Abstract
Background
The demand for estimates of biological nitrogen (N) fixation inputs in agricultural systems is driven by the need to effectively manage the global N cycle.
Scope
We present a methodology for quantifying N2 fixation by the grain legume-rhizobia symbioses that can be used for any year or sequence of years for which area and production statistics for legume oilseed and pulse crops were available and at country-to-global scales. The coefficients used in the templates – harvest index, N harvest index, %N shoots, %N grain and a factor to account for below-ground N – were aggregated from 224 reports containing > 4,000 observations. Values for the % total crop N derived from atmospheric N2 (%Ndfa) for specific grain legumes and regions were determined in a companion paper. The grain legumes were estimated to fix a global total of 35.5 Tg N in the year 2018 - 25.0 Tg for soybean (Glycine max), 7.2 Tg for the pulses and 3.3 Tg for groundnut (Arachis hypogaea). Soybean dominated global grain legume N2 fixation, with 38 % of total N fixed associated with soybean in South and Central America and a further 22 % by soybean in North America.
Conclusions
The updated estimates of N2 fixation by the grain legumes inform us of a substantial and increasing role that biological N2 fixation plays in global agricultural systems. The challenge remains to reliably estimate N inputs from other N2-fixing organisms that are active in these systems.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Anglade J, Billen G, Garnier J (2015) Relationships for estimating N2 fixation in legumes: incidence for N balance of legume-based cropping systems in Europe. Ecosphere 6(3):1–24. https://doi.org/10.1890/ES14-00353.1
Angus JF, Grace PR (2017) Nitrogen balance in Australia and nitrogen use efficiency on Australian farms. Soil Res 55:435–450. https://doi.org/10.1071/SR16325
Angus JF, Peoples MB (2012) Nitrogen from Australian dryland pastures. Crop Pasture Sci 63:746–758. https://doi.org/10.1071/CP12161
Arcand MM, Knight JD, Farrell RE (2013) Estimating belowground nitrogen inputs of pea and canola and their contribution to soil inorganic N pools using 15N labeling. Plant Soil 371:67–80
Arcand MM, Lemke R, Farrell RE, Knight JD (2014) Nitrogen supply from below ground residues of lentil and wheat to a subsequent wheat crop. Biol Fertil Soils 50:507–515
Baddeley JA, Jones S, Topp CFE, Watson CA, Helming J, Stoddard L (2013) Integrated analysis of biological nitrogen fixation (BNF) in Europe. Legume Futures Report 1.5. Available from https://www.legumefutures.eu
Balboa GR, Sadras VO, Ciampitti IA (2018) Shifts in soybean yield, nutrient uptake, and nutrient stoichiometry: a historical synthesis-analysis. Crop Sci 58:43–54. https://doi.org/10.2135/cropsci2017.06.0349
Barbosa JZ, Hungria M, da Silva Sena JV, Poggere G, dos Reis AR, Corrêa RS (2021) Meta-analysis reveals benefits of co-inoculation of soybean with Azospirillum brasilense and Bradyrhizobium spp. in Brazil. Appl Soil Ecol 163:103913
Basigalup D, del Carmen Spada M, Odorizzi A, Arolfo V (2018) Global interaction for alfalfa innovation. Proceedings of the Second World Alfalfa Conference, Cordoba, Argentina. Available from http://www.worldalfalfacongress.org/resumenes.pdf
Bei QC, Liu G, Tang HY, Cadisch G, Rasche F, Xie ZB (2013) Heterotrophic and phototrophic 15N2 fixation and distribution of fixed 15 N in a flooded rice soil system. Soil Biol Biochem 59:25–31
Bender RR, Haegele JW, Below FE (2015) Nutrient uptake, partitioning, and remobilization in modern soybean varieties. Agron J 107(2):563–573
Billen G, Lassaletta L, Garnier J (2014) A biogeochemical view of the global agro-food system: nitrogen flows associated with protein production, consumption and trade. Glob Food Sec 3:209–219. https://doi.org/10.1016/j.gfs.2014.08.003
Boddey RM, Macedo R, Tarré RM, Ferreira E, Oliveira OC, Rezende CP, Cantarutti RB, Pereira JM, Alves BJR, Urquiaga S (2004) Nitrogen cycling in Brachiaria pastures: the key to understanding the process of pasture decline. Agr Ecosyst Environ 103:389–403
Borst HL, Thatcher LE (1931) Life history and composition of the soybean plant. Ohio Agric Exp Stn Bull 494:51–96
Bouwman AF, Beusen AH, Lassaletta L, van Apeldoorn DF, van Grinsven HJ, Zhang J, van Ittersum MK (2017) Lessons from temporal and spatial patterns in global use of N and P fertilizer on cropland. Sci Rep 7(1):40366. https://doi.org/10.1038/srep40366
Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372
Chalk PM (2016) The strategic role of 15 N in quantifying the contribution of endophytic N2 fixation to the N nutrition of non-legumes. Symbiosis 69:63–80
Chalk PM (2020) Whither the enigma of soil nitrogen balance sheets? Plant Soil 456:455–460
Chalk PM, Peoples MB, McNeill AM, Boddey RM, Unkovich MJ, Gardener MJ, Silva CF, Chen DL (2014) Methodologies for estimating nitrogen transfer between legumes and companion species in agro-ecosystems: a review of 15 N-enriched techniques. Soil Biol Biochem 73:10–21
Divito GA, Echeverría HE, Andrade FH, Sadras VO (2016) Soybean shows an attenuated nitrogen dilution curve irrespective of maturity group and sowing date. Field Crop Res 186:1–9
Donahue JM, Bai H, Almtarfi H, Zakeri H, Fritschi FB (2020) The quantity of nitrogen derived from symbiotic N fixation but not the relative contribution of N fixation to total N uptake increased with breeding for greater soybean yields. Field Crop Res 259:107945
Fageria NK, Santos AB (2008) Yield physiology of dry bean. J Plant Nutr 31:983–1004
FAOSTAT (2021a) http://www.fao.org/faostat/en/#data/QC. Accessed Mar 2021
FAOSTAT (2021b) http://www.fao.org/faostat/en/#data/RFN. Accessed Mar 2021
FAOSTAT (2021c) http://www.fao.org/faostat/en/#data/RL. Accessed Apr 2021
Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc B 368:20130164. https://doi.org/10.1098/rstb.2013.0164
Fustec J, Lesuffleur F, Mahieu S, Cliquet J-B (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66
Gan YB, Stulen I, Posthumus F, van Keulen H, Kuiper PJC (2002) Effects of N management on growth, N2 fixation and yield of soybean. Nutr Cycl Agroecosyst 62:163–174
Gardner M, Peoples M, Condon J, Li G, Conyers M, Dear B (2012) Evaluating the importance of a potential source of error when applying shoot 15N labeling techniques to legumes to quantify the below-ground transfer of nitrogen to other species. In: Proceedings of the 16th Australian Agronomy Conference, Armidale, NSW, Australia. https://researchoutput.csu.edu.au/ws/portalfiles/portal/9719030/40605manuscipt.pdf
Gaspar AP, Laboski CAM, Naeve SL, Conley SP (2017) Dry matter and nitrogen uptake, partitioning, and removal across wide range of soybean seed yield levels. Crop Sci 57:2170–2182
Gasser M, Hammelehle A, Oberson A, Frossard E, Mayer J (2015) Quantitative evidence of overestimated rhizodeposition using 15 N leaf-labelling. Soil Biol Biochem 85:10–20
Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CAB International, Wallingford, p 423
Giller KE, Franke AC, Abaidoo R, Baijukya F, Bala A, Boahen S, Dashiell K, Kantengwa S, Sanginga J-M, Sanginga N, Simmons AJ, Turner A, de Wolf J, Woomer P, Vanlauwe B (2013) N2Africa: Putting nitrogen fixation to work for smallholder farmers in Africa. In: Vanlauwe B, van Asten PJA, Blomme G (eds) Agro-ecological intensification of agricultural systems in the African highlands. Routledge, London, pp 156–174
Greenwood DJ, Lemaire G, Gosse G, Cruz P, Draycott A, Neeteson JJ (1990) Decline in percentage N of C3 and C4 crops with increasing plant mass. Ann Bot 66:425–436
Hammond LC, Black CA, Norman AG (1951) Nutrient uptake by soybeans on two Iowa soils. Ohio Agric Exp Stn Bull 384:463–512
Hanway JJ, Weber CR (1971) Dry matter accumulation in soybean (Glycine max (L.) Merrill) plants as influenced by N, P, and K fertilization. Agron J 63,:63–266. https://doi.org/10.2134/agronj1971.00021962006300020020x
Hanway JJ, Weber CR (1971) Accumulation of N, P, and K by soybean (Glycine max (L.) Merrill) Plants. Agron J 63:406–408
Heffer P, Prud’homme M (2016) Global nitrogen fertiliser demand and supply: trend, current level and outlook. Proceedings of the 2016 International Nitrogen Initiative Conference. Solutions to improve nitrogen use efficiency for the world. 4–8 December 2016, Melbourne, Australia. https://www.ini2016.com
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological N2 fixation in agricultural systems. Plant Soil 311:1–18. https://doi.org/10.1007/s11104-008-9668-3
Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331:413–425. https://doi.org/10.1007/s11104-009-0262-0
Hupe A, Schulz H, Bruns C, Joergensen RG, Wichern F (2016) Digging in the dirt – inadequacy of belowground plant biomass quantification. Soil Biol Biochem 96:137–144
IFASTAT (2021) International Fertilizer Association statistics. https://www.ifastat.org/. Accessed Mar 2021
James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crop Res 65:197–209
Janzen HH, Bruinsma Y (1989) Methodology for the quantification of root and rhizosphere nitrogen dynamics by exposure of shoots to 15 N-labelled ammonia. Soil Biol Biochem 21:189–196
Jensen ES (1996) Rhizodeposition of N by pea and barley and its effect on soil N dynamics. Soil Biol Biochem 28:65–71
Jensen ES, Carlsson G, Hauggaard-Nielsen H (2020) Intercropping of grain legumes and cereals improves the use of soil N resources and reduces the requirement for synthetic fertilizer N: a global-scale analysis. Agron Sustain Dev 40 (5). https://doi.org/10.1007/s13593-020-0607-x
Jing MA, Bei QC, Wang XJ, Liu G, Cadisch G, Lin XW, Zhu JG, Sun XO, Xie ZB (2019) Paddy system with a hybrid rice enhances Cyanobacteria Nostoc and increases N2 fixation. Pedosphere 29(3):374–387
Karimi R, Pogue SJ, Kröbel R, Beauchemin KA, Schwinghamer T, Janzen HH (2020) An updated nitrogen budget for Canadian agroecosystems. Agr Ecosyst Environ 304. https://doi.org/10.1016/j.agee.2020.107046
Khan DF, Peoples MB, Chalk PM, Herridge DF (2002) Quantifying below-ground nitrogen of legumes 2. A comparison of 15 N and non isotopic methods. Plant Soil 239:277–289
Khan WDF, Peoples MB, Schwenke GD, Felton WL, Chen D, Herridge D (2003) Effects of below ground nitrogen on N balances of field-grown fababean, chickpea, and barley. Aust J Agric Res 54:333–340
Laberge G, Frank AC, Ambus P, Høgh-Jensen H (2009) Nitrogen rhizodeposition from soybean (Glycine max) and its impact on nutrient budgets in two contrasting environments of the Guinean savannah zone of Nigeria. Nutr Cycl Agroecosyst 84:49–58
Ladha JK, Tirol-Padre A, Reddy CK, Cassman KG, Verma S, Powlson DS, van Kessel C, Richter DdeB, Chakraborty D, Pathak H (2016) Global nitrogen budgets in cereals: a 50-year assessment for maize, rice, and wheat production systems. Sci Rep 6:19355. https://doi.org/10.1038/srep19355
Lassaletta L, Billen G, Grizzetti B, Anglade J, Garnier J (2014) 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environ Res Lett 9:105011
Lassaletta L, Billen G, Grizzetti B, Garnier J, Leach AM, Galloway JN (2014) Food and feed trade as a driver in the global nitrogen cycle: 50-year trends. Biogeochemistry 118(1–3):225–241. https://doi.org/10.1007/s10533-013-9923-4
Lassaletta L, Billen G, Garnier J, Bouwman L, Velazquez E, Mueller ND, Gerber JS (2016) Nitrogen use in the global food system: past trends and future trajectories of agronomic performance, pollution, trade, and dietary demand. Environ Res Lett 11:095007
Lemaire G, Jeuffroy M-H, Gastal F (2008) Diagnosis tool for plant and crop N status in vegetative stage: Theory and practices for crop N management. Eur J Agron 28:614–624
Liu J, Junguo Liu, You L, Amini M, Obersteiner M, Herrero M, Zehnder AJB, Yang H (2010) A high-resolution assessment on global nitrogen flows in cropland. Proc Natl Acad Sci 107(17):8035–8040. https://doi.org/10.1073/pnas.0913658107
López-Bellido L, Benítez-Vega J, García P, Redondo R, López-Bellido RJ (2011) Tillage system effect on nitrogen rhizodeposited by faba bean and chickpea. Field Crop Res 120:189–195
Mahieu S (2009) Assessment of the below ground contribution of field grown pea (Pisum sativum L.) to the soil N pool. Dissertation. Ecole Superieure d’Agriculture d’Angers, Angers
Mahieu S, Fustec J, Faure M-L, Corre-Hellou G, Crozat Y (2007) Comparison of two 15 N labelling methods for assessing nitrogen rhizodeposition of pea. Plant Soil 295:193–205
Mahieu S, Fustec J, Jensen ES, Crozat Y (2009) Does labelling frequency affect N rhizodeposition assessment using the cotton-wick method? Soil Biol Biochem 41:2236–2243
Mayer J, Buegger F, Jensen ES, Schloter M, Heß J (2003) Estimating N rhizodeposition of grain legumes using a 15 N in situ stem labelling method. Soil Biol Biochem 35:21–28
McNeill AM, Fillery IRP (2008) Field measurement of lupin belowground nitrogen accumulation and recovery in the subsequent cereal-soil system in a semi-arid Mediterranean-type climate. Plant Soil 302:297–316
Mogollon JM, Lassaletta L, Beusen AHW, van Grinsven HJM, Westhoek H, Bouwman AF (2018) Assessing future reactive nitrogen inputs into global croplands based on the shared socioeconomic pathways. Environ Res Lett 13:044008. https://doi.org/10.1088/1748-9326/aab212
Ney B, Dore T, Sagan M (1997) Grain Legumes. In: Lemaire G (ed) Diagnosis of the nitrogen status in crops. Springer, Berlin. https://doi.org/10.1007/978-3-642-60684-7_6
Pate JS, Farquhar GD (1988) Role of the crop plant in cycling of nitrogen. In: Wilson JR (ed) ‘Advances in nitrogen cycling in agricultural ecosystems. CAB International, Wales, pp 23–45
Peoples MB, Giller KE, Jensen ES, Herridge DF (2021) Quantifying country-to-global scale nitrogen fixation for grain legumes: I. Reliance on nitrogen fixation of soybean, groundnut and pulses. Plant Soil 469:1–14. https://doi.org/10.1007/s11104-021-05167-6
Phelan P, Moloney AP, McGeough EJ, Humphreys J, Bertilsson J, O’Riordan EG, O’Kiely P (2015) Forage legumes for grazing and conserving in ruminant production systems. Crit Rev Plant Sci 34:281–326. https://doi.org/10.1080/07352689.2014.898455
Poth M, La Favre JS, Focht DD (1986) Quantification by direct 15 N dilution of fixed N2 incorporation in to soil by Cajanus cajan (pigeon pea). Soil Biol Biochem 18:125–127
Rasmussen J, Gylfadóttirc T, Dhalama NR, De Notaris C (2019) Temporal fate of 15 N and 14 C leaf-fed to red and white clover in pure stand or mixture with grass – Implications for estimation of legume derived N in soil and companion species. Soil Biol Biochem 133:60–71
Rausch LL, Gibbs HK, Schelly I, Brandão A, Morton DC, Filho AC, Strassburg B, Walker N, Noojipady P, Barreto P, Meyer D (2019) Soy expansion in Brazil’s Cerrado. Conserv Lett 12:e12671
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512
Rochester IJ, Peoples MB, Constable GA, Gault RR (1998) Faba beans and other legumes add nitrogen to irrigated cotton cropping systems. Aust J Exp Agric 38:253–260
Roger P, Ladha JK (1992) Biological nitrogen fixation in wetland rice fields: estimation and contributions to N balance. Plant Soil 141:41–55
Russell CA, Fillery IRP (1996) In situ 15 N labelling of lupin below-ground biomass. Aust J Agric Res 47:1035–1046
Russell CA, Fillery IRP (1996) Estimates of lupin belowground biomass nitrogen, dry matter, and nitrogen turnover to wheat. Aust J Agric Res 47:1047–1059
Santachiara G, Salvagiotti F, Gerde JA, Rotundo JL (2018) Does biological nitrogen fixation modify soybean nitrogen dilution curves? Field Crop Res 223:171–178
Santos MS, Nogueira MA, Hungria M (2019) Microbial inoculants: reviewing the past and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 9:205. https://doi.org/10.1186/s13568-019-0932-0
Santos MS, Nogueira MA, Hungria M (2021) Outstanding impact of Azospirillum brasilense strains Ab-V5 and Ab-V6 on the Brazilian agriculture: Lessons that farmers are receptive to adopt new microbial inoculants. Rev Bras Cienc Solo 45:e0200128. https://doi.org/10.36783/18069657rbcs20200128
Saxena NP, Sheldrake AR (1980) Physiology of growth, development, and yield of chickpeas in India. Accessed at https://www.researchgate.net/publication/286389111_Physiology_of_growth_development_and_yield_of_chickpeas_in_India
Schapaugh WT, Wilcox JR (1980) Relationships between harvest indices and other plant characteristics in soybeans. Crop Sci 20:529–533
Smil V (1999) Nitrogen in crop production: an account of global flows. Global Biogeochem Cycles 13:647–662
Song X-P, Hansen MC, Potapov P, Adusei B, Pickering J, Adami M, Lima A, Zalles V, Stehman SV, Di Bella CM, Conde MC, Copati EJ, Fernandes LB, Hernandez-Serna A, Jantz SM, Pickens AH, Turubanova S, Tyukavina A (2021) Massive soybean expansion in South America since 2000 and implications for conservation. Nat Sustain. https://doi.org/10.1038/s41893-021-00729-z
Soper FM, Taylor BN, Winbourne JB, Wong MY, Dynarski KA, Reis CRG, Peoples MB, Cleveland CC, Reed SC, Menge DNL, Perakis SS (2021) A roadmap for sampling and scaling biological nitrogen fixation in terrestrial ecosystems. Methods Ecol Evol 00:1–16. https://doi.org/10.1111/2041-210X.13586
Sullivan BW, Smith WK, Townsend AR, Nasto MK, Reed SC, Chazdon RL, Cleveland CC (2014) Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc Natl Acad Sci 111:8101–8106
Unkovich M, Baldock J (2008) Measurement of asymbiotic N2 fixation in Australian agriculture. Soil Biol Biochem 40:2915–2921
Unkovich M, Baldock J, Forbes M (2010) Variability in harvest index of grain crops and potential significance for carbon accounting: examples from Australian agriculture. Adv Agron 105:173–219
Unkovich M, Herridge D, James EK, Giller K, Peoples MB (2020) Reliable quantification of N2 fixation by non-legumes remains problematic. Nutr Cycl Agroecosyst 118:223–225. https://doi.org/10.1007/s10705-020-10083-9
Urquiaga S, Jantalia CP, Zotarelli L, Araujo ES, Alves BJR, Boddey RM, Cabezas WL, Dos Santos HP, Torres E (2006) Nitrogen dynamics in soybean-based crop rotations under conventional and zero tillage in Brazil. Management practices for improving sustainable crop production in tropical acid soils. International Atomic Energy Agency, Vienna, pp 13–46. https://www-pub.iaea.org/MTCD/publications/PDF/Pub1285_web.pdf
Vanlauwe B, Hungria M, Kanampiu F, Giller KE (2019) The role of legumes in the sustainable intensification of African smallholder agriculture: Lessons learnt and challenges for the future. Agric Ecosyst Environ 284:106583
Voisin A, Salon C, Munier-Jolain NG, Ney B (2002) Effect of mineral nitrogen on nitrogen nutrition and biomass partitioning between the shoot and roots of pea (Pisum sativum L.). Plant Soil 242:251–262
Wichern F, Mayer J, Joergensen RG, Muller T (2007) Rhizodeposition of C and N in peas and oats after 13 C–15 N double labelling under field conditions. Soil Biol Biochem 39:2527–2537
Wichern F, Mayer J, Joergensen RG, Muller T (2007) Release of C and N from roots of peas and oats and their availability to soil microorganisms. Soil Biol Biochem 39:2829–2839
Wichern F, Eberhardt E, Mayer J, Joergensen RG, Muller T (2008) Nitrogen rhizodeposition in agricultural crops: methods, estimates and future prospects. Soil Biol Biochem 40:30–48
Yang JY, Drury CF, Yang CF, De Jong XM, Huffman R, Campbell EC, Kirkwood CA (2010) Estimating biological N2 fixation in Canadian agricultural land using legume yields. Agr Ecosyst Environ 137:192–201
Yasmin K, McNeill AM (2002) Influence of water stress on the soil nitrogen balance at harvest following chickpea and grasspea. In 13th Australian Nitrogen Fixation Conference Abstracts. Aust. Soc for Nitrogen Fixation. Adelaide
Yasmin K, Cadisch G, Baggs EM (2010) The significance of belowground fractions when considering N and C partitioning within chickpea (Cicer arietinum L.). Plant Soil 327:247–259
Zang HD, Yang XC, Feng XM, Qian X, Hu YG, Ren CZ, Zeng Z (2015) Rhizodeposition of nitrogen and carbon by mungbean (Vigna radiata L.) and its contribution to intercropped oats (Avena nuda L.). PLoS ONE 10:e0121132
Zang H, Xian Q, Wene, Hu Y, Ren C, Zeng Z, Guo L, Wang C (2018) Contrasting carbon and nitrogen rhizodeposition patterns of soya bean (Glycine max L.) and oat (Avena nuda L.). Eur J Soil Sci. https://doi.org/10.1111/ejss.12556
Zebarth BJ, Alder V, Sheard RW (1991) In situ labelling of legume residues with a foliar application of an N-15 enriched urea solution. Commun Soil Sci Plant Anal 22:437–447
Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature doi. https://doi.org/10.1038/nature15743
Zhang K, Zhao J, Wang X, Xu H, Zang H, Liu J, HU Y, Zeng Z (2019) Estimates on nitrogen uptake in the subsequent wheat by aboveground and root residue and rhizodeposition of using peanut labelled with 15N isotope on the North China Plain. J Integr Agric 18(3):571–579
Zhang X, Davidson EA, Zou T, Lassaletta L, Quan Z, Li T, Zhang W (2020) Quantifying nutrient budgets for sustainable nutrient management. Global Biogeochem Cycles 34:e2018GB006060. https://doi.org/10.1029/2018GB006060
Acknowledgements
We thank Dr Euan James, The James Hutton Institute, Scotland, and Dr Bob Boddey, EMBRAPA, Brazil, for valuable discussion and comments during the course of manuscript preparation. We also gratefully acknowledge the valuable feedback on the manuscript by Dr Murray Unkovich, University of Adelaide, Australia.
Funding
Financial support for a 4-week study visit for MBP from Wageningen University & Research (WUR) is gratefully acknowledged.
Author information
Authors and Affiliations
Contributions
The large dataset was generated by DFH and MBP and analysed by DFH. The manuscript was drafted by DFH. During a 2-year period leading to submission, all authors contributed to regular, extensive discussions about the review and provided critical insights into various aspects of biological N2 fixation. All authors contributed to and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
None.
Ethics approval and consent to participate
Not applicable.
Consent for publication
All authors have agreed on submission of this manuscript to Plant and Soil for publication.
Additional information
Responsible Editor: Alexia Stokes.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 379 KB)
Rights and permissions
About this article
Cite this article
Herridge, D.F., Giller, K.E., Jensen, E.S. et al. Quantifying country-to-global scale nitrogen fixation for grain legumes II. Coefficients, templates and estimates for soybean, groundnut and pulses. Plant Soil 474, 1–15 (2022). https://doi.org/10.1007/s11104-021-05166-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05166-7