Skip to main content
Log in

Dynamic carbon-nitrogen coupling under global change

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Carbon-nitrogen coupling is a fundamental principle in ecosystem ecology. However, how the coupling responds to global change has not yet been examined. Through a comprehensive and systematic literature review, we assessed how the dynamics of carbon processes change with increasing nitrogen input and how nitrogen processes change with increasing carbon input under global change. Our review shows that nitrogen input to the ecosystem mostly stimulates plant primary productivity but inconsistently decreases microbial activities or increases soil carbon sequestration, with nitrogen leaching and nitrogenous gas emission rapidly increasing. Nitrogen fixation increases and nitrogen leaching decreases to improve soil nitrogen availability and support plant growth and ecosystem carbon sequestration under elevated CO2 and temperature or along ecosystem succession. We conclude that soil nitrogen cycle processes continually adjust to change in response to either overload under nitrogen addition or deficiency under CO2 enrichment and ecosystem succession to couple with carbon cycling. Indeed, processes of both carbon and nitrogen cycles continually adjust under global change, leading to dynamic coupling in carbon and nitrogen cycles. The dynamic coupling framework reconciles previous debates on the “uncoupling” or “decoupling” of ecosystem carbon and nitrogen cycles under global change. Ecosystem models failing to simulate these dynamic adjustments cannot simulate carbon-nitrogen coupling nor predict ecosystem carbon sequestration well.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aber, J., McDowell, W., Nadelhoffer, K., Magill, A., Berntson, G., Kamakea, M., McNulty, S., Currie, W., Rustad, L., and Fernandez, I. (1998). Nitrogen saturation in temperate forest ecosystems. Bioscience 48, 921–934.

    Article  Google Scholar 

  • Alexander, H.D., and Mack, M.C. (2016). A canopy shift in interior Alaskan boreal forests: consequences for above- and belowground carbon and nitrogen pools during post-fire succession. Ecosystems 19, 98–114.

    Article  CAS  Google Scholar 

  • Asner, G.P., Seastedt, T.R., and Townsend, A.R. (1997). The decoupling of terrestrial carbon and nitrogen cycles. Bioscience 47, 226–234.

    Article  Google Scholar 

  • Bai, E., Li, S., Xu, W., Li, W., Dai, W., and Jiang, P. (2013). A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytol 199, 441–451.

    Article  PubMed  Google Scholar 

  • Bedison, J.E., and McNeil, B.E. (2009). Is the growth of temperate forest trees enhanced along an ambient nitrogen deposition gradient? Ecology 90, 1736–1742.

    Article  PubMed  Google Scholar 

  • Beier, C., Emmett, B., Penuelas, J., Schmidt, I., Tietema, A., Estiarte, M., Gundersen, P., Llorens, L., Riisnielsen, T., and Sowerby, A. (2008). Carbon and nitrogen cycles in European ecosystems respond differently to global warming. Sci Total Environ 407, 692–697.

    Article  CAS  PubMed  Google Scholar 

  • Braakhekke, M.C., Rebel, K.T., Dekker, S.C., Smith, B., Beusen, A.H.W., and Wassen, M.J. (2017). Nitrogen leaching from natural ecosystems under global change: a modelling study. Earth Syst Dynam 8, 1121–1139.

    Article  Google Scholar 

  • Bubier, J.L., Moore, T.R., and Bledzki, L.A. (2007). Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog. Glob Change Biol 13, 1168–1186.

    Article  Google Scholar 

  • Butterly, C.R., Phillips, L.A., Wiltshire, J.L., Franks, A.E., Armstrong, R. D., Chen, D., Mele, P.M., and Tang, C. (2016). Long-term effects of elevated CO2 on carbon and nitrogen functional capacity of microbial communities in three contrasting soils. Soil Biol Biochem 97, 157–167.

    Article  CAS  Google Scholar 

  • Carter, M.S., Larsen, K.S., Emmett, B., Estiarte, M., Field, C., Leith, I.D., Lund, M., Meijide, A., Mills, R.T.E., Niinemets, Ü., et al. (2012). Synthesizing greenhouse gas fluxes across nine European peatlands and shrublands —responses to climatic and environmental changes. Biogeosciences 9, 3739–3755.

    Article  CAS  Google Scholar 

  • Chapin, D.M., and Bledsoe, C.S. (1992). Nitrogen fixation in arctic plant communities. In: Chapin III, F.S., Jefferies, R.L., Reynold, J.F., Shaver, J.R., and Svoboda, J., eds. Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective. New York: Academic Press.

    Google Scholar 

  • Chapin, F.S., Matson, P.A., and Vitousek, P.M. (2011). Principles of Terrestrial Ecosystem Ecology. New York: Springer.

    Book  Google Scholar 

  • Chen, R., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., Lin, X., Blagodatskaya, E., and Kuzyakov, Y. (2014). Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Change Biol 20, 2356–2367.

    Article  Google Scholar 

  • Cheng, S., Wang, L., Fang, H., Yu, G., Yang, X., Li, X., Si, G., Geng, J., He, S., and Yu, G. (2016). Nonlinear responses of soil nitrous oxide emission to multi-level nitrogen enrichment in a temperate needle-broadleaved mixed forest in Northeast China. Catena 147, 556–563.

    Article  CAS  Google Scholar 

  • Cheng, Y., Wang, J., Wang, J., Wang, S., Chang, S.X., Cai, Z., Zhang, J., Niu, S., and Hu, S. (2020). Nitrogen deposition differentially affects soil gross nitrogen transformations in organic and mineral horizons. Earth Sci Rev 201, 103033.

    Article  CAS  Google Scholar 

  • Cleveland, C.C., Houlton, B.Z., Smith, W.K., Marklein, A.R., Reed, S.C., Parton, W., Del Grosso, S.J., and Running, S.W. (2013). Patterns of new versus recycled primary production in the terrestrial biosphere. Proc Natl Acad Sci USA 110, 12733–12737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleveland, C.C., Townsend, A.R., Schimel, D.S., Fisher, H., Howarth, R. W., Hedin, L.O., Perakis, S.S., Latty, E.F., von Fischer, J.C., Elseroad, A., et al. (1999). Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob Biogeochem Cycle 13, 623–645.

    Article  CAS  Google Scholar 

  • Cleveland, C.C., Townsend, A.R., Taylor, P., Alvarez-Clare, S., Bustamante, M.M.C., Chuyong, G., Dobrowski, S.Z., Grierson, P., Harms, K.E., Houlton, B.Z., et al. (2011). Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pantropical analysis. Ecol Lett 14, 939–947.

    Article  PubMed  Google Scholar 

  • Craine, J.M., Morrow, C., and Fierer, N. (2007). Microbial nitrogen limitation increases decomposition. Ecology 88, 2105–2113.

    Article  PubMed  Google Scholar 

  • Crews, T.E., Blesh, J., Culman, S.W., Hayes, R.C., Jensen, E.S., Mack, M. C., Peoples, M.B., and Schipanski, M.E. (2016). Going where no grains have gone before: From early to mid-succession. Agr Ecosyst Environ 223, 223–238.

    Article  Google Scholar 

  • Crowther, T.W., Riggs, C., Lind, E.M., Borer, E.T., Seabloom, E.W., Hobbie, S.E., Wubs, J., Adler, P.B., Firn, J., Gherardi, L., et al. (2019). Sensitivity of global soil carbon stocks to combined nutrient enrichment. Ecol Lett 22, 936–945.

    Article  CAS  PubMed  Google Scholar 

  • Dai, Z., Yu, M., Chen, H., Zhao, H., Huang, Y., Su, W., Xia, F., Chang, S. X., Brookes, P.C., Dahlgren, R.A., et al. (2020). Elevated temperature shifts soil N cycling from microbial immobilization to enhanced mineralization, nitrification and denitrification across global terrestrial ecosystems. Glob Change Biol 26, 5267–5276.

    Article  Google Scholar 

  • Davies-Barnard, T., Meyerholt, J., Zaehle, S., Friedlingstein, P., Brovkin, V., Fan, Y., Fisher, R.A., Jones, C.D., Lee, H., Peano, D., et al. (2020). Nitrogen cycling in CMIP6 land surface models: progress and limitations. Biogeosciences 17, 5129–5148.

    Article  CAS  Google Scholar 

  • de Graaff, M.A., van Groenigen, K.J., Six, J., Hungate, B., and van Kessel, C. (2006). Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12, 2077–2091.

    Article  Google Scholar 

  • de Vries, W., Solberg, S., Dobbertin, M., Sterba, H., Laubhahn, D., Reinds, G.J., Nabuurs, G.J., Gundersen, P., and Sutton, M.A. (2008). Ecologically implausible carbon response? Nature 451, E1–E3.

    Article  CAS  PubMed  Google Scholar 

  • Dentener, F., Drevet, J., Lamarque, J.F., Bey, I., Eickhout, B., Fiore, A.M., Hauglustaine, D., Horowitz, L.W., Krol, M., Kulshrestha, U.C., et al. (2006). Nitrogen and sulfur deposition on regional and global scales: A multimodel evaluation. Glob Biogeochem Cycle 20, GB4003.

    Article  Google Scholar 

  • Dise, N.B., and Wright, R.F. (1995). Nitrogen leaching from European forests in relation to nitrogen deposition. For Ecol Manage 71, 153–161.

    Article  Google Scholar 

  • Dynarski, K.A., and Houlton, B.Z. (2018). Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytol 217, 1050–1061.

    Article  CAS  PubMed  Google Scholar 

  • Elbert, W., Weber, B., Burrows, S., Steinkamp, J., Büdel, B., Andreae, M. O., and Pöschl, U. (2012). Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5, 459–462.

    Article  CAS  Google Scholar 

  • Elser, J.J., Bracken, M.E.S., Cleland, E.E., Gruner, D.S., Harpole, W.S., Hillebrand, H., Ngai, J.T., Seabloom, E.W., Shurin, J.B., and Smith, J.E. (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10, 1135–1142.

    Article  PubMed  Google Scholar 

  • Esser, G., Kattge, J., and Sakalli, A. (2011). Feedback of carbon and nitrogen cycles enhances carbon sequestration in the terrestrial biosphere. Glob Change Biol 17, 819–842.

    Article  Google Scholar 

  • Fang, J., Kato, T., Guo, Z., Yang, Y., Hu, H., Shen, H., Zhao, X., Kishimoto-Mo, A.W., Tang, Y., and Houghton, R.A. (2014). Evidence for environmentally enhanced forest growth. Proc Natl Acad Sci USA 111, 9527–9532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang, Y., Gundersen, P., Vogt, R.D., Koba, K., Chen, F., Chen, X.Y., and Yoh, M. (2011). Atmospheric deposition and leaching of nitrogen in Chinese forest ecosystems. J For Res 16, 341–350.

    Article  CAS  Google Scholar 

  • Fay, P.A., Prober, S.M., Harpole, W.S., Knops, J.M.H., Bakker, J.D., Borer, E.T., Lind, E.M., MacDougall, A.S., Seabloom, E.W., Wragg, P.D., et al. (2015). Grassland productivity limited by multiple nutrients. Nat Plants 1, 15080.

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Martínez, M., Vicca, S., Janssens, I.A., Luyssaert, S., Campioli, M., Sardans, J., Estiarte, M., and Peñuelas, J. (2014). Spatial variability and controls over biomass stocks, carbon fluxes, and resource-use efficiencies across forest ecosystems. Trees 28, 597–611.

    Article  Google Scholar 

  • Finzi, A.C., Moore, D.J.P., DeLucia, E.H., Lichter, J., Hofmockel, K.S., Jackson, R.B., Kim, H.S., Matamala, R., McCarthy, H.R., Oren, R., et al. (2006). Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87, 15–25.

    Article  PubMed  Google Scholar 

  • Fleischer, K., Rebel, K.T., van der Molen, M.K., Erisman, J.W., Wassen, M. J., van Loon, E.E., Montagnani, L., Gough, C.M., Herbst, M., Janssens, I.A., et al. (2013). The contribution of nitrogen deposition to the photosynthetic capacity of forests. Glob Biogeochem Cycle 27, 187–199.

    Article  CAS  Google Scholar 

  • Goll, D.S., Brovkin, V., Parida, B.R., Reick, C.H., Kattge, J., Reich, P.B., van Bodegom, P.M., and Niinemets, Ü. (2012). Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9, 3547–3569.

    Article  CAS  Google Scholar 

  • Gundale, M.J., Nilsson, M., Bansal, S., and Jäderlund, A. (2012). The interactive effects of temperature and light on biological nitrogen fixation in boreal forests. New Phytol 194, 453–463.

    Article  CAS  PubMed  Google Scholar 

  • Hall, S.J., and Matson, P.A. (1999). Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature 400, 152–155.

    Article  CAS  Google Scholar 

  • Harpole, W.S., Ngai, J.T., Cleland, E.E., Seabloom, E.W., Borer, E.T., Bracken, M.E.S., Elser, J.J., Gruner, D.S., Hillebrand, H., Shurin, J.B., et al. (2011). Nutrient co-limitation of primary producer communities. Ecol Lett 14, 852–862.

    Article  PubMed  Google Scholar 

  • Hartman, W.H., and Richardson, C.J. (2013). Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS ONE 8, e57127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedin, L.O., Brookshire, E.N.J., Menge, D.N.L., and Barron, A.R. (2009). The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst 40, 613–635.

    Article  Google Scholar 

  • Houlton, B.Z., Morford, S.L., and Dahlgren, R.A. (2018). Convergent evidence for widespread rock nitrogen sources in Earth’s surface environment. Science 360, 58–62.

    Article  CAS  PubMed  Google Scholar 

  • Houlton, B.Z., Wang, Y.P., Vitousek, P.M., and Field, C.B. (2008). A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330.

    Article  CAS  PubMed  Google Scholar 

  • Hu, S., Chapin III, F.S., Firestone, M.K., Field, C.B., and Chiariello, N.R. (2001). Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409, 188–191.

    Article  CAS  PubMed  Google Scholar 

  • Hungate, B.A., Dukes, J.S., Shaw, M.R., Luo, Y., and Field, C.B. (2003). Nitrogen and climate change. Science 302, 1512–1513.

    Article  CAS  PubMed  Google Scholar 

  • Hungate, B.A., Stiling, P.D., Dijkstra, P., Johnson, D.W., Ketterer, M.E., Hymus, G.J., Hinkle, C.R., and Drake, B.G. (2004). CO2 elicits long-term decline in nitrogen fixation. Science 304, 1291.

    Article  CAS  PubMed  Google Scholar 

  • Ibáñez, I., Zak, D.R., Burton, A.J., and Pregitzer, K.S. (2018). Anthropogenic nitrogen deposition ameliorates the decline in tree growth caused by a drier climate. Ecology 99, 411–420.

    Article  PubMed  Google Scholar 

  • Janssens, I.A., Dieleman, W., Luyssaert, S., Subke, J.A., Reichstein, M., Ceulemans, R., Ciais, P., Dolman, A.J., Grace, J., Matteucci, G., et al. (2010). Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3, 315–322.

    Article  CAS  Google Scholar 

  • Kicklighter, D.W., Melillo, J.M., Monier, E., Sokolov, A.P., and Zhuang, Q. (2019). Future nitrogen availability and its effect on carbon sequestration in Northern Eurasia. Nat Commun 10, 3024.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiese, R., Heinzeller, C., Werner, C., Wochele, S., Grote, R., and Butterbach-Bahl, K. (2011). Quantification of nitrate leaching from German forest ecosystems by use of a process oriented biogeochemical model. Environ Pollut 159, 3204–3214.

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum, M.U.F., Guo, L.B., and Gifford, R.M. (2008). Observed and modelled soil carbon and nitrogen changes after planting a Pinus radiata stand onto former pasture. Soil Biol Biochem 40, 247–257.

    Article  CAS  Google Scholar 

  • Knops, J.M.H., and Tilman, D. (2000). Dynamics of soil nitrogen and carbon accumulation for 61 years after agricultural abandonment. Ecology 81, 88–98.

    Article  Google Scholar 

  • Knorr, M., Frey, S.D., and Curtis, P.S. (2005). Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86, 3252–3257.

    Article  Google Scholar 

  • Kortelainen, P., Saukkonen, S., and Mattsson, T. (1997). Leaching of nitrogen from forested catchments in Finland. Glob Biogeochem Cycle 11, 627–638.

    Article  CAS  Google Scholar 

  • LeBauer, D.S., and Treseder, K.K. (2008). Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379.

    Article  PubMed  Google Scholar 

  • Lewis, W.M., Melack, J.M., McDowell, W.H., McClain, M., and Richey, J. E. (1999). Nitrogen yields from undisturbed watersheds in the Americas. Biogeochemistry 46, 149–162.

    Article  CAS  Google Scholar 

  • Li, D., Niu, S., and Luo, Y. (2012). Global patterns of the dynamics of soil carbon and nitrogen stocks following afforestation: a meta-analysis. New Phytol 195, 172–181.

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Zheng, Z., Wang, W., Biederman, J.A., Xu, X., Ran, Q., Qian, R., Xu, C., Zhang, B., Wang, F., et al. (2020a). Terrestrial N2O emissions and related functional genes under climate change: a global metaanalysis. Glob Change Biol 26, 931–943.

    Article  Google Scholar 

  • Li, Z., Tang, Z., Song, Z., Chen, W., Tian, D., Tang, S., Wang, X., Wang, J., Liu, W., Wang, Y., et al. (2022). Variations and controlling factors of soil denitrification rate. Glob Change Biol 28, 2133–2145.

    Article  Google Scholar 

  • Li, Z., Tian, D., Wang, B., Wang, J., Wang, S., Chen, H.Y.H., Xu, X., Wang, C., He, N., and Niu, S. (2019). Microbes drive global soil nitrogen mineralization and availability. Glob Change Biol 25, 1078–1088.

    Article  Google Scholar 

  • Li, Z., Zeng, Z., Tian, D., Wang, J., Fu, Z., Zhang, F., Zhang, R., Chen, W., Luo, Y., and Niu, S. (2020b). Global patterns and controlling factors of soil nitrification rate. Glob Change Biol 26, 4147–4157.

    Article  Google Scholar 

  • Liang, J., Qi, X., Souza, L., and Luo, Y. (2016). Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a metaanalysis. Biogeosciences 13, 2689–2699.

    Article  CAS  Google Scholar 

  • Liu, S., Ji, C., Wang, C., Chen, J., Jin, Y., Zou, Z., Li, S., Niu, S., and Zou, J. (2018). Climatic role of terrestrial ecosystem under elevated CO2: a bottom-up greenhouse gases budget. Ecol Lett 21, 1108–1118.

    Article  PubMed  Google Scholar 

  • Lourenço, K.S., Dimitrov, M.R., Pijl, A., Soares, J.R., do Carmo, J.B., van Veen, J.A., Cantarella, H., and Kuramae, E.E. (2018). Dominance of bacterial ammonium oxidizers and fungal denitrifiers in the complex nitrogen cycle pathways related to nitrous oxide emission. GCB Bioenergy 10, 645–660.

    Article  Google Scholar 

  • Lu, M., Zhou, X., Luo, Y., Yang, Y., Fang, C., Chen, J., and Li, B. (2011). Minor stimulation of soil carbon storage by nitrogen addition: a metaanalysis. Agr Ecosyst Environ 140, 234–244.

    Article  CAS  Google Scholar 

  • Luo, Y., Field, C.B., and Mooney, H.A. (1994). Predicting responses of photosynthesis and root fraction to elevated [CO2]a: interactions among carbon, nitrogen, and growth. Plant Cell Environ 17, 1195–1204.

    Article  Google Scholar 

  • Luo, Y., Su, B.O., Currie, W.S., Dukes, J.S., Finzi, A., Hartwig, U., Hungate, B., McMURTRIE, R.E., Oren, R., Parton, W.J., et al. (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54, 731.

    Article  Google Scholar 

  • Mack, M.C., Schuur, E.A.G., Bret-Harte, M.S., Shaver, G.R., and Chapin III, F.S. (2004). Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431, 440–443.

    Article  CAS  PubMed  Google Scholar 

  • Magnani, F., Mencuccini, M., Borghetti, M., Berbigier, P., Berninger, F., Delzon, S., Grelle, A., Hari, P., Jarvis, P.G., Kolari, P., et al. (2007). The human footprint in the carbon cycle of temperate and boreal forests. Nature 447, 849–851.

    Article  CAS  Google Scholar 

  • Mason, R.E., Craine, J.M., Lany, N.K., Jonard, M., Ollinger, S.V., Groffman, P.M., Fulweiler, R.W., Angerer, J., Read, Q.D., Reich, P. B., et al. (2022). Evidence, causes, and consequences of declining nitrogen availability in terrestrial ecosystems. Science 376, eabh3767.

    Article  CAS  PubMed  Google Scholar 

  • Menge, D.N.L., and Crews, T.E. (2016). Can evolutionary constraints explain the rarity of nitrogen-fixing trees in high-latitude forests? New Phytol 211, 1195–1201.

    Article  PubMed  Google Scholar 

  • Metcalfe, D.B., Eisele, B., and Hasselquist, N.J. (2013). Effects of nitrogen fertilization on the forest floor carbon balance over the growing season in a boreal pine forest. Biogeosciences 10, 8223–8231.

    Article  Google Scholar 

  • Meyer, N., Welp, G., Bornemann, L., and Amelung, W. (2017). Microbial nitrogen mining affects spatio-temporal patterns of substrate-induced respiration during seven years of bare fallow. Soil Biol Biochem 104, 175–184.

    Article  CAS  Google Scholar 

  • Moorhead, D.L., and Sinsabaugh, R.L. (2006). A theoretical model of litter decay and microbial interaction. Ecol Monogr 76, 151–174.

    Article  Google Scholar 

  • Morford, S.L., Houlton, B.Z., and Dahlgren, R.A. (2011). Increased forest ecosystem carbon and nitrogen storage from nitrogen rich bedrock. Nature 477, 78–81.

    Article  CAS  PubMed  Google Scholar 

  • Morford, S.L., Houlton, B.Z., and Dahlgren, R.A. (2016). Direct quantification of long-term rock nitrogen inputs to temperate forest ecosystems. Ecology 97, 54–64.

    Article  PubMed  Google Scholar 

  • Morris, S.J., Bohm, S., Haile-Mariam, S., and Paul, E.A. (2007). Evaluation of carbon accrual in afforested agricultural soils. Glob Change Biol 13, 1145–1156.

    Article  Google Scholar 

  • Niu, S., Classen, A.T., Dukes, J.S., Kardol, P., Liu, L., Luo, Y., Rustad, L., Sun, J., Tang, J., Templer, P.H., et al. (2016). Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19, 697–709.

    Article  PubMed  Google Scholar 

  • Niu, S., Wu, M., Han, Y.I., Xia, J., Zhang, Z., Yang, H., and Wan, S. (2010). Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Glob Change Biol 16, 144–155.

    Article  Google Scholar 

  • Norby, R.J., Warren, J.M., Iversen, C.M., Medlyn, B.E., and McMurtrie, R. E. (2010). CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107, 19368–19373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Sullivan, O.S., Horswill, P., Phoenix, G.K., Lee, J.A., and Leake, J.R. (2011). Recovery of soil nitrogen pools in species-rich grasslands after 12 years of simulated pollutant nitrogen deposition: a 6-year experimental analysis. Glob Change Biol 17, 2615–2628.

    Article  Google Scholar 

  • Patil, R.H., Laegdsmand, M., Olesen, J.E., and Porter, J.R. (2010). Effect of soil warming and rainfall patterns on soil N cycling in Northern Europe. Agr Ecosyst Environ 139, 195–205.

    Article  CAS  Google Scholar 

  • Peñuelas, J., Janssens, I.A., Ciais, P., Obersteiner, M., and Sardans, J. (2020). Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health. Glob Chang Biol 26, 1962–1985.

    Article  Google Scholar 

  • Peñuelas, J., Sardans, J., Rivas-ubach, A., and Janssens, I.A. (2012). The human-induced imbalance between C, N and P in Earth’s life system. Glob Change Biol 18, 3–6.

    Article  Google Scholar 

  • Piao, S., Sitch, S., Ciais, P., Friedlingstein, P., Peylin, P., Wang, X., Ahlström, A., Anav, A., Canadell, J.G., Cong, N., et al. (2013). Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends. Glob Change Biol 19, 2117–2132.

    Article  Google Scholar 

  • Reed, S.C., Cleveland, C.C., and Townsend, A.R. (2011). Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42, 489–512.

    Article  Google Scholar 

  • Rousk, K., and Michelsen, A. (2017). Ecosystem nitrogen fixation throughout the snow-free period in subarctic tundra: effects of willow and birch litter addition and warming. Glob Change Biol 23, 1552–1563.

    Article  Google Scholar 

  • Ruiz-Vera, U.M., De Souza, A.P., Long, S.P., and Ort, D.R. (2017). The role of sink strength and nitrogen availability in the down-regulation of photosynthetic capacity in field-grown Nicotiana tabacum L. at elevated CO2 concentration. Front Plant Sci 8, 998.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rustad, L., Campbell, J., Marion, G., Norby, R., Mitchell, M., Hartley, A., Cornelissen, J., and Gurevitch, J. (2001). A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126, 543–562.

    Article  CAS  PubMed  Google Scholar 

  • Sardans, J., Alonso, R., Janssens, I.A., Carnicer, J., Vereseglou, S., Rillig, M.C., Fernández-Martínez, M., Sanders, T.G.M., and Peñuelas, J. (2016). Foliar and soil concentrations and stoichiometry of nitrogen and phosphorous across European Pinus sylvestrisforests: relationships with climate, N deposition and tree growth. Funct Ecol 30, 676–689.

    Article  Google Scholar 

  • Schimel, J., and Weintraub, M.N. (2003). The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35, 549–563.

    Article  CAS  Google Scholar 

  • Shcherbak, I., Millar, N., and Robertson, G.P. (2014). Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci USA 111, 9199–9204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, J., Dai, W., Peng, B., Liu, J., He, T., Jiang, P., Han, S., and Bai, E. (2018). Does the accelerated soil N cycling sustain N demand of Quercus mongolica after decade-long elevated CO2 treatment? Biogeochemistry 139, 197–213.

    Article  Google Scholar 

  • Sun, Y., Wang, C., Chen, H.Y.H., Liu, Q., Ge, B., and Tang, B. (2022). A global meta-analysis on the responses of C and N concentrations to warming in terrestrial ecosystems. Catena 208, 105762.

    Article  CAS  Google Scholar 

  • Sutton, M.A., Simpson, D., Levy, P.E., Smith, R.I., Reis, S., van Oijen, M., and de Vries, W. (2008). Uncertainties in the relationship between atmospheric nitrogen deposition and forest carbon sequestration. Glob Change Biol 14, 2057–2063.

    Article  Google Scholar 

  • Thomas, R.Q., Zaehle, S., Templer, P.H., and Goodale, C.L. (2013). Global patterns of nitrogen limitation: confronting two global biogeochemical models with observations. Glob Change Biol 19, 2986–2998.

    Article  Google Scholar 

  • Thornton, P.E., Lamarque, J.F., Rosenbloom, N.A., and Mahowald, N.M. (2007). Influence of carbon-nitrogen cycle coupling on land model response to CO2 fertilization and climate variability. Glob Biogeochem Cycle 21, GB4018.

    Article  Google Scholar 

  • Tian, D., and Niu, S. (2015). A global analysis of soil acidification caused by nitrogen addition. Environ Res Lett 10, 024019.

    Article  Google Scholar 

  • Tian, D., Wang, H., Sun, J., and Niu, S. (2016a). Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity. Environ Res Lett 11, 024012.

    Article  Google Scholar 

  • Tian, D., Niu, S., Pan, Q., Ren, T., Chen, S., Bai, Y., Han, X., and Whitehead, D. (2016b). Nonlinear responses of ecosystem carbon fluxes and water-use efficiency to nitrogen addition in Inner Mongolia grassland. Funct Ecol 30, 490–499.

    Article  Google Scholar 

  • Tian, D., Reich, P.B., Chen, H.Y.H., Xiang, Y., Luo, Y., Shen, Y., Meng, C., Han, W., and Niu, S. (2019). Global changes alter plant multi-element stoichiometric coupling. New Phytol 221, 807–817.

    Article  CAS  PubMed  Google Scholar 

  • Tian, D., Xiang, Y., Wang, B., Li, M., Liu, Y., Wang, J., Li, Z., and Niu, S. (2018). Cropland abandonment enhances soil inorganic nitrogen retention and carbon stock in China: a meta-analysis. Land Degrad Dev 29, 3898–3906.

    Article  Google Scholar 

  • Todd-Brown, K.E.O., Randerson, J.T., Post, W.M., Hoffman, F.M., Tarnocai, C., Schuur, E.A.G., and Allison, S.D. (2013). Causes of variation in soil carbon simulations from CMIP5 Earth system models and comparison with observations. Biogeosciences 10, 1717–1736.

    Article  Google Scholar 

  • Treseder, K.K. (2008). Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11, 1111–1120.

    Article  PubMed  Google Scholar 

  • Vergutz, L., Manzoni, S., Porporato, A., Novais, R.F., and Jackson, R.B. (2012). Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82, 205–220.

    Article  Google Scholar 

  • Vitousek, P.M. (2004). Nutrient Cycling and Limitation: Hawai’i as a model system. Princeton: Princeton University Press.

    Book  Google Scholar 

  • Vitousek, P.M., and Howarth, R.W. (1991). Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13.

  • Vitousek, P.M., Menge, D.N.L., Reed, S.C., and Cleveland, C.C. (2013). Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Phil Trans R Soc B 368, 20130119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker, A.P., Zaehle, S., Medlyn, B.E., De Kauwe, M.G., Asao, S., Hickler, T., Parton, W., Ricciuto, D.M., Wang, Y., Wårlind, D., et al. (2015). Predicting long-term carbon sequestration in response to CO2 enrichment: how and why do current ecosystem models differ? Glob Biogeochem Cycle 29, 476–495.

    Article  CAS  Google Scholar 

  • Wang, G., Li, J., Ravi, S., Dukes, D., Gonzales, H.B., and Sankey, J.B. (2019). Post-fire redistribution of soil carbon and nitrogen at a grassland-shrubland ecotone. Ecosystems 22, 174–188.

    Article  CAS  Google Scholar 

  • Wieder, W.R., Bonan, G.B., and Allison, S.D. (2013). Global soil carbon projections are improved by modelling microbial processes. Nat Clim Change 3, 909–912.

    Article  CAS  Google Scholar 

  • Wieder, W.R., Cleveland, C.C., Smith, W.K., and Todd-Brown, K. (2015). Future productivity and carbon storage limited by terrestrial nutrient availability. Nat Geosci 8, 441–444.

    Article  CAS  Google Scholar 

  • Wild, B., Li, J., Pihlblad, J., Bengtson, P., and Rütting, T. (2019). Decoupling of priming and microbial N mining during a short-term soil incubation. Soil Biol Biochem 129, 71–79.

    Article  CAS  Google Scholar 

  • Xing, A., Du, E., Shen, H., Xu, L., de Vries, W., Zhao, M., Liu, X., and Fang, J. (2022). Nonlinear responses of ecosystem carbon fluxes to nitrogen deposition in an old-growth boreal forest. Ecol Lett 25, 77–88.

    Article  PubMed  Google Scholar 

  • Xu, C., Xu, X., Ju, C., Chen, H.Y.H., Wilsey, B.J., Luo, Y., and Fan, W. (2021). Long-term, amplified responses of soil organic carbon to nitrogen addition worldwide. Glob Change Biol 27, 1170–1180.

    Article  CAS  Google Scholar 

  • Xu, W., and Yuan, W. (2017). Responses of microbial biomass carbon and nitrogen to experimental warming: a meta-analysis. Soil Biol Biochem 115, 265–274.

    Article  CAS  Google Scholar 

  • Wu, Q., Zhang, C., Liang, X., Zhu, C., Wang, T., and Zhang, J. (2020). Elevated CO2 improved soil nitrogen mineralization capacity of rice paddy. Sci Total Environ 710, 136438.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y., Luo, Y., and Finzi, A.C. (2011). Carbon and nitrogen dynamics during forest stand development: a global synthesis. New Phytol 190, 977–989.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y., Shi, Y., Sun, W., Chang, J., Zhu, J., Chen, L., Wang, X., Guo, Y., Zhang, H., Yu, L., et al. (2022). Terrestrial carbon sinks in China and around the world and their contribution to carbon neutrality. Sci China Life Sci 65, 861–895.

    Article  CAS  PubMed  Google Scholar 

  • Yue, K., Peng, Y., Fornara, D.A., Van Meerbeek, K., Vesterdal, L., Yang, W., Peng, C., Tan, B., Zhou, W., Xu, Z., et al. (2019). Responses of nitrogen concentrations and pools to multiple environmental change drivers: a meta-analysis across terrestrial ecosystems. Global Ecol Biogeogr 28, 690–724.

    Article  Google Scholar 

  • Yuan, Z.Y., and Chen, H.Y.H. (2009). Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Glob Ecol Biogeogr 18, 11–18.

    Article  Google Scholar 

  • Zaehle, S., and Dalmonech, D. (2011). Carbon-nitrogen interactions on land at global scales: current understanding in modelling climate biosphere feedbacks. Curr Opin Environ Sust 3, 311–320.

    Article  Google Scholar 

  • Zaehle, S., Medlyn, B.E., De Kauwe, M.G., Walker, A.P., Dietze, M.C., Hickler, T., Luo, Y., Wang, Y.P., El-Masri, B., Thornton, P., et al. (2014). Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate Free-Air CO2 Enrichment studies. New Phytol 202, 803–822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, T., Chen, H.Y.H., and Ruan, H. (2018a). Global negative effects of nitrogen deposition on soil microbes. ISME J 12, 1817–1825.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, T., Luo, Y., Chen, H.Y.H., and Ruan, H. (2018b). Responses of litter decomposition and nutrient release to N addition: a meta-analysis of terrestrial ecosystems. Appl Soil Ecol 128, 35–42.

    Article  Google Scholar 

  • Zheng, M., Zhou, Z., Luo, Y., Zhao, P., and Mo, J. (2019). Global pattern and controls of biological nitrogen fixation under nutrient enrichment: A meta-analysis. Glob Change Biol 25, 3018–3030.

    Article  Google Scholar 

  • Zheng, M., Zhou, Z., Zhao, P., Luo, Y., Ye, Q., Zhang, K., Song, L., and Mo, J. (2020). Effects of human disturbance activities and environmental change factors on terrestrial nitrogen fixation. Glob Change Biol 26, 6203–6217.

    Article  Google Scholar 

  • Zhou, Z., Wang, C., Zheng, M., Jiang, L., and Luo, Y. (2017). Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115, 433–441.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31988102) and the National Key Research and Development Program of China (2022YFF0802102).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shuli Niu.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niu, S., Song, L., Wang, J. et al. Dynamic carbon-nitrogen coupling under global change. Sci. China Life Sci. 66, 771–782 (2023). https://doi.org/10.1007/s11427-022-2245-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-022-2245-y

Navigation