Nutrient Cycling in Agroecosystems

, Volume 101, Issue 2, pp 211–222 | Cite as

Nitrous oxide emissions from perennial grass–legume intercrop for bioenergy use

  • Kenedy E. Epie
  • Liisa Saikkonen
  • Arja Santanen
  • Seija Jaakkola
  • Pirjo Mäkelä
  • Asko Simojoki
  • Frederick L. Stoddard
Original Article


Bioenergy cropping, like all agricultural practices, may lead to the release of greenhouse gases. This study was aimed at determining biomass and energy yields of reed canary grass (RCG) (Phalaris arundinacea), galega (Galega orientalis) and a mixture of these, and to relate these to fluxes of nitrous oxide (N2O), a potent greenhouse gas, emitted from the soils. Plots including a bare fallow as control were established in 2008. Gases emitted from the soil surface were collected in closed chambers from May 2011 to May 2013, except during periods of snow cover, and analysed by gas chromatography. Seasonal and annual cumulative emissions of N2O and CO2 equivalents per unit energy yield were calculated. Soil moisture content, nitrate (NO3 )-N and ammonium (NH4 +)-N were also determined. Both species composition and crop yields affected energy yields and N2O emission from the soil. The annual cumulative emissions from mixture were marginally lower than those from fertilized RCG soils. Fertilized RCG produced twice as much biomass and correspondingly higher nitrogen and energy yields, so its low emission of N2O per Mg of dry matter was not significantly different from that of the mixtures. Cropping an RCG–galega mixture for biofuel may replace N fertilizer input since it resulted in lowering N2O fluxes, but requires management to maintain grass as the major component in order to minimize N2O emissions. In a time of climate change, low-input bioenergy crops may be a suitable strategy for land left uncropped after ploughing for one season or longer.


Energy yields Galega Intercropping N fertilizer Nitrous oxide Reed canary grass 



This work was partly funded by the Academy of Finland Grant 1124435, ‘Carbon-sequestering species mixtures for sustainable energy cropping’ and Legume Futures (Legume-supported cropping systems for Europe), a collaborative research project funding from the European Union’s Seventh Programme for research, technological development and demonstration under grant agreement No 245216. The Graduate School for Agricultural Production Sciences of the University of Helsinki, and the Ella and Georg Ehrnrooth Foundation are also thanked for their financial support. The authors would also like to express gratitude to Miia Collander and Markku Tykkyläinen for technical assistance.


  1. Adler PR, Del Grosso SJ, Parton WJ (2007) Life-cycle assessment of net greenhouse gas flux for bioenergy cropping systems. Ecol Appl 17:675–691PubMedCrossRefGoogle Scholar
  2. Aulakh MS, Rennie DA, Paul EA (1982) Gaseous nitrogen losses from cropped and summer-fallowed soils. Can J Soil Sci 62:187–196CrossRefGoogle Scholar
  3. Azam F, Müller C, Weiske A, Benckiser G, Ottow JCG (2002) Nitrification and denitrification as sources of atmospheric nitrous oxide—role of oxidizable carbon and applied nitrogen. Biol Fertil Soils 35:54–61CrossRefGoogle Scholar
  4. Börjesson PII (1996) Energy analysis of biomass production and transportation. Biomass Bioenergy 11:305–318CrossRefGoogle Scholar
  5. Bouwman AF (1990) Exchange of greenhouse gases between terrestrial ecosystems and the atmosphere. In: Bouwman AF (ed) Soils and the greenhouse effect. Wiley, New York, pp 249–279Google Scholar
  6. Brentrup F, Palliere C (2008) GHG emissions and energy efficiency in European nitrogen fertiliser production and use. In: Proceedings of international fertiliser society, December 11, YorkGoogle Scholar
  7. Butler TJ, Muir JP, Huo C, Guretzky JA (2013) Switchgrass biomass and nitrogen yield with over-seeded cool-season forages in the southern Great Plains. Bioenergy Res 6:44–52CrossRefGoogle Scholar
  8. Conrad R, Seiler W, Bunse G (1983) Factors influencing the loss of fertilizer nitrogen into the atmosphere as N2O. J Geophys Res 88:6709–6718CrossRefGoogle Scholar
  9. Crutzen PJ, Mosier AR, Smith KA, Winiwarter W (2008) N2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos Chem Phys 8:389–395CrossRefGoogle Scholar
  10. Dobbie KE, Smith KA (2003) Nitrous oxide emission factors for agricultural soil in Great Britain: the impact of soil water-filled pore space and other controlling variables. Glob Change Biol 9:204–218CrossRefGoogle Scholar
  11. Drewer J, Finch JW, Lloyd CR, Baggs EM, Skiba U (2012) How do soil emissions of N2O, CH4 and CO2 from perennial bioenergy crops differ from arable annual crop? GCB Bioenergy 4:408–419CrossRefGoogle Scholar
  12. Dumbleton F (1997) Biomass conversion technologies: an overview. Asp Appl Biol 49:341–347Google Scholar
  13. Einsle O, Kroneck PMH (2004) Structural basis of denitrification. Biol Chem 385:875–883PubMedCrossRefGoogle Scholar
  14. El Bassam N (2010) Handbook of bioenergy crops: a complete reference to species, development and applications. Earthscan Ltd., LondonGoogle Scholar
  15. European Commission (EC) (2009) Official Journal of the European Union, Directive 2009/28/EC of the European Parliament and of the council of 23 April 2009 on the promotion of the use of energy from renewable sources and amending and subsequently repealing Directives 2001/77/EC and 2003/30/ECGoogle Scholar
  16. European Commission (EC) (2013) Official Journal of the European Union commision implementing decision of 30 May 2013 on recognition of the ‘Biograce GHG calculation tool’ for demonstrating compliance with the sustainability criteria under Directives 98/70/EC and 2009/28/EC of the European Parliament and of the Council.
  17. Farrell AE, Plevin RJ, Turner BT, Jones AD, OHare M, Kammen DM (2006) Ethanol can contribute to energy and environmental goals. Science 311:506–508PubMedCrossRefGoogle Scholar
  18. Flechard CR, Ambus P, Skiba U, Rees RM, Hensen A, Amstel A, Dasselaar AP, Soussana JF, Jones M, Clifton-Brown J, Raschi A, Horvath L, Neftel A, Joscher M, Ammann C, Leifeld J, Fuhrer J, Calanca P, Thalman E, Pilegaard L, Di Marco C, Campbell C, Nemitz E, Hargreaves KJ, Levy PE, Ball BC, Jones SK, van de Bulk WCM, Groot T, Blom M, Domingues R, Kasper G, Allar A, Caschia E, Cellier P, Laville P, Henault C, Bizouard F, Abdalla M, Williams M, Baronti S, Berretti F, Grosz B (2007) Effects of climate and management intensity on nitrous oxide emissions in grassland systems across Europe. Agric Ecosyst Environ 121:135–152CrossRefGoogle Scholar
  19. Granli T, Bockman OC (1994) Nitrous oxide from agriculture. Nor J Agric 12:7–128Google Scholar
  20. Hadders G, Olsson R (1997) Harvest of grass for combustion in late summer and in spring. Biomass Bioenergy 12:171–175CrossRefGoogle Scholar
  21. Inselsbacher E, Wanek W, Ripka K et al (2011) Greenhouse gas fluxes respond to different N fertilizer types due to altered plant-soil—microbe interactions. Plant Soil 343:17–35CrossRefGoogle Scholar
  22. Jaakkola A, Simojoki A (1998) Effect of soil wetness on air composition and nitrous oxide emission in a loam soil. Agric Food Sci Finl 7:491–505Google Scholar
  23. Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJR, Morrison MJ (2012) Legumes for mitigation of climate change and provision of feedstock for biofuels and biorefineries: a review. Agron Sustain Dev 32:329–364CrossRefGoogle Scholar
  24. Kim H, Kim S, Dale BE (2009) Biofuels, land use change, and greenhouse gas emissions. Environ Sci Technol 43:961–967PubMedCrossRefGoogle Scholar
  25. Klumpp K, Bloor JMG, Ambus P, Soussana JF (2011) Effects of clover density on N2O emissions and plant-soil N transfers in a fertilised upland pasture. Plant Soil 343:97–107CrossRefGoogle Scholar
  26. Kryzeviciene A, Jasinskas A, Gulbinas A (2008) Perennial grasses as a source of bioenergy in Lithuania. Agron Res 6:229–239Google Scholar
  27. Kusa K, Sawamoto T, Hatano R (2002) Nitrous oxide emissions for 6 years from a gray lowland soil cultivated with onions in Hokkaido, Japan. Nutr Cycl Agroecosyst 63:239–247CrossRefGoogle Scholar
  28. Ledgard S, Schils R, Eriksen J, Luo J (2009) Environmental impacts of grazed clover/grass pastures. Ir J Agric Food Res 48:209–226Google Scholar
  29. Lee J, Hopmans JW, Kessel CV et al (2008) Tillage and seasonal emissions of CO2, N2O and NO across a seed bed and at the field scale in a Mediterranean climate. Agric Ecosyst Environ 129:378–390CrossRefGoogle Scholar
  30. Lewandowski I, Scurlock JMO, Lindvall E, Christou M (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25:335–361CrossRefGoogle Scholar
  31. Lumpkins BS, Batal AB, Dale NM (2004) Evaluation of a distillers dried grains with solubles as a feed ingredient for broilers. Poult Sci 83:1891–1896PubMedCrossRefGoogle Scholar
  32. Machefert SE, Dise NB, Goulding KWT, Whitehead PG (2002) Nitrous oxide emission from a range of land uses across Europe. Hydrol Earth Syst Sci 6:325–337CrossRefGoogle Scholar
  33. Mosier AR, Duxbury JM, Freney JR, Heinemeyer O, Minami K (1996) Nitrous oxide from agricultural fields: assessment, measurement and mitigation. Plant Soil 181:95–108CrossRefGoogle Scholar
  34. Myhre G, Shindell D, Bréon FM, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque JF, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forc-ing. In: Stocker TF, Qin D, Plattner GK, 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, CambridgeGoogle Scholar
  35. Penttilä A, Slade EM, Simojoki A, Riutta T, Minkkinen K, Roslin T (2013) Quantifying beetle-mediated effects on gas fluxes from dung Pats. PLoS One 8:e71454. doi: 10.1371/journal.pone.0071454 PubMedCentralPubMedCrossRefGoogle Scholar
  36. Portmann RW, Daniel JS, Ravishankara AR (2012) Stratospheric ozone depletion due to nitrous oxide: influences of other gases. Philos Trans R Soc Biol Sci 367:1256–1264CrossRefGoogle Scholar
  37. Ranucci S, Bertolini T, Vitale L, Di Tommasi P, Ottaiano L, Oliva M, Amato U, Fierro A, Magliulo V (2011) The influence of management and environmental variables on soil N2O emissions in a crop system in Southern Italy. Plant Soil 343:83–96CrossRefGoogle Scholar
  38. Ravishankara AR, Daniel JS, Pertmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125PubMedCrossRefGoogle Scholar
  39. Regina K, Kaseva J, Esala M (2013) Emissions of nitrous oxide from boreal agricultural mineral soils—statistical models based on measurements. Agric Ecosyst Environ 164:131–136CrossRefGoogle Scholar
  40. Robertson GP, Groffman PM (2014) Nitrogen transformations. In: Paul EA (ed) Soil microbiology, ecology and biochemistry, 4th edn. Academic, BurlingtonGoogle Scholar
  41. Rochette P, Janzen HH (2005) Towards a revised coefficient for estimating N2O emissions from legumes. Nutr Cycl Agroecosyst 73:171–179CrossRefGoogle Scholar
  42. Ruz-Jerez BE, White RE, Ball PR (1994) Long-term measurement of denitrification in three contrasting pastures grazed by sheep. Soil Biol Biochem 26:29–39CrossRefGoogle Scholar
  43. Sahramaa M, Ihamäki H, Jauhiainen L (2003) Variation of biomass related variables of reed canary grass. Agric Food Sci Finl 12:213–225Google Scholar
  44. Scanlon TM, Kiley G (2003) Ecosystem-scale measurements of nitrous oxide fluxes for an intensely grazed, fertilized grassland. Geophys Res Lett. doi: 10.1029/2003GL017454 Google Scholar
  45. Simek M, Virtanen S, Kristufek V, Simojoki A, Yli-Halla M (2011) Evidence of rich microbial communities in the subsoil of a boreal acid sulphate soil conducive to greenhouse gas emissions. Agric Ecosyst Environ 140:113–122CrossRefGoogle Scholar
  46. Simojoki A, Jaakkola A (2000) Effect of nitrogen fertilization, cropping and irrigation on soil air composition and nitrous oxide emission in a loamy clay. Eur J Soil Sci 51:413–424CrossRefGoogle Scholar
  47. Smith MS, Tiedje JM (1979) The effect of roots on soil denitrification. Soil Sci Soc Am J 43:951–955CrossRefGoogle Scholar
  48. Stephenson AL, Dennis JS, Scott SA (2008) Improving the sustainability of the production of biodiesel from oilseed rape in the UK. Process Saf Environ Prot 86:427–440CrossRefGoogle Scholar
  49. Syväsalo E, Regina K, Pihlatie M, Esala M (2004) Emissions of nitrous oxide from boreal agricultural clay and loamy sand soils. Nutr Cycl Agroecosyst 69:155–165CrossRefGoogle Scholar
  50. Tunå P, Hulteberg C, Ahlgren S (2013) Techno-economic assessment of non-fossil ammonia production. DOI, Environ Prog Sustain Energy. doi: 10.1002/ep.11886 Google Scholar
  51. Tuomisto HL, Helenius J (2008) Comparison of energy and greenhouse gas balances of biogas with other transport biofuel options based on domestic agricultural biomass in Finland. Agric Food Sci 17:240–251CrossRefGoogle Scholar
  52. Van Beek CL, Pleijter M, Jacobs CMJ, Velthof GL, van Groenigen JW, Kuikman PJ (2010) Emissions of N2O from fertilized and grazed grassland on organic soil in relation to groundwater level. Nutr Cycl Agroecosyst 86:331–340CrossRefGoogle Scholar
  53. Van der Weerden T, de Klein C, Kelliher F (2010) Influence of pore size distribution and soil water content on N2O response curves. In: 19th World Congress of Soil Science, Soil Solutions for a Changing World 1—6 August 2010, Brisbane, Australia. Published on DVDGoogle Scholar
  54. Wei XR, Hao MD, Xue XH, Shi P, Horton R, Wang A, Zang YF (2010) Nitrous oxide emission from highland winter wheat field after long-term fertilization. Biogeosciences 7:3301–3310CrossRefGoogle Scholar
  55. Willey RS (1979) Intercropping—its importance and research needs. Part 1. Competition and yield advantages. Field Crop Abstr 32:1–10Google Scholar
  56. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18CrossRefGoogle Scholar
  57. Yang LF, Cai ZC (2005) The effect of growing soybean (Glycine max L.) on N2O emission from soil. Soil Biol Biochem 37:1205–1209CrossRefGoogle Scholar
  58. Zhang LH, Chen YN, Zhao RF, Li WH (2010) Significance of temperature and soil moisture content on soil respiration in three desert ecosystems in Northwest China. J Arid Environ 74:1200–1211CrossRefGoogle Scholar
  59. Zhong Z, Lemke RL, Nelson LM (2009) Nitrous oxide emissions associated with nitrogen fixation by grain legumes. Soil Biol Biochem 41:2283–2291CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Kenedy E. Epie
    • 1
  • Liisa Saikkonen
    • 3
  • Arja Santanen
    • 1
  • Seija Jaakkola
    • 1
  • Pirjo Mäkelä
    • 1
  • Asko Simojoki
    • 2
  • Frederick L. Stoddard
    • 1
  1. 1.Department of Agricultural SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Department of Food and Environmental SciencesUniversity of HelsinkiHelsinkiFinland
  3. 3.Department of Economics and ManagementUniversity of HelsinkiHelsinkiFinland

Personalised recommendations