Plant communities are being exposed to changing environmental conditions all around the globe, leading to alterations in plant diversity, community composition, and ecosystem functioning. For herbaceous understorey communities in temperate forests, responses to global change are postulated to be complex, due to the presence of a tree layer that modulates understorey responses to external pressures such as climate change and changes in atmospheric nitrogen deposition rates. Multiple investigative approaches have been put forward as tools to detect, quantify and predict understorey responses to these global-change drivers, including, among others, distributed resurvey studies and manipulative experiments. These investigative approaches are generally designed and reported upon in isolation, while integration across investigative approaches is rarely considered. In this study, we integrate three investigative approaches (two complementary resurvey approaches and one experimental approach) to investigate how climate warming and changes in nitrogen deposition affect the functional composition of the understorey and how functional responses in the understorey are modulated by canopy disturbance, that is, changes in overstorey canopy openness over time. Our resurvey data reveal that most changes in understorey functional characteristics represent responses to changes in canopy openness with shifts in macroclimate temperature and aerial nitrogen deposition playing secondary roles. Contrary to expectations, we found little evidence that these drivers interact. In addition, experimental findings deviated from the observational findings, suggesting that the forces driving understorey change at the regional scale differ from those driving change at the forest floor (i.e., the experimental treatments). Our study demonstrates that different approaches need to be integrated to acquire a full picture of how understorey communities respond to global change.

Białowieża Geobotanical Station Faculty of Biology University of Warsaw Białowieża Poland

Botany Department School of Natural Sciences Trinity College Dublin Dublin Ireland

Department of Botany Faculty of Biological Sciences University of Wrocław Wrocław Poland

Department of Botany Faculty of Science Palacký University in Olomouc Olomouc Czech Republic

Department of Botany University of Wisconsin Madison Madison Wisconsin USA

Department of Plant Sciences University of Oxford Oxford UK

Department of Plant Systematics Ecology and Theoretical Biology ELTE Eötvös Loránd University Budapest Hungary

Department Silviculture and Forest Ecology of the Temperate Zones University of Göttingen Göttingen Germany

Division of Forest Nature and Landscape Department of Earth and Environmental Sciences KU Leuven Leuven Belgium

Environment Agency Austria Vienna Austria

Faculty of Biology University of Latvia Riga Latvia

Faculty of Environmental Sciences Czech University of Life Sciences Prague Czech Republic

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Prague Czech Republic

Forest and Nature Lab Department of Environment Ghent University Melle Belgium

Forest Ecology and Forest Management Group Wageningen University and Research Wageningen The Netherlands

Forest Research Institute Raszyn Poland

General Botany Institute for Biochemistry and Biology University of Potsdam Potsdam Germany

German Centre for Integrative Biodiversity Research Leipzig Germany

Institute of Biology University of Rzeszów Rzeszów Poland

Institute of Botany Czech Academy of Sciences Brno Czech Republic

Institute of Botany Czech Academy of Sciences Průhonice Czech Republic

Institute of Ecology and Evolution Friedrich Schiller University Jena Jena Germany

Institute of Ecology Leuphana University Lüneburg Lüneburg Germany

Jules Verne University of Picardie Amiens France

Laboratoire ecosystèmes et sociétés en montagne St Martin d'Hères France

Leibniz Centre for Agricultural Landscape Research Müncheberg Germany

Museum of Natural History Faculty of Biological Sciences University of Wrocław Wrocław Poland

Research Institute for Nature and Forest Brussels Belgium

Swedish University of Agricultural Sciences Southern Swedish Forest Research Centre Lomma Sweden

Technical University in Zvolen Zvolen Slovakia

The UWA Institute of Agriculture The University of Western Australia Perth Western Australia Australia

UK Centre for Ecology and Hydrology Bangor UK

UK Centre for Ecology and Hydrology Lancaster University Bailrigg UK

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Axmanová, I., Zelený, D., Li, C., & Chytrý, M. (2011). Environmental factors influencing herb layer productivity in Central European oak forests: Insights from soil and biomass analyses and a phytometer experiment. Plant and Soil, 342, 183-194. https://doi.org/10.1007/s11104-010-0683-9

Baeten, L., Hermy, M., & Verheyen, K. (2009). Environmental limitation contributes to the differential colonization capacity of two forest herbs. Journal of Vegetation Science, 20(2), 209-223. https://doi.org/10.1111/j.1654-1103.2009.05595.x

Baeten, L., Verheyen, K., Wirth, C., Bruelheide, H., Bussotti, F., Finér, L., Jaroszewicz, B., Selvi, F., Valladares, F., Allan, E., Ampoorter, E., Auge, H., Avǎcǎriei, D., Barbaro, L., Bǎrnoaiea, I., Bastias, C. C., Bauhus, J., Beinhoff, C., Benavides, R., … Scherer-Lorenzen, M. (2013). A novel comparative research platform designed to determine the functional significance of tree species diversity in European forests. Perspectives in Plant Ecology, Evolution and Systematics, 15(5), 281-291. https://doi.org/10.1016/j.ppees.2013.07.002

Bates, D., Mächler, M., Bolker, M. B., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01

Bjorkman, A. D., Myers-Smith, I. H., Elmendorf, S. C., Normand, S., Rüger, N., Beck, P. S. A., Blach-Overgaard, A., Blok, D., Cornelissen, J. H. C., Forbes, B. C., Georges, D., Goetz, S. J., Guay, K. C., Henry, G. H. R., HilleRisLambers, J., Hollister, R. D., Karger, D. N., Kattge, J., Manning, P., … Weiher, E. (2018). Plant functional trait change across a warming tundra biome. Nature, 562(7725), 57-62. https://doi.org/10.1038/s41586-018-0563-7

Blondeel, H., Perring, M. P., Depauw, L., De Lombaerde, E., Landuyt, D., De Frenne, P., & Verheyen, K. (2020). Light and warming drive forest understorey community development in different environments. Global Change Biology, 26(3), 1681-1696. https://doi.org/10.1111/gcb.14955

Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J. W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., & De Vries, W. (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity: A synthesis. Ecological Applications, 20(1), 30-59. https://doi.org/10.1890/08-1140.1

Chelli, S., Simonetti, E., Wellstein, C., Campetella, G., Carnicelli, S., Andreetta, A., Giorgini, D., Puletti, N., Bartha, S., & Canullo, R. (2019). Effects of climate, soil, forest structure and land use on the functional composition of the understory in Italian forests. Journal of Vegetation Science, 30(6), 1110-1121. https://doi.org/10.1111/jvs.12792

De Frenne, P., De Schrijver, A., Graae, B. J., Gruwez, R., Tack, W., Vandelook, F., Hermy, M., & Verheyen, K. (2010). The use of open-top chambers in forests for evaluating warming effects on herbaceous understorey plants. Ecological Research, 25(1), 163-171. https://doi.org/10.1007/s11284-009-0640-3

De Frenne, P., Rodríguez-Sánchez, F., Coomes, D. A., Baeten, L., Verstraeten, G., Vellend, M., Bernhardt-Römermann, M., Brown, C. D., Brunet, J., Cornelis, J., Decocq, G. M., Dierschke, H., Eriksson, O., Gilliam, F. S., Hédl, R., Heinken, T., Hermy, M., Hommel, P., Jenkins, M. A., … Verheyen, K. (2013). Microclimate moderates plant responses to macroclimate warming. PNAS, 110(46), 18561-18565. https://doi.org/10.1073/pnas.1311190110

De Frenne, P., Rodríguez-Sánchez, F., De Schrijver, A., Coomes, D. A., Hermy, M., Vangansbeke, P., & Verheyen, K. (2015). Light accelerates plant responses to warming. Nature Plants, 1(9), 15110. https://doi.org/10.1038/nplants.2015.110

De Lombaerde, E., Baeten, L., Verheyen, K., Perring, M. P., Ma, S., & Landuyt, D. (2021). Understorey removal effects on tree regeneration in temperate forests: A meta-analysis. Journal of Applied Ecology, 58(1), 9-20. https://doi.org/10.1111/1365-2664.13792

De Pauw, K., Sanczuk, P., Meeussen, C., Depauw, L., De Lombaerde, E., Govaert, S., Vanneste, T., Brunet, J., Cousins, S. A. O., Gasperini, C., Hedwall, P., Iacopetti, G., Lenoir, J., Plue, J., Selvi, F., Spicher, F., Uria-Diez, J., Verheyen, K., Vangansbeke, P., & De Frenne, P. (2022). Forest understorey communities respond strongly to light in interaction with forest structure, but not to microclimate warming. New Phytologist, 233(1), 219-235. https://doi.org/10.1111/nph.17803

Depauw, L., Perring, M. P., Landuyt, D., Maes, S. L., Blondeel, H., De Lombaerde, E., Brūmelis, G., Brunet, J., Closset-Kopp, D., Czerepko, J., Decocq, G., Den Ouden, J., Gawryś, R., Härdtle, W., Hédl, R., Heinken, T., Heinrichs, S., Jaroszewicz, B., Kopecký, M., … Verheyen, K. (2020). Light availability and land-use history drive biodiversity and functional changes in forest herb layer communities. Journal of Ecology, 108(4), 1411-1425. https://doi.org/10.1111/1365-2745.13339

Ellenberg, H., Weber, H. E., Düll, R., Wirth, V., & Werner, W. (2001). Zeigerwerte van Pflanzen in Mitteleuropa. Scripta Geobotanica, 18, 1-262.

Erisman, J. W., & Draaijers, G. (2003). Deposition to forests in Europe: Most important factors influencing dry deposition and models used for generalisation. Environmental Pollution, 124(3), 379-388. https://doi.org/10.1016/S0269-7491(03)00049-6

Fischer, M., Bossdorf, O., Gockel, S., Hänsel, F., Hemp, A., Hessenmöller, D., Korte, G., Nieschulze, J., Pfeiffer, S., Prati, D., Renner, S., Schöning, I., Schumacher, U., Wells, K., Buscot, F., Kalko, E. K. V., Linsenmair, K. E., Schulze, E. D., & Weisser, W. W. (2010). Implementing large-scale and long-term functional biodiversity research: The Biodiversity Exploratories. Basic and Applied Ecology, 11(6), 473-485. https://doi.org/10.1016/j.baae.2010.07.009

Gilliam, F. S. (2006). Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. Journal of Ecology, 94(6), 1176-1191. https://doi.org/10.1111/j.1365-2745.2006.01155.x

Gilliam, F. S. (2007). The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience, 57(10), 845-858. https://doi.org/10.1641/B571007

Gilliam, F. S., Welch, N. T., Phillips, A. H., Billmyer, J. H., Peterjohn, W. T., Fowler, Z. K., Walter, C. A., Burnham, M. B., May, J. D., & Adams, M. B. (2016). Twenty-five-year response of the herbaceous layer of a temperate hardwood forest to elevated nitrogen deposition. Ecosphere, 7(4), 1-16. https://doi.org/10.1002/ecs2.1250

Hedwall, P. O., Uria-Diez, J., Brunet, J., Gustafsson, L., Axelsson, A. L., & Strengbom, J. (2021). Interactions between local and global drivers determine long-term trends in boreal forest understorey vegetation. Global Ecology and Biogeography, 30(9), 1765-1780. https://doi.org/10.1111/geb.13324

Heinrichs, S., Bernhardt-Römermann, M., & Schmidt, W. (2010). The estimation of aboveground biomass and nutrient pools of understorey plants in closed Norway spruce forests and on clearcuts. European Journal of Forest Research, 129(4), 613-624. https://doi.org/10.1007/s10342-010-0362-7

Hermy, M. (1985). Ecologie en fytosociologie van oude en jonge bossen in binnen-Vlaanderen. University of Ghent.

Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1-26. https://doi.org/10.18637/JSS.V082.I13

Lai, M., He, S., Yu, S., & Jin, G. (2018). Effects of experimental N addition on plant diversity in an growth temperate forest. Ecology and Evolution, 8(11), 5900-5911. https://doi.org/10.1002/ece3.4127

Landuyt, D., De Lombaerde, E., Perring, M. P., Hertzog, L. R., Ampoorter, E., Maes, S. L., De Frenne, P., Ma, S., Proesmans, W., Blondeel, H., Sercu, B. K., Wang, B., Wasof, S., & Verheyen, K. (2019). The functional role of temperate forest understorey vegetation in a changing world. Global Change Biology, 25(11), 3625-3641. https://doi.org/10.1111/gcb.14756

Landuyt, D., Maes, S. L., Depauw, L., Ampoorter, E., Blondeel, H., Perring, M. P., Brūmelis, G., Brunet, J., Decocq, G., den Ouden, J., Härdtle, W., Hédl, R., Heinken, T., Heinrichs, S., Jaroszewicz, B., Kirby, K. J., Kopecký, M., Máliš, F., Wulf, M., & Verheyen, K. (2020). Drivers of aboveground understorey biomass and nutrient stocks in temperate deciduous forests. Journal of Ecology, 108(3), 982-997. https://doi.org/10.1111/1365-2745.13318

Landuyt, D., Perring, M., Blondeel, H., De Lombaerde, E., Depauw, L., Lorer, E., Maes, S., & Verheyen, K. (2023). Changes in the functional composition of the understorey across European temperate forests, in relation to changes in canopy openness, changes in N deposition rates and climate warming. Figshare. Dataset. https://doi.org/10.6084/m9.figshare.24598458

Lemmon, P. E. (1956). A spherical densiometer for estimating forest overstory density. Forest Science, 2(4), 314-320. https://doi.org/10.1093/forestscience/2.4.314

Lüdecke, D. (2022). sjPlot: Data visualization for statistics in social science. https://cran.r-project.org/package=sjPlot

Luo, Y., Melillo, J., Niu, S., Beier, C., Clark, J. S., Classen, A. T., Davidson, E., Dukes, J. S., Evans, R. D., Field, C. B., Czimczik, C. I., Keller, M., KIimball, B. A., Kueppers, L. M., Norby, R. J., Pelini, S. L., Pendall, E., Rastetter, E., Six, J., … Torn, M. S. (2011). Coordinated approaches to quantify long-term ecosystem dynamics in response to global change. Global Change Biology, 17(2), 843-854. https://doi.org/10.1111/j.1365-2486.2010.02265.x

Maes, S. L., Blondeel, H., Perring, M. P., Depauw, L., Brūmelis, G., Brunet, J., Decocq, G., den Ouden, J., Härdtle, W., Hédl, R., Heinken, T., Heinrichs, S., Jaroszewicz, B., Kirby, K., Kopecký, M., Máliš, F., Wulf, M., & Verheyen, K. (2019). Litter quality, land-use history, and nitrogen deposition effects on topsoil conditions across European temperate deciduous forests. Forest Ecology and Management, 433, 405-418. https://doi.org/10.1016/j.foreco.2018.10.056

Malhi, Y., Franklin, J., Seddon, N., Solan, M., Turner, M. G., Field, C. B., & Knowlton, N. (2020). Climate change and ecosystems: Threats, opportunities and solutions. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1794), 20190104. https://doi.org/10.1098/rstb.2019.0104

Maskell, L. C., Smart, S. M., Bullock, J. M., Thompson, K., & Stevens, C. J. (2010). Nitrogen deposition causes widespread loss of species richness in British habitats. Global Change Biology, 16(2), 671-679. https://doi.org/10.1111/j.1365-2486.2009.02022.x

Mazalla, L., & Diekmann, M. (2022). Regression to the mean in vegetation science. Journal of Vegetation Science, 33(2), 1-8. https://doi.org/10.1111/jvs.13117

Parmesan, C., & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42. https://doi.org/10.1038/nature01286

Perring, M. P., Bernhardt-Römermann, M., Baeten, L., Midolo, G., Blondeel, H., Depauw, L., Landuyt, D., Maes, S. L., De Lombaerde, E., Carón, M. M., Vellend, M., Brunet, J., Chudomelová, M., Decocq, G., Diekmann, M., Dirnböck, T., Dörfler, I., Durak, T., De Frenne, P., … Verheyen, K. (2018). Global environmental change effects on plant community composition trajectories depend upon management legacies. Global Change Biology, 24(4), 1722-1740. https://doi.org/10.1111/gcb.14030

R Core Team. (2022). R: A language and environment for statistical computing. https://www.r-project.org/

Richard, B., Dupouey, J. L., Corcket, E., Alard, D., Archaux, F., Aubert, M., Boulanger, V., Gillet, F., Langlois, E., Macé, S., Montpied, P., Beaufils, T., Begeot, C., Behr, P., Boissier, J. M., Camaret, S., Chevalier, R., Decocq, G., Dumas, Y., … Lenoir, J. (2021). The climatic debt is growing in the understorey of temperate forests: Stand characteristics matter. Global Ecology and Biogeography, 30(7), 1474-1487. https://doi.org/10.1111/geb.13312

Rustad, L. E. (2008). The response of terrestrial ecosystems to global climate change: Towards an integrated approach. Science of the Total Environment, 404(2-3), 222-235. https://doi.org/10.1016/j.scitotenv.2008.04.050

Segar, J., Pereira, H., Baeten, L., Bernhardt-Römermann, M., De Frenne, P., Fernández, N., Gilliam, F., Lenoir, J., Ortmann-Ajkai, A., Verheyen, K., Waller, D., Teleki, B., Berki, I., Brunet, J., Chudomelová, M., Decocq, G., Dirnböck, T., Hédl, R., Heinken, T., … Staude, I. (2022). Divergent roles of herbivory in eutrophying forests. Nature Communications, 13, 7837. https://doi.org/10.1038/s41467-022-35282-6

Spicer, M. E., Mellor, H., & Carson, W. P. (2020). Seeing beyond the trees: A comparison of tropical and temperate plant growth forms and their vertical distribution. Ecology, 101(4), 1-9. https://doi.org/10.1002/ecy.2974

Staude, I. R., Waller, D. M., Bernhardt-Römermann, M., Bjorkman, A. D., Brunet, J., De Frenne, P., Hédl, R., Jandt, U., Lenoir, J., Máliš, F., Verheyen, K., Wulf, M., Pereira, H. M., Vangansbeke, P., Ortmann-Ajkai, A., Pielech, R., Berki, I., Chudomelová, M., Decocq, G., … Baeten, L. (2020). Replacements of small- by large-ranged species scale up to diversity loss in Europe's temperate forest biome. Nature Ecology and Evolution, 4(6), 802-808. https://doi.org/10.1038/s41559-020-1176-8

Stevens, J. T., Safford, H. D., Harrison, S., & Latimer, A. M. (2015). Forest disturbance accelerates thermophilization of understory plant communities. Journal of Ecology, 103(5), 1253-1263. https://doi.org/10.1111/1365-2745.12426

Strengbom, J., Näsholm, T., & Ericson, L. (2004). Light, not nitrogen, limits growth of the grass Deschampsia flexuosa in boreal forests. Canadian Journal of Botany, 82(4), 430-435. https://doi.org/10.1139/b04-017

Van Calster, H., Baeten, L., Verheyen, K., De Keersmaeker, L., Dekeyser, S., Rogister, J. E., & Hermy, M. (2008). Diverging effects of overstorey conversion scenarios on the understorey vegetation in a former coppice-with-standards forest. Forest Ecology and Management, 256(4), 519-528. https://doi.org/10.1016/j.foreco.2008.04.042

van de Waal, D. B., & Litchman, E. (2020). Multiple global change stressor effects on phytoplankton nutrient acquisition in a future ocean. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1798), 1-8. https://doi.org/10.1098/rstb.2019.0706

Vanneste, T., Valdés, A., Verheyen, K., Perring, M. P., Bernhardt-Römermann, M., Andrieu, E., Brunet, J., Cousins, S. A. O., Deconchat, M., De Smedt, P., Diekmann, M., Ehrmann, S., Heinken, T., Hermy, M., Kolb, A., Lenoir, J., Liira, J., Naaf, T., Paal, T., … De Frenne, P. (2019). Functional trait variation of forest understorey plant communities across Europe. Basic and Applied Ecology, 34, 1-14. https://doi.org/10.1016/j.baae.2018.09.004

Verheyen, K., Baeten, L., De Frenne, P., Bernhardt-Römermann, M., Brunet, J., Cornelis, J., Decocq, G., Dierschke, H., Eriksson, O., Hédl, R., Heinken, T., Hermy, M., Hommel, P., Kirby, K., Naaf, T., Peterken, G., Petřík, P., Pfadenhauer, J., Van Calster, H., … Verstraeten, G. (2012). Driving factors behind the eutrophication signal in understorey plant communities of deciduous temperate forests. Journal of Ecology, 100(2), 352-365. https://doi.org/10.1111/j.1365-2745.2011.01928.x

Verheyen, K., De Frenne, P., Baeten, L., Waller, D. M., Hédl, R., Perring, M. P., Blondeel, H., Brunet, J., Chudomelová, M., Decocq, G., De Lombaerde, E., Depauw, L., Dirnböck, T., Durak, T., Eriksson, O., Gilliam, F. S., Heinken, T., Heinrichs, S., Hermy, M., … Bernhardt-Römermann, M. (2017). Combining biodiversity resurveys across regions to advance global change research. Bioscience, 67(1), 73-83. https://doi.org/10.1093/biosci/biw150

Von Arx, G., Graf Pannatier, E., Thimonier, A., & Rebetez, M. (2013). Microclimate in forests with varying leaf area index and soil moisture: Potential implications for seedling establishment in a changing climate. Journal of Ecology, 101(5), 1201-1213. https://doi.org/10.1111/1365-2745.12121

von Liebig, J. (1855). Die Grundsätze der Agricultur-Chemie mit Rücksicht auf die in England angestellten Untersuchungen. Vieweg.

Westoby, M. (1998). A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil, 199(2), 213-227. https://doi.org/10.1023/A:1004327224729

Zellweger, F., Coomes, D., Lenoir, J., Depauw, L., Maes, S. L., Wulf, M., Kirby, K. J., Brunet, J., Kopecký, M., Máliš, F., Schmidt, W., Heinrichs, S., den Ouden, J., Jaroszewicz, B., Buyse, G., Spicher, F., Verheyen, K., & De Frenne, P. (2019). Seasonal drivers of understorey temperature buffering in temperate deciduous forests across Europe. Global Ecology and Biogeography, 28(12), 1774-1786. https://doi.org/10.1111/geb.12991

Zellweger, F., de Frenne, P., Lenoir, J., Vangansbeke, P., Verheyen, K., Bernhardt-Römermann, M., Baeten, L., Hédl, R., Berki, I., Brunet, J., van Calster, H., Chudomelová, M., Decocq, G., Dirnböck, T., Durak, T., Heinken, T., Jaroszewicz, B., Kopecký, M., Máliš, F., … Coomes, D. (2020). Forest microclimate dynamics drive plant responses to warming. Science, 368(6492), 772-775. https://doi.org/10.1126/science.aba6880

Zhang, S., Landuyt, D., Verheyen, K., & De Frenne, P. (2022). Tree species mixing can amplify microclimate offsets in young forest plantations. Journal of Applied Ecology, 59(6), 1428-1439. https://doi.org/10.1111/1365-2664.14158

Zhang, S., Verheyen, K., De Frenne, P., & Landuyt, D. (2022). Tree species mixing affects throughfall in a young temperate forest plantation. Agricultural and Forest Meteorology, 327, 109220. https://doi.org/10.1016/j.agrformet.2022.109220