Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass (original) (raw)

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.

Change history

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

References

  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. 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. 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. 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. 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. 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. Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).
    Google Scholar
  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. Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).
    CAS Google Scholar
  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. 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. Le Quéré, C. et al. Global Carbon Budget 2018. Earth Syst. Sci. Data 10, 2141–2194 (2018).
    Google Scholar
  13. Campbell, J. E. et al. Large historical growth in global terrestrial gross primary production. Nature 544, 84–87 (2017).
    CAS Google Scholar
  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. 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. 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. 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. Liu, Y. Y. et al. Recent reversal in loss of global terrestrial biomass. Nat. Clim. Change 5, 470–474 (2015).
    Google Scholar
  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. 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. 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. 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. 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. 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).
  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. 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. 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. 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. 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. Medlyn, B. E. et al. Using ecosystem experiments to improve vegetation models. Nat. Clim. Change 5, 528–534 (2015).
    Google Scholar
  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. 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. 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. 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. 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. Wang, B. & Qiu, Y. L. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363 (2006).
    CAS Google Scholar
  37. Stekhoven, D. J. & Buhlmann, P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics 28, 112–118 (2011).
    Google Scholar
  38. Van Lissa, C. J. MetaForest: exploring heterogeneity in meta-analysis using random forests. Preprint at https://psyarxiv.com/myg6s/ (2017).
  39. Viechtbauer, W. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 3 (2010).
    Google Scholar
  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. 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. 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. 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. 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. 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. Del Re, A. C. & Hoyt, W. T. MAd: meta-analysis with mean differences. R version 0.8-2 (2014).
  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. 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. 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. 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. 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. 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. 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. Pan, Y. et al. A large and persistent carbon sink in the world's forests. Science 333, 988–993 (2011).
    CAS Google Scholar

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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

Authors and Affiliations

  1. Department of Earth System Science, Stanford University, Stanford, CA, USA
    César Terrer & Robert B. Jackson
  2. Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Barcelona, Spain
    César Terrer
  3. Ecosystems Services and Management Program, International Institute for Applied Systems Analysis, Laxenburg, Austria
    César Terrer, Ian McCallum & Oskar Franklin
  4. Woods Institute for the Environment and Precourt Institute for Energy, Stanford University, Stanford, CA, USA
    Robert B. Jackson & Christopher B. Field
  5. AXA Chair Programme in Biosphere and Climate Impacts, Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, UK
    I. Colin Prentice
  6. Department of Biological Sciences, Macquarie University, North Ryde, New South Wales, Australia
    I. Colin Prentice
  7. Department of Earth System Science, Tsinghua University, Beijing, China
    I. Colin Prentice
  8. Department of Environmental Science, Policy and Management, UC Berkeley, Berkeley, CA, USA
    Trevor F. Keenan
  9. Climate and Ecosystem Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
    Trevor F. Keenan
  10. Department of Microbiology and Ecosystem Science, Division of Terrestrial Ecosystem Research, Faculty of Life Sciences, University of Vienna, Vienna, Austria
    Christina Kaiser
  11. Evolution and Ecology Program, International Institute for Applied Systems Analysis, Laxenburg, Austria
    Christina Kaiser
  12. Centre of Excellence PLECO (Plants and Ecosystems), Biology Department, University of Antwerp, Wilrijk, Belgium
    Sara Vicca & Kevin Van Sundert
  13. Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA, USA
    Joshua B. Fisher
  14. Joint Institute for Regional Earth System Science and Engineering, University of California at Los Angeles, Los Angeles, CA, USA
    Joshua B. Fisher
  15. Department of Forest Resources, University of Minnesota, St. Paul, MN, USA
    Peter B. Reich
  16. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia
    Peter B. Reich
  17. CREAF, Cerdanyola del Vallès, Spain
    Benjamin D. Stocker & Josep Peñuelas
  18. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA
    Bruce A. Hungate & Victor O. Leshyk
  19. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA
    Bruce A. Hungate & Victor O. Leshyk
  20. CSIC, Global Ecology Unit CREAF-CEAB-UAB, Bellaterra, Spain
    Josep Peñuelas
  21. Environmental Biology Department, Institute of Environmental Sciences, Leiden University, Leiden, the Netherlands
    Nadejda A. Soudzilovskaia
  22. College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland, Australia
    Lucas A. Cernusak
  23. Department of Forest, Rangeland and Fire Sciences, College of Natural Resources, University of Idaho, Moscow, ID, USA
    Alan F. Talhelm
  24. Sino-French Institute for Earth System Science, College of Urban and Environmental Sciences, Peking University, Beijing, China
    Shilong Piao
  25. Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, China
    Shilong Piao
  26. Land & Environmental Management, AgResearch, Palmerston North, New Zealand
    Paul C. D. Newton
  27. School of Biological Sciences, University of Tasmania, Hobart, Tasmania, Australia
    Mark J. Hovenden
  28. Rangeland Resources & Systems Research Unit, Agricultural Research Service, United States Department of Agriculture, Fort Collins, CO, USA
    Dana M. Blumenthal
  29. School of Geographical Sciences, Nanjing University of Information Science and Technology, Nanjing, China
    Yi Y. Liu
  30. Department of Plant Ecology, Justus Liebig University of Giessen, Giessen, Germany
    Christoph Müller
  31. School of Biology and Environmental Science, University College Dublin, Belfield, Ireland
    Christoph Müller
  32. Smithsonian Tropical Research Institute, Balboa, Republic of Panama
    Klaus Winter
  33. Department of Psychiatry and Neuropsychology, Maastricht University, Maastricht, the Netherlands
    Wolfgang Viechtbauer
  34. Department of Methodology and Statistics, Utrecht University, Utrecht, the Netherlands
    Caspar J. Van Lissa
  35. Soil Chemistry, Wageningen University, Wageningen, the Netherlands
    Marcel R. Hoosbeek
  36. Institute of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan
    Makoto Watanabe
  37. Graduate School of Agriculture, Hokkaido University, Sapporo, Japan
    Takayoshi Koike
  38. USDA, Agricultural Research Service, Grassland, Soil and Water Research Laboratory, Temple, TX, USA
    H. Wayne Polley

Authors

  1. César Terrer
  2. Robert B. Jackson
  3. I. Colin Prentice
  4. Trevor F. Keenan
  5. Christina Kaiser
  6. Sara Vicca
  7. Joshua B. Fisher
  8. Peter B. Reich
  9. Benjamin D. Stocker
  10. Bruce A. Hungate
  11. Josep Peñuelas
  12. Ian McCallum
  13. Nadejda A. Soudzilovskaia
  14. Lucas A. Cernusak
  15. Alan F. Talhelm
  16. Kevin Van Sundert
  17. Shilong Piao
  18. Paul C. D. Newton
  19. Mark J. Hovenden
  20. Dana M. Blumenthal
  21. Yi Y. Liu
  22. Christoph Müller
  23. Klaus Winter
  24. Christopher B. Field
  25. Wolfgang Viechtbauer
  26. Caspar J. Van Lissa
  27. Marcel R. Hoosbeek
  28. Makoto Watanabe
  29. Takayoshi Koike
  30. Victor O. Leshyk
  31. H. Wayne Polley
  32. Oskar Franklin

Contributions

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 toCésar Terrer.

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The authors declare no competing interests.

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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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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). https://doi.org/10.1038/s41558-019-0545-2

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