Aboveground–belowground interactions as a source of complementarity effects in biodiversity experiments
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.
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.
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.
KeywordsBiodiversity–ecosystem functioning Decomposers Plant diversity–productivity relationship Soil feedback Soil mutualists Soil pathogens
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).
- Bardgett RD (2005) The biology of soil. A community and ecosystem approach. Oxford University Press, OxfordGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Hutchinson GE (1978) An introduction to population ecology. Yale University Press, New HavenGoogle Scholar
- 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
- 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
- Loreau M, Naeem S, Inchausti P (2002) Biodiversity and ecosystem functioning—Synthesis and perspectives. Oxford University Press Inc., New YorkGoogle Scholar
- 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
- 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
- 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
- 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
- Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
- 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
- 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
- Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University PressGoogle Scholar
- 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
- Weisser WW, Siemann E (2004) Insects and ecosysten function.—Ecological studies 173. Springer Verlag, HeidelbergGoogle Scholar
- 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