Abstract
Background and aims
Soil aggregation is a crucial aspect of ecosystem functioning in terrestrial ecosystems. Arbuscular mycorrhizal fungi (AMF) play a key role in soil aggregate formation and stabilization. Here we quantitatively analyzed the importance of experimental settings as well as biotic and abiotic factors for the effectiveness of AMF to stabilize soil macroaggregates.
Methods
We gathered 35 studies on AMF and soil aggregation and tested 13 predictor variables for their relevance with a boosted regression tree analysis and performed a meta-analysis, fitting individual random effects models for each variable.
Results and conclusions
The overall mean effect of inoculation with AMF on soil aggregation was positive and predictor variable means were all in the range of beneficial effects. Pot studies and studies with sterilized sandy soil, near neutral soil pH, a pot size smaller than 2.5 kg and a duration between 2.2 and 5 months were more likely to result in stronger effects of AMF on soil aggregation than experiments in the field, with non-sterilized or fine textured soil or an acidic pH. This is the first study to quantitatively show that the effect of AMF inoculation on soil aggregation is positive and context dependent. Our findings can help to improve the use of this important ecosystem process, e.g. for inoculum application in restoration sites.
Similar content being viewed by others
References
Adams DC, Gurevitch J, Rosenberg MS (1997) Resampling tests for meta-analysis of ecological data. Ecology 78:1277–1283
Alguacil MD, Caravaca F, Diaz G, Marin P, Roldan A (2004) Establishment of Retama sphaerocarpa L. seedlings on a degraded semiarid soil as influenced by mycorrhizal inoculation and sewage-sludge amendment. J Plant Nutr Soil Sci-Z Pflanzenernahr Bodenkd 167:637–644
Alguacil MM, Caravaca F, Azcon R, Roldan A (2008) Changes in biological activity of a degraded Mediterranean soil after using microbially-treated dry olive cake as a biosolid amendment and arbuscular mycorrhizal fungi. Eur J Soil Biol 44:347–354
Ambriz E, Baez-Perez A, Sanchez-Yanez JM, Moutoglis P, Villegas J (2010) Fraxinus-Glomus-Pisolithus symbiosis: plant growth and soil aggregation effects. Pedobiologia 53:369–373
Amézketa E (1999) Soil aggregate stability: a review. J Sustain Agric 14:83–151
Andrade G, Linderman RG, Bethlenfalvay GJ (1998a) Bacterial associations with the mycorrhizosphere and hyphosphere of the arbuscular mycorrhizal fungus Glomus mosseae. Plant Soil 202:79–87
Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1998b) Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202:89–96
Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246
Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Auge RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97
Baath E, Hayman DS (1984) Effect of soil volume and plant density on mycorrhizal infection and growth response. Plant Soil 77:373–376
Barto EK, Alt F, Oelmann Y, Wilcke W, Rillig MC (2010) Contributions of biotic and abiotic factors to soil aggregation across a land use gradient. Soil Biol Biochem 42:2316–2324
Bearden BN, Petersen L (2000) Influence of arbuscular mycorrhizal fungi on soil structure and aggregate stability of a vertisol. Plant Soil 218:173–183
Bethlenfalvay GJ, Barea JM (1994) Mycorrhizae in sustainable agriculture. Am J Altern Agric 9:157–161
Borenstein M, Hedges L, Higgins J, Rothstein H (2009) Introduction to meta-analysis. Wiley, New-York
Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22
Chaudhary VB, Bowker MA, O’Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC (2009) Untangling the biological contributions to soil stability in semiarid shrublands. Ecol Appl 19:110–122
Chen FS, Zeng DH, He XY (2006) Small-scale spatial variability of soil nutrients and vegetation properties in semi-arid northern China. Pedosphere 16:778–787
Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22
Copas J, Shi JQ (2000) Meta-analysis, funnel plots and sensitivity analysis. Biostatistics (Oxford, England) 1:247–262
Corrêa A, Gurevitch J, Martins-Loução MA, Cruz C (2012) C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121:449–463
De’ath G (2007) Boosted trees for ecological modeling and prediction. Ecology 88:243–251
Diaz-Zorita M, Perfect E, Grove JH (2002) Disruptive methods for assessing soil structure. Soil Tillage Res 64:3–22
Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813
Endlweber K, Scheu S (2006) Establishing arbuscular mycorrhiza-free soil: a comparison of six methods and their effects on nutrient mobilization. Appl Soil Ecol 34:276–279
Enkhtuya B, Vosatka M (2005) Interaction between grass and trees mediated by extraradical mycelium of symbiotic arbuscular mycorrhizal fungi. Symbiosis 38:261–276
Enkhtuya B, Oskarsson U, Dodd JC, Vosatka M (2003) Inoculation of grass and tree seedlings used for reclaiming eroded areas in Iceland with mycorrhizal fungi. Folia Geobot 38:209–222
Garcia-Cruz A, Flores-Roman D, Garcia-Calderon NE, Ferrera-Cerrato R, Velazquez-Rodriguez AS (2007) Tepetate habilitation by effect of biological improvers. Agrociencia 41:723–731
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344
Hastie T (2011) Generalized additive models. Package ‘gam’ for R
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156
Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480
Herman DJ, Firestone MK, Nuccio E, Hodge A (2012) Interactions between an arbuscular mycorrhizal fungus and a soil microbial community mediating litter decomposition. FEMS Microbiol Ecol 80:236–247
Herold A, McNeil PH (1979) Restoration of photosynthesis in pot-bound tobacco plants. J Exp Bot 30:1187–1194
Hijmans RJ, Phillips S, Leathwick JR, Elith J (2013) Package ‘dismo’—Species distribution modeling version 0.7-23
Hodge A (2001) Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol 151:725–734
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407
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 Phytol 120:371–380
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586
Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–1908
Juma NG (1999) Introduction to soil science and soil resources, volume 1 of the series ‘The pedosphere and its dynamics: a systems approach to soil science’. Salman Productions Inc
Kemper WD, Rosenau RC (eds) (1986) Methods of soil analysis. Part I. Physical and mineralogical methods
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Klironomos JN, Allen MF, Rillig MC, Piotrowski J, Makvandi-Nejad S, Wolfe BE, Powell JR (2005) Abrupt rise in atmospheric CO2 overestimates community response in a model plant-soil system. Nature 433:621–624
Kohler J, Tortosa G, Cegarra J, Caravaca F, Roldan A (2008) Impact of DOM from composted “alperujo” on soil structure, AM fungi, microbial activity and growth of Medicago sativa. Waste Manage 28:1423–1431
Kohler J, Caravaca F, Alguacil MD, Roldan A (2009a) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions. Soil Biol Biochem 41:1710–1716
Kohler J, Caravaca F, Roldan A (2009b) Effect of drought on the stability of rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl Soil Ecol 42:160–165
Koide RT (1991) Nutrient supply, nutrient demand and plant-response to mycorrhizal infection. New Phytol 117:365–386
Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148:511–517
Kucey RMN, Janzen HH (1987) Effects of VAM and reduced nutrient availability on growth and phosphorus and micronutrient uptake of wheat and field beans under greenhouse conditions. Plant Soil 104:71–78
Kumar S, Stohlgren TJ, Chong GW (2006) Spatial heterogeneity influences native and nonnative plant species richness. Ecology 87:3186–3199
Lajeunesse MJ (2011) On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049–2055
Lajeunesse MJ, Forbes MR (2003) Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecol Lett 6:448–454
Lax A, Diaz E, Castillo V, Albaladejo J (1994) Reclamation of physical and chemical-properties of a salinized soil by organic amendment. Arid Soil Res Rehabil 8:9–17
Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204
Lynch JM, Bragg E (1985) Microorganisms and soil aggregate stability. Adv Soil Sci 2:133–171
Marschner P, Solaiman Z, Rengel Z (2005) Growth, phosphorus uptake, and rhizosphere microbial-community composition of a phosphorus-efficient wheat cultivar in soils differing in pH. J Plant Nutr Soil Sci 168:343–351
Miller RM, Jastrow JD (1992) The role of mycorrhizal fungi in soil conservation. In: Mycorrhizae in sustainable agriculture. pp 29–44
Milleret R, Le Bayon RC, Lamy F, Gobat JM, Boivin P (2009) Impact of roots, mycorrhizas and earthworms on soil physical properties as assessed by shrinkage analysis. J Hydrol 373:499–507
Mummey DL, Antunes PM, Rillig MC (2009) Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol Biochem 41:1173–1179
Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Pietikäinen A, Mikola J, Vestberg M, Setälä H (2009) Defoliation effects on Plantago lanceolata resource allocation and soil decomposers in relation to AM symbiosis and fertilization. Soil Biol Biochem 41:2328–2335
Piotrowski JS, Denich T, Klironomos JN, Graham JM, Rillig MC (2004) The effects of arbuscular mycorrhizas on soil aggregation depend on the interaction between plant and fungal species. New Phytol 164:365–373
Poorter H, Buehler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850
R Development Core Team (2012) R: a language and environment for statistical computing. http://www.r-project.org/
Ridgeway G (2012) Package ‘gbm’—Generalized Boosted Regression Models version 1.6-3.2
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53
Rosenberg NJ, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis version. Sinauer Assoc, Sunderland
Schreiner RP, Bethlenfalvay GJ (1997) Plant and soil response to single and mixed species of arbuscular mycorrhizal fungi under fungicide stress. Appl Soil Ecol 7:93–102
Schreiner RP, Mihara KL, McDaniel H, Bethlenfalvay GJ (1997) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188:199–209
Siddiky MRK, Kohler J, Cosme M, Rillig MC (2012) Soil biota effects on soil structure: interactions between arbuscular mycorrhizal fungal mycelium and collembola. Soil Biol Biochem 50:33–39
Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597
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
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, San Diego, p 605
Tisdall JM (1994) Possible role of soil-microorganisms in aggregation in soils. Plant Soil 159:115–121
Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163
Toljander JF, Santos-Gonzalez JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2012) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109
Veresoglou SD, Rillig MC (2011) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217
Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562
Wagg C, Jansa J, Schmid B, van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009
Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461
Zhou ZY, Sun OJ, Luo ZK, Jin HM, Chen QS, Han XG (2008) Variation in small-scale spatial heterogeneity of soil properties and vegetation with different land use in semiarid grassland ecosystem. Plant Soil 310:103–112
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
This work was funded by a grant from the Deutsche Forschungsgemeinschaft (German Research Foundation). SDV was supported by an EU Marie Curie fellowship. AL was funded by the Dahlem Center of Plant Science of Freie Universität Berlin.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Nico Eisenhauer.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 498 kb)
Rights and permissions
About this article
Cite this article
Leifheit, E.F., Veresoglou, S.D., Lehmann, A. et al. Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374, 523–537 (2014). https://doi.org/10.1007/s11104-013-1899-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-013-1899-2