Biology and Fertility of Soils

, Volume 43, Issue 5, pp 541–548 | Cite as

Effects of a plant parasitic nematode (Heterodera trifolii) on clover roots and soil microbial communities

  • Amy M. Treonis
  • Roger Cook
  • Lorna Dawson
  • Susan J. Grayston
  • Tony Mizen
Original Paper


We studied the effects of the root endoparasitic nematode Heterodera trifolii on rhizodeposition and the root architecture of white clover (Trifolium repens). Rhizosphere solutions were collected from the root systems of plants growing with and without H. trifolii (200 juveniles per inoculated plant) in sand-based microlysimeters. The organic carbon (C) content of these solutions was analyzed, and they were applied to plant-free soils to investigate microbial responses. Although plant biomass was unaffected by nematodes, the architecture of the root systems was significantly altered, with a decrease in overall root length and an increase in the density of lateral branches from the primary root. The presence of nematodes reduced the concentration of organic compounds in the rhizosphere solutions but only on the final sampling date (75 days). Analysis of microbial signature phospholipid fatty acids revealed no change in the structure of the microbial communities in soils to which rhizosphere solutions were applied. However, these microorganisms did respond with changes in substrate utilization patterns (community-level physiological profiles). Microbes in soils that received rhizosphere solutions from the nematode-infected clover showed lower utilization of most substrates but higher utilization of oligosugars. These responses appear to be related to changes in roots and rhizodeposition associated with nematode infection of clover roots. The results of this study suggest that root herbivory can negatively impact carbon-limited soil microbial communities via changes in root architecture that moderate rhizodeposition.


Belowground herbivory CLPPs PLFA Rhizodeposition Root architecture 


  1. Alston DG, Schmitt DP (1988) Development of Heterodera glycines life stages as influenced by temperature. J Nematol 20:366–372PubMedGoogle Scholar
  2. Bardgett RD, Cook R (1998) Functional aspects of soil animal diversity in agricultural grasslands. Appl Soil Ecol 10:263–276CrossRefGoogle Scholar
  3. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268Google Scholar
  4. 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 30:1867–1878CrossRefGoogle Scholar
  5. Bardgett RD, Cook R, Yeates GW, Denton CS (1999a) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33CrossRefGoogle Scholar
  6. Bardgett RD, Denton CS, Cook R (1999b) Below-ground herbivory promotes soil nutrient transfer and root growth in grassland. Ecol Lett 2:357–360CrossRefGoogle Scholar
  7. Berntson GM (1992) A computer-program for characterizing root system branching patterns. Plant Soil 140:145–149CrossRefGoogle Scholar
  8. Bostock RM, Stermer BA (1989) Perspectives on wound healing in resistance to pathogens. Annu Rev Phytopathol 27:343–371CrossRefGoogle Scholar
  9. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid and direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842CrossRefGoogle Scholar
  10. Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon sources in sole carbon utilization tests to discriminate soil microbial communities. J Microbiol Meth 30:33–41CrossRefGoogle Scholar
  11. Dawson LA, Grayston SJ, Murray PJ, Pratt SM (2002) Root feeding behavior of Tipula paludosa (Meig.) (Diptera: Tipulidae) on Lolium perenne (L.) and Trifolium repens (L.). Soil Biol Biochem 34:609–615CrossRefGoogle Scholar
  12. Dawson LA, Grayston SJ, Murray PJ, Cook R, Gange AC, Ross JM, Pratt SM, Duff EI, Treonis A (2003) Influence of pasture management (nitrogen and lime addition and insecticide treatment) on soil organisms and pasture root system dynamics in the field. Plant Soil 255:121–130CrossRefGoogle Scholar
  13. Denton CS, Badgett RD, Cook R, Hobbs PJ (1999) Low amounts of root herbivory positively influence the rhizosphere microbial community in a temperate grassland soil. Soil Biol Biochem 31:155–165CrossRefGoogle Scholar
  14. Federle TW (1986) Microbial distribution in the soil—new techniques. In: Megusar F, Gantar M (eds) Perspectives in microbial ecology. Slovene Society for Microbiology, Ljubljana, pp 493–498Google Scholar
  15. Ferris JM, Ferris VR (1998) Biology of plant-parasitic nematodes. In: Barker KR, Pederson GA, Windham GL (eds) Plant and nematode interactions. American Society of Agronomy, Madison, pp 21–35Google Scholar
  16. Garland JL (1996) Analytical approaches to the characterisation of samples of microbial communities using patterns of potential C source utilisation. Soil Biol Biochem 28:213–221CrossRefGoogle Scholar
  17. Garland JL, Mills AL (1991) Classification and characterisation of heterotrophic microbial communities on the basis of patterns of community-level-sole-carbon-source utilisation. Appl Environ Microbiol 57:2351–2359PubMedGoogle Scholar
  18. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56CrossRefGoogle Scholar
  19. Grayston SJ, Dawson LA, Treonis AM, Murray PH, Ross J, Reid EJ, MacDougall R (2001a) Impact of root herbivory by insect larvae on soil microbial communities. Eur J Soil Biol 37:277–280CrossRefGoogle Scholar
  20. Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001b) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551CrossRefGoogle Scholar
  21. Ingham RE, Detling JK (1990) Effects of root-feeding nematodes on aboveground net primary production in a North American grassland. Plant Soil 121:279–281CrossRefGoogle Scholar
  22. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil-measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 415–471Google Scholar
  23. Moore JC, McCann K, Setala H, de Ruiter PC (2003) Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857Google Scholar
  24. Murray PJ, Hatch DJ, Cliquet JB (1996) Impact of insect root herbivory on the growth and nitrogen and carbon contents of white clover (Trifolium repens) seedlings. Can J Bot 74:1591–1595Google Scholar
  25. Nannipieri P, Ascher J, Cecccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  26. Pederson GA, Quesenberry KH (1998) Clovers and other forage legumes. In: Barker KR, Pederson GA, Windham GL (eds) Plant and nematode interactions. American Society of Agronomy, Madison, pp 399–425Google Scholar
  27. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894PubMedCrossRefGoogle Scholar
  28. Thornton B, Millard P, Galloway S (1993) The effects of temperature and form of nitrogen supply on the relative contribution of root uptake and remobilisation in supplying nitrogen for laminae regrowth of Lolium perenne L. J Exp Bot 44:1601–1606CrossRefGoogle Scholar
  29. Treonis AM, Grayston SJ, Murray PJ, Dawson LA (2005) Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Appl Soil Ecol 28:203–215CrossRefGoogle Scholar
  30. Tu C, Koenning SR, Hu S (2003) Root-parasitic nematodes enhance soil microbial activities and nitrogen mineralization. Microbial Ecol 46:134–144CrossRefGoogle Scholar
  31. Van der Putten WH, Anderson JM, Bardgett RD, Behan-Pelletier V, Bignell DE, Brown GG, Brown VK, Brussard L, Hunt HW, Ineson P, Jones TH, Lavelle P, Paul EA, St. John M, Wardle DA, Wojtowicz T, Wall DH (2004) The sustainable delivery of good and services provided by soil biota. In: DH Wall (ed) Sustaining biodiversity and ecosystem services in soils and sediments. Island, Washington, pp 15–43Google Scholar
  32. VanHecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:99–107CrossRefGoogle Scholar
  33. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  34. Yeates GW, Saggar S, Denton CD, Mercer CF (1998) Impact of clover cyst nematode (Heterodera trifolii) infection on soil microbial activity in the rhizosphere of white clover (Trifolium repens)—a pulse-labelling experiment. Nematologica 44:81–90CrossRefGoogle Scholar
  35. Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Amy M. Treonis
    • 1
    • 3
  • Roger Cook
    • 2
  • Lorna Dawson
    • 1
  • Susan J. Grayston
    • 1
    • 4
  • Tony Mizen
    • 2
  1. 1.The Macaulay InstituteCraigiebucklerUK
  2. 2.Institute for Grassland and Environmental ResearchAberystwyth Research StationAberystwythUK
  3. 3.Department of BiologyUniversity of RichmondRichmondUSA
  4. 4.Department of Forest SciencesUniversity of British ColumbiaVancouverCanada

Personalised recommendations