Abstract
Direct quantification of terrestrial biosphere responses to global change is crucial for projections of future climate change in Earth system models. Here, we synthesized ecosystem carbon-cycling data from 1,119 experiments performed over the past four decades concerning changes in temperature, precipitation, CO2 and nitrogen across major terrestrial vegetation types of the world. Most experiments manipulated single rather than multiple global change drivers in temperate ecosystems of the USA, Europe and China. The magnitudes of warming and elevated CO2 treatments were consistent with the ranges of future projections, whereas those of precipitation changes and nitrogen inputs often exceeded the projected ranges. Increases in global change drivers consistently accelerated, but decreased precipitation slowed down carbon-cycle processes. Nonlinear (including synergistic and antagonistic) effects among global change drivers were rare. Belowground carbon allocation responded negatively to increased precipitation and nitrogen addition and positively to decreased precipitation and elevated CO2. The sensitivities of carbon variables to multiple global change drivers depended on the background climate and ecosystem condition, suggesting that Earth system models should be evaluated using site-specific conditions for best uses of this large dataset. Together, this synthesis underscores an urgent need to explore the interactions among multiple global change drivers in underrepresented regions such as semi-arid ecosystems, forests in the tropics and subtropics, and Arctic tundra when forecasting future terrestrial carbon-climate feedback.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The data supporting the results can be found in Song, J., Wan, S., Ru, J., Zhou, Z., Shao, P., Han, H., Lei, L., Wang, J., Li, X., Zhang, Q., Li, X., Su, F., Liu, B., Yang, F., Ma, G., Zhang, K., Hu, M., Yan, C., Zhang, A., Zhong, M., Hui, Y., Li, Y. & Zheng, M. Figshare https://doi.org/10.6084/m9.figshare.7442915.
References
Curtis, P. S. & Wang, X. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113, 299–313 (1998).
Rustad, L. E. et al. A meta-analysis of the responses of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562 (2001).
Xia, J. & Wan, S. Global response patterns of terrestrial plant species to nitrogen addition. New Phytol. 179, 428–439 (2008).
Lin, D., Xia, J. & Wan, S. Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. New Phytol. 188, 187–198 (2010).
Wu, Z., Dijkstra, P., Koch, G. W., Peñuelas, J. & Hungate, B. A. Responses of terrestrial ecosystem to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biol. 17, 927–942 (2011).
Beier, C. et al. Precipitation manipulation experiments—challenges and recommendations for the future. Ecol. Lett. 15, 899–911 (2012).
Knapp, A. K. et al. A reality check for climate change experiments: do they reflect the real world? Ecology 99, 2145–2151 (2018).
Kardol, P., De Long, J. R. & Sundqvist, M. K. Crossing the threshold: the power of multi-level experiments in identifying global change responses. New Phytol. 196, 323–326 (2012).
Dukes, J. S., Classen, A. T., Wan, S. & Langley, J. A. Using results from global change experiments to inform land model development and calibration. New Phytol. 204, 744–746 (2014).
De Kauwe, M. G. et al. Where does the carbon go? A model-data intercomparison of vegetation carbon allocation and turnover processes at two temperate forest free-air CO2 enrichment sites. New Phytol. 203, 883–899 (2014).
Medlyn, B. E. et al. Using ecosystem experiments to improve vegetation models. Nat. Clim. Change 5, 528–534 (2015).
Norby, R. J. et al. Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. New Phytol. 209, 17–28 (2016).
Wang, X. et al. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature 506, 212–215 (2014).
Ahlström, A. et al. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science 348, 895–899 (2015).
Schuur, E. A. G. et al. Climate change and the permafrost carbon feedback. Nature 520, 171–179 (2015).
IPCC Climate Change 2014: Synthesis Report (eds. Core Writing Team, Pachauri R. K. & Meyer L. A.) (IPCC, 2014).
Lamarque, J.-F. et al. Global and regional evolution of short-lived radiatively-active gases and aerosols in the Representative Concentration Pathways. Clim. Change 109, 191–212 (2011).
Melillo, J. M. et al. Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc. Natl Acad. Sci. USA 108, 9508–9512 (2011).
Hopkins, F. M., Torn, M. S. & Trumbore, S. E. Warming accelerates decomposition of decades-old carbon in forest soils. Proc. Natl Acad. Sci. USA 109, E1753–E1761 (2012).
Hoeppner, S. S. & Dukes, J. S. Interactive responses of old-field plant growth and composition to warming and precipitation. Global Change Biol. 18, 1754–1768 (2012).
Liu, W., Zhang, Z. & Wan, S. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biol. 15, 184–195 (2009).
Reich, P. B. et al. Effects of climate warming on photosynthesis in boreal tree species depend on soil moisture. Nature 562, 263–267 (2018).
Liu, L. et al. A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Global Change Biol. 22, 1394–1405 (2016).
Mahecha, M. D. et al. Global convergence in the temperature sensitivity of respiration at ecosystem level. Science 329, 838–840 (2010).
Dacal, M., Bradford, M. A., Plaza, C., Maestre, F. T. & García-Palacios, P. Soil microbial respiration adapts to ambient temperature in global drylands. Nat. Ecol. Evol. 3, 232–238 (2019).
Knapp, A. K. & Smith, M. D. Variation among biomes in temporal dynamics of aboveground primary production. Science 291, 481–484 (2001).
Knapp, A. K. et al. Consequences of more extreme precipitation regimes for terrestrial ecosystems. BioScience 58, 811–821 (2008).
Knapp, A. K., Ciais, P. & Smith, M. D. Reconciling inconsistencies in precipitation-productivity relationships: implications for climate change. New Phytol. 214, 41–47 (2017).
Huxman, T. E. et al. Convergence across biomes to a common rain-use efficiency. Nature 429, 651–654 (2004).
Smith, M. D. et al. Global environmental change and the nature of aboveground net primary productivity responses: insights from long-term experiments. Oecologia 177, 935–947 (2015).
Trugman, A. T. et al. Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol. Lett. 21, 1552–1560 (2018).
Litton, C. M., Raich, J. W. & Ryan, M. G. Carbon allocation in forest ecosystems. Global Change Biol. 13, 2089–2109 (2007).
Meier, I. C. & Leuschner, C. Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biol. 14, 2081–2095 (2008).
Vicca, S. et al. Urgent need for a common metric to make precipitation manipulation experiments comparable. New Phytol. 195, 518–522 (2012).
Reinsch, S. et al. Shrubland primary production and soil respiration diverge along European climate gradient. Sci. Rep. 7, 43952 (2017).
Leakey, A. D. B. et al. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60, 2859–2876 (2009).
Mooney, H. A., Drake, B. G., Luxmoore, R. J., Oechel, W. C. & Pitelka, L. F. Predicting ecosystem responses to elevated CO2 concentrations. BioScience 41, 96–104 (1991).
Fatichi, S. et al. Partitioning direct and indirect effects reveals the response of water-limited ecosystems to elevated CO2. Proc. Natl Acad. Sci. USA 113, 12757–12762 (2016).
Hovenden, M. J., Newton, P. C. D. & Wills, K. E. Seasonal not annual rainfall determines grassland biomass response to carbon dioxide. Nature 511, 583–586 (2014).
Hovenden, M. J. et al. Globally consistent influences of seasonal precipitation limit grassland biomass response to CO2. Nat. Plants 5, 167–173 (2019).
Obermeier, W. A. et al. Reduced CO2 fertilization effect in temperate C3 grasslands under more extreme weather conditions. Nat. Clim. Change 7, 137–141 (2017).
Norby, R. J., Wullschleger, S. D., Gunderson, C. A., Johnson, D. W. & Ceulemans, R. Tree responses to rising CO2: implications for the future forest. Plant Cell Environ. 22, 683–714 (1999).
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).
Piao, S. et al. Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends. Global Change Biol. 19, 2117–2132 (2013).
Nie, M., Lu, M., Bell, J., Raut, S. & Pendall, E. Altered root traits due to elevated CO2: a meta-analysis. Global Ecol. Biogeogr. 22, 1095–1105 (2013).
Suter, D. et al. Elevated CO2 increases carbon allocation to the roots of Lolium perenne under free-air CO2 enrichment but not in a controlled environment. New Phytol. 154, 65–75 (2002).
Arnone, J. A. et al. Dynamics of root systems in native grasslands: effects of elevated atmospheric CO2. New Phytol. 147, 73–85 (2000).
Iversen, C. M. Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol. 186, 346–357 (2010).
Hungate, B. A. et al. The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388, 576–579 (1997).
Van Groenigen, K. J., Qi, X., Osenberg, C. W., Luo, Y. & Hungate, B. A. Faster decomposition under increased atmospheric CO2 limits soil carbon storage. Science 344, 508–509 (2014).
Song, J. et al. Elevated CO2 does not stimulate carbon sink in a semi-arid grassland. Ecol. Lett. 22, 458–468 (2019).
Luo, Y. & Weng, E. Dynamic disequilibrium of the terrestrial carbon cycle under global change. Trends Ecol. Evol. 26, 96–104 (2011).
LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).
Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nat. Geosci. 3, 315–322 (2010).
Vicca, S. et al. Fertile forests produce biomass more efficiently. Ecol. Lett. 15, 520–526 (2012).
Verlinden, M. S. et al. Favorable effect of mycorrhizae on biomass production efficiency exceeds their carbon cost in a fertilization experiment. Ecology 99, 2525–2534 (2018).
Friedlingstein, P., Joel, G., Field, C. B. & Fung, I. Y. Toward an allocation scheme for global terrestrial carbon models. Global Change Biol. 5, 755–770 (1999).
Smithwick, E. A., Lucash, M. S., McCormack, M. L. & Sivandran, G. Improving the representation of roots in terrestrial models. Ecol. Modell. 291, 193–204 (2014).
Ye, C. et al. Reconciling multiple impacts of nitrogen enrichment on soil carbon: plant, microbial and geochemical controls. Ecol. Lett. 21, 1162–1173 (2018).
Leuzinger, S. et al. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol. Evol. 26, 236–241 (2011).
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. Global Change Biol. 18, 2681–2693 (2012).
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. Global Change Biol. 21, 4303–4319 (2015).
Zhou, L. et al. Interactive effects of global change factors on soil respiration and its components: a meta-analysis. Global Change Biol. 22, 3157–3169 (2016).
Yue, K. et al. Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common. Ecol. Lett. 20, 663–672 (2017).
Larsen, K. S. et al. Reduced N cycling in response to drought, warming, and elevated CO2 in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Global Change Biol. 17, 1884–1899 (2011).
Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. & Field, C. B. Nitrogen and climate change. Science 302, 1512–1513 (2003).
Shaw, M. R. et al. Grassland responses to global environmental changes suppressed by elevated CO2. Science 298, 1987–1990 (2002).
Lu, M. et al. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology 94, 726–738 (2013).
Wang, X. et al. Soil respiration under climate warming: differential response of heterotrophic and autotrophic respiration. Global Change Biol. 20, 3229–3237 (2014).
Wand, S. J., Midgley, G. F., Jones, M. H. & Curtis, P. S. Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biol. 5, 723–741 (1999).
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).
Luo, Y., Hui, D. & Zhang, D. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63 (2006).
Sillen, W. M. A. & Dieleman, W. I. J. Effects of elevated CO2 and N fertilization on plant and soil carbon pools of managed grasslands: a meta-analysis. Biogeosciences 9, 2247–2258 (2012).
Tian, D., Wang, H., Sun, J. & Niu, S. Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity. Environ. Res. Lett. 11, 024012 (2016).
De Boeck, H. J. et al. Global change experiments: challenges and opportunities. BioScience 65, 922–931 (2015).
Estiarte, M. et al. Few multi-year precipitation-reduction experiments find a shift in the productivity-precipitation relationship. Global Change Biol. 22, 2570–2581 (2016).
Kreyling, J., Jentsch, A. & Beier, C. Beyond realism in climate change experiments: Gradient approaches identify thresholds and tipping points. Ecol. Lett. 17, 125–e1 (2014).
Jentsch, A., Kreyling, J. & Beierkuhnlein, C. A new generation of climate-change experiments: events, not trends. Front. Ecol. Environ. 5, 365–374 (2007).
Thompson, R. M., Beardall, J., Beringer, J., Grace, M. & Sardina, P. Means and extremes: building variability into community-level climate change experiments. Ecol. Lett. 16, 799–806 (2013).
Kayler, Z. E. et al. Experiments to confront the environmental extremes of climate change. Front. Ecol. Environ. 13, 219–225 (2015).
Zhu, K., Chiariello, N. R., Tobeck, T., Fukami, T. & Field, C. B. Nonlinear, interacting responses to climate limit grassland production under global change. Proc. Natl Acad. Sci. USA 113, 10589–10594 (2016).
Langley, J. A. & Megonigal, J. P. Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466, 96–99 (2010).
Smith, M. D. The ecological role of climate extremes: current understanding and future prospects. J. Ecol. 99, 651–655 (2011).
Kreyling, J. et al. To replicate, or not to replicate—that is the question: how to tackle nonlinear responses in ecological experiments. Ecol. Lett. 21, 1629–1638 (2018).
De Martonne, E. Une nouvelle fonction climatologique: l’indice d’aridité. La Météorologie 2, 449–458 (1926).
Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).
Lajeunesse, M. J. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92, 2049–2055 (2011).
Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Software 36, 1–48 (2010).
R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2010).
Jennions, M. D., Lortie, C. J., Rosenberg, M. S. & Rothstein, H. R. in Handbook of Meta-Analysis in Ecology and Evolution (eds Koricheva, J., Gurevitch, J. & Mengersen, K.) 207–236 (Princeton Univ. Press, 2013).
Acknowledgements
We thank J. Wang (Hebei University), S. Yang (Institute of Botany, Chinese Academy of Sciences), L. Zhou (East China Normal University), C. Qiao (Xinyang Normal University) and H. Li (Henan University) for their help in meta-analyses and interaction analyses, and H. Li, Y. Liu (Institute of Tibetan Plateau Research, Chinese Academy of Sciences) and Y. He (Peking University) for their help in plotting figures. This work was financially supported by the National Natural Science Foundation of China (grant nos. 31430015 and 31830012). This study emerged from the INTERFACE Workshop in Beijing, China (https://www.bio.purdue.edu/INTERFACE/) supported by the US NSF DEB-0955771. We also acknowledge support from the ClimMani COST action (ES1308).
Author information
Authors and Affiliations
Contributions
S.W. designed the research. J.S., J.R., Z.Z., P.S., H.H., D.W., L. Lei, J.W., Xiaona L., Q.Z., Xiaoming L., F.S., B.L., F.Y., G.M., G.L., Yanchun L., Yinzhan L., Z.Y., K.Z., Y.M., M.H., C.Y., A.Z., M. Zhong, Y.H., Y. Li. and M. Zheng collected the 2,230 publications. J.S., J.R., Z.Z. and Q.L. performed the data extraction and analysis as well as figure plotting. J.S., S.W. and S.P. wrote the first draft of the manuscript, and A.K.K., A.T.C., S.V., P.C., M.J.H., S.L., C.B., P.K., J.X., Y. Luo, D.G., J.A.L., J.Z., J.S.D., J.T., J.C., K.S.H., L.M.K., L.R., L. Liu, M.D.S., P.H.T., R.Q.T., R.J.N., R.P.P., S.N., S.F. and Y.W. contributed substantially to revisions.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary information
Supplementary Figs. 1–20, Tables 1–4 and text.
Supplementary data
Cross-reference table of 1,119 experiments and 2,230 publications.
Rights and permissions
About this article
Cite this article
Song, J., Wan, S., Piao, S. et al. A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat Ecol Evol 3, 1309–1320 (2019). https://doi.org/10.1038/s41559-019-0958-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-019-0958-3
This article is cited by
-
Growing biomass carbon stock in China driven by expansion and conservation of woody areas
Nature Geoscience (2024)
-
Whole-soil warming leads to substantial soil carbon emission in an alpine grassland
Nature Communications (2024)
-
Contributions of ecological restoration policies to China’s land carbon balance
Nature Communications (2024)
-
Unexpected sustained soil carbon flux in response to simultaneous warming and nitrogen enrichment compared with single factors alone
Nature Ecology & Evolution (2024)
-
Mycorrhizal type regulates trade-offs between plant and soil carbon in forests
Nature Climate Change (2024)