Abstract
Indirect emission of nitrous oxide (N2O) through groundwater and surface drainage is commonly estimated based on the apparent positive relationship between the concentrations of nitrate ([NO3 −]) and dissolved N2O ([N2O]) for regional and national assessments. Field observations of the ratio of [N2O]–[NO3 −], however, rarely follow such relationship due to the complexity in N2O dynamics. Here we hypothesized that the temporal variation in [N2O] involves a phase shift as a function of [NO3 −] during heterotrophic denitrification (HD) based on the fact that high [NO3 −] inhibits N2O reduction to dinitrogen. We tested this hypothesis using the long-term, high frequency dataset of subsurface drainage water from the lysimeters under a cultivated soil in Japan. We identified the cases where [N2O] increased under high [NO3 −] conditions (phase 1) and decreased under low [NO3 −] conditions (phase 2) during the non-rainy periods. When [NO3 −] exceeded 20.4 mg N L−1 across the entire dataset, we found the positive correlation between [N2O] and the concentration of dissolved carbon dioxide ([CO2]), an end-product of HD, in accordance with phase 1. When [NO3 −] was <5 mg N L−1 and [CO2] was >28.3 mg C L−1, we found the positive correlation between [N2O] and [NO3 −], which agrees with phase 2. With this phase shift, [N2O]–[NO3 −] ratio increased (phase 1) and reached a plateau (phase 2). Our results suggest that the progress of HD, especially phase 1, contributes to the increases in [N2O]–[NO3 −] ratio and thus site-specific emission factor of N2O, EF5g.
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References
Blackmer AM, Bremner JM (1978) Inhibitory effect of nitrate on reduction of N2O to N2 by soil microorganisms. Soil Biol Biochem 10:187–191
Deurer M, von der Heide C, Böttcher J, Duijnisveld WHM, Weymann D, Well R (2008) The dynamics of N2O near the groundwater table and the transfer of N2O into the unsaturated zone: a case study from a sandy aquifer in Germany. Catena 72:362–373
Firestone MK, Firestone RB, Tiedje JM (1980) Nitrous oxide from soil denitrification—factors controlling its biological production. Science 208:749–751
Groffman PM, Howard G, Gold AJ, Nelson WM (1996) Microbial nitrate processing in shallow groundwater in a riparian forest. J Environ Qual 25:1309–1316
Grøn C, Tørsløv J, Albrechtsen HJ, Jensen HM (1992) Biodegradability of dissolved organic carbon in groundwater from an unconfined aquifer. Sci Total Environ 117:241–251
Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45
Hedin LO, von Fischer JC, Ostrom NE, Kennedy BP, Brown MG, Robertson GP (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79:684–703
Hill AR, Devito KJ, Campagnolo S, Sanmugadas K (2000) Subsurface denitrification in a forest riparian zone: interactions between hydrology and supplies of nitrate and organic carbon. Biogeochemistry 51:193–223
IPCC (2006) N2O emissions from managed soils, and CO2 emissions from lime and urea application. In: Eggleston HS, Buendia L, Miwa K, Ngara T, Tanabe K (eds) Agriculture, forestry and other land use: 2006 IPCC guidelines for national greenhouse gas inventories. IGES, Hayama, pp 11.1–11.54
Liu S, Qin Y, Zou J, Liu Q (2010) Effects of water regime during rice-growing season on annual direct N2O emission in a paddy rice–winter wheat rotation system in southeast China. Sci Total Environ 408:906–913
McCarty GW, Bremner JM (1992) Availability of organic carbon for denitrification of nitrate in subsoils. Biol Fertil Soils 14:219–222
Minamikawa K, Nishimura S, Sawamoto T, Nakajima Y, Yagi K (2010) Annual emissions of dissolved CO2, CH4, and N2O in the subsurface drainage from three cropping systems. Glob Change Biol 16:796–809
Minamikawa K, Nishimura S, Nakajima Y, Osaka K, Sawamoto T, Yagi K (2011a) Upward diffusion of nitrous oxide produced by denitrification near shallow groundwater table in the summer: a lysimeter experiment. Soil Sci Plant Nutr 57:719–732
Minamikawa K, Hayakawa A, Nishimura S, Akiyama H, Yagi K (2011b) Comparison of indirect nitrous oxide emission through lysimeter drainage between an Andosol upland field and a Fluvisol paddy field. Soil Sci Plant Nutr 57:843–854
Mosier AR, Kroeze C, Nevison C, Oenema O, Seitzinger S, van Cleemput O (1998) Closing the global N2O budget: nitrous oxide emissions through the agricultural nitrogen cycle: OECD/IPCC/IEA phase II development of IPCC guidelines for national greenhouse gas inventory methodology. Nutr Cycl Agroecosyst 52:225–248
Mühlherr IH, Hiscock KM (1998) Nitrous oxide production and consumption in British limestone aquifers. J Hydrol 211:126–139
Muñoz-Leoz B, Antigüedad I, Garbisu C, Ruiz-Romera E (2011) Nitrogen transformations and greenhouse gas emissions from a riparian wetland soil: an undisturbed soil column study. Sci Total Environ 409:763–770
Myhre G, Shindell D, Bréon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 714
Nishimura S, Akiyama H, Sudo S, Fumoto T, Cheng W, Yagi K (2011) Combined emission of CH4 and N2O from a paddy field was reduced by preceding upland crop cultivation. Soil Sci Plant Nutr 57:167–178
Obenhuber DC, Lowrance R (1991) Reduction of nitrate in aquifer microcosms by carbon additions. J Environ Qual 20:255–258
Qualls RG, Haines BL (1992) Biodegradability of dissolved organic matter in forest throughfall, soil solution, and stream water. Soil Sci Soc Am J 56:578–586
Reay DS, Edwards AC, Smith KA (2009) Importance of indirect nitrous oxide emissions at the field, farm and catchment scale. Agric Ecosyst Environ 133:163–169
Sawamoto T, Nakajima Y, Kasuya M, Tsuruta H, Yagi K (2005) Evaluation of emission factors for indirect N2O emission due to nitrogen leaching in agro-ecosystems. Geophys Res Lett 32:L03403
Senbayram M, Chen R, Budai A, Bakken L, Dittert K (2012) N2O emission and the N2O/(N2O + N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations. Agric Ecosyst Environ 147:4–12
Smith P, Martino D, Cai Z et al (2007) Agriculture. In: Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA (eds) Climate change 2007: mitigation contribution of working group III to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 498–540
Spalding RF, Gormly JR, Nash KG (1978) Carbon contents and sources in ground waters of the central Platte region in Nebraska. J Environ Qual 7:428–434
Taylor PG, Townsend AR (2010) Stoichiometric control of organic carbon-nitrate relationships from soils to the sea. Nature 464:1178–1181
United Nations Framework Convention on Climate Change (2012) Greenhouse gas inventory data. http://unfccc.int/ghg_data/items/3800.php. Accessed 1 Jan 2013
Vilain G, Garnier J, Tallec G, Tournebize J (2012) Indirect N2O emissions from shallow groundwater in an agricultural catchment (Seine Basin, France). Biogeochemistry 111:253–271
Von der Heide C, Böttcher J, Deurer M, Weymann D, Well R, Duijnisveld WHM (2008) Spatial variability of N2O concentrations and of denitrification-related factors in the surficial groundwater of a catchment in Northern Germany. J Hydrol 360:230–241
Wagai R, Sollins P (2002) Biodegradation and regeneration of water-soluble carbon in a forest soil: leaching column study. Biol Fertil Soils 35:18–26
Weier KL, Doran JW, Power JF, Walters DT (1993) Denitrification and the dinitrogen nitrous oxide ratio as affected by soil water, available carbon and nitrate. Soil Sci Soc Am J 57:67–72
Weymann D, Well R, Flessa H, von der Heide C, Deurer M, Meyer K, Konrad C, Walther W (2008) Groundwater N2O emission factors of nitrate-contaminated aquifers as derived from denitrification progress and N2O accumulation. Biogeosciences 5:1215–1226
Zhou S, Sakiyama Y, Riya S, Song X, Terada A, Hosomi M (2012) Assessing nitrification and denitrification in a paddy soil with different water dynamics and applied liquid cattle waste using the 15N isotopic technique. Sci Total Environ 430:93–100
Zhu X, Burger M, Doane TA, Horwath WR (2013) Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc Natl Acad Sci USA 110:6328–6333
Acknowledgments
We would like to thank Drs. Shigeto Sudo and Hiroko Akiyama (NIAES, Japan) for their help using the gas analysis system. We also would like to thank Dr. Syuntaro Hiradate (NIAES, Japan) for his valuable comments on the bioavailability of DOC. A portion of this study was funded by the Japan Society for the Promotion of Science (JSPS) through the Grant-in-Aid for JSPS Fellows (20-361).
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Minamikawa, K., Wagai, R., Nishimura, S. et al. Heterotrophic denitrification constrains the upper limit of dissolved N2O-nitrate concentration ratio in agricultural groundwater. Nutr Cycl Agroecosyst 101, 181–191 (2015). https://doi.org/10.1007/s10705-014-9668-z
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DOI: https://doi.org/10.1007/s10705-014-9668-z