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Soil, land care and environmental research
RESEARCH ARTICLE

Impact of arbuscular mycorrhizal fungi and earthworms on soil aggregate stability, glomalin, and performance of pigeonpea, Cajanus cajan

Mary N. Muchane https://orcid.org/0000-0002-7694-4863 A B E , Mirjam M. Pulleman B C , Bernard Vanlauwe D , Joyce Jefwa A and Thomas W. Kuyper B
+ Author Affiliations
- Author Affiliations

A Botany Department, National Museums of Kenya, PO Box 40658, 00100 Nairobi, Kenya.

B Soil Biology Group, Wageningen University, PO Box 47, 6700 AA Wageningen, The Netherlands.

C International Center for Tropical Agriculture (CIAT), KM17 Recta Cali-Palmira, Palmira, Colombia.

D International Institute of Tropical Agriculture (IITA), PO Box 30772, 00100 Nairobi, Kenya.

E Corresponding author. Email: mmurethi@yahoo.com; mnyawira@museums.or.ke

Soil Research 57(1) 53-65 https://doi.org/10.1071/SR18096
Submitted: 6 April 2018  Accepted: 22 October 2018   Published: 11 December 2018

Abstract

Earthworms and arbuscular mycorrhizal fungi (AMF) modify soil physical and chemical properties. However, little is known about how their interactions affect water-stable aggregation, glomalin and crop performance. A greenhouse experiment was run for 9 months to test the effects of earthworms (endogeic, Pontoscolex corethrurus; and epigeic, Dichogaster bolaui) and AMF (none, Glomus etunicatum and Scutellospora verrucosa) on water-stable aggregation, glomalin levels in aggregate size classes and crop performance. The test crop was pigeonpea (Cajanus cajan (L.) Millsp.). The soil material used for the experiment was a humic nitisol from central Kenya mixed with sand (ratio 1 : 1). Grass residue (equivalent to 20 t ha–1) was placed on top. The AMF root colonisation and external hyphal length, water-stable macroaggregates and microaggregates, total and easily-extractable glomalin in aggregate size classes, plant biomass and plant N and P uptake were measured. Earthworms were a major source of variation for soil aggregation, glomalin content and crop performance. The epigeic earthworms (D. bolaui) increased the amount of water-stable macroaggregates (by 10%) and glomalin in microaggregates and improved crop (growth and biomass) performance. The endogeic earthworms (P. corethrurus) reduced external hyphal length, root colonisation and crop performance but had no effect on water-stable aggregates and glomalin levels in in aggregate size classes. A significant AMF × earthworm interaction was observed for plant biomass and concentrations of nitrogen (N) and phosphorus (P). The AMF species together with epigeic earthworms increased plant biomass and N and P concentrations. Our results contribute to the understanding of interactions between AMF and earthworms in relation to soil aggregation, plant productivity and nutrient uptake.

Additional keywords: epigeic, endogeic, soil biota, soil fertility, soil structure, integrated soil fertility management (ISFM).


References

Anderson JM, Ingram JS (1993) ‘Tropical soil biology and fertility: a handbook of methods of analysis.’ (CAB International: Wallingford, UK)

Ayuke FO, Brussaard L, Vanlauwe B, Six J, Lelei DK, Kibunja CN, Pulleman MM (2011) Soil fertility management: Impacts on soil macrofauna, soil aggregation and soil organic matter allocation. Applied Soil Ecology 48, 53–62.
Soil fertility management: Impacts on soil macrofauna, soil aggregation and soil organic matter allocation.Crossref | GoogleScholarGoogle Scholar |

Blanchart E, Albrecht A, Brown G, Decaens T, Duboisset A, Lavelle P, Mariani L, Roose E (2004) Effects of tropical endogeic earthworms on soil erosion. Agriculture, Ecosystems & Environment 104, 303–315.
Effects of tropical endogeic earthworms on soil erosion.Crossref | GoogleScholarGoogle Scholar |

Bossuyt H, Six J, Hendrix PF (2006) Interactive effects of functionally different earthworms species on aggregation and incorporation and decomposition of newly added residues carbon. Geoderma 130, 14–25.
Interactive effects of functionally different earthworms species on aggregation and incorporation and decomposition of newly added residues carbon.Crossref | GoogleScholarGoogle Scholar |

Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. European Journal of Soil Biology 36, 177–198.
Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains.Crossref | GoogleScholarGoogle Scholar |

Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agriculture, Ecosystems & Environment 116, 72–84.
Mycorrhizas and tropical soil fertility.Crossref | GoogleScholarGoogle Scholar |

Dempsey MA, Fisk MC, Yavitt JB, Fahey TJ, Balser TC (2013) Exotic earthworms alter soil microbial community composition and function. Soil Biology & Biochemistry 67, 263–270.
Exotic earthworms alter soil microbial community composition and function.Crossref | GoogleScholarGoogle Scholar |

Eisenhauer N, König S, Sabais ACW, Renker C, Buscot F, Scheu S (2009) Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biology & Biochemistry 41, 561–567.
Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated.Crossref | GoogleScholarGoogle Scholar |

Elliott ET (1986) Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50, 627–633.
Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils.Crossref | GoogleScholarGoogle Scholar |

FAO (1991) ‘Guidelines for soil profile description’, 3rd edn. (Soil Resources Management and Conservation Service, Land and Water Development Division, FAO: Rome)

Gange AC (1993) Translocation of mycorrhizal fungi by earthworms during early succession. Soil Biology & Biochemistry 25, 1021–1026.
Translocation of mycorrhizal fungi by earthworms during early succession.Crossref | GoogleScholarGoogle Scholar |

Giannopoulos G, Pulleman MM, Van Groenigen JW (2010) Interactions between residue placement and earthworm ecological strategy affect aggregate turnover and N2O dynamics in agricultural soils. Soil Biology & Biochemistry 42, 618–625.
Interactions between residue placement and earthworm ecological strategy affect aggregate turnover and N2O dynamics in agricultural soils.Crossref | GoogleScholarGoogle Scholar |

Giannopoulos G, Van Groenigen JW, Pulleman MM (2011) Earthworm-induced N2O emissions in sandy soil with surface-applied crop residues. Pedobiologia 54, S103–S111.
Earthworm-induced N2O emissions in sandy soil with surface-applied crop residues.Crossref | GoogleScholarGoogle Scholar |

Gillespie AW, Farrell RE, Walley FL, Ross AR, Leinweber P, Eckhardt KU, Regier TZ, Blyth RI (2011) Glomalin-related soil protein contains non-mycorrhizal-related heat-stable proteins, lipids and humic materials. Soil Biology & Biochemistry 43, 766–777.
Glomalin-related soil protein contains non-mycorrhizal-related heat-stable proteins, lipids and humic materials.Crossref | GoogleScholarGoogle Scholar |

Green SV, Cavigelli MA, Dao TH, Flanagan DC (2005) Soil physical properties and aggregate-associated C, N, and P distributions in organic and conventional cropping systems. Soil Science 170, 822–831.
Soil physical properties and aggregate-associated C, N, and P distributions in organic and conventional cropping systems.Crossref | GoogleScholarGoogle Scholar |

Gulde S, Chung H, Amelung W, Chang C, Six J (2008) Soil carbon saturation controls labile and stable carbon pool dynamics. Soil Science Society of America Journal 72, 605–612.
Soil carbon saturation controls labile and stable carbon pool dynamics.Crossref | GoogleScholarGoogle Scholar |

Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
N:P ratios in terrestrial plants: variation and functional significance.Crossref | GoogleScholarGoogle Scholar |

Hallett P, Feeney D, Bengough A, Rillig M, Scrimgeour C, Young I (2009) Disentangling the impact of AM fungi versus roots on soil structure and water transport. Plant and Soil 314, 183–196.
Disentangling the impact of AM fungi versus roots on soil structure and water transport.Crossref | GoogleScholarGoogle Scholar |

Harinikumar KM, Bagyaraj DJ (1994) Potential of earthworms, ants, millipedes, and termites for dissemination of vesicular-arbuscular mycorrhizal fungi in soil. Biology and Fertility of Soils 18, 115–118.
Potential of earthworms, ants, millipedes, and termites for dissemination of vesicular-arbuscular mycorrhizal fungi in soil.Crossref | GoogleScholarGoogle Scholar |

Hart MM, Reader RJ (2002a) Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biology and Fertility of Soils 36, 357–366.
Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium.Crossref | GoogleScholarGoogle Scholar |

Hart MM, Reader RJ (2002b) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist 153, 335–344.
Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America 107, 13754–13759.
Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling.Crossref | GoogleScholarGoogle Scholar |

Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120, 371–380.
External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots.Crossref | GoogleScholarGoogle Scholar |

Janssen BH (2011) Simple models and concepts as tools for the study of sustained soil productivity in long-term experiments. I. New soil organic matter and residual effect of P from fertilizers and farmyard manure in Kabete, Kenya. Plant and Soil 339, 3–16.
Simple models and concepts as tools for the study of sustained soil productivity in long-term experiments. I. New soil organic matter and residual effect of P from fertilizers and farmyard manure in Kabete, Kenya.Crossref | GoogleScholarGoogle Scholar |

Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences of the United States of America 107, 2093–2098.
Resource limitation is a driver of local adaptation in mycorrhizal symbioses.Crossref | GoogleScholarGoogle Scholar |

Kale RD, Karmegam N (2010) The role of earthworms in tropics with emphasis on Indian ecosystems. Applied and Environmental Soil Science 414356
The role of earthworms in tropics with emphasis on Indian ecosystems.Crossref | GoogleScholarGoogle Scholar |

Kimetu JM, Nugendi DN, Bationo A, Palm CA, Mutuo PK, Kihara J, Nandwa S, Giller K (2006) Partial balance of nitrogen in a maize cropping system in humic nitisol of Central Kenya. Nutrient Cycling in Agroecosystems 76, 261–270.
Partial balance of nitrogen in a maize cropping system in humic nitisol of Central Kenya.Crossref | GoogleScholarGoogle Scholar |

Kohler-Milleret R, Le Bayon RC, Chenu C, Gobat JM, Boivin P (2013) Impact of two root systems, earthworms and mycorrhizae on the physical properties of an unstable silt loam Luvisol and plant production. Plant and Soil 370, 251–265.
Impact of two root systems, earthworms and mycorrhizae on the physical properties of an unstable silt loam Luvisol and plant production.Crossref | GoogleScholarGoogle Scholar |

Koide RT, Peoples MS (2013) Behavior of Bradford-reactive substances is consistent with predictions for glomalin. Applied Soil Ecology 63, 8–14.
Behavior of Bradford-reactive substances is consistent with predictions for glomalin.Crossref | GoogleScholarGoogle Scholar |

Kuyper TW, Giller KE (2011) Biodiversity and ecosystem functioning below-ground. In ‘Agro-biodiversity management for food security - a critical review’. (Eds JM Lenné and DM Woods) pp. 134–149. (CABI, Oxfordshire, UK)

Lavelle P, Spain AV (2001) ‘Soil ecology.’ (Kluwer Academic Publishers: Amsterdam)

Lee KK, Reddy MV, Wani SP, Trimurtulu N (1996) Vesicular-arbuscular mycorrhizal fungi in earthworm casts and surrounding soil in relation to soil management of a semi-arid tropical Alfisol. Applied Soil Ecology 3, 177–181.
Vesicular-arbuscular mycorrhizal fungi in earthworm casts and surrounding soil in relation to soil management of a semi-arid tropical Alfisol.Crossref | GoogleScholarGoogle Scholar |

Li H, Li X, Dou Z, Zhang J, Wang C (2012a) Earthworm (Aporrectodea trapezoides) – mycorrhiza (Glomus intraradices) interaction and nitrogen and phosphorus uptake by maize. Biology and Fertility of Soils 48, 75–85.
Earthworm (Aporrectodea trapezoides) – mycorrhiza (Glomus intraradices) interaction and nitrogen and phosphorus uptake by maize.Crossref | GoogleScholarGoogle Scholar |

Li H, Xiang D, Wang C, Li X, Luo Y (2012b) Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhiza fungus (Glomus intraradices) on enzyme activities of a sterilized soil-sand mixture and nutrient uptake by maize. Biology and Fertility of Soils 48, 879–887.
Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhiza fungus (Glomus intraradices) on enzyme activities of a sterilized soil-sand mixture and nutrient uptake by maize.Crossref | GoogleScholarGoogle Scholar |

Li H, Wang C, Li X, Christie P, Dou Z, Zhang J, Xiang D (2013a) Impact of the earthworm Aporrectodea trapezoides and the arbuscular mycorrhizal fungus Glomus intraradices in 15N uptake by maize from wheat straw. Biology and Fertility of Soils 49, 263–271.
Impact of the earthworm Aporrectodea trapezoides and the arbuscular mycorrhizal fungus Glomus intraradices in 15N uptake by maize from wheat straw.Crossref | GoogleScholarGoogle Scholar |

Li H, Wang C, Li X, Xiang D (2013b) Inoculating maize fields with earthworms (Aporrectodea trapezoides) and an arbuscular mycorrhizal fungus (Rhizophagus intraradices) improves mycorrhizal community structure and increases plant nutrient uptake. Biology and Fertility of Soils 49, 1167–1178.
Inoculating maize fields with earthworms (Aporrectodea trapezoides) and an arbuscular mycorrhizal fungus (Rhizophagus intraradices) improves mycorrhizal community structure and increases plant nutrient uptake.Crossref | GoogleScholarGoogle Scholar |

Ma Y, Dickinson NM, Wong MH (2006) Beneficial effects of earthworms and arbuscular mycorrhizal fungi on establishment of leguminous trees on Pb/Zn mine tailings. Soil Biology & Biochemistry 38, 1403–1412.
Beneficial effects of earthworms and arbuscular mycorrhizal fungi on establishment of leguminous trees on Pb/Zn mine tailings.Crossref | GoogleScholarGoogle Scholar |

Márquez CO, Garcia VJ, Cambardella CA, Schultz RC, Isenhar TM (2004) Aggregate-size stability distribution and soil stability. Soil Science Society of America Journal 68, 725–735.
Aggregate-size stability distribution and soil stability.Crossref | GoogleScholarGoogle Scholar |

Mason P, Ingleby K (1998) ‘Mycorrhiza working manual.’ (ITP: Scotland)

Milleret R, Bayon RL, Gabot JN (2009a) Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant and Soil 316, 1–12.
Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass.Crossref | GoogleScholarGoogle Scholar |

Milleret R, Le Bayon RC, Lamy F, Gobat JM, Boivin P (2009b) Impact of roots, mycorrhizas and earthworms on soil physical properties as assessed by shrinkage analysis. Journal of Hydrology 373, 499–507.
Impact of roots, mycorrhizas and earthworms on soil physical properties as assessed by shrinkage analysis.Crossref | GoogleScholarGoogle Scholar |

Murage EW, Karanja NK, Smithson PC, Woomer PL (2000) Diagnostic indicators of soil quality in productive and non-productive smallholders’ fields of Kenya’s Central Highlands. Agriculture, Ecosystems & Environment 79, 1–8.
Diagnostic indicators of soil quality in productive and non-productive smallholders’ fields of Kenya’s Central Highlands.Crossref | GoogleScholarGoogle Scholar |

Nie J, Zhou JM, Wang HY, Chen XQ, Du CW (2007) Effect of long-term rice straw return on soil glomalin, carbon and nitrogen. Pedosphere 17, 295–302.
Effect of long-term rice straw return on soil glomalin, carbon and nitrogen.Crossref | GoogleScholarGoogle Scholar |

Ortiz-Ceballos AI, Peña-Cabriales JJ, Fragoso C, Brown GG (2007) Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvet bean mulch. Biology and Fertility of Soils 44, 181–186.
Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvet bean mulch.Crossref | GoogleScholarGoogle Scholar |

Pattinson GS, Smith SE, Doube BM (1997) Earthworm Aporrectodea trapezoides had no effect on the dispersal of a vesicular-arbuscular mycorrhizal fungus, Glomus intraradices. Soil Biology & Biochemistry 29, 1079–1088.
Earthworm Aporrectodea trapezoides had no effect on the dispersal of a vesicular-arbuscular mycorrhizal fungus, Glomus intraradices.Crossref | GoogleScholarGoogle Scholar |

Piotrowski JS, Denich T, Klironomos JN, Graham JM, Rillig MC (2004) The effects of arbuscular mycorrhizae on soil aggregation depend on the interaction between plant and fungal species. New Phytologist 164, 365–373.
The effects of arbuscular mycorrhizae on soil aggregation depend on the interaction between plant and fungal species.Crossref | GoogleScholarGoogle Scholar |

Pulleman MM, Six J, Uyl A, Marinissen JCY, Jongmans AG (2005) Earthworms and management affect organic matter incorporation and microaggregate formation in agricultural soils. Applied Soil Ecology 29, 1–15.
Earthworms and management affect organic matter incorporation and microaggregate formation in agricultural soils.Crossref | GoogleScholarGoogle Scholar |

Reddell P, Spain AV (1991) Earthworms as vectors of viable propagules of mycorrhizal fungi. Soil Biology & Biochemistry 23, 767–774.
Earthworms as vectors of viable propagules of mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytologist 171, 41–53.
Mycorrhizas and soil structure.Crossref | GoogleScholarGoogle Scholar |

Rillig MC, Wright SF, Eviner V (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant and Soil 238, 325–333.
The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species.Crossref | GoogleScholarGoogle Scholar |

Sahu SK, Mishra SK, Senapati BK (1988) Population biology and reproductive strategy of Dichogaster bolaui (Oligochaeta: Octochaetidae) in two tropical agroecosystems. Proceedings: Animal Sciences 97, 239–250.

Sakala WD, Cadisch G, Giller KE (2000) Interactions between residues of maize and pigeonpea and mineral N fertilizers during decomposition and N mineralization. Soil Biology & Biochemistry 32, 679–688.
Interactions between residues of maize and pigeonpea and mineral N fertilizers during decomposition and N mineralization.Crossref | GoogleScholarGoogle Scholar |

Schindler FV, Mercer EJ, Rice JA (2007) Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content. Soil Biology & Biochemistry 39, 320–329.
Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content.Crossref | GoogleScholarGoogle Scholar |

Schroeder MS, Janos DP (2004) Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas. Plant and Soil 264, 335–348.
Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar |

Six J, Elliott ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry 32, 2099–2103.
Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture.Crossref | GoogleScholarGoogle 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 Research 79, 7–31.
A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics.Crossref | GoogleScholarGoogle Scholar |

Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis’, 3rd edition. (Academic Press: London)

Treseder KK, Turner KM (2007) Glomalin in ecosystems. Soil Science Society of America Journal 71, 1257–1266.
Glomalin in ecosystems.Crossref | GoogleScholarGoogle Scholar |

Trouvelot A, Kough JL Gianinazzi-Pearson V (1986) Mésure du taux de mycorhization VA d’un système radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle. In ‘Physiological and genetic aspects of mycorrhizae’. (Eds V Gianinazzi-Pearson and S Gianinazzi) pp. 217–221. (INRA: Paris)

Tuffen F, Eason WR, Scullion J (2002) The effect of earthworms and arbuscular mycorrhizal fungi on growth of and 32P transfer between Allium porrum plants. Soil Biology & Biochemistry 34, 1027–1036.
The effect of earthworms and arbuscular mycorrhizal fungi on growth of and 32P transfer between Allium porrum plants.Crossref | GoogleScholarGoogle Scholar |

van Groenigen JW, Lubbers IM, Vos HMJ, Brown GG, De Deyn GB, Van Groenigen KJ (2014) Earthworms increase plant production: a meta-analysis. Nature Scientific Reports 4, 6365
Earthworms increase plant production: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Vanlauwe B, Tittonell P, Mukalama J (2006) Within-farm soil fertility gradients affect response of maize to fertiliser application in western Kenya. Nutrient Cycling in Agroecosystem 76, 171–182.
Within-farm soil fertility gradients affect response of maize to fertiliser application in western Kenya.Crossref | GoogleScholarGoogle Scholar |

Vanlauwe B, Bationo A, Chianu J, Giller KE, Merckx R, Mokwunye U, Ohiokpehai O, Pypers P, Tabo R, Shepherd K, Smaling E, Woomer PL, Sanginga N (2010) Integrated Soil Fertility Management: operational definition and consequences for implementation and dissemination. Outlook on Agriculture 39, 17–24.
Integrated Soil Fertility Management: operational definition and consequences for implementation and dissemination.Crossref | GoogleScholarGoogle Scholar |

Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Science 161, 575–586.
Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil 198, 97–107.
A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Wright SF, Green VS, Cavigelli MA (2007) Glomalin in aggregate size classes from three different farming systems. Soil & Tillage Research 94, 546–549.
Glomalin in aggregate size classes from three different farming systems.Crossref | GoogleScholarGoogle Scholar |

Xiang D, Li H (2014) Nutrient uptake in mycorrhizal plants – role of earthworms. Acta Agriculturae Scandinavica, Section B – Soil & Plant Science 64, 434–441.
Nutrient uptake in mycorrhizal plants – role of earthworms.Crossref | GoogleScholarGoogle Scholar |

Yu X, Cheng J, Wong MH (2005) Earthworm–mycorrhiza interaction on Cd uptake and growth of ryegrass. Soil Biology & Biochemistry 37, 195–201.
Earthworm–mycorrhiza interaction on Cd uptake and growth of ryegrass.Crossref | GoogleScholarGoogle Scholar |