Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 8 2009 10.5194/bg-6-1695-2009 http://www.biogeosciences.net/6/1695/2009/ http://www.biogeosciences.net/6/1695/2009/bg-6-1695-2009.html http://www.biogeosciences.net/6/1695/2009/bg-6-1695-2009.pdf 1695 1706 2009-08-21 Biodiversity for multifunctional grasslands: equal productivity in high-diversity low-input and low-diversity high-input systems A. Weigelt alexandra.weigelt@uni-jena.de W. W. Weisser N. Buchmann M. Scherer-Lorenzen Institute of Ecology, University of Jena, Dornburger Strasse 159, 07743 Jena, Germany Institute of Plant Sciences, ETH Zurich, Universitaetsstrasse 2, 8092 Zurich, Switzerland Modern grassland management seeks to provide many ecosystem services and experimental studies in resource-poor grasslands have shown a positive relationship between plant species richness and a variety of ecosystem functions. Thus, increasing species richness might help to enhance multifunctionality in managed grasslands if the relationship between species richness and ecosystem functioning is equally valid in high-input grassland systems. We tested the relative effects of low-input to high-input management intensities and low to high plant species richness. Using a combination of mowing frequencies (1, 2 or 4 cuts per season) and fertilisation levels (0, 100 and 200 kg N ha−1 a−1), we studied the productivity of 78 experimental grassland communities of increasing plant species richness (1, 2, 4, 8 or 16 species with 1 to 4 functional groups) in two successive years. Our results showed that in both years higher diversity was more effective in increasing productivity than higher management intensity: the 16-species mixtures had a surplus of 449 g m−2 y−1 in 2006 and 492 g m−2 y−1 in 2007 over the monoculture yields whereas the high-input management resulted in only 315 g m−2 y−1 higher productivity in 2006 and 440 g m−2 y−1 in 2007 than the low-input management. In addition, high-diversity low-input grassland communities had similar productivity as low-diversity high-input communities. The slopes of the biodiversity – productivity relationships significantly increased with increasing levels of management intensity in both years. We conclude that the biological mechanisms leading to enhanced biomass production in diverse grassland communities are as effective for productivity as a combination of several agricultural measures. Our results demonstrate that high-diversity low-input grassland communities provide not only a high diversity of plants and other organisms, but also ensure high forage yields, thus granting the basis for multifunctional managed grasslands. Aarssen, L. W.: High productivity in grassland ecosystems: effected by species diversity or productive species?, Oikos, 80(1), 183–184, 1997. Balmford, A., Bruner, A., Cooper, P., Costanza, R., Farber, S., Green, R. E., Jenkins, M., Jefferiss, P., Jessamy, V., Madden, J., Munro, K., Myers, N., Naeem, S., Paavola, J., Rayment, M., Rosendo, S., Roughgarden, J., Trumper, K., and Turner, R. K.: Ecology – Economic reasons for conserving wild nature, Science, 297, 950–953, 2002. Balvanera, P., Pfisterer, A. B., Buchmann, N., He, J.-S., Nakashizuka, T., Raffaelli, D., and Schmid, B.: Quantifying the evidence for biodiversity effects on ecosystem functioning and services, Ecol. Lett., 9, 1146–1156, 2006. Barnes, R. F., Nelson, C. F., Collins, M., and Moore, K. J.: Forages. An introduction to grassland agriculture, Iowa State Press, Ames, 6th edn., 2003. Barnes, R. F., Nelson, C. F., Moore, K. J., and Collins, M.: Forages. To the science of grassland agriculture, Blackwell Publishing, Ames, Oxford, Victoria, 6th edn., 2007. Bullock, J. M., Pywell, R. F., and Walker, K. J.: Long-term enhancement of agricultural production by restoration of biodiversity, J. Appl. Ecol., 44, 6–12, 2007. Cardinale, B. J., Srivastava, D. S., Duffy, J. E., Wright, J. P., Downing, A. L., Sankaran, M., and Jouseau, C.: Effects of biodiversity on the functioning of trophic groups and ecosystems, Nature, 443, 989–992, 2006. Cardinale, B. J., Wrigh, J. P., Cadotte, M. W., Carroll, I. T., Hector, A., Srivastava, D. S., Loreau, M., and Weis, J. J.: Impacts of plant diversity on biomass production increase through time because of species complementarity, P. Natl. Acad. Sci. USA, 104, 18123–18128, 2007. Di Tommaso, A. and Aarssen, L. W.: Resource manipulations in natural vegetation: a review, Vegetatio, 84, 9–29, 1989. Diaz, S., Fargione, J., Chapin~III, F. S., and Tilman, D.: Biodiversity loss threatens human well-being, Plos Biol., 4, 1300–1305, 2006. Dimitrakopoulos, P. G. and Schmid, B.: Biodiversity effects increase linearly with biotope space, Ecol. Lett., 7, 574–583, 2004. Fargione, J., Hill, J., Tilman, D., Polasky, S., and Hawthorne, P.: Biofuels: Effects on land and fire – Response, Science, 321, 199–200, 2008a. Fargione, J., Hill, J., Tilman, D., Polasky, S., and Hawthorne, P.: Land clearing and the biofuel carbon debt, Science, 319, 1235–1238, 2008b. Fridley, J. D.: Resource availability dominates and alters the relationship between species diversity and ecosystem productivity in experimental plant communities, Oecologia, 132, 271–277, 2002. Fridley, J. D.: Diversity effects on production in different light and fertility environments: an experiment with communities of annual plants, J. Ecol., 91, 396–406, 2003. Gough, L., Osenberg, G. W., Gross, K. L., and Collins, S. L.: Fertilization effects on species density and primary productivity in herbaceous plant communities, Oikos, 89, 428–439, 2000. Gross, N., Suding, K. N., Lavorel, S., and Roumet, C.: Complementarity as a mechanism of coexistence between functional groups of grasses, J. Ecol., 95, 1296–1305, 2007. Hartwig, U. A.: The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level, Perspect. Plant Ecol., 1, 92–120, 1998. He, J.-S., Bazzaz, F. A., and Schmid, B.: Interactive effects of diversity, nutrients and elevated CO2 on experimental plant communities, Oikos, 97, 337–348, 2002. Hector, A., Schmid, B., Beierkuhnlein, C., Caldeira, M. C., Diemer, M., Dimitrakopoulos, P. G., Finn, J. A., Freitas, H., Giller, P. S., Good, J., Harris, R., Hogberg, P., Huss-Danell, K., Joshi, J., Jumpponen, A., Korner, C., Leadley, P. W., Loreau, M., Minns, A., Mulder, C. P. H., O'Donovan, G., Otway, S. J., Pereira, J. S., Prinz, A., Read, D. J., Scherer-Lorenzen, M., Schulze, E. D., Siamantziouras, A. S. D., Spehn, E. M., Terry, A. C., Troumbis, A. Y., Woodward, F. I., Yachi, S., and Lawton, J. H.: Plant diversity and productivity experiments in European grasslands, Science, 286, 1123–1127, 1999. Hector, A. and Loreau, M.: Relationships between biodiverstiy and production in grasslands at local and regional scales, in: Grassland: a global resource, edited by: McGilloway, D. A., Wageningen Academic Publishers, Wageningen, 295–304, 2005. Hector, A. and Bagchi, R.: Biodiversity and ecosystem multifunctionality, Nature, 448, 188–191, 2007. Hill, J., Polasky, S., Nelson, E., Tilman, D., Huo, H., Ludwig, L., Neumann, J., Zheng, H. C., and Bonta, D.: Climate change and health costs of air emissions from biofuels and gasoline, P. Natl. Acad. Sci. USA, 106, 2077–2082, 2009. Hodgson, J. G., Montserrat-Marti, G., Tallowin, J., Thompson, K., Diaz, S., Cabido, M., Grime, J. P., Wilson, P. J., Band, S. R., Bogard, A., Cabido, R., Caceres, D., Castro-Diez, P., Ferrer, C., Maestro-Martinez, M., Perez-Rontome, M. C., Charles, M., Cornelissen, J. H. C., Dabbert, S., Perez-Harguindeguy, N., Krimly, T., Sijtsma, F. J., Strijker, D., Vendramini, F., Guerrero-Campo, J., Hynd, A., Jones, G., Romo-Diez, A., Espuny, L. D., Villar-Salvador, P., and Zak, M. R.: How much will it cost to save grassland diversity?, Biol. Conserv., 122, 263–273, 2005. Hooper, D. U., Chapin, F. S. I., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A. J., Vandermeer, J., and Wardle, D. A.: Effects of biodiversity on ecosystem functioning: a consensus of current knowledge, Ecol. Monogr., 75, 3–35, 2005. Hopkins, A.: Herbage production, in: Grass: its production and utilization, edited by: Hopkins, A., Blackwell Publishing, Oxford, 99–110, 2000. Huston, M. A.: Hidden Treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity, Oecologia, 110, 449–460, 1997. Kinzig, A. P., Pacala, S. W., and Tilman, D.: The Functional Consequences of Biodiversity, Princeton University Press, Princeton, 2002. Kirwan, L., Lüscher, A., Sebastia, M. T., Finn, J. A., Collins, R. P., Porqueddu, C., Helgadottir, S., Baadshaug, O. H., Brophy, C., Coran, C., Dalmannsdottir, S., Delgado, I., Elgersma, A., Fothegill, P., Frankow-Lindberg, B. E., Golinski, P., Grieu, P., Gustavsson, A. M., Höglind, M., Hueguenin-Elie, O., Iliadis, C., Jorgensen, M., Kadziuliene, Z., Karyotis, T., Lunnan, Malengier, M., Maltoni, S., Meyer, V., Nyfeler, D., Nykanen-Kurki, P., Parente, J., Smit, H. J., Thumm, U., and Connolly, J.: Evenness drives consistent diversity effects in intensive grassland systems across 28~European sites, J. Ecol., 95, 530–539, 2007. Kleijn, D. and Sutherland, W. J.: How effective are European agri-environment schemes in conserving and promoting biodiversity?, J. Appl. Ecol., 40, 947–969, 2003. Lemaire, G., Wilkins, R., and Hodgson, J.: Challenges for grassland science: managing research priorities, Agr. Ecosyst. Environ., 108, 99–108, 2005. Loreau, M.: Biodiversity and ecosystem functioning: A mechanistic model, P. Natl. Acad. Sci. USA, 95, 5632–5636, 1998. Loreau, M., Naeem, S., and Inchausti, P.: Biodiversity and Ecosystem Functioning – Synthesis and Perspectives, Oxford University Press, Oxford, 2002. Lüscher, A., Finn, J. A., Connolly, J., Sebastia, M. T., Collins, R., Fothergill, M., Porqueddu, C., Brophy, C., Huguenin-Elie, M., Kirwan, L., Nyfeler, D., and Helgadottir, A.: Benefits of sward diversity for agricultural grasslands, Biodiversity, 9, 29–32, 2008. Marquard, E., Weigelt, A., Temperton, V. M., Roscher, C., Schumacher, J., Buchmann, N., Fischer, M., Weisser, W. W., and Schmid, B.: Plant species richness and functional composition drive overyielding in a 6-year grassland experiment, J. Ecol., 97, 696–704, 2009. Milcu, A., Partsch, S., Scherber, C. D., Weisser, W. W., and Scheu, S.: Earthworms and legumes control litter decomposition in a plant diversity gradient, Ecology, 89, 1872–1882, 2008. Mwangi, P. N., Schmitz, M., Scherber, C., Roscher, C., Schumacher, J., Scherer-Lorenzen, M., Weisser, W. W., and Schmid, B.: Niche pre-emption increases with species richness in experimental plant communities, J. Ecol., 95, 65–78, 2007. Nyfeler, D., Huguenin-Elie, M., Frossard, E., and Lüscher, A.: Regulation of symbiotic nitrogen fixation in grass-clover mixtures, Grassland Sci. Eur., 11, 246–248, 2006. Nyfeler, D., Huguenin-Elie, M., Suter, M., Frossard, E., and Lüscher, A.: Well-balanced grass-legume mixtures with low nitrogen fertilization can be as productive as highly fertilized grass monocultures, Grassland Sci. Eur., 13, 197–199, 2008. Oelmann, Y., Wilcke, W., Temperton, V. M., Buchmann, N., Roscher, C., Schumacher, J., Schulze, E. D., and Weisser, W. W.: Soil and plant nitrogen pools as related to plant diversity in an experimental grassland, Soil Sci. Soc. Am. J., 71, 720–729, 2007. Plantureux, S., Peeters, A., and McCracken, D.: Biodiversity in intensive grasslands: Effect of management, improvement and challenges, Agronomy Research, 3, 153–164, 2005. Reich, P. B., Knops, J., Tilman, D., Craine, J., Ellsworth, D., Tjoelker, M., Lee, T., Wedin, D., Naeem, S., Bahauddin, D., Hendrey, G., Jose, S., Wrage, K., Goth, J., and Bengston, W.: Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition, Nature, 410, 809–812, 2001. Reich, P. B., Tilman, D., Naeem, S., Ellsworth, D. S., Knops, J., Craine, J., Wedin, D., and Trost, J.: Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N, P. Natl. Acad. Sci. USA, 101, 10101–10106, 2004. Rixen, C., Huovinen, C., Huovinen, K., Stöckli, V., and Schmid, B.: A plant diversity$\times$water chemistry experiment in subalpine grassland, Perspect, Plant Ecol., 10, 51–61, 2007. Robertson, G. P. and Swinton, S. M.: Reconciling agricultural productivity and environmental integrity: a grand challenge for agriculture, Front. Ecol. Environ., 3, 38–46, 2005. Roscher, C., Schumacher, J., Baade, J., Wilcke, W., Gleixner, G., Weisser, W. W., Schmid, B., and Schulze, E. D.: The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community, Basic Appl. Ecol., 5, 107–121, 2004. Roscher, C., Temperton, V. M., Scherer-Lorenzen, M., Schmitz, M., Schumacher, J., Schmid, B., Buchmann, N., Weisser, W. W., and Schulze, E. D.: Overyielding in experimental grassland communities – irrespective of species pool or spatial scale, Ecol. Lett., 8, 419–429, 2005. Roscher, C., Temperton, V. M., Buchmann, N., and Schulze, E. D.: Community assembly and biomass production in regularly and never weeded experimental grasslands, Acta Oecol., 35, 206–217, 2009a. Roscher, C., Beßler, H., Oelmann, Y., Engels, C., Wilcke, W., and Schulze, E. D.: Resources, recruitment limitation and invader species identity determine pattern of spontaneous invasion in experimental grasslands, J. Ecol., 97, 32–47, 2009b. Sanderson, M. A., Skinner, R. H., Barker, D. J., Edwards, G. R., Tracy, B. F., and Wedin, D. A.: Plant species diversity and management of temperate forage and grazing land ecosystems, Crop Sci., 44, 1132–1144, 2004. Sanderson, M. A., Goslee, S. C., Soder, K. J., Skinner, R. H., Tracy, B. F., and Deak, A.: Plant species diversity, ecosystem function, and pasture management – A perspective, Can. J. Plant Sci., 87, 479–487, 2007. Scherer-Lorenzen, M., Palmborg, C., Prinz, A., and Schulze, E. D.: The role of plant diversity and composition for nitrate leaching in grasslands, Ecology, 84, 1539–1552, 2003. Siemann, E., Tilman, D., Haarstad, J., and Ritchie, M.: Experimental tests of the dependence of arthropod diversity on plant diversity, Am. Nat., 152, 738–750, 1998. Smit, H. J., Metzger, M. J., and Ewert, F.: Spatial distribution of grassland productivity and land use in Europe, Agr. Syst., 98, 208–219, 2008. Spehn, E., Scherer-Lorenzen, M., Schmid, B., Hector, A., Caldeira, M. C., Dimitrakopoulos, P. G., Finn, J. A., Jumpponen, A., O'Donovan, G., Pereira, J. S., Schulze, E. D., Troumbis, A. Y., and Körner, C.: The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen, Oikos, 98, 205–218, 2002. Spehn, E., Hector, A., Joshi, J., Scherer-Lorenzen, M., Schmid, B., Bazeley-White, E., Beierkuhnlein, C., Caldeira, M. C., Diemer, M., Dimitrakopoulos, P. G., Finn, J. A., Koricheva, J., Leadley, P., Loreau, M., Minns, A., Mulder, C. P. H., O'Donovan, G., Otway, S., Palmborg, C., Pereira, J. S., Pfisterer, A. B., Prinz, A., Read, D. J., Schulze, E. D., Siamantziouras, A.-S. D., Terry, A. C., Troumbis, A. Y., Woodward, F. I., Yachi, S., and Lawton, J. H.: Ecosystem effects of biodiversity manipulations in European grasslands, Ecol. Monogr., 75, 37–63, 2005. Symstad, A.: A test of the effects of functional group richness and composition on grassland invasibility, Ecology, 81, 99–109, 2000. Tallowin, J. R. B. and Jefferson, R. G.: Hay production from lowland semi-natural grasslands: a review of implications for ruminant livestock systems, Grass Forage Sci., 54, 99–115, 1999. Tilman, D., Wedin, D., and Knops, J.: Productivity and sustainability influenced by biodiversity in grassland ecosystems, Nature, 379, 718–720, 1996. Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and Siemann, E.: The influence of functional diversity and composition on ecosystem processes, Science, 277, 1300–1302, 1997a. Tilman, D., Lehman, C. L., and Thomson, K. T.: Plant diversity and ecosystem productivity: theoretical considerations, P. Natl. Acad. Sci. USA, 94, 1857–1861, 1997b. Tilman, D., Reich, P., Knops, J., Wedin, D., Mielke, T., and Lehman, C.: Diversity and Productivity in a Long-Term Grassland Experiment, Science, 294, 843–845, 2001. Tilman, D.: Carbon-Negative Biofuels from Low-Input High-Diversity Grassland Biomass, Science, 314, 1598–1600, 2006. Tilman, D., Reich, P. B., and Knops, J. M. H.: Biodiversity and ecosystem stability in a decade-long grassland experiment, Nature, 442, 629–632, 2006. Tilman, D., Hill, J., and Lehman, C.: Response to comment on "Carbon-negative biofuels from low-input high-diversity grassland biomass", Science, 316(5831), p 1567, 2007. Tscharntke, T., Klein, A.-M., Kruess, A., Steffan-Dewenter, I., and Thies, C.: Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management, Ecol. Lett., 8, 857–874, 2005. Tylianakis, J. M., Rand, T. A., Kahmen, A., Klein, A.-M., Buchmann, N., Perner, J., and Tscharntke, T.: Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems, Plos Biol., 6, 947–956, 2008. Voigtländer, G. and Jacob, H.: Gründlandwirtschaft und Futterbau, Ulmer Verlag, 1987. Von Felten, S., Buchmann, N., Hector, A., Niklaus, P. A., Schmid, B., and Scherer-Lorenzen, M.: Belowground nitrogen partitioning in experimental grassland plant communities of varying species richness, Ecology, 90, 1389–1399, 2009. Weigelt, A., Schumacher, J., Roscher, C., and Schmid, B.: Does biodiversity increase spatial stability in plant community biomass?, Ecol. Lett., 11, 338–347, 2008.