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.
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References
Allan E, Van Ruijven J, Crawley MJ (2010) Foliar fungal pathogens and grassland biodiversity. Ecology 91:2572–2582
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 91:3252–3260
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 97:901–912
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 46:35–42
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 9:1146–1156
Bardgett RD (2005) The biology of soil. A community and ecosystem approach. Oxford University Press, Oxford
Bardgett RD, Cook R (1998) Functional aspects of soil animal diversity in agricultural grasslands. Appl Soil Ecol 10:263–276
Bardgett RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31:317–321
Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268
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 York
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641
Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814
Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160
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 45:1266–1273
Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417
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 25:468–478
Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624
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 6:231–238
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 91:3027–3036
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
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 298:615–618
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 8:1165–1174
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 104:18123–18128
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 98:572–592
Carson WP, Root RB (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia 121:260–272
Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187
Collins SL, Knapp AK, Briggs JM, Blair JM, Steinauer EM (1998) Modulation of diversity by grazing and mowing in native tallgrass prairie. Science 280:745–747
Cragg RG, Bardgett RD (2001) How changes in soil fauna diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081
De Deyn GB, van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633
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 422:711–713
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 188:1055–1064
Dean JM, Mescher MC, De Moraes CM (2009) Plant-rhizobia mutualism influences aphid abundance on soybean. Plant Soil 323:187–196
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 72:313–327
Dimitrakopoulos PG, Schmid B (2004) Biodiversity effects increase linearly with biotope space. Ecol Lett 7:574–583
Dromph KM, Cook R, Ostle NJ, Bardgett RD (2006) Root parasite induced nitrogen transfer between plants is density dependent. Soil Biol Biochem 38:2495–2498
Eisenhauer N (2010) The action of an animal ecosystem engineer: Identification of the main mechanisms of earthworm impacts on soil microarthropods. Pedobiologia 53:343–352
Eisenhauer N, Scheu S (2008a) Earthworms as the drivers of the competition between grasses and legumes. Soil Biol Biochem 40:2650–2659
Eisenhauer N, Scheu S (2008b) Invasibility of experimental grassland communities: the role of earthworms, plant functional group identity and seed size. Oikos 117:1026–1036
Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2008) Animal ecosystem engineers modulate the diversity-invasibility relationship. PLoS ONE 3:e3489
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 41:2430–2443
Eisenhauer N, Milcu A, Nitschke N, Sabais ACW, Scherber C, Scheu S (2009b) Earthworm and belowground competition effects on plant productivity. Oecologia 161:291–301
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 41:561–567
Eisenhauer N, Hörsch V, Moeser J, Scheu S (2010a) Synergistic effects of microbial and animal decomposers on plant and herbivore performance. Basic Appl Ecol 11:23–34
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 91:485–496
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:e16055
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:e24087
Endlweber K, Scheu S (2007) Interactions between myccorhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43:741–749
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 274:871–876
Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity–productivity relationship in an N-limited grassland. Ecology 90:408–418
Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on ecosystem function. Ecol Lett 8:846–856
Gamfeldt L, Hillebrand H, Jonsson PR (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89:1223–1231
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246
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 24:101–111
Gehring C, Bennett A (2009) Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environm Entomol 38:93–102
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 107–122
Grubb P (1977) The maintenance of species richness in plant communities: the importance of regeneration niche. Biol Rev 52:107–145
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 12:1029–1039
Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:239–244
Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999
Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195
Hättenschwiler S, Gasser P (2005) Soil animals alter plant litter diversity effects on decomposition. Proc Natl Acad Sci USA 102:1519–1524
Hättenschwiler S, Vitousek PM (2000) The role of polyphenolsin terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–242
Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Ann Rev Ecol Evol Syst 36:191–218
Haystead A, Malajczuk N, Grove TS (1988) Underground transfer of nitrogen between pasture plant infected with arbuscular myccorrhizal fungi. New Phytol 108:417–423
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–191
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 103:45–58
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 306:1019–1020
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 107:13754–13759
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 13:394–407
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 107:87–94
Hooper DU, Dukes JS (2004) Overyielding among plant functional groups in a long-term experiment. Ecol Lett 7:95–105
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 50:1049–1061
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 75:3–35
Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 108:449–460
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 289:1255a
Hutchinson GE (1978) An introduction to population ecology. Yale University Press, New Haven
Isbell F, Polley HW, Wilsey BJ (2009a) Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol Lett 12:443–451
Isbell F, Polley HW, Wilsey BJ (2009b) Species interaction mechanisms maintain grassland plant species diversity. Ecology 90:1821–1830
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
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957
Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545
Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255
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 126:317–327
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
Kempel A, Brandl R, Schädler M (2009) Symbiotic soil microorganisms as players in aboveground plant-herbivore interactions – the role of rhizobia. Oikos 118:634–640
Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300
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 3:106–113
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Klironomos JN, McCune J, Hart M, Neville J (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141
Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235
Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedback: a meta-analytical review. Ecol Lett 9:980–992
Laakso J, Setälä H (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87:57–64
Langenheder S, Bulling MT, Solan M, Prosser JI (2010) Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLoS ONE 5:e10834
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
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 137:22–31
Lohmann M, Scheu S, Müller C (2008) Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia 160:289–298
Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci USA 95:5632–5636
Loreau M (2004) Does functional redundancy exist? Oikos 104:606–611
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
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 294:804–808
Loreau M, Naeem S, Inchausti P (2002) Biodiversity and ecosystem functioning—Synthesis and perspectives. Oxford University Press Inc., New York
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10
Maherali H, Klironomos JN (2007) Influence of phylogeny and fungal community assembly and ecosystem functioning. Science 316:1746–1748
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 43:276–287
Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41
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 90:3290–3302
Marquard E, Weigelt A, Roscher C, Gubsch M, Lipowsky A, Schmid B (2009b) Positive biodiversity–productivity relationship due to increased plant density. J Ecol 97:696–704
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 255:105–119
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 415:68–71
McNaughton SJ, Banyikwa FF, McNaughton MM (1997) Promotion of the cycling of diet-enhancing nutrients by African grazers. Science 278:1798–1800
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 107:14251–14256
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 92:333–343
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 169–180
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 112:513–524
Milcu A, Schumacher J, Scheu S (2006b) Earthworms (Lumbricus terrestris) affect plant seedling recruitment and microhabitat heterogeneity. Funct Ecol 20:261–268
Milcu A, Partsch S, Scherber C, Weisser WW, Scheu S (2008) Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 89:1872–1882
Milcu A, Thebault E, Scheu S, Eisenhauer N (2010) Plant diversity enhances the reliability of belowground processes. Soil Biol Biochem 42:2102–2110
Moore JC, McKann K, Setälä H, de Ruiter PC (2003) Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857
Mulder CPH, Koricheva J, Huss-Danell K, Högberg P, Joshi J (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecol Lett 2:237–246
Mulder CPH, Jumpponen A, Högberg P, Huss-Danell K (2002) How plant diversity and legumes affect nitrogen dynamics in experimental grassland communities. Oecologia 133:412–421
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 347:249–262
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 62:105–116
Partsch S, Milcu A, Scheu S (2006) Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 87:2548–2558
Petermann JS, Fergus A, Turnbull LA, Schmid B (2008) Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:2399–2406
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 6:248–256
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 410:809–812
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124
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 8:419–429
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 96:477–488
Sabais ACW, Scheu S, Eisenhauer N (2011) Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecol 37:195–202
Schädler M, Jung G, Brandl R, Auge H (2004) Secondary seccession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252
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 94:922–931
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 468:553–556
Scherber C, Specht J, Köhler G, Mitschunas N, Weisser WW (2010b) Functional identity versus species richness: Herbivory resistance in plant communities. Oecologia 163:707–717
Scheu S (2001) Plants and generalist predators as links between the below-ground and above-ground system. Basic Appl Ecol 2:3–13
Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:1–11
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
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 92:296–303
Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London
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 147:357–366
Spehn EM, Joshi J, Schmid B, Alphei J, Körner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230
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 98:205–218
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 105:18842–18847
Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998
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 151:190–205
Thebault E, Loreau M (2003) Food-web constraints on biodiversity–ecosystem functioning relationships. Proc Natl Acad Sci USA 100:14949–14954
Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861
Tiunov AV, Scheu S (1999) Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris L. (Lumbricidae). Soil Biol Biochem 31:2039–2048
Tiunov AV, Scheu S (2005) Facilitative interactions rather than resource partitioning drive diversity-functioning relationships in laboratory fungal communities. Ecol Lett 8:618–625
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 396:69–72
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 11:296–310
Van der Putten WH, Van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56
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 16:547–554
Van Ruijven J, Berendse F (2005) Diversity-productivity relationships: Initial effects, long-term patters, and underlying mechanisms. Proc Natl Acad Sci USA 102:695–700
Van Ruijven J, Berendse F (2009) Long-term persistence of a positive plant diversity–productivity relationship in the absence of legumes. Oikos 118:101–106
Vandermeer J (1981) The interference production principle: an ecological theory for agriculture. BioScience 31:361–364
Vanette RL, Hunter MD (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76
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 90:90–99
Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562
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 53:41–48
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 163:1033–1042
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 90:1389–1399
Vos VCA, van Ruijven J, Berg MP, Peeters THM, Berendse F (2011) Macro-detritivore identity drives leaf litter diversity effects. Oikos 120:1092–1098
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
Wagg C, Stadler M, Schmid B, van der Heijden MAG (2011b) Mycorrhizal fungal idenity and diversity relaxes plant-plant competition. Ecology 92:1303–1313
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
Wardle DA (1999) Is ‘sampling effect’ a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87:403–407
Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press
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 155–168
Wardle DA, Nilsson M-C, Gallet C, Zackrisson O (1998) An ecosystem-level perspective of allelopathy. Biol Rev 73:305–319
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633
Weisser WW, Siemann E (2004) Insects and ecosysten function.—Ecological studies 173. Springer Verlag, Heidelberg
Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348
Wolters V (2001) Biodiversity of soil animals and its function. Eur J Soil Biol 37:221–227
Worm B, Duffy JE (2003) Biodiversity, productivity and stability in real food webs. Trends Ecol Evol 18:628–632
Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56:203–209
Wright JP, Gurney SC, Jones CG (2004) Patch dynamics in a landscape modified by ecosystem engineers. Oikos 105:336–348
Wurst S (2010) Effects of earthworms on above- and belowground herbivores. Appl Soil Ecol 45:123–130
Wurst S, Jones TH (2003) Indirect effects of earthworms (Aporrectodea caliginosa) on an above-ground tritrophic interaction. Pedobiologia 47:91–97
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 163:169–176
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 117:711–718
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84:2042–2050
Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD (2010) Sustaining multiple ecosystem functions in grassland requires higher biodiversity. Proc Natl Acad Sci USA 107:1443–1446
Acknowledgements
I thank Wolfgang W. Weisser for inviting the present review paper to the ESA meeting in Austin, Texas (2011) and for helpful comments on an earlier version of this paper. Comments by Stefan Scheu, Christiane Roscher, Kevin Mueller, Forest Isbell and Cindy Buschena helped to improve this paper. I moreover thank Lois Chaplin, Alexandre Jousset, Stephan König and Claudio Valverde for providing pictures, and Richard Bardgett for help with the illustration of figures. I thank two anonymous reviewers for constructive comments that improved the paper considerably. Further, I gratefully acknowledge funding by the Deutsche Forschungsgemeinschaft (German Research Foundation; Ei 862/1-1).
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Eisenhauer, N. Aboveground–belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351, 1–22 (2012). https://doi.org/10.1007/s11104-011-1027-0
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DOI: https://doi.org/10.1007/s11104-011-1027-0