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Revaluating ocean warming impacts on global phytoplankton

Nature Climate Change volume 6, pages 323–330 (2016)Cite this article

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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.

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Figure 1: Photophysiology of phytoplankton.
Figure 2: Modelling photoacclimation in the surface ocean mixed layer.
Figure 3: Carbon-to-chlorophyll (θ) variability in the global ocean.
Figure 4: Temporal patterns in satellite-observed carbon-to-chlorophyll (θ) and model-based variability attributable to photoacclimation.
Figure 5: Physiological contributions to global chlorophyll anomalies.

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References

  1. Irwin, A. J. & Oliver, M. J. Are ocean deserts getting larger? Geophys. Res. Lett. 36, L18609 (2009).

    Article  Google Scholar 

  2. McClain, C. R., Signorini, S. R. & Christian, J. R. Subtropical gyre variability observed by ocean-color satellites. Deep-Sea Res. II 51, 281–301 (2004).

    Article  CAS  Google Scholar 

  3. Polovina, J. J., Howell, E. A. & Abecassis, M. Ocean’s least productive waters are expanding. Geophys. Res. Lett. 35, 3618 (2008).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Behrenfeld, M. J., Halsey, K. & Milligan, A. Evolved physiological responses of phytoplankton to their integrated growth environment. Phil. Trans. R. Soc. B 363, 2687–2703 (2008).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. 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 

  8. Gregg, W. W., Casey, N. W. & McClain, C. R. Recent trends in global ocean chlorophyll. Geophys. Res. Lett. 32, L03606 (2005).

    Google Scholar 

  9. Kahru, M., Kudela, R., Manzano-Sarabia, M. & Mitchell, B. G. Trends in primary production in the California Current detected with satellite data. J. Geophys. Res. 114, C02004, 10340 (2009).

    Article  Google Scholar 

  10. Boyce, D. G., Lewis, M. L. & Worm, B. Global phytoplankton decline over the past century. Nature 466, 591–596 (2010).

    Article  CAS  Google Scholar 

  11. Laws, E. A. & Bannister, T. T. 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).

    Article  CAS  Google Scholar 

  12. Geider, R. J. 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).

    Article  CAS  Google Scholar 

  13. 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 

  14. Halsey, K. H. & Jones, B. M. Phytoplankton strategies for photosynthetic energy allocation. Annu. Rev. Mar. Sci. 7, 265–297 (2015).

    Article  Google Scholar 

  15. Escoubas, J. 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).

    Article  CAS  Google Scholar 

  16. Durnford, D. G. & Falkowski, P. G. Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth. Res. 53, 229–241 (1997).

    Article  CAS  Google Scholar 

  17. Oelze, M., Kandlbinder, A. & Dietz, K. Redox regulation and overreduction control in the photosynthesizing cell: Complexity in redox networks. Biochim. Biophys. 1780, 1261–1272 (2008).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  19. Cooley, J., Howitt, C. & Vermaas, W. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Behrenfeld, M. J. & Milligan, A. J. Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5, 217–246 (2013).

    Article  Google Scholar 

  22. Fujiki, T., Hosaka, T., Kimoto, H., Ishimaru, T. & Saino, T. 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).

    Article  CAS  Google Scholar 

  23. Peltier, G. & Cournac, L. Chlororespiration. Ann. Rev. Plant Biol. 53, 523–550 (2002).

    Article  CAS  Google Scholar 

  24. Vermaas, W. F. J. Encyclopedia of Life Sciences (John Wiley, 2001).

    Google Scholar 

  25. Behrenfeld, M. J., Marañón, E., Siegel, D. A. & Hooker, S. B. A photoacclimation and nutrient based model of light-saturated photosynthesis for quantifying oceanic primary production. Mar. Ecol. Prog. Ser. 228, 103–117 (2002).

    Article  CAS  Google Scholar 

  26. MacIntyre, H. L., Kana, T. M., Anning, T. & Geider, R. J. Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J. Phycol. 38, 17–38 (2002).

    Article  Google Scholar 

  27. Westberry, T. K., Behrenfeld, M. J., Siegel, D. A. & Boss, E. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22, GB2024 (2008).

    Article  Google Scholar 

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

    Article  Google Scholar 

  29. Behrenfeld, M. J. & Falkowski, P. G. A consumer’s guide to phytoplankton primary productivity models. Limnol. Oceanogr. 42, 1479–1491 (1997).

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Maritorena, S., Siegel, D. A. & Peterson, A. R. Optimization of a semianalytical ocean color model for global-scale applications. Appl. Opt. 41, 2705–2714 (2002).

    Article  Google Scholar 

  32. Lee, Z. P., Carder, K. L. & Arnone, R. A. Deriving inherent optical properties from water color: A multi-band quasi-analytical algorithm for optically deep waters. Appl. Opt. 41, 5755–5772 (2002).

    Article  Google Scholar 

  33. Huot, Y., Morel, A., Twardowski, M. S., Stramski, D. & Reynolds, R. A. Particle optical backscattering along a chlorophyll gradient in the upper layer of the eastern South Pacific Ocean. Biogeoscience 5, 495–507 (2008).

    Article  CAS  Google Scholar 

  34. Martinez-Vicente, V., Dall’olmo, G., Tarran, G., Boss, E. & Sathyendranath, S. Optical backscattering is correlated with phytoplankton carbon across the Atlantic Ocean. Geophys. Res. Lett. 40, 1154–1158 (2013).

    Article  CAS  Google Scholar 

  35. Graff, J. R., Milligan, A. J. & Behrenfeld, M. J. The measurement of phytoplankton biomass using flow-cytometric sorting and elemental analysis of carbon. Limnol. Oceanogr. Method 10, 910–920 (2012).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Mitchell, B. G. & Kahru, M. Bio-optical algorithms for ADEOS-2 GLI. J. Remote Sens. Soc. Jpn 29, 80–85 (2009).

    Google Scholar 

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

    Article  Google Scholar 

  39. Westberry, T. K., Boss, E. & Lee, Z. The influence of Raman scattering on ocean color inversion models. Appl. Opt. 52, 5552–5561 (2013).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  42. Lozier, M. S., Dave, A. C., Palter, J. B., Gerber, L. M. & Barber, R. T. On the relationship between stratification and primary productivity in the North Atlantic. Geophys. Res. Lett. 38, L18609 (2011).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  44. Doney, S. C. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  46. Boyd, P. W., Lennartz, S. T., Glover, D. M. & Doney, S. C. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nature Clim. Change 5, 71–79 (2015).

    Article  Google Scholar 

  47. Halsey, K. H., Milligan, A. J. & Behrenfeld, M. J. Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites 4, 260–280 (2014).

    Article  Google Scholar 

Download references

Acknowledgements

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

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Authors and 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

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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.

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Correspondence to Michael J. Behrenfeld.

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Behrenfeld, M., O’Malley, R., Boss, E. et al. Revaluating ocean warming impacts on global phytoplankton. Nature Clim Change 6, 323–330 (2016). https://doi.org/10.1038/nclimate2838

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