A shift in sulfur-cycle manipulation from atmospheric emissions to agricultural additions


Burning fossil fuels has resulted in a prominent yet unintended manipulation of the global sulfur cycle. Emissions of sulfur dioxide and reactive sulfur to the atmosphere have caused widespread health and environmental impacts and have led, ultimately, to calls to decrease sulfur emissions. However, anthropogenic modification of the sulfur cycle is far from over. Using four contrasting case studies from across the United States, we show how high levels of sulfur are added to croplands as fertilizers and pesticides and constitute a major yet under-studied environmental perturbation. Long-term sulfur additions to crops probably cause similar consequences for the health of soil and downstream aquatic ecosystems as those observed in regions historically impacted by acid rain, yet the cascade of effects has not been broadly explored. A new wave of research on the sulfur cycle will require studies that examine the integrated roles of climate, hydrology and other element cycles in modifying sulfur processes and flows within and downgradient of agricultural source areas. Such research must include not only scientists, but also farmers, regulating authorities and land managers who are engaged in developing approaches to monitor and mitigate environmental and human health impacts.

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Fig. 1: Atmospheric S deposition to the United States.
Fig. 2: Current S use in US crops relative to the peak of atmospheric deposition (1973).
Fig. 3: Case study areas used to evaluate S mass balances.

Airbus, USGS, NGA, NASA, CGIAR, NCEAS, NLS, OS, NMA, Geodatastyrelsen, GSA, GSI and the GIS User Community.

Fig. 4: Sulfur mass balances for regional case study areas.
Fig. 5: Sources and effects of S in non-agricultural and agricultural areas.

Data availability

Data for the atmospheric S deposition estimates are available through the National Atmospheric Deposition Program (https://nadp.slh.wisc.edu/) for wet deposition, the US Environmental Protection Agency Clean Air Status and Trends Network (https://www.epa.gov/castnet) for dry deposition, and the PRISM spatial climate database (https://www.prism.oregonstate.edu/) for precipitation quantity. Data for sulfate export and stream discharge are available through the United States Geological Survey (https://waterdata.usgs.gov/nwis).

Code availability

Code for the kriging analysis and modelling of atmospheric S deposition is available on GitHub (https://github.com/h-fakhraei/s_deposition.git). Code and information about Weighted Regressions on Time, Discharge and Season modelling of sulfate export are available at https://github.com/USGS-R/EGRET.


  1. 1.

    Lamarque, J.-F. et al. Multi-model mean nitrogen and sulfur deposition from the Atmospheric Chemistry and Climate Model Intercomparison Project (ACCMIP): evaluation of historical and projected future changes. Atmos. Chem. Phys. 13, 6247–6294 (2013).

    Google Scholar 

  2. 2.

    Galloway, J. N. Anthropogenic mobilization of sulphur and nitrogen: immediate and delayed consequences. Annu. Rev. Energy Env. 21, 261–292 (1996).

    Google Scholar 

  3. 3.

    Cowling, E. B. Acid precipitation in historical perspective. Environ. Sci. Technol. 16, 110A–123A (1982).

    Google Scholar 

  4. 4.

    Gorham, E. On the acidity and salinity of rain. Geochim. Cosmochim. Acta 7, 231–239 (1955).

    Google Scholar 

  5. 5.

    Likens, G. E. & Bormann, F. H. Acid rain: a serious regional environmental problem. Science 184, 1176–1179 (1974).

    Google Scholar 

  6. 6.

    Goyer, R. A. et al. Potential human health effects of acid rain: report of a workshop. Environ. Health Perspect. 60, 355–368 (1985).

    Google Scholar 

  7. 7.

    Likens, G. E., Driscoll, C. T. & Buso, D. C. Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272, 244–246 (1996).

    Google Scholar 

  8. 8.

    Johnson, A. H. & Siccama, T. G. Acid deposition and forest decline. Environ. Sci. Technol. 17, 294A–305A (1983).

    Google Scholar 

  9. 9.

    Schulze, E.-D. Air pollution and forest decline in a spruce (Picea abies) forest. Science 244, 776–783 (1989).

    Google Scholar 

  10. 10.

    Driscoll, C. T. et al. Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects and management strategies. BioScience 51, 180–198 (2001).

    Google Scholar 

  11. 11.

    Mitchell, M. J. & Likens, G. E. Watershed sulfur biogeochemistry: shift from atmospheric deposition dominance to climatic regulation. Environ. Sci. Technol. 45, 5267–5271 (2011).

    Google Scholar 

  12. 12.

    EPA Air Emissions Data (EPA, accessed 14 April 2020); https://go.nature.com/3fiYt3p

  13. 13.

    Klimont, Z., Smith, S. J. & Cofala, J. The last decade of global anthropogenic sulfur dioxide: 2000–2011 emissions. Environ. Res. Lett. 8, 014003 (2013).

    Google Scholar 

  14. 14.

    Learn More About Sulphur (The Sulphur Institute, 2020); https://go.nature.com/32OHX87

  15. 15.

    China Statistical Yearbook 2017 (National Bureau of Statistics of China, accessed 1 March 2019); https://go.nature.com/2E7z6E2

  16. 16.

    Thompson, J. F. Sulfur metabolism in plants. Annu. Rev. Plant Physiol. 18, 59–84 (1967).

    Google Scholar 

  17. 17.

    Anderson, J. W. in The Biochemistry of Plants Vol. 16 (ed. Miflin, B. J.) 327–381 (Academic Press, 1990).

  18. 18.

    Canfield, D. E. & Raiswell, R. The evolution of the sulfur cycle. Am. J. Sci. 299, 697–723 (1999).

    Google Scholar 

  19. 19.

    Jackson, G. D. Effects of nitrogen and sulfur on canola yield and nutrient uptake. Agron. J. 92, 644–649 (2000).

    Google Scholar 

  20. 20.

    Ma, B.-L. et al. Growth, yield, and yield components of canola as affected by nitrogen, sulfur, and boron application. J. Plant Nutr. Soil Sci. 178, 658–670 (2015).

    Google Scholar 

  21. 21.

    Clark, N., Orloff, S. & Ottman, M. Fertilizing high yielding alfalfa in California and Arizona. Better Crops with Plant Food 101, 21–23 (2017).

    Google Scholar 

  22. 22.

    Haneklaus, S., Bloem, E., Schnug, E., de Kok, L. J. & Stulen, I. in Handbook of Plant Nutrition (eds Barker, A. V. & Pilbeam, D. J.) Ch. 7 (CRC Press, 2006).

  23. 23.

    Chien, S. H. et al. Agronomic effectiveness of granular nitrogen/phosphorus fertilizers containing elemental sulfur with and without ammonium sulfate: a review. Agron. J. 108, 1203–1213 (2016).

    Google Scholar 

  24. 24.

    Dick, W. A., Kost, D. & Chen, L. in Sulfur: A Missing Link Between Soils, Crops, and Nutrition (ed. Jez, J.) Ch. 5 (ASA, CSSA, SSSA, 2008).

  25. 25.

    Schnug, E. & Evans, E. J. Monitoring of the sulfur supply of agricultural crops in northern Europe. Phyton 32, 119–122 (1992).

    Google Scholar 

  26. 26.

    Gaspar, A. P., Laboski, C. A. M., Naeve, S. L. & Conley, S. P. Secondary and micronutrient uptake, partitioning, and removal across a wide range of soybean seed yield levels. Agron. J. 110, 1328–1338 (2008).

    Google Scholar 

  27. 27.

    Fernández, F. G., Ebelhar, S., Greer, K. & Brown, H. Corn response to sulfur in Illinois FREC 2011 Report (FREC, 2012); https://go.nature.com/32PDORh

  28. 28.

    Steinke, K., Rutan, J. & Thurgood, L. Corn response to nitrogen at multiple sulfur rates. Agron. J. 107, 1347–1354 (2015).

    Google Scholar 

  29. 29.

    Sutradhar, A. K., Kaiser, D. E. & Fernández, F. G. Does total nitrogen/sulfur ratio predict nitrogen or sulfur requirement for corn? Soil Sci. Soc. Am. J. 81, 564–577 (2017).

    Google Scholar 

  30. 30.

    Kurbondski, A. J., Kaiser, D. E., Rosen, C. J. & Sutradhar, A. K. Does irrigated corn require multiple applications of sulfur? Soil Sci. Soc. Am. J. 83, 1124–1136 (2019).

    Google Scholar 

  31. 31.

    Ketterings, Q. M. et al. Soil and tissue testing for sulfur management of alfalfa in New York State. Soil Sci. Soc. Am. J. 76, 298–306 (2012).

    Google Scholar 

  32. 32.

    Haupt, G., Lauzon, J. & Hall, B. Sulfur fertilization: improving alfalfa yield and quality. Crops Soils 48, 26–30 (2015).

    Google Scholar 

  33. 33.

    Data and Statistics (USDA NASS, accessed 20 May 2019); https://go.nature.com/3hxxAcK

  34. 34.

    California Pesticide Information Portal (CalPIP) (California Department of Pesticide Regulation, accessed 20 May 2019); https://calpip.cdpr.ca.gov/main.cfm

  35. 35.

    Orem, W. et al. Sulfur in the South Florida ecosystem: distribution, sources, biogeochemistry, impacts, and management for restoration. Crit. Rev. Environ. Sci. Technol. 41, 249–288 (2011).

    Google Scholar 

  36. 36.

    Gabriel, M., Redfield, G. & Rumbold, D. Sulfur as a regional water quality concern in South Florida 2008 South Florida Environmental Report, Appendix 3B-2 (South Florida Water Management District, 2008).

  37. 37.

    Shainberg, I. et al. in Advances in Soil Science (ed. Stewart, B. A.) 1–111 (Springer, 1989).

  38. 38.

    DeSutter, T. M. & Cihacek, L. J. Potential agricultural uses of flue gas desulfurization gypsum in the Northern Great Plains. Agron. J. 101, 817–825 (2009).

    Google Scholar 

  39. 39.

    Ritchey, K. D., Feldhake, C. M., Clark, R. B. & de Sousa, D. M. G. in Agricultural Utilization of Urban and Industrial By-Products Vol. 58 (eds Karlen, D. L. et al.) Ch. 8 (ASA, CSSA, SSSA, 1995).

  40. 40.

    Driscoll, C. T., Driscoll, K. M., Fakhraei, H. & Civerolo, K. Long-term temporal trends and spatial patterns in the acid-base chemistry of lakes in the Adirondack region of New York in response to decreases in acidic deposition. Atmos. Environ. 146, 5–14 (2016).

    Google Scholar 

  41. 41.

    Rice, K. C., Scanlon, T. M., Lynch, J. A. & Cosby, B. J. Decreased atmospheric sulfur deposition across the southeastern U.S.: when will watersheds release stored sulfate. Environ. Sci. Technol. 48, 10071–10078 (2014).

    Google Scholar 

  42. 42.

    Beaton, J. D. Sulfur requirements of cereals, tree fruits, vegetables, and other crops. Soil Sci. 101, 267–282 (1966).

    Google Scholar 

  43. 43.

    Rehm, G. W. & Clapp, J. G. in Sulfur: A Missing Link between Soils, Crops, and Nutrition (ed. Jez, J.) Ch. 9 (ASA, CSSA, SSSA, 2008).

  44. 44.

    Kaiser, D. E. & Kim, K.-I. Soybean response to sulfur fertilizer applied as a broadcast or starter using replicated strip trials. Agron. J. 105, 1189–1198 (2013).

    Google Scholar 

  45. 45.

    David, M. B., Gentry, L. E. & Mitchell, C. A. Riverine response of sulfate to declining atmospheric sulfur deposition in agricultural watersheds. J. Environ. Qual. 45, 1313–1319 (2016).

    Google Scholar 

  46. 46.

    Wine (Agricultural Marketing Resource Center, 2019); https://go.nature.com/2WO6eHl

  47. 47.

    Hinckley, E. L. S. & Matson, P. A. Transformations, transport, and potential unintended consequences of high sulfur inputs to Napa Valley vineyards. Proc. Natl Acad. Sci. USA 108, 14005–14010 (2011).

    Google Scholar 

  48. 48.

    Williams, J. S. & Cooper, R. M. The oldest fungicide and newest phytoalexin – a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathol. 53, 263–279 (2004).

    Google Scholar 

  49. 49.

    Grape Acreage Reports Listing (USDA National Agricultural Statistics Service, accessed 21 May 2019); https://go.nature.com/38pHlXb

  50. 50.

    US Drought Portal (NIDIS, accessed 21 May 2019); https://go.nature.com/39pyo0w

  51. 51.

    Rice, R. W., Gilbert, R. A. & McCray, J. M. Nutritional requirements for Florida sugarcane Sugarcane Cultural Practices (Sugarcane Handbook), UF-IFAS Extension SS-AGR-228 (Univ. of Florida, 2006).

  52. 52.

    McCray, J. M. Elemental sulfur recommendations for sugarcane on Florida organic soils Sugarcane Cultural Practices (Sugarcane Handbook), UF-IFAS Extension SS-AGR-429 (Univ. of Florida, 2019); http://edis.ifas.ufl.edu/ag429

  53. 53.

    National Research Council Progress Toward Restoring the Everglades: The Fifth Biennial Review: 2014 (The National Academies Press, 2014).

  54. 54.

    Schueneman, T. J. Characterization of sulfur sources in the EAA. Annu. Proc. Soil Crop Sci. Soc. Florida 60, 49–52 (2001).

    Google Scholar 

  55. 55.

    Lanning, M. et al. Intensified vegetation water use under acid deposition. Sci. Adv. 5, eaav5168 (2019).

    Google Scholar 

  56. 56.

    Lu, X. et al. Plant acclimation to long-term high nitrogen deposition in an N-rich tropical forest. Proc. Natl Acad. Sci. USA 115, 5187–5192 (2018).

    Google Scholar 

  57. 57.

    Podar, M. et al. Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci. Adv. 1, e1500675 (2015).

    Google Scholar 

  58. 58.

    Driscoll, C. T., Mason, R. P., Chan, H. M., Jacob, D. J. & Pirrone, N. Mercury as a global pollutant: Sources, pathways, and effects. Environ. Sci. Technol. 47, 4967–4983 (2013).

    Google Scholar 

  59. 59.

    Schmeltz, D. et al. MercNet: a national monitoring network to assess responses to changing mercury emissions in the United States. Ecotoxicology 20, 1713–1725 (2011).

    Google Scholar 

  60. 60.

    US Environmental Protection Agency 2011 National Listing of Fisheries Advisories EPA-820-F-13-058 (EPA, 2013).

  61. 61.

    Gilmour, C. C. et al. Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades. Biogeochemistry 40, 327–345 (1998).

    Google Scholar 

  62. 62.

    Bailey, L. T. et al. Influence of porewater sulfide on methylmercury production and partitioning in sulfate-impacted lake sediments. Sci. Total Environ. 580, 1197–1204 (2017).

    Google Scholar 

  63. 63.

    Wasik, J. K. C. et al. The effects of hydrologic fluctuation and sulfate regeneration on mercury cycling in an experimental peatland. J. Geophys. Res. Biogeosciences 120, 1697–1715 (2015).

    Google Scholar 

  64. 64.

    Benoit, J. M. et al. in Biogeochemistry of Environmentally Important Trace Elements (eds Cai, Y. & Braids, O. C.) 262–297 (ACS, 2002).

  65. 65.

    Chen, C. Y., Driscoll, C. T. & Kamman, N. C. in Mercury in the Environment: Pattern and Process (ed. Bank, M.) 143–166 (Univ. of California Press, 2012).

  66. 66.

    Robinson, A., Richey, A., Slotton, D., Collins, J. & Davis, J. North Bay Mercury Biosentinel Project 2016–2017 Contribution # 868 (San Francisco Estuary Institute, Aquatic Science Center, 2018).

  67. 67.

    Marvin-DiPasquale, M., Agee, J. L., Bouse, R. M. & Jaffe, B. E. Microbial cycling of mercury in contaminated pelagic and wetland sediments of San Pablo Bay, California. Environ. Geol. 43, 260–267 (2003).

    Google Scholar 

  68. 68.

    Wiener, J. G., Evers, D. C., Gay, D. A., Morrison, H. A. & Williams, K. A. Mercury contamination in the Laurentian Great Lakes region: introduction and overview. Environ. Pollut. 161, 243–251 (2012).

    Google Scholar 

  69. 69.

    Smolders, A. J. P., Lamers, L. P. M., Lucassen, E. C. H. E. T., Van Dervelde, G. & Roelofs, J. G. M. Internal eutrophication: how it works and what to do about it–a review. Chem. Ecol. 22, 93–111 (2006).

    Google Scholar 

  70. 70.

    Caraco, N. F., Cole, J. J. & Likens, G. E. Evidence for sulphate-controlled phosphorus release from sediments of aquatic systems. Nature 341, 316–318 (1989).

    Google Scholar 

  71. 71.

    Smolders, A. J. P., Lucassen, E. C. H. E. T., Bobbink, R., Roelofs, J. G. M. & Lamers, L. P. M. How nitrate leaching from agricultural lands provokes phosphate eutrophication in groundwater fed wetlands: the sulphur bridge. Biogeochemistry 98, 1–7 (2010).

    Google Scholar 

  72. 72.

    van der Welle, M. E. W., Roelofs, J. G. M. & Lamers, L. P. M. Multi-level effects of sulphur–iron interactions in freshwater wetlands in The Netherlands. Sci. Total Environ. 406, 426–429 (2008).

    Google Scholar 

  73. 73.

    De Kok, L. J., Durenkamp, M., Yang, L. & Stulen, I. in Sulfur in Plants, An Ecological Perspective (eds Hawkesford, M. J. & De Kok, L. J.) Ch. 5 (Springer, 2007).

  74. 74.

    Lamers, L. P. M. et al. Sulfide as a soil phytotoxin—a review. Front. Plant Sci. 4, 268 (2013).

    Google Scholar 

  75. 75.

    Koch, M. S., Mendelssohn, I. A. & McKee, K. L. Mechanism for the hydrogen sulfide‐induced growth limitation in wetland macrophytes. Limnol. Oceanogr. 35, 399–408 (1990).

    Google Scholar 

  76. 76.

    Gao, S., Tanji, K. K. & Scardaci, S. C. Impact of rice straw incorporation on soil redox status and sulfide toxicity. Agron. J. 96, 70–76 (2004).

    Google Scholar 

  77. 77.

    Lamers, L. P. M., Tomassen, H. B. M. & Roelofs, J. G. M. Sulfate-induced eutrophication and phytotoxicity in freshwater wetlands. Environ. Sci. Technol. 32, 199–205 (1998).

    Google Scholar 

  78. 78.

    Li, S., Mendelssohn, I. A., Chen, H. & Orem, W. H. Does sulphate enrichment promote the expansion of Typha domingensis (cattail) in the Florida Everglades? Freshw. Biol. 54, 1909–1923 (2009).

    Google Scholar 

  79. 79.

    Ye, M., Beach, J., Martin, J. & Senthilselvan, A. Occupational pesticide exposures and respiratory health. Int. J. Environ. Res. Public Health 10, 6442–6471 (2013).

    Google Scholar 

  80. 80.

    Hoppin, J. A., Umbach, D. M., London, S. J., Alavanja, M. C. R. & Sandler, D. P. Chemical predictors of wheeze among farmer pesticide applicators in the Agricultural Health Study. Am. J. Respir. Crit. Care Med. 165, 683–689 (2002).

    Google Scholar 

  81. 81.

    Degryse, F., Ajiboye, B., Baird, R., da Silva, R. C. & McLaughlin, M. J. Oxidation of elemental sulfur in granular fertilizers depends on the soil-exposed surface area. Soil Sci. Soc. Am. J. 80, 294–305 (2016).

    Google Scholar 

  82. 82.

    Guo, J. H. et al. Significant acidification in major Chinese croplands. Science 327, 1008–1010 (2010).

    Google Scholar 

  83. 83.

    Clark, M. & Tilman, D. Comparative analysis of environmental impacts of agricultural production systems, agricultural input efficiency, and food choice. Environ. Res. Lett. 12, 064016 (2017).

    Google Scholar 

  84. 84.

    Galloway, J. N. et al. The nitrogen cascade. BioScience 53, 341–356 (2003).

    Google Scholar 

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Development of this Perspective was supported by a National Geographic Society Expand the Field Grant and a National Science Foundation CAREER Award (NSF EAR no. 1945388) to E.-L.S.H. and the Hubbard Brook Long-term Ecological Research Program supported by the National Science Foundation to C.T.D. (NSF DEB no. 33401200201861).

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E.-L.S.H. and C.T.D. designed and wrote the paper, and interpreted modelling simulations. J.T.C. and H.F. conducted the modelling simulations and contributed to the Supplementary Information.

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Correspondence to Eve-Lyn S. Hinckley.

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Hinckley, E.S., Crawford, J.T., Fakhraei, H. et al. A shift in sulfur-cycle manipulation from atmospheric emissions to agricultural additions. Nat. Geosci. 13, 597–604 (2020). https://doi.org/10.1038/s41561-020-0620-3

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