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.

Biological ramifications of climate-change-mediated oceanic multi-stressors

Nature Climate Change volume 5, pages 71–79 (2015)Cite this article

Subjects

Abstract

Climate change is altering oceanic conditions in a complex manner, and the concurrent amendment of multiple properties will modify environmental stress for primary producers. So far, global modelling studies have focused largely on how alteration of individual properties will affect marine life. Here, we use global modelling simulations in conjunction with rotated factor analysis to express model projections in terms of regional trends in concomitant changes to biologically influential multi-stressors. Factor analysis demonstrates that regionally distinct patterns of complex oceanic change are evident globally. Preliminary regional assessments using published evidence of phytoplankton responses to complex change reveal a wide range of future responses to interactive multi-stressors with <20–300% shifts in phytoplankton physiological rates, and many unexplored potential interactions. In a future ocean, provinces will encounter different permutations of change that will probably alter the dominance of key phytoplankton groups and modify regional productivity, ecosystem structure and biogeochemistry. Consideration of regionally distinct multi-stressor patterns can help guide laboratory and field studies as well as the interpretation of interactive multi-stressors in global models.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Global maps of the change in four illustrative ocean properties between the decades (mean of 2081–2100) minus present (mean 1981–2000) from the CESM1(BEC) model simulations.
Figure 2: Relationship between global and regional climate-driven trends in ocean properties.
Figure 3: Results of the factor analysis (Factors 1–6) based on data presented in Fig. 1 (two-dimensional global maps of the change in each ocean property between the decades 2081–2100 minus 1981–2000).

References

  1. Doney, S. C. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512–1516 (2010).

    Article  CAS  Google Scholar 

  2. Gruber, N. Warming up, turning sour, losing breath: Ocean biogeochemistry under global change. Phil. Trans. R. Soc. A 369, 1980–1996 (2011).

    Article  CAS  Google Scholar 

  3. IPCC Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

    Google Scholar 

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

    Article  Google Scholar 

  5. Riebesell, U. & Tortell, P. in Ocean Acidification (eds Gattuso, J-P. & Hansson, L.) 99–116 (Oxford Univ. Press, 2011).

    Google Scholar 

  6. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Article  CAS  Google Scholar 

  7. Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: Projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).

    Article  Google Scholar 

  8. Hood, R. R. et al. Pelagic functional group modeling: Progress, challenges and prospects. Deep-Sea Res. II 53, 459–512 (2006).

    Article  Google Scholar 

  9. Dutkiewicz, S., Scott, J. R. & Follows, M. J. Winners and losers: Ecological and biogeochemical changes in a warming ocean. Glob. Biogeochem. Cycles 27, 463–477 (2013).

    Article  CAS  Google Scholar 

  10. Boyd, P. W., Strzepek, R., Fu, F. X. & Hutchins, D. A. Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnol. Oceanogr. 55, 1353–1376 (2010).

    Article  CAS  Google Scholar 

  11. Boyd, P. W. & Hutchins, D. A. Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar. Ecol. Prog. Ser. 470, 125–135 (2012).

    Article  Google Scholar 

  12. Edwards, M., Reid, P. C. & Planque, B. Long-term and regional variability of phytoplankton biomass in the Northeast Atlantic (1960–1995). ICES J. Mar. Sci. 58, 39–49 (2001).

    Article  Google Scholar 

  13. Folt, C. L., Chen, C. Y., Moore, M. V. & Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).

    Article  Google Scholar 

  14. Rose, J. M. et al. Synergistic effects of iron and temperature on Antarctic phytoplankton and microzooplankton assemblages. Biogeosciences 6, 3131–3147 (2009).

    Article  CAS  Google Scholar 

  15. Hurrell, J. W. et al. The Community Earth System Model: A framework for collaborative research. Bull. Am. Meteorol. Soc. 94, 1339–1360 (2013).

    Article  Google Scholar 

  16. Moore, J. K., Lindsay, K., Doney, S. C., Long, M. C. & Misumi, K. Marine ecosystem dynamics and biogeochemical cycling in the Community Earth System Model CESM1(BGC). J. Clim. 26, 9291–9321 (2013).

    Article  Google Scholar 

  17. Steinacher, M., Joos, F., Frölicher, T. L., Plattner, G-K. & Doney, S. C. Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6, 515–533 (2009).

    Article  CAS  Google Scholar 

  18. Boyd, P. W. & Doney, S. C. Modelling regional responses by marine pelagic ecosystems to global climate change. Geophys. Res. Lett. 29, 531–534 (2002).

    Article  Google Scholar 

  19. Moore, C. M. et al. Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nature Geosci. 2, 867–871 (2009).

    Article  CAS  Google Scholar 

  20. Boyd, P. W. et al. Marine phytoplankton temperature versus growth responses from polar to tropical waters---Outcome of a scientific community-wide study. PLoS ONE 8, e63091 (2013).

    Article  CAS  Google Scholar 

  21. Hutchins, D. A. & Bruland, K. W. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature 393, 561–564 (1998).

    Article  CAS  Google Scholar 

  22. Feng, Y. et al. Effects of increased p CO 2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Mar. Ecol. Prog. Ser. 388, 13–25 (2009).

    Article  CAS  Google Scholar 

  23. Fu, F-X., Warner, M. E., Zhang, Y., Feng, Y. & Hutchins, D. A. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43, 485–496 (2007).

    Article  Google Scholar 

  24. Balch, W. M. et al. The contribution of coccolithophores to the optical and inorganic carbon budgets during the Southern Ocean Gas Experiment: New evidence in support of the “Great Calcite Belt” hypothesis. J. Geophys. Res. 116 (Special Issue, C00F06), 1–14 (2011).

    Article  Google Scholar 

  25. Johnson, Z. I. et al. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311, 1737–1740 (2006).

    Article  CAS  Google Scholar 

  26. Ward, B. A., Dutkiewicz, S., Moore, C. M. & Follows, M. J. Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol. Oceanogr. 58, 2059–2075 (2013).

    Article  CAS  Google Scholar 

  27. Hutchins, D. A., Fu, F-X., Webb, E. A., Walworth, N. & Tagliabue, A. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nature Geosci. 6, 790–795 (2013).

    Article  CAS  Google Scholar 

  28. Strzepek, R. F., Hunter, K. A., Frew, R. D., Harrison, P. J. & Boyd, P. W. Iron–light interactions differ in Southern Ocean phytoplankton. Limnol. Oceanogr. 57, 1182–1200 (2012).

    Article  CAS  Google Scholar 

  29. Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).

    Article  CAS  Google Scholar 

  30. Nielsdóttir, 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 

  31. Zondervan, I. The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—a review. Deep-Sea Res. II 54, 521–537 (2007).

    Article  Google Scholar 

  32. Tortell, P. D. et al. CO2 sensitivity of Southern Ocean phytoplankton. Geophys. Res. Lett. 35, L04605 (2008).

    Article  Google Scholar 

  33. Flombaum, P. et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  35. Mulholland, M. R. The fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences 4, 37–51 (2007).

    Article  CAS  Google Scholar 

  36. Hutchins, D. A., Mulholland, M. R. & Fu, F-X. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22, 128–145 (2009).

    Article  Google Scholar 

  37. Thomalla, S. J. et al. Variable export fluxes and efficiencies for calcite, opal, and organic carbon in the Atlantic Ocean: A ballast effect in action? Glob. Biogeochem. Cycles 22, GB1010 (2008).

    Article  Google Scholar 

  38. Geider, R. J., MacIntyre, H. L. & Kana, T. M. A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients, and temperature. Limnol. Oceanogr. 43, 679–694 (1998).

    Article  CAS  Google Scholar 

  39. Marinov, I. et al. North–south asymmetry in the modeled phytoplankton response to climate change over the 21st century. Glob. Biogeochem. Cycles 27, 1274–1290 (2013).

    Article  CAS  Google Scholar 

  40. Oschlies, A., Schulz, K. G., Riebesell, U. & Schmittner, A. Simulated 21st century’s increase in oceanic suboxia by CO2-enhanced biotic carbon export. Glob. Biogeochem. Cycles 22, GB4008 (2008).

    Article  Google Scholar 

  41. Gehlen, M., Gruber, N., Gangsto, R., Bopp, L. & Oschlies, A. in Ocean Acidification (eds Gattuso, J-P. & Hansson, L.) Ch. 12, (Oxford Univ. Press, 2011).

    Google Scholar 

  42. Moore, J. K., Doney, S. C. & Lindsay, K. Upper ocean ecosystem dynamics and iron cycling in a global 3-D model. Glob. Biogeochem. Cycles 18, GB4028 (2004).

    Article  Google Scholar 

  43. Glover, D. M., Jenkins, W. J. & Doney, S. C. Modeling Methods for Marine Science 571 (Cambridge Univ. Press, 2011).

    Book  Google Scholar 

  44. Conte, M. H., Thompson, A. T., Lesley, D. & Harris, R. P. Genetic and physiological influences on the alkenone/alkenoate versus growth temperature relationship in Emiliania huxleyi and Gephyrocapsa oceanica. Geochim. Cosmochim. Acta 62, 51–68 (1998).

    Article  CAS  Google Scholar 

  45. Langer, G. et al. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem. Geophys. Geosyst. 7, Q09006 (2006).

    Article  Google Scholar 

  46. Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nature Clim. Change 3, 979–984 (2013).

    Article  CAS  Google Scholar 

  47. Boyd, P. W., LaRoche, J., Gall, M., Frew, R. & McKay, R. M. L. Role of iron, light, and silicate in controlling algal biomass in subantarctic waters SE of New Zealand. J. Geophys. Res. 104, 13395–13408 (1999).

    Article  CAS  Google Scholar 

  48. Martin-Jezequel, V. et al. Silicon metabolism in diatoms: Implications for growth. J. Phycol. 36, 821–840 (2000).

    Article  CAS  Google Scholar 

  49. Boyd, P. W. et al. Control of phytoplankton growth by iron supply and irradiance in the subantarctic Southern Ocean: Experimental results from the SAZ Project. J. Geophys. Res. 106, 31573–31583 (2001).

    Article  CAS  Google Scholar 

  50. Winter, A., Nendriks, J., Beaufort, L., Rickaby, R. E. M. & Brown, C. W. Poleward expansion of coccolithophores Emiliania huxleyi. J. Plankton Res. 36, 316–325 (2013).

    Article  Google Scholar 

Download references

Acknowledgements

S.C.D. acknowledges support from the Center for Microbial Oceanography Research and Education (C-MORE; grant EF-0424599), a National Science Foundation Science and Technology Center. P.W.B. acknowledges support from IMAS, University of Tasmania. S.T.L. acknowledges support from H. Biester and Heinrich-Boell-Foundation.

Author information

Authors and Affiliations

  1. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania 7005, Australia

    Philip W. Boyd

  2. Institute for Geoecology, TU Braunschweig, 38106 Braunschweig, Germany

    Sinikka T. Lennartz

  3. Geomar, Helmholtz-Center for Oceanographic Research, 24105 Kiel, Germany

    Sinikka T. Lennartz

  4. Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA

    David M. Glover & Scott C. Doney

Authors
  1. Philip W. Boyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sinikka T. Lennartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David M. Glover
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Scott C. Doney
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.W.B. and S.C.D. designed the study; S.T.L. carried out the statistical analyses and provided the display items; D.M.G. carried out the statistical analysis; P.W.B. wrote the manuscript with contributions from S.C.D., S.T.L. and D.M.G.

Corresponding author

Correspondence to Philip W. Boyd.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boyd, P., Lennartz, S., Glover, D. et al. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nature Clim Change 5, 71–79 (2015). https://doi.org/10.1038/nclimate2441

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2441

This article is cited by

Search

Advanced 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