Skip to main content
SpringerLink
Log in

Plant-mediated rhizospheric interactions in maize-pigeon pea intercropping enhance soil aggregation and organic phosphorus storage

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

In Malawi, strategies are being sought to boost maize production through improvements in soil fertility. This study assessed the impact of intercropping maize (Zea mays) with pigeon pea (Cajanus cajan) in Lixisols of Malawi on yield, biological N fixation, soil aggregation, and P forms within soil aggregates.

Methods

Maize and pigeon pea were grown intercropped in pots, with varying degrees of root interaction in order to understand the relative importance of biochemical versus physical rhizospheric interactions. Following harvest, soils were separated into aggregate fractions using wet-sieving, and the nutrient content of all fractions was assessed.

Results

The proportion of macroaggregates and microaggregates increased by 52 and 111%, respectively, in the intercropping treatment compared to sole maize, which significantly increased organic P storage in the microaggregates of intercropped compared to sole maize (84 versus 29 mg P kg−1, respectively). Biologically fixed N increased from 89% in the sole pigeon pea to 96% in the intercropped system.

Conclusions

Intercropping maize with pigeon pea can have a significant and positive impact on soil structure as well as nutrient storage in these high P-sorbing soils. This is caused primarily by physical root contact and to a lesser degree by biochemical activities.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Adu-Gyamfi JJ, Fujita K, Ogata S (1989) Phosphorus absorption and utilization efficiency of pigeon pea (Cajanus cajan (L) Millsp.) in relation to dry matter production and dinitrogen fixation. Plant Soil 119:315–324

    Article  CAS  Google Scholar 

  • Adu-Gyamfi JJ, Myaka FA, Sakala WD, Odgaard R, Vesterager JM, Høgh-Jensen H (2007) Biological nitrogen fixation and nitrogen and phosphorus budgets in farmer-managed intercrops of maize-pigeonpea in semi-arid southern and eastern Africa. Plant Soil 295:127–136

    Article  CAS  Google Scholar 

  • Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Am Assoc Adv Sci Pub 248:477–480

    CAS  Google Scholar 

  • Ae N, Arihara J, Okada K, Yoshihara T, Otani T, Johansen C (1993) The role of piscidic acid secreted by pigeonpea roots grown in an Alfisol with low-P fertility. Genetic aspects of plant mineral nutrition. Springer, Netherland, pp. 279–288

    Google Scholar 

  • Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility. A handbook of methods. CAB International, Wallingford, Oxon

    Google Scholar 

  • Ascencio J (1996) Growth strategies and utilization of phosphorus in Cajanus cajan L. Millsp. And Desmodium tortuosum (Sw.) DC under phosphorus deficiency. Commun Soil Sci Plan 27(5–8):1971–1993

    Article  CAS  Google Scholar 

  • Ayaga G, Todd A, Brookes PC (2006) Enhanced biological cycling of phosphorous increases its availability to crops in low-input sub-Saharan farming systems. Soil Biol Biochem 38:81–90

    Article  CAS  Google Scholar 

  • Bekunda M, Sanginga N, Woomer PL (2010) Restoring soil fertility in sub-Sahara Africa. Adv Agron 108:183–286

    Article  Google Scholar 

  • Bezner-Kerr R, Snapp S, Chirwa M, Shumba L, Msachi R (2007) Participatory research on legume diversification with Malawian smallholder farmers for improved human nutrition and soil fertility. Exp Agric 43(4):437–453

    Google Scholar 

  • Bowman RA, Moir JO (1993) Basic EDTA as an extractant for soil organic phosphorus. Soil Sci Soc Am J 57:1516–1518

    Article  CAS  Google Scholar 

  • Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22

    Article  CAS  Google Scholar 

  • Bünemann EK, Smithson PC, Jama B, Frossard E, Oberson A (2004) Maize productivity and nutrient dynamics in maize-fallow rotations in western Kenya. Plant Soil 264:195–208

    Article  Google Scholar 

  • Cambardella CA, Elliott ET (1993) Carbon and nitrogen distribution in aggregates from cultivated and native grassland soils. Soil Sci Soc Am J 57:1071–1076

    Article  CAS  Google Scholar 

  • Cornell RM, Schwertmann U (2003) The iron oxides: structure, properties, reactions, occurrences, and uses. Wiley-VCH Berlag GmbH & Co. KGaA, Weinheim, pp. 1–646

    Book  Google Scholar 

  • Degens BP (1997) Macro-aggregation of soils by biological bonding and binding mechanisms and the factors affecting these: a review. Aust J Soil Res 35:431–459

    Article  Google Scholar 

  • De Gryze S, Six J, Brits C, Merckx R (2005) A quantification of short-term macroaggregate dynamics: influences of wheat residue input and texture. Soil Biol Biochem 37(1):55–66

    Article  CAS  Google Scholar 

  • Dick RP (1992) A review: long-term effects of agricultural systems on soil biochemical and microbial parameters. Agric Ecosyst Environ 40:25–36

    Article  CAS  Google Scholar 

  • FAO STAT (2014). Maize yields across Malawi. http://faostat3.fao.org/browse/Q/QC/E. Accessed 24 May 2016

  • Fonte SJ, Nesper M, Hegglin D, Velásquez JE, Ramirez B, Rao IM, Bernasconi SM, Bünemann EK, Frossard E, Oberson A (2014) Pasture degradation impacts soil phosphorus storage via changes to aggregate-associated soil organic matter in highly weathered tropical soils. Soil Biol Biochem 68:150–157

    Article  CAS  Google Scholar 

  • Fustec J, Lesuffleur F, Mahieu S, Cliquet JB (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66

    Article  CAS  Google Scholar 

  • Garland G, Bünemann E, Six J (2016) New soil aggregate fractionation methodology to understand phosphorus transformations in iron oxide-rich tropical agricultural soils. Eur J Soil Sci. doi:10.1111/ejss.12396

    Google Scholar 

  • Gathumbi SM, Cadisch G, Giller KE (2002) 15N natural abundance as a tool for assessing N2-fixation of herbaceous, shrub, and tree legumes in improved fallows. Soil Biol Biochem 34:1059–1071

    Article  CAS  Google Scholar 

  • Gaume A, Mächler F, De León C, Narro L, Frossard E (2001) Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228:253–264

    Article  CAS  Google Scholar 

  • George TS, Gregory PJ, Robinson JS, Buresh RJ (2002) Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant Soil 246:65–73

    Article  CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource- soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture plants without soil. Univ calif Agric Exp Stn Berkeley. Circular 347:1–39

    Google Scholar 

  • Hochholdinger F (2009) The maize root system: morphology, anatomy, and genetics. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its bioogy. Sprint Science and Business Media, LLC, p 145–160

  • Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling, Soil Biology, vol 26. Springer, Heidelberg

    Chapter  Google Scholar 

  • Jastrow JD, Miller RM, Lussenhop J (1998) Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30(7):905–916

    Article  CAS  Google Scholar 

  • Katayama K, Ito O, Matsunaga R, Adu-Gyamfi JJ, Rao TP, Anders MM, Lee KK (1995) Nitrogen balance and root behavior in four pigeon pea-based intercropping systems. Fert Res 42:315–319

    Article  CAS  Google Scholar 

  • Kuono K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:1353–1357

    Article  Google Scholar 

  • Lal R (2006) Enhancing crop yields in the developing countries through restoration of the soil organic carbon pool in agricultural lands. Land Degrad Dev 17:197–209

    Article  Google Scholar 

  • Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot 94:297–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. PNAS 104(27):11192–11196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Shen J, Zhang F, Clairotte M, Drevon JJ, Le Cadre E, Hinsinger P (2008) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Tricum turgidum durum L.) grown in monocropping and intercropping systems. Plant Soil 213:139–150

    Article  Google Scholar 

  • Makumba W, Akinnifesi FK, Janssen BH (2009) Spatial rooting patterns of gliricidia, pigeon pea and maize intercrops and effect on profile soil N and P distribution in southern Malawi. Afr J Agric Res 4(4):278–288

    Google Scholar 

  • Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Alston AM, Martin JK (1986) Measurement of phosphorus in the soil microbial biomass: a modified procedure for field soils. Soil Biol Biochem 18:437–443

    Article  CAS  Google Scholar 

  • Mhango WG, Snapp SS, Phiri GYK (2012) Opportunities and constraints to legume diversification for sustainable maize production on smallholder farms in Malawi. Renew Agr Food Syst 28(3):234–244

    Article  Google Scholar 

  • Mummey DL, Holben WE, Six J, Stahl PD (2006) Spatial stratification of soil microbial populations in diverse soils: Rubrobacteria and gemmatimonads are abundant in water-stable microaggregate interiors while acidobacteria are primarily associated with macroaggregates. Microb Ecol 51:404–411

    Article  PubMed  Google Scholar 

  • Myaka FM, Sakala WD, Adu-Gyamfi JJ, Kamalongo D, Ngwira A, Odgaard R, Nielsen NE, Høgh-Jensen H (2006) Yields and accumulations of N and P in farmer-managed intercrops of maize-pigeonpea in semi-arid Africa. Plant Soil 285:207–220

    Article  CAS  Google Scholar 

  • Nesper M, Bünemann EK, Fonte SJ, Rao IM, Velásquez JE, Ramirez B, Hegglin D, Frossard E, Oberson A (2015) Pasture degradation decreases organic P content of tropical soils due to soil structural decline. Geoderma 257-258:123–133

    Article  CAS  Google Scholar 

  • Ngwira AR, Kabambe VH, Kambauwa G, Mhango WG, Mwale CD, Chimphero L, Chimbizi A, Mapfumo P (2012) Scaling out best fit legume technologies for soil fertility enhancement among smallholder farmers in Malawi. Afr J Agric Res 7(6):918–928

    Article  Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120

    Article  CAS  Google Scholar 

  • Oades JM, Waters AG (1991) Aggregate hierarchy in soils. Aust J Soil Res 29:815–828

    Article  Google Scholar 

  • Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin D (eds) Organic phosphorus in the environment. CABI, Wallingord, Oxon, pp. 133–164

    Chapter  Google Scholar 

  • Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an Oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210

    Article  CAS  Google Scholar 

  • Oberson A, Pypers P, Bünemann EK, Frossard E (2011) Management impacts on biological phosphorus cycling in cropped soils. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling, Soil Biology, vol 26. Springer, Heidelberg, pp. 431–458

    Chapter  Google Scholar 

  • Odeny DA (2007) The potential of pigeonpea (Cajanus cajan (L.) Millsp.) in Africa. Nat Resour Forum 31:297–305

    Article  Google Scholar 

  • Ohno R, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Am J 55:892–895

    Article  CAS  Google Scholar 

  • Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:3–28

    Article  CAS  Google Scholar 

  • Phiri AT, Msaky JJ, Mrema J, Kanyama-Phiri GY, Harawa R (2013) Assessment of nutrient and biomass yield of medium and long duration pigeon pea in a pigeon pea-groundnut intercropping system in Malawi. J Sust Soc 2(1):36–48

    Google Scholar 

  • Poll C, Ingwersen J, Stemmer M, Gerzabek MH, Kandeler E (2006) Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57:583–595

    Article  Google Scholar 

  • Raghothama K (2005) Phosphorus and plant nutrition: an overview. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America. Madison, WI, USA. Phosphorus: Agriculture and the Environment, Agronomy Monograph no. 46, p 355–378

  • Ranjard L, Richaume A (2001) Quantitative and qualitative microscale distribution of bacteria in soil. Res Microbiol 152:707–716

    Article  CAS  PubMed  Google Scholar 

  • Sainju UM, Terrill TH, Gelaye S, Singh BP (2003) Soil aggregation and carbon and nitrogen pools under rhizoma peanut and perennial weeds. Soil Sci Soc Am J 67:146–155

    Article  CAS  Google Scholar 

  • Sanchez PA (2002) Soil fertility and hunger in Africa. Science 295:2019–2020

    Article  CAS  PubMed  Google Scholar 

  • Shearer G, Kohl DH (1986) N2 fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756

    CAS  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120

    Article  CAS  Google Scholar 

  • Sinaj S, Frossard E, Fardeau JC (1997) Isotopically exchangeable phosphate in size fractionated and unfractionated soils. Soil Sci Soc Am J 61:1413–1417

    Article  CAS  Google Scholar 

  • Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–1377

    Article  CAS  Google Scholar 

  • Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103

    Article  CAS  Google Scholar 

  • Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31

    Article  Google Scholar 

  • Tang C, Unkovich MJ, Bowden JW (1999) Factors affecting soil acidification under legumes. III. Acid production by N2-fixing legumes as influenced by nitrate supply. New Phytol 143:513–521

    Article  CAS  Google Scholar 

  • Tiessen H, Frossard E, Mermut AR, Nyamekye AL (1991) Phosphorus sorption and properties of ferruginous nodules from semiarid soils from Ghana and Brazil. Geoderma 48:373–389

    Article  CAS  Google Scholar 

  • Tobita S, Ito O, Matsunaga R, Tao TP, Rego TJ, Johansen C, Yoneyama T (1994) Field evaluation of nitrogen fixation and use of nitrogen fertilizer by sorghum/pigeon pea intercropping on an Alfisol in the Indian semi-arid tropics. Biol Fertil Soils 17:241–248

    Article  Google Scholar 

  • Traore O, Groleau-Renaud V, Plantureux S, Tubeileh A, Bœuf-Tremblay V (2000) Effect of root mucilage and modeled root exudates on soil structure. Eur J Soil Sci 51:575–581

    Article  Google Scholar 

  • Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey R, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. ACIAR Monograph No. 136, pp 1–258

  • van Bavel CHM (1950) Mean weight-diameter of soil aggregates as a statistical index of aggregation. Soil Sci Soc Am Proc 14:20–23

    Article  Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochem 37:63–75

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Sieglinde Snapp, Dr. Regis Chikowo and Betserai Isaac Nyoka for help with obtaining the soil for the greenhouse trial, Dr. Federica Tamburini for help with the mass spectrometer measurements, as well as Silvan Strebel and Dr. Ping Huang for help with laboratory analyses.

Author information

Authors and Affiliations

  1. Department of Environmental Systems Science, Group of Sustainable Agroecosystems, Swiss Federal Institute of Technology, ETH Zurich, CH-8092, Zurich, Switzerland

    Gina Garland & J. Six

  2. Department of Environmental Systems Science, Group of Plant Nutrition, Swiss Federal Institute of Technology, ETH Zurich, CH-8315, Lindau, Switzerland

    E. K. Bünemann, A. Oberson & E. Frossard

  3. Research Institute of Organic Agriculture (FiBL), CH-5070, Frick, Ackerstrasse, Switzerland

    E. K. Bünemann

Authors
  1. Gina Garland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. K. Bünemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Oberson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Frossard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Six
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gina Garland.

Additional information

Responsible Editor: Ellis Hoffland.

Electronic supplementary material

Appendix Table 1

Description of nutrient solution added to greenhouse pots modified from Hoagland and Arnon (1950). The element added is the total amount added over course of the trial, which was split into four applications during the growing season (DOCX 41 kb)

Appendix Table 2

Recovery for all C, N, and P pools from the soil aggregate fractions relative to bulk soil measurements. Values presented are the average (n = 3) with standard deviation in parentheses (DOCX 119 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garland, G., Bünemann, E.K., Oberson, A. et al. Plant-mediated rhizospheric interactions in maize-pigeon pea intercropping enhance soil aggregation and organic phosphorus storage. Plant Soil 415, 37–55 (2017). https://doi.org/10.1007/s11104-016-3145-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3145-1

Keywords

Search

Navigation