Skip to main content
Springer Nature Link
Log in

Quantifying country-to-global scale nitrogen fixation for grain legumes: I. Reliance on nitrogen fixation of soybean, groundnut and pulses

  • Marschner Review
  • Published:
Save article
View saved research
Plant and Soil Aims and scope Submit manuscript

A Correction to this article was published on 23 October 2024

This article has been updated

Abstract

Background

We collated estimates of the percentage of legume N derived from atmospheric N2 (%Ndfa) for 14 major grain legumes and then analysed and aggregated the data to derive average values for different crops and regions/countries. The effects of cultivation year and whether data collected from experimental plots were relevant to crops growing in farmers’ fields were examined.

Scope

A total of 5374 %Ndfa estimates (observations) were sourced, 4205 from field experiments and 1169 on-farm measurements collected from farmer-grown crops. The largest number of reports (82) and %Ndfa estimates (1391) were for soybean.

Conclusions

The %Ndfa estimates for each legume species were consistent across years, except for soybean in North America. For some species estimates were also similar across geographic regions. There were no significant differences (P > 0.05) between estimates of %Ndfa derived from experimental plots and farmer-grown legume crops for nine of the 10 crops evaluated. Three distinct groups were identified with statistically-similar average %Ndfa values with associated standard deviations, namely: pigeonpea, faba bean and lupin – 74±11.8 %; groundnut, green and black gram, cowpea, chickpea, field pea, lentil, vetches and Bambara groundnut – 62±13.4 %; common bean – 38±11.1 %. There were three distinct different regional groupings for soybean: Brazil – 78±6.3 %; North America, Argentina, Asia, Africa and Oceania – 61±14.0 %; Europe – 44±13.8 %. Our findings provide more certainty and simplify the challenge of using field-scale measures of legume %Ndfa to estimate country-to-global inputs of fixed N from grain legumes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Change history

Abbreviations

N2 :

Dinitrogen

N:

Nitrogen

%Ndfa:

Percentage of the legume N derived from atmospheric N2

References

  • Akter Z, Pageni BB, Lupwayi NZ, Balasubramanian PM (2018) Biological nitrogen fixation by irrigated dry bean (Phaseolus vulgaris L.) genotypes. Can J Plant Sci 98:1159–1167

    Article  CAS  Google Scholar 

  • Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9

    Article  CAS  Google Scholar 

  • 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):37

    Article  Google Scholar 

  • Bell MJ, Wright GC, Suryantini, Peoples MB (1994) The N2-fixing capacity of peanut cultivars with differing assimilate partitioning characteristics. Aust J Agric Res 45:1455–1468

    Article  Google Scholar 

  • Beshir HM, Walley FL, Bueckert R, Tar’an B (2015) Response of snap bean cultivars to rhizobium inoculation under dryland agriculture in Ethiopia. Agronomy 5:291–308

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boddey RM, Urquiaga S, Neves MCP (1990) Quantification of the contribution of N2 fixation to field-grown grain legumes - A strategy for the practical application of the 15N isotope dilution technique. Soil Biol Biochem 22:649–655

    Article  CAS  Google Scholar 

  • Cao PC, Lu C, Yu Z (2018) Historical nitrogen fertilizer use in agricultural ecosystems of the contiguous United States during 1850–2015: application rate, time, and fertilizer types. Earth Syst Sci Data 10:969–984

    Article  Google Scholar 

  • Cernay C, Pelzer E, Makowski D (2016) A global experimental dataset for assessing grain legume production. Sci Data 3:160084. https://doi.org/10.1038/sdata.2016.84

  • Chalk PM (1985) Estimation of N2 fixation by isotope dilution: an appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 17:389–410

    Article  CAS  Google Scholar 

  • Chalk PM, Craswell ET (2018) An overview of the role and significance of 15N methodologies in quantifying biological N2 fixation (BNF) and BNF dynamics in agro-ecosystems. Symbiosis 75:1–16

    Article  CAS  Google Scholar 

  • Ciampitti IA, Salvagiotti F (2018) New insights into soybean biological nitrogen fixation. Agron J 110:1185–1196

    Article  CAS  Google Scholar 

  • Collino DJ, Salvagiotti F, Perticari A, Piccinetti C, Ovando G, Urquiaga S, Racca RW (2015) Biological nitrogen fixation in soybean in Argentina: relationships with crop, soil, and meterological factors. Plant Soil 392:239–252

    Article  CAS  Google Scholar 

  • Donahue JM, Bai H, Almtarfi H, Zakeri, Fritschi FB (2020) The quantity of nitrogen derived from symbiotic N fixation but not the relative contribution of N fixation to the total N uptake increased with breeding for greater soybean yields. Field Crop Res 259:107945

    Article  Google Scholar 

  • Egli DB (2008) Comparison of corn and soybean yields in the United States: historical trends and future prospects. Agron J 100(S3):S79–S88

    Article  Google Scholar 

  • Espinoza S, Ovalle C, Zagal E, Matus I, Tay J, Peoples MB, del Pozo A (2012) Contribution of legumes to wheat productivity in Mediterranean environments of central Chile. Field Crop Res 13:150–159

    Article  Google Scholar 

  • Evans J, McNeill AM, Unkovich MJ, Fettell NA, Heenan DP (2001) Net nitrogen balances for cool-season grain legumes crops and contribution to wheat nitrogen uptake: a review. Aust J Agric Res 41:347–359

    Article  CAS  Google Scholar 

  • FAOSTAT (2021) FAO Crop statistics. http://www.fao.org/faostat/en/#data/QC/visualize/. Accessed Feb 2021

  • Gan Y, 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

    Article  CAS  Google Scholar 

  • George T, Singleton PW (1992) Nitrogen assimilation traits and dinitrogen fixation in soybean and common bean. Agron J 84:1020–1028

    Article  CAS  Google Scholar 

  • Giller KE (1990) Assessment and improvement of nitrogen fixation in tropical Phaseolus vulgaris L. Soil Use Manag 6:82–84

    Article  Google Scholar 

  • Giller KE (2001) Nitrogen fixation in tropical cropping systems. CAB International, Wallingford, p 423

    Book  Google Scholar 

  • Giller KE, Nambiar PTC, Srinivasa Rao B, Dart PJ, Day JM (1987) A comparison of nitrogen fixation in genotypes of groundnut (Arachis hypogaea L.) using 15N-isotope dilution. Biol Fertil Soils 5:23–25

    Article  Google Scholar 

  • Graham PH (1981) Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: A review. Field Crop Res 4:93–112

    Article  Google Scholar 

  • Guffy RD, Vanden Heuvel RM, Vasilas BL, Nelson RL, Frobish MA, Hesketh JD (1989) Evaluation of the N2-fixation capacity of four soybean genotypes by several methods. Soil Biol Biochem 21:339–342

    Article  Google Scholar 

  • Guinet M, Nicolardot B, Revellin C, Durey V, Carlsson G, Voisin AS (2018) Comparative effects of inorganic N on plant growth and N2 fixation of ten legume crops: towards a better understanding of the differential response among species. Plant Soil 432:207–227

    Article  CAS  Google Scholar 

  • Habinshuti SJ, Maseko ST, Dakora FD (2021) Inhibition of N2 fixation by N fertilization of common bean (Phaseolus vulgaris L.) plants grown on farmers’ fields in the Eastern Cape of South Africa, measured using 15N natural abundance and tissue ureide analysis. Front Agron. https://doi.org/10.3389/fagro.2021.692933

    Article  Google Scholar 

  • Ham GE, Caldwell AC (1978) Fertilizer placements effects on soybean seed yield, N2 fixation, and 32P uptake. Agron J 70:779–783

    Article  CAS  Google Scholar 

  • Hauggaard-Nielsen H, Holdensen L, Wulfsohn D, Jensen ES (2010) Spatial variation of N2-fixation in field pea (Pisum sativum L.) at the field scale determined by the 15N natural abundance method. Plant Soil 327:167–184

    Article  CAS  Google Scholar 

  • Herridge DF, Peoples MB (2002) Timing of xylem sampling for ureide analysis of nitrogen fixation. Plant Soil 238:57–67

    Article  CAS  Google Scholar 

  • Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using ureide and natural 15N abundance methods. Plant Physiol 93:708–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB (1995) Chickpea increases soil-N fertility in cereal systems through nitrate sparing and N2 fixation. Soil Biol Biochem 27:545–551

    Article  CAS  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • Herridge DF, Giller KE, Jensen ES, Peoples MB (2021) Quantifying country-to-global scale nitrogen fixation for crop legumes. II. Coefficients, templates and estimates for soybean, groundnut and pulses. Plant Soil (in Press)

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crop Res 65:151–164

    Article  Google Scholar 

  • Hungria M, Franchini JC, Campo RJ, Crispino CC, Moraes JZ, Sibaldelli RNR, Mendes IC, Arihara J (2006) Nitrogen nutrition of soybean in Brazil: Contributions of biological N2 fixation and N fertilizer to grain yield. Can J Plant Sci 86:927–939

    Article  Google Scholar 

  • Jensen ES (1986) Symbiotic N2 fixation in pea and field pea estimated by 15N fertilizer dilution in field experiments with barley as a reference crop. Plant Soil 92:3–13

    Article  CAS  Google Scholar 

  • Jensen ES, Peoples MB, Hauggaard-Nielsen H (2010) Faba bean in cropping systems. Field Crop Res 115:203–216

    Article  Google Scholar 

  • Karimi R, Pogue SJ, Kröbel R, Beauchemin KA, Schwinghamer T, Janzen HH (2020) An updated nitrogen budget for Canadian agroecosystems. Agric Ecosyst Environ 304:107046

    Article  CAS  Google Scholar 

  • Kipe-Nolt JA, Giller KE (1993) A field evaluation using the 15N isotope dilution method of lines of Phaseolus vulgaris L. bred for increased nitrogen fixation. Plant Soil 152:107–114

    Article  Google Scholar 

  • Kohl DH, Shearer G, Harper JE (1980) Estimates of N2 fixation based on differences in the natural abundance of 15N in nodulating and nonnodulating isolines of soybeans. Plant Physiol 66:61–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lupwayi NZ, Soon YK (2015) Carbon and nitrogen release from legume crop residues for three subsequent crops. Soil Sci Soc Am J 79:1650–1659

    Article  CAS  Google Scholar 

  • Maskey SL, Bhattarai S, Peoples MB, Herridge DF (2001) On-farm measurements of nitrogen fixation by winter and summer legumes in the Hills and Terai regions of Nepal. Field Crop Res 70:209–221

    Article  Google Scholar 

  • Naab JB, Chimphango SBM, Dakora FD (2009) N2 fixation in cowpea plants grown in farmers’ fields in the Upper West Region of Ghana, measured using 15N natural abundance. Symbiosis 48:37–46

    Article  CAS  Google Scholar 

  • Peoples MB, Gault RR, Lean B, Sykes JD, Brockwell J (1995) Nitrogen fixation by soybean in commercial irrigated crops of central and southern New South Wales. Soil Biol Biochem 27:553–561

    Article  CAS  Google Scholar 

  • Peoples MB, Ladha JK, Herridge DF (1995) Enhancing legume N2 fixation through plant and soil management. Plant Soil 174:83–101

    Article  CAS  Google Scholar 

  • Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rekasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009a) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17

    Article  CAS  Google Scholar 

  • Peoples MB, Unkovich MJ, Herridge DF (2009b) Measuring symbiotic nitrogen fixation by legumes. In: Emerich DW, Krishnan HB (eds) Nitrogen fixation in crop production, Agronomy monograph 52. American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America Madison, Wisconsin, pp 125–170

    Google Scholar 

  • Peoples MB, Swan AD, Goward L, Kirkegaard JA, Hunt JR, Li GD, Schwenke GD, Herridge DF, Moodie M, Wilhelm N, Potter T, Denton MD, Browne C, Phillips LA, Khan DF (2017) Soil mineral nitrogen benefits derived from legumes and comparisons of the apparent recovery of legume or fertiliser nitrogen by wheat. Soil Res 55:600–615

    Article  CAS  Google Scholar 

  • Rawal V, Navarro DK (2019) The global economy of pulses. FAO, Rome. 174 pp. http://www.fao.org/publications/card/en/c/I7108EN/. Accessed May 2021

  • Redden RJ, Herridge DF (1999) Evaluation of genotypes of navy and culinary bean (Phaseolus vulgaris L.) selected for superior growth and nitrogen fixation. Aust J Exp Agric 39:975–980

    Article  Google Scholar 

  • Reinprecht Y, Schram L, Marsolais F, Smith TH, Hill B, Pauls KP (2020) Effects of nitrogen application on nitrogen fixation in common bean production. Front Plant Sci 11:1172

    Article  Google Scholar 

  • Rennie RJ (1984) Comparison of N balance and 15N isotope dilution to quantify N2 fixation in field-grown legumes. Agron J 76:786–790

    Article  Google Scholar 

  • Ruiz Sainz JE, Zhou JC, Rodriguez-Navarro DN, Vinardell JM, Thomas-Oates JE (2005) Soybean cultivation and BNF in China. In: Werner D, Newton WE (eds) Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment. Springer, Dordrecht, pp 67–87

    Chapter  Google Scholar 

  • Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer in soybeans: A review. Field Crop Res 108:1–13

    Article  Google Scholar 

  • Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: A meta-analysis. Field Crop Res 240:106–115

    Article  Google Scholar 

  • Schipanski ME, Drinkwater E, Russelle MP (2010) Understanding the variability in soybean nitrogen fixation across agroecosystems. Plant Soil 329:379–397

    Article  CAS  Google Scholar 

  • Schwenke GD, Peoples MB, Turner GL, Herridge DF (1998) Does nitrogen fixation of commercial dryland chickpea and faba bean crops in north-west New South Wales maintain or enrich soil nitrogen? Aust J Exp Agric 38:61–70

    Article  Google Scholar 

  • Tamagno S, Balboa GR, Assefa Y, Kovács P, Casteel SN, Salvagiotti F (2018) Nutrient partitioning and stoichiometry in soybean: A synthesis-analysis. Field Crop Res 200:18–27

    Article  Google Scholar 

  • Torabian S, Farhangi-Abriz S, Denton MD (2019) Do tillage systems influence nitrogen fixation in legumes? A review. Soil Tillage Res 185:113–121

    Article  Google Scholar 

  • Unkovich MJ, Pate JS (2000) An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crop Res 65:211–228

    Article  Google Scholar 

  • Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems, ACIAR Monograph 136, Australian Centre for International Agricultural Research, Canberra, 258 pp

  • Unkovich MJ, Baldock J, Peoples MB (2010) Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes. Plant Soil 329:75–89

    Article  CAS  Google Scholar 

  • USDA (2020) Fertilizer use and price. https://www.ers.usda.gov/data-products/fertilizer-use-and-price/ Accessed April 2021

  • van Kessel C, Hartley C (2000) Agricultural management of grain legumes: has it led to an increase in nitrogen fixation? Field Crop Res 65:165–181

    Article  Google Scholar 

  • 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. https://doi.org/10.1016/j.agee.2019.106583

  • Voisin A-S, Salon C, Munier-Jolain NG, Ney B (2002) Quantitative effects of soil nitrate, growth potential and phenology on symbiotic nitrogen fixation of pea (Pisum sativum L.). Plant Soil 243:31–42

    Article  CAS  Google Scholar 

  • Walley FL, Clayton GW, Miller PR, Carr PM, Lafond GP (2007) Nitrogen economy of pulse crop production in the Northern Great Plains. Agron J 99:1710–1718

    Article  CAS  Google Scholar 

  • Weber CR (1966) Nodulating and nonnodulating soybean isolines: II. Response to applied nitrogen and modified soil conditions. Agron J 58:46–49

    Article  CAS  Google Scholar 

  • Wilker J, Humphries S, Rosas-Sotomayor JC, Cerna MG, Torkameaneh D, Edwards M, Navabi A, Pauls KP (2020) Genetic diversity, nitrogen fixation, and water use efficiency in a panel of Honduran common bean (Phaseolus vulgaris L.) landraces and modern genotypes. Plants 9:1238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wortmann CS, Lunze L, Ochwoh VA, Lynch J (1995) Bean improvement for low fertility soils in Africa. Afr Crop Sci J 3:469–477

    Google Scholar 

  • 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

  • Zheng M, Zhou Z, Luo Y, Zhao P, Mo J (2019) Global pattern and controls of biological nitrogen fixation under enrichment: A meta-analysis. Glob Change Biol 25:3018–3303

    Article  Google Scholar 

  • Zou W (2020) Northeast institute of geography and agroecology. Chinese Academy of Sciences, Harbin

Download references

Acknowledgements

Dr Mark Peoples is indebted to the Production Ecology & Resource Conservation Graduate School of Wageningen University, the Netherlands for financial support for a four-week study visit in 2019 which was responsible for the genesis of this publication. We gratefully acknowledge the contributions of discussions held with Dr Robert Boddey, Embrapa Agrobiologia, Seropédica, Brazil and Dr Murray Unkovich, University of Adelaide, Australia to the manuscript’s development.

Funding

Support to initiate the current publication was provided by Wageningen University, the Netherlands and CSIRO, Australia.

Author information

Authors and Affiliations

  1. CSIRO Agriculture and Food, GPO Box 1700, Canberra, ACT, 2601, Australia

    Mark B. Peoples

  2. Plant Production Systems, Wageningen University & Research, PO Box 430, 6700AK, Wageningen, The Netherlands

    Ken E. Giller

  3. Department of Biosystems and Technology, Swedish University of Agricultural Sciences, PO Box 103, SE-230 53, Alnarp, Sweden

    Erik S. Jensen

  4. School of Environmental and Rural Science, University of New England, 2351, Armidale, NSW, Australia

    David F. Herridge

Authors
  1. Mark B. Peoples
    View author publications

    Search author on:PubMed Google Scholar

  2. Ken E. Giller
    View author publications

    Search author on:PubMed Google Scholar

  3. Erik S. Jensen
    View author publications

    Search author on:PubMed Google Scholar

  4. David F. Herridge
    View author publications

    Search author on:PubMed Google Scholar

Contributions

The large dataset was generated and analysed by MBP and DFH. The manuscript was drafted by MBP. 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 read and approved the final manuscript.

Corresponding author

Correspondence to Mark B. Peoples.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for participate

Not applicable.

Consent for publication

All authors have agreed on submission of this manuscript to Plant and Soil for publication.

Conflict of interest/competing interests

None to declare.

Additional information

Responsible Editor: Alexia Stokes.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: The equation in Figure 3 caption was corrected.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peoples, M.B., Giller, K.E., Jensen, E.S. et al. 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 (2021). https://doi.org/10.1007/s11104-021-05167-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1007/s11104-021-05167-6

Keywords

Profiles

  1. Ken E. Giller View author profile