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.

  • Article
  • Published:

Growth responses of a green alga to multiple environmental drivers

Abstract

One feature of global change is that biota must respond not to single, but to multiple environmental drivers. By growing a model photosynthetic microbe in environments containing between one and eight different drivers, including changes in CO2, temperature, and pH, in different combinations, we show that the number as well as the identities of drivers explain shifts in population growth rates. This is because the biotic response to multiple environmental drivers depends on the response to the single dominant driver, and the chance of a driver of large effect being present increases with the number of drivers. Interactions between drivers slightly counteract the expected drop in growth. Our results demonstrate that population growth declines in a predictable way with the number of environmental drivers, and provide an empirically supported model for scaling up from studies on organismal responses to single drivers to predict responses to large numbers of environmental drivers.

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

Access options

Buy this article

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

Figure 1: Cartoon of the effects of multiple drivers on organismal function using an environmental tolerance curve.
Figure 2: Population growth rate of C. reinhardtii under zero to eight environmental drivers.
Figure 3: Population growth rates of C. reinhardtii in test environments containing high CO2, low pH, and high temperature.

Similar content being viewed by others

References

  1. 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 

  2. 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 

  3. Folt, C. & Chen, C. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).

    Article  Google Scholar 

  4. Christensen, M. R. et al. Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob. Change Biol. 12, 2316–2322 (2006).

    Article  Google Scholar 

  5. 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 

  6. Boyd, P. & Brown, C. Modes of interactions between environmental drivers and marine biota. Front. Mar. Sci. 2, 9 (2015).

    Google Scholar 

  7. Gao, K., Ruan, Z. & Villafane, V. Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 54, 1855–1862 (2009).

    Article  CAS  Google Scholar 

  8. Gao, K. et al. Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Clim. Change 2, 519–523 (2012).

    Article  CAS  Google Scholar 

  9. Sciandra, A., Harlay, J. & Lefèvre, D. Response of coccolithophorid Emiliania huxleyi to elevated partial pressure of CO2 under nitrogen limitation. Mar. Ecol. Prog. Ser. 261, 111–122 (2003).

    Article  Google Scholar 

  10. Lefebvre, S. C. et al. Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: Potential implications of ocean acidification for the carbon cycle. Glob. Change Biol. 18, 493–503 (2012).

    Article  Google Scholar 

  11. Feng, Y. et al. Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43, 87–98 (2008).

    Article  CAS  Google Scholar 

  12. Wu, Y., Gao, K. & Riebesell, U. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7, 2915–2923 (2010).

    Article  CAS  Google Scholar 

  13. Fischer, B. B., Rüfenacht, K., Dannenhauer, K., Wiesendanger, M. & Eggen, R. I. L. Multiple stressor effects of high light irradiance and photosynthetic herbicides on growth and survival of the green alga Chlamydomonas reinhardtii. Environ. Toxicol. Chem. 29, 2211–2219 (2010).

    Article  CAS  Google Scholar 

  14. Eyre-Walker, A. & Keightley, P. D. The distribution of fitness effects of new mutations. Nature Rev. Genet. 8, 610–618 (2007).

    Article  CAS  Google Scholar 

  15. Troedsson, C. et al. Effects of ocean acidification, temperature and nutrient regimes on the appendicularian Oikopleura dioica: A mesocosm study. Mar. Biol. 160, 2175–2187 (2012).

    Article  Google Scholar 

  16. Beardall, J., Stojkovic, S. & Larsen, S. Living in a high CO2 world: Impacts of global climate change on marine phytoplankton. Plant Ecol. Divers. 2, 191–205 (2009).

    Article  Google Scholar 

  17. Gruber, N. Warming up, turning sour, losing breath: Ocean biogeochemistry under global change. Phil. Trans. A 369, 1980–96 (2011).

    Article  CAS  Google Scholar 

  18. Lagator, M., Vogwill, T., Mead, A., Colegrave, N. & Neve, P. Herbicide mixtures at high doses slow the evolution of resistance in experimentally evolving populations of Chlamydomonas reinhardtii. New Phytol. 198, 938–945 (2013).

    Article  CAS  Google Scholar 

  19. Falk, S., Samuelsson, G. & Oquist, G. Temperature-dependent photoinhibition and recovery of photosynthesis in the green alga Chlamydomonas reinhardtii acclimated to 12 and 27 °C. Physiol. Planta 78, 173–180 (1990).

    Article  CAS  Google Scholar 

  20. Van Dam, J. W., Negri, A. P., Mueller, J. F., Altenburger, R. & Uthicke, S. Additive pressures of elevated sea surface temperatures and herbicides on symbiont-bearing foraminifera. PLoS ONE 7, e33900 (2012).

    Article  CAS  Google Scholar 

  21. Kobayashi, Y. et al. Algae sense exact temperatures: Small heat shock proteins are expressed at the survival threshold temperature in Cyanidioschyzon merolae and Chlamydomonas reinhardtii. Genome Biol. Evol. 6, 2731–2740 (2014).

    Article  CAS  Google Scholar 

  22. Larras, F. et al. The effect of temperature and a herbicide mixture on freshwater periphytic algae. Ecotoxicol. Environ. Saf. 98, 162–170 (2013).

    Article  CAS  Google Scholar 

  23. Sorokin, C. & Krauss, R. W. The Effects of light intensity on the growth rates of green algae. Plant Physiol. 33, 109–113 (1958).

    Article  CAS  Google Scholar 

  24. Osborne, B. A. & Raven, J. A. Growth light level and photon absorption by cells of Chlamydomonas rheinhardtii, Dunaliella tertiolecta (Chlorophyceae, Volvocales), Scenedesmus obliquus (Chlorophyceae, Chlorococcales) and Euglena viridis (Euglenophyceae, Euglenales). Br. Phycol. J. 21, 303–313 (1986).

    Article  Google Scholar 

  25. Gerloff-Elias, A., Spijkerman, E. & Pröschold, T. Effect of external pH on the growth, photosynthesis and photosynthetic electron transport of Chlamydomonas acidophila Negoro, isolated from an extremely acidic lake (pH 2.6). Plant Cell Environ. 28, 1218–1229 (2005).

    Article  CAS  Google Scholar 

  26. Krause, G. & Weis, E. Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Physiol. Plant Mol. Biol 42, 313–349 (1991).

    Article  CAS  Google Scholar 

  27. Riebesell, U. Effects of CO2 Enrichment on Marine Phytoplankton. J. Oceanogr. 60, 719–729 (2004).

    Article  CAS  Google Scholar 

  28. Collins, S., Sültemeyer, D. & Bell, G. Changes in C uptake in populations of Chlamydomonas reinhardtii selected at high CO2 . Plant Cell Environ. 29, 1812–1819 (2006).

    Article  CAS  Google Scholar 

  29. Engel, A. et al. Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments Marie-Dominique Pizay. Limnol. Oceanogr. 50, 493–507 (2005).

    Article  CAS  Google Scholar 

  30. Merchant, S. S. et al. Between a rock and a hard place: Trace element nutrition in Chlamydomonas. Biochim. Biophys. Acta Mol. Cell Res. 1763, 578–594 (2006).

    Article  CAS  Google Scholar 

  31. Bölling, C. & Fiehn, O. Metabolite profiling of Chlamydomonas reinhardti under nutrient deprivation. Plant Physiol. 139, 1995–2005 (2005).

    Article  Google Scholar 

  32. Wykoff, D. D., Davies, J. P., Melis, A. & Grossman, A. R. The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol. 117, 129–139 (1998).

    Article  CAS  Google Scholar 

  33. Smith, R. C. et al. Ozone depletion: Ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255, 952–959 (1992).

    Article  CAS  Google Scholar 

  34. Sinha, R. P. & Hader, D. P. Life under solar UV radiation in aquatic organisms. Adv. Space Res. 30, 1547–1556 (2002).

    Article  CAS  Google Scholar 

  35. Irihimovitch, V. & Yehudai-Resheff, S. Phosphate and sulfur limitation responses in the chloroplast of Chlamydomonas reinhardtii. FEMS Microbiol. Lett. 283, 1–8 (2008).

    Article  CAS  Google Scholar 

  36. Hartmann, M. et al. Comparison of phosphate uptake rates by the smallest plastidic and aplastidic protists in the North Atlantic subtropical gyre. FEMS Microbiol. Ecol. 78, 327–335 (2011).

    Article  CAS  Google Scholar 

  37. Lin, Y. J., Karuppiah, M., Shaw, A. & Gupta, G. Effect of simulated sunlight on atrazine and metolachlor toxicity of surface waters. Ecotoxicol. Environ. Saf. 43, 35–37 (1999).

    Article  CAS  Google Scholar 

  38. Mayer, P., Frickmann, J., Christensen, E. R. & Nyholm, N. Influence of growth conditions on the results obtained in algal toxicity tests. Environ. Toxicol. Chem. 17, 1091–1098 (1998).

    Article  CAS  Google Scholar 

  39. Harris, E. H. The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use (Academic Press, 1989).

    Google Scholar 

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

    Google Scholar 

  41. Collins, S. Many possible worlds: Expanding the ecological scenarios in experimental evolution. Evol. Biol. 38, 3–14 (2010).

    Article  Google Scholar 

  42. Bell, G. Evolutionary rescue and the limits of adaptation. Phil. Trans. R. Soc. B 368, 1–6 (2013).

    Article  Google Scholar 

  43. Leonardos, N. & Geider, R. J. Elevated atmospheric carbon dioxide increases organic carbon fixation by Emiliania Huxleyi (Haptophyta), under nutrient-limited high-light conditions1. J. Phycol. 41, 1196–1203 (2005).

    Article  CAS  Google Scholar 

  44. Schippers, P., Lurling, M. & Scheffer, M. Increase of atmospheric CO2 promotes phytoplankton productivity. Ecol. Lett. 7, 446–451 (2004).

    Article  Google Scholar 

  45. De Baar, H. J. W. Synthesis of iron fertilization experiments: From the Iron Age in the Age of Enlightenment. J. Geophys. Res. 110, C09S16 (2005).

    Article  Google Scholar 

  46. Hein, M. & Sand-Jensen, K. CO2 increases oceanic primary production. Nature 388, 526–527 (1997).

    Article  CAS  Google Scholar 

  47. Dupont, S. & Portner, H. Get ready for ocean acidification. Nature 498, 429 (2013).

    Article  CAS  Google Scholar 

  48. Hutchins, D. A. et al. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293–1304 (2007).

    Article  CAS  Google Scholar 

  49. Bindoff, N. L. et al. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) Ch. 10, 747–845 (Cambridge Univ. Press, 2007).

    Google Scholar 

  50. Meehl, G. A. et al. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) Ch. 5, 386–432 (Cambridge Univ. Press, 2007).

    Google Scholar 

  51. Müller, P., Li, X. P. & Niyogi, K. K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558–1566 (2001).

    Article  Google Scholar 

  52. Fischer, B. B., Wiesendanger, M. & Eggen, R. I. L. Growth condition-dependent sensitivity, photodamage and stress response of Chlamydomonas reinhardtii exposed to high light conditions. Plant Cell Physiol. 47, 1135–1145 (2006).

    Article  CAS  Google Scholar 

  53. Pröschold, T., Harris, E. H. & Coleman, A. W. Portrait of a species: Chlamydonomas reinhardtii. Genetics 170, 1601–1610 (2005).

    Article  Google Scholar 

  54. Coleman, A. W. & Mai, J. C. Ribosomal DNA and ITS-2 sequence comparisons as a tool for predicting genetic relatedness. J. Mol. Evol. 45, 168–177 (1997).

    Article  CAS  Google Scholar 

  55. Collins, S. & De Meaux, J. Adaptation to different rates of environmental change in Chlamydomonas. Evolution 63, 2952–2965 (2009).

    Article  Google Scholar 

  56. R Core Team R A Language and Environment for Statistical Computing (2013); http://www.R-project.org

    Google Scholar 

Download references

Acknowledgements

We thank N. Colegrave for discussion on experimental design and statistics, J. Hadfield for discussion on statistics, H. Kuehne for technical assistance, and M. Waterfall for assistance with flow cytometry. This work was supported by the European Research Council (ERC) (FP7 grant number 260266) and a Royal Society (UK) University Research Fellowship to S.C.

Author information

Authors and Affiliations

Authors

Contributions

G.B. and S.C. designed the experiment, G.B. performed experiments and S.C. supervised laboratory work. Both authors contributed to statistical analysis and writing the article.

Corresponding author

Correspondence to Sinéad Collins.

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

Brennan, G., Collins, S. Growth responses of a green alga to multiple environmental drivers. Nature Clim Change 5, 892–897 (2015). https://doi.org/10.1038/nclimate2682

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2682

This article is cited by

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