Plant and Soil

, Volume 351, Issue 1–2, pp 1–22 | Cite as

Aboveground–belowground interactions as a source of complementarity effects in biodiversity experiments

Marschner Review

Abstract

Background

The positive relationship between biodiversity and ecosystem functioning (BEF) is due mainly to complementarity between species. Most BEF studies primarily focused on plant interactions; however, plants are embedded in a dense network of multitrophic interactions above and below the ground, which are likely to play a crucial role in BEF relationships.

Scope

In the present review I point out the relevance of aboveground–belowground interactions as a source of complementarity effects in grassland biodiversity experiments. A review of the current knowledge on the role of decomposers, arbuscular mycorrhizal fungi, rhizobia, plant growth promoting rhizobacteria, invertebrate ecosystem engineers, herbivores, pathogens and predators in biodiversity experiments, indicates that soil biota can drive both positive and negative complementarity between plant species via a multitude of mechanisms.

Conclusions

I pose four main processes by which aboveground–belowground interactions determine positive complementarity effects: enlarging biotope space, mediating legume effects, increasing plant community resistance, and maintaining plant diversity. By contrast, soil biota may also reinforce negative complementarity effects by competing with plants for nutrients or by exerting herbivore or pathogen pressure, thereby reducing community productivity. Thus, considering aboveground–belowground interactions as well as interactions between antagonistic and mutualistic consumers may improve the mechanistic understanding of complementarity effects in plant diversity–ecosystem functioning experiments and should inspire future research.

Keywords

Biodiversity–ecosystem functioning Decomposers Plant diversity–productivity relationship Soil feedback Soil mutualists Soil pathogens 

References

  1. Allan E, Van Ruijven J, Crawley MJ (2010) Foliar fungal pathogens and grassland biodiversity. Ecology 91:2572–2582PubMedCrossRefGoogle Scholar
  2. Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to niche plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260PubMedCrossRefGoogle Scholar
  3. Ayres E, Steltzer H, Berg S, Wall DH (2009) Soil biota accelerate decomposition in high-elevation forests by specializing in the breakdown of litter produced by the plant above them. J Ecol 97:901–912CrossRefGoogle Scholar
  4. Bakker MG, Glover JD, Mai JG, Kinkel LL (2010) Plant community effects on the diversity and pathogen suppressive activity of soil streptomycetes. Appl Soil Ecol 46:35–42CrossRefGoogle Scholar
  5. Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156PubMedCrossRefGoogle Scholar
  6. Bardgett RD (2005) The biology of soil. A community and ecosystem approach. Oxford University Press, OxfordGoogle Scholar
  7. Bardgett RD, Cook R (1998) Functional aspects of soil animal diversity in agricultural grasslands. Appl Soil Ecol 10:263–276CrossRefGoogle Scholar
  8. Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321CrossRefGoogle Scholar
  9. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268CrossRefGoogle Scholar
  10. Bardgett RD, Wardle DA (2010) Aboveground–belowground linkages, biotic interactions, ecosystem processes, and global change. Oxford series in ecology and evolution. Oxford University Press, New YorkGoogle Scholar
  11. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641PubMedCrossRefGoogle Scholar
  12. Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814PubMedCrossRefGoogle Scholar
  13. Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160PubMedCrossRefGoogle Scholar
  14. Bell JR, Traugott M, Sunderland KD, Skirvin DJ, Mead A, Kravar-Garde L, Reynolds K, Fenlon JS, Symondson WOC (2008) Beneficial links for the control of aphids: the effects of compost applications on predators and prey. J Appl Ecol 45:1266–1273CrossRefGoogle Scholar
  15. Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417PubMedCrossRefGoogle Scholar
  16. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478PubMedCrossRefGoogle Scholar
  17. Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624PubMedCrossRefGoogle Scholar
  18. Bezemer TM, Graca O, Rousseau R, van der Putten WH (2004) Above- and belowground trophic interactions on creeping thistle (Cirsium arvense) in high- and low-diversity plant communities: potential for biotic resistance? Plant Biol 6:231–238PubMedCrossRefGoogle Scholar
  19. Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, van Hal R, Harvey JA, Hedlund K, Maraun M, Mikola J, Mladenov AG, Robin C, de Ruiter PC, Scheu S, Setälä H, Smilauer P, van der Putten WH (2010) Divergent composition but similar function of soil food webs of individual plants: plant species and community effects. Ecology 91:3027–3036PubMedCrossRefGoogle Scholar
  20. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631CrossRefGoogle Scholar
  21. Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setälä H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil fauna community composition on model grassland ecosystems. Science 298:615–618PubMedCrossRefGoogle Scholar
  22. Bruno JF, Boyer KE, Lee SC, Kertesz JS (2005) Effects of macroalgal species identity and richness on primary production in benthic marine communities. Ecol Lett 8:1165–1174PubMedCrossRefGoogle Scholar
  23. Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci USA 104:18123–18128PubMedCrossRefGoogle Scholar
  24. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592PubMedCrossRefGoogle Scholar
  25. Carson WP, Root RB (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia 121:260–272CrossRefGoogle Scholar
  26. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187CrossRefGoogle Scholar
  27. Collins SL, Knapp AK, Briggs JM, Blair JM, Steinauer EM (1998) Modulation of diversity by grazing and mowing in native tallgrass prairie. Science 280:745–747PubMedCrossRefGoogle Scholar
  28. Cragg RG, Bardgett RD (2001) How changes in soil fauna diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081CrossRefGoogle Scholar
  29. De Deyn GB, van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633PubMedCrossRefGoogle Scholar
  30. De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, de Ruiter PC, Verhoef HA, Bezemer TM, van der Putten WH (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713PubMedCrossRefGoogle Scholar
  31. De Graaff M-A, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064PubMedCrossRefGoogle Scholar
  32. Dean JM, Mescher MC, De Moraes CM (2009) Plant-rhizobia mutualism influences aphid abundance on soybean. Plant Soil 323:187–196CrossRefGoogle Scholar
  33. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327PubMedCrossRefGoogle Scholar
  34. Dimitrakopoulos PG, Schmid B (2004) Biodiversity effects increase linearly with biotope space. Ecol Lett 7:574–583CrossRefGoogle Scholar
  35. Dromph KM, Cook R, Ostle NJ, Bardgett RD (2006) Root parasite induced nitrogen transfer between plants is density dependent. Soil Biol Biochem 38:2495–2498CrossRefGoogle Scholar
  36. Eisenhauer N (2010) The action of an animal ecosystem engineer: Identification of the main mechanisms of earthworm impacts on soil microarthropods. Pedobiologia 53:343–352CrossRefGoogle Scholar
  37. Eisenhauer N, Scheu S (2008a) Earthworms as the drivers of the competition between grasses and legumes. Soil Biol Biochem 40:2650–2659CrossRefGoogle Scholar
  38. Eisenhauer N, Scheu S (2008b) Invasibility of experimental grassland communities: the role of earthworms, plant functional group identity and seed size. Oikos 117:1026–1036CrossRefGoogle Scholar
  39. Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2008) Animal ecosystem engineers modulate the diversity-invasibility relationship. PLoS ONE 3:e3489PubMedCrossRefGoogle Scholar
  40. Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Weigelt A, Engels C, Scheu S (2009a) Plant community impacts on the structure of earthworm communities depend on season and change with time. Soil Biol Biochem 41:2430–2443CrossRefGoogle Scholar
  41. Eisenhauer N, Milcu A, Nitschke N, Sabais ACW, Scherber C, Scheu S (2009b) Earthworm and belowground competition effects on plant productivity. Oecologia 161:291–301PubMedCrossRefGoogle Scholar
  42. Eisenhauer N, König S, Sabais ACW, Renker C, Buscot F, Scheu S (2009c) Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biol Biochem 41:561–567CrossRefGoogle Scholar
  43. Eisenhauer N, Hörsch V, Moeser J, Scheu S (2010a) Synergistic effects of microbial and animal decomposers on plant and herbivore performance. Basic Appl Ecol 11:23–34CrossRefGoogle Scholar
  44. Eisenhauer N, Beßler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010b) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496PubMedCrossRefGoogle Scholar
  45. Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Brenner J, Engels C, Klarner B, Maraun M, Partsch S, Roscher C, Schonert F, Temperton VM, Thomisch K, Weigelt A, Weisser WW, Scheu S (2011a) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS ONE 6:e16055PubMedCrossRefGoogle Scholar
  46. Eisenhauer N, Migunova VD, Ackermann M, Ruess L, Scheu S (2011b) Changes in plant species richness induce functional shifts in soil nematode communities in experimental grassland. PLoS ONE 6:e24087PubMedCrossRefGoogle Scholar
  47. Endlweber K, Scheu S (2007) Interactions between myccorhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43:741–749CrossRefGoogle Scholar
  48. Fargione J, Tilman D, Dybinski R, HilleRisLambers J, Clark C, Harpole WS, Knops JMH, Reich PB, Loreau M (2007) From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc Roy Soc B 274:871–876CrossRefGoogle Scholar
  49. Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity–productivity relationship in an N-limited grassland. Ecology 90:408–418PubMedCrossRefGoogle Scholar
  50. Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on ecosystem function. Ecol Lett 8:846–856CrossRefGoogle Scholar
  51. Gamfeldt L, Hillebrand H, Jonsson PR (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89:1223–1231PubMedCrossRefGoogle Scholar
  52. Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  53. Gastine A, Scherer-Lorenzen M, Leadley PW (2003) No consistent effects of plant diversity on root biomass, soil biota and soil abiotic conditions in temperate grassland communities. Appl Soil Ecol 24:101–111CrossRefGoogle Scholar
  54. Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environm Entomol 38:93–102CrossRefGoogle Scholar
  55. Grant JD (1983) The activities of earthworms and the fates of seeds. In: Satchell JE (ed) Earthworm ecology: From Darwin to vermiculture. Chapman & Hall, London, pp 107–122Google Scholar
  56. Grubb P (1977) The maintenance of species richness in plant communities: the importance of regeneration niche. Biol Rev 52:107–145CrossRefGoogle Scholar
  57. Haddad NM, Cruitsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039PubMedCrossRefGoogle Scholar
  58. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:239–244CrossRefGoogle Scholar
  59. Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999PubMedCrossRefGoogle Scholar
  60. Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195CrossRefGoogle Scholar
  61. Hättenschwiler S, Gasser P (2005) Soil animals alter plant litter diversity effects on decomposition. Proc Natl Acad Sci USA 102:1519–1524PubMedCrossRefGoogle Scholar
  62. Hättenschwiler S, Vitousek PM (2000) The role of polyphenolsin terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–242PubMedCrossRefGoogle Scholar
  63. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Ann Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  64. Haystead A, Malajczuk N, Grove TS (1988) Underground transfer of nitrogen between pasture plant infected with arbuscular myccorrhizal fungi. New Phytol 108:417–423CrossRefGoogle Scholar
  65. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–191PubMedCrossRefGoogle Scholar
  66. Hedlund K, Regina IS, van der Putten WH, Leps J, Diaz T, Korthals GW, Lavorel S, Brown VK, Gormsen D, Mortimer SR, Barrueco CR, Roy J, Smilauer P, Smilauerova M, van Dijk C (2003) Plant species diversity, plant biomass and responses of the soil community on abandoned land across Europe: Idiosyncracy or above-belowground time lags. Oikos 103:45–58CrossRefGoogle Scholar
  67. Heemsbergen DA, Berg MP, Loreau M, van Hal JR, Faber JH, Verhoef HA (2004) Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306:1019–1020PubMedCrossRefGoogle Scholar
  68. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759PubMedCrossRefGoogle Scholar
  69. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407PubMedCrossRefGoogle Scholar
  70. Holland JN, Cheng W, Crossley DA Jr (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C-fluxes using carbon-14. Oecologia 107:87–94CrossRefGoogle Scholar
  71. Hooper DU, Dukes JS (2004) Overyielding among plant functional groups in a long-term experiment. Ecol Lett 7:95–105CrossRefGoogle Scholar
  72. Hooper DU, Bignell DE, Brown VK, Brussard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, van der Putten WH, de Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Biocience 50:1049–1061CrossRefGoogle Scholar
  73. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstadt AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  74. Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 108:449–460CrossRefGoogle Scholar
  75. Huston MA, Aarsen LW, Austin MP, Cade BS, Fridley JD, Garnier E, Grime JP, Hodgson J, Lauenroth WK, Thompson K, Vandermeer JH, Wardle DA (2000) No consistent effect of plant diversity on productivity. Nature 289:1255aGoogle Scholar
  76. Hutchinson GE (1978) An introduction to population ecology. Yale University Press, New HavenGoogle Scholar
  77. Isbell F, Polley HW, Wilsey BJ (2009a) Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol Lett 12:443–451PubMedCrossRefGoogle Scholar
  78. Isbell F, Polley HW, Wilsey BJ (2009b) Species interaction mechanisms maintain grassland plant species diversity. Ecology 90:1821–1830PubMedCrossRefGoogle Scholar
  79. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature. doi:10.1038/nature10282
  80. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  81. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  82. Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545PubMedCrossRefGoogle Scholar
  83. Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255PubMedCrossRefGoogle Scholar
  84. Kardol P, Bezemer TM, van der Wal A, van der Putten WH (2005) Successional trajectories of nematode and plant communities in a chronosequence of ex-arable land. Biological Conservation 126:317–327CrossRefGoogle Scholar
  85. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143PubMedCrossRefGoogle Scholar
  86. Kempel A, Brandl R, Schädler M (2009) Symbiotic soil microorganisms as players in aboveground plant-herbivore interactions – the role of rhizobia. Oikos 118:634–640Google Scholar
  87. Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300CrossRefGoogle Scholar
  88. Kiers ET, Lovelock CE, Krueger EL, Herre EA (2000) Differential effects of tropical arbuscular mycorrhizal fungal inocula on root colonization and tree seedling growth: implications for tropical forest diversity. Ecol Lett 3:106–113CrossRefGoogle Scholar
  89. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  90. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  91. Klironomos JN, McCune J, Hart M, Neville J (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141CrossRefGoogle Scholar
  92. Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235CrossRefGoogle Scholar
  93. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097PubMedCrossRefGoogle Scholar
  94. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedback: a meta-analytical review. Ecol Lett 9:980–992CrossRefGoogle Scholar
  95. Laakso J, Setälä H (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87:57–64CrossRefGoogle Scholar
  96. Langenheder S, Bulling MT, Solan M, Prosser JI (2010) Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLoS ONE 5:e10834PubMedCrossRefGoogle Scholar
  97. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379PubMedCrossRefGoogle Scholar
  98. Lee TD, Reich PB, Scheu S (2003) Legume presence increases photosynthesis and N concentrations of co-occurring non-fixers but does not modulate their responsiveness to carbon dioxide enrichment. Oecologia 137:22–31PubMedCrossRefGoogle Scholar
  99. Lohmann M, Scheu S, Müller C (2008) Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia 160:289–298CrossRefGoogle Scholar
  100. Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci USA 95:5632–5636PubMedCrossRefGoogle Scholar
  101. Loreau M (2004) Does functional redundancy exist? Oikos 104:606–611CrossRefGoogle Scholar
  102. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76PubMedCrossRefGoogle Scholar
  103. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808PubMedCrossRefGoogle Scholar
  104. Loreau M, Naeem S, Inchausti P (2002) Biodiversity and ecosystem functioning—Synthesis and perspectives. Oxford University Press Inc., New YorkGoogle Scholar
  105. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  106. Maherali H, Klironomos JN (2007) Influence of phylogeny and fungal community assembly and ecosystem functioning. Science 316:1746–1748PubMedCrossRefGoogle Scholar
  107. Maraun M, Alphei J, Bonkowski M, Buryn R, Migge S, Peter M, Schaefer M, Scheu S (1999) Middens of the earthworm L. terrestris (Lumbricidae): microhabitats for micro- and Mesofauna in forest soil. Pedobiologia 43:276–287Google Scholar
  108. Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41PubMedCrossRefGoogle Scholar
  109. Marquard E, Weigelt A, Temperton VM, Roscher C, Schumacher J, Buchmann N, Fischer M, Weisser WW, Schmid B (2009a) Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 90:3290–3302PubMedCrossRefGoogle Scholar
  110. Marquard E, Weigelt A, Roscher C, Gubsch M, Lipowsky A, Schmid B (2009b) Positive biodiversity–productivity relationship due to increased plant density. J Ecol 97:696–704CrossRefGoogle Scholar
  111. Mathesius U (2003) Conservation and divergence of signaling 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 255:105–119CrossRefGoogle Scholar
  112. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71PubMedCrossRefGoogle Scholar
  113. McNaughton SJ, Banyikwa FF, McNaughton MM (1997) Promotion of the cycling of diet-enhancing nutrients by African grazers. Science 278:1798–1800PubMedCrossRefGoogle Scholar
  114. Miki T, Ushido M, Fukui S, Kondoh M (2010) Functional diversity of microbial decomposers facilitates plant coexistence in a plant-microbe-soil feedback model. Proc Natl Acad Sci USA 107:14251–14256PubMedCrossRefGoogle Scholar
  115. 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 92:333–343CrossRefGoogle Scholar
  116. Mikola J, Bardgett RD, Hedlund K (2002) Biodiversity, ecosystem functioning and soil decomposer food webs. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 169–180Google Scholar
  117. Milcu A, Partsch S, Langel R, Scheu S (2006a) The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112:513–524CrossRefGoogle Scholar
  118. Milcu A, Schumacher J, Scheu S (2006b) Earthworms (Lumbricus terrestris) affect plant seedling recruitment and microhabitat heterogeneity. Funct Ecol 20:261–268CrossRefGoogle Scholar
  119. Milcu A, Partsch S, Scherber C, Weisser WW, Scheu S (2008) Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 89:1872–1882PubMedCrossRefGoogle Scholar
  120. Milcu A, Thebault E, Scheu S, Eisenhauer N (2010) Plant diversity enhances the reliability of belowground processes. Soil Biol Biochem 42:2102–2110CrossRefGoogle Scholar
  121. Moore JC, McKann K, Setälä H, de Ruiter PC (2003) Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857CrossRefGoogle Scholar
  122. Mulder CPH, Koricheva J, Huss-Danell K, Högberg P, Joshi J (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecol Lett 2:237–246CrossRefGoogle Scholar
  123. Mulder CPH, Jumpponen A, Högberg P, Huss-Danell K (2002) How plant diversity and legumes affect nitrogen dynamics in experimental grassland communities. Oecologia 133:412–421CrossRefGoogle Scholar
  124. Naeem S, Thomson LJ, Lawler SP, Lawton JH, Woodfin RM (1995) Empirical evidence that declining species-diversity alter the performance of terrestrial ecosystems. Philos Trans R Soc Lond B Biol Sci 347:249–262CrossRefGoogle Scholar
  125. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116CrossRefGoogle Scholar
  126. Partsch S, Milcu A, Scheu S (2006) Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 87:2548–2558PubMedCrossRefGoogle Scholar
  127. Petermann JS, Fergus A, Turnbull LA, Schmid B (2008) Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:2399–2406PubMedCrossRefGoogle Scholar
  128. Polley HW, Wisley BJ, Derner JD (2003) Do species evenness and plant diversity influence the magnitude of selection and complementarity effects in annual plant species mixtures? Ecol Lett 6:248–256CrossRefGoogle Scholar
  129. Reich PB, Knops J, Tilman D, Craine J, Ellsworth D, Tjoelker M, Lee T, Wedink D, Naeem S, Bahauddin D, Hendrey G, Jose S, Wrage K, Goth J, Bengston W (2001) Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–812PubMedCrossRefGoogle Scholar
  130. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124CrossRefGoogle Scholar
  131. Roscher C, Temperton VM, Scherer-Lorenzen M, Schmitz M, Schumacher J, Schmid B, Buchmann N, Weisser WW, Schulze E-D (2005) Overyielding in experimental grassland communities—irrespective of species pool or spatial scale. Ecol Lett 8:419–429CrossRefGoogle Scholar
  132. Roscher C, Thein S, Schmid B, Scherer-Lorenzen M (2008) Complementary nitrogen use among potentially dominant species in a biodiversity experiment varies between two years. J Ecol 96:477–488CrossRefGoogle Scholar
  133. Sabais ACW, Scheu S, Eisenhauer N (2011) Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecol 37:195–202CrossRefGoogle Scholar
  134. Schädler M, Jung G, Brandl R, Auge H (2004) Secondary seccession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252PubMedCrossRefGoogle Scholar
  135. Scherber C, Milcu A, Partsch S, Scheu S, Weisser WW (2006) The effects of plant diversity and insect herbivory on performance of individual plant species in experimental grassland. J Ecol 94:922–931CrossRefGoogle Scholar
  136. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Schulze E-D, Roscher C, Weigelt A, Allan E, Beßler H, Bonkowski M, Buchmann N, Buscot F, Clement LW, Ebeling A, Engels C, Fischer M, Halle S, Kertscher I, Klein A-M, Koller R, König S, Kowalski E, Kummer V, Kuu A, Lange M, Lauterbach D, Middelhoff C, Migunova VD, Milcu A, Müller R, Partsch S, Petermann JS, Renker C, Rottstock T, Sabais ACW, Scheu S, Schumacher J, Temperton VM, Tscharnke T (2010a) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556PubMedCrossRefGoogle Scholar
  137. Scherber C, Specht J, Köhler G, Mitschunas N, Weisser WW (2010b) Functional identity versus species richness: Herbivory resistance in plant communities. Oecologia 163:707–717PubMedCrossRefGoogle Scholar
  138. Scheu S (2001) Plants and generalist predators as links between the below-ground and above-ground system. Basic Appl Ecol 2:3–13CrossRefGoogle Scholar
  139. Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:1–11CrossRefGoogle Scholar
  140. 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 119:541–551Google Scholar
  141. Schnitzer S, Klironomos J, Hille Ris Lambers J, Kinkle L, Reich PB, Xiao K, Rillig M, Sikes B, Callaway R, Mangan S, Van Nes E, Scheffer M (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303PubMedCrossRefGoogle Scholar
  142. Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280CrossRefGoogle Scholar
  143. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  144. Smith FA, Jakobsen I, Smith SE (2000) Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol 147:357–366CrossRefGoogle Scholar
  145. Spehn EM, Joshi J, Schmid B, Alphei J, Körner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230CrossRefGoogle Scholar
  146. Spehn EM, Scherer-Lorenzen M, Schmid B, Hector A, Caldeira MC, Dimitrakopoulos PG, Finn JA, Jumpponen A, O’Donnovan G, Pereira JS, Schulze E-D, Troumbis AY, Körner C (2002) The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 98:205–218CrossRefGoogle Scholar
  147. Stachowicz JJ, Best RJ, Bracken MES, Graham MH (2008) Complementary in marine biodiversity manipulations: reconciling divergent evidence from field and mesocosm experiments. Proc Natl Acad Sci USA 105:18842–18847PubMedCrossRefGoogle Scholar
  148. Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998CrossRefGoogle Scholar
  149. Temperton VM, Mwangi PN, Scherer-Lorenzen M, Schmid B, Buchmann N (2007) Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 151:190–205PubMedCrossRefGoogle Scholar
  150. Thebault E, Loreau M (2003) Food-web constraints on biodiversity–ecosystem functioning relationships. Proc Natl Acad Sci USA 100:14949–14954PubMedCrossRefGoogle Scholar
  151. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720CrossRefGoogle Scholar
  152. Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861PubMedCrossRefGoogle Scholar
  153. Tiunov AV, Scheu S (1999) Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris L. (Lumbricidae). Soil Biol Biochem 31:2039–2048CrossRefGoogle Scholar
  154. Tiunov AV, Scheu S (2005) Facilitative interactions rather than resource partitioning drive diversity-functioning relationships in laboratory fungal communities. Ecol Lett 8:618–625CrossRefGoogle Scholar
  155. Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Myccorhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  156. Van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedCrossRefGoogle Scholar
  157. Van der Putten WH, Van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56CrossRefGoogle Scholar
  158. Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554CrossRefGoogle Scholar
  159. Van Ruijven J, Berendse F (2005) Diversity-productivity relationships: Initial effects, long-term patters, and underlying mechanisms. Proc Natl Acad Sci USA 102:695–700PubMedCrossRefGoogle Scholar
  160. Van Ruijven J, Berendse F (2009) Long-term persistence of a positive plant diversity–productivity relationship in the absence of legumes. Oikos 118:101–106CrossRefGoogle Scholar
  161. Vandermeer J (1981) The interference production principle: an ecological theory for agriculture. BioScience 31:361–364CrossRefGoogle Scholar
  162. Vanette RL, Hunter MD (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76CrossRefGoogle Scholar
  163. Viketoft M, Bengtsson J, Sohlenius B, Berg MP, Petchey O, Palmborg C, Huss-Danell K (2009) Long-term effects of plant diversity and composition on soil nematode communities in model grasslands. Ecology 90:90–99PubMedCrossRefGoogle Scholar
  164. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562PubMedCrossRefGoogle Scholar
  165. Von Berg K, Thies C, Tscharnke T, Scheu S (2009) Cereal aphid control by generalist predators in presence of belowground alternative prey: complementary predation as affected by prey density. Pedobiologia 53:41–48CrossRefGoogle Scholar
  166. Von Berg K, Thies C, Tscharnke T, Scheu S (2010) Changes in herbivore control in arable fields by detrital subsidies depend on predator species and vary in space. Oecologia 163:1033–1042CrossRefGoogle Scholar
  167. Von Felten S, Hector A, Buchmann N, Niklaus PA, Schmid B, Scherer-Lorenzen M (2009) Belowground nitrogen partitioning in experimental grassland plant communities of varying species richness. Ecology 90:1389–1399CrossRefGoogle Scholar
  168. Vos VCA, van Ruijven J, Berg MP, Peeters THM, Berendse F (2011) Macro-detritivore identity drives leaf litter diversity effects. Oikos 120:1092–1098CrossRefGoogle Scholar
  169. Wagg C, Jansa J, Schmid B, van der Heijden MGA (2011a) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett. doi:10.1111/j.1461-0248.2011.01666.x
  170. Wagg C, Stadler M, Schmid B, van der Heijden MAG (2011b) Mycorrhizal fungal idenity and diversity relaxes plant-plant competition. Ecology 92:1303–1313PubMedCrossRefGoogle Scholar
  171. Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  172. Wardle DA (1999) Is ‘sampling effect’ a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87:403–407CrossRefGoogle Scholar
  173. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University PressGoogle Scholar
  174. Wardle DA, van der Putten WH (2002) Biodiversity, ecosystem functioning and above-ground-below-ground linkages. In: Loreau S, Naeem S, Inchausti O (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 155–168Google Scholar
  175. Wardle DA, Nilsson M-C, Gallet C, Zackrisson O (1998) An ecosystem-level perspective of allelopathy. Biol Rev 73:305–319CrossRefGoogle Scholar
  176. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  177. Weisser WW, Siemann E (2004) Insects and ecosysten function.—Ecological studies 173. Springer Verlag, HeidelbergGoogle Scholar
  178. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedCrossRefGoogle Scholar
  179. Wolters V (2001) Biodiversity of soil animals and its function. Eur J Soil Biol 37:221–227CrossRefGoogle Scholar
  180. Worm B, Duffy JE (2003) Biodiversity, productivity and stability in real food webs. Trends Ecol Evol 18:628–632CrossRefGoogle Scholar
  181. Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56:203–209CrossRefGoogle Scholar
  182. Wright JP, Gurney SC, Jones CG (2004) Patch dynamics in a landscape modified by ecosystem engineers. Oikos 105:336–348CrossRefGoogle Scholar
  183. Wurst S (2010) Effects of earthworms on above- and belowground herbivores. Appl Soil Ecol 45:123–130CrossRefGoogle Scholar
  184. Wurst S, Jones TH (2003) Indirect effects of earthworms (Aporrectodea caliginosa) on an above-ground tritrophic interaction. Pedobiologia 47:91–97CrossRefGoogle Scholar
  185. Wurst S, Dugassa-Gobena D, Langel R, Bonkowski M, Scheu S (2004) Combined effects of earthworms and vascular-arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176Google Scholar
  186. Wurst S, Allema B, Duyts H, van der Putten WH (2008) Earthworms counterbalance the negative effect of microorganisms on plant diversity and enhance the tolerance of grasses to nematodes. Oikos 117:711–718CrossRefGoogle Scholar
  187. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84:2042–2050CrossRefGoogle Scholar
  188. Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD (2010) Sustaining multiple ecosystem functions in grassland requires higher biodiversity. Proc Natl Acad Sci USA 107:1443–1446PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA

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