Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass

Abstract

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 global-scale response to eCO2 we derive from experiments is similar to past changes in greenness9 and biomass10 with rising CO2, suggesting that CO2 will continue to stimulate plant biomass in the future despite the constraining effect of soil nutrients. Our research reconciles conflicting evidence on CO2 fertilization across scales and provides an empirical estimate of the biomass sensitivity to eCO2 that may help to constrain climate projections.

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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 https://github.com/cesarterrer/CO2_Upscaling.

References

  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).

  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).

  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).

  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).

  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).

  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).

  7. 7.

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

  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).

  10. 10.

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

  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).

  12. 12.

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

  13. 13.

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

  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).

  15. 15.

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

  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).

  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).

  18. 18.

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

  19. 19.

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

  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).

  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).

  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).

  24. 24.

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

  25. 25.

    Soudzilovskaia, N. A. et al. Global mycorrhizal plants distribution linked to terrestrial carbon stocks. Preprint at bioRxiv https://www.biorxiv.org/content/10.1101/331884v2 (2018).

  26. 26.

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

  27. 27.

    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).

  28. 28.

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

  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).

  30. 30.

    Riley, W. J., Zhu, Q. & Tang, J. Y. Weaker land–climate feedbacks from nutrient uptake during photosynthesis-inactive periods. Nat. Clim. Change 202, 1002–1006 (2018).

  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).

  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).

  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).

  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).

  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).

  36. 36.

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

  37. 37.

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

  38. 38.

    Van Lissa, C. J. MetaForest: exploring heterogeneity in meta-analysis using random forests. Preprint at https://psyarxiv.com/myg6s/ (2017).

  39. 39.

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

  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).

  41. 41.

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

  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).

  43. 43.

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

  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).

  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).

  48. 48.

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

  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).

  50. 50.

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

  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).

  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).

  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).

  54. 54.

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

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Acknowledgements

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.

Correspondence to César Terrer.

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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.

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

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