 37.

    & Bio-optical algorithms for ADEOS-2 GLI. J. Remote Sens. Soc. Jpn 29, 80–85 (2009).

  38. 38.

    & Global and regional evaluation of the SeaWiFS chlorophyll data set. Remote Sens. Environ. 93, 463–479 (2004).

  39. 39.

    , & The influence of Raman scattering on ocean color inversion models. Appl. Opt. 52, 5552–5561 (2013).

  40. 40.

    et al. Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity. Biogeoscience 7, 621–640 (2010).

  41. 41.

    Climate-mediated dance of the plankton. Nature Clim. Change 4, 880–887 (2014).

  42. 42.

    , , , & On the relationship between stratification and primary productivity in the North Atlantic. Geophys. Res. Lett. 38, L18609 (2011).

  43. 43.

    et al. Global assessment of ocean carbon export using food-web models and satellite observations. Glob. Biogeochem. Cycles 28, 181–196 (2014).

  44. 44.

    et al. Skill metrics for confronting global upper ocean ecosystem- biogeochemistry models against field and remote sensing data. J. Mar. Syst. 76, 95–112 (2009).

  45. 45.

    et al. Satellite-detected fluorescence reveals global physiology of ocean phytoplankton. Biogeoscience 6, 779–794 (2009).

  46. 46.

    , , & Biological ramifications of climate-change-mediated oceanic multi-stressors. Nature Clim. Change 5, 71–79 (2015).

  47. 47.

    , & Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites 4, 260–280 (2014).

Download references

Acknowledgements

This work was supported by the National Aeronautics and Space Administration’s Ocean Biology and Biogeochemistry Program.

Author information

Affiliations

  1. Department of Botany and Plant Pathology, Cordley Hall 2082, Oregon State University, Corvallis, Oregon 97331-2902, USA

    • Michael J. Behrenfeld
    • , Robert T. O’Malley
    • , Toby K. Westberry
    • , Jason R. Graff
    • , Allen J. Milligan
    •  & Matthew B. Brown
  2. School of Marine Sciences, 5706 Aubert Hall, University of Maine, Orono, Maine 04469-5741, USA

    • Emmanuel S. Boss
  3. Department of Microbiology, 220 Nash Hall, Oregon State University, Corvallis, Oregon 97330, USA

    • Kimberly H. Halsey
  4. Earth Research Institute and Department of Geography, University of California, Santa Barbara, California 93106-3060, USA

    • David A. Siegel

Authors

  1. Search for Michael J. Behrenfeld in:

  2. Search for Robert T. O’Malley in:

  3. Search for Emmanuel S. Boss in:

  4. Search for Toby K. Westberry in:

  5. Search for Jason R. Graff in:

  6. Search for Kimberly H. Halsey in:

  7. Search for Allen J. Milligan in:

  8. Search for David A. Siegel in:

  9. Search for Matthew B. Brown in:

Contributions

M.J.B. designed the study; M.J.B., R.T.O’M. and E.S.B. conducted satellite data analyses and photoacclimation model development; M.J.B. and R.T.O’M. prepared display items; M.J.B. wrote the manuscript with contributions from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Michael J. Behrenfeld.

Supplementary information

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nclimate2838

Further reading