Biology and Fertility of Soils

, Volume 55, Issue 8, pp 789–800 | Cite as

Sequential defoliation impacts on colonisation of roots of Lolium rigidum by arbuscular mycorrhizal fungi were primarily determined by root responses

  • Jing-Wei FanEmail author
  • Zakaria M. Solaiman
  • Bede S. Mickan
  • Yan-Lei Du
  • Feng-Min Li
  • Lynette K. Abbott
Original Paper


Defoliation often has little effect on the percent plant root length colonised by arbuscular mycorrhizal (AM) fungi, and this has been interpreted as a lack of support for the carbon limitation hypothesis. We performed an experiment with three levels of repeated defoliation (none, every 3 weeks and weekly) of Lolium rigidum growing in pasture soil, and assessed colonisation of roots by naturally occurring AM fungi over 4 months in the glasshouse. Surprisingly, the percent root length colonised by AM fungi increased with defoliation. We also assessed root mass and the length of colonised root to obtain an estimate of the quantity of mycorrhizal root. As expected, both root mass and length of mycorrhizal root decreased with defoliation, as did soluble sugars in the roots. Thus, increasing the frequency of defoliation reduced mycorrhizas consistent with the carbon-limitation hypothesis. Such a decline in mass of mycorrhizal root could contribute to reducing soil biological fertility in pastures over time.


Carbon limitation hypothesis Grazing Pasture Rhizosphere Soluble carbon Arbuscular mycorrhiza 



Jing-Wei Fan appreciated financial support from the China Scholarship Council for 18 months of study at The University of Western Australia (UWA). We thank Professor Jacob Weiner at University of Copenhagen and two anonymous reviewers for helpful comments on an earlier version of the paper.

Funding information

This research was supported by the National Nature Science Foundation of China (31700333), the ‘111’ programme (2007B051), Chinese Postdoctoral Science Foundation (2017M613241) and the Fundamental Research Funds for Central Universities (lzujbky-2018-it08).


  1. Abbott LK, Robson AD (1978) Growth of subterranean clover in relation to the formation of endomycorrhizas by introduced and indigenous fungi in a field soil. New Phytol 81:575–585. CrossRefGoogle Scholar
  2. Abbott LK, Robson AD (1981a) Infectivity and effectiveness of five endomycorrhizal fungi: competition with indigenous fungi in field soils. Aust J Agric Res 32:621–630. CrossRefGoogle Scholar
  3. Abbott LK, Robson AD (1981b) Infectivity and effectiveness of vesicular arbuscular mycorrhizal fungi: effect of inoculum type. Aust J Agric Res 32:631–639. CrossRefGoogle Scholar
  4. Abbott LK, Lumley S (2014) Assessing economic benefits of arbuscular mycorrhizal fungi as a potential indicator of soil health. In: Solaiman ZM, Abbott LK, Varma A (Eds) Mycorrhizal Fungi: use in sustainable agriculture and land restoration, Soil biology, vol 41. Springer, Berlin, pp 17–31. CrossRefGoogle Scholar
  5. Abbott LK, Johnson NC (2017) Introduction: perspectives on mycorrhizas and soil fertility. In: Johnson NC, Gehring C, Jansa J (Eds) Mycorrhizal mediation of soil: fertility, structure, and carbon storage. Elsevier, Dordrecht, pp 93–105. CrossRefGoogle Scholar
  6. Allsopp N (1998) Effect of defoliation on the arbuscular mycorrhizas of three perennial pasture and rangeland grasses. Plant Soil 202:117–124. CrossRefGoogle Scholar
  7. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268. CrossRefGoogle Scholar
  9. Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878. CrossRefGoogle Scholar
  10. Barto EK, Rillig MC (2010) Does herbivory really suppress mycorrhiza? A meta-analysis. J Ecol 98:745–753. CrossRefGoogle Scholar
  11. 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. CrossRefGoogle Scholar
  12. Bazot S, Mikola J, Nguyen C, Robin C (2005) Defoliation-induced changes in carbon allocation and root soluble carbon concentration in field-grown Lolium perenne plants: do they affect carbon availability, microbes and animal trophic groups in soil? Funct Ecol 19:886–896. CrossRefGoogle Scholar
  13. Blakemore LC, Searle PL, Daly BK (1987) Methods for chemical analysis of soils. NZ Soil Bureau scientific report, vol 80. Department of Scientific and Industrial Research, Lower HuttGoogle Scholar
  14. Bourdôt GW, Leathwick DM, Hurrell GA (2000) Longevity of Californian thistle roots. In: Zydenbos SM (Eds) New Zealand plant protection, New Zealand Plant Protection Society, vol 53. Inc, Havelock North, pp 258–261Google Scholar
  15. Camenzind T, Homeier J, Dietrich K, Hempel S, Hertel D, Krohn A, Leuschner C, Oelmann Y, Olsson PA, Suárez JP, Rillig MC (2016) Opposing effects of nitrogen versus phosphorus additions on mycorrhizal fungal abundance along an elevational gradient in tropical montane forests. Soil Biol Biochem 94:37–47. CrossRefGoogle Scholar
  16. Carvalho M, Brito I, Alho L, Goss MJ (2015) Assessing the progress of colonization by arbuscular mycorrhiza of four plant species under different temperature regimes. J Plant Nutr Soil Sci 178:515–522. CrossRefGoogle Scholar
  17. Chen SM, Lin S, Loges R, Reinsch T, Hasler M, Taube F (2016) Independence of seasonal patterns of root functional traits and rooting strategy of a grass-clover sward from sward age and slurry application. Grass Forage Sci 71:607–621. CrossRefGoogle Scholar
  18. Colwell J (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust J Exp Agric Anim Husb 3:190–197CrossRefGoogle Scholar
  19. Dawson LA, Grayston SJ, Paterson E (2000) Effects of grazing on the roots and rhizosphere of grasses. In: Lemaire G, Hodgson J, de Moraes A, Nabinger C, de F Carvalho PC (Eds) Grassland ecophysiology and grazing ecology. CABI Publishing, Wallingford, pp 61–84Google Scholar
  20. 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 3:149–159. CrossRefGoogle Scholar
  21. Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60. CrossRefGoogle Scholar
  22. Elliott GA, Robson AD, Abbott LK (1993) Effects of phosphate and nitrogen application on death of the root cortex in spring wheat. New Phytol 123:375–382. CrossRefGoogle Scholar
  23. Fan J-W, Du Y-L, Wang B-R, Turner NC, Wang T, Abbott LK, Stefanova K, Siddique KHM, Li F-M (2016) Forage yield, soil water depletion, shoot nitrogen and phosphorus uptake and concentration, of young and old stands of alfalfa in response to nitrogen and phosphorus fertilisation in a semiarid environment. Field Crop Res 198:247–257. CrossRefGoogle Scholar
  24. Gazey C, Abbott LK, Robson AD (1993) VA mycorrhizal spores from three species of Acaulospora: germination, longevity and hyphal growth. Mycol Res 97:785–790. CrossRefGoogle Scholar
  25. Gazey C, Abbott LK, Robson AD (2004) Indigenous and introduced arbuscular mycorrhizal fungi contribute to plant growth in two agricultural soils from south-western Australia. Mycorrhiza 14:355–362. CrossRefPubMedGoogle Scholar
  26. Gehring CA, Whitham TG (2002) Mycorrhizae-herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (Eds) Mycorrhizal ecology, Ecological studies (analysis and synthesis), vol 157. Springer, Berlin, pp 295–320. CrossRefGoogle Scholar
  27. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. CrossRefGoogle Scholar
  28. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  29. Hamilton EW, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873. CrossRefGoogle Scholar
  30. Hart MM, Reader RJ (2002) Does percent root length colonization and soil hyphal length reflect the extent of colonization for all AMF? Mycorrhiza 12:297–301. CrossRefPubMedGoogle Scholar
  31. Hartley SE, Amos L (1999) Competitive interactions between Nardus stricta L. and Calluna vulgaris (L.) Hull: the effect of fertilizer and defoliation on above- and below-ground performance. J Ecol 87:330–340. CrossRefGoogle Scholar
  32. Hepper CM (1985) Influence of age of roots on the pattern of vesicular-arbuscular mycorrhizal infection in leek and clover. New Phytol 101:685–693. CrossRefGoogle Scholar
  33. Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289. CrossRefPubMedGoogle Scholar
  34. Huang B (2000) Role of root morphological and physiological characteristics in drought resistance of plants. In: Wilkinson RE (Eds) Plant-environmental interactions. Marcel Dekker Inc., New York, pp 39–64Google Scholar
  35. Ijdo M, Schtickzelle N, Cranenbrouck S, Declerck S (2010) Do arbuscular mycorrhizal fungi with contrasting life-history strategies differ in their responses to repeated defoliation? FEMS Microbiol Ecol 72:114–122. CrossRefPubMedGoogle Scholar
  36. Isbell RF (2002) The Australian soil classification, vol 4. CSIRO Publishing, Collingwood, AustraliaCrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. Jakobsen I, Gazey C, Abbott LK (2001) Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol 149:95–103. CrossRefGoogle Scholar
  39. Johnson NC, Gehring C, Jansa J (2017) Mycorrhizal mediation of soil: fertility, structure, and carbon storage. Elsevier, NetherlandsGoogle Scholar
  40. Kempers AJ, Luft AG (1988) Re-examination of the determination of environmental nitrate as nitrite by reduction with hydrazine. Analyst 113:1117–1120. CrossRefPubMedGoogle Scholar
  41. Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, Delaux P-M, Klingl V, Röpenack-Lahaye Ev, Wang TL, Eisenreich W, Dörmann P, Parniske M, Gutjahr C (2017) Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife 6: e29107.
  42. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. CrossRefGoogle Scholar
  43. Klironomos JN, McCune J, Moutoglis P (2004) Species of arbuscular mycorrhizal fungi affect mycorrhizal responses to simulated herbivory. Appl Soil Ecol 26:133–141. CrossRefGoogle Scholar
  44. Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211. CrossRefPubMedGoogle Scholar
  45. Lehmann A, Leifheit EF, Rillig MC (2017) Mycorrhizas and soil aggregation. In: Johnson NC, Gehring C, Jansa J (Eds) Mycorrhizal mediation of soil: fertility, structure, and carbon storage. Elsevier, Dordrecht, pp 241–262. CrossRefGoogle Scholar
  46. Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595. CrossRefGoogle Scholar
  47. López-Mársico L, Altesor A, Oyarzabal M, Baldassini P, Paruelo JM (2015) Grazing increases below-ground biomass and net primary production in a temperate grassland. Plant Soil 392:155–162. CrossRefGoogle Scholar
  48. Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GED, Eastmond PJ (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356:1175–1178. CrossRefPubMedGoogle Scholar
  49. MacLeod WJ, Robson AD, Abbott LK (1986) Effects of phosphate supply and inoculation with a vesicular-arbuscular mycorrhizal fungus on the death of the root cortex of wheat, rape and subterranean clover. New Phytol 103:349–357. CrossRefGoogle Scholar
  50. Marín-Guirao L, Sandoval-Gil JM, Bernardeau-Esteller J, Ruíz JM, Sánchez-Lizaso JL (2013) Responses of the Mediterranean seagrass Posidonia oceanica to hypersaline stress duration and recovery. Mar Environ Res 84:60–75. CrossRefPubMedGoogle Scholar
  51. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501. CrossRefGoogle Scholar
  52. Mendoza R, García I, Deplama D, López CF (2016) Competition and growth of a grass–legume mixture fertilised with nitrogen and phosphorus: effect on nutrient acquisition, root morphology and symbiosis with soil microorganisms. Crop Pasture Sci 67:629–640. CrossRefGoogle Scholar
  53. Mickan BS, Abbott LK, Stefanova K, Solaiman ZM (2016) Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil. Mycorrhiza 26:565–574. CrossRefPubMedGoogle Scholar
  54. Mickan BS, Hart MM, Solaiman ZM, Jenkins S, Siddique KHM, Abbott LK (2017) Molecular divergence of fungal communities in soil, roots and hyphae highlight the importance of sampling strategies. Rhizosphere 4:104–111. CrossRefGoogle Scholar
  55. Mikola J, Kytöviita M-M (2002) Defoliation and the availability of currently assimilated carbon in the Phleum pratense rhizosphere. Soil Biol Biochem 34:1869–1874. CrossRefGoogle Scholar
  56. Miller RM, Miller SP, Jastrow JD, Rivetta CB (2002) Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytol 155:149–162. CrossRefGoogle Scholar
  57. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. CrossRefGoogle Scholar
  58. Nelson DW, Sommers LE (1980) Total nitrogen analysis of soil and plant-tissues. J Assoc Off Anal Chem 63:770–778Google Scholar
  59. Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583. CrossRefPubMedGoogle Scholar
  60. Pearson JN, Schweiger P (1993) Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders associated with subterranean clover: dynamics of colonization, sporulation and soluble carbohydrates. New Phytol 124:215–219. CrossRefGoogle Scholar
  61. Pearson JN, Abbott LK, Jasper DA (1993) Mediation of competition between two colonizing VA mycorrhizal fungi by the host plant. New Phytol 123:93–98. CrossRefGoogle Scholar
  62. 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 55:158–161. CrossRefGoogle Scholar
  63. 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. CrossRefGoogle Scholar
  64. Richards JH (1984) Root growth response to defoliation in two Agropyron bunchgrasses: field observations with an improved root periscope. Oecologia 64:21–25. CrossRefPubMedGoogle Scholar
  65. Rillig MC, Aguilar-Trigueros CA, Camenzind T, Cavagnaro TR, Degrune F, Hohmann P, Lammel DR, Mansour I, Roy J, van der Heijden MGA, Yang G (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol 222:1171–1175. CrossRefPubMedGoogle Scholar
  66. Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170:357–368. CrossRefPubMedGoogle Scholar
  67. Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol 220:1092–1107. CrossRefPubMedGoogle Scholar
  68. Scheltema MA, Abbott LK, Robson AD, De'Ath G (1985) The spread of Glomus fasciculatum through roots of Trifolium subterraneum and Lolium rigidum. New Phytol 100:105–114. CrossRefGoogle Scholar
  69. Scheltema MA, Abbott LK, Robson AD, De’Ath G (1987) The spread of mycorrhizal infection by Gigaspora calospora from a localized inoculum. New Phytol 106:727–734. CrossRefGoogle Scholar
  70. Schwab SM, Menge JA, Tinker PB (1991) Regulation of nutrient transfer between host and fungus in vesicular-arbuscular mycorrhizas. New Phytol 117:387–398. CrossRefGoogle Scholar
  71. Schweiger PF, Robson AD, Barrow JN (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytol 131:247–254. CrossRefGoogle Scholar
  72. Searle PL (1984) The berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. Analyst 109:549–568. CrossRefGoogle Scholar
  73. Sturite I, Henriksen TM, Breland TA (2007) Longevity of white clover (Trifolium repens) leaves, stolons and roots, and consequences for nitrogen dynamics under northern temperate climatic conditions. Ann Bot 100:33–40. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Su Y-Y, Guo L-D (2007) Arbuscular mycorrhizal fungi in non-grazed, restored and over-grazed grassland in the Inner Mongolia steppe. Mycorrhiza 17:689–693. CrossRefPubMedGoogle Scholar
  75. Turrini A, Bedini A, Loor MB, Santini G, Sbrana C, Giovannetti M, Avio L (2018) Local diversity of native arbuscular mycorrhizal symbionts differentially affects growth and nutrition of three crop plant species. Biol Fert Soils 54:203–217. CrossRefGoogle Scholar
  76. van der Heyde M, Bennett JA, Pither J, Hart M (2017) Longterm effects of grazing on arbuscular mycorrhizal fungi. Agric Ecosyst Environ 243:27–33. CrossRefGoogle Scholar
  77. van der Krift TAJ, Berendse F (2002) Root life spans of four grass species from habitats differing in nutrient availability. Funct Ecol 16:198–203. CrossRefGoogle Scholar
  78. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. CrossRefGoogle Scholar
  79. Vierheilig H, Ocampo JA (1991) Susceptibility and effectiveness of vesicular-arbuscular mycorrhizae in wheat cultivars under different growing conditions. Biol Fert Soils 11:290–294. CrossRefGoogle Scholar
  80. Walter J, Grant K, Beierkuhnlein C, Kreyling J, Weber M, Jentsch A (2012) Increased rainfall variability reduces biomass and forage quality of temperate grassland largely independent of mowing frequency. Agric Ecosyst Environ 148:1–10. CrossRefGoogle Scholar
  81. Wang Z, Zhang Q, Staley C, Gao H, Ishii S, Wei X, Liu J, Cheng J, Hao M, Sadowsky MJ (2019) Impact of long-term grazing exclusion on soil microbial community composition and nutrient availability. Biol Fert Soils 55:121–134. CrossRefGoogle Scholar
  82. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. CrossRefPubMedGoogle Scholar
  83. Wearn JA, Gange AC (2007) Above-ground herbivory causes rapid and sustained changes in mycorrhizal colonization of grasses. Oecologia 153:959–971. CrossRefPubMedGoogle Scholar
  84. Wells CE, Eissenstat DM (2003) Beyond the roots of young seedlings: the influence of age and order on fine root physiology. J Plant Growth Regul 21:324–334. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jing-Wei Fan
    • 1
    • 2
    • 3
    Email author
  • Zakaria M. Solaiman
    • 2
    • 3
  • Bede S. Mickan
    • 2
    • 3
  • Yan-Lei Du
    • 1
  • Feng-Min Li
    • 1
  • Lynette K. Abbott
    • 2
    • 3
  1. 1.State Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life SciencesLanzhou UniversityLanzhouChina
  2. 2.UWA School of Agriculture and EnvironmentThe University of Western AustraliaPerthAustralia
  3. 3.UWA Institute of AgricultureThe University of Western AustraliaPerthAustralia

Personalised recommendations