Skip to main content
SpringerLink
Log in

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

  • Published:
Plant and Soil Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altieri M G 1991 How can we best use biodiversity in agroecosystems? Outlook Agric. 20, 15-23.

    Google Scholar 

  • Anderson R V and Coleman D C 1977 The use of glass microbeads in ecological experiments with bacteriophagic nematodes. J. Nematol. 9, 319-322.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • Bardgett R D and Cook R 1998 Functional aspects of soil animal diversity in agricultural grasslands. Appl. Soil Ecol. 10, 263-276.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Brown V K and Gange A C 1990 Insect herbivory below ground. Adv. Ecol. Res. 20, 1-59.

    Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Hodda M and Wanless F R 1994a Nematodes from an English chalk grassland: species distribution. Nematologica 40, 116-132.

    Article  Google Scholar 

  • Hodda M and Wanless F R 1994b Nematodes from an English chalk grassland: population ecology. Pedobiologia 38, 530-545.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Holland E A and Detling J K 1990 Plant response to herbivory and below-ground nitrogen cycling. Ecology 71, 1040-1049.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • McNaughton S J 1979 Grazing as an optimization process: grassland ungulate relationships in the Serengeti ecosystem. Amer. Nat. 113, 691-703.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Menge B A 1995 Indirect effects in marine rocky interaction webs: pattern and importance. Ecol. Monog. 65, 21-74.

    Article  Google Scholar 

  • Mikola J and Setälä H 1998 No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79, 153-164.

    Article  Google Scholar 

  • Oostenbrink M 1967 Studies on the emergence of encysted Heterodera larvae. Meded Rijksfac Landb Wet Gent 32, 503-539.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pastor J, Naiman R J, Dewey B and McInnes P 1988 Moose, microbes and the boreal forest. BioScience 38, 770-777.

    Article  Google Scholar 

  • 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 

  • Risley L S and Crossley D A Jr 1988 Herbivore-caused greenfall in the southern Appalachians. Ecology 69, 1118-1127.

    Article  Google Scholar 

  • 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 

  • Ruess R W and Seagle S W 1994 Landscape patterns in soil microbial processes in the Serengeti National Park, Tansania. Ecology 75, 892-904.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Van der Putten W H and Peters B A M 1997 How soil-borne pathogens may affect plant competition. Ecology 78, 1785-1795.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Wootton J T 1994 The nature and consequences of indirect effects in ecological communities. Ann. Rev. Ecol. System. 25, 443-466.

    Article  Google Scholar 

  • 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 

  • 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).

  • Yeates G W 1979 Soil nematodes in terrestrial ecosystems. J. Nematol. 11, 213-229.

    CAS  PubMed  Google Scholar 

  • Yeates G W 1984 Variation in soil nematode diversity under pasture with soil and year. Soil Biol. Biochem. 16, 95-102.

    Google Scholar 

  • Yeates G W 1998 Soil nematode assemblages: regulators of ecosystem productivity. Phytoparasitica 26, 97-100.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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).

Download references

Author information

Author notes

  1. Richard D. Bardgett

    Present address: Department of Biological Sciences, Institute of Environmental and Natural Sciences, University of Lancaster, Lancaster, LA1 4YQ, UK FAX No

Authors and Affiliations

  1. School of Biological Sciences, University of Manchester, Oxford Road, Manchester, M13 9PT, UK

    Richard D. Bardgett & Crystal S. Denton

  2. Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, SY23 3EB, UK

    Roger Cook & Crystal S. Denton

  3. Landcare Research, Private Bag 11052, Palmerston North, New Zealand

    Gregor W. Yeates

Authors
  1. Richard D. Bardgett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roger Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregor W. Yeates
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Crystal S. Denton
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bardgett, R.D., Cook, R., Yeates, G.W. et al. The influence of nematodes on below-ground processes in grassland ecosystems. Plant and Soil 212, 23–33 (1999). https://doi.org/10.1023/A:1004642218792

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004642218792

Search

Navigation