Abstract
The recent ‘warming hiatus’ presents an excellent opportunity to investigate climate sensitivity of carbon cycle processes. Here we combine satellite and atmospheric observations to show that the rate of net biome productivity (NBP) has significantly accelerated from −0.007 ± 0.065 PgC yr−2 over the warming period (1982 to 1998) to 0.119 ± 0.071 PgC yr−2 over the warming hiatus (1998–2012). This acceleration in NBP is not due to increased primary productivity, but rather reduced respiration that is correlated (r = 0.58; P = 0.0007) and sensitive (γ = 4.05 to 9.40 PgC yr−1 per °C) to land temperatures. Global land models do not fully capture this apparent reduced respiration over the warming hiatus; however, an empirical model including soil temperature and moisture observations better captures the reduced respiration.
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References
Le Quéré, C. et al. Global carbon budget 2014. Earth Syst. Sci. Data 7, 47–85 (2015).
Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).
Bacastow, R. et al. Atmospheric carbon dioxide, the Southern Oscillation, and the weak 1975 El Niño. Science 210, 66–68 (1980).
Bousquet, P. et al. Regional changes in carbon dioxide fluxes of land and oceans since 1980. Science 290, 1342–1346 (2000).
Cox, P. M. et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494, 341–344 (2013).
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).
Doughty, C. E. & Goulden, M. L. Are tropical forests near a high temperature threshold? J. Geophys. Res. 113, G00B07 (2008).
Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).
Hoffman, F. M. et al. Causes and implications of persistent atmospheric carbon dioxide biases in Earth System Models. J. Geophys. Res. 119, 141–162 (2014).
Smith, W. K. et al. Large divergence of satellite and Earth system model estimates of global terrestrial CO2 fertilization. Nat. Clim. Change 6, 306–310 (2016).
Schulze, E.-D., Wirth, C. & Heimann, M. Managing forests after Kyoto. Science 289, 2058–2059 (2000).
Chapin, F. III et al. Reconciling carbon-cycle concepts, terminology, and methods. Ecosystems 9, 1041–1050 (2006).
Ballantyne, A. et al. Audit of the global carbon budget: estimate errors and their impact on uptake uncertainty. Biogeosciences 12, 2565–2584 (2015).
Fyfe, J. C., Gillett, N. P. & Zwiers, F. W. Overestimated global warming over the past 20 years. Nat. Clim. Change 3, 767–769 (2013).
Marotzke, J. & Forster, P. M. Forcing, feedback and internal variability in global temperature trends. Nature 517, 565–570 (2015).
Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).
Taylor, K. E., Stouffer, R. J. & Meehl, G. A. An overview of CMIP5 and the experiment design. Bull. Am. Meteorol. Soc. 93, 485–498 (2012).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).
Sulman, B. N. et al. Impact of hydrological variations on modeling of peatland CO2 fluxes: results from the North American Carbon Program site synthesis. J. Geophys. Res. 117, G01031 (2012).
Davidson, E. A., Samanta, S., Caramori, S. S. & Savage, K. The dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Glob. Change Biol. 18, 371–384 (2012).
Chen, S., Zou, J., Hu, Z., Chen, H. & Lu, Y. Global annual soil respiration in relation to climate, soil properties and vegetation characteristics: summary of available data. Agric. For. Meteorol. 198, 335–346 (2014).
Jung, M. et al. Recent decline in the global land evapotranspiration trend due to limited moisture supply. Nature 467, 951–954 (2010).
Reich, P. B. et al. Boreal and temperate trees show strong acclimation of respiration to warming. Nature 531, 633–636 (2016).
Piao, S. et al. Forest annual carbon cost: a global-scale analysis of autotrophic respiration. Ecology 91, 652–661 (2010).
Suseela, V., Conant, R. T., Wallenstein, M. D. & Dukes, J. S. Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob. Change Biol. 18, 336–348 (2012).
Anav, A. et al. Spatiotemporal patterns of terrestrial gross primary production: a review. Rev. Geophys. 53, 785–818 (2015).
Beer, C. et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329, 834–838 (2010).
Luyssaert, S. et al. CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob. Change Biol. 13, 2509–2537 (2007).
Högberg, P. et al. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792 (2001).
van der Werf, G. R. et al. Interannual variability in global biomass burning emissions from 1997 to 2004. Atmos. Chem. Phys. 6, 3423–3441 (2006).
Raymond, P. A. et al. Global carbon dioxide emissions from inland waters. Nature 503, 355–359 (2013).
Zhao, M. & Running, S. W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943 (2010).
Sarmiento, J. L. et al. Trends and regional distributions of land and ocean carbon sinks. Biogeosciences 7, 2351–2367 (2010).
Gu, L. et al. Response of a deciduous forest to the Mount Pinatubo eruption: enhanced photosynthesis. Science 299, 2035–2038 (2003).
Lucht, W. et al. Climatic control of the high-latitude vegetation greening trend and Pinatubo effect. Science 296, 1687–1689 (2002).
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).
England, M. H., Kajtar, J. B. & Maher, N. Robust warming projections despite the recent hiatus. Nat. Clim. Change 5, 394–396 (2015).
Smith, N. G., Malyshev, S. L., Shevliakova, E., Kattge, J. & Dukes, J. S. Foliar temperature acclimation reduces simulated carbon sensitivity to climate. Nat. Clim. Change 6, 407–411 (2016).
Lombardozzi, D. L., Bonan, G. B., Smith, N. G., Dukes, J. S. & Fisher, R. A. Temperature acclimation of photosynthesis and respiration: a key uncertainty in the carbon cycle-climate feedback. Geophys. Res. Lett. 42, 8624–8631 (2015).
Huntingford, C. et al. Simulated resilience of tropical rainforests to CO2-induced climate change. Nat. Geosci. 6, 268–273 (2013).
Harris, I., Jones, P., Osborn, T. & Lister, D. Updated high-resolution grids of monthly climatic observations–the CRU TS3. 10 Dataset. Intl J. Climatol. 34, 623–642 (2014).
Team G. GISS Surface Temperature Analysis (GISTEMP) (NASA Goddard Institute for Space Studies, accessed 13 May 2015); http://data.giss.nasa.gov/gistempp
Vose, R. S. et al. NOAA’s merged land–ocean surface temperature analysis. Bull. Am. Meteorol. Soc. 93, 1677–1685 (2012).
Running, S. W. et al. A continuous satellite-derived measure of global terrestrial primary production. Bioscience 54, 547–560 (2004).
Jones, P. et al. Hemispheric and large-scale land-surface air temperature variations: an extensive revision and an update to 2010. J. Geophys. Res. 117, D05127 (2012).
Zhu, Z. et al. Global data sets of vegetation leaf area index (LAI) 3g and Fraction of Photosynthetically Active Radiation (FPAR) 3g derived from Global Inventory Modeling and Mapping Studies (GIMMS) Normalized Difference Vegetation Index (NDVI3g) for the period 1981 to 2011. Remote Sensing 5, 927–948 (2013).
Zhao, M., Running, S., Heinsch, F. A. & Nemani, R. in Land Remote Sensing and Global Environmental Change (eds Ramachandran, B., Justice, C. O. & Abrams, M. J.) 635–660 (Springer, 2011).
Samanta, A. et al. Comment on ‘Drought-induced reduction in global terrestrial net primary production from 2000 through 2009’. Science 333, 1093 (2011).
Heinsch, F. A. et al. Evaluation of remote sensing based terrestrial productivity from MODIS using regional tower eddy flux network observations. IEEE Trans. Geosci. Remote Sensing 44, 1908–1925 (2006).
Cleveland, C. C. et al. A comparison of plot-based satellite and Earth system model estimates of tropical forest net primary production. Glob. Biogeochem. Cycles 29, 626–644 (2015).
Jung, M. et al. Global patterns of land-atmosphere fluxes of carbon dioxide, latent heat, and sensible heat derived from eddy covariance, satellite, and meteorological observations. J. Geophys. Res. 116 (2011).
Zhao, M., Running, S. W. & Nemani, R. R. Sensitivity of Moderate Resolution Imaging Spectroradiometer (MODIS) terrestrial primary production to the accuracy of meteorological reanalyses. J. Geophys. Res. 111, G01002 (2006).
Le Quéré, C. et al. The global carbon budget 1959–2011. Earth Syst. Sci. Data 5, 165–185 (2013).
van der Werf, G. R. et al. Global fire emissions and the contribution of deforestation, savanna, forest, agricultural, and peat fires (1997–2009). Atmos. Chem. Phys. 10, 11707–11735 (2010).
Masarie, K. A. & Tans, P. P. Extension and integration of atmospheric carbon dioxide data into a globally consistent measurement record. J. Geophys. Res. 100, 11593–11610 (1995).
Andres, R. J., Boden, T. A. & Higdon, D. A new evaluation of the uncertainty associated with CDIAC estimates of fossil fuel carbon dioxide emission. Tellus B 66, 23616 (2014).
Houghton, R. A. Land-use change and the carbon cycle. Glob. Change Biol. 1, 275–287 (1995).
Stocker, B., Strassmann, K. & Joos, F. Sensitivity of Holocene atmospheric CO2 and the modern carbon budget to early human land use: analyses with a process-based model. Biogeosciences 8, 69–88 (2011).
Jain, A. K., Meiyappan, P., Song, Y. & House, J. I. CO2 emissions from land-use change affected more by nitrogen cycle, than by the choice of land-cover data. Glob. Change Biol. 19, 2893–2906 (2013).
Friedlingstein, P. et al. Update on CO2 emissions. Nat. Geosci. 3, 811–812 (2010).
Erb, K.-H. et al. Bias in the attribution of forest carbon sinks. Nat. Clim. Change 3, 854–856 (2013).
Ballantyne, A., Alden, C., Miller, J., Tans, P. & White, J. Increase in observed net carbon dioxide uptake by land and oceans during the past 50 years. Nature 488, 70–72 (2012).
Morton, D. C. Forest carbon fluxes: a satellite perspective. Nat. Clim. Change 6, 346–348 (2016).
Francey, R. J. et al. Atmospheric verification of anthropogenic CO2 emission trends. Nat. Clim. Change 3, 520–524 (2013).
Ishidoya, S. et al. Time and space variations of the O2/N2 ratio in the troposphere over Japan and estimation of the global CO2 budget for the period 2000–2010. Tellus B 64, 18964 (2012).
Manning, A. C. & Keeling, R. F. Global oceanic and land biotic carbon sinks from the Scripps atmospheric oxygen flask sampling network. Tellus B 58, 95–116 (2006).
Sitch, S. et al. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob. Change Biol. 9, 161–185 (2003).
Smith, B., Prentice, I. C. & Sykes, M. T. Representation of vegetation dynamics in the modelling of terrestrial ecosystems: comparing two contrasting approaches within European climate space. Glob. Ecol. Biogeogr. 10, 621–637 (2001).
Cox, P. M., Huntingford, C. & Harding, R. J. A canopy conductance and photosynthesis model for use in a GCM land surface scheme. J. Hydrol. 212, 79–94 (1998).
Woodward, F. I. & Lomas, M. R. Vegetation dynamics—simulating responses to climatic change. Biol. Rev. 79, 643–670 (2004).
Zaehle, S. & Friend, A. D. Carbon and nitrogen cycle dynamics in the O-CN land surface model I: model description, site-scale evaluation, and sensitivity to parameter estimates. Glob. Biogeochem. Cycles 24, GB1005 (2010).
Krinner, G. et al. A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. Glob. Biogeochem. Cycles 19, GB1015 (2005).
Oleson, K. et al. Improvements to the Community Land Model and their impact on the hydrological cycle. J. Geophys. Res. 113, G01021 (2008).
Exbrayat, J. F., Pitman, A. J., Zhang, Q., Abramowitz, G. & Wang, Y. P. Examining soil carbon uncertainty in a global model: response of microbial decomposition to temperature, moisture and nutrient limitation. Biogeosciences 10, 7095–7108 (2013).
Hengl, T. et al. SoilGrids1km—global soil information based on automated mapping. PLoS ONE 9, e105992 (2014).
Sen, P. K. Estimates of the regression coefficient based on Kendall’s tau. J. Am. Stat. Assoc. 63, 1379–1389 (1968).
Jones, P., Parker, D., Osborn, T. & Briffa, K. Trends: A Compendium of Data on Global Change 1–5 (Oak Ridge National Laboratory, Carbon Dioxide Information Analysis Center, 2006).
Karl, T. R. et al. Possible artifacts of data biases in the recent global surface warming hiatus. Science 348, 1469–1472 (2015).
Trenberth, K. E. Has there been a hiatus? Science 349, 691–692 (2015).
Li, W. et al. Reducing uncertainties in decadal variability of the global carbon budget with multiple datasets. Proc. Natl Acad. Sci. 113, 13104–13108 (2016).
Acknowledgements
This work was stimulated by a workshop on abrupt changes in the global carbon cycle sponsored by Princeton University and the The Finnish Society of Sciences and Letters. Further support for this research was provided by NSF-DEB no. 1550932 and USDA no. MONZ-1302. W.R.L.A. was supported by a NOAA global change fellowship and W.K.S. was supported by a Luc Hoffman Fellowship. Satellite observations and MOD-17 algorithm development were supported by NASA grant NNX08AG87A to S.W.R. We are also grateful to the global citizens and NOAA scientists who have helped maintain the global atmospheric CO2 observation network. This work was greatly improved through input from colleagues D. Lombardozzi and B. Sullivan.
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This study was conceived of at a workshop hosted by J.S. and P.K. and the study was designed by A.B., W.A. and W.S. Atmospheric data were analysed by A.B. and P.T. The compilation and analysis of satellite data was conducted by W.S. and S.R. Simulation data from ESMs were accessed and analysed by A.A., P.F. and E.S. and simulation data from DGVMs was provided by B.P. All authors contributed during the writing of the paper.
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Ballantyne, A., Smith, W., Anderegg, W. et al. Accelerating net terrestrial carbon uptake during the warming hiatus due to reduced respiration. Nature Clim Change 7, 148–152 (2017). https://doi.org/10.1038/nclimate3204
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DOI: https://doi.org/10.1038/nclimate3204
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