Plant and Soil

, Volume 212, Issue 1, pp 23–33

The influence of nematodes on below-ground processes in grassland ecosystems

  • Richard D. Bardgett
  • Roger Cook
  • Gregor W. Yeates
  • Crystal S. Denton
Article

Abstract

This review summarises recent information on beneficial roles that soil nematodes play in the cycling of carbon and other plant nutrients in grassland ecosystems. In particular, we focus on the role of the two dominant functional groups of nematodes, namely the microbial- and root-feeders, and how their activities may enhance soil ecosystem-level processes of nutrient cycling and, ultimately, plant productivity in managed and unmanaged grassland ecosystems. We report recent experiments which show that low amounts of root herbivory by nematodes can increase the allocation of photoassimilate carbon to roots, leading to increased root exudation and microbial activity in the rhizosphere. The effects of these interactions on soil nutrient cycling and plant productivity are discussed. Evidence is presented to show that the feeding activities of microbial-feeding nematodes can enhance nutrient mineralization and plant nutrient uptake in grasslands, but that these responses are highly species-specific and appear to be strongly regulated by higher trophic groups of fauna (top-down regulation). We recommend that future studies of the roles of nematodes in grasslands ecosystems should consider these more complex trophic interactions and also the effects of species diversity of nematodes on soil ecosystem-level processes.

ecosystem grasslands microorganisms mineralization nematodes roots soil 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altieri M G 1991 How can we best use biodiversity in agroecosystems? Outlook Agric. 20, 15-23.Google Scholar
  2. Anderson R V and Coleman D C 1977 The use of glass microbeads in ecological experiments with bacteriophagic nematodes. J. Nematol. 9, 319-322.PubMedGoogle Scholar
  3. Anderson R V, Elliott E T, Coleman D C and Cole C V 1981 Effect of the nematodes Acrobeloides sp. and Mesodiplogaster lheritieri on substrate utilization and nitrogen and phosphorus mineralization in soil. Ecology 62, 549-555.CrossRefGoogle Scholar
  4. Bardgett R D 1996 Potential effects on the soil mycoflora of changes in the UK agricultural policy for upland grasslands. In Fungi and Environmental Change. Eds J C Frankland, N Magan and G M Gadd. pp 163-183. British Mycological Society Symposium, Cambridge University Press.Google Scholar
  5. Bardgett R D and Cook R 1998 Functional aspects of soil animal diversity in agricultural grasslands. Appl. Soil Ecol. 10, 263-276.CrossRefGoogle Scholar
  6. Bardgett R D and Fai K C 1999 Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol. Biochem. 31, 1007-1014.CrossRefGoogle Scholar
  7. Bardgett R D, Frankland J C and Whittaker J B 1993 The effects of agricultural practices on the soil biota of some upland grasslands. Agric. Ecosyst. Environ. 45, 25-45.CrossRefGoogle Scholar
  8. Bardgett R D, Leemans D K, Cook R, Hobbs P J 1997 Seasonality of soil biota of grazed and ungrazed hill grasslands. Soil Biol. Biochem. 29, 1285-1294.CrossRefGoogle Scholar
  9. Bardgett R D, Keiller S, Cook R and Gilburn A 1998a Dynamic interactions between soil animals and microorganisms in upland grassland soils amended with sheep dung: a microcosm study. Soil Biol. Biochem. 30, 531-539.CrossRefGoogle Scholar
  10. Bardgett R D, Wardle D A and Yeates G W 1998b Linking aboveground and below-ground food webs: how plant responses to foliar herbivory influence soil organisms. Soil Biol. Biochem. 30, 1867-1878.CrossRefGoogle Scholar
  11. Brown V K and Gange A C 1990 Insect herbivory below ground. Adv. Ecol. Res. 20, 1-59.Google Scholar
  12. Brussaard L, Noordhuis R, Geurs M and Bouwman L A 1995 Nitrogen mineralization in soil in microcosms with and without bacterivorous nematodes and nematophageous mites. Acta Zool. Fenn. 196, 15-21.Google Scholar
  13. Coleman D C, Cole C V, Anderson R V, Blaha M, Campion M K, Clarholm M, Elliot E T, Hunt H W, Schaefer B and Sinclair J 1977 Analysis of rhizosphere-saprophage interactions in terrestrial ecosystems. Ecol. Bull. 25, 299-309.Google Scholar
  14. Cook R and Plowright R A 1983 Incidence and effects of nematodes on white clover. Proceedings of the 10th International Congress of Plant Protection, Brighton, UK.Google Scholar
  15. Cook R and Yeates G W 1994 Nematode pests of grassland and forage crops. In Plant Parasitic Nematodes in Temperate Agriculture. Eds K Evans, D L Trudgill and J M Webster. pp 305-350. CAB International, Wallingford.Google Scholar
  16. Coulson J C and Whittaker J B 1978 Ecology of moorland animals. In Production Ecology of British Moors and Montane Grasslands. Eds. O W Heal and D F Perkins. pp 52-93. Springer-Verlag, London.Google Scholar
  17. Curry J P 1969 The qualitative and quantitative composition of the fauna of an old grassland site at Celbridge, Co. Kildare. Soil Biol. Biochem. 1, 221-227.CrossRefGoogle Scholar
  18. Denton C S, Bardgett R D, Cook R and Hobbs P J 1999 Low amounts of root herbivory positively influences the rhizosphere microbial community of a temperate grassland soil. Soil Biol. Biochem. 31, 155-165.CrossRefGoogle Scholar
  19. Dyer M I, Acra M A, Wang G M, Coleman D C, Freckman D W, McNaughton S J and Strain B R 1991 Source-sink carbon relations in two Panicum coloratum ecotypes in response to herbivory. Ecology 72, 1472-1483.CrossRefGoogle Scholar
  20. Griffiths B S and Bardgett R D 1997 Interactions between microbial feeding invertebrates and soil microorganisms. In Modern Soil Microbiology. Eds J D van Elsas, E Wellington and J T Trevors. pp 165-182. Marcell Dekker, New York.Google Scholar
  21. Hiernaux P and Turner M D 1996 The effect of clipping on growth and nutrient uptake of Sahelian annual rangelands. J. Appl. Ecol. 33, 387-399.CrossRefGoogle Scholar
  22. Hodda M and Wanless F R 1994a Nematodes from an English chalk grassland: species distribution. Nematologica 40, 116-132.CrossRefGoogle Scholar
  23. Hodda M and Wanless F R 1994b Nematodes from an English chalk grassland: population ecology. Pedobiologia 38, 530-545.Google Scholar
  24. Holland J N 1996 Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems. Appl. Soil Ecol. 2, 275-279.CrossRefGoogle Scholar
  25. Holland E A and Detling J K 1990 Plant response to herbivory and below-ground nitrogen cycling. Ecology 71, 1040-1049.CrossRefGoogle Scholar
  26. Holland J N, Cheng W and Crossley D A Jr 1996 Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107, 87-94.CrossRefGoogle Scholar
  27. Ingham R E and Detling J K 1984Plant-herbivore interactions in a North American mixed-grass prairie III. Soil nematode populations and root biomass on Cynomys ludovicianus colonies and adjacent uncolonized areas. Oecologia 63, 307-313.CrossRefGoogle Scholar
  28. Ingham R E and Detling J K 1986 Effects of defoliation and nematode consumption on growth and leaf gas exchange in Bouteloua curtipendula. Oikos 46, 23-28.Google Scholar
  29. Ingham R E, Trofymow J A, Ingham E R and Coleman D C 1985 Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol. Monog. 55, 119-140.CrossRefGoogle Scholar
  30. Jones C G, Ostfeld R S, Richard M P, Schauber E M and Wolff J W 1998 Chain reactions linking acorns to gypsy moth outbreaks and lyme disease risk. Science 279, 1023-1026.PubMedCrossRefGoogle Scholar
  31. McNaughton S J 1979 Grazing as an optimization process: grassland ungulate relationships in the Serengeti ecosystem. Amer. Nat. 113, 691-703.CrossRefGoogle Scholar
  32. McNaughton S J, Banyikwa F F and McNaughton M M 1997 Promotion of the cycling of diet-enhancing nutrients by African grazers. Science 278, 1798-1800.PubMedCrossRefGoogle Scholar
  33. McNaughton S J, Banyikwa F F and McNaughton M M 1998 Root biomass and productivity in a grazing ecosystem: the Serengeti. Ecology 79, 587-592.CrossRefGoogle Scholar
  34. Mawdsley J L and Bardgett R D 1997 Continuous defoliation of perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) and associated changes in the microbial population of an upland grassland soil. Biol. Fertil. Soils 24, 52-58.CrossRefGoogle Scholar
  35. Merrill E H, Stanton N L and Hak J C 1994 Responses of bluebunch wheatgrass, Idaho fescue and nematodes to ungulate grazing in Yellowstone National Park. Oikos 69, 231-240.Google Scholar
  36. Menge B A 1995 Indirect effects in marine rocky interaction webs: pattern and importance. Ecol. Monog. 65, 21-74.CrossRefGoogle Scholar
  37. Mikola J and Setälä H 1998 No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79, 153-164.CrossRefGoogle Scholar
  38. Oostenbrink M 1967 Studies on the emergence of encysted Heterodera larvae. Meded Rijksfac Landb Wet Gent 32, 503-539.Google Scholar
  39. Parker L W, Santos P F, Phillips J and Whitford W G 1984 Carbon and nitrogen dynamics during the decomposition of litter and roots of a Chiuahuan desert annual, Lepidium lasicarpum. Ecol. Monog. 54, 339-360.CrossRefGoogle Scholar
  40. Pastor J, Naiman R J, Dewey B and McInnes P 1988 Moose, microbes and the boreal forest. BioScience 38, 770-777.CrossRefGoogle Scholar
  41. Petersen H and Luxton M 1982 A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 287-388.Google Scholar
  42. Risley L S and Crossley D A Jr 1988 Herbivore-caused greenfall in the southern Appalachians. Ecology 69, 1118-1127.CrossRefGoogle Scholar
  43. Ruess R W and McNaughton S J 1987 Grazing and the dynamics of nutrient and energy regulated microbial processes in the Serengeti grasslands. Oikos 49, 101-110.Google Scholar
  44. Ruess R W and Seagle S W 1994 Landscape patterns in soil microbial processes in the Serengeti National Park, Tansania. Ecology 75, 892-904.CrossRefGoogle Scholar
  45. Santos P F, Phillips J and Whitford W G 1981 The role of mites and nematodes in early stages of buried litter decomposition in a desert. Ecology 62, 664-669.CrossRefGoogle Scholar
  46. Seastedt T R, Ramundo R A and Hayes D C 1988 Maximization of densities of soil animals by foliage herbivory: empirical evidence, graphical and conceptual models. Oikos 51, 243-248.Google Scholar
  47. Van der Putten W H and Peters B A M 1997 How soil-borne pathogens may affect plant competition. Ecology 78, 1785-1795.CrossRefGoogle Scholar
  48. Wallace L L and Macko S A 1993 Nutrient acquisition by clipped plants as a measure of competitive success: the effects of compensation. Funct. Ecol. 7, 326-331.CrossRefGoogle Scholar
  49. Woods L E, Cole C V, Elliot E T, Anderson R V and Coleman D C 1982 Nitrogen transformations in soil as affected by bacterial:microfaunal interactions. Soil Biol. Biochem. 14, 93-98.CrossRefGoogle Scholar
  50. Wootton J T 1994 The nature and consequences of indirect effects in ecological communities. Ann. Rev. Ecol. System. 25, 443-466.CrossRefGoogle Scholar
  51. Wardle D A, Yeates G W, Watson R N and Nicholson K S 1995 The detritus food-web and diversity of soil fauna as indicators of disturbance regimes in agro-ecosystems. Oikos 73, 155-166.Google Scholar
  52. Wardle D A, Bonner K I, Barker G M, Yeates G W, Nicholson K S, Bardgett R D, Watson R N, Ghani A 1998 Experimental reduction of plant functional diversity in a perennial grassland: implications for vegetation dynamics, decomposer food-webs, soil biodiversity and ecosystem function. Ecol. Monogr. (In press).Google Scholar
  53. Yeates G W 1979 Soil nematodes in terrestrial ecosystems. J. Nematol. 11, 213-229.PubMedGoogle Scholar
  54. Yeates G W 1984 Variation in soil nematode diversity under pasture with soil and year. Soil Biol. Biochem. 16, 95-102.Google Scholar
  55. Yeates G W 1998 Soil nematode assemblages: regulators of ecosystem productivity. Phytoparasitica 26, 97-100.Google Scholar
  56. Yeates G W, Bongers T, de Goede R G M, Freckman D W, Georgieva S S 1993 Feeding habits in soil nematode families and genera - an outline for soil ecologists. J. Nematol. 25, 315-331.PubMedGoogle Scholar
  57. Yeates G W, Bardgett R D, Cook R, Hobbs P J, Bowling P J and Potter J F 1997 Faunal and microbial diversity in three Welsh grassland soils under conventional and organic management regimes. J. Appl. Ecol. 34, 453-470.CrossRefGoogle Scholar
  58. Yeates G W, Saggar S, Denton C S and Mercer C F 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, 81-90.CrossRefGoogle Scholar
  59. Yeates G W, Bardgett R D, Mercer C F, Saggar S and Feltham C W 1999a The impact of feeding by five nematodes on 14C distribution in soil microbial biomas and nematodes: initial observations. NZ J. Zool. 26, 87.Google Scholar
  60. Yeates G W, Saggar S, Hedley C B and Mercer C F 1999b Increase in 14C-carbon translocation to the soil microbial biomass when five species of plant-parasitic nematodes infect roots of white clover. Nematology (In press).Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Richard D. Bardgett
    • 1
  • Roger Cook
    • 2
  • Gregor W. Yeates
    • 3
  • Crystal S. Denton
    • 1
    • 2
  1. 1.School of Biological SciencesUniversity of ManchesterManchesterUK
  2. 2.Institute of Grassland and Environmental ResearchPlas Gogerddan, AberystwythCeredigionUK
  3. 3.Landcare ResearchPalmerston NorthNew Zealand
  4. 4.Department of Biological Sciences, Institute of Environmental and Natural SciencesUniversity of LancasterLancasterUK FAX No

Personalised recommendations