, Volume 27, Issue 5, pp 431–440 | Cite as

Arbuscular mycorrhizal fungus responses to disturbance are context-dependent

  • Mieke van der Heyde
  • Brian Ohsowski
  • Lynette K. Abbott
  • Miranda Hart
Original Article


Anthropogenic disturbance is one of the most important forces shaping soil ecosystems. While organisms that live in the soil, such as arbuscular mycorrhizal (AM) fungi, are sensitive to disturbance, their response is not always predictable. Given the range of disturbance types and differences among AM fungi in their growth strategies, the unpredictability of the responses of AM fungi to disturbance is not surprising. We investigated the role of disturbance type (i.e., soil disruption, agriculture, host perturbation, and chemical disturbance) and fungus identity on disturbance response in the AM symbiosis. Using meta-analysis, we found evidence for differential disturbance response among AM fungal species, as well as evidence that particular fungal species are especially susceptible to certain disturbance types, perhaps because of their life history strategies.

Key words

AMF Agriculture Root colonization Disturbance types Life history strategies 



MMH was funded by an NSERC Discovery Grant as well as a Gledden Fellowship through the Institute of Advanced Studies at The University of Western Australia. Thanks to Kristin Aleklett for helping with data collection.

Supplementary material

572_2016_759_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 25 kb)
572_2016_759_MOESM2_ESM.txt (257 kb)
ESM 2 (TXT 256 kb)


  1. Avio L, Castaldini M, Fabiani A, Bedini S, Sbrana C, Turrini A, Giovannetti M (2013) Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol and Biochem 67:285–294CrossRefGoogle Scholar
  2. Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98(4):745–753CrossRefGoogle Scholar
  3. Berga M, Szekely AJ, Langenheder S (2012) Effects of disturbance intensity and frequency on bacterial community composition and function. PLoS One 7(5):1–11CrossRefGoogle Scholar
  4. Biermann B, Linderman RG (1983) Use of vesicular-arbuscular mycorrhizal roots, intraradical vesicles and extraradical vesicles as inoculum. New Phytol 95(1):97–105CrossRefGoogle Scholar
  5. Boerner REJ, DeMars BG, Leicht PN (1996) Spatial patterns of mycorrhizal infectiveness of soils long a successional chronosequence. Mycorrhiza 6(2):79–90CrossRefGoogle Scholar
  6. Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol and Fert of Soils 48:911–922CrossRefGoogle Scholar
  7. Brundrett MC, Ashwath N (2013) Glomeromycotan mycorrhizal fungi from tropical Australia III. Measuring diversity in natural and disturbed habitats. Plant Soil 370(1–2):419–433CrossRefGoogle Scholar
  8. Brundrett MC, Jasper DA, Ashwath N (1999) Glomalean mycorrhizal fungi from tropical Australia: II. The effect of nutrient levels and host species on the isolation of fungi. Mycorrhiza 8(6):315–321CrossRefGoogle Scholar
  9. Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Tr in Plnt Sci 18(9):484–491CrossRefGoogle Scholar
  10. Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192(1):15–22CrossRefGoogle Scholar
  11. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310CrossRefPubMedGoogle Scholar
  12. Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbio Ecol 78(1):103–115CrossRefGoogle Scholar
  13. de la Providenicia IE, de Souza FA, Fernandez F, Delmas NS, Declerck S (2005) Arbuscular mycorrhizal fungi reveal distinct patterns of anastomosis and hyphal formation mechanisms healing between different phylogenic groups. New Phytol 165(1):261–271CrossRefGoogle Scholar
  14. de Souza FA, Dalpe Y, Declerck S, de la Provedencia IE, Sejalon-Delmas N (2005) Life history strategies in Gigasporaceae: insight from monoxenic culture. In: Declerck S, Strullu DG, Fortin A (eds) Soil biology, vol 4. Spriner, Berlin HeidelbergGoogle Scholar
  15. Declerck S, D’Or D, Bivort C, de Souza FA (2004) Development of extraradical mycelium of Scutellospora reticulata under root-organ culture: spore production and function of auxiliary cells. Mycol Rsch 108:84–92CrossRefGoogle Scholar
  16. Deorr TB, Redente EF, Reeves FB (1984) Effects of soil disturbance on plant succession and levels of mycorrhizal fungi in a sagebrush-grassland community. J of Rnge Mgmt 37(2):135–139CrossRefGoogle Scholar
  17. Douds DD, Galvez L, Janke RR, Wagoner P (1995) Effect of tillage and farming system upon populations and distribution of vesicular-arbuscular mycorrhizal fungi. Agri, Ecosys and Env 52:111–118CrossRefGoogle Scholar
  18. Estaun MV (1989) Effect of sodium chloride and mannitol on germination and hyphal growth of the vesiculararbuscular mycorrhizal fungus Glomus mossae. Agric Ecosyst Environ 29:123–129CrossRefGoogle Scholar
  19. Evans DG, Miller MH (1988) Vesicular-arbuscular mycorrhizas and the soil-disturbance-induced reduction of nutrient absorption in maize. I. Causal relations. New Phytol 110:67–74CrossRefGoogle Scholar
  20. Evans DG, Miller MH (1990) The role of the external mycelial network in the effect of soil disturbance upon vesicular—arbuscular mycorrhizal colonization of maize. New Phytol 114:65–71CrossRefGoogle Scholar
  21. FAO (2011) The state of the world’s land and water resources for food and agriculture, managing systems at risk. Food and Agriculture Organization of the United Nations, Rome and Earthscan, LondonGoogle Scholar
  22. Fichtner A, von Oheimb G, Hardtle W, Wilken C, Gutknecht JLM (2014) Effects of anthropogenic disturbances on soil microbial communities in oak forests persist for more than 100 Years. Soil Biol and Biochem 70:79–87CrossRefGoogle Scholar
  23. Fitter AH (2005) Darkness visible: reflections on underground ecology. J of Ecol 93:231–243CrossRefGoogle Scholar
  24. Gehring CA, Whitham TG (2002) Mycorrhiza-herbivore interactions: population and community consequences. In: Van Der Heijden M, Sanders I (eds) Mycorrhizal Ecology. Springer, New York, pp 295–320CrossRefGoogle Scholar
  25. Guadarrama P, Castillo S, Ramos-Zapata JA, Hernández-Cuevas LV, Camargo-Ricalde SL (2014) Arbuscular mycorrhizal fungal communities in changing environments: the effects of seasonality and anthropogenic disturbance in a seasonal dry forest. Pedobiologia 57(2):87–95CrossRefGoogle Scholar
  26. Hart MM, Reader RJ (2002a) Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biol and Fert of Soils 36(5):357–366CrossRefGoogle Scholar
  27. Hart MM, Reader RJ (2002b) Does percent root length colonization and soil hyphal length reflect the extent of colonization for all AMF? Mycorrhiza 12(6):297–301CrossRefPubMedGoogle Scholar
  28. Hart MM, Reader RJ (2002c) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153(2):335–344CrossRefGoogle Scholar
  29. Hart MM, Reader RJ (2004) Do arbuscular mycorrhizal fungi recover from soil disturbance differently? Trop Ecol 45(1):97–111Google Scholar
  30. Hart MM, Reader RJ (2005) The role of the external mycelium in early colonization for three arbuscular mycorrhizal fungal species with different colonization strategies. Pedobiologia 49(3):269–279CrossRefGoogle Scholar
  31. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JP (1998) Ploughing up the wood-wide web? Nature 394(6692):431CrossRefPubMedGoogle Scholar
  32. Hokka V, Mikola J, Vestberg M, Setälä H (2004) Interactive effects of defoliation and an AM fungus on plants and soil organisms in experimental legume-grass communities. Oikos 106(1):73–84CrossRefGoogle Scholar
  33. Huston MA (1994) Biological diversity. Cambridge University PressGoogle Scholar
  34. Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12(5):225–234CrossRefPubMedGoogle Scholar
  35. Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13(4):1164–1176CrossRefGoogle Scholar
  36. Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276(1–2):163–176CrossRefGoogle Scholar
  37. Jansa J, Wiemken A, Frossard E (2006) The effects of agricultural practices on arbuscular mycorrhizal fungi. Geol Soc, London, Spec Pub 266(1):89–115CrossRefGoogle Scholar
  38. Jasper DA, Robson AD, Abbot LK (1989) Soil disturbance hyphae of reduces the infectivity of external hyphae of vesicular-arbuscular mycorrhizal fungi. New Phytol 112(1):93–99CrossRefGoogle Scholar
  39. Jasper DA, Abbott LK, Robson AD (1991) The effect of soil disturbance on vesicular-arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytol 118(3):471–476CrossRefGoogle Scholar
  40. Jasper DA, Abbott LK, Robson AD (1993) The survival of infective hyphae of vesicular-arbuscular mycorrhizal fungi in dry soil: an interaction with sporulation. New Phytol 124:473–479CrossRefGoogle Scholar
  41. Johnson NC, Zak DR, Tilman D, Pfleger FL (1991) International association for ecology dynamics of vesicular-arbuscular mycorrhizae during old field succession. Oevologia 86(3):349–358Google Scholar
  42. Klironomos JN, Hart MM, Gurney JE, Moutoglis P (2001) Interspecific differences in the tolerance of arbuscular mycorrhizal fungi to freezing and drying. Can J of Bot 79(10):1161–1166CrossRefGoogle Scholar
  43. Knapp G, Hartung J (2003) Improved tests for a random effects meta-regression with a single covariate. Stat in Med 22:2693–2710CrossRefGoogle Scholar
  44. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc of the Nat Acad of Sci 101(8):2369–2374CrossRefGoogle Scholar
  45. Koch, AM, Antunes PM, Maherali H, Hart M, Klironomos J (2017) Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. New Phytologist: in pressGoogle Scholar
  46. Köhl L, Oehl F, van der Heijden MGA (2014) Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecol Appl 24(7):1842–1853CrossRefGoogle Scholar
  47. Lekberg Y, Schnoor TK, Kjøller R, Gibbons SM, Hansen LH, Al-Soud WA, Sørensen SJ, Rosendahl S (2012) 454-Sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J of Ecol 100:151–160CrossRefGoogle Scholar
  48. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316(5832):1746–1748CrossRefPubMedGoogle Scholar
  49. Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J (2005) Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 16(1):61–66CrossRefPubMedGoogle Scholar
  50. McGonigle T, Miller M (1993) Responses of mycorrhizae and shoot phosphorus of maize to the frequency and timing of soil disturbance. Mycorrhiza 4:63–68CrossRefGoogle Scholar
  51. McGonigle T, Miller M (1996) Development of fungi below ground in association with plants growing in disturbed and undisturbed soils. Soil Biol Biochem 28:263–269CrossRefGoogle Scholar
  52. McGonigle T, Miller M (2000) The inconsistent effect of soil disturbance on colonization of roots by arbuscular mycorrhizal fungi: a test of the inoculum density hypothesis. Appl Soil Ecol 14:147–155CrossRefGoogle Scholar
  53. McIntyre S, Lavorel S, Tremont RM (1995) Plant life-history attributes : their relationship to disturbance. Ecol 83(1):31–44CrossRefGoogle Scholar
  54. McMillen BG, Juniper S, Abbott LK (1998) Inhibition of hyphal growth of a vesicular-arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biol Biochem 30(13):1639–1646Google Scholar
  55. Moora M, Davison J, Opik M, Metsis M, Saks U, Jairus T, Vasar M, Zobel M (2014) Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 90(3):609–621CrossRefPubMedGoogle Scholar
  56. Morton JB, Redecker D (2001) Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93(1):181–195CrossRefGoogle Scholar
  57. Munkvold L, Kjller R, Vestberg M, Rosendahl S (2004) Functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164(2):357–364CrossRefGoogle Scholar
  58. Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from in the field root pathogenic fungi. J of Ecol 83(6):991–1000CrossRefGoogle Scholar
  59. Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agri, Ecosys & Env 134:257–268CrossRefGoogle Scholar
  60. Opik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188(1):223–241CrossRefPubMedGoogle Scholar
  61. Peyret-Guzzon M, Stockinger H, Bouffaud ML, Farcy P, Wipf D, Redecker D (2016) Arbuscular mycorrhizal fungal communities and Rhizophagus irregularis populations shift in response to short-term ploughing and fertilisation in a buffer strip. Mycorrhiza 26(1):33–46CrossRefPubMedGoogle Scholar
  62. Picone C (2006) Diversity and abundance of arbuscular-mycorrhizal fungus spores in tropical forest and pasture. Biotropica 32(4a):734–750CrossRefGoogle Scholar
  63. Porter WM, Robson AD, Abbott LK (1987) Field survey of the distribution of vesicular-arbuscular mycorrhizal fungi in relation to soil pH. J Appl Ecol 24(2):659Google Scholar
  64. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc Biol Sci/The Roy Soc 276(1676):4237–4245CrossRefGoogle Scholar
  65. Pringle A, Bever JD (2002) Divergent Phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Amer J of Bot 89(9):1439–1446CrossRefGoogle Scholar
  66. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL
  67. Ropars J, Corradi N (2015) Homokaryotic vs heterokaryotic mycelium in arbuscular mycorrhizal fungi: different techniques, different results? New Phytol 208:638–641CrossRefPubMedGoogle Scholar
  68. Rosendahl S, Matzen HB (2008) Genetic structure of arbuscular mycorrhizal populations in fallow and cultivated soils. New Phytol 179(4):1154–1161CrossRefPubMedGoogle Scholar
  69. Rúa MA, Antonnika A, Antunes PM, Chaudhary BV, Gehring C, Lamity LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Laieunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122. doi: 10.1186/s12862-016-0698-9 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21(3):211–220CrossRefPubMedGoogle Scholar
  71. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164(9):1144–1151Google Scholar
  72. Sharmah D, Jha DK (2014) Diversity of arbuscular mycorrhizal fungi in disturbed and undisturbed forests of Karbi Anglong Hills of Assam, India. Agri Rsch 3:229–238CrossRefGoogle Scholar
  73. Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J of Ecol 97(6):1274–1280CrossRefGoogle Scholar
  74. Soteras F, Grilli G, Cofré MN, Marro N, Becerra A (2015) Arbuscular mycorrhizal fungal composition in high montane forests with different disturbance histories in Central Argentina. Appl Soil Ecol 85:30–37CrossRefGoogle Scholar
  75. Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300(5622):1138–1140CrossRefPubMedGoogle Scholar
  76. Stahl PD, Williams SE, Christensen M (1988) Efficacy of native vesicular-arbuscular mycorrhizal fungi after severe soil disturbance. New Phytol 110:347–354CrossRefGoogle Scholar
  77. Stover HJ, Thorn RG, Bowles JM, Bernards MA, Jacobs CR (2012) Arbuscular mycorrhizal fungi and vascular plant species abundance and community structure in tallgrass prairies with varying agricultural disturbance histories. Appl Soil Ecol 60:61–70CrossRefGoogle Scholar
  78. Tommerup IC (1983) Temperature relations of spore germination and hyphal growth of vesicular-arbuscular mycorrhizal fungi in soil. Trans of the Brit Mycol Soc 81(2):381–387CrossRefGoogle Scholar
  79. Torrecillas E, Alguacil MM, Roldan A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78(17):6180–6186CrossRefPubMedPubMedCentralGoogle Scholar
  80. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorous, and atmospheric CO2 in field studies. New Phytol 164:347–355Google Scholar
  81. Treseder KK, Mack MC, Cross A (2004) Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl 14(6):1826–1838CrossRefGoogle Scholar
  82. Uibopuu A, Moora M, Saks Ü, Daniell T, Zobel M, Öpik M (2009) Differential effect of arbuscular mycorrhizal fungal communities from ecosystems along management gradient on the growth of forest understorey plant species. Soil Biol Biochem 41(10):2141–2146CrossRefGoogle Scholar
  83. Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11(8):1555–1564CrossRefPubMedGoogle Scholar
  84. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J of Stat Softw 36(3):1–48CrossRefGoogle Scholar
  85. Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem Multifunctionality. Proc of the Nat Acad of Sci of the USA 111(14):5266–5270CrossRefGoogle Scholar
  86. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633Google Scholar
  87. Wetzel K, Silva G, Matczinski U, Oehl F, Fester T (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol and Biochem 72:88–96CrossRefGoogle Scholar
  88. Wright SF, Starr JL, Paltineanu IC (1999) Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci Soc of Am J 63(6):1825CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Mieke van der Heyde
    • 1
  • Brian Ohsowski
    • 2
  • Lynette K. Abbott
    • 3
  • Miranda Hart
    • 1
  1. 1.BiologyUniversity of British Columbia OkanaganKelownaCanada
  2. 2.Institute of Environmental Sustainability, Lakeshore CampusLoyola University ChicagoChicagoUSA
  3. 3.School of Earth and Environment, The UWA Institute of Agriculture, Faculty of ScienceThe University of Western AustraliaPerthAustralia

Personalised recommendations