Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T17:24:32.114Z Has data issue: false hasContentIssue false
  • English
  • Français

Using stable isotopes to follow excreta N dynamics and N2O emissions in animal production systems

Published online by Cambridge University Press:  06 June 2013

T. J. Clough ,
C. Müller  and
R. J. Laughlin
T. J. Clough*
Affiliation:
Department of Soil and Physical Sciences, Faculty of Agriculture and Life Sciences, Lincoln University, Lincoln 7647, New Zealand
C. Müller
Affiliation:
Institut für Pflanzenökologie, Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring 26-32 (IFZ), D-35392 Giessen, Germany
R. J. Laughlin
Affiliation:
Agri-Food and Biosciences Institute, Newforge Lane, Belfast, BT9 5PX Northern Ireland, UK
*
†E-mail: [email protected]
Get access

Abstract

Nitrous oxide (N2O) is a potent greenhouse gas and the dominant anthropogenic stratospheric ozone-depleting emission. The tropospheric concentration of N2O continues to increase, with animal production systems constituting the largest anthropogenic source. Stable isotopes of nitrogen (N) provide tools for constraining emission sources and, following the temporal dynamics of N2O, providing additional insight and unequivocal proof of N2O source, production pathways and consumption. The potential for using stable isotopes of N is underutilised. The intent of this article is to provide an overview of what these tools are and demonstrate where and how these tools could be applied to advance the mitigation of N2O emissions from animal production systems. Nitrogen inputs and outputs are dominated by fertiliser and excreta, respectively, both of which are substrates for N2O production. These substrates can be labelled with 15N to enable the substrate-N to be traced and linked to N2O emissions. Thus, the effects of changes to animal production systems to reduce feed-N wastage by animals and fertiliser wastage, aimed at N2O mitigation and/or improved animal or economic performance, can be traced. Further 15N-tracer studies are required to fully understand the dynamics and N2O fluxes associated with excreta, and the biological contribution to these fluxes. These data are also essential for the new generation of 15N models. Recent technique developments in isotopomer science along with stable isotope probing using multiple isotopes also offer exciting capability for addressing the N2O mitigation quest.

Keywords

15Nclimate changeexcretanitrogen isotopesnitrous oxide
Type
Full Paper
Information
animal , Volume 7 , Issue s2: Greenhouse Gases & Animal Agriculture Conference (GGAA 2013), 23rd ‐ 26th June 2013, Dublin, Ireland , June 2013 , pp. 418 - 426
Copyright
Copyright © The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbasi, MK, Muller, C 2011. Trace gas fluxes of CO2, CH4 and N2O in a permanent grassland soil exposed to elevated CO2 in the Giessen FACE study. Atmospheric Chemistry and Physics 11, 9333–9342.Google Scholar
Barraclough, D, Puri, G 1995. The use of 15N pool dilution and enrichment to separate the heterotrophic and autotrophic pathways of nitrification. Soil Biology & Biochemistry 27, 17–22.Google Scholar
Bergsma, TT, Ostrom, NE, Emmons, M, Robertson, GP 2001. Measuring simultaneous fluxes from soil of N2O and N2 in the field using the 15N-Gas “nonequilibrium” technique. Environmental Science and Technology 35, 4307–4312.Google Scholar
Bergstermann, A, Cardenas, L, Bol, R, Gilliam, L, Goulding, K, Meijide, A, Scholefield, D, Vallejo, A, Well, R 2011. Effect of antecedent soil moisture conditions on emissions and isotopologue distribution of N2O during denitrification. Soil Biology & Biochemistry 43, 240–250.Google Scholar
Berntsen, J, Petersen, BM, Sorensen, P, Olesen, JE 2007. Simulating residual effects of animal manures using N-15 isotopes. Plant and Soil 290, 173–187.Google Scholar
Boast, CW, Mulvaney, RL, Baveye, P 1988. Evaluation of nitrogen-15 tracer techniques for direct measurement of denitrification in soil: I. Theory. Soil Science Society of America Journal 52, 1317–1322.Google Scholar
Bol, R, Toyoda, S, Yamulki, S, Hawkins, JMB, Cardenas, LM, Yoshida, N 2003. Dual isotope and isotopomer ratios of N2O emitted from a temperate grassland soil after fertiliser application. Rapid Communications in Mass Spectrometry 17, 1–7.Google Scholar
Bosshard, C, Sorensen, P, Frossard, E, Dubois, D, Mader, P, Nanzer, S, Oberson, A 2009. Nitrogen use efficiency of N-15-labelled sheep manure and mineral fertiliser applied to microplots in long-term organic and conventional cropping systems. Nutrient Cycling in Agroecosystems 83, 271–287.Google Scholar
Bosshard, C, Oberson, A, Leinweber, P, Jandl, G, Knicker, H, Wettstein, HR, Kreuzer, M, Frossard, E 2011. Characterization of fecal nitrogen forms produced by a sheep fed with N-15 labeled ryegrass. Nutrient Cycling in Agroecosystems 90, 355–368.Google Scholar
Braker, G, Conrad, R 2011. Diversity, structure, and size of N2O-producing microbial communities in soils—what matters for their functioning? In Advances in Applied Microbiology, Vol. 75 (ed. AI Laskin, S Sariaslani and GM Gadd), pp. 33–70. Elsevier Inc., Amsterdam, The Netherlands.CrossRefGoogle Scholar
Buckley, DH, Huangyutitham, V, Hsu, SF, Nelson, TA 2007. Stable isotope probing with 15N2 reveals novel noncultivated diazotrophs in soil. Applied and Environmental Microbiology 73, 3196–3204.Google Scholar
Campanella, MV, Bisigato, AJ 2010. What causes changes in plant litter quality and quantity as consequence of grazing in the Patagonian Monte: plant cover reduction or changes in species composition? Austral Ecology 35, 787–793.Google Scholar
Cardenas, LM, Chadwick, D, Scholefield, D, Fychan, R, Marley, CL, Jones, R, Bol, R, Well, R, Vallejo, A 2007. The effect of diet manipulation on nitrous oxide and methane emissions from manure application to incubated grassland soils. Atmosphere Environment 41, 7096–7107.Google Scholar
Carter, MS, Ambus, P 2006. Biologically fixed N2 as a source for N2O production in a grass-clover mixture, measured by N-15. Nutrient Cycling in Agroecosystems 74, 13–26.Google Scholar
Chapuis-Lardy, L, Wrage, N, Metay, A, Chotte, JL, Bernoux, M 2007. Soils, a sink for N2O? A review. Global Change Biology 13, 1–17.Google Scholar
Clough, TJ, Kelliher, FM, Wang, YP, Sherlock, RR 2006. Diffusion of N-15-labelled N2O into soil columns: a promising method to examine the fate of N2O in subsoils. Soil Biology & Biochemistry 38, 1462–1468.Google Scholar
Davidson, EA 2009. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geosciences 2, 659–662.Google Scholar
Delgado, JA, Del Grosso, SJ, Ogle, SM 2010. N-15 isotopic crop residue cycling studies and modeling suggest that IPCC methodologies to assess residue contributions to N2O-N emissions should be reevaluated. Nutrient Cycling in Agroecosystems 86, 383–390.Google Scholar
Denman, KL, Brasseur, G, Chidthaisong, A, Ciais, P, Cox, PM, Dickinson, RE, Hauglustaine, D, Heinze, C, Holland, E, Jacob, D, Lohmann, U, Ramachandran, S, da Silva Dias, PL, Wofsy, SC, Zhang, X 2007. Couplings between changes in the climate system and biogeochemistry. In Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In (ed. S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor and HL Miller), pp. 499–587. Cambridge University Press, Cambridge.Google Scholar
Dittert, K, Bol, R, King, R, Chadwick, D, Hatch, D 2001. Use of a novel nitrification inhibitor to reduce nitrous oxide emission from N-15 labelled dairy slurry injected into soil. Rapid Communications in Mass Spectrometry 115, 1291–1296.Google Scholar
Forster, P, Ramaswamy, V, Artaxo, P, Berntsen, T, Betts, R, Fahey, DW, Haywood, J, Lean, J, Lowe, DC, Myhre, G, Nganga, J, Prinn, RG, Raga, G, Schulz, M, Van Dorland, R 2007. Changes in atmospheric constituents and in radiative forcing. In Climate change 2007: the physical basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor and HL Miller), pp. 129–234. Cambridge University Press, Cambridge.Google Scholar
Friedman, L, Bigeleisen, J 1950. Oxygen and nitrogen isotope effects in the decomposition of ammonium nitrate. The Journal of Chemical Physics 18, 1325–1331.Google Scholar
Frimpong, KA, Baggs, EM 2010. Do combined applications of crop residues and inorganic fertilizer lower emission of N2O from soil? Soil Use and Management 26, 412–424.Google Scholar
Frimpong, KA, Yawson, DO, Baggs, EM, Agyarko, K 2011. Does incorporation of cowpea-maize residue mixes influence nitrous oxide emission and mineral nitrogen release in a tropical luvisol? Nutrient Cycling in Agroecosystems 91, 281–292.Google Scholar
Fry, B 2006. Stable isotope ecology. Springer, USA.Google Scholar
Giannopoulos, G, van Groenigen, JW, Pulleman, MM 2011. Earthworm-induced N2O emissions in a sandy soil with surface-applied crop residues. Pedobiologia 54, S103–S111.Google Scholar
Griffith, D, Parkes, SD, Haverd, V, Paton-Walsh, C, Wilson, SR 2009. Absolute calibration of the intramolecular site preference of N-15 fractionation in tropospheric N2O by FT-IR spectroscopy. Analytical Chemistry 81, 2227–2234.Google Scholar
Hauck, RD, Meisinger, JJ, Mulvaney, RL 1994. Practical considerations in the use of nitrogen tracers in agricultural and environmental research. In Methods of soil analysis, part 2. Microbiological and biochemical properties_SSSA book series, no. 5 (ed. RW Weaver), pp. 907–950. Soil Science Society of America, Madison, WI, USA.Google Scholar
Ishii, S, Ohno, H, Tsuboi, M, Otsuka, S, Senoo, K 2011. Identification and isolation of active N2O reducers in rice paddy soil. International Society for Microbial Ecology Journal 5, 1936–1945.Google Scholar
Jinuntuya-Nortman, M, Sutka, RL, Ostrom, PH, Gandhi, H, Ostrom, NE 2008. Isotopologue fractionation during microbial reduction of N2O within soil mesocosms as a function of water-filled pore space. Soil Biology & Biochemistry 40, 2273–2280.Google Scholar
Jost, DI, Joergensen, RG, Sundrum, A 2013. Effect of cattle faeces with different microbial biomass content on soil properties, gaseous emissions and plant growth. Biology and Fertility of Soils 49, 61–70.Google Scholar
Junk, G, Svec, H 1958. The absolute abundance of the nitrogen isotopes in the atmosphere and compressed gas from various sources. Geochimica et Cosmochimica Acta 14, 234–243.Google Scholar
Kaiser, J, Park, S, Boering, KA, Brenninkmeijer, CAM, Hilkert, A, Rockmann, T 2004. Mass spectrometric method for the absolute calibration of the intermolecular nitrogen isotope distribution in nitrous oxide. Annalytical Bioanalytical Chemistry 378, 256–269.Google Scholar
Kendall, C, Caldwell, EA 1998. Fundamentals of isotope geochemistry. In Isotope tracers in catchment hydrology (ed. C Kendall and JJ McDonnell), pp. 51–86. Elsevier Science, Amsterdam.Google Scholar
Kirkham, D, Bartholomew, WV 1954. Equations for following nutrient transformations in soil, utilizing tracer data. Soil Science Society of America Proceedings 18, 33–34.Google Scholar
Knowles, R, Blackburn, TH 1993. Nitrogen isotope techniques. Academic Press Inc., San Diego. Elsevier Inc., Amsterdan, The Netherlands.Google Scholar
Kool, DM, Van Groenigen, JW, Wrage, N 2011a. Determination of nitrous oxide based on nitrogen and oxygen isotope tracing: dealing with oxygen exchange. In Methods in enzymology vol 46: research on nitrification and related processes, Pt B (ed. MG Klotz and LY Stein), pp. 139–160. Elsevier Inc., Amsterdam, The Netherlands.Google Scholar
Kool, DM, Dolfing, J, Wrage, N, Van Groenigen, JW 2011b. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biology & Biochemistry 43, 174–178.Google Scholar
Kool, DM, Hoffland, E, Abrahamse, SPA, van Groenigen, JW 2006. What artificial urine composition is adequate for simulating soil N2O fluxes and mineral N dynamics? Soil Biology & Biochemistry 38, 1757–1763.Google Scholar
Kool, DM, Wrage, N, Oenema, O, Dolfing, J, Van Groenigen, JW 2007. Oxygen exchange between (de) nitrification intermediates and H2O and its implications for source determination of NO3− and N2O: a review. Rapid Communications in Mass Spectrometry 21, 3569–3578.Google Scholar
Kool, DM, Muller, C, Wrage, N, Oenema, O, Van Groenigen, JW 2009a. Oxygen exchange between nitrogen oxides and H2O can occur during nitrifier pathways. Soil Biology & Biochemistry 41, 1632–1641.Google Scholar
Kool, DM, Wrage, N, Oenema, O, Harris, D, Van Groenigen, JW 2009b. The O-18 signature of biogenic nitrous oxide is determined by O exchange with water. Rapid Communications in Mass Spectrometry 23, 104–108.Google Scholar
Kool, DM, Wrage, N, Zechmeister-Boltenstern, S, Pfeffer, M, Brus, D, Oenema, O, Van Groenigen, JW 2010. Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labelling method. European Journal of Soil Science 61, 759–772.Google Scholar
Koster, JR, Cardenas, L, Senbayram, M, Bol, R, Well, R, Butler, M, Muhling, KH, Dittert, K 2011. Rapid shift from denitrification to nitrification in soil after biogas residue application as indicated by nitrous oxide isotopomers. Soil Biology & Biochemistry 43, 1671–1677.Google Scholar
Lampe, C, Dittert, K, Sattelmacher, B, Wachendorf, M, Loges, R, Taube, F 2006. Sources and rates of nitrous oxide application of N-15-labelled emissions from grazed grassland after mineral fertilizer and slurry. Soil Biology & Biochemistry 38, 2602–2613.Google Scholar
Laughlin, RJ, Stevens, RJ, Zhuo, S 1997. Determining nitrogen-15 in ammonium by producing nitrous oxide. Soil Science Society of America Journal 61, 462–465.Google Scholar
Lodge, GM, King, KL, Harden, S 2006. Effects of pasture treatments on detached pasture litter mass, quality, litter loss, decomposition rates, and residence time in northern New South Wales. Australian Journal of Agricultural Research 57, 1073–1085.Google Scholar
Maeda, K, Toyoda, S, Shimojima, R, Osada, T, Hanajima, D, Morioka, R, Yoshida, N 2010. Source of nitrous oxide emissions during the cow manure composting process as revealed by isotopomer analysis of and amoA abundance in betaproteobacterial ammonia-oxidizing bacteria. Applied and Environmental Microbiology 76, 1555–1562.Google Scholar
Mary, B, Recous, S, Robin, D 1998. A model for calculating nitrogen fluxes in soil using tracing. Soil Biology & Biochemistry 30, 1963–1979.Google Scholar
Mathieu, O, Lévêque, J, Hénault, C, Ambus, P, Milloux, M-J, Andreux, F 2007. Influence of 15N enrichment on the net isotopic fractionation factor during the reduction of nitrate to nitrous oxide in soil. Rapid Communications in Mass Spectrometry 21, 1447–1451.Google Scholar
Meijide, A, Cardenas, LM, Bol, R, Bergstermann, A, Goulding, K, Well, R, Vallejo, A, Scholefield, D 2010. Dual isotope and isotopomer measurements for the understanding of N2O production and consumption during denitrification in an arable soil. Applied & Environmental Microbiology 76, 1555–1562.Google Scholar
Mohn, J, Tuzson, B, Manninen, A, Yoshida, N, Toyoda, S, Brand, WA, Emmenegger, L 2012. Site selective real-time measurements of atmospheric N2O isotopomers by laser spectroscopy. Atmospheric Measurement Techniques 5, 1601–1609.Google Scholar
Mosier, AR, Schimel, DS 1993. Nitrification and denitrification. In Nitrogen isotope techniques (ed. R Knowles and TH Blackburn), pp. 181–208. Academic Press Inc., San Diego.Google Scholar
Muller, C, Rutting, T, Kattge, J, Laughlin, RJ, Stevens, RJ 2007. Estimation of parameters in complex N-15 tracing models by Monte Carlo sampling. Soil Biology & Biochemistry 39, 715–736.Google Scholar
Mulvaney, RL 1993. Mass spectrometry. In Nitrogen isotope techniques (ed. R Knowles and TH Blackburn), pp. 11–57. Academic Press Inc., San Diego.Google Scholar
Mulvaney, RL, Boast, CW 1986. Equations for determination of nitrogen-15 labeled dinitrogen and nitrous oxide by mass spectrometry. Soil Science Society of America Journal 50, 360–363.Google Scholar
Myrold, DD, Tiedje, JM 1986. Simultaneous estimation of several nitrogen-cycle rates using N-15 theory and application. Soil Biology & Biochemistry 18, 559–568.Google Scholar
Nelissen, V, Rütting, T, Huygen, D, Staelens, J, Ruysschaerta, G, Boeckx, P 2012. Maize biochars accelerate short-term soil nitrogen dynamics in a loamy sand soil. Soil Biology & Biochemistry 55, 20–27.Google Scholar
OECD_FAO 2012. OECD-FAO Agricultural Outlook 2012-2021 (ed. aAOotU Nations). OECD Publishing. http://www.oecd.org/site/oecd-faoagriculturaloutlook/##publication2012Google Scholar
Oenema, O, Wrage, N, Velthof, GL, van Groenigen, JW, Dolfing, J, Kuikman, PJ 2005. Trends in global nitrous oxide emissions from animal production systems. Nutrient Cycling in Agroecosystems 72, 51–65.Google Scholar
Ostrom, NE, Sutka, RL, Ostrom, PH, Grandy, AS, Huizinga, KM, Gandhi, H, von Fischer, JC, Robertson, GP 2010. Isotopologue data reveal bacterial denitrification as the primary source of N2O during a high flux event following cultivation of a native temperate grassland. Soil Biology & Biochemistry 42, 499–506.Google Scholar
Pal, P, Clough, TJ, Kelliher, FM, Sherlock, RR 2013. Nitrous oxide emissions from in situ deposition of 15N labeled ryegrass litter in a pasture soil. Journal of Environmental Quality 42, 323–331.Google Scholar
Pal, P, Clough, TJ, Kelliher, FM, van Koten, C, Sherlock, RR 2012. Intensive cattle grazing affects pasture litter-fall: an unrecognized nitrous oxide source. Journal of Environmental Quality 41, 444–448.Google Scholar
Park, S, Pérez, P, Boering, KA, Trumbore, SE, Gil, J, Marquina, S, Tyler, SC 2011. Can N2O stable isotopes and isotopomers be useful tools to characterize sources and microbial pathways of N2O production and consumption in tropical soils? Global Biogeochemical Cycles 25, 1–16.Google Scholar
Park, S, Croteau, P, Boering, KA, Etheridge, DM, Ferretti, D, Fraser, PJ, Kim, KR, Krummel, PB, Langenfelds, RL, van Ommen, TD, Steele, LP, Trudinger, CM 2012. Trends and seasonal cycles in the isotopic composition of nitrous oxide since 1940. Nature Geoscience 5, 261–265.Google Scholar
Pattey, E, Strachan, IB, Desjardins, RL, Edwards, GC, Dow, D, MacPherson, JI 2006. Application of a tunable diode laser to the measurement of CH4 and N2O fluxes from field to landscape scale using several micrometeorological techniques. Agriculture and Forest Meteorology 136, 222–236.Google Scholar
Paul, JW, Beauchamp, EG 1995. Availability of manure slurry ammonium for corn using N-15-labelled (NH4)2SO4. Canadian Journal of Soil Science 75, 35–42.Google Scholar
Perez, T, Garcia-Montiel, D, Trumbore, S, Tyler, S, De Camargo, P, Moreira, M, Piccolo, M, Cerri, C 2006. Nitrous oxide nitrification and denitrification N-15 enrichment factors from Amazon forest soils. Ecological Applications 16, 2153–2167.Google Scholar
Powell, JM, Wu, ZG, Kelling, K, Cusick, P, Munoz, G 2004. Differential nitrogen-15 labeling of dairy manure components for nitrogen cycling studies. Agronomy Journal 96, 433–441.Google Scholar
Radajewski, S, McDonald, IR, Murrell, JC 2003. Stable isotope probing of nucleic acids: a window to the function of uncultured microorganisms. Current Opinion in Biotechnology 14, 296–302.Google Scholar
Ravishankara, AR, Daniel, JS, Portmann, RW 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125.Google Scholar
Rockmann, T, Kaiser, J, Brenninkmeijer, CAM, Brand, WA 2003. Gas chromatography/isotope-ratio mass spectrometry method for high- precision position-dependent N-15 and O-18 measurements of atmospheric nitrous oxide. Rapid Communications in Mass Spectrometry 17, 1897–1908.Google Scholar
Ruetting, T, Mueller, C 2007. N-15 tracing models with a Monte Carlo optimization procedure provide new insights on gross N transformations in soils. Soil Biology & Biochemistry 39, 2351–2361.Google Scholar
Rütting, T 2012. Ignoring isotopic fractionation does not bias quantifications of gross nitrogen transformations. Rapid Communications in Mass Spectrometry 26, 1639–1640.Google Scholar
Schils, RLM, Eriksen, J, Ledgard, SF, Vellinga, TV, Kuikman, PJ, Luo, J, Petersen, SO, Velthof, GL 2013. Strategies to mitigate nitrous oxide emissions from herbivore production systems. Animal 7, 29–40.Google Scholar
Schouten, S, van Groenigen, JW, Oenema, O, Cayuela, ML 2012. ‘Bioenergy from cattle manure? Implications of anaerobic digestion and subsequent pyrolysis for carbon and nitrogen dynamics in soil’. Global Change Biology Bioenergy 4, 751–760.Google Scholar
Sharp, Z 2007. Priciples of stable isotope geochemistry. Pearson Prentice Hall, Upper Saddle River, New Jersey.Google Scholar
Sorensen, P, Thomsen, IK 2005. Production of nitrogen-15-labeled pig manure for nitrogen cycling studies. Soil Science Society of America Journal 69, 1639–1643.Google Scholar
Stange, F, Dohling, F 2005. 15N tracing model SimKIM to analyse the NO and N2O production during autotrophic, heterotrophic nitrification, and denitrification in soils. Isotopes in Environmental & Health Studies 41, 261–274.Google Scholar
Stark, JM, Hart, RH 1996. Diffusion technique for preparing salt solutions, Kjeldahl digests, and persulfate digests for nitrogen-15 analysis. Soil Science Society of America Journal 60, 1846–1855.Google Scholar
Stevens, RJ, Laughlin, RJ 1994. Determining nitrogen-15 in nitrite or nitrate by producing nitrous oxide. Soil Science Society of America Journal 58, 1108–1116.Google Scholar
Stevens, RJ, Laughlin, RJ 1998. Measurement of nitrous oxide and di-nitrogen emissions from agricultural soils. Nutrient Cycling in Agroecosystems 52, 131–139.Google Scholar
Stevens, RJ, Laughlin, RJ, Atkins, GJ, Prosser, SJ 1993. Automated determination of nitrogen-15 labelled dinitrogen and nitrous oxide by mass spectrometry. Soil Science Society of America Journal 57, 981–988.Google Scholar
Sutka, RL, Ostrom, NE, Ostrom, PH, Gandhi, H, Breznak, JA 2003. Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Communications in Mass Spectrometry 17, 738–745.Google Scholar
Sutka, RL, Ostrom, NE, Ostrom, PH, Breznak, JA, Gandhi, H, Pitt, AJ, Li, F 2006. Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Applied and Environmental Microbiology 72, 638–644.Google Scholar
Taghizadeh-Toosi, A, Clough, TJ, Condron, LM, Sherlock, RR, Anderson, CR, Craigie, RA 2011. Biochar incorporation into pasture soil suppresses in situ N2O emissions from ruminant urine patches. Journal of Environmental Quality 40, 468–476.Google Scholar
Toyoda, S, Yoshida, N 1999. Determination of nitrogen isotopomers of nitrous oxide on a modified isotope ratio mass spectrometer. Analytical Chemistry 71, 4711–4718.Google Scholar
Toyoda, S, Mutobe, H, Yanmagishi, H, Yoshida, N, Tanji, Y 2005. Fractionation of N2O isotopomers during production by denitrifier. Soil Biology & Biochemistry 37, 1535–1545.Google Scholar
Toyoda, S, Yano, M, Nishimura, S, Akiyama, H, Hayakawa, A, Koba, K, Sudo, S, Yagi, K, Makabe, A, Tobari, Y, Ogawa, NO, Ohkouchi, N, Yamada, K, Yoshida, N 2011. Characterization and production and consumption processes of N2O emitted from temperate agricultural soils determined via isotopomer ratio analysis. Global Biogeochemical Cycles 25, 1–17.Google Scholar
Well, R, Kurganova, I, de Gerenyu, VL, Flessa, H 2006. Isotopomer signatures of soil-emitted N2O under different moisture conditions – a microcosm study with arable loess soil. Soil Biology & Biochemistry 38, 2923–2933.Google Scholar
Well, R, Flessa, H, Xing, L, Ju, XT, Romheld, V 2008. Isotopologue ratios of N2O emitted from microcosms with NH4+ fertilized arable soils under conditions favoring nitrification. Soil Biology & Biochemistry 40, 2416–2426.Google Scholar
Wrage, N, Velthof, GL, van Beusichem, ML, Oenema, O 2001. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology & Biochemistry 33, 1723–1732.Google Scholar
Wrage, N, van Groenigen, JW, Oenema, O, Baggs, EM 2005. A novel dual-isotope labelling method for distinguishing between soil sources of N2O. Rapid Communications in Mass Spectrometry 19, 3298–3306.Google Scholar
Yamulki, S, Toyoda, S, Yoshida, N, Veldkamp, E, Grant, B, Bol, R 2001. Diurnal fluxes and the isotopomer ratios of N2O in a temperate grassland following urine amendment. Rapid Communications in Mass Spectrometry 15, 1263–1269.Google Scholar
Yoshida, N, Toyoda, S 2000. Constraining the atmospheric N2O budget from intramolecular site preference in N2O isotopomers. Nature 405, 330–334.Google Scholar
Yue, XL, Liao, SQ, Ji, HJ, Zhang, WL, Zuo, YB, Rong, XN 2012. Nitrogen-15 labeling and nitrogen transformation in silage maize-cattle manure system. Zhongguo Shengtai Nongye Xuebao/Chinese Journal of Eco-agriculture Vol. 20, 24–27.Google Scholar