Advertisement

Plant and Soil

, Volume 410, Issue 1–2, pp 273–281 | Cite as

Unraveling the role of hyphal networks from arbuscular mycorrhizal fungi in aggregate stabilization of semiarid soils with different textures and carbonate contents

  • J. Kohler
  • A. Roldán
  • M. Campoy
  • F. Caravaca
Regular Article

Abstract

Aims

Our study was intended to elucidate the involvement of three species of arbuscular mycorrhizal fungi (AMF) in the formation and stabilization of aggregates in semiarid soils with different textures and calcium carbonate contents.

Methods

We used a root-hyphae compartment approach to compare the effect of three AMF (Rhizophagus irregularis, Septoglomus deserticola, and Gigaspora gigantea) on the structural stability of the hyphosphere (root-free hyphae) and mycorrhizosphere (hyphae + root) soil of Olea europaea plants grown in two soils differing in their texture (sandy loam and silty loam) and calcium carbonate content.

Results

Only the R. irregularis strain significantly increased the percentage of stable aggregates in both types of soil, being the increases higher in the hyphosphere compartment (on average, about 30 % compared to non-inoculated soil). In the hyphosphere compartment of both soils, the hyphal length developed by plants inoculated with R. irregularis was 81 % greater than that of non-inoculated plants. The effect of the AMF on soil aggregation was mediated by mechanical entanglement of mycorrhizal fungal hyphae but without a contribution of labile carbohydrates.

Conclusion

The ability of extraradical hyphae to improve soil structure was independent of the soil texture and content of carbonates.

Keywords

Aggregate stability AMF Hyphosphere Mycorrhizal hyphae Semiarid soils 

Notes

Acknowledgements

This research was supported by the Seneca Foundation (Project FS-11828/PI/09). The authors wish to thank Dr. D.J. Walker for the English revision.

References

  1. Asano M, Wagai R (2014) Evidence of aggregate hierarchy at micro- to submicron scales in an allophanic Andisol. Geoderma 216:62–74CrossRefGoogle Scholar
  2. Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496CrossRefGoogle Scholar
  3. Black CA, Evans DD, White JL, Ensminger LE, Clark FE (1965) Methods of soil analysis. Part 2. ASA and SSSA, Madison, Wisconsin, USAGoogle Scholar
  4. Brink RH, Dubach P, Lynch DL (1960) Measurements of carbohydrates in soil hydrolyzates with anthrone. Soil Sci 89:157–166CrossRefGoogle Scholar
  5. Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22CrossRefGoogle Scholar
  6. Caravaca F, Barea JM, Figueroa D, Roldán A (2002a) Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for enhancing reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Appl Soil Ecol 20:107–118CrossRefGoogle Scholar
  7. Caravaca F, Hernández T, García C, Roldán A (2002b) Improvement of rhizosphere aggregate stability of afforested semiarid plant species subjected to mycorrhizal inoculation and compost addition. Geoderma 108:133–144CrossRefGoogle Scholar
  8. Caravaca F, Lax A, Albaladejo J (2004) Aggregate stability and carbon characteristics of particle-size fractions in cultivated and forested soils of semiarid Spain. Soil Till Res 78:83–90CrossRefGoogle Scholar
  9. Caravaca F, Alguacil MM, Barea JM, Roldán A (2005) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem 37:227–233CrossRefGoogle Scholar
  10. Chenu C, Le Bissonnais Y, Arrouays D (2000) Organic matter influence on clay wettability and soil aggregate stability. Soil Sci Soc Am J 64:1479–1486CrossRefGoogle Scholar
  11. Chivenge P, Vanlauwe B, Gentile R, Six J (2011) Comparison of organic versus mineral resource effects on short-term aggregate carbon and nitrogen dynamics in a sandy soil versus a fine textured soil. Agric Ecosyst Environ 140:361–371CrossRefGoogle Scholar
  12. Daynes CN, Field DJ, Saleeba JA, Cole MA, McGee PA (2013) Development and stabilisation of soil structure via interactions between organic matter, arbuscular mycorrhizal fungi and plant roots. Soil Biol Biochem 57:683–694CrossRefGoogle Scholar
  13. Degens BP, Sparling GP, Abbott LK (1996) Increasing the length of hyphae in a sandy soil increases the amount of water-stable aggregates. Appl Soil Ecol 3:149–159CrossRefGoogle Scholar
  14. Fernández C, Alonso C, Babín MM, Pro J, Carbonell G, Tarazona JV (2004) Ecotoxicological assessment of doxycycline in aged pig manure using multispecies soil systems. Sci Total Environ 323:63–69CrossRefPubMedGoogle Scholar
  15. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–499CrossRefGoogle Scholar
  16. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13CrossRefPubMedGoogle Scholar
  17. Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation—a meta-analysis. Plant Soil 374:523–537CrossRefGoogle Scholar
  18. Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer, Dordrecht, pp 3–18CrossRefGoogle Scholar
  19. Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphae production of vesicular-arbuscular mycorrhizal fungi in pasture and tail grass prairie communities. Oecologia 103:17–23CrossRefGoogle Scholar
  20. Muthukumar T, Udaiyan K (2000) Influence of organic manures on arbuscular mycorrhizal fungi associated with Vigna unguiculata (L.) Walp. in relation to tissue nutrients and soluble carbohydrate in roots under field conditions. Biol Fertil Soils 31:114–120CrossRefGoogle Scholar
  21. Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337CrossRefGoogle Scholar
  22. Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400CrossRefGoogle Scholar
  23. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  24. 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 164:365–373CrossRefGoogle Scholar
  25. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 17:41–53CrossRefGoogle Scholar
  26. Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119:572–577CrossRefGoogle Scholar
  27. Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191CrossRefGoogle Scholar
  28. Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388CrossRefPubMedGoogle Scholar
  29. Roldán A, García-Orenes F, Lax A (1994) An incubation experiment to determine factors involving aggregation changes in an arid soil receiving urban refuse. Soil Biol Biochem 26:1699–1707CrossRefGoogle Scholar
  30. Roldán A, Carrasco L, Caravaca F (2006) Stability of desiccated rhizosphere soil aggregates of mycorrhizal Juniperus oxycedrus grown in a desertified soil amended with a composted organic residue. Soil Biol Biochem 38:2722–2730CrossRefGoogle Scholar
  31. Schreiner RP, Mihara KL, McDaniel H, Bethlenfalvay GJ (1997) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188:199–209CrossRefGoogle Scholar
  32. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  33. 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 Till Res 79:7–31CrossRefGoogle Scholar
  34. Skidmore EL, Layton JB (1992) Dry-soil aggregate stability as influenced by selected soil properties. Soil Sci Soc Am J 56:557–561CrossRefGoogle Scholar
  35. SSS (2010) Keys to Soil Taxonomy, first Ed. USDA. Natural Resources Conservation Service, Washington DCGoogle Scholar
  36. Tisdall JM (1994) Possible role of soil-microorganisms in aggregation in soils. Plant Soil 159:115–121CrossRefGoogle Scholar
  37. Tisdall JM, Oades JM (1982) Organic matter and water stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  38. Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78:6180–6186CrossRefPubMedPubMedCentralGoogle Scholar
  39. Virto I, Gartzia-Bengoetxea N, Fernandez-Ugalde O (2011) Role of organic matter and carbonates in soil aggregation estimated using laser diffractometry. Pedosphere 21:566–572CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • J. Kohler
    • 1
    • 2
  • A. Roldán
    • 3
  • M. Campoy
    • 3
  • F. Caravaca
    • 3
  1. 1.Institut für Biologie, Plant EcologyFreie Universität BerlinBerlinGermany
  2. 2.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany
  3. 3.Department of Soil and Water ConservationCSIC-Centro de Edafología y Biología Aplicada del SeguraMurciaSpain

Personalised recommendations