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	<journal>
		<journal_title>Biogeosciences</journal_title>
		<journal_url>www.biogeosciences.net</journal_url>
		<issn>1726-4170</issn>
		<eissn>1726-4189</eissn>
		<volume_number>5</volume_number>
		<issue_number>2</issue_number>
		<publication_year>2008</publication_year>
	</journal>
	<doi>10.5194/bg-5-585-2008</doi>
	<article_url>http://www.biogeosciences.net/5/585/2008/</article_url>
	<abstract_html>http://www.biogeosciences.net/5/585/2008/bg-5-585-2008.html</abstract_html>
	<fulltext_pdf>http://www.biogeosciences.net/5/585/2008/bg-5-585-2008.pdf</fulltext_pdf>
	<start_page>585</start_page>
	<end_page>594</end_page>
	<publication_date>2008-04-21</publication_date>
	<article_title content_type="html">Biomass production in experimental grasslands of different species richness during three years of climate warming</article_title>
	<authors>
		<author numeration="1" affiliations="1">
			<name>H. J. De Boeck</name>
			<email>hans.deboeck@ua.ac.be</email>
		</author>
		<author numeration="2" affiliations="1">
			<name>C. M. H. M. Lemmens</name>
		</author>
		<author numeration="3" affiliations="1">
			<name>C. Zavalloni</name>
		</author>
		<author numeration="4" affiliations="1">
			<name>B. Gielen</name>
		</author>
		<author numeration="5" affiliations="3">
			<name>S. Malchair</name>
		</author>
		<author numeration="6" affiliations="3">
			<name>M. Carnol</name>
		</author>
		<author numeration="7" affiliations="2">
			<name>R. Merckx</name>
		</author>
		<author numeration="8" affiliations="1">
			<name>J. Van den Berge</name>
		</author>
		<author numeration="9" affiliations="1">
			<name>R. Ceulemans</name>
		</author>
		<author numeration="10" affiliations="1">
			<name>I. Nijs</name>
		</author>
	</authors>
	<affiliations>
		<affiliation numeration="1" content_type="html">Research Group of Plant and Vegetation Ecology, Department of Biology, Universiteit Antwerpen (Campus Drie Eiken), Universiteitsplein 1, B-2610 Wilrijk, Belgium</affiliation>
		<affiliation numeration="2" content_type="html">Division Soil and Water Management, Faculty of Bioscience Engineering, Katholieke Universiteit Leuven, Kasteelpark Arenberg 20, B-3001 Leuven/Heverlee, Belgium</affiliation>
		<affiliation numeration="3" content_type="html">Lab. of Plant and Microbial Ecology, Institute of Plant Biology B22, Univ. of Liège, Sart Tilman, B-4000 Liège, Belgium</affiliation>
	</affiliations>
	<abstract content_type="html">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&amp;deg;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 (&amp;ndash;29%) and belowground (&amp;ndash;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.</abstract>
	<references>
		<reference numeration="1" content_type="text">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&amp;ndash;77, 2006. </reference>
		<reference numeration="2" content_type="text">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&amp;ndash;318, 2003. </reference>
		<reference numeration="3" content_type="text">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&amp;ndash;848, 2002. </reference>
		<reference numeration="4" content_type="text">Cernusca, A.: Energy exchange within individual layers of a meadow, Oecologia, 23, 141&amp;ndash;149, 1976. </reference>
		<reference numeration="5" content_type="text">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&amp;ndash;916, 2002. </reference>
		<reference numeration="6" content_type="text">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&amp;ndash;261, 2006a. </reference>
		<reference numeration="7" content_type="text">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&amp;ndash;278, 2006b. </reference>
		<reference numeration="8" content_type="text">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&amp;ndash;104, 2007a. </reference>
		<reference numeration="9" content_type="text">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 CO&lt;sub&gt;2&lt;/sub&gt; fluxes in experimental grasslands?, New Phytol., 175, 512&amp;ndash;522, 2007b. </reference>
		<reference numeration="10" content_type="text">De Valpine, P., and Harte, J.: Plant responses to experimental warming in a montane meadow, Ecology, 82, 637&amp;ndash;648, 2001. </reference>
		<reference numeration="11" content_type="text">Eatherall, A.: Modelling climate change impacts on ecosystems using linked models and a GIS, Climatic Change, 35, 17&amp;ndash;34, 1997. </reference>
		<reference numeration="12" content_type="text">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&amp;ndash;227, 2004. </reference>
		<reference numeration="13" content_type="text">Fridley, J. D.: The influence of species diversity on ecosystem productivity: how, where and why?, Oikos, 93, 514&amp;ndash;526, 2001. </reference>
		<reference numeration="14" content_type="text">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&amp;ndash;63, 2005. </reference>
		<reference numeration="15" content_type="text">Gielen, B., Naudts, K., D&apos;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&amp;ndash;262, 2007. </reference>
		<reference numeration="16" content_type="text">Gillman, L. N., and Wright, S. D.: The influence of productivity on the species richness of plants: A critical assessment, Ecology, 87, 1234&amp;ndash;1243, 2006. </reference>
		<reference numeration="17" content_type="text">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&apos;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&amp;ndash;1127, 1999. </reference>
		<reference numeration="18" content_type="text">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&apos;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. </reference>
		<reference numeration="19" content_type="text">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&amp;ndash;35, 2005. </reference>
		<reference numeration="20" content_type="text">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. </reference>
		<reference numeration="21" content_type="text">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. </reference>
		<reference numeration="22" content_type="text">Kahmen, A., Perner, J., and Buchmann, N.: Diversity-dependent productivity in semi-natural grasslands following climate perturbations, Funct. Ecol., 19, 594&amp;ndash;601, 2005. </reference>
		<reference numeration="23" content_type="text">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&amp;ndash;1179, 2004. </reference>
		<reference numeration="24" content_type="text">Larcher W.: Physiological plant ecology, 4th edition, Springer-Verlag, Berlin, 2003. </reference>
		<reference numeration="25" content_type="text">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&amp;ndash;254, 2006. </reference>
		<reference numeration="26" content_type="text">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 CO&lt;sub&gt;2&lt;/sub&gt; conditions, New Phytol., 150, 385&amp;ndash;395, 2001. </reference>
		<reference numeration="27" content_type="text">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. </reference>
		<reference numeration="28" content_type="text">Loreau, M., and Hector, A.: Partitioning selection and complementarity in biodiversity experiments, Nature, 412, 72&amp;ndash;76, 2001. </reference>
		<reference numeration="29" content_type="text">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&amp;ndash;773, 2006. </reference>
		<reference numeration="30" content_type="text">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. </reference>
		<reference numeration="31" content_type="text">Mokany, K., Raison, R. J., and Prokushkin, A. S.: Critical analysis of root: shoot ratios in terrestrial biomes, Global Change Biol., 12, 84&amp;ndash;96, 2006. </reference>
		<reference numeration="32" content_type="text">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&amp;ndash;699, 1995 </reference>
		<reference numeration="33" content_type="text">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&amp;ndash;702, 1997. </reference>
		<reference numeration="34" content_type="text">Naeem, S., and Li, S.B.: Biodiversity enhances ecosystem reliability, Nature, 390, 507-509, 1997. </reference>
		<reference numeration="35" content_type="text">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. </reference>
		<reference numeration="36" content_type="text">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&amp;ndash;955, 1997. </reference>
		<reference numeration="37" content_type="text">Norby, R. J., and Luo, Y. Q.: Evaluating ecosystem responses to rising atmospheric CO&lt;sub&gt;2&lt;/sub&gt; and global warming in a multi-factor world, New Phytol., 162, 281&amp;ndash;293, 2004. </reference>
		<reference numeration="38" content_type="text">Pfisterer, A. B., and Schmid, B.: Diversity-dependent production can decrease the stability of ecosystem functioning, Nature, 416, 84-86, 2002. </reference>
		<reference numeration="39" content_type="text">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&amp;ndash;812, 2001. </reference>
		<reference numeration="40" content_type="text">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&amp;ndash;651, 2007. </reference>
		<reference numeration="41" content_type="text">Riedo, M., Gyalistras, D., and Fuhrer, J.: Pasture responses to elevated temperature and doubled CO&lt;sub&gt;2&lt;/sub&gt; concentration: assessing the spatial pattern across an alpine landscape, Climate Research, 17, 19&amp;ndash;31, 2001. </reference>
		<reference numeration="42" content_type="text">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 &amp;ndash; irrespective of species pool or spatial scale, Ecol. Lett., 8, 419&amp;ndash;429, 2005. </reference>
		<reference numeration="43" content_type="text">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&amp;ndash;562, 2001. </reference>
		<reference numeration="44" content_type="text">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&amp;ndash;1774, 2000. </reference>
		<reference numeration="45" content_type="text">Saleska, S. R., Harte, J., and Torn, M. S.: The effect of experimental ecosystem warming on CO&lt;sub&gt;2&lt;/sub&gt; fluxes in a montane meadow, Global Change Biol., 5, 125&amp;ndash;141, 1999. </reference>
		<reference numeration="46" content_type="text">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&amp;ndash;205, 2007. </reference>
		<reference numeration="47" content_type="text">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&amp;ndash;778, 2004. </reference>
		<reference numeration="48" content_type="text">van Ruijven, J., and Berendse, F.: Diversity-productivity relationships: Initial effects, long-term patterns, and underlying mechanisms, P. Natl. Acad. Sci. USA, 102, 695&amp;ndash;700, 2005. </reference>
		<reference numeration="49" content_type="text">Walther, G.-R.: Plants in a warmer world, Perspect. Plant Ecol., 6, 169&amp;ndash;185, 2003. </reference>
		<reference numeration="50" content_type="text">Wang, X. Z.: Effects of species richness and elevated carbon dioxide on biomass accumulation: a synthesis using meta-analysis, Oecologia, 152, 595&amp;ndash;605, 2007. </reference>
		<reference numeration="51" content_type="text">Wardle, D. A., and Peltzer, D. A.: Interspecific interactions and biomass allocation among grassland plant species, Oikos, 100, 497&amp;ndash;506, 2003. </reference>
		<reference numeration="52" content_type="text">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&amp;ndash;952, 2003. </reference>
		<reference numeration="53" content_type="text">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&amp;ndash;684, 2000. </reference>
	</references>
</article>

