The use of fossil fuels and fertilizers has increased the amount of biologically reactive nitrogen in the atmosphere over the past century. As a consequence, forests in industrialized regions have experienced greater rates of nitrogen deposition in recent decades. This unintended fertilization has stimulated forest growth, but has also affected soil microbial activity, and thus the recycling of soil carbon and nutrients. A meta-analysis suggests that nitrogen deposition impedes organic matter decomposition, and thus stimulates carbon sequestration, in temperate forest soils where nitrogen is not limiting microbial growth. The concomitant reduction in soil carbon emissions is substantial, and equivalent in magnitude to the amount of carbon taken up by trees owing to nitrogen fertilization. As atmospheric nitrogen levels continue to rise, increased nitrogen deposition could spread to older, more weathered soils, as found in the tropics; however, soil carbon cycling in tropical forests cannot yet be assessed.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Davidson, E. A. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geosci. 2, 659–662 (2009).
Denman, K. L. et al. in IPCC Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.), 499–587 (Cambridge Univ. Press, 2007).
Galloway, J. N. et al. Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226 (2004).
Dentener, F. et al. Nitrogen and sulfur deposition on regional and global scales: A multimodel evaluation. Glob. Biogeochem. Cycles 20, GB4003 (2006).
Lamarque, J. F. et al. Assessing future nitrogen deposition and carbon cycle feedback using a multimodel approach: Analysis of nitrogen deposition. J. Geophys. Res. 110, D19303 (2005).
Aber, J. D., Nadelhoffer, K. J., Steudler, P. & Melillo, J. M. Nitrogen saturation in northern forest ecosystems. Bioscience 39, 378–386 (1989).
Vitousek, P. M. et al. Human alteration of the global nitrogen cycle: Sources and consequences. Ecol. Appl. 7, 737–750 (1997).
Maskell, L. C., Smart, S. M., Bullock, J. M., Thompson, K. & Stevens, C. J. Nitrogen deposition causes widespread loss of species richness in British habitats. Glob. Change Biol. 16, 671–679 (2010).
de Vries, W., van der Salm, C., Reinds, G. J. & Erisman, J. W. Element fluxes through European forest ecosystems and their relationships with stand and site characteristics. Environ. Pollut. 148, 501–513 (2007).
Dise, N. B., Rothwell, J. J., Gauci, V., van der Salm, C., & de Vries, W. Predicting dissolved inorganic nitrogen leaching in European forests using two independent databases. Sci. Total Environ. 407, 1798–1808 (2009).
Högberg, P., Fan, H. B., Quist, M., Binkley, D. & Tamm, C. O. Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob. Change Biol. 12, 489–499 (2006).
Reay, D. S., Dentener, F., Smith, P., Grace, J. & Feely, R. A. Global nitrogen deposition and carbon sinks. Nature Geosci. 1, 430–437 (2008).
Ciais, P. et al. Carbon accumulation in European forests. Nature Geosci. 1, 425–429 (2008).
Pregitzer, K. S., Burton, A. J., Zak, D. R. & Talhelm, A. F. Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Glob. Change Biol. 14, 142–153 (2008).
Thomas, R. Q., Canham, C. D., Weathers, K. C. & Goodale, C. L. Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geosci. 3, 13–17 (2010).
Magnani, F. et al. The human footprint in the carbon cycle of temperate and boreal forests. Nature 447, 848–850 (2007).
de Vries, W. et al. Ecologically implausible carbon response? Nature 451, E1–E3 (2008).
Sutton, M. A. et al. Uncertainties in the relationship between atmospheric nitrogen deposition and forest carbon sequestration. Glob. Change Biol. 14, 2057–2063 (2008).
Janssens, I. A. & Luyssaert, S. Nitrogen's carbon bonus. Nature Geosci. 2, 318–319 (2009).
Elvir, J. A., Wiersma, G. B., White, A. S. & Fernandez, I. J. Effects of chronic ammonium sulfate treatment on basal area increment in red spruce and sugar maple at the Bear Brook watershed in Maine. Can. J. Forest Res. 33, 862–869 (2003).
Olsson, P., Linder, S., Giesler, R. & Högberg, P. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob. Change Biol. 11, 1745–1753 (2005).
Hyvönen, R. et al. The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol. 173, 463–480 (2007).
Fog, K. The effect of added nitrogen on the rate of decomposition of organic-matter. Biol. Rev. 63, 433–462 (1988).
Berg, B. & Matzner, E. Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ. Rev. 5, 1–25 (1997).
Melillo, J. M., Aber, J. D. & Muratore, J. F. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63, 621–626 (1982).
Aber, J. D. & Melillo, J. M. Litter decomposition — measuring relative contributions of organic-matter and nitrogen to forest soils. Can. J. Bot. 58, 416–421 (1980).
Swift, M. J., Heal, O. W. & Anderson, J. M. (eds) Decomposition in Terrestrial Ecosystems (Blackwell Scientific, 1979).
McClaugherty, C. & Berg, B. Cellulose, lignin and nitrogen concentrations as rate regulating factors in late stages of forest litter decomposition. Pedobiologia 30, 101–112 (1987).
Knorr, M., Frey, S. D. & Curtis, P. S. Nitrogen additions and litter decomposition: A meta-analysis. Ecology 86, 3252–3257 (2005).
Rosenberg, M. S., Adams, D. C. & Gurevitch, J. Metawin: Statistical Software for Meta-Analysis (Sinauer Associates Inc., 2000).
Hanson, P. J., Edwards, N. T., Garten, C. T. & Andrews, J. A. Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48, 115–146 (2000).
Subke, J. A., Inglima, I. & Cotrufo, M. F. Trends and methodological impacts in soil CO2 efflux partitioning: A metaanalytical review. Glob. Change Biol. 12, 921–943 (2006).
Kutsch, W., Bahn, M. & Heinemeyer, A. (eds) Soil Carbon Dynamics: An Integrated Methodology (Cambridge Univ. Press, 2009).
Ekblad, A. & Högberg, P. Natural abundance of C-13 in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127, 305–308 (2001).
Sampson, D. A., Janssens, I. A., Yuste, J. C. & Ceulemans, R. Basal rates of soil respiration are correlated with photosynthesis in a mixed temperate forest. Glob. Change Biol. 13, 2008–2017 (2007).
Högberg, P. et al. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792 (2001).
Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007).
Cheng, W. & Johnson, D. W. Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202, 167–174 (1998).
Kuzyakov, Y. Review: Factors affecting rhizosphere priming effects. J. Plant Nutr. Soil Sci. 165, 382–396 (2002).
Martikainen, P. J., Aarnio, T., Taavitsainen, V. M., Paivinen, L. & Salonen, K. Mineralization of carbon and nitrogen in soil samples taken from 3 fertilized pine stands — long-term effects. Plant Soil 114, 99–106 (1989).
Ågren, G. I., Bosatta, E. & Magill, A. H. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128, 94–98 (2001).
Oren, R. et al. Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411, 469–472 (2001).
Butnor, J. R., Johnsen, K. H., Oren, R. & Katul, G. G. Reduction of forest floorrespiration by fertilization on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands. Glob. Change Biol. 9, 849–861 (2003).
Ceulemans, R. & Mousseau, M. Tansley review no-71 — Effects of elevated atmospheric CO2 on woody-plants. New Phytol. 127, 425–446 (1994).
de Vries, W. et al. The impact of nitrogen deposition on carbon sequestration by European forests and heathlands. Forest Ecol. Manag. 258, 1814–1823 (2009).
Hyvönen, R. et al. Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe. Biogeochemistry 89, 121–137 (2008).
Treseder, K. K. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11, 1111–1120 (2008).
Litton, C. M., Raich, J. W. & Ryan, M. G. Carbon allocation in forest ecosystems. Glob. Change Biol. 13, 2089–2109 (2007).
Treseder, K. K. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164, 347–355 (2004).
Högberg, M. N., Baath, E., Nordgren, A., Arnebrant, K. & Högberg, P. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs — a hypothesis based on field observations in boreal forest. New Phytol. 160, 225–238 (2003).
Ruhling, A. & Tyler, G. Effects of simulated nitrogen deposition to the forest floor on the macrofungal flora of a beech forest. Ambio 20, 261–263 (1991).
Tietema, A. Microbial carbon and nitrogen dynamics in coniferous forest floor material collected along a European nitrogen deposition gradient. Forest Ecol. Manag. 101, 29–36 (1998).
Egerton-Warburton, L. M. & Allen, E. B. Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol. Appl. 10, 484–496 (2000).
Johnson, N. C. Can fertilization of soil select less mutualistic mycorrhizae. Ecol. Appl. 3, 749–757 (1993).
van Diepen, L. T. A., Lilleskov, E. A., Pregitzer, K. S. & Miller, R. M. Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol. 176, 175–183 (2007).
Phillips, R. P. & Fahey, T. J. Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol. 176, 655–664 (2007).
Gadgil, R. L. & Gadgil, P. D. Mycorrhiza and litter decomposition. Nature 233, 133 (1971).
Högberg, M. N. & Högberg, P. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 154, 791–795 (2002).
van Groenigen, K. J. et al. Element interactions limit soil carbon storage. Proc. Natl Acad. Sci. USA 103, 6571–6574 (2006).
Hoosbeek, M. R. et al. More new carbon in the mineral soil of a poplar plantation under free air carbon enrichment (POPFACE): Cause of increased priming effect? Glob. Biogeochem. Cycles 18, GB1040 (2004).
Wu, J., Brookes, P. C. & Jenkinson, D. S. Formation and destruction of microbial biomass during the decomposition of glucose and ryegrass in soil. Soil Biol. Biochem. 25, 1435–1441 (1993).
Kuzyakov, Y., Friedel, J. K. & Stahr, K. Review of mechanisms and quantification of priming effects. Soil Biol. Biochem. 32, 1485–1498 (2000).
Fontaine, S., Bardoux, G., Abbadie, L. & Mariotti, A. Carbon input to soil may decrease soil carbon content. Ecol. Lett. 7, 314–320 (2004).
Subke, J. A. et al. Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia 139, 551–559 (2004).
Merckx, R., Dijkstra, A., Denhartog, A. & Vanveen, J. A. Production of root-derived material and associated microbial-growth in soil at different nutrient levels. Biol. Fert. Soils 5, 126–132 (1987).
Lekkerkerk, L., Lundkvist, H., Ågren, G. I., Ekbohm, G. & Bosatta, E. Decomposition of heterogeneous substrates — an experimental investigation of a hypothesis on substrate and microbial properties. Soil Biol. Biochem. 22, 161–167 (1990).
Liljeroth, E., Vanveen, J. A. & Miller, H. J. Assimilate translocation to the rhizosphere of two wheat lines and subsequent utilization by rhizosphere microorganisms at two soil-nitrogen concentrations. Soil Biol. Biochem. 22, 1015–1021 (1990).
Mangenot, F. & Reymond, G. Populations microbiennes des bois. V. Influences de quelques sources de carbone et d'azote sur la décomposition d'une sciure. Rev. Gen. Bot. 70, 107–129 (1963).
Compton, J. E., Watrud, L. S., Porteous, L. A. & DeGrood, S. Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. Forest Ecol. Manag. 196, 143–158 (2004).
Frey, S. D., Knorr, M., Parrent, J. L. & Simpson, R. T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol. Manag. 196, 159–171 (2004).
Feng, X. J., Simpson, A. J., Wilson, K. P., Williams, D. D. & Simpson, M. J. Increased cuticular carbon sequestration and lignin oxidation in response to soil warming. Nature Geosci. 1, 836–839 (2008).
Sinsabaugh, R. L., Gallo, M. E., Lauber, C., Waldrop, M. P. & Zak, D. R. Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75, 201–215 (2005).
Keeler, B. L., Hobbie, S. E. & Kellogg, L. E. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: Implications for litter and soil organic matter decomposition. Ecosystems 12, 1–15 (2009).
Carreiro, M. M., Sinsabaugh, R. L., Repert, D. A. & Parkhurst, D. F. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81, 2359–2365 (2000).
Sjoberg, G., Nilsson, S. I., Persson, T. & Karlsson, P. Degradation of hemicellulose, cellulose and lignin in decomposing spruce needle litter in relation to N. Soil Biol. Biochem. 36, 1761–1768 (2004).
DeForest, J. L., Zak, D. R., Pregitzer, K. S. & Burton, A. J. Atmospheric nitrate deposition and the microbial degradation of cellobiose and vanillin in a northern hardwood forest. Soil Biol. Biochem. 36, 965–971 (2004).
Saiya-Cork, K. R., Sinsabaugh, R. L. & Zak, D. R. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309–1315 (2002).
Keyser, P., Kirk, T. K. & Zeikus, J. G. Ligninolytic enzyme-system of phanerochaete-chrysosporium — synthesized in absence of lignin in response to nitrogen starvation. J. Bacteriol. 135, 790–797 (1978).
Tien, M. & Myer, S. B. Selection and characterization of mutants of phanerochaete-chrysosporium exhibiting ligninolytic activity under nutrient-rich conditions. Appl. Environ. Microbiol. 56, 2540–2544 (1990).
Waldrop, M. P. & Zak, D. R. Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9, 921–933 (2006).
DeForest, J. L., Zak, D. R., Pregitzer, K. S. & Burton, A. J. Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci. Soc. Am. J. 68, 132–138 (2004).
Oades, J. M. Soil organic-matter and structural stability — mechanisms and implications for management. Plant Soil 76, 319–337 (1984).
Thorn, K. A. & Mikita, M. A. Ammonia fixation by humic substances — a N-15 and C-13 NMR-study. Sci. Total Environ. 113, 67–87 (1992).
Nömmik, H. & Vahtras, K. Retention and fixation of ammonium and ammonia in soils. Agronomy Monographs 22, 123–171 (1982).
Burdon, J. Are the traditional concepts of the structures of humic substances realistic? Soil Sci. 166, 752–769 (2001).
Clinton, P. W., Newman, R. H. & Allen, R. B. Immobilization of N-15 in forest litter studied by N-15 CPMAS NMR spectroscopy. Eur. J. Soil Sci. 46, 551–556 (1995).
Aber, J. et al. Nitrogen saturation in temperate forest ecosystems — Hypotheses revisited. Bioscience 48, 921–934 (1998).
Sutton, R. & Sposito, G. Molecular structure in soil humic substances: The new view. Environ. Sci. Technol. 39, 9009–9015 (2005).
Bowden, R. D., Davidson, E., Savage, K., Arabia, C. & Steudler, P. Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. Forest Ecol. Manag. 196, 43–56 (2004).
Schulze, E. D. et al. Importance of methane and nitrous oxide for Europe's terrestrial greenhouse-gas balance. Nature Geosci. 2, 842–850 (2009).
Janssens, I. A. et al. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Glob. Change Biol. 7, 269–278 (2001).
Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).
Luyssaert, S. et al. CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob. Change Biol. 13, 2509–2537 (2007).
Reichstein, M. et al. Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis. Glob. Change Biol. 13, 634–651 (2007).
Piao, S. L. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).
Schulze, E. D., Oren, R. & Lange, O. L. in Processes Leading to Forest Decline Vol. 77 (eds Schulze, E. D., Lange, O. L. & Oren, R.) 460–468 (Springer, 1989).
Braun, S., Thomas, V. F. D., Quiring, R. & Fluckiger, W. Environ. Pollut. 10.1016/j.envpol.2009.11.030 (in the press).
Matson, P. A., McDowell, W. H., Townsend, A. R. & Vitousek, P. M. The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46, 67–83 (1999).
Bonan, G. Carbon cycle: Fertilizing change. Nature Geosci. 1, 645–646 (2008).
Zaehle, S., Friedlingstein, P. & Friend, A. D. Terrestrial nitrogen feedbacks may accelerate future climate change. Geophys. Res. Lett. 37, L01401 (2010).
This paper is dedicated to the memory of L. Misson, good friend and esteemed scientist. The authors acknowledge J. Gash for language editing. I.A.J. and R.C. acknowledge support from the UA-Research Centre of Excellence ECO Methusalem funding, the EC-FP7 project GHG Europe, and the Flemish National Science Foundation (FWO-Flanders). S.L. is funded by the ERC starting grant 242564. B.E.L. acknowledges the Office of Science (BER) US Department of Energy (award DE-FG02-04ER63911) for support of Ameriflux synthesis. J.A.S. acknowledges support from the UK Natural Environment Research Council (grant NE/E004512/1).
The authors declare no competing financial interests.
About this article
Cite this article
Janssens, I., Dieleman, W., Luyssaert, S. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geosci 3, 315–322 (2010). https://doi.org/10.1038/ngeo844
Response of litter decomposition and the soil environment to one-year nitrogen addition in a Schrenk spruce forest in the Tianshan Mountains, China
Scientific Reports (2022)
Effects of Short-term N Addition on Fine Root Morphological Features and Nutrient Stoichiometric Characteristics of Zanthoxylum bungeanum and Medicago sativa Seedlings in Southwest China Karst Area
Journal of Soil Science and Plant Nutrition (2022)
Soil phosphorus availability and stoichiometry determine microbial activity and functional diversity of fluvo-aquic soils under long-term fertilization regimes
Journal of Soils and Sediments (2022)
Environmental Science and Pollution Research (2022)