"This is the peer reviewed version of the following article: Ratcliffe, S. et al. Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol. Lett. 20, 1414–1426 (2017)., which has been published in final form at [http://onlinelibrary.wiley.com/doi/10.1111/ele.12849/epdf]. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving."
All documents in ORBi are protected by a user license.
FunDivEUROPE; Functional diversity; growing season length; multifunctionality; resource heterogeneity; species richness; water availability
Abstract :
[en] The importance of biodiversity in supporting ecosystem functioning is generally well accepted.
However, most evidence comes from small-scale studies, and scaling-up patterns of biodiversity–
ecosystem functioning (B-EF) remains challenging, in part because the importance of environmental
factors in shaping B-EF relations is poorly understood. Using a forest research platform in
which 26 ecosystem functions were measured along gradients of tree species richness in six regions
across Europe, we investigated the extent and the potential drivers of context dependency of BEF
relations. Despite considerable variation in species richness effects across the continent, we
found a tendency for stronger B-EF relations in drier climates as well as in areas with longer
growing seasons and more functionally diverse tree species. The importance of water availability
in driving context dependency suggests that as water limitation increases under climate change,
biodiversity may become even more important to support high levels of functioning in European
forests.
Ratcliffe, Sophia ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie végétale et microbienne
Wirth, C.; Department of Systematic Botany and Functional Biodiversity, University of Leipzig, Johannisallee 21-23, Leipzig, Germany, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, Leipzig, Germany, Max-Planck-Institute for Biogeochemistry, Hans-Knöll-Str. 10, Jena, Germany
Jucker, T.; Forest Ecology and Conservation, Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, United Kingdom, CSIRO Land and Water Flagship, Private Bag 5, P.O. Wembley, WA, Australia
van der Plas, F.; Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, Switzerland, Senckenberg Gesellschaft für Naturforschung, Biodiversity and Climate Research Centre, Senckenberganlage 25, Frankfurt, Germany
Scherer-Lorenzen, M.; Faculty of Biology/Geobotany, University of Freiburg, Schänzlestr. 1, Freiburg, Germany
Bruelheide, H.; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, Leipzig, Germany, Institute of Biology/Geobotany and Botanical Garden, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, Halle (Saale), Germany
Ohse, B.; Department of Systematic Botany and Functional Biodiversity, University of Leipzig, Johannisallee 21-23, Leipzig, Germany
Paquette, A.; Centre for Forest Research (CFR), Université du Québec à Montréal, Montréal, QC, Canada
Bastias, C. C.; MNCN-CSIC, Serrano 115 bis, Madrid, Spain
Bauhus, J.; Faculty of Environment and Natural Resources, Chair of Silviculture, University of Freiburg, Fahnenbergplatz, Freiburg, Germany
Bonal, D.; INRA, UMR EEF, Champenoux, France
Bouriaud, O.; Faculty of Forestry, Stefan cel Mare University of Suceava, Universitatii Street 13, Suceava, Romania
Bussotti, F.; Department of Agri-Food and Environmental Science (DISPAA), Laboratory of Environmental and Applied Botany, University of Firenze, Piazzale delle Cascine 28, Firenze, Italy
Carnol, Monique ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie végétale et microbienne
Castagneyrol, B.; INRA, UMR 1202 BIOGECO, Cestas, France, University Bordeaux, BIOGECO, UMR 1202, Pessac, France
Chećko, E.; Białowieża Geobotanical Station, Faculty of Biology, University of Warsaw, Białowieża, Poland
Dawud, S. M.; Department of Forestry, College of Agriculture, Wollo University, P.O.Box 1145, Dessie, Ethiopia
Wandeler, H. D.; Department of Earth and Environmental Sciences, University of Leuven, Celestijnenlaan 200E Box 2411, Leuven, Belgium
Domisch, T.; Natural Resources Institute Finland (Luke), Yliopistokatu 6, Joensuu, Finland
Finér, L.; Natural Resources Institute Finland (Luke), Yliopistokatu 6, Joensuu, Finland
Fischer, M.; Institute of Plant Sciences, University of Bern, Altenbergrain 21, Bern, Switzerland
Fotelli, M.; Forest Research Institute of Thessaloniki, Greek Agricultural Organization-Dimitra, Vassilika, Thessaloniki, Greece
Gessler, A.; Swiss Federal Research Institute WSL, Research Unit Forest Dynamics, Zuercherstr 111, Birmensdorf, Switzerland
Granier, A.; INRA, UMR EEF, Champenoux, France
Grossiord, C.; Earth and Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM, United States
Guyot, V.; INRA, UMR 1202 BIOGECO, Cestas, France, University Bordeaux, BIOGECO, UMR 1202, Pessac, France
Haase, J.; Faculty of Biology/Geobotany, University of Freiburg, Schänzlestr. 1, Freiburg, Germany, Institute for Terrestrial Ecosystems, Department of Environmental Systems Science, ETH Zurich, Universitaetsstrasse 16, Zurich, Switzerland, Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Zurich, Switzerland
Hättenschwiler, S.; Centre of Evolutionary and Functional Ecology (CEFE UMR 5175 – University of Montpellier – University Paul-Valery Montpellier – EPHE), 1919 route de Mende, Montpellier, France
Jactel, H.; INRA, UMR 1202 BIOGECO, Cestas, France, University Bordeaux, BIOGECO, UMR 1202, Pessac, France
Jaroszewicz, B.; Białowieża Geobotanical Station, Faculty of Biology, University of Warsaw, Białowieża, Poland
Joly, F.-X.; Centre of Evolutionary and Functional Ecology (CEFE UMR 5175 – University of Montpellier – University Paul-Valery Montpellier – EPHE), 1919 route de Mende, Montpellier, France
Kambach, S.; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, Leipzig, Germany, Institute of Biology/Geobotany and Botanical Garden, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, Halle (Saale), Germany, Department of Community Ecology, Helmholtz Centre for Environmental Research – UFZ, Theodor-Lieser-Straße 4, Halle, Germany
Kolb, S.; Forest Research Institute Baden Wuerttemberg, Wonnhaldestr.4, Freiburg im Breisgau, Germany
Koricheva, J.; School of Biological Sciences, Royal Holloway University of London, Surrey, Egham, United Kingdom
Liebersgesell, M.; Department of Systematic Botany and Functional Biodiversity, University of Leipzig, Johannisallee 21-23, Leipzig, Germany, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, Leipzig, Germany
Milligan, H.; School of Biological Sciences, Royal Holloway University of London, Surrey, Egham, United Kingdom
Müller, S.; Faculty of Biology/Geobotany, University of Freiburg, Schänzlestr. 1, Freiburg, Germany
Muys, B.; Department of Earth and Environmental Sciences, University of Leuven, Celestijnenlaan 200E Box 2411, Leuven, Belgium
Nguyen, D.; Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden, Department of Organismal Biology, Uppsala University, Uppsala, Sweden
Nock, C.; Faculty of Biology/Geobotany, University of Freiburg, Schänzlestr. 1, Freiburg, Germany, Faculty of Environment and Natural Resources, Chair of Silviculture, University of Freiburg, Fahnenbergplatz, Freiburg, Germany
Pollastrini, M.; Department of Agri-Food and Environmental Science (DISPAA), Laboratory of Environmental and Applied Botany, University of Firenze, Piazzale delle Cascine 28, Firenze, Italy
Purschke, O.; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, Leipzig, Germany
Radoglou, K.; Department of Forestry and Management of the Environment and Natural Resources, Democritus University of Thrace (DUTH), Pantazidou 193Nea Orestiada, Greece
Raulund-Rasmussen, K.; Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, Frederiksberg C, Denmark
Roger, F.; Department of Marine Sciences, University of Gothenburg, Carl Skottsbergs gata 22B, Göteborg, Sweden
Ruiz-Benito, P.; Grupo de Ecología y Restauración Forestal, Departamento de Ciencias de la Vida, Universidad de Alcalá, Edificio de Ciencias, Campus Universitario, Alcalá de Henares, Madrid, Spain
Seidl, R.; Institute of Silviculture, University of Natural Resources and Life Sciences (BOKU), Vienna, Austria
Selvi, F.; Department of Agri-Food and Environmental Science (DISPAA), Laboratory of Environmental and Applied Botany, University of Firenze, Piazzale delle Cascine 28, Firenze, Italy
Seiferling, I.; Centre de Recherche sur les Interactions Bassins Versants-Écosystèmes Aquatiques, Université du Québec, 3351 Boulevard des Forges, Trois-Rivières, QC, Canada, Senseable City Laboratory, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, United States
Stenlid, J.; Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden
Allan, E., Manning, P., Alt, F., Binkenstein, J., Blaser, S., Blüthgen, N. et al. (2015). Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett., 18, 834–843.
Baeten, L., Verheyen, K., Wirth, C., Bruelheide, H., Bussotti, F., Finér, L. et al. (2013). A novel comparative research platform designed to determine the functional significance of tree species diversity in European forests. Perspect. Plant Ecol. Evol. Syst., 15, 281–291.
Bauhus, J. & Schmerbeck, J. (2010). Silvicultural options to enhance and use forest plantation biodiversity. In: Ecosystem Goods and Services from Plant Forest (eds. Bauhus, J., der van Meer, P. & Kanninen, M.). Earthscan, London, UK, pp. 96–139.
Bauhus, J., Forrester, D.I., Gardiner, B., Jactel, H., Vallejo, R. & Pretzsch, H. (2017). Ecological stability of mixed-species forests. In: Mixed-Species Forests-Ecology and Management (ed. Pretzsch, H., Forrester, D.I. & Bauhus, J.). Springer-Verlag, Heidelberg, pp. 337–382.
Bell, A. & Jones, K., Pretzsch, H., Forrester, D.I. & Bauhus, J. (2015). Explaining fixed effects: random effects modeling of time-series cross-sectional and panel data. Polit. Sci. Res. Method, 3, 133–153.
Brady, N.C. & Weil, R.R. (2016). The nature and properties of soils, 15th edn. Pearson Education, Columbus.
Brassard, B.W., Chen, H.Y.H., Cavard, X., Yuan, Z., Reich, P.B., Bergeron, Y. et al. (2013). Tree species diversity increases fine root productivity through increased soil volume filling. J. Ecol., 101, 210–219.
Byrnes, J.E.K., Gamfeldt, L., Isbell, F., Lefcheck, J.S., Griffin, J.N., Hector, A. et al. (2014). Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol. Evol., 5, 111–124.
Cardinale, B.J., Nelson, K. & Palmer, M.A. (2000). Linking species diversity to the functioning of ecosystems: on the importance of environmental context. Oikos, 91, 175–183.
Cardinale, B.J., Gross, K., Fritschie, K., Flombaum, P., Fox, J.W., Rixen, C. et al. (2013). Biodiversity simultaneously enhances the production and stability of community biomass, but the effects are independent. Ecology, 94, 1697–1707.
Castagneyrol, B., Jactel, H., Vacher, C., Brockerhoff, E.G. & Koricheva, J. (2014). Effects of plant phylogenetic diversity on herbivory depend on herbivore specialization. J. Appl. Ecol., 51, 134–141.
Chesson, P. (2000). General theory of competitive coexistence in spatially-varying environments. Theor. Popul. Biol., 58, 211–237.
Cleland, E.E., Chuine, I., Menzel, A., Mooney, H.A. & Schwartz, M.D. (2007). Shifting plant phenology in response to global change. Trends Ecol. Evol., 22, 357–365.
Comita, L.S., Muller-Landau, H.C., Aguilar, S. & Hubbell, S.P. (2010). Asymmetric density dependence shapes species abundances in a tropical tree community. Science, 329, 330–332.
Dawud, S.M., Raulund-Rasmussen, K., Ratcliffe, S., Domisch, T., Finér, L., Joly, F.-X. et al. (2017). Tree species functional group is a more important driver of soil properties than tree species diversity across major European forest types. Funct. Ecol., 31, 1153–1162.
Díaz, S. & Cabido, M. (2001). Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol. Evol., 16, 646–655.
Dimitrakopoulos, P.G. & Schmid, B. (2004). Biodiversity effects increase linearly with biotope space. Ecol. Lett., 7, 574–583.
Dooley, Á., Isbell, F., Kirwan, L., Connolly, J., Finn, J.A. & Brophy, C. (2015). Testing the effects of diversity on ecosystem multifunctionality using a multivariate model. Ecol. Lett., 18, 1242–1251.
Forrester, D.I. (2014). The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process. For. Ecol. Manage., 312, 282–292.
Forrester, D.I. & Pretzsch, H. (2015). Tamm review: on the strength of evidence when comparing ecosystem functions of mixtures with monocultures. For. Ecol. Manage., 356, 41–53.
Forrester, D.I., Bonal, D., Dawud, S.M., Gessler, A., Granier, A., Pollastrini, M. et al. (2016). Drought responses by individual tree species are not often correlated with tree species diversity in European forests. J. Appl. Ecol., 53, 1725–1734.
Gamfeldt, L., Hillebrand, H. & Jonsson, P.R. (2008). Multiple functions increase the important of biodiversity for overall ecosystem functioning. Ecology, 89, 1223–1231.
Gamfeldt, L., Snäll, T., Bagchi, R., Jonsson, M., Gustafsson, L., Kjellander, P. et al. (2013). Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun., 4, 1–8.
Gelman, A. & Hill, J. (2007). Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press, New York.
Granier, A., Bréda, N., Biron, P. & Villette, S. (1999). A lumped water balance model to evaluate duration and intesity of drought constraints in forest stands. Ecol. Model., 116, 269–283.
Grossiord, C., Granier, A., Ratcliffe, S., Bouriaud, O., Bruelheide, H., Chećko, E. et al. (2014). Tree diversity does not always improve resistance of forest ecosystems to drought. Proc. Natl Acad. Sci. U. S. A., 111, 14812–14815.
Guyot, V., Castagneyrol, B., Vialatte, A., Deconchat, M. & Jactel, H. (2016). Tree diversity reduces pest damage in mature forests across Europe. Biol. Lett., 12, 20151037.
Handa, I.T., Aerts, R., Berendse, F., Berg, M.P., Bruder, A., Butenschoen, O. et al. (2014). Consequences of biodiversity loss for litter decomposition across biomes. Nature, 509, 218–221.
Hättenschwiler, S., Tiunov, A. & Scheu, S. (2005). Biodiversity and litter deomposition in terrestrial ecosystems. Annu. Rev. Ecol. Evol., 36, 191–218.
Hector, A., Bell, T., Hautier, Y., Isbell, F., Kéry, M., Reich, P.B. et al. (2011). BUGS in the analysis of biodiversity experiments: species richness and composition are of similar importance for grassland productivity. PLoS ONE, 6, e17434.
Hooper, D.U. & Vitousek, P.M. (1998). Effects of plant composition and diversity on nutrient cycling. Ecol. Monogr., 68, 121–149.
Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S. et al. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr., 75, 3–35.
Jacob, D., Petersen, J., Eggert, B., Alias, A., Christensen, O.B., Bouwer, L.M. et al. (2014). EURO-CORDEX: new high-resolution climate change projections for European impact research. Reg. Environ. Chang., 14, 563–578.
Jactel, H., Bauhus, J., Boberg, J., Bonal, D., Castagneyrol, B., Gardiner, B. et al. (2017). Tree diversity drives forest stand resistance to natural disturbances. Curr. For. Rep., 3, 223–243.
Jucker, T., Bouriaud, O., Avacaritei, D. & Coomes, D.A. (2014). Stabilizing effects of diversity on aboveground wood production in forest ecosystems: linking patterns and processes. Ecol. Lett., 17, 1560–1569.
Jucker, T., Bouriaud, O. & Coomes, D.A. (2015). Crown plasticity enables trees to optimize canopy packing in mixed-species forests. Funct. Ecol., 29, 1078–1086.
Jucker, T., Avăcăriței, D., Bărnoaiea, I., Duduman, G., Bouriaud, O. & Coomes, D.A. (2016). Climate modulates the effects of tree diversity on forest productivity. J. Ecol., 104, 388–398.
Knoke, T., Ammer, C., Stimm, B. & Mosandl, R. (2008). Admixing broadleaved to coniferous tree species: a review on yield, ecological stability and economics. Eur. J. For. Res., 127, 89–101.
Liang, J., Crowther, T.W., Picard, N., Wiser, S., Zhou, M., Alberti, G. et al. (2016). Positive biodiversity–productivity relationship predominant in global forests. Science, 354, aaf8957.
Loreau, M., Mouquet, N. & Gonzalez, A. (2003). Biodiversity as spatial insurance in heterogeneous landscapes. Proc. Natl Acad. Sci. U. S. A., 100, 12765–12770.
Pacala, S.W. & Tilman, D. (1994). Limiting similarity in mechanistic and spatial models of plant competition in heterogeneous environments. Am. Nat., 143, 222–257.
Paquette, A. & Messier, C. (2011). The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob. Ecol. Biogeogr., 20, 170–180.
Pavoine, S. & Bonsall, M.B. (2011). Measuring biodiversity to explain community assembly: a unified approach. Biol. Rev. Camb. Philos. Soc., 86, 792–812.
van der Plas, F., Manning, P., Allen, E., Scherer-Lorenzen, M., Verheyen, K., Wirth, C. et al. (2016). ‘Jack-of-all-trades’ effects drive biodiversity-ecosystem multifunctionality relationships. Nat. Commun., 7, 11109.
Pretzsch, H., Bielak, K., Block, J., Bruchwald, A., Dieler, J., Ehrhart, H.-P. et al. (2013a). Productivity of mixed versus pure stands of oak (Quercus petraea (Matt.) Liebl. and Quercus robur L.) and European beech (Fagus sylvatica L.) along an ecological gradient. Eur. J. For. Res., 132, 263–280.
Pretzsch, H., Schütze, G. & Uhl, E. (2013b). Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biol., 15, 483–495.
Pretzsch, H., Biber, P., Schütze, G., Uhl, E. & Rötzer, T. (2014). Forest stand growth dynamics in Central Europe have accelerated since 1870. Nat. Commun., 5, 4967.
Ratcliffe, S., Liebergesell, M., Ruiz Benito, P., Madrigal González, J., Muñoz Castañeda, J.M., Kändler, G. et al. (2016). Modes of functional biodiversity control on tree productivity across the European continent. Glob. Ecol. Biogeogr., 25, 251–262.
Richards, A.E., Forrester, D.I., Bauhus, J. & Scherer-Lorenzen, M. (2010). The influence of mixed tree plantations on the nutrition of individual species: a review. Tree Physiol., 30, 1192–1208.
Ruiz-Benito, P., Ratcliffe, S., Jump, A.S., Gómez-Aparicio, L., Madrigal-González, J., Wirth, C. et al. (2017). Functional diversity underlies demographic responses to environmental variation in European forests. Glob. Ecol. Biogeogr., 26, 128–141.
Sapijanskas, J., Paquette, A., Potvin, C., Kunert, N. & Loreau, M. (2014). Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences. Ecology, 95, 2479–2492.
Seddon, A.W., Macias-Fauria, M., Long, P.R., Benz, D. & Willis, K.J. (2016). Sensitivity of global terrestrial ecosystems to climate variability. Nature, 531, 229–232.
Soliveres, S., van der Plas, F., Manning, P., Prati, D., Gossner, M.M., Renner, S.C. et al. (2016). Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature, 536, 456–459.
Spasojevic, M.J., Bahlai, C.A., Bradley, B.A., Butterfield, B.J., Tuanmu, M.N., Sistla, S. et al. (2016). Scaling up the diversity-resilience relationship with trait databases and remote sensing data: the recovery of productivity after wildfire. Glob. Chang. Biol., 22, 1421–1432.
Srivastava, D.S. & Vellend, M. (2005). Biodiversity-ecosystem function research: is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst., 36, 267–294.
Stahl, U., Kattge, J., Reu, B., Voigt, W., Ogle, K., Dickie, J. et al. (2013). Whole-plant trait spectra of North American woody plant species reflect fundamental ecological strategies. Ecosphere, 4, 1–28.
Stan Development Team (2016). RStan: the R interface to Stan. R package version 2.14.1. http://mc-stan.org/.
Stephenson, N.L. (1998). Actual evapotranspiration and deficit: biologically meaningful correlates of vegetation distribution across spatial scales. J. Biogeogr., 25, 855–870.
Tobner, C.M., Paquette, A., Reich, P.B., Gravel, D. & Messier, C. (2014). Advancing biodiversity-ecosystem functioning science using high-density tree-based experiments over functional diversity gradients. Oecologia, 174, 609–621.
Toïgo, M., Vallet, P., Perot, T., Bontemps, J.-D., Piedallu, C. & Courbaud, B. (2015). Over-yielding in mixed forests decreases with site productivity. J. Ecol., 103, 502–512.
Wacker, L., Baudois, O., Eichenberger-Glinz, S. & Schmid, B. (2008). Environmental heterogeneity increases complementarity in experimental grassland communities. Basic Appl. Ecol., 9, 467–474.
Westoby, M., Falster, D.S., Moles, A.T., Vesk, P.A. & Wright, I.J. (2002). Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Syst., 33, 125–159.