Losses of nitrogen from agriculture are a major threat to environmental and human health at local, regional and global scales. Emerging evidence shows that climate change and intensive agricultural management will interact to increase the harmful effects and undermine current mitigation efforts. Identifying effective mitigation strategies and supporting policies requires an integrated understanding of the processes underlying potential agricultural nitrogen responses to climate change. In this Review, we describe these processes, propose a set of multi-scale principles to guide research and policy for decreasing nitrogen losses in the future, and describe the economic factors that could constrain or enable their implementation.
Subscribe to Journal
Get full journal access for 1 year
only $8.67 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Fowler, D. et al. The global nitrogen cycle in the twenty-first century. Philos. Trans. R. Soc. Lond. Ser. B 368, 20130164 (2013).
Zhang, X. et al. Managing nitrogen for sustainable development. Nature 528, 51–59 (2015).
Erisman, J. W. et al. Consequences of human modification of the global nitrogen cycle. Philos. Trans. R. Soc. Lond. Ser. B 368, 20130116 (2014).
Vermeulen, S. J. et al. Addressing uncertainty in adaptation planning for agriculture. Proc. Natl Acad. Sci. USA 110, 8357–8362 (2013).
Robertson, G. P. & Vitousek, P. M. Nitrogen in agriculture: balancing the cost of an essential resource. Annu. Rev. Environ. Resour. 34, 97–125 (2009).
Stuart, D. et al. The need for a coupled human and natural systems understanding of agricultural nitrogen loss. Bioscience 65, 571–578 (2015).
Austin, A. T. et al. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221–235 (2004).
Greaver, T. L. et al. Key ecological responses to nitrogen are altered by climate change. Nat. Clim. Change 6, 836–843 (2016).
Kirtman, B. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. et al.) 953–1028 (IPCC, Cambridge Univ. Press, 2013).
Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Change 4, 17–22 (2014).
Fay, P. A. et al. Relative effects of precipitation variability and warming on tallgrass prairie ecosystem function. Biogeosciences 8, 3053–3068 (2011).
Sinha, E., Michalak, A. M. & Balaji, V. Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357, 405–408 (2017).
Lam, S. K., Chen, D., Norton, R., Armstrong, R. & Mosier, A. R. Nitrogen dynamics in grain crop and legume pasture systems under elevated atmospheric carbon dioxide concentration: a meta-analysis. Glob. Change Biol. 18, 2853–2859 (2012).
Steward, D. R. et al. Tapping unsustainable groundwater stores for agricultural production in the High Plains Aquifer of Kansas, projections to 2110. Proc. Natl Acad. Sci. USA 110, E3477–E3486 (2013).
Cassman, K. G., Dobermann, A. & Walters, D. T. Agroecosystems, nitrogen-use efficiency, and nitrogen management. Ambio 31, 132–140 (2002).
Turner, R. E. & Rabalais, N. N. Linking landscape and water quality in the Mississippi River Basin for 200 years. Bioscience 53, 563–572 (2003).
Wu, Z., Dijkstra, P., Koch, G. W., Peñuelas, J. & Hungate, B. A. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob. Change Biol. 17, 927–942 (2011).
Deser, C., Knutti, R., Solomon, S. & Phillips, A. S. Communication of the role of natural variability in future North American climate. Nat. Clim. Change 2, 775–779 (2012).
Harding, K. J. & Snyder, P. K. Examining future changes in the character of Central U.S. warm-season precipitation using dynamical downscaling. J. Geophys. Res. Atmos. 119, 13116–13136 (2014).
Patricola, C. M. & Cook, K. H. Mid-twenty-first century warm season climate change in the Central United States. Part I: regional and global model predictions. Clim. Dyn. 40, 551–568 (2013).
Feng, Z. et al. More frequent intense and long-lived storms dominate the springtime trend in central US rainfall. Nat. Commun. 7, 13429 (2016).
Swain, S. & Hayhoe, K. CMIP5 projected changes in spring and summer drought and wet conditions over North America. Clim. Dyn. 44, 2737–2750 (2015).
Villarini, G. et al. On the frequency of heavy rainfall for the Midwest of the United States. J. Hydrol. 400, 103–120 (2011).
Manzoni, S., Moyano, F., Kätterer, T. & Schimel, J. Modeling coupled enzymatic and solute transport controls on decomposition in drying soils. Soil Biol. Biochem. 95, 275–287 (2016).
Manzoni, S., Schimel, J. P. & Porporato, A. Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93, 930–938 (2012).
Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).
Stark, J. M. & Firestone, M. K. Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl. Environ. Microbiol. 61, 218–221 (1995).
Larsen, K. S. et al. Reduced N cycling in response to elevated CO2, warming, and drought in a Danish heathland: synthesizing results of the CLIMAITE project after two years of treatments. Glob. Change Biol. 17, 1884–1899 (2011).
Gonzalez-Dugo, V., Durand, J. & Gastal, F. Water deficit and nitrogen nutrition of crops. A review. Agron. Sustain. Dev. 30, 529–544 (2010).
Liu, J. et al. A high-resolution assessment on global nitrogen flows in cropland. Proc. Natl Acad. Sci. USA 107, 8035–8040 (2010).
Grandy, A., Kallenbach, C., Loecke, T. D., Snapp, S. S. & Smith, R. G. Microbial Ecology in Sustainable Agroecosystems (eds Cheeke, T. E., Coleman, D. C. & Wall, D. H.) 113–132 (CRC Press, Boca Raton, 2012).
Pang, X. & Letey, J. Organic farming: challenge of timing nitrogen availability to crop nitrogen requirements. Soil Sci. Soc. Am. J 64, 247–253 (2000).
Sawyer, J. et al. Concepts and Rationale for Regional Nitrogen Rate Guidelines for Corn Concepts and Rationale for Regional Nitrogen Rate Guidelines for Corn (Iowa State Univ. Extension, 2006).
Drinkwater, L. E. & Snapp, S. Nutrients in agroecosystems: rethinking the management paradigm. Adv. Agron. 92, 163–186 (2007).
Basche, A. D., Miguez, F. E., Kaspar, T. C. & Castellano, M. J. Do cover crops increase or decrease nitrous oxide emissions? A meta-analysis. J. Soil Water Conserv. 69, 471–482 (2014).
Castellano, M. J., Lewis, D. B., Andrews, D. M. & McDaniel, M. D. in Hydropedology (ed. Lin, H.) 711–735 (Elsevier, Oxford, 2012).
Hansen, M., Clough, T. J. & Elberling, B. Flooding-induced N2O emission bursts controlled by pH and nitrate in agricultural soils. Soil Biol. Biochem. 69, 17–24 (2014).
Chen, Z. et al. Increased N2O emissions during soil drying after waterlogging and spring thaw in a record wet year. Soil Biol. Biochem. 101, 152–164 (2016).
Congreves, K. A. et al. How does climate variability influence nitrogen loss in temperate agroecosystems under contrasting management systems? Agric. Ecosyst. Environ. 227, 33–41 (2016).
Wang, Z., Qi, Z., Xue, L., Bukovsky, M. & Helmers, M. J. Modeling the impacts of climate change on nitrogen losses and crop yield in a subsurface drained field. Clim. Change 129, 323–335 (2015).
Patil, R. H., Laegdsmand, M., Olesen, J. E. & Porter, J. R. Effect of soil warming and rainfall patterns on soil N cycling in Northern Europe. Agric. Ecosyst. Environ. 139, 195–205 (2010).
Jabloun, M., Schelde, K., Tao, F. & Olesen, J. E. Effect of temperature and precipitation on nitrate leaching from organic cereal cropping systems in Denmark. Eur. J. Agron. 62, 55–64 (2015).
Nangia, V., Gowda, P. H., Mulla, D. J. & Sands, G. R. Modeling impacts of tile drain spacing and depth on nitrate-nitrogen losses. Vadose Zone J. 9, 61–72 (2010).
Castellano, M. J. et al. Hydrological and biogeochemical controls on the timing and magnitude of nitrous oxide flux across an agricultural landscape. Glob. Change Biol. 16, 2711–2720 (2010).
Butterbach-Bahl, K. & Dannenmann, M. Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate. Curr. Opin. Environ. Sustain. 3, 389–395 (2011).
Akiyama, H., Yagi, K. & Yan, X. Direct N2O emissions from rice paddy fields: summary of available data. Glob. Biogeochem. Cycles 19, 1–10 (2005).
Hatfield, J. L. et al. Climate impacts on agriculture: implications for crop production. Agron. J. 103, 351–370 (2011).
Dannenmann, M. et al. Climate change impairs nitrogen cycling in european beech forests. PLoS ONE 11, 1–24 (2016).
Liang, L. L., Grantz, D. A. & Jenerette, G. D. Multivariate regulation of soil CO2 and N2O pulse emissions from agricultural soils. Glob. Change Biol. 22, 1286–1298 (2016).
Gelfand, I., Cui, M., Tang, J. & Robertson, G. P. Short-term drought response of N2O and CO2 emissions from mesic agricultural soils in the US Midwest. Agric. Ecosyst. Environ. 212, 127–133 (2015).
Gentry, L. E., David, M. B., Smith, K. M. & Kovacic, D. A. Nitrogen cycling and tile drainage nitrate loss in a corn/soybean watershed. Agric. Ecosyst. Environ. 68, 85–97 (1998).
Morecroft, M. D., Burt, T. P., Taylor, M. E. & Rowland, A. P. Effects of the 1995–1997 drought on nitrate leaching in lowland England. Soil Use Manag. 16, 117–123 (2000).
Loecke, T. D. et al. Weather whiplash in agricultural regions drives deterioration of water quality. Biogeochemistry 133, 7–15 (2017).
Mazdiyasni, O. & AghaKouchak, A. Substantial increase in concurrent droughts and heatwaves in the United States. Proc. Natl Acad. Sci. USA 112, 11484–11489 (2015).
Jin, Z. et al. The combined and separate impacts of climate extremes on the current and future US rainfed maize and soybean production under elevated CO2. Glob. Change Biol. 23, 2687–2704 (2017).
Ainsworth, E. & Rogers, A. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant. Cell Environ. 30, 258–270 (2007).
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).
Shimono, H., Nakamura, H., Hasegawa, T. & Okada, M. Lower responsiveness of canopy evapotranspiration rate than of leaf stomatal conductance to open-air CO2 elevation in rice. Glob. Change Biol. 19, 2444–2453 (2013).
Gray, S. B. et al. Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean. Nat. Plants 2, 16132 (2016).
Jin, Z., Ainsworth, E. A., Leakey, A. D. B. & Lobell, D. B. Increasing drought and diminishing benefits of elevated carbon dioxide for soybean yields across the US Midwest. Glob. Change Biol. 24, e522–e533 (2018).
Gardner, J. B. & Drinkwater, L. E. The fate of nitrogen in grain cropping systems: a meta-analysis of 15N field experiments. Ecol. Appl. 19, 2167–2184 (2009).
Mclellan, E. et al. Reducing nitrogen export from the corn belt to the Gulf of Mexico: agricultural strategies for remediating hypoxia. J. Am. Water Resour. Assoc. 51, 263–289 (2015).
Scavia, D. et al. Ensemble modeling informs hypoxia management in the northern Gulf of Mexico. Proc. Natl Acad. Sci. USA 114, 201705293 (2017).
Iqbal, J. et al. Extreme weather-year sequences have non-additive effects on environmental nitrogen losses. Glob. Change Biol. 24, e303–e317 (2018).
Slingo, J. & Palmer, T. Uncertainty in weather and climate prediction. Philos. Trans. R. Soc. Lond. Ser. A 369, 4751–4767 (2011).
Sela, S. et al. Adapt-N outperforms grower-selected nitrogen rates in Northeast and Midwestern United States strip trials. Agron. J. 108, 1726–1734 (2016).
Lynch, J. P. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot. 112, 347–357 (2013).
Colmer, T. D. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ. 26, 17–36 (2003).
Koebernick, N. et al. High-resolution synchrotron imaging shows that root hairs influence rhizosphere soil structure formation. New Phytol. 216, 124–135 (2017).
Ahmed, M. A., Kroener, E., Holz, M., Zarebanadkouki, M. & Carminati, A. Mucilage exudation facilitates root water uptake in dry soils. Funct. Plant Biol. 41, 1129–1137 (2014).
Zhu, B. et al. Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol. Biochem. 76, 183–192 (2014).
Austin, E. E., Wickings, K., McDaniel, M. D., Robertson, G. P. & Grandy, A. S. Cover crop root contributions to soil carbon in a no-till corn bioenergy cropping system. Glob. Change Biol. Bioenergy 9, 1252–1263 (2017).
Lin, B. B. Resilience in agriculture through crop diversification: adaptive management for environmental change. Bioscience 61, 183–193 (2011).
Liebman, M. & Schulte, L. A. Enhancing agroecosystem performance and resilience through increased diversification of landscapes and cropping systems. Elementa 3, 1–7 (2015).
Gentry, L. F., Ruffo, M. L. & Below, F. E. Identifying factors controlling the continuous corn yield penalty. Agron. J. 105, 295–303 (2013).
Gaudin, A. C. M. et al. Increasing crop diversity mitigates weather variations and improves yield stability. PLoS ONE 10, e0113261 (2015).
McDaniel, M., Tiemann, L. & Grandy, A. Does agricultural crop diversity enhance soil microbial biomass and organic matter dynamics? A meta-analysis. Ecol. Appl. 24, 560–570 (2014).
Grandy, A. S., Robertson, G. P. & Philip, G. Land-use intensity effects on soil organic carbon accumulation rates and mechanisms. Ecosystems 10, 58–73 (2007).
Bowles, T. M., Jackson, L. E., Loeher, M. & Cavagnaro, T. R. Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects. J. Appl. Ecol. 54, 1785–1793 (2017).
Rawls, W. J., Pachepsky, Y. A., Ritchie, J. C., Sobecki, T. M. & Bloodworth, H. Effect of soil organic carbon on soil water retention. Geoderma 116, 61–76 (2003).
Basche, A. D. et al. Soil water improvements with the long-term use of a winter rye cover crop. Agric. Water Manag. 172, 40–50 (2016).
Daigh, A. L. et al. Soil water during the drought of 2012 as affected by rye cover crops in fields in Iowa and Indiana. J. Soil Water Conserv. 69, 564–573 (2014).
Bowles, T. M., Barrios-Masias, F. H., Carlisle, E. A., Cavagnaro, T. R. & Jackson, L. E. Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci. Total Environ. 566–567, 1223–1234 (2016).
Bowles, T. M., Jackson, L. E. & Cavagnaro, T. R. Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob. Change Biol. 24, e171–e182 (2018).
Cavagnaro, T. R., Bender, S. F., Asghari, H. R. & van der Heijden, M. G. A. The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci. 20, 283–290 (2015).
Williams, A. et al. Reconciling opposing soil processes in row-crop agroecosystems via soil functional zone management. Agric. Ecosyst. Environ. 236, 99–107 (2017).
Kallenbach, C. & Grandy, A. S. Controls over soil microbial biomass responses to carbon amendments in agricultural systems: a meta-analysis. Agric. Ecosyst. Environ. 144, 241–252 (2011).
Kallenbach, C. M., Grandy, A. S., Frey, S. D. & Diefendorf, A. F. Microbial physiology and necromass regulate agricultural soil carbon accumulation. Soil Biol. Biochem. 91, 279–290 (2015).
Reese, C. L. et al. Winter cover crops impact on corn production in semiarid regions. Agron. J. 106, 1479–1488 (2014).
Qi, Z., Helmers, M. J. & Kaleita, A. L. Soil water dynamics under various agricultural land covers on a subsurface drained field in north-central Iowa, USA. Agric. Water Manag. 98, 665–674 (2011).
Tonitto, C., David, M. B. & Drinkwater, L. E. Replacing bare fallows with cover crops in fertilizer-intensive cropping systems: a meta-analysis of crop yield and N dynamics. Agric. Ecosyst. Environ. 112, 58–72 (2006).
Panagopoulos, Y. et al. Surface water quality and cropping systems sustainability under a changing climate in the Upper Mississippi River Basin. J. Soil Water Conserv. 69, 483–494 (2014).
Williams, A. et al. A comparison of soil hydrothermal properties in zonal and uniform tillage systems across the US Corn Belt. Geoderma 273, 12–19 (2016).
Trenberth, K. E. Changes in precipitation with climate change. Clim. Res. 47, 123–138 (2011).
Nearing, M. A. et al. Modeling response of soil erosion and runoff to changes in precipitation and cover. Catena 61, 131–154 (2005).
Zhou, X. et al. Nutrient removal by prairie filter strips in agricultural landscapes. J. Soil Water Conserv. 69, 54–64 (2014).
Addy, K. et al. Denitrifying bioreactors for nitrate removal: a meta-analysis. J. Environ. Qual. 45, 873 (2016).
Hansen, A. T., Dolph, C. L., Foufoula-Georgiou, E. & Finlay, J. C. Contribution of wetlands to nitrate removal at the watershed scale. Nat. Geosci. 11, 127–132 (2018).
Samuelson, W. & Zeckhauser, R. Status quo bias in decision making. J. Risk Uncertain. 1, 7–59 (1988).
Barbier, E. B. Valuing ecosystem services as productive inputs. Econ. Policy 22, 178–229 (2007).
Atallah, S. S., Gómez, M. I. & Jaramillo, J. A Bioeconomic model of ecosystem services provision: coffee berry borer and shade-grown coffee in Colombia. Ecol. Econ. 144, 129–138 (2018).
Rejesus, R. M. & Hornbaker, R. H. Economic and environmental evaluation of alternative pollution-reducing nitrogen management practices in central Illinois. Agric. Ecosyst. Environ. 75, 41–53 (1999).
Di Falco, S. & Chavas, J.-P. On crop biodiversity, risk exposure, and food security in the highlands of Ethiopia. Am. J. Agric. Econ. 91, 599–611 (2009).
Di Falco, S. On the value of agricultural biodiversity. Annu. Rev. Resour. Econ. 4, 207–223 (2012).
Stuart, D. & Gillon, S. Scaling up to address new challenges to conservation on US farmland. Land Use Policy 31, 223–236 (2013).
Reimer, A. & Prokopy, L. One federal policy, four different policy contexts: an examination of agri-environmental policy implementation in the Midwestern United States. Land Use Policy 38, 605–614 (2014).
Healthly Soils Program California Department of Food and Agriculture https://www.cdfa.ca.gov/oefi/healthysoils/ (2017).
Cassidy, E. S., West, P. C., Gerber, J. S. & Foley, J. A. Redefining agricultural yields: from tonnes to people nourished per hectare. Environ. Res. Lett. 8, 034015 (2013).
Muller, A. et al. Strategies for feeding the world more sustainably with organic agriculture. Nat. Commun. 8, 1290 (2017).
Del Grosso, S. J. et al. Introducing the GRACEnet/REAP Data Contribution, Discovery, and Retrieval System. J. Environ. Qual. 42, 1274–1280 (2013).
Logan, T. J., Eckert, D. J. & Beak, D. G. Tillage, crop and climatic effects of runoff and tile drainage losses of nitrate and four herbicides. Soil Tillage Res. 30, 75–103 (1994).
Lawlor, P. A., Helmers, M. J., Baker, J. L., Melvin, S. W. & Lemke, D. W. Nitrogen application rate effect on nitrate-nitrogen concentration and loss in subsurface drainage for a corn-soybean rotation. Trans. ASABE 51, 83–94 (2008).
Butterbach-Bahl, K., Baggs, E. M., Dannenmann, M., Kiese, R. & Zechmeister-Boltenstern, S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos. Trans. R. Soc. Lond. Ser. B 368, 20130122 (2013).
Kleber, M. et al. in Advances in Agronomy Vol. 130 (ed. Sparks, D. L.) Ch. 1, 1–140 (Elsevier, Oxford, 2015).
We acknowledge funding to T.M.B. from a US Department of Agriculture Agriculture and Food Research Initiative Education and Literacy Initiative (AFRI ELI) postdoctoral fellowship (2017-67012-26094), to A.S.G. from US Department of Agriculture National Institute of Food and Agriculture Agriculture Experiment Station (NIFA AES) project CA-D-PLS-2332-H, and to W.R.W. from US Department of Agriculture (NIFA 2015-67003-23485) and US Environmental Protection Agency. We thank C. Stewart and V. Jin for providing data and assistance with DAYCENT modelling. We acknowledge the Kellogg Biological Station Long-term Ecological Research Program and GRACEnet for data used to make Fig. 2a and Fig. 2b,c, respectively.
The authors declare no competing interests.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Bowles, T.M., Atallah, S.S., Campbell, E.E. et al. Addressing agricultural nitrogen losses in a changing climate. Nat Sustain 1, 399–408 (2018) doi:10.1038/s41893-018-0106-0
Yields and resilience outcomes of organic, cover crop, and conventional practices in a Mediterranean climate
Scientific Reports (2019)
Environmental Science & Technology (2019)
Field Crops Research (2019)
Frontiers in Microbiology (2019)
Journal of Applied Ecology (2019)