bryophytes; buffering; community temperature index; ecological indicator values; forest flora; global warming; microclimate; plant community; thermophilization; vascular plants; Ecology; Plant Science
Abstract :
[en] Question: Ecological indicator values (EIVs) reflect species‘ optimal conditions on an environmental gradient, such as temperature. Averaged over a community, they are used to quantify thermophilization stemming from climate change, i.e. the reshuffling of communities toward more warm-adapted species. In forests, understorey plant communities do not keep up with global warming and accumulate a climatic debt. Although the causes are still debated, this thermal lag may be partly explained by forest microclimate buffering. For the first time, we test whether community means of EIVs are able to capture microclimate (here, under forest canopies) temperature across, or also within forests. Location: 157 forest plots across three French deciduous forests covering a large macroclimatic gradient. Methods: To assess whether EIVs can be used to infer the mean and range of microclimate temperature in forests, we measured understorey air temperature for ca. 1 year (10 months) with sensors located 1 m above the ground. We surveyed bryophytes and vascular plants within 400-m2 plots, and computed floristic temperature from ordinal-scale EIVs (Ellenberg, Julve) and degree-scale EIVs (ClimPlant, Bryophytes of Europe Traits) for both temperature and continentality, i.e. temperature annual range. Finally, we fitted linear models to assess whether EIVs could explain the mean and range of microclimate temperature in forests. Results: Vascular plant and bryophyte communities successfully reflected differences in mean annual temperatures across forests but largely failed to do so for microclimate variation within forests. Bryophytes did not perform better than vascular plants to infer microclimate conditions. The annual range of microclimate temperatures was poorly associated with ordinal-scale EIVs for continentality but was positively correlated with degree-scale EIVs for annual range within lowland forests, especially for vascular plant communities. Conclusion: Overall, the capabilities of EIVs to infer microclimate was inconsistent. Refined EIVs for temperature are needed to capture forest microclimates experienced by understorey species.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Gril, Eva ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Spicher, Fabien ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Vanderpoorten, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - Unité aCREA-Ulg (Conseils et Recherches en Ecologie Appliquée)
Vital, Germain; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Brasseur, Boris ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Gallet-Moron, Emilie ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Le Roux, Vincent ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Decocq, Guillaume ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Lenoir, Jonathan ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Marrec, Ronan ; UMR CNRS 7058 “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN), Université de Picardie Jules Verne, Amiens, France
Language :
English
Title :
Ecological indicator values of understorey plants perform poorly to infer forest microclimate temperature
We sincerely thank the interns who contributed to temperature data collection in the field, namely Hugo Mahier, Ambre Châline, Soline Chaudet and Hugo Hayé. We also thank the RENECOFOR network and the National Forest Office (ONF), especially all agents who helped with the project. Finally, we thank the editor Sabine Rumpf and two anonymous reviewers, for their suggestions that significantly clarified and improved our paper.JL acknowledges funding from the Agence Nationale de la Recherche (ANR), under the framework of the young investigators’ funding scheme (JCJC Grant N°ANR‐19‐CE32‐0005‐01: IMPRINT project), which funded EG's PhD, and the collaborative research program funding scheme (PRC Grant N°ANR‐21‐CE32‐0012‐03: MaCCMic project), as well as the Région Hauts‐de‐France, the Ministère de l'Enseignement Supérieur et de la Recherche and the European Fund for Regional Economic Development for their financial support to the CPER ECRIN program.
Aarssen, L.W., Schamp, B.S. & Pither, J. (2006) Why are there so many small plants? Implications for species coexistence. Journal of Ecology, 94, 569–580.
Ashcroft, M.B. & Gollan, J.R. (2012) Fine-resolution (25 m) topoclimatic grids of near-surface (5 cm) extreme temperatures and humidities across various habitats in a large (200 × 300 km) and diverse region. International Journal of Climatology, 32, 2134–2148.
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.
Becker Scarpitta, A., Bardat, J., Lalanne, A. & Vellend, M. (2017) Long-term community change: bryophytes are more responsive than vascular plants to nitrogen deposition and warming. Journal of Vegetation Science, 28, 1220–1229.
Becker-Scarpitta, A., Auberson-Lavoie, D., Aussenac, R. & Vellend, M. (2022) Different temporal trends in vascular plant and bryophyte communities along elevational gradients over four decades. Ecology and Evolution, 12, e9102.
Berg, C., Welk, E. & Jäger, E.J. (2017) Revising Ellenberg's indicator values for continentality based on global vascular plant species distribution. Applied Vegetation Science, 20, 482–493.
Bernhardt-Römermann, M., Poschlod, P. & Hentschel, J. (2018) BryForTrait—a life-history trait database of forest bryophytes. Journal of Vegetation Science, 29, 798–800.
Bertrand, R., Lenoir, J., Piedallu, C., Riofrío-Dillon, G., de Ruffray, P., Vidal, C. et al. (2011) Changes in plant community composition lag behind climate warming in lowland forests. Nature, 479, 517–520.
Bertrand, R., Riofrío-Dillon, G., Lenoir, J., Drapier, J., de Ruffray, P., Gégout, J.-C. et al. (2016) Ecological constraints increase the climatic debt in forests. Nature Communications, 7, 12643.
Borderieux, J., Gégout, J.-C. & Serra-Diaz, J.M. (2023) High landscape-scale forest cover favours cold-adapted plant communities in agriculture–forest mosaics. Global Ecology and Biogeography, 32, 893–903.
Bramer, I., Anderson, B.J., Bennie, J., Bladon, A.J., De Frenne, P., Hemming, D. et al. (2018) Advances in monitoring and modelling climate at ecologically relevant scales. In: Bohan, D.A., Dumbrell, A.J., Woodward, G. & Jackson, M. (Eds.) Advances in ecological research. Amsterdam, the Netherlands: Academic Press, pp. 101–161. Next Generation Biomonitoring: Part 1.
Bruelheide, H., Dengler, J., Purschke, O., Lenoir, J., Jiménez-Alfaro, B., Hennekens, S.M. et al. (2018) Global trait–environment relationships of plant communities. Nature Ecology & Evolution, 2, 1906–1917.
Christiansen, D.M., Iversen, L.L., Ehrlén, J. & Hylander, K. (2022) Changes in forest structure drive temperature preferences of boreal understorey plant communities. Journal of Ecology, 110, 631–643.
Chytrý, M., Hennekens, S.M., Jiménez-Alfaro, B., Knollová, I., Dengler, J., Jansen, F. et al. (2016) European Vegetation Archive (EVA): an integrated database of European vegetation plots. Applied Vegetation Science, 19, 173–180.
Chytrý, M., Tichý, L., Dřevojan, P., Sádlo, J. & Zelený, D. (2018) Ellenberg-type indicator values for the Czech flora. Preslia, 90, 83–103.
De Frenne, P., Lenoir, J., Luoto, M., Scheffers, B.R., Zellweger, F., Aalto, J. et al. (2021) Forest microclimates and climate change: importance, drivers and future research agenda. Global Change Biology, 27, 2279–2297.
De Frenne, P., Rodríguez-Sánchez, F., Coomes, D.A., Baeten, L., Verstraeten, G., Vellend, M. et al. (2013) Microclimate moderates plant responses to macroclimate warming. Proceedings of the National Academy of Sciences of the United States of America, 110, 18561–18565.
De Frenne, P. & Verheyen, K. (2016) Weather stations lack forest data. Science, 351, 234.
Delignette-Muller, M.L. & Dutang, C. (2015) Fitdistrplus: AnRPackage for fitting distributions. Journal of Statistical Software, 64.
Dengler, J., Jansen, F., Chusova, O., Hüllbusch, E., Nobis, M.P., Meerbeek, K.V. et al. (2023) Ecological Indicator Values for Europe (EIVE) 1.0. Vegetation Classification and Survey, 4, 7–29.
Depauw, L., Perring, M.P., Landuyt, D., Maes, S.L., Blondeel, H., Lombaerde, E.D. et al. (2021) Evaluating structural and compositional canopy characteristics to predict the light-demand-signature of the forest understorey in mixed, semi-natural temperate forests. Applied Vegetation Science, 24, e1253.
Diekmann, M. (2003) Species indicator values as an important tool in applied plant ecology—a review. Basic and Applied Ecology, 4, 493–506.
Dietz, L., Collet, C., Dupouey, J.-L., Lacombe, E., Laurent, L. & Gégout, J.-C. (2020) Windstorm-induced canopy openings accelerate temperate forest adaptation to global warming. Global Ecology and Biogeography, 29, 2067–2077.
Ellenberg, H. (1974) Indicator values of vascular plants in central Europe. Scripta Geobotanica, 9, 1–97.
Fenton, N.J. & Frego, K.A. (2005) Bryophyte (moss and liverwort) conservation under remnant canopy in managed forests. Biological Conservation, 122, 417–430.
Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315.
Furness, S.B. & Grime, J.P. (1982) Growth rate and temperature responses in bryophytes: II. A comparative study of species of contrasted ecology. Journal of Ecology, 70, 525–536.
Gégout, J.-C., Coudun, C., Bailly, G. & Jabiol, B. (2005) EcoPlant: a forest site database linking floristic data with soil and climate variables. Journal of Vegetation Science, 16, 257–260.
George, A.D., Thompson, F.R. & Faaborg, J. (2015) Using LiDAR and remote microclimate loggers to downscale near-surface air temperatures for site-level studies. Remote Sensing Letters, 6, 924–932.
Gottfried, M., Pauli, H., Futschik, A., Akhalkatsi, M., Barančok, P., Benito Alonso, J.L. et al. (2012) Continent-wide response of mountain vegetation to climate change. Nature Climate Change, 2, 111–115.
Govaert, S., Vangansbeke, P., Blondeel, H., Steppe, K., Verheyen, K. & Frenne, P.D. (2021) Rapid thermophilization of understorey plant communities in a 9 year-long temperate forest experiment. Journal of Ecology, 109, 2434–2447.
Gril, E., Spicher, F., Greiser, C., Ashcroft, M.B., Pincebourde, S., Durrieu, S. et al. (2023) Slope and equilibrium: a parsimonious and flexible approach to model microclimate. Methods in Ecology and Evolution, 14, 885–897.
Haesen, S., Lembrechts, J.J., De Frenne, P., Lenoir, J., Aalto, J., Ashcroft, M.B. et al. (2021) ForestTemp—sub-canopy microclimate temperatures of European forests. Global Change Biology, 27, 6307–6319.
Haesen, S., Lenoir, J., Gril, E., Frenne, P.D., Lembrechts, J., Kopecký, M. et al. (2023) Uncovering the hidden niche: incorporating microclimate temperature into species distribution models. https://doi.org/10.32942/X21600
He, X., He, K.S. & Hyvönen, J. (2016) Will bryophytes survive in a warming world? Perspectives in Plant Ecology, Evolution and Systematics, 19, 49–60.
Hutsemékers, V., Mouton, L., Westenbohm, H., Collart, F. & Vanderpoorten, A. (2023) Disentangling climate change from air pollution effects on epiphytic bryophytes. Global Change Biology, 29, 3990–4000.
Hylander, K., Jonsson, B.G. & Nilsson, C. (2002) Evaluating buffer strips along boreal streams using bryophytes as indicators. Ecological Applications, 12, 797–806.
Julve, P. (2015) Baseflor. Index Botanique, écologique et Chorologique de la Flore de France.
Käfer, J. & Witte, J.-P.M. (2004) Cover-weighted averaging of indicator values in vegetation analyses. Journal of Vegetation Science, 15, 647–652.
Karger, D.N., Conrad, O., Böhner, J., Kawohl, T., Kreft, H., Soria-Auza, R.W. et al. (2017) Climatologies at high resolution for the earth's land surface areas. Scientific Data, 4, 170122.
Kiebacher, T., Meier, M., Kipfer, T. & Roth, T. (2023) Thermophilisation of communities differs between land plant lineages, land use types and elevation. Scientific Reports, 13, 11395.
Kutnar, L., Kermavnar, J. & Sabovljević, M.S. (2023) Congruence between vascular plants and bryophytes in response to ecological conditions in sustainably managed temperate forests (taxonomic- and trait-based levels). Plant Ecology, 224, 1001–1014. Available from: https://doi.org/10.1007/s11258-023-01357-7
Laliberté, E., Legendre, P. & Shipley, B. (2022) FD: measuring functional diversity (FD) from multiple traits, and other tools for functional ecology.
Lenoir, J., Gégout, J.C., Dupouey, J.L., Bert, D. & Svenning, J.-C. (2010) Forest plant community changes during 1989–2007 in response to climate warming in the Jura Mountains (France and Switzerland). Journal of Vegetation Science, 21, 949–964.
Lenoir, J., Gril, E., Durrieu, S., Horen, H., Laslier, M., Lembrechts, J.J. et al. (2022) Unveil the unseen: using LiDAR to capture time-lag dynamics in the herbaceous layer of European temperate forests. Journal of Ecology, 110, 282–300.
Lüdecke, D. (2021) sjPlot: Data Visualization for Statistics in Social Science.
Macek, M., Kopecký, M. & Wild, J. (2019) Maximum air temperature controlled by landscape topography affects plant species composition in temperate forests. Landscape Ecology, 34, 2541–2556.
Maclean, I.M.D., Hopkins, J.J., Bennie, J., Lawson, C.R. & Wilson, R.J. (2015) Microclimates buffer the responses of plant communities to climate change. Global Ecology and Biogeography, 24, 1340–1350.
Man, M., Wild, J., Macek, M. & Kopecký, M. (2022) Can high-resolution topography and forest canopy structure substitute microclimate measurements? Bryophytes say no. Science of the Total Environment, 821, 153377.
Marcenò, C. & Guarino, R. (2015) A test on Ellenberg indicator values in the Mediterranean evergreen woods (Quercetea ilicis). Rendiconti Lincei, 26, 345–356.
Martin, G., Devictor, V., Motard, E., Machon, N. & Porcher, E. (2019) Short-term climate-induced change in French plant communities. Biology Letters, 15, 20190280.
Mills, S.E. & Macdonald, S.E. (2005) Factors influencing bryophyte assemblage at different scales in the Western Canadian boreal Forest. The Bryologist, 108, 86–100.
Otýpková, Z. (2009) The influence of sample plot size on evaluations with Ellenberg indicator values. Biologia, 64, 1123–1128.
Pacheco-Riaño, L.C., Høistad Schei, F., Flantua, S.G.A. & Grytnes, J.-A. (2023) Lags in the response of plant assemblages to global warming depends on temperature-change velocity. Global Ecology and Biogeography, 32, 719–733.
Paus, A. (2013) Human impact, soil erosion, and vegetation response lags to climate change: challenges for the mid-Scandinavian pollen-based transfer-function temperature reconstructions. Vegetation History and Archaeobotany, 22, 269–284.
Pearson, R.G. & Dawson, T.P. (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecology and Biogeography, 12, 361–371.
Pinto, P.E., Dupouey, J.-L., Hervé, J.-C., Legay, M., Wurpillot, S., Montpied, P. et al. (2016) Optimizing the bioindication of forest soil acidity, nitrogen and mineral nutrition using plant species. Ecological Indicators, 71, 359–367.
Potter, K.A., Woods, H.A. & Pincebourde, S. (2013) Microclimatic challenges in global change biology. Global Change Biology, 19, 2932–2939.
Richard, B., Dupouey, J.-L., Corcket, E., Alard, D., Archaux, F., Aubert, M. et al. (2021) The climatic debt is growing in the understorey of temperate forests: stand characteristics matter. Global Ecology and Biogeography, 30, 1474–1487.
Sanczuk, P., De Lombaerde, E., Haesen, S., Van Meerbeek, K., Luoto, M., Van der Veken, B. et al. (2022) Competition mediates understorey species range shifts under climate change. Journal of Ecology, 110, 1813–1825.
Schall, P. & Heinrichs, S. (2020) Comment on “Forest microclimate dynamics drive plant responses to warming”. Science, 370, eabd9920.
Soberón, J. & Arroyo-Peña, B. (2017) Are fundamental niches larger than the realized? Testing a 50-year-old prediction by Hutchinson. PLoS ONE, 12, e0175138.
Szymura, T.H., Szymura, M. & Macioł, A. (2014) Bioindication with Ellenberg's indicator values: a comparison with measured parameters in central European oak forests. Ecological Indicators, 46, 495–503.
Tichý, L., Axmanová, I., Dengler, J., Guarino, R., Jansen, F., Midolo, G. et al. (2023) Ellenberg-type indicator values for European vascular plant species. Journal of Vegetation Science, 34, e13168.
Ulrich, E. (1995) The renecofor-network: objectives and realization. Revue Forestière Française, 47, 107–124.
van Zuijlen, K., Nobis, M.P., Hedenäs, L., Hodgetts, N., Calleja Alarcón, J.A., Albertos, B. et al. (2023) Bryophytes of Europe traits (BET) data set: a fundamental tool for ecological studies. Journal of Vegetation Science, 34, e13179.
Vanderpoorten, A., Patiño, J., Désamoré, A., Laenen, B., Górski, P., Papp, B. et al. (2019) To what extent are bryophytes efficient dispersers? Journal of Ecology, 107, 2149–2154.
Vangansbeke, P., Máliš, F., Hédl, R., Chudomelová, M., Vild, O., Wulf, M. et al. (2021) ClimPlant: realized climatic niches of vascular plants in European forest understoreys. Global Ecology and Biogeography, 30, 1183–1190.
Zellweger, F., Coomes, D., Lenoir, J., Depauw, L., Maes, S.L., Wulf, M. et al. (2019) Seasonal drivers of understorey temperature buffering in temperate deciduous forests across Europe. Global Ecology and Biogeography, 28, 1774–1786.
Zellweger, F., Frenne, P.D., Lenoir, J., Vangansbeke, P., Verheyen, K., Bernhardt-Römermann, M. et al. (2020) Forest microclimate dynamics drive plant responses to warming. Science, 368, 772–775.
Zolotova, E., Ivanova, N. & Ivanova, S. (2023) Global overview of modern research based on Ellenberg indicator values. Diversity, 15, 14.
