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.
Subscribe to Journal
Get full journal access for 1 year
only $14.08 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.
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 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.
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).
Galloway, J. N. Anthropogenic mobilization of sulphur and nitrogen: immediate and delayed consequences. Annu. Rev. Energy Env. 21, 261–292 (1996).
Cowling, E. B. Acid precipitation in historical perspective. Environ. Sci. Technol. 16, 110A–123A (1982).
Gorham, E. On the acidity and salinity of rain. Geochim. Cosmochim. Acta 7, 231–239 (1955).
Likens, G. E. & Bormann, F. H. Acid rain: a serious regional environmental problem. Science 184, 1176–1179 (1974).
Goyer, R. A. et al. Potential human health effects of acid rain: report of a workshop. Environ. Health Perspect. 60, 355–368 (1985).
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).
Johnson, A. H. & Siccama, T. G. Acid deposition and forest decline. Environ. Sci. Technol. 17, 294A–305A (1983).
Schulze, E.-D. Air pollution and forest decline in a spruce (Picea abies) forest. Science 244, 776–783 (1989).
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).
Mitchell, M. J. & Likens, G. E. Watershed sulfur biogeochemistry: shift from atmospheric deposition dominance to climatic regulation. Environ. Sci. Technol. 45, 5267–5271 (2011).
EPA Air Emissions Data (EPA, accessed 14 April 2020); https://go.nature.com/3fiYt3p
Klimont, Z., Smith, S. J. & Cofala, J. The last decade of global anthropogenic sulfur dioxide: 2000–2011 emissions. Environ. Res. Lett. 8, 014003 (2013).
Learn More About Sulphur (The Sulphur Institute, 2020); https://go.nature.com/32OHX87
China Statistical Yearbook 2017 (National Bureau of Statistics of China, accessed 1 March 2019); https://go.nature.com/2E7z6E2
Thompson, J. F. Sulfur metabolism in plants. Annu. Rev. Plant Physiol. 18, 59–84 (1967).
Anderson, J. W. in The Biochemistry of Plants Vol. 16 (ed. Miflin, B. J.) 327–381 (Academic Press, 1990).
Canfield, D. E. & Raiswell, R. The evolution of the sulfur cycle. Am. J. Sci. 299, 697–723 (1999).
Jackson, G. D. Effects of nitrogen and sulfur on canola yield and nutrient uptake. Agron. J. 92, 644–649 (2000).
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).
Clark, N., Orloff, S. & Ottman, M. Fertilizing high yielding alfalfa in California and Arizona. Better Crops with Plant Food 101, 21–23 (2017).
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).
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).
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).
Schnug, E. & Evans, E. J. Monitoring of the sulfur supply of agricultural crops in northern Europe. Phyton 32, 119–122 (1992).
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).
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
Steinke, K., Rutan, J. & Thurgood, L. Corn response to nitrogen at multiple sulfur rates. Agron. J. 107, 1347–1354 (2015).
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).
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).
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).
Haupt, G., Lauzon, J. & Hall, B. Sulfur fertilization: improving alfalfa yield and quality. Crops Soils 48, 26–30 (2015).
Data and Statistics (USDA NASS, accessed 20 May 2019); https://go.nature.com/3hxxAcK
California Pesticide Information Portal (CalPIP) (California Department of Pesticide Regulation, accessed 20 May 2019); https://calpip.cdpr.ca.gov/main.cfm
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).
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).
Shainberg, I. et al. in Advances in Soil Science (ed. Stewart, B. A.) 1–111 (Springer, 1989).
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).
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).
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).
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).
Beaton, J. D. Sulfur requirements of cereals, tree fruits, vegetables, and other crops. Soil Sci. 101, 267–282 (1966).
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).
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).
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).
Wine (Agricultural Marketing Resource Center, 2019); https://go.nature.com/2WO6eHl
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).
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).
Grape Acreage Reports Listing (USDA National Agricultural Statistics Service, accessed 21 May 2019); https://go.nature.com/38pHlXb
US Drought Portal (NIDIS, accessed 21 May 2019); https://go.nature.com/39pyo0w
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).
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
National Research Council Progress Toward Restoring the Everglades: The Fifth Biennial Review: 2014 (The National Academies Press, 2014).
Schueneman, T. J. Characterization of sulfur sources in the EAA. Annu. Proc. Soil Crop Sci. Soc. Florida 60, 49–52 (2001).
Lanning, M. et al. Intensified vegetation water use under acid deposition. Sci. Adv. 5, eaav5168 (2019).
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).
Podar, M. et al. Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci. Adv. 1, e1500675 (2015).
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).
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).
US Environmental Protection Agency 2011 National Listing of Fisheries Advisories EPA-820-F-13-058 (EPA, 2013).
Gilmour, C. C. et al. Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades. Biogeochemistry 40, 327–345 (1998).
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).
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).
Benoit, J. M. et al. in Biogeochemistry of Environmentally Important Trace Elements (eds Cai, Y. & Braids, O. C.) 262–297 (ACS, 2002).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Lamers, L. P. M. et al. Sulfide as a soil phytotoxin—a review. Front. Plant Sci. 4, 268 (2013).
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).
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).
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).
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).
Ye, M., Beach, J., Martin, J. & Senthilselvan, A. Occupational pesticide exposures and respiratory health. Int. J. Environ. Res. Public Health 10, 6442–6471 (2013).
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).
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).
Guo, J. H. et al. Significant acidification in major Chinese croplands. Science 327, 1008–1010 (2010).
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).
Galloway, J. N. et al. The nitrogen cascade. BioScience 53, 341–356 (2003).
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).
The authors declare no competing interests.
Peer review information Primary Handling Editor: Rebecca Neely.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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
Fates and fingerprints of sulfur and carbon following wildfire in economically important croplands of California, U.S.
Science of The Total Environment (2021)