Traditional approaches in trait-based community ecology typically expect that trait filtering across broad environmental gradients is largely due to replacement of species, rather than intraspecific trait adjustments. Recently, the role of intraspecific trait variability has been largely highlighted as an important contributor mediating the ability of communities to persist under changing conditions and determining the community-level trait variation, particularly across limited environmental gradients. Unfortunately, few studies quantify the relative importance of species turnover versus intraspecific variability mediating the response of communities different from vascular plants. Here, we studied the functional changes in epiphytic lichen communities within 23 beech forests across large latitudinal (ca. 3,000 km) and environmental gradients in Europe to quantify the relative contribution of species turnover and intraspecific variability and the role of climate controlling community-level trait changes. For 58 lichen species, we focused on a set of 10 quantitative functional traits potentially affected by climatic conditions and related to photosynthetic performance (n = 1,184 thalli), water use strategy (n = 1,018 thalli), and nutrient uptake (n = 1,179 thalli). Our results showed that intraspecific trait variability explained most of the functional changes in lichen communities in response to the latitudinal gradient. Further, such functional changes were determined by the covariation between intraspecific trait variability and species turnover, which varied in sign depending on the trait considered. Finally, different climatic predictors explained functional variation due to both intraspecific trait variability and species turnover. We propose that lichen communities cope with contrasting climatic conditions by adjusting the functional trait values of the most abundant species within the communities rather than by the replacement of the species. Consequently, intraspecific variability should be explicitly incorporated to understand the effect of environmental changes on lichen communities, even over large environmental variations, better. Our results challenge the universality of the hypothesis that species turnover chiefly drives functional trait changes across large environmental gradients and call for a wider test of such important assumptions in trait ecology in different organism types and ecosystems.

Área de Biodiversidad y Conservación Departamento de Biología Geología Física y Química Inorgánica ESCET Universidad Rey Juan Carlos c Tulipán s n 28933 Móstoles Spain

Centro de Investigaciones sobre Desertificación Carretera Moncada Náquera km 4 5 46113 Valencia Spain

Department of Botany Faculty of Sciences University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

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Albert, C. H., W. Thuiller, N. G. Yoccoz, R. Douzet, S. Aubert, and S. Lavorel. 2010. A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Functional Ecology 24:1192-1201.

Aragón, G., I. Martínez, and A. García. 2012. Loss of epiphytic diversity across a latitudinal gradient in southern Europe. Science of Total Environment 426:188-195.

Asplund, J., and D. A. Wardle. 2014. Within-species variability is the main driver of community-level responses of traits of epiphytes across a long-term chronosequence. Functional Ecology 28:1513-1522.

Auger, S., and B. Shipley. 2013. Inter-specific and intra-specific trait variation across short environmental gradients in an old-growth temperate forest. Journal of Vegetation Science 24:419-428.

Barnes, J. D., L. Balaguer, E. Manrique, S. Elvira, and A. W. Davison. 1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32:85-100.

Baselga, A. 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography 19:134-143.

Baselga, A., and C. D. L. Orme. 2012. betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution 3:808-812.

Belluau, M., and B. Shipley. 2018. Linking hard and soft traits: Physiology, morphology and anatomy interact to determine habitat affinities to soil water availability in herbaceous dicots. PLoS ONE 13:1-15.

Björklund, M., E. Ranta, V. Kaitala, L. A. Bach, P. Lundberg, and N. C. Stenseth. 2009. Quantitative trait evolution and environmental change. PLoS ONE 4:4521.

Cardós, J. L. H., M. Prieto, M. Jylhä, G. Aragón, M. C. Molina, I. Martínez, and J. Rikkinen. 2019. A case study on the re-establishment of the cyanolichen symbiosis: where do the compatible photobionts come from? Annals of Botany 124:379-388.

Carvajal, D. E., A. P. Loayza, R. S. Rios, C. A. Delpiano, and F. A. Squeo. 2018. A hyper-arid environment shapes an inverse pattern of the fast-slow plant economics spectrum for above-, but not below-ground resource acquisition strategies. Journal of Ecology 107:1079-1092.

Clauzade, G., and C. Roux. 1985. Likenoj de Okcidenta Europa. Ilustrita determinlibro. Bulletin de la Société Botanique du Centre-Ouest 7:1-893.

Cornelissen, J. H. C., S. I. Lang, N. A. Soudzilovskaia, and H. J. During. 2007. Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany 99:987-1001.

de Bello, F., et al. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiversity and Conservation 19:2873-2893.

de Bello, F., S. Lavorel, S. Lavergne, C. H. Albert, I. Boulangeat, F. Mazel, and W. Thuiller. 2013. Hierarchical effects of environmental filters on the functional structure of plant communities: a case study in the French Alps. Ecography 36:393-402.

Dĺaz, S. and M. Cabido. 2001. Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology & Evolution 16:646-655.

Ellis, C. J. 2012. Lichen epiphyte diversity: a species, community and trait-based review. Perspectives in Plant Ecology, Evolution and Systematics 14:131-152.

Fridley, J. D., and J. P. Grime. 2010. Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity. Ecology 91:2272-2283.

Garcia-Raventós, A., A. Viza, J. M. Tierno de Figueroa, J. L. Riera, and C. Múrria. 2017. Seasonality, species richness and poor dispersion mediate intraspecific trait variability in stonefly community responses across an elevational gradient. Freshwater Biology 62:916-928.

Garnier, E., G. Laurent, A. Bellmann, S. Debian, P. Berthelier, B. Ducout, and M. L. Navas. 2001. Consistency of species ranking based on functional leaf traits. New Phytologist 152:69-83.

Gauslaa, Y. 2014. Rain, dew, and humid air as drivers of morphology, function and spatial distribution in epiphytic lichens. Lichenologist 46:1-16.

Gauslaa, Y., and D. Coxson. 2011. Interspecific and intraspecific variations in water storage in epiphytic old forest foliose lichens. Botany-Botanique 89:787-798.

Giordani, P., G. Brunialti, G. Bacaro, and J. Nascimbene. 2012. Functional traits of epiphytic lichens as potential indicators of environmental conditions in forest ecosystems. Ecological Indicators 18:413-420.

Honegger, R. 2003. The impact of different long-term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biology 5:324-330.

Johansson, O., A. Nordin, J. Olofsson, and K. Palmqvist. 2010. Responses of epiphytic lichens to an experimental whole-tree nitrogen-deposition gradient. New Phytologist 4:1075-1084.

Karger, D. N., O. Conrad, J. Böhner, T. Kawohl, H. Kreft, R. Soria-Auza, N. E. Zimmerman, H. P. Linder, and M. Kessler. 2017. Climatologies at high resolution for the earth’s land surface areas. Scientific Data 4:1-20.

Kichenin, E., D. A. Wardle, D. A. Peltzer, C. W. Morse, and G. T. Freschet. 2013. Contrasting effects of plant inter- and intraspecific variation on community-level trait measures across an environmental gradient. Functional Ecology 27:1254-1261.

Kimball, S., A. L. Angert, T. E. Huxman, and D. L. Venable. 2010. Contemporary climate change in the Sonoran Desert favors cold-adapted species. Global Change Biology 16:1555-1565.

Kumordzi, B. B., D. A. Wardle, and G. T. Freschet. 2014. Plant assemblages do not respond homogenously to local variation in environmental conditions: functional responses differ with species identity and abundance. Journal of Vegetation Science 26:32-45.

Laliberté, E., and P. Legendre. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299-305.

Lepš, J., F. de Bello, P. Šmilauer, and J. Doležal. 2011. Community trait response to environment: disentangling species turnover vs intraspecific trait variability effects. Ecography 34:856-863.

Liu, G. F., X. H. Ye, Z. Y. Huang, and J. H. C. Cornelissen. 2019. Leaf and root nutrient concentrations and stoichiometry across aridity and soil fertility gradients. Journal of Vegetation Science 30:291-300.

Marks, C. O. 2007. The causes of variation in tree seedling traits: the roles of environmental selection versus chance. Evolution 61:455-469.

Matos, P., P. Pinho, G. Aragón, I. Martínez, A. Nunes, A. M. V. M. Soares, and C. Branquinho. 2015. Lichen traits responding to aridity. Journal of Ecology 103:451-458.

Merinero, S., O. Hilmo, and Y. Gauslaa. 2014. Size is a main driver for hydration traits in cyano- and cephalolichens of boreal rainforest canopies. Fungal Ecology 7:59-66.

Moretti, M., et al. 2017. Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits. Functional Ecology 37:558-567.

Palmqvist, K., D. Campbell, A. Ekblad, and H. Johansson. 1998. Photosynthetic capacity in relation to nitrogen content and its partitioning in lichens with different photobionts. Plant, Cell and Environment 21:361-372.

Palmqvist, K., and B. Sundberg. 2000. Light use efficiency of dry matter gain in five macrolichens: relative impact of microclimate conditions and species-specific traits. Plant, Cell and Environment 23:1-14.

Pinho, P., T. Dias, C. Cruz, Y. Sim Tang, M. A. Sutton, M. A. Martins-Loução, C. Máguas, and C. Branquinho. 2011. Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. Journal of Applied Ecology 48:1107-1116.

Poorter, H., Ü. Niinemets, L. Poorter, I. J. Wright, and R. Villar. 2009. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182:565-588.

Prentice, I. C., W. Cramer, S. P. Harrison, R. Leemans, R. A. Monserud, and A. M. Solomon. 1992. Special Paper: a global biome model based on plant physiology and dominance, soil properties and climate. Journal of Biogeography 19:117-134.

Prieto, M., I. Martínez, G. Aragón, and M. Verdú. 2017. Phylogenetic and functional structure of lichen communities under contrasting environmental conditions. Journal of Vegetation Science 28:871-881.

R Development Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.r-project.org

Roos, R. E., K. van Zuijlen, T. Birkemoe, K. Klanderud, S. I. Lang, S. Bokhorst, D. A. Wardle, and J. Asplund. 2019. Contrasting drivers of community-level trait variation for vascular plants, lichens and bryophytes across an elevational gradient. Functional Ecology 33:2430-2446.

Shipley, B., F. de Bello, J. H. C. Cornelissen, E. Laliberté, D. C. Laughlin, and P. B. Reich. 2016. Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180:923-931.

Siefert, A., et al. 2015. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters 18:1406-1419.

Smith, C. W., A. Aptroot, B. J. Coppins, A. Fletcher, O. L. Gilbert, P. W. James, and P. A. Wolseley. 2009. The lichens of Great Britain and Ireland. Second edition. The British Lichen Society, Department of Botany, The Natural History Museum, London, UK.

Webb, C. T., J. A. Hoeting, G. M. Ames, M. I. Pyne, and N. LeRoy Poff. 2010. A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecology Letters 13:267-283.

Wellburn, A. R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144:307-313.

Wright, I. J., et al. 2004. The worldwide leaf economics spectrum. Nature 428:821-827.