References

Biogeosciences

1726-4189

Copernicus GmbH

Göttingen, Germany

10.5194/bg-5-585-2008

Biomass production in experimental grasslands of different species richness during three years of climate warming

De Boeck

H. J.

¹ Lemmens

C. M. H. M.

¹ Zavalloni

¹ Gielen

¹ Malchair

³ Carnol

³ Merckx

² Van den Berge

¹ Ceulemans

¹ Nijs

Research Group of Plant and Vegetation Ecology, Department of Biology, Universiteit Antwerpen (Campus Drie Eiken), Universiteitsplein 1, B-2610 Wilrijk, Belgium

Division Soil and Water Management, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, Kasteelpark Arenberg 20, B-3001 Leuven/Heverlee, Belgium

Lab. of Plant and Microbial Ecology, Institute of Plant Biology B22, Univ. of Liège, Sart Tilman, B-4000 Liège, Belgium

21 04 2008

5 2 585 594

This is an open-access article ditributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

This article is available from http://www.biogeosciences.net/5/585/2008/bg-5-585-2008.html

The full text article is available as a PDF file from http://www.biogeosciences.net/5/585/2008/bg-5-585-2008.pdf

Here we report on the single and combined impacts of climate warming and species richness on the biomass production in experimental grassland communities. Projections of a future warmer climate have stimulated studies on the response of terrestrial ecosystems to this global change. Experiments have likewise addressed the importance of species numbers for ecosystem functioning. There is, however, little knowledge on the interplay between warming and species richness. During three years, we grew experimental plant communities containing one, three or nine grassland species in 12 sunlit, climate-controlled chambers in Wilrijk, Belgium. Half of these chambers were exposed to ambient air temperatures (unheated), while the other half were warmed by 3°C (heated). Equal amounts of water were added to heated and unheated communities, so that warming would imply drier soils if evapotranspiration was higher. Biomass production was decreased due to warming, both aboveground (–29%) and belowground (–25%), as negative impacts of increased heat and drought stress in summer prevailed. Complementarity effects, likely mostly through both increased aboveground spatial complementarity and facilitative effects of legumes, led to higher shoot and root biomass in multi-species communities, regardless of the induced warming. Surprisingly, warming suppressed productivity the most in 9-species communities, which may be attributed to negative impacts of intense interspecific competition for resources under conditions of high abiotic stress. Our results suggest that warming and the associated soil drying could reduce primary production in many temperate grasslands, and that this will not necessarily be mitigated by efforts to maintain or increase species richness.

References 1

Aerts, R., Cornelissen, J. H. C., and Dorrepaal, E.: Plant performance in a warmer world: General responses of plants from cold, northern biomes and the importance of winter and spring events, Plant Ecol., 182, 65–77, 2006.

Calfapietra, C., Gielen, B., Sabatti, M., De Angelis, P., Miglietta, F., Scarascia-Mugnozza, G., Ceulemans, R.: Do above-ground growth dynamics of poplar change with time under CO2 enrichment?, New Phytol., 160, 305–318, 2003.

Callaway, R. M., Brooker, R. W., Choler, P., Kikvidze, Z., Lortie, C. J., Michalet, R., Paolini, L., Pugnaire, F. I., Newingham, B., Cook, B. J., and Aschehoug, E. T.: Positive interactions among alpine plants increase with stress, Nature, 417, 844–848, 2002.

Cernusca, A.: Energy exchange within individual layers of a meadow, Oecologia, 23, 141–149, 1976.

Chaves, M. M., Pereira, J. S., Maroco, J., Rodrigues, M. L., Ricardo, C. P. P., Osorio, M. L., Carvalho, I., Faria, T., and Pinheiro, C.: How plants cope with water stress in the field. Photosynthesis and growth, Ann. Bot., 89, 907–916, 2002.

De Boeck, H. J., Lemmens, C. M. H. M., Bossuyt, H., Malchair, S., Carnol, M., Merckx, R., Nijs, I., and Ceulemans, R.: How do climate warming and plant species richness affect water use in experimental grasslands?, Plant Soil, 288, 249–261, 2006a.

De Boeck, H. J., Nijs, I., Lemmens, C. M. H. M., and Ceulemans, R. Underlying effects of spatial aggregation (clumping) in relationships between plant diversity and resource uptake, Oikos, 113, 269–278, 2006b.

De Boeck, H. J, Lemmens, C. M. H. M., Gielen, B., Bossuyt, H., Malchair, S., Carnol, M., Merckx, R., Ceulemans, R., Nijs, I.: Combined effects of climate warming and plant diversity loss on above- and below-ground grassland productivity, Env. Exp. Bot., 60, 95–104, 2007a.

De Boeck, H. J., Lemmens, C. M. H. M., Vicca, S., Van den Berge, J., Van Dongen, S., Janssens, I., Ceulemans, R., Nijs, I.: How do climate warming and species richness affect CO2 fluxes in experimental grasslands?, New Phytol., 175, 512–522, 2007b.

De Valpine, P., and Harte, J.: Plant responses to experimental warming in a montane meadow, Ecology, 82, 637–648, 2001.

Eatherall, A.: Modelling climate change impacts on ecosystems using linked models and a GIS, Climatic Change, 35, 17–34, 1997.

Edwards, E. J., Benham, D. G., Marland, L. A., and Fitter, A. H.: Root production is determined by radiation flux in a temperate grassland community, Global Change Biol., 10, 209–227, 2004.

Fridley, J. D.: The influence of species diversity on ecosystem productivity: how, where and why?, Oikos, 93, 514–526, 2001.

Gielen, B., De Boeck, H. J., Lemmens, C. M. H. M., Valcke, R., Nijs, I., and Ceulemans, R.: Grassland species will not necessarily benefit from future elevated air temperatures: a chlorophyll fluorescence approach to study autumn physiology, Physiol. Plantarum, 125, 52–63, 2005.

Gielen, B., Naudts, K., D'Haese, D., Lemmens, C. M. H. M., De Boeck, H. J., Biebaut, E., Serneels, R., Valcke, R., Nijs, I., Ceulemans, R.: Effects of climate warming and species richness on photochemistry of grasslands, Physiol. Plantarum, 131, 251–262, 2007.

Gillman, L. N., and Wright, S. D.: The influence of productivity on the species richness of plants: A critical assessment, Ecology, 87, 1234–1243, 2006.

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., Högberg, P., Huss-Danell, K., Joshi, J., Jumpponen, A., Körner, 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., Schmid, B., Beierkuhnlein, C., Caldeira, M. C., Diemer, M., Dimitrakopoulos, P. G., Finn, J. A., Freitas, H., Giller, P. S., Good, J., Harris, R., Högberg, P., Huss-Danell, K., Joshi, J., Jumpponen, A., Körner, 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.: No consistent effect of plant diversity on productivity: Response, Science, 289, 1255, 2000.

Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Setala, 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.

Huston, M. A., Aarssen, L. W., Austin, M. P., Cade, B. S., Fridley, J. D., Garnier, E., Grime, J. P., Hodgson, J., Lauenroth, W. K., Thompson, K., Vandermeer, J. H., and Wardle, D. A.: No consistent effect of plant diversity on productivity, Science, 289, 1255, 2000.

IPCC: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, edited by Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M., and Miller, H. L., Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2007.

Kahmen, A., Perner, J., and Buchmann, N.: Diversity-dependent productivity in semi-natural grasslands following climate perturbations, Funct. Ecol., 19, 594–601, 2005.

Klein, J. A., Harte, J., and Zhao, X. Q.: Experimental warming causes large and rapid species loss, dampened by simulated grazing, on the Tibetan Plateau, Ecol. Lett., 7, 1170–1179, 2004.

Larcher W.: Physiological plant ecology, 4th edition, Springer-Verlag, Berlin, 2003.

Lemmens, C. M. H. M., De Boeck, H. J., Gielen, B., Bossuyt, H., Malchair, S., Carnol, M., Merckx, R., Nijs, I., and Ceulemans, R.: End-of-season effects of elevated temperature on ecophysiological processes of grassland species at different species richness levels, Env. Exp. Bot., 56, 245–254, 2006.

Lilley, J. M., Bolger, T. P., Peoples, M. B., and Gifford, R. M.: Nutritive value and the nitrogen dynamics of \textitTrifolium subterraneum and \textitPhalaris aquatica under warmer, high CO2 conditions, New Phytol., 150, 385–395, 2001.

Littell, R. C., Milliken, G. A., Stroup, W. W., Wolfinger, R. D., and Schabenberger, O.: SAS for Mixed Models, Second Edition, SAS Institute Inc., Cary, NC, 2006.

Loreau, M., and Hector, A.: Partitioning selection and complementarity in biodiversity experiments, Nature, 412, 72–76, 2001.

Michalet, R., Brooker, R. W., Cavieres, L. A., Kikvidze, Z., Lortie, C. J., Pugnaire, F. I., Valiente-Banuet, A., and Callaway, R. M.: Do biotic interactions shape both sides of the humped-back model of species richness in plant communities?, Ecol. Lett., 9, 767–773, 2006.

Middelboe, A. L., and Binzer, T.: Importance of canopy structure on photosynthesis in single- and multi-species assemblages of marine macroalgae, Oikos, 107, 422-432, 2004.

Mokany, K., Raison, R. J., and Prokushkin, A. S.: Critical analysis of root: shoot ratios in terrestrial biomes, Global Change Biol., 12, 84–96, 2006.

Mou, P., Jones, R. H., Mitchell, R. J., and Zutter B.: Spatial-distribution of roots in sweetgum and loblolly-pine monocultures and relationships with aboveground biomass and soil nutrients, Funct. Ecol., 9, 689–699, 1995

Myneni,~R. B., Keeling, C. D., Tucker, C. J., Asrar, G., and Namani, R. R.: Increased plant growth in the northern high latitudes from 1981 to 1991, Nature, 386, 698–702, 1997.

Naeem, S., and Li, S.B.: Biodiversity enhances ecosystem reliability, Nature, 390, 507-509, 1997.

Nippert, J. B., Knapp, A. K., and Briggs, J. M.: Intra-annual rainfall variability and grassland productivity: can the past predict the future?, Plant Ecol., 184, 65-74, 2006.

Nobel, P. S.: Root distribution and seasonal production in the northwestern Sonoran desert for a C-3 subshrub, a C-4 bunchgrass, and a CAM leaf succulent, Am. J. Bot., 84, 949–955, 1997.

Norby, R. J., and Luo, Y. Q.: Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world, New Phytol., 162, 281–293, 2004.

Pfisterer, A. B., and Schmid, B.: Diversity-dependent production can decrease the stability of ecosystem functioning, Nature, 416, 84-86, 2002.

Reich, P. B., Knops, J., Tilman, D., Craine, J., Ellsworth, D., Tjoekler, D., Lee, T., Wedin, D., Naeem, S., Bahauddin, D., Hendrey, G., Jose, S., Wrage, K., Goth, J., and Bengtson, W.: Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition, Nature, 410, 809–812, 2001.

Reichstein, M., Ciais, P., Papale, D., Valentini, R., Running, S., Viovy, N., Cramer, W., Granier, A., Ogée, J., Allard, V., Aubinet, M., Bernhofer, C., Buchmann, N., Carrara, A., Grünwald, T., Heimann, M., Heinesch, B., Knohl, A., Kutsch, W., Loustau, D., Manca, G., Matteucci, G., Miglietta, F., Ourcival, J. M., Pilegaard, K., Pumpanen, J., Rambal, S., Schaphoff, S., Seufert, G., Soussana, J.-F., Sanz, M.-J., Vesala, T., and Zhao, M.: Reduction of ecosystem productivity and respiration during the European summer 2003 climate anomaly: a joint flux tower, remote sensing and modelling analysis, Global Change Biol., 13, 634–651, 2007.

Riedo, M., Gyalistras, D., and Fuhrer, J.: Pasture responses to elevated temperature and doubled CO2 concentration: assessing the spatial pattern across an alpine landscape, Climate Research, 17, 19–31, 2001.

Roscher, C., Temperton, V. M., Scherer-Lorenzen, M., Schmitz, M., Schumacher, M., 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.

Rustad, L. E., Campbell, J. L., Marion, G. M., Norby, R. J., Mitchell, M. J., Hartley, A. E., Cornelissen, J. H. C., and Gurevitch, J.: A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming, Oecologia, 126, 543–562, 2001.

Sala, O. E., Chapin, F. S. III, Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., Kinzig, A., Leemans, R., Lodge, D. M., Mooney, H. A., Oesterheld, M., Le Roy Poff, N., Sykes, M. T., Walker, B. H., Walker, M., and Wall, D. H.: Global bio-diversity scenarios for the year 2100, Science, 287, 1770–1774, 2000.

Saleska, S. R., Harte, J., and Torn, M. S.: The effect of experimental ecosystem warming on CO2 fluxes in a montane meadow, Global Change Biol., 5, 125–141, 1999.

Temperton, V. M., Mwangi, P. M., Scherer-Lorenzen, M., Schmid, B., Buchmann, M.: Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment, Oecologia, 151, 190–205, 2007.

Van Peer, L., Nijs, I., Reheul, D., and De Cauwer, B.: Species richness and susceptibility to heat and drought extremes in synthesized grassland ecosystems: compositional vs physiological effects, Funct. Ecol., 18, 769–778, 2004.

van Ruijven, J., and Berendse, F.: Diversity-productivity relationships: Initial effects, long-term patterns, and underlying mechanisms, P. Natl. Acad. Sci. USA, 102, 695–700, 2005.

Walther, G.-R.: Plants in a warmer world, Perspect. Plant Ecol., 6, 169–185, 2003.

Wang, X. Z.: Effects of species richness and elevated carbon dioxide on biomass accumulation: a synthesis using meta-analysis, Oecologia, 152, 595–605, 2007.

Wardle, D. A., and Peltzer, D. A.: Interspecific interactions and biomass allocation among grassland plant species, Oikos, 100, 497–506, 2003.

Weltzin, J. F., Loik, M. E., Schwinning, S., Williams, D. G.,~Fay, P. A.,~Haddad, B. M.,~Harte, J.,~Huxman, T. E.,~Knapp, A. K.,~Lin, G.,~Pockman, W. T.,~Shaw, M. R.,~Small, E. E.,~Smith, M. D.,~Smith, S. D.,~Tissue, D. T., and~Zak, J. C.: Assessing the response of terrestrial ecosystems to potential changes in precipitation, Bioscience, 53, 941–952, 2003.

White, T. A., Campbell, B. D., Kemp, P. D., and Hunt, C. L.: Sensitivity of three grassland communities to simulated extreme temperature and rainfall events, Global Change Biol., 6, 671–684, 2000.