Oecologia

, Volume 141, Issue 1, pp 84–93 | Cite as

Aphid effects on rhizosphere microorganisms and microfauna depend more on barley growth phase than on soil fertilization

  • Mette Vestergård
  • Lisa Bjørnlund
  • Søren Christensen
Plant Animal Interactions

Abstract

This paper gives the first reports on aphid effects on rhizosphere organisms as influenced by soil nutrient status and plant development. Barley plants grown in pots fertilized with N but without P (N), with N and P (NP), or not fertilized (0) were sampled in the early growth phase (day 25), 1 week before and 1 week after spike emergence. Aphids were added 16 days before sampling was carried out. In a separate experiment belowground respiration was measured on N and NP fertilized plant–soil systems with aphid treatments comparable to the first experiment. Aphids reduced numbers of rhizosphere bacteria and fungal feeding nematodes 1 week before spike emergence. Before spike emergence, aphids reduced belowground respiration in NP treatments. These findings strongly indicate that aphids reduced allocation of photoassimilates to roots and deposition of root exudates in the growth phase of the plant. Contrary to this, 1 week after spike emergence numbers of bacteria, fungal feeding nematodes and Protozoa were higher in rhizospheres of plants subjected to aphids probably because aphids enhanced root mortality and root decomposition. Protozoa and bacterial feeding nematodes were stimulated at different experimental conditions with nematodes being the dominant bacterial grazers at N fertilization and Protozoa in the NP treatment before spike emergence.

Keywords

Aboveground–belowground interactions Bacteria Protozoa Nematodes Root respiration 

Notes

Acknowledgements

We thank Annette Spangenberg and Esben Vedel for laboratory assistance. Lars Monrad Hansen (Danish Institute of Agricultural Sciences), kindly provided us with an aphid culture, and Keld Skov Nielsen (Royal Veterinary and Agricultural University), provided us with barley seeds. Comments by Marzcia Techau and two anonymous referees on earlier drafts improved the manuscript significantly.

References

  1. Alström S (1987) Influence of root-zone inhabiting bacteria on growth of plants and soilborne pathogens. Doctoral dissertation. Department of Plant and Forest Protection, Swedish University of Agricultural Sciences, UppsalaGoogle Scholar
  2. Anderson RV, Elliott ET, McClellan JF, Coleman DC, Cole CV, Hunt HW (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. III. Biotic interactions of bacteria, amoebae, and nematodes. Microb Ecol 4:361–371Google Scholar
  3. Bajorat B, Blumendeller C, Schönbeck F (1995) Influence of direct and indirect damages to root systems on plant efficiency. Z Pflanzenk Pflanzenschutz 102:561–573Google Scholar
  4. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19Google Scholar
  5. Bongers T (1994) De nematoden van Nederland, 2nd edn. Pirola, SchoorlGoogle Scholar
  6. Cheng W, Coleman DC, Box JE (1990) Root dynamics, production and distribution in agroecosystems on the Georgia Piedmont using minirhizotrons. J Appl Ecol 27:592–604CrossRefGoogle Scholar
  7. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187CrossRefGoogle Scholar
  8. Coleman DC, Anderson RV, Cole CV, Elliott ET, Woods L, Campion MK (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. IV. Flows of metabolic and biomass carbon. Microb Ecol 4:373–380Google Scholar
  9. Darbyshire JF, Wheatley RE, Greaves MP, Inkson RHE (1974) A rapid micromethod for estimating bacterial and protozoan populations in soil. Rev Ecol Biol Sol 11:465–475Google Scholar
  10. Elliott ET, Anderson RV, Coleman DC, Cole CV (1980) Habitable pore space and microbial trophic interactions. Oikos 35:327–335Google Scholar
  11. Ettema CH, Bongers T (1993) Characterization of nematode colonization and succession in disturbed soil using the Maturity Index. Biol Fertil Soils 16:79–85Google Scholar
  12. de Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L). Biol Fertil Soils 24:358–364CrossRefGoogle Scholar
  13. Gange AC, Bower E, Brown VK (1999) Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120:123–131CrossRefGoogle Scholar
  14. Grant CA, Flaten DN, Tomasiewicz DJ, Sheppard SC (2001) The importance of early season phosphorus nutrition. Can J Plant Sci 81:211–224Google Scholar
  15. Gregory PJ, Atwell BJ (1991) The fate of carbon in pulse-labelled crops of barley and wheat. Plant Soil 136:205–213Google Scholar
  16. Griffiths BS (1990) A comparison of microbial-feeding nematodes and protozoa in the rhizosphere of different plants. Biol Fertil Soils 9:83–88Google Scholar
  17. Griffiths BS, Welschen R, van Arendonk JJCM, Lambers H (1992) The effect of nitrate-nitrogen supply on bacteria and bacterial-feeding fauna in the rhizosphere of different grass species. Oecologia 91:253–259Google Scholar
  18. Gröntoft M, Jonasson T (1992) Influence of Heterodera schachtii on Verticillium wilt symptoms in oilseed rape. J Phytopathol 134:170–174Google Scholar
  19. Guitian R, Bardgett RD (2000) Plant and soil microbial responses to defoliation in temperate semi-natural grassland. Plant Soil 220:271–277CrossRefGoogle Scholar
  20. Hale BK, Bale JS, Pritchard J, Masters GJ, Brown VK (2003) Effects of host plant drought stress on the performance of the bird cherry-oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis. Ecol Entomol 28:666–677CrossRefGoogle Scholar
  21. Holland JN (1995) Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems. Appl Soil Ecol 2: 275–279CrossRefGoogle Scholar
  22. Holland JN, Cheng W, Crossley DA (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107:87–94Google Scholar
  23. Jensen B (1993) Rhizodeposition by 14CO2-pulse-labelled spring barley grown in small field plots on sandy loam. Soil Biol Biochem 25:1553–1559CrossRefGoogle Scholar
  24. Johansson G (1992) Below-ground carbon distribution in barley (Hordeum vulgare L.) with and without nitrogen fertilization. Plant Soil 144:93–99Google Scholar
  25. Kedrowski RA (1983) Extraction and analysis of nitrogen, phosphorus and carbon fractions in plant material. J Plant Nutr 6:989–1011Google Scholar
  26. van der Krift TAJ, Kuikman PJ, Möller F, Berendse F (2001) Plant species and nutritional-mediated control over rhizodeposition and root decomposition. Plant Soil 228:191–200CrossRefGoogle Scholar
  27. Kurek E, Jaroszuk-Ściseł J (2003) Rye (Secale cereale) growth promotion by Pseudomonas fluorescens strains and their interactions with Fusarium culmorum under various soil conditions. Biol Control 26:48–56CrossRefGoogle Scholar
  28. Liljeroth E, van Veen JA, Miller HJ (1990) Assimilate translocation to the rhizosphere of two wheat lines and subsequent utilization by rhizosphere microorganisms at two soil nitrogen concentrations. Soil Biol Biochem 22:1015–1021CrossRefGoogle Scholar
  29. Masters GJ, Brown VK (1992) Plant-mediated interactions between two spatially separated insects. Funct Ecol 6:175–179Google Scholar
  30. Masters GJ, Brown VK, Gange AC (1993) Plant mediated interactions between above- and below-ground insect herbivores. Oikos 66:148–151Google Scholar
  31. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  32. Merckx R, Dijkstra A, den Hartog A, van Veen JA (1987) Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol Fertil Soils 5:126–132Google Scholar
  33. Merrill EH, Stanton NL, Hak JC (1994) Responses of bluebunch wheatgrass, Idaho fescue, and nematodes to ungulate grazing in Yellowstone National Park. Oikos 69:231–240Google Scholar
  34. Mikola J, Yeates GW, Barker GM, Wardle DA, Bonner KI (2001) Effects of defoliation intensity on soil food-web properties in an experimental grassland community. Oikos 92:333–343Google Scholar
  35. Miles PW (1989) Specific responses and damage caused by Aphidoidea. In: Minks AK, Harrewijn P (eds) Aphids. Their biology, natural enemies and control, vol C. Elsevier, Amsterdam, pp 23–48Google Scholar
  36. Moran NA, Whitham TG (1990) Interspecific competition between root-feeding and leaf-galling aphids mediated by host-plant resistance. Ecology 71:1050–1058Google Scholar
  37. Nicol JM, Davies KA, Hancock TW, Fisher JM (1999) Yield loss caused by Pratylenchus thornei on wheat in South Australia. J Nematol 31:367–376CrossRefGoogle Scholar
  38. Page FC (1988) A new key to freshwater and soil gymnamoebae. Freshwater Biological Association, AmblesideGoogle Scholar
  39. Riedell WE, Kieckhefer RW (1995) Feeding damage effects of three aphid species on wheat root growth. J Plant Nutr 18:1881–1891Google Scholar
  40. Rosolem CA, Witacker JPT, Vanzolini S, Ramos VJ (1999) The significance of root growth on cotton nutrition in an acidic low-P soil. Plant Soil 212:185–190Google Scholar
  41. de Ruiter PC, Moore JC, Zwart KB, Bouwman LA, Hassink J, Bloem J, de Vos JA, Marinissen JCY, Didden WAM, Lebbink G, Brussard L (1993) Simulation of nitrogen mineralization in the below-ground food webs of two winter wheat fields. J Appl Ecol 30:95–106Google Scholar
  42. Rønn R, Ekelund F, Christensen S (1995) Optimizing soil extract and broth media for MPN-enumeration of naked amoebae and heterotrophic flagellates in soil. Pedobiologia 39:10–19Google Scholar
  43. Rønn R, Grunert J, Ekelund F (2001) Protozoan response to addition of the bacteria Mycobacterium chlorophenolicum and Pseudomonas chlororaphis to soil microcosms. Biol Fertil Soils 33:126–131CrossRefGoogle Scholar
  44. Rønn R, McCaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–6105CrossRefGoogle Scholar
  45. Saggar S, Hedley C, Mackay AD (1997) Partitioning and translocation of photosynthetically fixed 14C in grazed hill pastures. Biol Fertil Soils 25:152–158CrossRefGoogle Scholar
  46. Salt DT, Fenwick P, Whittaker JB (1996) Interspecific herbivore interactions in a high CO2 environment: root and shoot aphids feeding on Cardamine. Oikos 77:326–330Google Scholar
  47. Seastedt TR, Ramundo RA, Hayes DC (1988) Maximization of densities of soil animals by foliage herbivory: empirical evidence, graphical and conceptual models. Oikos 51:243–248Google Scholar
  48. Smith JP, Schowalter TD (2001) Aphid-induced reduction of shoot and root growth in Douglas-fir seedlings. Ecol Entomol 26:411–416CrossRefGoogle Scholar
  49. Stanton NL (1983) The effect of clipping and phytophagous nematodes on net primary production of blue grama, Bouteloua gracilis. Oikos 40:249–257Google Scholar
  50. Steingrobe B, Schmid H, Claassen N (2001a) Root production and root mortality of winter barley and its implication with regard to phosphate acquisition. Plant Soil 237:239–248CrossRefGoogle Scholar
  51. Steingrobe B, Schmid H, Gutser R, Claassen N (2001b) Root production and root mortality of winter wheat grown on sandy and loamy soils in different farming systems. Biol Fertil Soils 33:331–339CrossRefGoogle Scholar
  52. Stout JD, Heal OW (1967) Protozoa. In: Burger A, Raw F (eds) Soil biology. Academic Press, London, pp 149–195Google Scholar
  53. Swinnen J (1994) Rhizodeposition and turnover of root-derived organic material in barley and wheat under conventional and integrated management. Agric Ecosyst Environ 51:115–128CrossRefGoogle Scholar
  54. Swinnen J, van Veen JA, Merckx R (1995) Carbon fluxes in the rhizosphere of winter wheat and spring barley with conventional vs integrated farming. Soil Biol Biochem 27:811–820CrossRefGoogle Scholar
  55. Techau MEC, Bjørnlund L, Christensen S. Simulated herbivory effects on rhizosphere organisms in Pea (Pisum sativum) depended on phosphate. Plant Soil (in press)Google Scholar
  56. Vestergård M (2004) Nematode assemblages in the rhizosphere of spring barley (Hordeum vulgare L.) depended on fertilisation and plant growth phase. Pedobiologia 48:257–265CrossRefGoogle Scholar
  57. Wall-Freckman D, Huang SP (1998) Response of the soil nematode community in a shortgrass steppe to long-term and short-term grazing. Appl Soil Ecol 9:39–44CrossRefGoogle Scholar
  58. Wamberg C, Christensen S, Jakobsen I (2003) Interaction between foliar-feeding insects, mycorrhizal fungi, and rhizosphere protozoa on pea plants. Pedobiologia 47:281–287Google Scholar
  59. Wurst S, Langel R, Reineking A, Bonkowski M, Scheu S (2003) Effects of earthworms and organic litter distribution on plant performance and aphid reproduction. Oecologia 137:90–96CrossRefGoogle Scholar
  60. Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Mette Vestergård
    • 1
  • Lisa Bjørnlund
    • 1
  • Søren Christensen
    • 1
  1. 1.Department of Terrestrial Ecology, Biological InstituteUniversity of CopenhagenCopenhagen ØDenmark

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