Plant and Soil

, Volume 321, Issue 1–2, pp 213–233 | Cite as

Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots

  • Michael BonkowskiEmail author
  • Cécile Villenave
  • Bryan Griffiths
Review Article


For decades, the term “rhizosphere fauna” has been used as a synonym to denote agricultural pests among root herbivores, mainly nematodes and insect larvae. We want to break with this constrictive view, since the connection between plants and rhizosphere fauna is far more complex than simply that of resource and consumer. For example, plant roots have been shown to be neither defenceless victims of root feeders, nor passive recipients of nutrients, but instead play a much more active role in defending themselves and in attracting beneficial soil microorganisms and soil fauna. Most importantly, significant indirect feed-backs exist between consumers of rhizosphere microorganisms and plant roots. In fact, the majority of soil invertebrates have been shown to rely profoundly on the carbon inputs from roots, breaking with the dogma of soil food webs being mainly fueled by plant litter input from aboveground. In this review we will highlight areas of recent exciting progress and point out the black boxes that still need to be illuminated by rhizosphere zoologists and ecologists.


Rhizosphere food web Root herbivores Signalling Microbial vectors Root growth Energy channel 



We are very grateful to Prof. Dr. Donald Phillips and Dr. Tama Fox, Plant Sciences Department, University of California, Davis, USA, for their collaborative support for MB and for providing the data on DAPG production by pseudomonads for this review.


  1. Albers D, Schaefer M, Scheu S (2006) Incorporation of plant carbon into the soil animal food web of an arable system. Ecology 87:235–245. doi: 10.1890/04-1728 PubMedCrossRefGoogle Scholar
  2. Arndt H, Schmidt-Denter K, Auer B, Weitere M (2003) Protozoans and biofilms. In: Krumbein WE, Paterson DM, Zavarzin GA (eds) Fossil and recent biofilms. Kluwer Academic, Dordrecht, pp 173–189Google Scholar
  3. Ayres E, Dromph KM, Cook R, Ostle N, Bardgett RD (2007) The influence of below-ground herbivory and defoliation of a legume on nitrogen transfer to neighbouring plants. Funct Ecol 21:256–263. doi: 10.1111/j.1365-2435.2006.01227.x CrossRefGoogle Scholar
  4. Bais H, Park S, Weir T, Callaway R, Vivanco J (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32. doi: 10.1016/j.tplants.2003.11.008 PubMedCrossRefGoogle Scholar
  5. Bais H, Weir T, Perry L, Gilroy S, Vivanco J (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi: 10.1146/annurev.arplant.57.032905.105159 PubMedCrossRefGoogle Scholar
  6. Bakonyi G, Posta K, Kiss I, Fábián M, Nagy P, Nosek JN (2002) Density-dependent regulation of arbuscular mycorrhiza by collembola. Soil Biol Biochem 34:661–664. doi: 10.1016/S0038-0717(01)00228-0 CrossRefGoogle Scholar
  7. Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol Biochem 31:1007–1014. doi: 10.1016/S0038-0717(99)00014-0 CrossRefGoogle Scholar
  8. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268. doi: 10.1890/02-0274 CrossRefGoogle Scholar
  9. Bardgett R, Wardle D, Yeates G (1998) Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878. doi: 10.1016/S0038-0717(98)00069-8 CrossRefGoogle Scholar
  10. Bardgett R, Cook R, Yeates G, Denton C (1999a) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33. doi: 10.1023/A:1004642218792 CrossRefGoogle Scholar
  11. Bardgett R, Denton C, Cook R (1999b) Below-ground herbivory promotes soil nutrient transfer and root growth in grassland. Ecol Lett 2:357–360. doi: 10.1046/j.1461-0248.1999.00001.x CrossRefGoogle Scholar
  12. Bauer W, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433. doi: 10.1016/j.pbi.2004.05.008 PubMedCrossRefGoogle Scholar
  13. Beale E, Li G, Tan M-W, Rumbaugh KP (2006) Caenorhabditis elegans senses bacterial autoinducers. Appl Environ Microbiol 72:5135–5137PubMedCrossRefGoogle Scholar
  14. Beare M, Coleman D, Crossley D, Hendrix P, Odum E (1995) A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant Soil 170:5–22. doi: 10.1007/BF02183051 CrossRefGoogle Scholar
  15. Beyeler M, Keel C, Michaux P, Haas D (1999) Enhanced production of indole-3-acetic acid by a genetically modified strain of Pseudomonas fluorescens CHA0 affects root growth of cucumber, but does not improve protection of the plant against Phytium root rot. FEMS Microbiol Ecol 28:225–233. doi: 10.1111/j.1574-6941.1999.tb00578.x CrossRefGoogle Scholar
  16. Bezemer TM, Van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624. doi: 10.1016/j.tree.2005.08.006 PubMedCrossRefGoogle Scholar
  17. Bezemer TM, Wagenaar R, Dam NMV, Wäckers FL (2003) Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101:555–562. doi: 10.1034/j.1600-0706.2003.12424.x CrossRefGoogle Scholar
  18. Bezemer TM, De Deyn GB, Bossinga TM, Van Dam NM, Harvey JA, Van Der Putten WH (2005) Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecol Lett 8:652–661. doi: 10.1111/j.1461-0248.2005.00762.x CrossRefGoogle Scholar
  19. Bjørnlund L, Mørk S, Vestergard M, Rønn R (2006) Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley. Biol Fertil Soils 43:1–11. doi: 10.1007/s00374-005-0052-7 CrossRefGoogle Scholar
  20. Blanc C, Sy M, Djigal D, Brauman A, Normand P, Villenave C (2006) Nutrition on bacteria by bacterial-feeding nematodes and consequences on the structure of soil bacterial community. Eur J Soil Biol 42, Suppl 1:S70–S78CrossRefGoogle Scholar
  21. Blouin M, Zuily-Fodil Y, Pham-Thi AT, Laffray D, Reversat G, Pando A, Tondoh J, Lavelle P (2005) Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites. Ecol Lett 8:202–208CrossRefGoogle Scholar
  22. Boenigk J, Arndt H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie Leeuwenhoek 81:465–480PubMedCrossRefGoogle Scholar
  23. Boff MIC, Zoon FC, Smits PH (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomol Exp Appl 98:329–337. doi: 10.1023/A:1018907812376 CrossRefGoogle Scholar
  24. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631. doi: 10.1111/j.1469-8137.2004.01066.x CrossRefGoogle Scholar
  25. Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34:1709–1715. doi: 10.1016/S0038-0717(02)00157-8 CrossRefGoogle Scholar
  26. 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 36:135–147. doi: 10.1016/S1164-5563(00)01059-1 CrossRefGoogle Scholar
  27. Bonkowski M, Griffiths B, Scrimgeour C (2000b) Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Appl Soil Ecol 14:37–53. doi: 10.1016/S0929-1393(99)00047-5 CrossRefGoogle Scholar
  28. Bonkowski M, Griffiths BS, Ritz K (2000c) Food preferences of earthworms for soil fungi. Pedobiologia (Jena) 44:666–676. doi: 10.1078/S0031-4056(04)70080-3 CrossRefGoogle Scholar
  29. Bouwman LA, Zwart KB (1994) The ecology of bacterivorous protozoans and nematodes in arable soil. Agric Ecosyst Environ 51:145–160CrossRefGoogle Scholar
  30. Bracht Jørgensen H, Johansson T, Canbäck B, Hedlund K, Tunlid A (2005) Selective foraging of fungi by collembolans in soil. Biol Lett 1:243–246. doi: 10.1098/rsbl.2004.0286 CrossRefGoogle Scholar
  31. Bretherton S, Tordoff GM, Jones TH, Boddy L (2006) Compensatory growth of Phanerochaete velutina mycelial systems grazed by Folsomia candida (Collembola). FEMS Microbiol Ecol 58:33–40. doi: 10.1111/j.1574-6941.2006.00149.x PubMedCrossRefGoogle Scholar
  32. Brimecombe M, De Leij F, Lynch J (2000) Effect of introduced Pseudomonas fluorescens strains on soil nematode and protozoan populations in the rhizosphere of wheat and pea. Microb Ecol 38:387–397. doi: 10.1007/s002489901004 CrossRefGoogle Scholar
  33. Brown V, Gange A (1989) Differential effects of abobe- and below-ground insect herbivory during early plant succession. Oikos 54:67–76. doi: 10.2307/3565898 CrossRefGoogle Scholar
  34. Brussaard L (1998) Soil fauna, guilds, functional groups and ecosystem processes. Appl Soil Ecol 9:123–135CrossRefGoogle Scholar
  35. Caldwell KN, Anderson GL, Williams PL, Beuchat LR (2003) Attraction of a free-living nematode, Caenorhabditis elegans, to foodborne pathogenic bacteria and its potential as a vector of Salmonella poona for preharvest contamination of cantaloupe. J Food Prot 66:1964–1971PubMedGoogle Scholar
  36. Campell BC, Nes WD (1983) A reappraisal of sterol biosynthesis and metabolism in aphids. J Insect Physiol 29:149–156. doi: 10.1016/0022-1910(83)90138-5 CrossRefGoogle Scholar
  37. Chakraborty S (1983) Population dynamics of amobae in soils suppressive and non-suppressive to wheat take-all. Soil Biol Biochem 15:661–664. doi: 10.1016/0038-0717(83)90029-9 CrossRefGoogle Scholar
  38. Chantanao A, Jensen HJ (1969) Saprozoic nematodes as carriers and disseminators of plant pathogenic bacteria. J Nematol 1:216–218PubMedGoogle Scholar
  39. Chanway C, Turkington R, Holl F (1991) Ecological implications of specificity between plants and rhizosphere micro-organisms. Adv Ecol Res 21:121–169. doi: 10.1016/S0065-2504(08)60098-7 CrossRefGoogle Scholar
  40. Chen J, Ferris H (1999) The effects of nematode grazing on nitrogen mineralization during fungal decomposition of organic matter. Soil Biol Biochem 31:1265–1279. doi: 10.1016/S0038-0717(99)00042-5 CrossRefGoogle Scholar
  41. Christensen M (1989) A view of fungal ecology. Mycologia 81:1–19. doi: 10.2307/3759446 CrossRefGoogle Scholar
  42. Christensen S, Bjørnlund L, Vestergard M (2007) Decomposer biomass in the rhizosphere to assess rhizodeposition. Oikos 116:65–74CrossRefGoogle Scholar
  43. Ciche TA, Darby C, Ehlers R-U, Forst S, Goodrich-Blair H (2006) Dangerous liaisons: the symbiosis of entomopathogenic nematodes and bacteria. Biol Control 38:22–46. doi: 10.1016/j.biocontrol.2005.11.016 CrossRefGoogle Scholar
  44. Clapperton MJ, Lee NO, Binet F, Conner RL (2001) Earthworms indirectly reduce the effects of take-all (Gaeumannomyces graminis var. tritici) on soft white spring wheat (Triticum aestivum cv. Fielder). Soil Biol Biochem 33:1531–1538. doi: 10.1016/S0038-0717(01)00071-2 CrossRefGoogle Scholar
  45. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187. doi: 10.1016/0038-0717(85)90113-0 CrossRefGoogle Scholar
  46. Clarholm M (1994) The microbial loop in soil. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass. Wiley-Sayce, Chichester, pp 221–230Google Scholar
  47. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. doi: 10.1023/A:1020809400075 CrossRefGoogle Scholar
  48. Davis E, Hussey R, Baum T, Bakker J, Schots A (2000) Nematode parasitism genes. Annu Rev Phytopathol 38:365–396. doi: 10.1146/annurev.phyto.38.1.365 PubMedCrossRefGoogle Scholar
  49. Dawson LA, Grayston SJ, Murray PJ, Pratt SM (2002) Root feeding behaviour of Tipula paludosa (Meig.) (Diptera : Tipulidae) on Loliumn perenne (L.) and Trifolium repens (L.). Soil Biol Biochem 34:609–615. doi: 10.1016/S0038-0717(01)00217-6 CrossRefGoogle Scholar
  50. De Deyn GB, Van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633. doi: 10.1016/j.tree.2005.08.009 PubMedCrossRefGoogle Scholar
  51. De Deyn G, Raaijmakers C, Zoomer H, Berg M, de Ruiter P, Verhoef H, Bezemer T, van der Putten W (2003a) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713. doi: 10.1038/nature01548 PubMedCrossRefGoogle Scholar
  52. De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, De Ruiter PC, Verhoef HA, Bezemer TM, Van der Putten WH (2003b) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713. doi: 10.1038/nature01548 PubMedCrossRefGoogle Scholar
  53. De Leij FAAM, Dixon-Hardy JE, Lynch JM (2002) Effect of 2, 4-diacetylphloroglucinol-producing and non-producing strains of Pseudomonas fluorescens on root development of pea seedlings in three different soil types and its effect on nodulation by Rhizobium. Biol Fertil Soils 35:114–121. doi: 10.1007/s00374-002-0448-6 CrossRefGoogle Scholar
  54. De Mesel I, Derycke S, Moens T, Van Der Gucht K, Vincx M, Swings J (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6:733–744. doi: 10.1111/j.1462-2920.2004.00610.x PubMedCrossRefGoogle Scholar
  55. Denton CS, Bardgett 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 31:155–165. doi: 10.1016/S0038-0717(98)00118-7 CrossRefGoogle Scholar
  56. Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant Cell Environ . doi: 10.1111/j.1365-3040.2008.01913.x PubMedGoogle Scholar
  57. Dixon AFG (1985) Aphid ecology. Blackie, Glasgow London, p 157Google Scholar
  58. Dromph KM (2003) Collembolans as vectors of entomopathogenic fungi. Pedobiologia (Jena) 47:245–256. doi: 10.1078/0031-4056-00188 CrossRefGoogle Scholar
  59. Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438. doi: 10.1098/rsbl.2007.0232 PubMedCrossRefGoogle Scholar
  60. Ekelund F, Rønn R (1994) Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol Rev 15:321–353. doi: 10.1111/j.1574-6976.1994.tb00144.x PubMedCrossRefGoogle Scholar
  61. Elfstrand S, Lagerlöf J, Hedlund K, Mårtensson A (2008) Carbon routes from decomposing plant residues and living roots into soil food webs assessed with 13C labelling. Soil Biol Biochem 40:2530–2539. doi: 10.1016/j.soilbio.2008.06.013 CrossRefGoogle Scholar
  62. Endlweber K, Scheu S (2006) Effects of Collembola on root properties of two competing ruderal plant species. Soil Biol Biochem 38:2025–2031CrossRefGoogle Scholar
  63. Endlweber K, Scheu S (2007) Interactions between mycorrhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43:741–749. doi: 10.1007/s00374-006-0157-7 CrossRefGoogle Scholar
  64. Erb M, Ton J, Degenhardt J, Turlings TCJ (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874PubMedCrossRefGoogle Scholar
  65. Fitter AH, Gilligan CA, Hollingworth K, Kleczkowski A, Twyman RM, Pitchford JW (2005) Biodiversity and ecosystem function in soil. Funct Ecol 19:369–377. doi: 10.1111/j.0269-8463.2005.00969.x CrossRefGoogle Scholar
  66. Fu SL, Ferris H, Brown D, Plant R (2005) Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biol Biochem 37:1979–1987CrossRefGoogle Scholar
  67. Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372. doi: 10.1016/S0169-5347(00)01940-6 PubMedCrossRefGoogle Scholar
  68. Gange A, Brown V (1997) Multitrophic interactions in terrestrial systems. Blackwell, OxfordGoogle Scholar
  69. Geltzer JG (1963) On the behaviour of soil amoebae in the rhizospheres of plants. Pedobiologia (Jena) 2:249–251Google Scholar
  70. Gheysen G, Jones J (2006) Molecular aspects of plant-nematode interactions. In: Perry R, Moens M (eds) Plant Nematology. CABI, pp 234–254Google Scholar
  71. Goellner M, Wang X, Davis EL (2001) Endo-1, 4-glucanase expression in compatible plant nematode interactions. Plant Cell 13:2241–2255PubMedCrossRefGoogle Scholar
  72. Gormsen D, Olsson PA, Hedlund K (2004) The influence of collembolans and earthworms on AM fungal mycelium. Appl Soil Ecol 27:211–220CrossRefGoogle Scholar
  73. Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129. doi: 10.1094/MPMI.2000.13.10.1121 PubMedCrossRefGoogle Scholar
  74. Grayston SJ, Dawson LA, Treonis AM, Murray PJ, Ross J, Reid EJ, MacDougall R (2001) Impact of root herbivory by insect larvae on soil microbial communities. Eur J Soil Biol 37:277–280. doi: 10.1016/S1164-5563(01)01098-6 CrossRefGoogle Scholar
  75. Grewal PS (1991) Effects of Caenorhabditis elegans(Nematoda: Rhabditidae) on the spread of the bacterium Pseudomonas tolaasii in mushrooms (Agaricus bisporus). Ann Appl Biol 118:47–55. doi: 10.1111/j.1744-7348.1991.tb06084.x CrossRefGoogle Scholar
  76. Griffiths BS (1990) A comparison of microbial-feeding nematodes and protozoa in the rhizosphere of different plants. Biol Fertil Soils 9:83–88. doi: 10.1007/BF00335867 CrossRefGoogle Scholar
  77. Griffiths BS (1994) Soil nutrient flow. In: Darbyshire J (ed) Soil protozoa. CAB International, Wallingford, pp 65–91Google Scholar
  78. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319. doi: 10.1038/nrmicro1129 PubMedCrossRefGoogle Scholar
  79. Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153. doi: 10.1146/annurev.phyto.41.052002.095656 PubMedCrossRefGoogle Scholar
  80. Haase S, Ruess L, Neumann G, Marhan S, Kandeler E (2007) Low-level herbivory by root-knot nematodes (Meloidogyne incognita) modifies root hair morphology and rhizodeposition in host plants (Hordeum vulgare). Plant Soil 301:151–164. doi: 10.1007/s11104-007-9431-1 CrossRefGoogle Scholar
  81. Hall M, Hedlund K (1999) A soil mite uses fungal cues in search for its collembolan prey. Pedobiologia (Jena) 43:11–17Google Scholar
  82. Harold S, Tordoff GM, Jones TH, Boddy L (2005) Mycelial responses of Hypholoma fasciculare to collembola grazing: effect of inoculum age, nutrient status and resource quality. Mycol Res 109:927–935. doi: 10.1017/S095375620500331X PubMedCrossRefGoogle Scholar
  83. Harris KK, Boerner REJ (1990) Effects of belowground grazing by collembola on growth, mycorrhizal infection, and P uptake of Geranium robertianum. Plant Soil 129:203–210Google Scholar
  84. Hatch D, Murray P (1994) Transfer of nitrogen from damaged roots of white clover (Trifolium repens L.) to closely associated roots of intact perennial ryegrass (Lolium perenne L.). Plant Soil 166:181–185. doi: 10.1007/BF00008331 CrossRefGoogle Scholar
  85. Hedlund K, Sjögren Öhrn M (2000) Tritrophic interactions in a soil community enhance decomposition rates. Oikos 88:585–591CrossRefGoogle Scholar
  86. Henderson V, Katznelson H (1961) The effect of plant roots on the nematode population of the soil. Can J Microbiol 7:163–167PubMedCrossRefGoogle Scholar
  87. Herdler S, Kreuzer K, Scheu S, Bonkowskia M (2008) Interactions between arbuscular mycorrhizal fungi (Glomus intraradices, Glomeromycota) and amoebae (Acanthamoeba castellanii, Protozoa) in the rhizosphere of rice (Oryza sativa). Soil Biol Biochem 40:660–668. doi: 10.1016/j.soilbio.2007.09.026 CrossRefGoogle Scholar
  88. Horiuchi J-I, Prithiviraj B, Bais H, Kimball B, Vivanco J (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857. doi: 10.1007/s00425-005-0025-y PubMedCrossRefGoogle Scholar
  89. Huber B, Feldmann F, Köthe M, Vandamme P, Wopperer J, Riedel K, Eberl L (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect Immun 72:7220–7230. doi: 10.1128/IAI.72.12.7220-7230.2004 PubMedCrossRefGoogle Scholar
  90. 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 75:2146–2157Google Scholar
  91. Ingham RE, Trofymow JA, Ingham ER, Coleman DC (1985) Interactions of bacteria, fungi, and their nematode grazers: Effects on nutrient cycling and plant growth. Ecol Monographs 55:119–140CrossRefGoogle Scholar
  92. Jacobs M, Rubery PH (1988) Naturally-occuring auxin transport regulators. Science 241:346–349. doi: 10.1126/science.241.4863.346 PubMedCrossRefGoogle Scholar
  93. Jentschke G, Bonkowski M, Godbold DL, Scheu S (1995) Soil protozoa and forest tree growth: non-nutritional effects and interaction with mycorrhizae. Biol Fertil Soils 20:263–269. doi: 10.1007/BF00336088 CrossRefGoogle Scholar
  94. Jezbera J, Hornak K, Simek K (2006) Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients. Environ Microbiol 8:1330–1339. doi: 10.1111/j.1462-2920.2006.01026.x PubMedCrossRefGoogle Scholar
  95. Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309:1047. doi: 10.1126/science.1114769 PubMedCrossRefGoogle Scholar
  96. Jonas JL, Wilson GWT, White PM, Joern A (2007) Consumption of mycorrhizal and saprophytic fungi by Collembola in grassland soils. Soil Biol Biochem 39:2594–2602CrossRefGoogle Scholar
  97. Joseph C, Phillips D (2003) Metabolites from soil bacteria affect plant water relations. Plant Physiol Biochem 41:189–192. doi: 10.1016/S0981-9428(02)00021-9 CrossRefGoogle Scholar
  98. Joshi A, Chand R, Arun B, Singh R, Ortiz R (2007) Breeding crops for reduced-tillage management in the intensive, rice-wheat systems of South Asia. Euphytica 153:135–151. doi: 10.1007/s10681-006-9249-6 CrossRefGoogle Scholar
  99. Jousset A, Lara E, Wall LG, Valverde C (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microbiol 72:7083–7090. doi: 10.1128/AEM.00557-06 PubMedCrossRefGoogle Scholar
  100. Jousset A, Scheu S, Bonkowski M (2008) Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria. Funct Ecol 22:714–719CrossRefGoogle Scholar
  101. Jousset A, Péchy-Tarr M, Rochat L, Keel C, Scheu S, Bonkowski M (2009) Cheating and predation determine the toxin production by the biocontrol bacterium Pseudomonas fluorescens CHA0. (submitted)Google Scholar
  102. Kampichler C, Rolschewski J, Donnelly DP, Boddy L (2004) Collembolan grazing affects the growth strategy of the cord-forming fungus Hypholoma fasciculare. Soil Biol Biochem 36:591–599. doi: 10.1016/j.soilbio.2003.12.004 CrossRefGoogle Scholar
  103. Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406. doi: 10.1890/07-0471.1 PubMedCrossRefGoogle Scholar
  104. Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Defago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2, 4-diacetylphloroglucinol. Mol Plant Microbe Interact 5:4–13Google Scholar
  105. Kimpinski J, Sturz A (1996) Population growth of a rhabditid nematode on plant growth promoting bacteria from potato tubers and rhizosphere soil. J Nematol 28:682–686PubMedGoogle Scholar
  106. Klironomos JN, Hart MM (2001) Animal nitrogen swap for plant carbon. Nature 410:651–652. doi: 10.1038/35070643 PubMedCrossRefGoogle Scholar
  107. Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fertil Soils 21:43–52. doi: 10.1007/BF00335992 CrossRefGoogle Scholar
  108. Klironomos JN, Ursic M (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Biol Fertil Soils 26:250–253. doi: 10.1007/s003740050375 CrossRefGoogle Scholar
  109. Knox OGG, Killham K, Mullins CE, Wilson MJ (2003) Nematode-enhanced microbial colonization of the wheat rhizosphere. FEMS Microbiol Lett 225:227–233. doi: 10.1016/S0378-1097(03)00517-2 PubMedCrossRefGoogle Scholar
  110. Knox OGG, Killham K, Artz RRE, Mullins C, Wilson M (2004) Effect of nematodes on rhizosphere colonization by seed-applied bacteria. Appl Environ Microbiol 70:4666–4671. doi: 10.1128/AEM.70.8.4666-4671.2004 PubMedCrossRefGoogle Scholar
  111. Köthe M, Antl M, Huber B, Stoecker K, Ebrecht D, Steinmetz I, Eberl L (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell Microbiol 5:343–351. doi: 10.1046/j.1462-5822.2003.00280.x PubMedCrossRefGoogle Scholar
  112. Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S, Bonkowski M (2006) Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biol Biochem 38:1665–1672. doi: 10.1016/j.soilbio.2005.11.027 CrossRefGoogle Scholar
  113. 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 10:22–28Google Scholar
  114. Kuzyakov Y, Friedel J, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:185–1498CrossRefGoogle Scholar
  115. Laakso J, Setälä H (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87:57–64. doi: 10.2307/3546996 CrossRefGoogle Scholar
  116. Larsen T, Gorissen A, Krogh P, Ventura M, Magid J (2007) Assimilation dynamics of soil carbon and nitrogen by wheat roots and Collembola. Plant Soil 295:253–264. doi: 10.1007/s11104-007-9280-y CrossRefGoogle Scholar
  117. Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Appl Soil Ecol 33:152–175. doi: 10.1016/j.apsoil.2006.03.001 CrossRefGoogle Scholar
  118. Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97:762–769. doi: 10.3852/mycologia.97.4.762 CrossRefPubMedGoogle Scholar
  119. Liu XY, Shi M, Liao YH, Gao Y, Zhang ZK, Wen DH, Wu WZ, An CC (2006) Feeding characteristics of an amoeba (Lobosea: Naegleria) grazing upon cyanobacteria: food selection, ingestion and digestion progress. Microb Ecol 51:315–325. doi: 10.1007/s00248-006-9031-2 CrossRefGoogle Scholar
  120. Malamy J, Benfey P (1997) Lateral root formation in Arabidopsis thaliana. Plant Physiol 114:277Google Scholar
  121. Mao X, Hu F, Griffiths B, Li H (2006) Bacterial-feeding nematodes enhance root growth of tomato seedlings. Soil Biol Biochem 38:1615–1622CrossRefGoogle Scholar
  122. Mao X, Hu F, Griffiths B, Chen X, Liu M, Li H (2007) Do bacterial-feeding nematodes stimulate root proliferation through hormonal effects? Soil Biol Biochem 39:1816–1819. doi: 10.1016/j.soilbio.2007.01.027 CrossRefGoogle Scholar
  123. Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes—the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant Soil 255:105–119. doi: 10.1023/A:1026139026780 CrossRefGoogle Scholar
  124. Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe B, Bauer W (2003) Extensive and specific responses of a Eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449. doi: 10.1073/pnas.262672599 PubMedCrossRefGoogle Scholar
  125. Matz C, Kjelleberg S (2005) Off the hook—how bacteria survive protozoan grazing. Trends Microbiol 13:302–307. doi: 10.1016/j.tim.2005.05.009 PubMedCrossRefGoogle Scholar
  126. Matz C, Bergfeld T, Rice SA, Kjelleberg S (2004a) Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6:218–226. doi: 10.1111/j.1462-2920.2004.00556.x PubMedCrossRefGoogle Scholar
  127. Matz C, Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Jürgens K (2004b) Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl Environ Microbiol 70:1593–1599. doi: 10.1128/AEM.70.3.1593-1599.2004 PubMedCrossRefGoogle Scholar
  128. Maurhofer M, Baehler E, Notz R, Martinez V, Keel C (2004) Cross talk between 2, 4-diacetylphloroglucinol-producing biocontrol pseudomonads on wheat roots. Appl Environ Microbiol 70:1990–1998. doi: 10.1128/AEM.70.4.1990-1998.2004 PubMedCrossRefGoogle Scholar
  129. McKenzie Bird D (2004) Signaling between nematodes and plants. Curr Opin Plant Biol 7:372–376. doi: 10.1016/j.pbi.2004.05.005 CrossRefGoogle Scholar
  130. Montagnes DJS, Barbosa AB, Boenigk J, Davidson K, Jurgens K, Macek M, Parry JD, Roberts EC, Simek K (2007) Selective feeding behaviour of key free-living protists: avenues for continued study. In 10th Symposium on Aquatic Microbial Ecology (SAME 10). pp 83–98. Inter-Research, Faro, PORTUGAL.Google Scholar
  131. Moore JC, Hunt WH (1988) Resource compartmentation and the stability of real ecosystems. Nature 333:261–263. doi: 10.1038/333261a0 CrossRefGoogle Scholar
  132. Munn E, Munn P (2002) Feeding and digestion. In: Lee D (ed) The biology of nematodes. Taylor & Francis, Singapore, pp 211–232Google Scholar
  133. Murase J, Noll M, Frenzel P (2006) Impact of protists on the activity and structure of the bacterial community in a rice field soil. Appl Environ Microbiol 72:5436–5444. doi: 10.1128/AEM.00207-06 PubMedCrossRefGoogle Scholar
  134. 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 74:1591–1595. doi: 10.1139/b96-192 CrossRefGoogle Scholar
  135. Muscolo A, Bovalo F, Gionfriddo F, Nardi S (1999) Earthworm humic matter produces auxin-like effects on Daucus carota cell growth and nitrate metabolism. Soil Biol Biochem 31:1303–1311. doi: 10.1016/S0038-0717(99)00049-8 CrossRefGoogle Scholar
  136. Nardi S, Panuccio MR, Abenavoli MR, Muscolo A (1994) Auxin-like effect of humic substances extracted from faeces of Allolobophora caliginosa and A. rosea. Soil Biol Biochem 26:1341–1346. doi: 10.1016/0038-0717(94)90215-1 CrossRefGoogle Scholar
  137. Newsham KK, Rolf J, Pearce DA, Strachan RJ (2004) Differing preferences of Antarctic soil nematodes for microbial prey. Europ J Soil Biol 40:1–8CrossRefGoogle Scholar
  138. Ostle N, Briones MJI, Ineson P, Cole L, Staddon P, Sleep D (2007) Isotopic detection of recent photosynthate carbon flow into grassland rhizosphere fauna. Soil Biol Biochem 39:768–777. doi: 10.1016/j.soilbio.2006.09.025 CrossRefGoogle Scholar
  139. Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Europ J Soil Sci 54:741–750CrossRefGoogle Scholar
  140. Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3:537–546. doi: 10.1038/nrmicro1180 PubMedCrossRefGoogle Scholar
  141. Pfander I, Zettel J (2004) Chemical communication in Ceratophysella sigillata (Collembola: Hypogastruridae): intraspecific reaction to alarm substances. Pedobiologia (Jena) 48:575–580. doi: 10.1016/j.pedobi.2004.06.002 CrossRefGoogle Scholar
  142. Phillips DA, Streit W (1998) Modifying rhizosphere microbial communities to enhance nutrient availability in cropping systems. Field Crops Res 56:217–221. doi: 10.1016/S0378-4290(97)00133-0 CrossRefGoogle Scholar
  143. Phillips D, Joseph C, Yang G, Martinez-Romero E, Sanborn J, Volpin H (1999) Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proc Natl Acad Sci USA 96:12275–12280. doi: 10.1073/pnas.96.22.12275 PubMedCrossRefGoogle Scholar
  144. Phillips D, Ferris H, Cook D, Strong D (2003) Molecular control points in rhizosphere food webs. Ecology 84:816–826CrossRefGoogle Scholar
  145. Phillips D, Fox T, King M, Bhuvaneswari T, Teuber L (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894. doi: 10.1104/pp. 104.044222 PubMedCrossRefGoogle Scholar
  146. Pickup ZL, Pickup R, Parry JD (2007) Effects of bacterial prey species and their concentration on growth of the amoebae Acanthamoeba castellanii and Hartmannella vermiformis. Appl Environ Microbiol 73:2631–2634PubMedCrossRefGoogle Scholar
  147. Poll J, Marhan S, Haase S, Hallmann J, Kandeler E, Ruess L (2007) Low amounts of herbivory by root-knot nematodes affect microbial community dynamics and carbon allocation in the rhizosphere. FEMS Microbiol Ecol 62:268–279. doi: 10.1111/j.1574-6941.2007.00383.x PubMedCrossRefGoogle Scholar
  148. Pollierer M, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736. doi: 10.1111/j.1461-0248.2007.01064.x PubMedCrossRefGoogle Scholar
  149. Popeijus H, Overmars H, Jones J, Blok V, Goverse A, Helder J, Schots A, Bakker J, Smant G (2000) Enzymology—Degradation of plant cell walls by a nematode. Nature 406:36–37. doi: 10.1038/35017641 PubMedCrossRefGoogle Scholar
  150. Puthoff D, Nettleson D, Rodermel S, Baum T (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profile. Plant J 33:911–921. doi: 10.1046/j.1365-313X.2003.01677.x PubMedCrossRefGoogle Scholar
  151. Rantalainen ML, Fritze H, Haimi J, Kiikkila O, Pennanen T, Setala H (2004) Do enchytraeid worms and habitat corridors facilitate the colonisation of habitat patches by soil microbes? Biol Fertil Soils 39:200–208CrossRefGoogle Scholar
  152. Rantalainen M-L, Fritze H, Haimi J, Pennanen T, Setälä H (2005) Species richness and food web structure of soil decomposer community as affected by the size of habitat fragment and habitat corridors. Glob Change Biol 11:1614–1627. doi: 10.1111/j.1365-2486.2005.000999.x CrossRefGoogle Scholar
  153. Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880PubMedCrossRefGoogle Scholar
  154. Rasmann S, Turlings TCJ (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10:926–936. doi: 10.1111/j.1461-0248.2007.01084.x PubMedCrossRefGoogle Scholar
  155. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. doi: 10.1038/nature03451 PubMedCrossRefGoogle Scholar
  156. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312. doi: 10.1111/j.1469-8137.2005.01558.x PubMedCrossRefGoogle Scholar
  157. Renker C, Otto P, Schneider K, Zimdars B, Maraun M, Buscot F (2005) Oribatid mites as potential vectors for soil microfungi: study of mite-associated fungal species. Microb Ecol 50:518–528. doi: 10.1007/s00248-005-5017-8 PubMedCrossRefGoogle Scholar
  158. Riga E (2004) Orientation behavior. In: Gaugler R, Bilgrami AL (eds) Nematode behaviour. CABI, Wallingford, pp 63–90Google Scholar
  159. Robinson AF (2003) Nematode behaviour and migrations through soil and host tissue. In: Zhongxiao X, Chen SY, Dickson DW (eds) Nematology advances and perspectives. Volume 1, Nematode morphology, physiology, and ecology. CABI, Wallingford, pp 330–405Google Scholar
  160. Rodger S, Bengough AG, Griffiths BS, Stubbs V, Young IM (2003) Does the presence of detached root border cells of Zea mays alter the activity of the pathogenic nematode Meloidogyne incognita?. Phytopathology 93:1111–1114. doi: 10.1094/PHYTO.2003.93.9.1111 PubMedCrossRefGoogle Scholar
  161. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269. doi: 10.1038/nature04887 PubMedCrossRefGoogle Scholar
  162. Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J, The ISME Journal advance online publication 26 February 2009. doi: 10.1038/ismej.2009.11
  163. Rudrappa T, Biedrzycki ML, Bais HP (2008) Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol 64:153–166. doi: 10.1111/j.1574-6941.2008.00465.x PubMedCrossRefGoogle Scholar
  164. Sabatini MA, Innocenti G (2001) Effects of Collembola on plant-pathogenic fungus interactions in simple experimental systems. Biol Fertil Soils 33:62–66. doi: 10.1007/s003740000290 CrossRefGoogle Scholar
  165. Schädler M, Jung G, Brandl R, Auge H (2004) Secondary succession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252. doi: 10.1007/s00442-003-1425-y PubMedCrossRefGoogle Scholar
  166. Scheu S (1993) Cellulose and lignin decomposition in soils from different ecosystems on limestone as affected by earthworm processing. Pedobiologia 37:167–177Google Scholar
  167. Scheu S, Folger M (2004) Single and mixed diets in Collembola: effects on reproduction and stable isotope fractionation. Funct Ecol 18:94–102. doi: 10.1046/j.0269-8463.2004.00807.x CrossRefGoogle Scholar
  168. 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 223–264Google Scholar
  169. Scheu S, Simmerling F (2004) Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets. Oecologia 139:347–353. doi: 10.1007/s00442-004-1513-7 PubMedCrossRefGoogle Scholar
  170. Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivore and the herbivore system: effects of earthworms and collembola on plant growth and aphid development. Oecologia 119:541–551. doi: 10.1007/s004420050817 CrossRefGoogle Scholar
  171. Schulman O, Tiunov A (1999) Leaf litter fragmentation by the earthworm Lumbricus terrestris L. Pedobiologia 43:453–458Google Scholar
  172. Seres A, Bakonyi G, Posta K (2007) Collembola (Insecta) disperse the arbuscular mycorrhizal fungi in the soil: pot experiment. Pol J Ecol 55:395–399Google Scholar
  173. Setälä H (1995) Growth of birch and pine seedlings in relation to grazing by soil fauna on ectomycorrhizal fungi. Ecology 76:1844–1851. doi: 10.2307/1940716 CrossRefGoogle Scholar
  174. Shapiro J (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104. doi: 10.1146/annurev.micro.52.1.81 PubMedCrossRefGoogle Scholar
  175. Shiraishi H, Enami Y, Okano S (2003) Folsomia hidakana (Collembola) prevents damping-off disease in cabbage and Chinese cabbage by Rhizoctonia solani. Pedobiologia (Jena) 47:33–38. doi: 10.1078/0031-4056-00167 CrossRefGoogle Scholar
  176. Siddiqui IA, Haas D, Heeb S (2005) Extracellular protease of Pseudomonas fluorescens CHA0, a biocontrol factor with activity against the root-knot nematode Meloidogyne incognita. Appl Environ Microbiol 71:5646–5649. doi: 10.1128/AEM.71.9.5646-5649.2005 PubMedCrossRefGoogle Scholar
  177. Soler R, Bezemer TM, Cortesero AM, Van Der Putten WH, Vet LEM, Harvey JA (2007) Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid. Oecologia 152:257–264. doi: 10.1007/s00442-006-0649-z PubMedCrossRefGoogle Scholar
  178. Somasundaram S, Bonkowski M, Iijima M (2008) Functional role of mucilage-border cells: a complex facilitating protozoan effects on plant growth. Plant Prod Sci 11:344–351. doi: 10.1626/pps.11.344 CrossRefGoogle Scholar
  179. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. doi: 10.1111/j.1574-6976.2007.00072.x PubMedCrossRefGoogle Scholar
  180. Stanton NL (1988) The underground in grasslands. Annu Rev Ecol Syst 19:573–589. doi: 10.1146/ CrossRefGoogle Scholar
  181. Steinaker DF, Wilson SD (2008) Scale and density dependent relationships among roots, mycorrhizal fungi and collembola in grassland and forest. Oikos 117:703–710CrossRefGoogle Scholar
  182. Stephan A, Meyer A, Schmid B (2000) Plant diversity positively affects soil bacterial diversity in experimental grassland ecosystems. J Ecol 88:988–998. doi: 10.1046/j.1365-2745.2000.00510.x CrossRefGoogle Scholar
  183. Stephens P, Davoren C (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 29:511–516. doi: 10.1016/S0038-0717(96)00108-3 CrossRefGoogle Scholar
  184. Sundin P, Valeur A, Olsson S, Odham G (1990) Interactions between bacteria-feeding nematodes and bacteria in the rape rhizosphere: effects on root exudation and distribution of bacteria. FEMS Microbiol Ecol 73:13–22CrossRefGoogle Scholar
  185. Tapilskaja N (1967) Amoeba albida Nägler und ihre Beziehungen zu dem Pilz Verticillium dahliae Kleb, dem Erreger der Welkekrankheit von Baumwollpflanzen. Pedobiologia (Jena) 7:156–165Google Scholar
  186. Thimm T, Larink O (1995) Grazing preferences of some collembola for endomycorrhizal fungi. Biol Fertil Soils 19:266–268. doi: 10.1007/BF00336171 CrossRefGoogle Scholar
  187. Tiunov A, Scheu S (2005) Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 142:636–642. doi: 10.1007/s00442-004-1758-1 PubMedCrossRefGoogle Scholar
  188. Tordoff GM, Boddy L, Jones TH (2006) Grazing by Folsomia candida (Collembola) differentially affects mycelial morphology of the cord-forming basidiomycetes Hypholoma fasciculare, Phanerochaete uelutina and Resinicium bicolor. Mycol Res 110:335–345. doi: 10.1016/j.mycres.2005.11.012 PubMedCrossRefGoogle Scholar
  189. Tordoff GM, Boddy L, Jones TH (2008) Species-specific impacts of collembola grazing on fungal foraging ecology. Soil Biol Biochem 40:434–442. doi: 10.1016/j.soilbio.2007.09.006 CrossRefGoogle Scholar
  190. 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 28:203–215. doi: 10.1016/j.apsoil.2004.08.004 CrossRefGoogle Scholar
  191. Treonis AM, Cook R, Dawson L, Grayston SJ, Mizen T (2007) Effects of a plant parasitic nematode (Heterodera trifolii) on clover roots and soil microbial communities. Biol Fertil Soils 43:541–548. doi: 10.1007/s00374-006-0133-2 CrossRefGoogle Scholar
  192. Troelstra S, Wagenaar R, Smant W, Paters B (2001) Interpretation of bioassays in the study of interactions between soil organisms and plants: involvement of nutrient factors. New Phytol 150:697–706. doi: 10.1046/j.1469-8137.2001.00133.x CrossRefGoogle Scholar
  193. Tscharntke T, Hawkins B (2002) Multitrophic level interactions. Princeton University Press, New JerseyGoogle Scholar
  194. van Dam NM, Harvey JA, Wäckers FL, Bezemer TM, Van Der Putten WH, Vet LEM (2003) Interactions between aboveground and belowground induced responses against phytophages. Basic Appl Ecol 4:63–77CrossRefGoogle Scholar
  195. van Ruijven J, De Deyn G, Raaijmakers CE, Berendse F, van der Putten W (2005) Interactions between spatially separated herbivores indirectly alter plant diversity. Ecol Lett 8:30–37. doi: 10.1111/j.1461-0248.2004.00688.x CrossRefGoogle Scholar
  196. van Tol R, van der Sommen A, Boff M, van Bezooijen J, Sabelis M, Smits P (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4:292–294. doi: 10.1046/j.1461-0248.2001.00227.x CrossRefGoogle Scholar
  197. Venette R, Ferris H (1998) Influence of bacterial type and density on population growth of bacterial-feeding nematodes. Soil Biol Biochem 30:949–960CrossRefGoogle Scholar
  198. Venette R, Mostafa F, Ferris H (1997) Trophic interactions between bacterial-feeding nematodes in plant rhizospheres and the nematophagous fungus Hirsutella rhossiliensis to suppress Heterodera schachtii. Plant Soil 191:213–223CrossRefGoogle Scholar
  199. Vercauteren I, Engler JD, De Groodt R, Gheysen G (2002) An Arabidopsis thaliana pectin acetylesterase gene is upregulated in nematode feeding sites induced by root-knot and cyst nematodes. Mol Plant Microbe Interact 15:404–407. doi: 10.1094/MPMI.2002.15.4.404 PubMedCrossRefGoogle Scholar
  200. Veronico P, Jones J, Di Vito M, De Giorgi C (2001) Horizontal transfer of a bacterial gene involved in polyglutamate biosynthesis to the plant-parasitic nematode Meloidogyne artiellia. FEBS Lett 508:470–474. doi: 10.1016/S0014-5793(01)03132-5 PubMedCrossRefGoogle Scholar
  201. Vestergård M, Bjørnlund L, Henry F, Ronn R (2007) Decreasing prevalence of rhizosphere IAA producing and seedling root growth promoting bacteria with barley development irrespective of protozoan grazing regime. Plant Soil 295:115–125. doi: 10.1007/s11104-007-9267-8 CrossRefGoogle Scholar
  202. Wardle D (2002) Communities and ecosystems: Linking the aboveground and belowground components. Princeton University Press, New JerseyGoogle Scholar
  203. 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
  204. Weekers PHH, Bodelier PLE, Wijen JPH, Vogels GD (1993) Effects of grazing by the free-living soil amobae Acanthamoeba castellanii, Acanthamoeba polyphaga, and Hartmannella vermiformis on various bacteria. Appl Environ Microbiol 59:2317–2319PubMedGoogle Scholar
  205. Weisse T (2002) The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Antonie Leeuwenhoek 81:327–341PubMedCrossRefGoogle Scholar
  206. Weitere M, Bergfeld T, Rice SA, Matz G, Kjelleberg S (2005) Grazing resistance of Pseudomonas aeruginosa biofilms depends on type of protective mechanism, developmental stage and protozoan feeding mode. Environ Microbiol 7:1593–1601. doi: 10.1111/j.1462-2920.2005.00851.x PubMedCrossRefGoogle Scholar
  207. Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–5854. doi: 10.1128/AEM.67.12.5849-5854.2001 PubMedCrossRefGoogle Scholar
  208. Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol 23:596–599. doi: 10.1016/j.tree.2008.07.006 PubMedCrossRefGoogle Scholar
  209. Williamson VM, Gleason CA (2003) Plant–nematode interactions. Curr Opin Plant Biol 6:327–333. doi: 10.1016/S1369-5266(03)00059-1 PubMedCrossRefGoogle Scholar
  210. Wood J, Tordoff GM, Jones TH, Boddy L (2006) Reorganization of mycelial networks of Phanerochaete velutina in response to new woody resources and collembola (Folsomia candida) grazing. Mycol Res 110:985–993. doi: 10.1016/j.mycres.2006.05.013 PubMedCrossRefGoogle Scholar
  211. Wurst S, Jones H (2003) Indirect effects of earthworms (Aporrectodea caliginosa) on an above-ground tritrophic interaction. Pedobiologia (Jena) 47:91–97. doi: 10.1078/0031-4056-00173 CrossRefGoogle Scholar
  212. 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
  213. Wurst S, Dugassa-Gobena D, Langel R, Bonkowski M, Scheu S (2004) Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176CrossRefGoogle Scholar
  214. Wyss U (2002) Feeding behaviour of plant parasitic nematodes. In: Lee DL (ed) The biology of nematodes. Taylor & Francis, London, pp 462–513Google Scholar
  215. Yeates GW, Saggar S, Denton CS, 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 44:81–90Google Scholar
  216. Yeates G, Bardgett R, Mercer C, Saggar S, Feltham C (1999a) Increase in 14C-carbon translocation to the soil microbial biomass when five species of pant parasitic nematodes infect roots of white clover. Nematology 1:295–300. doi: 10.1163/156854199508298 CrossRefGoogle Scholar
  217. Yeates GW, Saggar S, Hedley CB, Mercer CF (1999b) Increase in 14C-carbon translocation to the soil microbial biomass when five species of plant-parasitic nematodes infect roots of white clover. Nematology 1:295–300. doi: 10.1163/156854199508298 CrossRefGoogle Scholar
  218. Young IM, Griffiths BG, Robertson WM (1996) Continuous foraging by bacterial-feeding nematodes. Nematologica 42:378–382Google Scholar
  219. Young KD (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70:660–703. doi: 10.1128/MMBR.00001-06 PubMedCrossRefGoogle Scholar
  220. Zandonadi D, Canellas L, Façanha A (2007) Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H + pumps activation. Planta 225:1583–1595. doi: 10.1007/s00425-006-0454-2 PubMedCrossRefGoogle Scholar
  221. Zwart KB, Kuikman PJ, Van Veen JA (1994) Rhizosphere protozoa: Their significance in nutrient dynamics. In: Darbyshire J (ed) Soil protozoa. CAB International, Wallingford, pp 93–121Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Michael Bonkowski
    • 1
    Email author
  • Cécile Villenave
    • 2
  • Bryan Griffiths
    • 3
  1. 1.Department of Terrestrial EcologyUniversity of Cologne, Zoological InstituteCologneGermany
  2. 2.Research Institute for DevelopmentIRD-SeqBio/SupAgroMontpellier cedex 1France
  3. 3.Teagasc, Environment Research CentreJohnstown Castle, Wexford, Co.WexfordIreland

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