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Endogeic earthworms modify soil phosphorus, plant growth and interactions in a legume–cereal intercrop

Abstract

Background and aims

Intercropping of legumes and cereals appears as an alternative agricultural practice to decrease the use of chemical fertilizers while maintaining high yields. A better understanding of the biotic and abiotic factors determining interactions between plants in such associations is required. Our study aimed to analyse the effect of earthworms on the legume–cereal interactions with a focus on the modifications induced by earthworms on the forms of soil phosphorus (P).

Methods

In a glasshouse experiment we investigated the effect of an endogeic earthworm (Allolobophora chlorotica) on the plant biomass and on N and P acquisition by durum wheat (Triticum turgidum durum L.) and chickpea (Cicer arietinum L.) either grown alone or intercropped. The modifications of the different organic and inorganic P forms in the bulk soil were measured.

Results

There was no overyielding of the intercrop in the absence of earthworms. Earthworms had a strong influence on biomass and resource allocation between roots and shoots whereas no modification was observed in terms of total biomass production and P acquisition. Earthworms changed the interaction between the intercropped species mainly by reducing the competition for nutrients. Facilitation (positive plant–plant interactions) was only observed for the root biomass and P acquisition in the presence of earthworms. Earthworms decreased the amount of organic P extracted with NaOH (Po NaOH), while they increased the water soluble inorganic P (Pi H2O) content.

Conclusions

In this experiment, earthworms could be seen as “troubleshooter” in plant–plant interaction as they reduced the competition between the intercropped species. Our study brings new insights into how earthworms affect plant growth and the P cycle.

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References

  1. Aikio S, Markkola AM (2002) Optimality and phenotypic plasticity of shoot-to-root ratio under variable light and nutrient availabilities. Evol Ecol 16:67–76

    Article  Google Scholar 

  2. Ali MA, Louche J, Legname E, Duchemin M, Plassard C (2009) Pinus pinaster seedlings and their fungal symbionts show high plasticity in phosphorus acquisition in acidic soils. Tree Physiol 29:1587–1597

    PubMed  Article  CAS  Google Scholar 

  3. Altieri MA, Nicholls CI (2005) Agroecology and the search for a truly sustainable agriculture. United Nations Environment Programme, Environmental Training Network for Latin America and the Caribbean, Mexico, 290 pages

    Google Scholar 

  4. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686

    Article  Google Scholar 

  5. Bedoussac L, Justes E (2010) The efficiency of a durum wheat–winter pea intercrop to improve yield and wheat grain protein concentration depends on N availability during early growth. Plant Soil 330:19–35

    Article  CAS  Google Scholar 

  6. Bennett AJ, Bending GD, Chandler D, Hilton S, Mills P (2012) Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biol Rev 87:52–71

    PubMed  Article  Google Scholar 

  7. Bernard L, Chapuis-Lardy L, Razafimbelo T et al (2012) Endogeic earthworms shape bacterial functional communities and affect organic matter mineralization in a tropical soil. ISME J 6:213–222

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  8. Bertness M, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    PubMed  Article  CAS  Google Scholar 

  9. Betencourt E, Duputel M, Colomb B, Desclaux D, Hinsinger P (2012) Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in a low P soil. Soil Biol Biochem 46:181–190

    Article  CAS  Google Scholar 

  10. Blanchart E, Albrecht A, Alegre J et al (1999) Effects of earthworms on soil structure and physical properties. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CABI, Wallingford, pp 149–172

    Google Scholar 

  11. Blouin M, Hodson ME, Delgado EA et al (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182

    Article  Google Scholar 

  12. Bommarco R, Kleijn D, Potts SG (2012) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238

    PubMed  Article  Google Scholar 

  13. Bouché MB (1977) Stratégies lombriciennes. Ecol Bull 25:122–132

    Google Scholar 

  14. Bowman RA, Cole CV (1978) An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Sci 125:95–101

    Article  CAS  Google Scholar 

  15. Brown GG, Edwards CA, Brussaard L (2004) How earthworms affect plant growth: burrowing into the mechanisms. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC Press, Boca Raton, pp 13–49

    Google Scholar 

  16. Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570

    Article  Google Scholar 

  17. Chapuis-Lardy L, Ramiandrisoa RS, Randriamanantsoa L, Morel C, Rabeharisoa L, Blanchart E (2009) Modification of P availability by endogeic earthworms (Glossoscolecidae) in Ferralsols of the Malagasy Highlands. Biol Fertil Soils 45:415–422

    Article  Google Scholar 

  18. Chapuis-Lardy L, Le Bayon R-C, Brossard M, Lopez-Hernandez D, Blanchart E (2011) Role of soil macrofauna in P cycling. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action—biological processes in soil phosphorus cycling. Springer, New York, pp 199–213

    Google Scholar 

  19. Clapperton MJ, Lee NO, Binet F, Conner RL (2001) Earthworms indirectly reduce the effects of take-all (Gaeumannomyces graminis var.tritici) on soft white spring wheat (Triticum aestivum cv. Fielder). Soil Biol Biochem 33:1531–1538

    Article  CAS  Google Scholar 

  20. Connolly J, Wayne P, Bazzaz FA (2001) Interspecific competition in plants: how well do current methods answer fundamental questions? Am Nat 157:107–125

    PubMed  Article  CAS  Google Scholar 

  21. Corre-Hellou G, Fustec J, Crozat Y (2006) Interspecific competition for soil N and its interaction with N2 fixation, leaf expansion and crop growth in pea–barley intercrops. Plant Soil 282:195–208

    Article  CAS  Google Scholar 

  22. Cu ST, Hutson J, Schuller KA (2005) Mixed culture of wheat ( Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant Soil 272:143–151

    Article  CAS  Google Scholar 

  23. Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50:463–477

    Article  CAS  Google Scholar 

  24. Dreyfus B, Dommergues Y (1980) Non inhibition de la fixation d’azote atmosphérique par l’azote combine chez une legumineuse à nodules caulinaires, Sesbania rostrata. C R Acad Sci Paris 291:767–770

    Google Scholar 

  25. Eisenhauer N, Scheu S (2008) Earthworms as drivers of the competition between grasses and legumes. Soil Biol Biochem 40:2650–2659

    Article  CAS  Google Scholar 

  26. Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2009) Earthworms enhance plant regrowth in a grassland plant diversity gradient. Eur J Soil Biol 45:455–458

    Article  Google Scholar 

  27. Giller KE, Beare MH, Lavelle P, Izac A, Swift MJ (1997) Agricultural intensification, soil biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16

    Article  Google Scholar 

  28. Hinsinger P, Betencourt E, Bernard L et al (2011a) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  29. Hinsinger P, Brauman A, Devau N et al (2011b) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61

    Article  CAS  Google Scholar 

  30. Jana U, Barot S, Blouin M et al (2010) Earthworms influence the production of above-and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana. Soil Biol Biochem 42:244–252

    Article  CAS  Google Scholar 

  31. Jolliffe PA (2000) The replacement series. J Ecol 88:371–385

    Article  Google Scholar 

  32. Jones L, Clements RO (1993) Development of a low input system for growing wheat (Triticum vulgare) in a permanent understorey of white clover (Trifolium repens). Ann Appl Biol 123:109–119

    Article  Google Scholar 

  33. Kreuzer K, Bonkowski M, Langel R, Scheu S (2004) Decomposer animals (Lumbricidae, Collembola) and organic matter distribution affect the performance of Lolium perenne (Poaceae) and Trifolium repens (Fabaceae). Soil Biol Biochem 36:2005–2011

    Article  CAS  Google Scholar 

  34. Kuczak CN, Fernandes E, Lehmann J, Rondon M, Luizao FJ (2006) Inorganic and organic phosphorus pools in earthworm casts (Glossoscolecidae) and a Brazilian rainforest Oxisol. Soil Biol Biochem 38:553–560

    Article  CAS  Google Scholar 

  35. Laossi K-R, Noguera DC, Bartolomé-Lasa A et al (2009) Effects of an endogeic and an anecic earthworm on the competition between four annual plants and their relative fecundity. Soil Biol Biochem 41:1668–1673

    Article  CAS  Google Scholar 

  36. Laossi K-R, Ginot A, Noguera DC, Blouin M, Barot S (2010) Earthworm effects on plant growth do not necessarily decrease with soil fertility. Plant Soil 328:109–118

    Article  CAS  Google Scholar 

  37. Lavelle P (1996) Diversity of soil fauna and ecosystem function. Biol Int 33:3–16

    Google Scholar 

  38. Lavelle P, Decaëns T, Aubert M et al (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15

    Article  Google Scholar 

  39. Le Bayon R-C, Binet F (2006) Earthworms change the distribution and availability of phosphorous in organic substrates. Soil Biol Biochem 38:235–246

    Article  CAS  Google Scholar 

  40. 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. Proc Natl Acad Sci 104:11192–11196

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  41. Li H, Shen J, Zhang F, Tang C, Lambers H (2008) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant Soil 312:139–150

    Article  CAS  Google Scholar 

  42. Logsdon SD, Linden DR (1992) Interactions of earthworms with soil physical conditions influencing plant growth. Soil Sci 154:330–337

    Article  Google Scholar 

  43. Lopez-Hernandez D, Lavelle P, Fardeau J-C, Nino M (1993) Phosphorus transformations in two P-sorption contrasting tropical soils during transit through Pontoscolex corethrurus (Glossoscolecidae: Oligochaeta). Soil Biol Biochem 25:789–792

    Article  CAS  Google Scholar 

  44. McLaughlin A, Mineau P (1995) The impact of agricultural practices on biodiversity. Agric Ecosyst Environ 55:201–212

    Article  Google Scholar 

  45. Milleret R, Le Bayoin R-C, Gobat J-M (2009) Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant Soil 316:1–12

    Article  CAS  Google Scholar 

  46. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  47. Muscolo A, Bovalo F, Gionfriddo F, Nardi S (1999) Earthworm humic matter produces auxin-like effects on Daucus carota cell growth and nitrate metabolism. Soil Biol Biochem 31:1303–1311

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  49. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture, Washington, DC

    Google Scholar 

  50. Partsch S, Milcu A, Scheu S (2006) Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 87:2548–2558

    PubMed  Article  Google Scholar 

  51. Postma-Blaauw MB, Bloem J, Faber JH et al (2006) Earthworm species composition affects the soil bacterial community and net nitrogen mineralization. Pedobiologia 50:243–256

    Article  CAS  Google Scholar 

  52. Puga-Freitas R, Barot S, Taconnat L, Renou J-P, Blouin M (2012) Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on growth, development and defence of the plant Arabidopsis thaliana. PLoS ONE 7:e49504

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  53. Quinn GGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  54. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN 3- 900051-07-0. Accessed at www.R-project.org

    Google Scholar 

  55. Raynaud X, Jaillard B, Leadley PW (2008) Plants may alter competition by modifying nutrient bioavailability in rhizosphere: a modeling approach. Am Nat 171:44–58

    PubMed  Article  Google Scholar 

  56. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  57. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856

    Google Scholar 

  58. Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development. Oecologia 119:541–551

    Article  Google Scholar 

  59. Schmidt O, Curry JP (1999) Effects of earthworms on biomass production, nitrogen allocation and nitrogen transfer in wheat–clover intercropping model systems. Plant Soil 214:187–198

    Article  CAS  Google Scholar 

  60. Snaydon RW (1991) Replacement or additive designs for competition studies? J Appl Ecol 28:930–946

    Article  Google Scholar 

  61. Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. In: Carter MR (ed) Soil sampling and methods analyses. 7:5–229

  62. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton

    Google Scholar 

  63. Vandermeer JH (1992) The ecology of intercropping. Cambridge University Press, Cambridge

    Google Scholar 

  64. Wang D, Marschner P, Solaiman Z, Rengel Z (2007) Growth, P uptake and rhizosphere properties of intercropped wheat and chickpea in soil amended with iron phosphate or phytate. Soil Biol Biochem 39:249–256

    Article  CAS  Google Scholar 

  65. Wurst S, Langel R, Scheu S (2005) Do endogeic earthworms change plant competition? A microcosm study. Plant Soil 271:123–130

    Article  CAS  Google Scholar 

  66. Zhang F, Li L (2003) Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248:305–312

    Article  CAS  Google Scholar 

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Acknowledgments

The study was funded by the PerfCom project (ANR-Systerra ANR-08-STRA-11, coordinated by Dr. P. Hinsinger). Many technical staff members and students are gratefully acknowledged: D. Arnal, A. Grau, C. Guilleré, C. Pernot, G. Souche, E. Russello. We also thank Dr. E. Betencourt, Dr. G. Carlsson, Dr. B. Cloutier-Hurteau, Dr. P. Coll, Dr. P. Deleporte (Eco&Sols) and Dr. E. Garnier (CEFE) for useful discussions.

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Correspondence to E. Blanchart.

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Responsible Editor: Hans Lambers.

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Appendix Figure A1

Effect of earthworms and plants on phosphorus forms and pH of soil. Concentrations of inorganic phosphorus forms extracted with H2O, NaHCO3 and NaOH are shown in graph a, b and c respectively. Organic phosphorus forms are shown in graph d and e for extractions with NaHCO3 and NaOH respectively. Graph f show pH values of soil. (PPTX 79 kb)

Appendix Table A1

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Appendix Table A2

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Coulis, M., Bernard, L., Gérard, F. et al. Endogeic earthworms modify soil phosphorus, plant growth and interactions in a legume–cereal intercrop. Plant Soil 379, 149–160 (2014). https://doi.org/10.1007/s11104-014-2046-4

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Keywords

  • Soil fauna
  • Nitrogen
  • Chickpea
  • Durum wheat
  • Resource allocation
  • Competition