Abstract
Aim
Incorporating non-bloat legumes into grass pastures can reduce enteric methane and alter cattle urinary urea N output by increasing protein intake. Deposition of high urea N urine influences soil N-cycling microbes and potentially N2O production. We studied how urine urea N concentration affects soil nitrifier and denitrifier abundances, activities, and N2O production.
Methods
15N13C-labelled urea dissolved in cattle urine was added at 3.5 and 7.0 g L−1 to soils from a grazed, non-bloat legume pasture and incubated under controlled conditions. CO2, N2O, 13C-CO2, and 15N-N2O production were quantified over 240 h, along with nitrifier and denitrifier N-cycling genes and mRNA transcripts.
Results
High urea urine increased total N2O relative to the control; low urea was not significantly different from the control or the high urea treatment. As a result, N2O-N emission factors were not significantly different between the low urea treatment (1.17%) and high urea treatment (0.94%). Doubling urea concentration doubled CO2-Curea and N2O-Nurea but not total N2O-N. Urine addition initially inhibited then increased AOB transcripts and gene abundances. nirK and nirS transcript abundances indicated that denitrification by ammonia oxidizers and/or heterotrophic denitrifiers dominated N2O production. Urine addition increased nosZ-II vs. nosZ-I transcripts, improving soil N2O reduction potential.
Conclusion
Characterizing this interplay between nitrifiers and denitrifiers improves the understanding of urine patch N2O sinks and source dynamics. This mechanistic information helps to explain the constrained short-term N2O emissions observed in response to excess urine N excretion from cattle consuming high protein diets, e.g. non-bloat legumes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Agriculture and Agri-Food Canada (1998) The Canadian System of Soil Classification, 3rd edn. NRC Research Press, Ottawa
Ambus P, Petersen SO, Soussana JF (2007) Short-term carbon and nitrogen cycling in urine patches assessed by combined carbon-13 and nitrogen-15 labelling. Agr Ecosyst Environ 121:84–92. https://doi.org/10.1016/j.agee.2006.12.007
Azam F, Muller C, Weiske A, Benckiser G, Ottow J (2002) Nitrification and denitrification as sources of atmospheric nitrous oxide - role of oxidizable carbon and applied nitrogen. Biol Fertil Soils 35:54–61. https://doi.org/10.1007/s00374-001-0441-5
Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388. https://doi.org/10.1007/s00374-005-0858-3
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Boon A, Robinson JS, Chadwick DR, Cardenas LM (2014) Effect of cattle urine addition on the surface emissions and subsurface concentrations of greenhouse gases in a UK peat grassland. Agr Ecosyst Environ 186:23–32. https://doi.org/10.1016/j.agee.2014.01.008
Breuillin-Sessoms F, Venterea RT, Sadowsky MJ, Coulter JA, Clough TJ, Wang P (2017) Nitrification gene ratio and free ammonia explain nitrite and nitrous oxide production in urea-amended soils. Soil Biol Biochem 111:143–153. https://doi.org/10.1016/j.soilbio.2017.04.007
Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans Royal Soc b: Biol Sci 368:20130122. https://doi.org/10.1098/rstb.2013.0122
Byrnes RC, Nùñez J, Arenas L, Rao I, Trujillo C, Alvarez C, Arango J, Rasche F, Chirinda N (2017) Biological nitrification inhibition by Brachiaria grasses mitigates soil nitrous oxide emissions from bovine urine patches. Soil Biol Biochem 107:156–163. https://doi.org/10.1016/j.soilbio.2016.12.029
Carey CJ, Dove NC, Beman JM, Hart SC, Aronson EL (2016) Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem 99:158–166. https://doi.org/10.1016/j.soilbio.2016.05.014
Carter MS (2007) Contribution of nitrification and denitrification to N2O emissions from urine patches. Soil Biol Biochem 39:2091–2102. https://doi.org/10.1016/j.soilbio.2007.03.013
Clark IM, Buchkina N, Jhurreea D, Goulding KWT, Hirsch PR (2012) Impacts of nitrogen application rates on the activity and diversity of denitrifying bacteria in the Broadbalk Wheat Experiment. Philos Trans Royal Soc b: Biol Sci 367:1235–1244. https://doi.org/10.1098/rstb.2011.0314
Clough TJ, Ray JL, Buckthought LE, Calder J, Baird D, O’Callaghan M, Sherlock RR, Condron LM (2009) The mitigation potential of hippuric acid on N2O emissions from urine patches: An in situ determination of its effect. Soil Biol Biochem 41:2222–2229. https://doi.org/10.1016/j.soilbio.2009.07.032
Congreves KA, Phan T, Farrell RE (2019) A new look at an old concept: using 15N2O isotopomers to understand the relationship between soil moisture and N2O production pathways. SOIL 5:265–274. https://doi.org/10.5194/soil-5-265-2019
de Klein CAM, Luo J, Woodward KB, Styles T, Wise B, Lindsey S, Cox N (2014) The effect of nitrogen concentration in synthetic cattle urine on nitrous oxide emissions. Agr Ecosyst Environ 188:85–92. https://doi.org/10.1016/j.agee.2014.02.020
Di HJ, Cameron KC (2008) Sources of nitrous oxide from 15N-labelled animal urine and urea fertiliser with and without a nitrification inhibitor, dicyandiamide (DCD). Soil Research 46:76–82. https://doi.org/10.1071/SR07093
Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624. https://doi.org/10.1038/ngeo613
Di HJ, Cameron KC, Shen J-P, Winefield CS, O’Callaghan M, Bowatte S, He J-Z (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394. https://doi.org/10.1111/j.1574-6941.2010.00861.x
Di HJ, Cameron KC, Sherlock RR, Shen J-P, He J-Z, Winefield CS (2010) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. J Soils Sediments 10:943–954. https://doi.org/10.1007/s11368-009-0174-x
Di HJ, Cameron KC, Podolyan A, Robinson A (2014) Effect of soil moisture status and a nitrification inhibitor, dicyandiamide, on ammonia oxidizer and denitrifier growth and nitrous oxide emissions in a grassland soil. Soil Biol Biochem 73:59–68. https://doi.org/10.1016/j.soilbio.2014.02.011
Dijkstra J, Oenema O, van Groenigen JW, Spek JW, van Vuuren AM, Bannink A (2013) Diet effects on urine composition of cattle and N2O emissions. Animal 7:292–302. https://doi.org/10.1017/S1751731113000578
Ding K, Luo J, Clough TJ, Ledgard S, Lindsey S, Di HJ (2022) In situ nitrous oxide and dinitrogen fluxes from a grazed pasture soil following cow urine application at two nitrogen rates. Sci Total Environ 838:156473. https://doi.org/10.1016/j.scitotenv.2022.156473
Domeignoz-Horta LA, Philippot L, Peyrard C, Bru D, Breuil M-C, Bizouard F, Justes E, Mary B, Léonard J, Spor A (2017) Peaks of in situ N2O emissions are influenced by N2O-producing and reducing microbial communities across arable soils. Glob Change Biol 00:1–11. https://doi.org/10.1111/gcb.13853
Enwall K, Throbäck IN, Stenberg M, Söderström M, Hallin S (2010) Soil Resources Influence Spatial Patterns of Denitrifying Communities at Scales Compatible with Land Management. Appl Environ Microbiol 76:2243–2250. https://doi.org/10.1128/AEM.02197-09
Food and Agricultural Organization of the United Nations (2015) World reference base for soil resources 2014, Update 2015. FAO, Rome
Fox J, Weisberg S (2019) An {R} Companion to Applied Regression, 3rd edn. Sage, Thousand Oaks
Fry B (2006) Stable Isotope Ecology. Springer Science, New York
Ganasamurthy S, Rex D, Samad MS, Richards KG, Lanigan GJ, Grelet G-A, Clough TJ, Morales SE (2021) Competition and community succession link N transformation and greenhouse gas emissions in urine patches. Sci Total Environ 779:146318. https://doi.org/10.1016/j.scitotenv.2021.146318
Graf DRH, Jones CM, Hallin S (2014) Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions. PLOS ONE 9:e114118. https://doi.org/10.1371/journal.pone.0114118
Hallin S, Philippot L, Löffler FE, Sanford RA, Jones CM (2018) Genomics and Ecology of Novel N2O-Reducing Microorganisms. Trends Microbiol 26:43–55. https://doi.org/10.1016/j.tim.2017.07.003
Hamonts K, Balaine N, Moltchanova E, Beare M, Thomas S, Wakelin SA, O’Callaghan M, Condron LM, Clough TJ (2013) Influence of soil bulk density and matric potential on microbial dynamics, inorganic N transformations, N2O and N2 fluxes following urea deposition. Soil Biol Biochem 65:1–11. https://doi.org/10.1016/j.soilbio.2013.05.006
Highton MP, Bakken LR, Dörsch P, Molstad L, Morales SE (2022) Nitrite accumulation and impairment of N2O reduction explains contrasting soil denitrification phenotypes. Soil Biology and Biochemistry 166:108529. https://doi.org/10.1016/j.soilbio.2021.108529
Hink L, Nicol GW, Prosser JI (2017) Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol 19:4829–4837. https://doi.org/10.1111/1462-2920.13282
Intergovernmental Panel on Climate Change (2006) N2O emissions from managed soils, and CO2 emissions from lime and urea application, in: Guidelines for National Greenhouse Gas Inventories, IGES
Intergovernmental Panel on Climate Change (2019) N2O emissions from managed soils, and CO2 emissions from lime and urea application, in: Refinement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories. IPCC, Geneva
Jarvis SC, Scholefield D, Pain B (1995) Nitrogen cycling in grazing systems. In: Bacon P (ed) Nitrogen fertilization in the environment. M. Dekker, New York, pp 381–420
Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641. https://doi.org/10.1038/ismej.2009.152
Jones SK, Rees RM, Skiba UM, Ball BC (2005) Greenhouse gas emissions from a managed grassland. Global Planet Chang Int Young Sci Global Chang Conf 2003(47):201–211. https://doi.org/10.1016/j.gloplacha.2004.10.011
Jones CM, Graf DR, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426. https://doi.org/10.1038/ismej.2012.125
Jones CM, Spor A, Brennan FP, Breuil M-C, Bru D, Lemanceau P, Griffiths B, Hallin S, Philippot L (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Chang 4:801–805. https://doi.org/10.1038/NCLIMATE2301
Koops H-P, Pommerening-Röser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37:1–9. https://doi.org/10.1111/j.1574-6941.2001.tb00847.x
Lenth R (2020) emmeans: Estimated Marginal Means, aka Least-Square Means. R package version 1.4.6. https://cran.r-project.org/package=emmeans
López-Aizpún M, Horrocks CA, Charteris AF, Marsden KA, Ciganda VS, Evans JR, Chadwick DR, Cárdenas LM (2020) Meta-analysis of global livestock urine-derived nitrous oxide emissions from agricultural soils. Glob Change Biol 26(4):2002–2013. https://doi.org/10.1111/gcb.15012
Maynard D, Kalra Y, Crumbaugh J (2008) Nitrate and Exchangeable Ammonium Nitrogen. In: Carter MR, Gregorich EG (eds) Soil Sampling and Methods of Analysis. CRC Press, Boca Raton, pp 97–106
McAuliffe GA, López-Aizpún M, Blackwell MSA, Castellano-Hinojosa A, Darch T, Evans J, Horrocks C, Le Cocq K, Takahashi T, Harris P, Lee MRF, Cardenas L (2020) Elucidating three-way interactions between soil, pasture and animals that regulate nitrous oxide emissions from temperate grazing systems. Agriculture, Ecosystems & Environment 300:106978. https://doi.org/10.1016/j.agee.2020.106978
Meinhardt KA, Stopnisek N, Pannu MW, Strand SE, Fransen SC, Casciotti KL, Stahl DA (2018) Ammonia-oxidizing bacteria are the primary N2O producers in an ammonia-oxidizing archaea dominated alkaline agricultural soil. Environ Microbiol 20:2195–2206. https://doi.org/10.1111/1462-2920.14246
Monaghan RM, Barraclough D (1992) Some chemical and physical factors affecting the rate and dynamics of nitrification in urine-affected soil. Plant Soil 143:11–18
Monaghan RM, Barraclough D (1993) Nitrous oxide and dinitrogen emissions from urine-affected soil under controlled conditions. Plant Soil 151:127–138. https://doi.org/10.1007/BF00010793
Moran MA, Satinsky B, Gifford SM, Luo H, Rivers A, Chan L-K, Meng J, Durham BP, Shen C, Varaljay VA, Smith CB, Yager PL, Hopkinson BM (2013) Sizing up metatranscriptomics. ISME J 794:237–243. https://doi.org/10.1038/ismej.2012.94
O’Callaghan M, Gerard EM, Carter PE, Lardner R, Sarathchandra U, Burch G, Ghani A, Bell N (2010) Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol Biochem 42:1425–1436. https://doi.org/10.1016/j.soilbio.2010.05.003
Oenema O, Wrage N, Velthof GL, van Groenigen JW, Dolfing J, Kuikman PJ (2005) Trends in Global Nitrous Oxide Emissions from Animal Production Systems. Nutr Cycl Agroecosyst 72:51–65. https://doi.org/10.1007/s10705-004-7354-2
Orwin KH, Bertram JE, Clough TJ, Condron LM, Sherlock RR, O’callaghan M, Ray J, Baird DB (2010) Impact of bovine urine deposition on soil microbial activity, biomass, and community structure. Appl Soil Ecol 44:89–100. https://doi.org/10.1016/j.apsoil.2009.10.004
Parkin TB (1987) Soil Microsites as a Source of Denitrification Variability. Soil Sci Soc Am J 51:1194–1199. https://doi.org/10.2136/sssaj1987.03615995005100050019x
Petersen SO, Roslev P, Bol R (2004) Dynamics of a Pasture Soil Microbial Community after Deposition of Cattle Urine Amended with 13C Urea. Appl Environ Microbiol 70:6363–6369. https://doi.org/10.1128/AEM.70.11.6363
Petersen SO, Stamatiadis S, Christofides C (2004) Short-term nitrous oxide emissions from pasture soil as influenced by urea level and soil nitrate. Plant Soil 267:117–127. https://doi.org/10.1007/s11104-005-4688-8
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: The quest for niche specialisation and differentiation. Trends Microbiol 20:523–531. https://doi.org/10.1016/j.tim.2012.08.001
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rex D, Clough TJ, Richards KG, de Klein C, Morales SE, Samad MS, Grant J, Lanigan GJ (2018) Fungal and bacterial contributions to codenitrification emissions of N2O and N2 following urea deposition to soil. Nutr Cycl Agroecosyst 110:135–149. https://doi.org/10.1007/s10705-017-9901-7
Rochette P, Worth DE, Lemke RL, McConkey BG, Pennock DJ, Wagner-Riddle C, Desjardins RJ (2008) Estimation of N2O emissions from agricultural soils in Canada. I. Development of a country-specific methodology. Can J Soil Sci 88:641–654. https://doi.org/10.4141/CJSS07025
Rochette P, Chantigny MH, Ziadi N, Angers DA, Bélanger G, Charbonneau É, Pellerin D, Liang C, Bertrand N (2014) Soil Nitrous Oxide Emissions after Deposition of Dairy Cow Excreta in Eastern Canada. J Environ Qual 43:829–841. https://doi.org/10.2134/jeq2013.11.0474
Samad MS, Ganasamurthy S, Highton MP, Bakken LR, Clough TJ, de Klein CAM, Richards KG, Lanigan GJ, Morales SE (2021) Urea treatment decouples intrinsic pH control over N2O emissions in soils. Soil Biology and Biochemistry 163:108461. https://doi.org/10.1016/j.soilbio.2021.108461
Selbie DR, Buckthought LE, Shepherd MA (2015) The Challenge of the Urine Patch for Managing Nitrogen in Grazed Pasture Systems. Adv Agron 129:229–292. https://doi.org/10.1016/bs.agron.2014.09.004
Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct Measurement of Oxygen Profiles and Denitrification Rates in Soil Aggregates. Soil Sci Soc Am J 49:645–651. https://doi.org/10.2136/sssaj1985.03615995004900030024x
Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2018) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 69:10–20. https://doi.org/10.1111/ejss.12539
Snider D, Thompson K, Wagner-Riddle C, Spoelstra J, Dunfield K (2015) Molecular techniques and stable isotope ratios at natural abundance give complementary inferences about N2O production pathways in an agricultural soil following a rainfall event. Soil Biol Biochem 88:197–213. https://doi.org/10.1016/j.soilbio.2015.05.021
Stein LY (2019) Insights into the physiology of ammonia-oxidizing microorganisms. Curr Opin Chem Biol 49:9–15. https://doi.org/10.1016/j.cbpa.2018.09.003
Sterngren AE, Hallin S, Bengtson P (2015) Archaeal Ammonia oxidizers dominate in numbers, but bacteria drive gross nitrification in N-amended grassland soil. Front Microbiol 6:1350. https://doi.org/10.3389/fmicb.2015.01350
Thomas BW, Gao X, Beck R, Hao X (2017) Are distinct nitrous oxide emission factors required for cattle urine and dung deposited on pasture in western Canada? Environ Sci Pollut Res 24:26142–26147. https://doi.org/10.1007/s11356-017-0392-5
Tian H, Xu R, Canadell JG, Thompson RL, Winiwarter W, Suntharalingam P, Davidson EA, Ciais P, Jackson RB, Janssens-Maenhout G, Prather MJ, Regnier P, Pan N, Pan S, Peters GP, Shi H, Tubiello FN, Zaehle S, Zhou F, Arneth A, Battaglia G, Berthet S, Bopp L, Bouwman AF, Buitenhuis ET, Chang J, Chipperfield MP, Dangal SRS, Dlugokencky E, Elkins JW, Eyre BD, Fu B, Hall B, Ito A, Joos F, Krummel PB, Landolfi A, Laruelle GG, Lauerwald R, Li W, Lienert S, Maavara T, MacLeod M, Millet DB, Olin S, Patra PK, Prinn RG, Raymond PA, Ruiz DJ, van der Werf GR, Vuichard N, Wang J, Weiss RF, Wells KC, Wilson C, Yang J, Yao Y (2020) A comprehensive quantification of global nitrous oxide sources and sinks. Nature 586:248–256. https://doi.org/10.1038/s41586-020-2780-0
Uchida Y, Clough TJ, Kelliher FM, Hunt JE, Sherlock RR (2011) Effects of bovine urine, plants and temperature on N2O and CO2 emissions from a sub-tropical soil. Plant Soil 345:171–186. https://doi.org/10.1007/s11104-011-0769-z
van Groenigen JW, Kuikman PJ, de Groot WJM, Velthof GL (2005) Nitrous oxide emission from urine-treated soil as influenced by urine composition and soil physical conditions. Soil Biol Biochem 37:463–473. https://doi.org/10.1016/J.SOILBIO.2004.08.009
van Groenigen JW, Velthof GL, van der Bolt FJE, Vos A, Kuikman PJ (2005b) Seasonal variation in N2O emissions from urine patches: Effects of urine concentration, soil compaction and dung. Plant Soil 273:15–27. https://doi.org/10.1007/s11104-004-6261-2
Venterea RT, Clough TJ, Coulter JA, Breuillin-Sessoms F, Wang P, Sadowsky MJ (2015) Ammonium sorption and ammonia inhibition of nitrite-oxidizing bacteria explain contrasting soil N2O production. Sci Rep 5:12153. https://doi.org/10.1038/srep12153
Wachendorf C, Lampe C, Taube F, Dittert K (2008) Nitrous oxide emissions and dynamics of soil nitrogen under 15N-labeled cow urine and dung patches on a sandy grassland soil. J Plant Nutr Soil Sci 171:171–180. https://doi.org/10.1002/jpln.200625217
Webster G, Embley TM, Freitag TE, Smith Z, Prosser JI (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7:676–684. https://doi.org/10.1111/j.1462-2920.2005.00740.x
Williams R, Haynes RJ (1994) Comparison of initial wetting pattern, nutrient concentrations in soil solution and the fate of 15N-labelled urine in sheep and cattle urine patch areas of pasture soil. Plant Soil 162:49–59
Williams PH, Jarvis SC, Dixon E (1998) Emission of nitric oxide and nitrous oxide from soil under field and laboratory conditions. Soil Biol Biochem 30:1885–1893. https://doi.org/10.1016/S0038-0717(98)00052-2
Wittorf L, Jones CM, Bonilla-Rosso G, Hallin S (2018) Expression of nirK and nirS genes in two strains of Pseudomonas stutzeri harbouring both types of NO-forming nitrite reductases. Res Microbiol 169:343–347. https://doi.org/10.1016/j.resmic.2018.04.010
Woods RR, Cameron KC, Edwards GR, Di HJ, Clough TJ (2017) 15N recoveries from ruminant urine patches on three forage types. Plant Soil 417:453–465. https://doi.org/10.1007/s11104-017-3270-5
Wrage-Mönnig N, Horn MA, Well R, Müller C, Velthof G, Oenema O (2018) The role of nitrifier denitrification in the production of nitrous oxide revisited. Soil Biol Biochem 123:A3–A16. https://doi.org/10.1016/j.soilbio.2018.03.020
Yamulki S, Wolf I, Bol R, Grant B, Brumme R, Veldkamp E, Jarvis SC (2000) Effects of dung and urine amendments on the isotopic content of N2O released from grasslands. Rapid Commun Mass Spectrom 14:1356–1360. https://doi.org/10.1002/1097-0231(20000815)14:15%3c1356::AID-RCM30%3e3.0.CO;2-C
Yoon S, Nissen S, Park D, Sanford RA, Löffler E (2016) Nitrous oxide reduction kinetics distinguish bacteria harboring clade I nosZ from those harboring clade II nosZ. Appl Environ Microbiol 82:3793–3800. https://doi.org/10.1128/AEM.00409-16.Editor
Acknowledgements
Thanks to the Prairie Environmental Agronomy Research Lab (PEARL) for greenhouse gas analyses. Thank you to the many University of Saskatchewan Department of Soil Science research technicians and students who assisted with technical advice and sampling.
Funding
Funding for this research was provided by the Canadian Agricultural Partnership through the Agriculture Greenhouse Gases Program (AGGP II, grant number AGGP 2–011) and Natural Sciences and Engineering Research Council Discovery Grants to MMA (RGPIN-2016–04968) and BLH (RGPIN-2019–04158). The funding sources had no involvement in study design, data collection, analysis, interpretation, manuscript writing, or the decision to publish.
Author information
Authors and Affiliations
Contributions
JCR conceived and designed the study, set up and conducted the experiment, performed laboratory and data analyses, and wrote the original draft of the manuscript; MMA and BLH conceived and designed the study, supervised the experiment, and reviewed and edited the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no known competing interests.
Additional information
Responsible Editor: Kari Dunfield.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Reimer, J.C., Arcand, M.M. & Helgason, B.L. Soil denitrification response to increased urea concentration constrains nitrous oxide emissions in a simulated cattle urine patch. Plant Soil 498, 125–145 (2024). https://doi.org/10.1007/s11104-023-06048-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06048-w