Plant-earthworm interactions: influence of age and proportion of casts in the soil on plant growth, morphology and nitrogen uptake

Abstract

Background and aims

Earthworms effect on plant growth is mediated by their dejections or “casts”, a complex mixture of organic matter, minerals and microbes. In casts, different processes such as organic matter mineralization and signal molecule production follow a complex temporal dynamics. An adaptation of root morphology to cast dynamics could allow an efficient nitrogen capture by the plant.

Methods

The plant Brachypodium distachyon was grown in a laboratory experiment with different proportions of casts of increasing ages. Casts were labelled with 15N to quantify the plant N uptake from the casts. Plant biomass and morphology, especially root system structure, were analysed.

Results

The age of casts had an effect on fine root length, highlighting the importance of the dynamics of cast maturation in root adaptation. Plant biomass production was affected by the interaction between the age and proportion of casts. A positive correlation between the 15N proportion in plant tissues and plant biomasses indicated that plants were more efficient in foraging N in casts than in the bulk soil.

Conclusions

Our results suggested that both a timely adaptation of the root system structure and a significant proportion of casts are necessary to observe a positive effect of casts on plant growth.

This is a preview of subscription content, access via your institution.

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

References

  1. Aira M, Monroy F, Domínguez J (2005) Ageing effects on nitrogen dynamics and enzyme activities in casts of Aporrectodea caliginosa (Lumbricidae). Pedobiologia 49:467–473

    CAS  Article  Google Scholar 

  2. Arancon NQ, Edwards CA (2011) The use of vermicomposts as soil amendments for production of field crops. In: Edwards CA, Arancon NQ, Sherman R (eds) Vermiculture technology: earthworms, organic wastes and environmental management. CRC Press, Boca Raton, pp 129–151

    Google Scholar 

  3. Arnone JA, Zaller JG (2014) Earthworm effects on native grassland root system dynamics under natural and increased rainfall. Front Plant Sci 5:152

    Article  PubMed  PubMed Central  Google Scholar 

  4. Baker GH, Carter PJ, Barrett VJ (1999) Influence of earthworms, Aporrectodea spp. (Lumbricidae), on pasture production in south-eastern Australia. Aust J Agric Res 50:1247–1257

    Article  Google Scholar 

  5. Blanchart E, Albrecht A, Alegre J, Duboisset A, Gilot C, Pashanasi B, Brussaard L 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 Publishing, Wallingford, pp 149–171

    Google Scholar 

  6. Blouin M, Puga-Freitas R (2011) Combined effects of contrast between poor and rich patches and overall nitrate concentration on Arabidopsis thaliana root system structure. Funct Plant Biol 38:364–371

    Article  Google Scholar 

  7. Blouin M, Zuily-Fodil Y, Pham-Thi AT, Laffray D, Reversat G, Pando A, Tondoh J, Lavelle P (2005) Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites. Ecol Lett 8:202–208

    Article  Google Scholar 

  8. Blouin M, Barot S, Lavelle P (2006) Earthworms (Millsonia anomala, Megascolecidae) do not increase rice growth through enhanced nitrogen mineralization. Soil Biol Biochem 38:2063–2068

    CAS  Article  Google Scholar 

  9. Blouin M, Mathieu J, Leadley PW (2012) Plant homeostasis, growth and development in natural and artificial soils. Ecol Complex 9:10–15

    Article  Google Scholar 

  10. Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J et al (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182

    Article  Google Scholar 

  11. Bouché MB (1977) Stratégies lombriciennes. In: Lohm U, Persson T (eds) Soil organisms as components of ecosystems. Ecology bulletin/NFR, Stockholm, pp 122–132

    Google Scholar 

  12. Bouma TJ, Nielsen KL, Koutstaal B (2000) Sample preparation and scanning protocol for computerised analysis of root length and diameter. Plant Soil 218:185–196

    CAS  Article  Google Scholar 

  13. Brown GG, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S, Barois I, Lavelle P, Blanchart E, Blakemore RJ, Spain AV, Boyer J (1999) Effects of earthworms on plant production in the tropics. In: Lavelle P, Brussaard L, Hendrix P (eds) Earthworm management in tropical agroecosystems. CAB International, Wallingford, pp 87–148

    Google Scholar 

  14. Canellas LP, Olivares FL, Okorokova-Facanha AL, Facanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Canellas LP, Dobbss LB, Oliveira AL, Chagas JG, Aguiar NO, Rumjanek VM, Novotny EH, Olivares FL, Spaccini R, Piccolo A (2012) Chemical properties of humic matter as related to induction of plant lateral roots. Eur J Soil Sci 63:315–324

    CAS  Article  Google Scholar 

  16. Chan KY, Baker GH, Conyers MK, Scott B, Munro K (2004) Complementary ability of three European earthworms (Lumbricidae) to bury lime and increase pasture production in acidic soils of south-eastern Australia. Appl Soil Ecol 26:257–271

    Article  Google Scholar 

  17. Crick JC, Grime JP (1987) Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology. New Phytol 107:403–414

    Article  Google Scholar 

  18. Fitter AH (1994) Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: Caldwell P (ed) Exploitation of environmental heterogeneity by plants. Academic Press, San Diego, pp 305–323

    Google Scholar 

  19. Garvin DF (2007) Brachypodium: a new monocot model plant system emerges. J Sci Food Agric 87:1177–1179

    CAS  Article  Google Scholar 

  20. Girin T, David LC, Chardin C, Sibout R, Krapp A, Ferrario-Méry S, Daniel-Vedele F (2014) Brachypodium: a promising hub between model species and cereals. J Exp Bot 65:5683–5696

    CAS  Article  PubMed  Google Scholar 

  21. Gross KL, Peters A, Pregitzer KS (1993) Fine root growth and demographic responses to nutrient patches in four old-field plant species. Oecologia 95:61–64

    Article  PubMed  Google Scholar 

  22. Himmelbauer ML, Loiskandl W, Kastanek F (2004) Estimating length, average diameter and surface area of roots using two different image analyses systems. Plant Soil 260:111–120

    CAS  Article  Google Scholar 

  23. Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411

    CAS  Article  PubMed  Google Scholar 

  24. Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640

    Article  PubMed  Google Scholar 

  25. Jackson RB, Caldwell MM (1989) The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials. Oecologia 81:149–153

    CAS  Article  PubMed  Google Scholar 

  26. Jackson RB, Caldwell MM (1992) Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass. Oecologia 91:457–462

    CAS  Article  PubMed  Google Scholar 

  27. Jana U, Barot S, Blouin M, Lavelle P, Laffray D, Repellin A (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

    CAS  Article  Google Scholar 

  28. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  29. Kotliar NB, Wiens JA (1990) Multiple scales of patchiness and patch structure: a hierarchical framework for the study of heterogeneity. Oikos 59:253–260

    Article  Google Scholar 

  30. Lamb EG, Haag JJ, Cahill JF (2004) Patch–background contrast and patch density have limited effects on root proliferation and plant performance in Abutilon theophrasti. Funct Ecol 18:836–843

    Article  Google Scholar 

  31. Laossi K-R, Ginot A, Noguera D, Blouin M, Barot S (2009) Earthworm effects on plant growth do not necessarily decrease with soil fertility. Plant Soil 328:109–118

    Article  Google Scholar 

  32. Larigauderie A, Richards JH (1994) Root proliferation characteristics of seven perennial arid-land grasses in nutrient-enriched microsites. Oecologia 99:102–111

    CAS  Article  PubMed  Google Scholar 

  33. Lavelle P, Martin A (1992) Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics. Soil Biol Biochem 24:1491–1498

    Article  Google Scholar 

  34. Lavelle P, Bignell D, Lepage M, Wolters W, Roger P et al (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Euro J soil Biol 33:159–193

    CAS  Google Scholar 

  35. Lavelle P, Decaens T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi J-P (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15

    Article  Google Scholar 

  36. Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic Press Inc., Cambridge

    Google Scholar 

  37. Martens DA, Frankenberger WT (1993) Stability of microbial-produced auxins derived from L-tryptophan added to soil. Soil Sci 155:263–271

    CAS  Article  Google Scholar 

  38. Monard C, Vandenkoornhuyse P, Le Bot B, Binet F (2011) Relationship between bacterial diversity and function under biotic control: the soil pesticide degraders as a case study. ISME J 5:1048–1056

    CAS  Article  PubMed  Google Scholar 

  39. Muscolo A, Cutrupi S, Nardi S (1998) IAA detection in humic substances. Soil Biol Biochem 30:1199–1201

    CAS  Article  Google Scholar 

  40. Puga-Freitas R, Abbad S, Gigon A, Garnier-Zarli E, Blouin M (2012a) Control of cultivable IAA-producing bacteria by the plant Arabidopsis thaliana and the earthworm Aporrectodea caliginosa. Appl Environ Soil Sci 2012:307415

    Article  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Quaggiotti S, Ruperti B, Pizzeghello D, Francioso O, Tugnoli V, Nardi S (2004) Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.) J Exp Bot 55:803–813

    CAS  Article  PubMed  Google Scholar 

  43. R Core Team (2014) R: a language and environment for statistical computing. R development Core team. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  44. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127:635–674

    CAS  Article  Google Scholar 

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

    Google Scholar 

  46. Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates Inc., Sunderland

    Google Scholar 

  47. van Groenigen J-W, Lubbers I, Vos H (2014) Earthworms increase plant production: a meta-analysis. Sci Rep 4:6365

    Article  PubMed  PubMed Central  Google Scholar 

  48. Zangerlé A, Hissler C, Blouin M, Lavelle P (2014) Near-infrared spectroscopy (NIRS) to estimate earthworm cast age. Soil Biol Biochem 70:47–53

    Article  Google Scholar 

  49. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci U S A 96:6529–6534

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Christelle Ngueda for the technical help and Beatriz Decencière, Amandine Hansart and Florent Massol of the CEREEP - Ecotron IDF/UMS CNRS/ENS 3194 for soil provision. This work was supported by grants from Région Ile-de-France, R2DS 2014-08 and by the French national program CNRS/INSU EC2CO. We are very grateful to Thomas Lerch and Naoise Nunan for their advices regarding the 15N-labeling of earthworm’ casts.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Manuel Blouin.

Additional information

Responsible Editor: Michael Luke McCormack

Electronic supplementary material

ESM 1

(DOCX 56 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Agapit, C., Gigon, A., Puga-Freitas, R. et al. Plant-earthworm interactions: influence of age and proportion of casts in the soil on plant growth, morphology and nitrogen uptake. Plant Soil 424, 49–61 (2018). https://doi.org/10.1007/s11104-017-3544-y

Download citation

Keywords

  • Biomass production
  • Cast
  • Earthworm
  • Nitrogen cycle
  • Plant development
  • Root morphology