Skip to main content

Thank you for visiting 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.

Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass

An Author Correction to this article was published on 26 May 2020

This article has been updated


Elevated CO2 (eCO2) experiments provide critical information to quantify the effects of rising CO2 on vegetation1,2,3,4,5,6. Many eCO2 experiments suggest that nutrient limitations modulate the local magnitude of the eCO2 effect on plant biomass1,3,5, but the global extent of these limitations has not been empirically quantified, complicating projections of the capacity of plants to take up CO27,8. Here, we present a data-driven global quantification of the eCO2 effect on biomass based on 138 eCO2 experiments. The strength of CO2 fertilization is primarily driven by nitrogen (N) in ~65% of global vegetation and by phosphorus (P) in ~25% of global vegetation, with N- or P-limitation modulated by mycorrhizal association. Our approach suggests that CO2 levels expected by 2100 can potentially enhance plant biomass by 12 ± 3% above current values, equivalent to 59 ± 13 PgC. The future effect of eCO2 we derive from experiments is geographically consistent with past changes in greenness9, but is considerably lower than the past effect derived from models10. If borne out, our results suggest that the stimulatory effect of CO2 on carbon storage could slow considerably this century. Our research provides an empirical estimate of the biomass sensitivity to eCO2 that may help to constrain climate projections.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Soil C:N and soil P are key plant resources driving the CO2 fertilization effect on above-ground biomass.
Fig. 2: Potential above-ground biomass enhancement in terrestrial ecosystems under elevated CO2.
Fig. 3: Comparison of the global effect of elevated CO2 with existing independent approaches.

Data availability

The biomass data from CO2 experiments summarized in Supplementary Fig. 2 supporting the findings of this study are available in published papers, and soil and climate data required to upscale CO2 effects are available in published datasets (Supplementary Table 2). Raw data can be obtained from the corresponding author on reasonable request.

Code availability

The R code used in the analysis presented in this paper is available online and can be accessed at

Change history

  • 26 May 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.


  1. 1.

    Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).

    CAS  Google Scholar 

  2. 2.

    McCarthy, H. R. et al. Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytol. 185, 514–528 (2010).

    CAS  Google Scholar 

  3. 3.

    Reich, P. B., Hobbie, S. E. & Lee, T. D. Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation. Nat. Geosci. 7, 920–924 (2014).

    CAS  Google Scholar 

  4. 4.

    Terrer, C., Vicca, S., Hungate, B. A., Phillips, R. P. & Prentice, I. C. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353, 72–74 (2016).

    CAS  Google Scholar 

  5. 5.

    Ellsworth, D. S. et al. Elevated CO2 does not increase eucalypt forest productivity on a low-phosphorus soil. Nat. Clim. Change 320, 279–282 (2017).

    Google Scholar 

  6. 6.

    Ainsworth, E. A. & Long, S. P. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 165, 351–372 (2005).

    Google Scholar 

  7. 7.

    Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).

    Google Scholar 

  8. 8.

    Ciais, P. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) 465–570 (IPCC, Cambridge Univ. Press, 2013).

  9. 9.

    Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).

    CAS  Google Scholar 

  10. 10.

    Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).

    CAS  Google Scholar 

  11. 11.

    Keenan, T. et al. Recent pause in the growth rate of atmospheric CO2 due to enhanced terrestrial carbon uptake. Nat. Commun. 7, 13428 (2016).

    CAS  Google Scholar 

  12. 12.

    Le Quéré, C. et al. Global Carbon Budget 2018. Earth Syst. Sci. Data 10, 2141–2194 (2018).

    Google Scholar 

  13. 13.

    Campbell, J. E. et al. Large historical growth in global terrestrial gross primary production. Nature 544, 84–87 (2017).

    CAS  Google Scholar 

  14. 14.

    Schimel, D., Stephens, B. B. & Fisher, J. B. Effect of increasing CO2 on the terrestrial carbon cycle. Proc. Natl Acad. Sci. USA 112, 436–441 (2015).

    CAS  Google Scholar 

  15. 15.

    Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).

    CAS  Google Scholar 

  16. 16.

    Hoosbeek, M. R. Elevated CO2 increased phosphorous loss from decomposing litter and soil organic matter at two FACE experiments with trees. Biogeochemistry 127, 89–97 (2016).

    CAS  Google Scholar 

  17. 17.

    Fernández-Martínez, M. et al. Global trends in carbon sinks and their relationships with CO2 and temperature. Nat. Clim. Change 10, 1–79 (2018).

    Google Scholar 

  18. 18.

    Liu, Y. Y. et al. Recent reversal in loss of global terrestrial biomass. Nat. Clim. Change 5, 470–474 (2015).

    Google Scholar 

  19. 19.

    Ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).

    CAS  Google Scholar 

  20. 20.

    Nasto, M. K., Winter, K., Turner, B. L. & Cleveland, C. C. Nutrient acquisition strategies augment growth in tropical N2 fixing trees in nutrient poor soil and under elevated CO2. Ecology 100, e02646 (2019).

  21. 21.

    Cernusak, L. A. et al. Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiol. 157, 372–385 (2011).

    CAS  Google Scholar 

  22. 22.

    Qie, L. et al. Long-term carbon sink in Borneo’s forests halted by drought and vulnerable to edge effects. Nat. Commun. 8, 1966 (2017).

    Google Scholar 

  23. 23.

    Almeida Castanho, A. D. et al. Changing Amazon biomass and the role of atmospheric CO2 concentration, climate, and land use. Glob. Biogeochem. Cycles 30, 18–39 (2016).

    Google Scholar 

  24. 24.

    Soudzilovskaia, N. A. et al. Global mycorrhizal plants distribution linked to terrestrial carbon stocks. Preprint at bioRxiv (2018).

  25. 25.

    Hodge, A. & Storer, K. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386, 1–19 (2015).

    CAS  Google Scholar 

  26. 26.

    Terrer, C. et al. Ecosystem responses to elevated CO2 governed by plant–soil interactions and the cost of nitrogen acquisition. New Phytol. 217, 507–522 (2018).

    CAS  Google Scholar 

  27. 27.

    Peñuelas, J. et al. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4, 2934 (2013).

    Google Scholar 

  28. 28.

    De Kauwe, M. G., Keenan, T., Medlyn, B. E., Prentice, I. C. & Terrer, C. Satellite based estimates underestimate the effect of CO2 fertilization on net primary productivity. Nat. Clim. Change 6, 892–893 (2016).

    Google Scholar 

  29. 29.

    Wieder, W. R., Cleveland, C. C., Smith, W. K. & Todd-Brown, K. Future productivity and carbon storage limited by terrestrial nutrient availability. Nat. Geosci. 8, 441–444 (2015).

    CAS  Google Scholar 

  30. 30.

    Medlyn, B. E. et al. Using ecosystem experiments to improve vegetation models. Nat. Clim. Change 5, 528–534 (2015).

    Google Scholar 

  31. 31.

    Dieleman, W. I. J. et al. Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob. Change Biol. 18, 2681–2693 (2012).

    Google Scholar 

  32. 32.

    Baig, S., Medlyn, B. E., Mercado, L. M. & Zaehle, S. Does the growth response of woody plants to elevated CO2 increase with temperature? A model-oriented meta-analysis. Glob. Change Biol. 21, 4303–4319 (2015).

    Google Scholar 

  33. 33.

    Terrer, C. et al. Response to comment on ‘Mycorrhizal association as a primary control of the CO2 fertilization effect’. Science 355, 358–358 (2017).

    CAS  Google Scholar 

  34. 34.

    Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642 (2014).

    Google Scholar 

  35. 35.

    Maherali, H., Oberle, B., Stevens, P. F., Cornwell, W. K. & McGlinn, D. J. Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am. Nat. 188, E113–E125 (2016).

    Google Scholar 

  36. 36.

    Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).

    CAS  Google Scholar 

  37. 37.

    Stekhoven, D. J. & Buhlmann, P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics 28, 112–118 (2011).

    Google Scholar 

  38. 38.

    Van Lissa, C. J. MetaForest: exploring heterogeneity in meta-analysis using random forests. Preprint at (2017).

  39. 39.

    Viechtbauer, W. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 3 (2010).

    Google Scholar 

  40. 40.

    Calcagno, V. & de Mazancourt, C. glmulti: an R package for easy automated model selection with (generalized) linear models. Journal of Statistical Software 34, 12 (2010).

    Google Scholar 

  41. 41.

    Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).

    Google Scholar 

  42. 42.

    Osenberg, C. W., Sarnelle, O., Cooper, S. D. & Holt, R. D. Resolving ecological questions through meta-analysis: goals, metrics, and models. Ecology 80, 1105–1117 (1999).

    Google Scholar 

  43. 43.

    Rubin, D. B. & Schenker, N. Multiple imputation in health-care databases: an overview and some applications. Stat. Med. 10, 585–598 (1991).

    CAS  Google Scholar 

  44. 44.

    Lajeunesse, M. J. Facilitating systematic reviews, data extraction and meta-analysis with the metagear package for R. Methods Ecol. Evol. 7, 323–330 (2016).

    Google Scholar 

  45. 45.

    Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. in Introduction to Meta-Analysis (eds Borenstein, M. et al.) 225–238 (John Wiley & Sons, Ltd, 2009).

  46. 46.

    Del Re, A. C. & Hoyt, W. T. MAd: meta-analysis with mean differences. R version 0.8-2 (2014).

  47. 47.

    Batjes, N. H. Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks. Geoderma 269, 61–68 (2016).

    CAS  Google Scholar 

  48. 48.

    Post, W. M., Pastor, J., Zinke, P. J. & Stangenberger, A. G. Global patterns of soil nitrogen storage. Nature 317, 613–616 (1985).

    Google Scholar 

  49. 49.

    Jiao, F., Shi, X.-R., Han, F.-P. & Yuan, Z.-Y. Increasing aridity, temperature and soil pH induce soil C-N-P imbalance in grasslands. Sci. Rep. 6, 19601 (2016).

    CAS  Google Scholar 

  50. 50.

    Wang, C. et al. Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat. Commun. 5, 4799 (2013).

    Google Scholar 

  51. 51.

    Zomer, R. J., Trabucco, A., Bossio, D. A. & Verchot, L. V. Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric. Ecosyst. Environ. 126, 67–80 (2008).

    Google Scholar 

  52. 52.

    Billings, S. A., Schaeffer, S. M. & Evans, R. D. Trace N gas losses and N mineralization in Mojave Desert soils exposed to elevated CO2. Soil Biol. Biochem. 34, 1777–1784 (2002).

    CAS  Google Scholar 

  53. 53.

    Evans, R. D. et al. Greater ecosystem carbon in the Mojave Desert after ten years exposure to elevated CO2. Nat. Clim. Change 4, 394–397 (2014).

    CAS  Google Scholar 

  54. 54.

    Pan, Y. et al. A large and persistent carbon sink in the world's forests. Science 333, 988–993 (2011).

    CAS  Google Scholar 

Download references


We thank C. Körner, R. Norby, M. Schneider, Y. Carrillo, E. Pendall, B. Kimball, M. Watanabe, T. Koike, G. Smith, S.J. Tumber-Davila, T. Hasegawa, B. Sigurdsson, S. Hasegawa, A.L. Abdalla-Filho and L. Fenstermaker for sharing data and advice. This research is a contribution to the AXA Chair Programme in Biosphere and Climate Impacts and the Imperial College initiative Grand Challenges in Ecosystems and the Environment. Part of this research was developed in the Young Scientists Summer Program at the International Institute for Systems Analysis, Laxenburg (Austria) with financial support from the Natural Environment Research Council (UK). C.T. also acknowledges financial support from the Spanish Ministry of Science, Innovation and Universities through the María de Maeztu programme for Units of Excellence (grant no. MDM-2015-0552). I.C.P. acknowledges support from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant no. 787203 REALM). S.V. and K.v.S. acknowledge support from the Fund for Scientific Research, Flanders (Belgium). T.F.K. acknowledges support by the Director, Office of Science, Office of Biological and Environmental Research of the US Department of Energy under contract DE-AC02-05CH11231 as part of the RuBiSCo SFA. J.P. acknowledges support from the European Research Council through Synergy grant no. ERC-2013-SyG-610028 ‘IMBALANCE-P’. T.F.K. and J.B.F. were supported in part by NASA IDS Award no. NNH17AE86I. J.B.F. was also supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research. J.B.F. contributed to this research from Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration. California Institute of Technology. N.A.S. was supported by Vidi grant no. 016.161.318 by the Netherlands Organization for Scientific Research. This paper is a contribution to the Global Carbon Project.

Author information




The study was originally conceived and developed by C.T., with ideas and contributions by R.J., I.C.P., O.F., T.F.K., P.B.R., C.K., S.V, B.S. and J.B.F. Data from DGVMs were analysed by T.F.K. Analysis of drivers was done by C.T and P.B.R. Statistical analysis was carried out by C.T., C.J.v.L. and W.V. Spatial analysis was done by C.T. and I.M. P.B.R., B.A.H., L.A.C., A.F.T., P.C.D.N., M.J.H., D.M.B., C.M., K.W., C.B.F., M.R.H., M.W., T.K., H.W.P. and many others ran the experiments. The initial manuscript was written by C.T. with input from all authors.

Corresponding author

Correspondence to César Terrer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information: Nature Climate Change thanks Shu Kee Lam, Bassil El Masri and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Discussion, Figs. 1–8, Tables 1–5 and references.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Terrer, C., Jackson, R.B., Prentice, I.C. et al. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat. Clim. Chang. 9, 684–689 (2019).

Download citation

Further reading


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