Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Hotspots of soil N2O emission enhanced through water absorption by plant residue

Nature Geoscience volume 10, pages 496–500 (2017)Cite this article

Subjects

Abstract

N2O is a highly potent greenhouse gas and arable soils represent its major anthropogenic source. Field-scale assessments and predictions of soil N2O emission remain uncertain and imprecise due to the episodic and microscale nature of microbial N2O production, most of which occurs within very small discrete soil volumes. Such hotspots of N2O production are often associated with decomposing plant residue. Here we quantify physical and hydrological soil characteristics that lead to strikingly accelerated N2O emissions in plant residue-induced hotspots. Results reveal a mechanism for microscale N2O emissions: water absorption by plant residue that creates unique micro-environmental conditions, markedly different from those of the bulk soil. Moisture levels within plant residue exceeded those of bulk soil by 4–10-fold and led to accelerated N2O production via microbial denitrification. The presence of large (Ø >35 μm) pores was a prerequisite for maximized hotspot N2O production and for subsequent diffusion to the atmosphere. Understanding and modelling hotspot microscale physical and hydrologic characteristics is a promising route to predict N2O emissions and thus to develop effective mitigation strategies and estimate global fluxes in a changing environment.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Gravimetric moisture content of corn and soybean leaves used in the incubations.
Figure 2: Decomposition of added plant residue.
Figure 3: Cumulative N2O emitted during 110 days (bars) and proportion of N2O generated by denitrification during 7 days of incubation (boxes).
Figure 4: Relative changes in O2 during the first 4 days of soil microcosm incubations.
Figure 5: Differences in N2O emission rates between soil microcosms with plant residues and control soil during 1–14 days of incubation.

Similar content being viewed by others

References

  1. Groffman, P. M. et al. Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93, 49–77 (2009).

    Article  Google Scholar 

  2. McClain, M. E. et al. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6, 301–312 (2003).

    Article  Google Scholar 

  3. Chen, H. H., Li, X. C., Hu, F. & Shi, W. Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Glob. Change Biol. 19, 2956–2964 (2013).

    Article  Google Scholar 

  4. Li, X. X., Petersen, S. O., Sorensen, P. & Olesen, J. E. Effects of contrasting catch crops on nitrogen availability and nitrous oxide emissions in an organic cropping system. Agric. Ecosyst. Environ. 199, 382–393 (2015).

    Article  Google Scholar 

  5. Petersen, S. O., Mutegi, J. K., Hansen, E. M. & Munkholm, L. J. Tillage effects on N2O emissions as influenced by a winter cover crop. Soil Biol. Biochem. 43, 1509–1517 (2011).

    Article  Google Scholar 

  6. Sanz-Cobena, A. et al. Do cover crops enhance N2O, CO2 or CH4 emissions from soil in Mediterranean arable systems? Sci. Tot. Environ. 466, 164–174 (2014).

    Article  Google Scholar 

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

    Article  Google Scholar 

  8. Gelfand, I., Shcherbak, I. I., Millar, N., Kravchenko, A. N. & Robertson, G. P. Long-term nitrous oxide fluxes in annual and perennial agricultural and unmanaged ecosystems in the upper Midwest USA. Glob. Change Biol. 22, 3594–3607 (2016).

    Article  Google Scholar 

  9. 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? Phil. Trans. R. Soc. B 368, 1621 (2013).

    Article  Google Scholar 

  10. Ciais, P. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (IPCC, Cambridge Univ. Press, 2013).

    Google Scholar 

  11. Forster, P. in Climate Change 2007: The Physical Science Basis (ed. Solomon, S.) (IPCC, Cambridge Univ. Press, 2007).

    Google Scholar 

  12. Kravchenko, A. N. & Robertson, G. P. Statistical challenges in analyses of chamber-based soil CO2 and N2O emissions data. Soil Sci. Soc. Am. J. 79, 200–211 (2015).

    Article  Google Scholar 

  13. Ambus, P. & Robertson, G. P. Automated near-continuous measurement of carbon dioxide and nitrous oxide fluxes from soil. Soil Sci. Soc. Am. J. 62, 394–400 (1998).

    Article  Google Scholar 

  14. Barton, L. et al. Sampling frequency affects estimates of annual nitrous oxide fluxes. Sci. Rep. 5, 15912 (2015).

    Article  Google Scholar 

  15. Ruan, L. L. & Robertson, G. P. Initial nitrous oxide, carbon dioxide, and methane costs of converting conservation reserve program grassland to row crops under no-till vs. conventional tillage. Glob. Change Biol. 19, 2478–2489 (2013).

    Article  Google Scholar 

  16. Kuzyakov, Y. & Blagodatskaya, E. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199 (2015).

    Article  Google Scholar 

  17. Ambus, P. & Christensen, S. Measurement of N2O emission from a fertilized grassland - an analysis of spatial variability. J. Geophys. Res. 99, 16549–16555 (1994).

    Article  Google Scholar 

  18. Haider, K., Mosier, A. & Heinemeyer, O. The effect of growing plants on denitrification at high soil nitrate concentrations. Soil Sci. Soc. Am. J. 51, 97–102 (1987).

    Article  Google Scholar 

  19. Parkin, T. B. Soil microsites as a source of denitrification variability. Soil Sci. Soc. Am. J. 51, 1194–1199 (1987).

    Article  Google Scholar 

  20. Sexstone, A. J., Revsbech, N. P., Parkin, T. B. & Tiedje, J. M. Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci. Soc. Am. J. 49, 645–651 (1985).

    Article  Google Scholar 

  21. Ball, B. C. Soil structure and greenhouse gas emissions: a synthesis of 20 years of experimentation. Eur. J. Soil Sci. 64, 357–373 (2013).

    Article  Google Scholar 

  22. Jungkunst, H. F., Freibauer, A., Neufeldt, H. & Bareth, G. Nitrous oxide emissions from agricultural land use in Germany—a synthesis of available annual field data. J. Plant Nutr. Soil Sci. 169, 341–351 (2006).

    Article  Google Scholar 

  23. Clemens, J., Schillinger, M. P., Goldbach, H. & Huwe, B. Spatial variability of N2O emissions and soil parameters of an arable silt loam—a field study. Biol. Fert. Soils 28, 403–406 (1999).

    Article  Google Scholar 

  24. Kravchenko, A. N. et al. Intra-aggregate pore structure influences phylogenetic composition of bacterial community in macroaggregates. Soil Sci. Soc. Am. J. 78, 1924–1939 (2014).

    Article  Google Scholar 

  25. Negassa, W. et al. Properties of soil pore space regulate pathways of plant residue decomposition and community structure of associated bacteria. PLoS ONE 10, e0123999 (2015).

    Article  Google Scholar 

  26. Wang, W., Kravchenko, A. N., Smucker, A. J. M., Liang, W. & Rivers, M. L. Intra-aggregate pore characteristics: X-ray computed microtomography analysis. Soil Sci. Soc. Am. J. 76, 1159–1171 (2012).

    Article  Google Scholar 

  27. Ostrom, N. E. & Ostrom, P. H. in The Isotopomers of Nitrous Oxide: Analytical Considerations and Application to Resolution of Microbial Production Pathways (ed. Baskara, M.) 453–476 (Springer, 2011).

    Google Scholar 

  28. Ostrom, N. E. & Ostrom, P. H. Mining the isotopic complexity of nitrous oxide: a review of challenges and opportunities. Biogeochemistry 132, 359–372 (2017).

    Article  Google Scholar 

  29. Breland, T. A. Enhanced mineralization and denitrification as a result of heterogeneous distribution of clover residues in soil. Plant Soil 166, 1–12 (1994).

    Article  Google Scholar 

  30. Loecke, T. D. & Robertson, G. P. Soil resource heterogeneity in terms of litter aggregation promotes nitrous oxide fluxes and slows decomposition. Soil Biol. Biochem. 41, 228–235 (2009).

    Article  Google Scholar 

  31. Magid, J., De Neergaard, A. & Brandt, M. Heterogeneous distribution may substantially decrease initial decomposition, long-term microbial growth and N-immobilization from high C-to-N ratio resources. Eur. J. Soil Sci. 57, 517–529 (2006).

    Article  Google Scholar 

  32. Markfoged, R., Nielsen, L. P., Nyord, T., Ottosen, L. D. M. & Revsbech, N. P. Transient N2O accumulation and emission caused by O2 depletion in soil after liquid manure injection. Eur. J. Soil Sci. 62, 541–550 (2011).

    Article  Google Scholar 

  33. Davidson, E. A., Keller, M., Erickson, H. E., Verchot, L. V. & Veldkamp, E. Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50, 667–680 (2000).

    Article  Google Scholar 

  34. Robertson, G. P. & Tiedje, J. M. Nitrous-oxide sources in aerobic soils—nitrification, denitrification and other biological processes. Soil Biol. Biochem. 19, 187–193 (1987).

    Article  Google Scholar 

  35. Li, X. X., Sorensen, P., Olesen, J. E. & Petersen, S. O. Evidence for denitrification as main source of N2O emission from residue-amended soil. Soil Biol. Biochem. 92, 153–160 (2016).

    Article  Google Scholar 

  36. Ostrom, N. E. et al. Isotopologue data reveal bacterial denitrification as the primary source of N2O during a high flux event following cultivation of a native temperate grassland. Soil Biol. Biochem. 42, 499–506 (2010).

    Article  Google Scholar 

  37. Petersen, S. O., Ambus, P., Elsgaard, L., Schjonning, P. & Olesen, J. E. Long-term effects of cropping system on N2O emission potential. Soil Biol. Biochem. 57, 706–712 (2013).

    Article  Google Scholar 

  38. Zhu, K., Ruun, S., Larsen, M., Glud, R. N. & Jensen, L. S. Heterogeneity of O2 dynamics in soil amended with animal manure and implications for greenhouse gas emissions. Soil Biol. Biochem. 84, 96–106 (2015).

    Article  Google Scholar 

  39. Adu, J. K. & Oades, J. M. Utilization of organic materials in soil aggregates by bacteria and fungi. Soil Biol. Biochem. 10, 117–122 (1978).

    Article  Google Scholar 

  40. Hassink, J. Effects of soil texture and structure on carbon and nitrogen mineralization in grassland soils. Biol. Fert. Soils 14, 126–134 (1992).

    Article  Google Scholar 

  41. Pimentel, L. G., Weiler, D. A., Pedroso, G. M. & Bayer, C. Soil N2O emissions following cover-crop residues application under two soil moisture conditions. J. Plant Nutr. Soil Sci. 178, 631–640 (2015).

    Article  Google Scholar 

  42. Jacinthe, P. A., Groffman, P. M., Gold, A. J. & Mosier, A. Patchiness in microbial nitrogen transformations in groundwater in a riparian forest. J. Environ. Qual. 27, 156–164 (1998).

    Article  Google Scholar 

  43. Jorgensen, B. B. & Revsbech, N. P. Diffusive boundary-layers and the oxygen-uptake of sediments and detritus. Limnol. Oceanogr. 30, 111–122 (1985).

    Article  Google Scholar 

  44. Balaine, N. et al. Changes in relative gas diffusivity explain soil nitrous oxide flux dynamics. Soil. Sci. Soc. Am. J. 77, 1496–1505 (2013).

    Article  Google Scholar 

  45. Clough, T. J., Sherlock, R. R. & Rolston, D. E. A review of the movement and fate of N2O in the subsoil. Nutr. Cycl. Agroecosyst. 72, 3–11 (2005).

    Article  Google Scholar 

  46. Liengaard, L. et al. Hot moments of N2O transformation and emission in tropical soils from the Pantanal and the Amazon (Brazil). Soil Biol. Biochem. 75, 26–36 (2014).

    Article  Google Scholar 

  47. Rabot, E., Henault, C. & Cousin, I. Effect of the soil water dynamics on nitrous oxide emissions. Geoderma 280, 38–46 (2016).

    Article  Google Scholar 

  48. Lal, R. Residue management, conservation tillage and soil restoration for mitigating greenhouse effect by CO2-enrichment. Soil Tillage. Res. 43, 81–107 (1997).

    Article  Google Scholar 

  49. Robertson, G. P. & Hamilton, S. K. in The Ecology of Agricultural Landscapes: Long-Term Research on the Path to Sustainability (eds Hamilton, S. K., Doll, J. E. & Robertson, G. P.) 1–32 (Oxford Univ. Press, 2015).

    Google Scholar 

  50. Senthilkumar, S., Kravchenko, A. N. & Robertson, G. P. Topography influences management system effects on total soil carbon and nitrogen. Soil Sci. Soc. Am. J. 73, 2059–2067 (2009).

    Article  Google Scholar 

  51. Syswerda, S. P., Corbin, A. T., Mokma, D. L., Kravchenko, A. N. & Robertson, G. P. Agricultural management and soil carbon storage in surface vs. deep layers. Soil Sci. Soc. Am. J. 75, 92–101 (2011).

    Article  Google Scholar 

  52. Rivers, M. L., Sutton, S. R. & Eng, P. Geoscience applications of x-ray computed microtomography. Dev. X-Ray Tomogr. II 3772, 78–86 (1999).

    Google Scholar 

  53. Kravchenko, A. N., Negassa, W., Guber, A. K. & Schmidt, S. New approach to measure soil particulate organic matter in intact samples using X-ray computed microtomography. Soil Sci. Soc. Am. J. 78, 1177–1185 (2014).

    Article  Google Scholar 

  54. Oh, W. & Lindquist, W. B. Image thresholding by indicator kriging. IEEE Trans. Pattern Anal. 21, 590–602 (1999).

    Article  Google Scholar 

  55. Wang, W., Kravchenko, A. N., Smucker, A. J. M. & Rivers, M. L. Comparison of image segmentation methods in simulated 2D and 3D microtomographic images of soil aggregates. Geoderma 162, 231–241 (2011).

    Article  Google Scholar 

  56. Lindquist, W. B., Venkatarangan, A., Dunsmuir, J. & Wong, T. F. Pore and throat size distributions measured from synchrotron X-ray tomographic images of Fontainebleau sandstones. J. Geophys. Res. 105, 21509–21527 (2000).

    Article  Google Scholar 

  57. Peth, S. et al. Three-dimensional quantification of intra-aggregate pore-space features using synchrotron-radiation-based microtomography. Soil Sci. Soc. Am. J. 72, 897–907 (2008).

    Article  Google Scholar 

  58. Dutta, T. et al. Vadose zone oxygen (O2) dynamics during drying and wetting cycles: an artificial recharge laboratory experiment. J. Hydrol. 527, 151–159 (2015).

    Article  Google Scholar 

  59. Resurreccion, A. C. et al. Hierarchical, bimodal model for gas diffusivity in aggregated, unsaturated soils. Soil Sci. Soc. Am. J. 74, 481–491 (2010).

    Article  Google Scholar 

  60. Currie, J. A. Gaseous diffusion in porous media .2. Dry granular materials. Br. J. Appl. Phys. 11, 318–324 (1960).

    Article  Google Scholar 

  61. Currie, J. A. Gas-diffusion through soil crumbs—the effects of compaction and wetting. J. Soil Sci. 35, 1–10 (1984).

    Article  Google Scholar 

  62. Sutka, R. L. et al. Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl. Environ. Microb. 72, 638–644 (2006).

    Article  Google Scholar 

  63. Sutka, R. L., Ostrom, N. E., Ostrom, P. H., Gandhi, H. & Breznak, J. A. Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun. Mass Spectrom. 18, 1411–1412 (2004).

    Article  Google Scholar 

  64. Toyoda, S. & Yoshida, N. Determination of nitrogen isotopomers of nitrous oxide on a modified isotope ratio mass spectrometer. Anal. Chem. 71, 4711–4718 (1999).

    Article  Google Scholar 

  65. Milliken, G. A. & Johnson, D. E. Analysis of Messy Data Volume I: Designed Experiments 2nd edn (Chemical Rubber Company, 2009).

    Book  Google Scholar 

  66. Winer, B. J. Statistical principles in Experimental Design (McGraw-Hill, 1971).

    Google Scholar 

Download references

Acknowledgements

We are indebted to K. Kahmark for conducting N2O analyses; to H. Gandhi and J. Haslun for conducting site-preference measurements; and to the KBS LTER team for agronomic management of the field experiment. Funding has been provided by the National Science Foundation’s Long-Term Ecological Research Program (DEB 1027253), by the National Science Foundation’s Geobiology and Low Temperature Geochemistry Program (Award no. 1630399), by the Department of Energy Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494), by Michigan State University’s AgBioResearch (Project GREEEN), and by Michigan State University’s Discretionary Funding Initiative. Portions of this work were performed at GeoSoilEnviroCARS (The University of Chicago, Sector 13), Advanced Photon Source (APS), Argonne National Laboratory. GeoSoilEnviroCARS is supported by the National Science Foundation - Earth Sciences (EAR-1128799) and Department of Energy—GeoSciences (DE-FG02-94ER14466).

Author information

Authors and Affiliations

  1. Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, Michigan, 48824, USA

    A. N. Kravchenko, E. R. Toosi, A. K. Guber & G. P. Robertson

  2. Department of Integrative Biology and DOE Great Lakes Bioenergy Research Institute, Michigan State University, East Lansing, Michigan, 48824, USA

    N. E. Ostrom

  3. Faculty of Resources and Environmental Science, Hubei University, Wuhan, 430052, China

    J. Yu

  4. Department of Agronomy, The University of Agriculture, Peshawar 25130, Khyber Pakhtunkhwa, Pakistan

    K. Azeem

  5. Center for Advanced Radiation Sources, The University of Chicago, Argonne National Lab, Argonne, Illinois, 60439, USA

    M. L. Rivers

  6. W. K. Kellogg Biological Station, Michigan State University, Hickory Corners, Michigan, 49060, USA

    G. P. Robertson

Authors
  1. A. N. Kravchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. R. Toosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. K. Guber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. E. Ostrom
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. Azeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. L. Rivers
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. P. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.N.K. developed concepts, conducted data analyses and wrote the paper. E.R.T. designed, led and conducted the research, and contributed to writing. A.K.G. and N.E.O. contributed to development of research concepts, research conduct and writing. J.Y., K.A. and M.L.R. contributed to research conduct. G.P.R. contributed to the development of research concepts and writing.

Corresponding author

Correspondence to A. N. Kravchenko.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 440 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kravchenko, A., Toosi, E., Guber, A. et al. Hotspots of soil N2O emission enhanced through water absorption by plant residue. Nature Geosci 10, 496–500 (2017). https://doi.org/10.1038/ngeo2963

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo2963

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene