Abstract

Carbon dioxide and nitrogen fertilization effects on ecosystem carbon sequestration may slow down in the future because of emerging nutrient constraints, climate change reducing the effect of fertilization, and expanding land use change and land management and disturbances. Further, record high temperatures and droughts are leading to negative impacts on carbon sinks. We suggest that, together, these two phenomena might drive a shift from a period dominated by the positive effects of fertilization to a period characterized by the saturation of the positive effects of fertilization on carbon sinks and the rise of negative impacts of climate change. We discuss the evidence and processes that are likely to be leading to this shift.

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References

  1. 1.

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

  2. 2.

    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).

  3. 3.

    Peñuelas, J. & Filella, I. Responses to a warming world. Science 294, 793–795 (2001).

  4. 4.

    IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) (Cambridge Univ. Press, Cambridge, 2014).

  5. 5.

    Fernandez-Martinez, M., Vicca, S., Janssens, I. A., Campioli, M. & Penuelas, J. Nutrient availability and climate as the main determinants of the ratio of biomass to NPP in woody and non-woody forest compartments. Trees Struct. Funct. 30, 775–783 (2016).

  6. 6.

    Le Quéré, C. et al. Global carbon budget 2016. Earth Syst. Sci. Data Discuss. 8, 605–649 (2016).

  7. 7.

    Fernández-Martínez, M. et al. Atmospheric deposition, CO2, and change in the land carbon sink. Sci. Rep. 7, 9632 (2017).

  8. 8.

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

  9. 9.

    Lewis, S. L. et al. Increasing carbon storage in intact African tropical forests. Nature 457, 1003–1006 (2009).

  10. 10.

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

  11. 11.

    Bellassen, V. et al. Reconstruction and attribution of the carbon sink of European forests between 1950 and 2000. Glob. Change Biol. 17, 3274–3292 (2011).

  12. 12.

    Zhang, F. et al. Attributing carbon changes in conterminous U. S. forests to disturbance and non-disturbance factors from 1901 to 2010. J. Geophys. Res. Biogeosci. 118, 1345–1346 (2013).

  13. 13.

    Niu, S., Sherry, R. A., Zhou, X. & Luo, Y. Ecosystem carbon fluxes in response to warming and clipping in a tallgrass prairie. Ecosystems 16, 948–961 (2013).

  14. 14.

    Zeng, W. & Wang, W. Combination of nitrogen and phosphorus fertilization enhance ecosystem carbon sequestration in a nitrogen-limited temperate plantation of northern China. For. Ecol. Manage. 341, 59–66 (2015).

  15. 15.

    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).

  16. 16.

    Raupach, M. R. et al. The declining uptake rate of atmospheric CO2 by land and ocean sinks. Biogeosciences 11, 3453–3475 (2014).

  17. 17.

    Peñuelas, J., Canadell, J. G. & Ogaya, R. Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Glob. Ecol. Biogeogr. 20, 597–608 (2011).

  18. 18.

    Van der Sleen, P. et al. No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat. Geosci. 8, 24–28 (2014).

  19. 19.

    Nabuurs, G.-J. et al. First signs of carbon sink saturation in European forest biomass. Nat. Clim. Change 3, 792–796 (2013).

  20. 20.

    Brienen, R. J. W. et al. Long-term decline of the Amazon carbon sink. Nature 519, 344–348 (2015).

  21. 21.

    Anderegg, W. R. L. et al. Tropical nighttime warming as a dominant driver of variability in the terrestrial carbon sink. Proc. Natl Acad. Sci. USA 112, 15591–15596 (2015).

  22. 22.

    Piao, S. et al. Weakening temperature control on the interannual variations of spring carbon uptake across northern lands. Nat. Clim. Change 7, 359–363 (2017).

  23. 23.

    Piao, S. et al. Evidence for a weakening relationship between interannual temperature variability and northern vegetation activity. Nat. Commun. 5, 5018 (2014).

  24. 24.

    Cordell, S., Mcclellan, M., Carter, Y. Y. & Hadway, L. J. Towards restoration of Hawaiian tropical dry forests: the Kaupulehu outplanting programme. Pacific Conserv. Biol. 14, 279–284 (2008).

  25. 25.

    Knorr, W., Arneth, A. & Jiang, L. Demographic controls of future global fire risk. Nat. Clim. Change 6, 2–8 (2016).

  26. 26.

    Crowther, T. et al. Quantifying global soil C losses in response to warming. Nature 104, 104–108 (2016).

  27. 27.

    Carey, J. C. et al. Temperature response of soil respiration largely unaltered with experimental warming. Proc. Natl Acad. Sci. USA 113, 13797–13802 (2016).

  28. 28.

    Davidson, E. A., Ishida, F. Y. & Nepstad, D. C. Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob. Change Biol. 10, 718–730 (2004).

  29. 29.

    Corlett, R. T. The impacts of droughts in tropical forests. Trends Plant Sci. 21, 584–593 (2016).

  30. 30.

    Saleska, S. R., Didan, K., Huete, A. R. & da Rocha, H. R. Amazon forests green-up during 2005 drought. Sci. Express 318, 612 (2007).

  31. 31.

    Schuur, E. A. G. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).

  32. 32.

    Gruber, N. et al. in The Global Carbon Cycle: Integrating Humans, Climate, and the Natural World (eds Field, C. B. & Raupach, M. R.) 45–76 (Island, Washington DC, 2004).

  33. 33.

    Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).

  34. 34.

    Reich, P. B. & Hobbie, S. E. Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nat. Clim. Change 3, 278–282 (2012).

  35. 35.

    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).

  36. 36.

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

  37. 37.

    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).

  38. 38.

    Vitousek, P. M., Porder, S., Houlton, B. Z. & Chadwick, O. A. Terrestrial phosphorus limitation : mechanisms, implications, and nitrogen–phosphorus interactions. Ecol. Appl. 20, 5–15 (2010).

  39. 39.

    Fu, Y. H. et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature 526, 104–107 (2015).

  40. 40.

    Korner, C. & Basler, D. Phenology under global warming. Science 327, 1461–1462 (2010).

  41. 41.

    Peng, S. et al. Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature 501, 88–92 (2013).

  42. 42.

    Meehl, G. A. & Tebaldi, C. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997 (2004).

  43. 43.

    Seneviratne, S. I. et al. in Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds Field, C. B. et al.) 109–230 (IPCC, Cambridge Univ. Press, Cambridge, 2012).

  44. 44.

    Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).

  45. 45.

    Wolf, S. et al. Warm spring reduced carbon cycle impact of the 2012 US summer drought. Proc. Natl Acad. Sci. USA 113, 5880–5885 (2016).

  46. 46.

    Dreesen, F. E., De Boeck, H. J., Janssens, I. A. & Nijs, I. Do successive climate extremes weaken the resistance of plant communities? An experimental study using plant assemblages. Biogeosciences 11, 109–121 (2014).

  47. 47.

    Granier, A. et al. Evidence for soil water control on carbon and water dynamics in European forests during the extremely dry year 2003. Agric. For. Meteorol. 143, 123–145 (2007).

  48. 48.

    Angert, A. et al. Drier summers cancel out the CO2 uptake enhancement induced by warmer springs. Proc. Natl Acad. Sci. USA 102, 10823–10827 (2005).

  49. 49.

    Orlowsky, B. & Seneviratne, S. I. Elusive drought: uncertainty in observed trends and short-and long-term CMIP5 projections. Hydrol. Earth Syst. Sci. 17, 1765–1781 (2013).

  50. 50.

    Allen, C. D., Breshears, D. D. & McDowell, N. G. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 1–55 (2015).

  51. 51.

    Doughty, C. E. et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015).

  52. 52.

    Zscheischler, J. et al. A few extreme events dominate global interannual variability in gross primary production. Environ. Res. Lett. 9, 35001 (2014).

  53. 53.

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

  54. 54.

    Van Groenigen, K. J. et al. Faster turnover of new soil carbon inputs under increased atmsopheric CO2. Glob. Change Biol. https://dx.doi.org/10.1111/gcb.13752 (2017)

  55. 55.

    Pechony, O. & Shindell, D. T. Driving forces of global wildfires over the past millennium and the forthcoming century. Proc. Natl Acad. Sci. USA 107, 19167–19170 (2010).

  56. 56.

    Ray, D. K. & Foley, J. Increasing global crop harvest frequency: recent trends and future directions. Environ. Res. Lett. 8, 44041 (2013).

  57. 57.

    Tian, H. et al. The terrestrial biosphere as a net source of greenhouse gases to the atmosphere. Nature 531, 225–228 (2016).

  58. 58.

    Luyssaert, S. et al. Land management and land-cover change have impacts of similar magnitude on surface temperature. Nat. Clim. Change 4, 389–393 (2014).

  59. 59.

    Peñuelas, J., Bartrons, M., Llusia, J. & Filella, I. Sensing the energetic status of plants and ecosystems. Trends Plant Sci. 20, 528–530 (2015).

  60. 60.

    Lawrence, D. M. et al. The Land Use Model Intercomparison Project (LUMIP) contribution to CMIP6: rationale and experimental design. Geosci. Model Dev. 9, 2973–2998 (2016).

  61. 61.

    Van Den Hurk, B. et al. LS3MIP (v1.0) contribution to CMIP6: the Land Surface, Snow and Soil moisture Model Intercomparison Project—aims, setup and expected outcome. Geosci. Model Dev. 9, 2809–2832 (2016).

  62. 62.

    Stegehuis, A. I. et al. Summer temperatures in Europe and land heat fluxes in observation-based data and regional climate model simulations. Clim. Dynam. 41, 455–477 (2013).

  63. 63.

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

  64. 64.

    Saatchi, S. S. et al. Benchmark map of forest carbon stocks in tropical regions across three continents. Proc. Natl Acad. Sci. USA 108, 9899–9904 (2011).

  65. 65.

    Jung, M., Reichstein, M., Schwalm, C. R., Huntingford, C. & Sitch, S. Compensatory water effects link yearly global land CO2 sink changes to temperature. Nature 541, 516–520 (2017).

  66. 66.

    Gill, A. L. & Finzi, A. C. Belowground carbon flux links biogeochemical cycles and resource-use efficiency at the global scale. Ecol. Lett. 19, 1419–1428 (2016).

  67. 67.

    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).

  68. 68.

    Drijfhout, S. et al. Catalogue of abrupt shifts in Intergovernmental Panel on Climate Change climate models. Proc. Natl Acad. Sci. USA 112, 777–786 (2015).

  69. 69.

    Haylock, M. R. et al. A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006. J. Geophys. Res. Atmos. 113, D20119 (2008).

  70. 70.

    Jacob, D. et al. EURO-CORDEX: new high-resolution climate change projections for European impact research. Reg. Environ. Change 14, 563–578 (2014).

  71. 71.

    Vautard, R. et al. The European climate under a 2 °C global warming. Environ. Res. Lett. 9, 34006 (2014).

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Acknowledgements

This Perspective was presented in the acceptance speech of the Ramon Margalef Prize in Ecology (November 2016) by J.P. The authors would like to acknowledge the financial support from the European Research Council Synergy grant ERC-SyG-2013-610028 IMBALANCE-P, the Spanish Government grant CGL2016-79835-P and the Catalan Government grant SGR 2014-274. The authors also acknowledge the improvement of the manuscript by C. Prentice.

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Affiliations

  1. CSIC, Global Ecology Unit CREAF-CEAB-UAB, Cerdanyola del Vallès, 08193, Catalonia, Spain

    • Josep Peñuelas
    • , Marcos Fernández-Martínez
    • , Jofre Carnicer
    •  & Jordi Sardans
  2. CREAF, Cerdanyola del Vallès, 08193, Catalonia, Spain

    • Josep Peñuelas
    • , Marcos Fernández-Martínez
    • , Jofre Carnicer
    •  & Jordi Sardans
  3. Laboratoire des Sciences du Climat et de l’Environnement, IPSL, 91191, Gif-sur-Yvette, France

    • Philippe Ciais
    •  & Robert Vautard
  4. Global Carbon Project, CSIRO Oceans and Atmosphere, Canberra, ACT 2601, Australia

    • Josep G. Canadell
  5. Research Group of Plant and Vegetation Ecology (PLECO), Department of Biology, University of Antwerp, B-2610, Wilrijk, Belgium

    • Ivan A. Janssens
  6. International Institute for Applied Systems Analysis (IIASA), Ecosystems Services and Management, Schlossplatz 1, A-2361, Laxenburg, Austria

    • Michael Obersteiner
  7. Department of Ecology, College of Urban and Environmental Sciences, Peking University 5 Yiheyuan Road, Haidian District, 100871, Beijing, China

    • Shilong Piao

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Contributions

J.P. designed the study. J.P., P.C., M.F.-M., R.V. and J.S. conducted the analyses with support from J.C., I.A.J., J.C., M.O. and S.P. The paper was drafted by J.P. and P.C. M.F.-M., R.V., J.S., J.C., I.A.J., J.C., M.O. and S.P. contributed to the interpretation of the results and to the text.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Josep Peñuelas.

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DOI

https://doi.org/10.1038/s41559-017-0274-8