Biotic Interactions in the Rhizosphere: Effects on Plant Growth and Herbivore Development

  • M. Bonkowski
  • S. Scheu
Part of the Ecological Studies book series (ECOLSTUD, volume 173)


Considerable progress has been made in understanding specific interactions of plant roots with rhizosphere microorganisms and interactions with the soil fauna. Due to their function in nutrient mineralization, the role of soil organisms is usually considered important in long-term processes such as decomposition of litter materials. It would be incorrect, however, to assume that effects of decomposer animals on plant performance solely result from improved plant uptake of nutrients. In recent years, our view has profoundly changed, giving soil organisms a much more active role by interacting with living plants, their symbionts and pathogens and thereby shaping ecosystem processes. It has to be appreciated that decomposer animals consist of very different functional groups which differentially affect microbial diversity and function in the rhizosphere, thereby modifying plant physiology, morphology and phenology. These interactions cascade up to herbivores above the ground, ultimately affecting the whole aboveground food web. In addition to changing bottom-up forces on the herbivore community, the decomposer system may strengthen top-down forces on aboveground herbivores by subsidizing generalist predators with prey. The full implications of this integrated view of terrestrial ecosystem function have yet to be explored. In arable systems, intelligent management practices have to be developed employing the decomposer community to help in plant nutrition, to foster plant defence against herbivores and to support the control of herbivore pest populations. Current practices based on soil tillage and inorganic nutrient inputs certainly are inadequate in this respect. In more natural ecosystems the role of the decomposer community as driving agent for plant competition and community composition via modifying the rhizosphere environment needs considerably more attention. Microorganisms have been identified as an important structuring force of natural plant communities in recent years; however, those organisms that regulate the structure and functioning of microbial communities so far have been widely neglected. A comprehensive understanding of regulating forces in arable and natural systems will not be achieved without integrating the animal community below the ground.


Arbuscular Mycorrhizal Fungus Soil Biol Biotic Interaction Generalist Predator Decomposer Community 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alphei J, Bonkowski M, Scheu S (1996) Protozoa, Nematoda and Lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106: 111 - 126CrossRefGoogle Scholar
  2. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradorhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204: 57 - 67CrossRefGoogle Scholar
  3. Arshad M, Frankenberger WT (1998) Plant growth-regulating substances in the rhizosphere: microbial production and functions. Adv Agron 62: 45 - 151CrossRefGoogle Scholar
  4. Bala A, Giller KE (2001) Symbiotic specificity of tropical tree rhizobia for host legumes. New Phytol 149: 495 - 507CrossRefGoogle Scholar
  5. Baldwin IT, Hamilton W (2000) Jasmonate-induced responses of Nicotiana sylvestris results in fitness costs due to impaired competitive ability for nitrogen. J Chem Ecol 26: 915 - 952CrossRefGoogle Scholar
  6. Barea JM, Navarro E, Montoya E (1976) Production of plant growth regulators by rhizosphere phosphate-solubilizing bacteria. J Appl Bacteriol 40: 129 - 134PubMedCrossRefGoogle Scholar
  7. Beggs JR, Rees JS (1999) Restructuring of Lepidoptera communities by introduced Vespula wasps in a New Zealand beech forest. Oecologia 119: 565 - 571CrossRefGoogle Scholar
  8. Bezdicek DF, Kennedy AC (1979) Economic microbial ecology: symbiontic nitrogen fixation and nitrogen cycling in terrestrial environments. In: Lynch JM, Hobbie JE (eds) Micro-organisms in action: concepts and applications in microbial ecology. Blackwell, Oxford, pp 241 - 260Google Scholar
  9. Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34: 1709 - 1715CrossRefGoogle Scholar
  10. Bonkowski M, Cheng W, Griffiths BS, Alphei J, Scheu S (2000a) Microbial–faunal interactions in the rhizosphere and effects on plant growth. Eur J Soil Biol 36: 135 - 147CrossRefGoogle Scholar
  11. Bonkowski M, Griffiths BS, Scrimgeour C (2000b) Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of rye-grass.Appl Soil Ecol 14: 37 - 53Google Scholar
  12. Bonkowski M, Geoghegan IE, Birch ANE, Griffiths BS (2001 a) Effects of soil decomposer invertebrates (protozoa and earthworms) on an above-ground phytophagous insect (cereal aphid), mediated through changes in the host plant. Oikos 95: 441 - 450Google Scholar
  13. Bonkowski M, Jentschke G, Scheu S (2001b) Contrasting effects of microbes in the rhizosphere: interactions of mycorrhiza (Paxillus involutus (Batsch) Fr.), naked amoebae (Protozoa) and Norway spruce seedlings (Picea abies Karst.). Appl Soil Ecol 18: 193 - 204CrossRefGoogle Scholar
  14. Borowicz VA (1997) A fungal root symbiont modifies plant resistance to an insect herbivore.Oecologia 112: 534 - 542Google Scholar
  15. Brown ME (1972) Plant growth substances produced by micro-organisms of soil and rhizosphere. J Appl Bacteriol 35: 443 - 451CrossRefGoogle Scholar
  16. Brown VK, Gange AC (2002) Tritrophic below- and above-ground interactions in succession. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 197 - 222CrossRefGoogle Scholar
  17. Brussaard L (1998) Soil fauna, guilds, functional groups and ecosystem processes. Appl Soil Ecol 9: 123 - 135CrossRefGoogle Scholar
  18. Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357 - 368CrossRefGoogle Scholar
  19. Campell BC, Nes WD (1983) A reappraisal of sterol biosynthesis and metabolism in aphids. J Insect Physiol 29: 149 - 156CrossRefGoogle Scholar
  20. Chanway CP, Nelson LM, Holl FB (1988) Cultivar specific growth promotion of spring wheat (Triticum aestivum L.) by co-existent Bacillus species. Can J Microbiol 34: 925 - 929CrossRefGoogle Scholar
  21. Chen BR, Wise DH (1999) Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80: 761 - 772CrossRefGoogle Scholar
  22. Chet I, Ordentlich A, Shapira R, Oppenheim A (199 1) Mechanisms of biocontrol of soil-borne plant pathogens by rhizobacteria. In: Kleister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 229 - 236Google Scholar
  23. Christensen M (1989) A view of fungal ecology. Mycologia 81: 1 - 19CrossRefGoogle Scholar
  24. Christensen S, Griffiths BS, Ekelund F, Rønn R (1992) Huge increase in bacterivores on freshly killed barley roots. FEMS Microbiol Ecol 86: 303 - 310CrossRefGoogle Scholar
  25. Cipollini D, Purrington CB, Bergelson J (2003) Costs of induced responses in plants. Basic Appl Ecol 4: 79 - 85CrossRefGoogle Scholar
  26. Clarholm M (1984) Microbes as predators or prey–heterotrophic, free-living protozoa: neglected microorganisms with an important task in regulating bacterial populations. In: Klug MJ, Reddy CA (eds) Current perspectives on microbial ecology. American Society of Microbiology, Washington, pp 321 - 326Google Scholar
  27. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17: 181 - 187CrossRefGoogle Scholar
  28. Cornelissen JHC, Aerts R, Cerabolini B, Werger MJA, van der Heijden MGA (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129: 611 - 619PubMedCrossRefGoogle Scholar
  29. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21: 1 - 18PubMedCrossRefGoogle Scholar
  30. Dixon AFG (1985) Aphid ecology. Blackie, GlasgowGoogle Scholar
  31. Fitter AH (1994) Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: Caldwell MM, Pearcey RW (eds) Exploitation of environmental heterogeneity by plants: ecophysiological processes above-and belowground. Academic Press, San Diego, pp 305 - 323CrossRefGoogle Scholar
  32. Fitter AH, Merryweather JW (1992) Why are some plants more mycorrhizal than others? An ecological enquiry. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 26 - 36Google Scholar
  33. Gange AC, Ayres RL (1999) On the relation between mycorrhizal colonization and plant “benefit”.Oikos 87: 615 - 621Google Scholar
  34. Gange AC, Nice HE (1997) Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization. New Phytol 137: 335 - 343CrossRefGoogle Scholar
  35. Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128: 79 - 87CrossRefGoogle Scholar
  36. Gange AC, Bower E, Brown VK (1999) Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120: 123 - 131CrossRefGoogle Scholar
  37. Gange AC, Stagg PG, Ward LK (2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol Lett 5: 11 - 15CrossRefGoogle Scholar
  38. Gehring GA, Whitham TG (2002) Mycorrhizae–herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer ecological studies analysis and synthesis, vol 157. Springer, Berlin Heidelberg New York, pp 295 - 320CrossRefGoogle Scholar
  39. Gershenzon J (1994) The cost of plant chemical defense against herbivory: a biochemical perspective. In: Bernays EA (ed) Insect–plant interactions. CRC Press, Boca Raton, pp 105 - 173Google Scholar
  40. Goverde M, van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (2000) Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125: 362 - 369CrossRefGoogle Scholar
  41. Graves JD, Watkins NK, Fitter AH, Robinson D, Scrimgeour C (1997) Intraspecific transfer of carbon between plants linked by a common mycorrhizal network. Plant Soil 192: 153 - 159CrossRefGoogle Scholar
  42. Griffiths BS (1994) Soil nutrient flow. In: Darbyshire JF (ed) Soil protozoa. CAB International, Wallingford, pp 65 - 91Google Scholar
  43. Griffiths BS, Caul S (1993) Migration of bacterial-feeding nematodes, but not protozoa, to decomposing grass residues. Biol Fert Soils 15: 201 - 207CrossRefGoogle Scholar
  44. Griffiths BS, Ekelund F, Rønn R, Christensen S (1993) Protozoa and nematodes on decomposing barley roots. Soil Biol Biochem 25: 1293 - 1295CrossRefGoogle Scholar
  45. Griffith GS, Cresswell A, Jones S, Allen DK (2000) The nitrogen handling characteristics of white clover (Trifolium repens L.) cultivars and a perennial ryegrass (Lolium perenne L.) cultivar. J Exp Bot 51: 1879 - 1892PubMedCrossRefGoogle Scholar
  46. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157: 262 - 281PubMedCrossRefGoogle Scholar
  47. Halaj J, Wise DH (2002) Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83: 3141 - 3151CrossRefGoogle Scholar
  48. Halitschke R, Keßler A, Kahl J, Lorenz A, Baldwin IT (2000) Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata. Oecologia 124: 408 - 417CrossRefGoogle Scholar
  49. Hamilton JG, Zangerl A, DeLucia EH, Berenbaum MR (2001) The carbon–nutrient balance hypothesis: its rise and fall. Ecol Lett 4: 86 - 95CrossRefGoogle Scholar
  50. Hawes MC (1991) Living plant cells released from the root cap: a regulator of microbial populations in the rhizosphere? In: Kleister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 51 - 59CrossRefGoogle Scholar
  51. Hawkins BA, Mills NJ, Jervis MA, Price PW (1999) Is the biological control of insects a natural phenomenon? Oikos 86: 493 - 506CrossRefGoogle Scholar
  52. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or to defend. Q Rev Biol 67: 283 - 335CrossRefGoogle Scholar
  53. Hiltner L (1904) Über neue Erfahrungen und Probleme auf dem Gebiet der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Arb Dtsch Landw Ges 98: 59 - 78Google Scholar
  54. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol 139: 479 - 494CrossRefGoogle Scholar
  55. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1999) Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biol Biochem 31: 1517 - 1530CrossRefGoogle Scholar
  56. Holland MA (1997) Occam’s razor applied to hormonology: are cytokinins produced by plants? Plant Physiol 115: 865 - 868PubMedPubMedCentralCrossRefGoogle Scholar
  57. Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25: 495 - 520CrossRefGoogle Scholar
  58. Huber-Sannwald E, Pyke DA, Caldwell MM (1997) Perception of neighbouring plants by rhizomes and roots: morphological manifestations of a clonal plant. Can J Bot 75: 2146 - 2157CrossRefGoogle Scholar
  59. Jentschke G, Bonkowski M, Godbold DL, Scheu S (1995) Soil protozoa and forest tree growth: non-nutritional effects and interaction with mycorrhizas. Biol Fertil Soils 20: 263 - 269CrossRefGoogle Scholar
  60. Jingguo W, Bakken LR (1997) Competition for nitrogen during mineralization of plant residues in soil: microbial response to C and N availability. Soil Biol Biochem 29: 163 - 170CrossRefGoogle Scholar
  61. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135: 575 - 585CrossRefGoogle Scholar
  62. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69: 373 - 386CrossRefGoogle Scholar
  63. Jones DL, Darrah PR (1995) Influx and efflux of organic acids across the soil–root interface of Zea mays L. and its implications in rhizosphere C flow. Plant Soil 173: 103 - 109CrossRefGoogle Scholar
  64. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12: 139 - 143PubMedCrossRefGoogle Scholar
  65. Kloepper JW, Leong J, Teitze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885–886CrossRefGoogle Scholar
  66. Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16: 315 - 322CrossRefGoogle Scholar
  67. Kuikman PJ, Jansen AG, van Veen JA, Zehnder AJB (1990) Protozoan predation and the turnover of soil organic carbon and nitrogen in the presence of plants. Biol Fertil Soils 10: 22 - 28CrossRefGoogle Scholar
  68. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165: 382 - 396CrossRefGoogle Scholar
  69. Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol 8: 298 - 300PubMedCrossRefGoogle Scholar
  70. Lavelle P, Bignell D, Lepage M, Wolters V, Roger P, Ineson P, Heal OW, Dhillion S (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Sci 33: 159 - 193Google Scholar
  71. Lawton JH, McNeill S (1979) Between the devil and the deep blue sea: on the problems of being a herbivore. In: Anderson RM, Turner BD, Taylor LR (eds) Population dynamics. Blackwell, Oxford, pp 223 - 244Google Scholar
  72. Lerdau M, Coley PD (2002) Benefits of the carbon–nutrient balance hypothesis. Oikos 98: 533 - 535CrossRefGoogle Scholar
  73. Lipson DA, Raab TK, Schmidt SK, Monson RK (1999a) Variation in competitive abilities of plants and microbes for specific amino acids. Biol Fertil Soils 29: 257 - 261CrossRefGoogle Scholar
  74. Lipson DA, Schmidt SK, Monson RK (1999b) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80: 162 - 163CrossRefGoogle Scholar
  75. Lorio P (1986) Growth-differentiation balance: a basis for understanding southern pine beetle–tree interactions. For Ecol Manage 14: 259 - 273CrossRefGoogle Scholar
  76. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129: 1 - 10CrossRefGoogle Scholar
  77. Marschner H (1992) Nutrient dynamics at the soil–root interface (rhizosphere). In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 3 - 12Google Scholar
  78. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100: 1444 - 1449PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11: 119 - 161CrossRefGoogle Scholar
  80. McNaughton SJ, Oesterheld M, Frank DA, Williams KJ (1989) Ecosystem-level patterns ofprimary productivity and herbivory in terrestrial habitats. Nature 341: 142 - 144PubMedCrossRefGoogle Scholar
  81. Moore JC, Hunt HW (1988) Resource compartmentation and the stability of real ecosystems. Nature 333: 261 - 263CrossRefGoogle Scholar
  82. Mutikainen P, Walls M, Ovaska J, Keinänen M, Julkunen-Tiitto R, Vapaavuori E (2002) Costs of herbivore resistance in clonal saplings of Betula pendula. Oecologia 133: 364 - 371CrossRefGoogle Scholar
  83. Newman EI (1988) Mycorrhizal links between plants: their functioning and ecological significance. Adv Ecol Res 18: 243 - 271CrossRefGoogle Scholar
  84. Nitao JK, Zangerl AR, Berenbaum MR (2002) CNB: requiescat in pace? Oikos 98: 540 - 546CrossRefGoogle Scholar
  85. Obreht Z, Kerby NW, Gantar M, Rowell P (1993) Effects of root-associated N2-fixing cyanobacteria on the growth and nitrogen content of wheat (Triticum vulgare L.) seedlings. Biol Fertil Soils 15: 68 - 72CrossRefGoogle Scholar
  86. Oksanen L, Aunapuu M, Oksanen T, Schneider M, Ekerholm P, Lundberg PA, Armulik T, Aruoja V, Bondestad L (1997) Outlines of food webs in a low arctic tundra landscape in relation to three theories on trophic dynamics. In: Gange AC, Brown VK (eds) Multitrophic interactions in terrestrial systems. Blackwell, Oxford, pp 351 - 373Google Scholar
  87. Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42: 207 - 220PubMedCrossRefGoogle Scholar
  88. Petersen DJ, Srinivasan M, Chanway CP (1996) Bacillus polymyxa stimulates increased Rhizobium etli populations and nodulation when co-resident in the rhizosphere of Phaseolus vulgaris. FEMS Microbiol Lett 142: 271 - 276Google Scholar
  89. Phillips DA, Strong DR (2003) Rhizosphere control points: molecules to food webs. Ecology 84: 815CrossRefGoogle Scholar
  90. Phillips DA, Ferris H, Cook DR, Strong DR (2003) Molecular control points in rhizosphere food webs. Ecology 84: 816 - 826CrossRefGoogle Scholar
  91. Polis GA (1991) Complex trophic interactions in deserts: an empirical critique of food-web theory.Am Nat 138: 123 - 155Google Scholar
  92. Polis GA (1994) Food webs, trophic cascades and community structure. Aust J Ecol 19: 121 - 136CrossRefGoogle Scholar
  93. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147: 813 - 846CrossRefGoogle Scholar
  94. Price PW (199 1) The plant vigor hypotheses and herbivore attack. Oikos 62:244-251Google Scholar
  95. Puri G, Ashman MR (1999) Microbial immobilization of 15N-labelled ammonium and nitrate in a temperate woodland soil. Soil Biol Biochem 31: 929 - 931CrossRefGoogle Scholar
  96. Reichle DE, O’Neill RV, Harris WF (1975) Principles of energy and material exchange in ecosystems. In: Van Dobben WH, Lowe McConnell RH (eds) Unifying concepts in ecology. Junk, The Hague, pp 27 - 43Google Scholar
  97. Reinhold-Hurek B, Hurek T (1997) Azoarcus spp. and their interactions with grass roots. Plant Soil 194: 57 - 64Google Scholar
  98. Ritz K, Griffiths BS (1987) Effects of carbon and nitrate additions to soil upon leaching of nitrate, microbial predators and nitrogen uptake by plants. Plant Soil 102: 289 - 237CrossRefGoogle Scholar
  99. Robinson D (1994) The response of plants to non-uniform supplies of nutrients. New Phytol 127: 635 - 674CrossRefGoogle Scholar
  100. Rolfe BG, Djordjevic MA, Weinman JJ, Mathesius U, Pittock C, Gärtner E, Ride EM, Dong Z, McCully M, McIver J (1997) Root morphogenesis in legumes and cereals and the effect of bacterial inoculation on root development. Plant Soil 194: 131 - 144CrossRefGoogle Scholar
  101. Rovira AD (199 1) Rhizosphere research–85 years of progress and frustration. In: Kleister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 3-13Google Scholar
  102. Ryle GJA, Powell CE, Gordon AJ (1979) The respiratory costs of nitrogen fixation in soybean, cowpea and white clover. J Exp Bot 30: 145 - 153CrossRefGoogle Scholar
  103. Scheu S (1993) There is an earthworm mobilizable nitrogen pool in soil. Pedobiologia 37: 1 - 7Google Scholar
  104. Scheu S (2001) Plants and generalist predators as links between the below-ground and above-ground system. Basic Appl Ecol 2: 3 - 13CrossRefGoogle Scholar
  105. Scheu S, Setälä H (2002) Multitrophic interactions in decomposer food webs. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 223 - 264CrossRefGoogle Scholar
  106. Scheu S, Theenhaus A, Jones H (1999) Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development.Oecologia 119: 541 - 551Google Scholar
  107. Schulman OP, Tiunov AV (1999) Leaf litter fragmentation by the earthworm Lumbricus terrestris L. Pedobiologia 43: 453 - 458Google Scholar
  108. Settle WH, Ariawan H, Tri Astuti E, Cahyana W, Hakim AL, Hindayana D, Sri Lestari A, Sartano P (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77: 1975 - 1988CrossRefGoogle Scholar
  109. Shishido M, Massicotte HB, Chanway CP (1996) Effect of plant growth promoting Bacillus strains on pine and spruce seedling growth and mycorrhizal infection. Ann Bot 77: 433 - 441CrossRefGoogle Scholar
  110. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  111. Snyder WE, Wise DH (1999) Predator interference and the establishment of generalist predator populations for biocontrol. Biol Control 15: 283 - 292CrossRefGoogle Scholar
  112. Söderström B (1992) The ecological potential of the ectomycorrhizal mycelium. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 77 - 83Google Scholar
  113. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24: 487 - 506Google Scholar
  114. Stephens PM, Davoren CW (1997) Influence of the earthworms Aporrectodea trapezoides and A. rosea on the disease severity of Rhizoctonia solani on subterranean clover and ryegrass. Soil Biol Biochem 29: 511 - 516CrossRefGoogle Scholar
  115. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47: 561 - 594PubMedCrossRefGoogle Scholar
  116. Meijden E, Klinkhamer PGL (2000) Conflicting interests of plants and the natural enemies of herbivores. Oikos 89: 202 - 208CrossRefGoogle Scholar
  117. Verhagen FJM, Hagemann PEJ, Woldendorp JW, Laanbroek HJ (1994) Competition for ammonium between nitrifying bacteria and plant roots in soil in pots; effects of grazing by flagellates and fertilization. Soil Biol Biochem 26: 89 - 96CrossRefGoogle Scholar
  118. Wamberg C, Christensen S, Jakobsen I (2003) Interaction between foliar-feeding insects, mycorrhizal fungi, and rhizosphere protozoa on pea plants. Pedobiologia 47: 281 - 287CrossRefGoogle Scholar
  119. Wang JG, Bakken LR (1997) Competition for nitrogen during mineralization of plant residues in soil: microbial response to C and N. Soil Biol Biochem 29: 163 - 170CrossRefGoogle Scholar
  120. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67: 321 - 358CrossRefGoogle Scholar
  121. Wardle DA, Yeates GW (1993) The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food webs. Oecologia 93: 303 - 306CrossRefGoogle Scholar
  122. White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin Heidelberg New YorkCrossRefGoogle Scholar
  123. Wise DH, Snyder WE, Tuntibunpakul P, Halaj J (1999) Spiders in decomposition food webs of agroecosystems: theory and evidence. J Arachnol 27: 363 - 370Google Scholar
  124. Wurst S, Jones TH (2003) Indirect effects of earthworms (Aporrectodea caliginosa) on an above-ground tritrophic interaction. Pedobiologia 47: 91 - 97CrossRefGoogle Scholar
  125. 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 - 96PubMedCrossRefGoogle Scholar
  126. Wurst S, Dugassa-Gobena D, Scheu S (2004) Earthworms and litter distribution affect plant defensive chemistry. J Chem Ecol 30 (4)Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • M. Bonkowski
  • S. Scheu

There are no affiliations available

Personalised recommendations