Abstract
Macroclimatic changes are impacting ecosystems worldwide. However, a large portion of terrestrial species live under conditions where impacts of macroclimate change are buffered, such as in the shade of trees, and how this buffering impacts future below-canopy biodiversity redistributions at the continental scale is unknown. Here we show that shady forest floors due to dense tree canopies mitigate severe warming impacts on forest biodiversity, while canopy opening amplifies macroclimate change impacts. A cross-continental transplant experiment in five contrasting biogeographical areas combined with experimental heating and irradiation treatments was used to parametize 25-m resolution mechanistic demographic distribution models and project the current and future distributions of 12 common understorey plant species, considering the effects of forest microclimate and forest cover density. These results highlight microclimates and forest density as powerful tools for forest managers and policymakers to shelter forest biodiversity from climate change.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Data availability
Macroclimate data are available through the global climate archive WorldClim (https://www.worldclim.org/data/index.html). Spatial temperature offset data between forest and open field conditions are available at https://doi.org/10.6084/m9.figshare.14618235.v4 (ref. 20). Tree cover density data are available at https://land.copernicus.eu/pan-european/high-resolution-layers/forests/tree-cover-density/status-maps/2015. Georeferenced observation records used for the continental-scale validation of the Demographic Distribution Models (DDMs) are available at https://doi.org/10.15468/dl.3nvzc8. All experimental plant demographic data and site-level environmental data are available at FigShare https://figshare.com/s/35b070818230ce5795d3 (ref. 60).
Code availability
All scripts to reproduce the methods, analyses and figures are available at FigShare https://figshare.com/s/35b070818230ce5795d3 (ref. 60).
References
Chen, I., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species of climate warming. Science 333, 1024–1027 (2011).
Lenoir, J. et al. Species better track climate warming in the oceans than on land. Nat. Ecol. Evol. 4, 1044–1059 (2020).
Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).
De Frenne, P. & Verheyen, K. Weather stations lack forest data. Science 351, 234 (2016).
Lembrechts, J. J. et al. Comparing temperature data sources for use in species distribution models: from in-situ logging to remote sensing. Glob. Ecol. Biogeogr. 28, 1578–1596 (2019).
De Frenne, P. et al. Latitudinal gradients as natural laboratories to infer species’ responses to temperature. J. Ecol. 101, 784–795 (2013).
Zellweger, F. et al. Forest microclimate dynamics drive plant responses to warming. Science 368, 772–775 (2020).
Bertrand, R. et al. Changes in plant community composition lag behind climate warming in lowland forests. Nature 479, 517–520 (2011).
Suggitt, A. J. et al. Extinction risk from climate change is reduced by microclimatic buffering. Nat. Clim. Change 8, 713–717 (2018).
Shepard, I. D., Wissinger, S. A. & Greig, H. S. Elevation alters outcome of competition between resident and range-shifting species. Glob. Change Biol. 27, 270–281 (2021).
Alexander, J. M., Diez, J. M. & Levine, J. M. Novel competitors shape species’ responses to climate change. Nature 525, 515–518 (2015).
Sanczuk, P. et al. Competition mediates understorey species range shifts under climate change. J. Ecology 110, 1813–1825 (2022).
Colwell, R. K. Spatial scale and the synchrony of ecological disruption. Nature 599, E8–E10 (2021).
De Frenne, P. et al. Microclimate moderates plant responses to macroclimate warming. Proc. Natl Acad. Sci. USA 110, 18561–18565 (2013).
Lenoir, J., Hattab, T. & Pierre, G. Climatic microrefugia under anthropogenic climate change: implications for species redistribution. Ecography 40, 253–266 (2017).
Dietz, L., Collet, C., Eric, J. D., Lisa, L. & Gégout, J. Windstorm-induced canopy openings accelerate temperate forest adaptation to global warming. J. Biogeogr. 29, 2067–2077 (2020).
Bertrand, R. et al. Ecological constraints increase the climatic debt in forests. Nat. Commun. 7, 12643 (2016).
Sanczuk, P. et al. Species distribution models and a 60-year-old transplant experiment reveal inhibited forest plant range shifts under climate change. J. Biogeogr. 49, 537–550 (2022).
De Frenne, P. et al. Global buffering of temperatures under forest canopies. Nat. Ecol. Evol. 3, 744–749 (2019).
Haesen, S. et al. ForestTemp–sub-canopy microclimate temperatures of European forests. Glob. Change Biol. 27, 6307–6319 (2021).
Meeussen, C. et al. Microclimatic edge-to-interior gradients of European deciduous forests. Agric. Meteorol. 311, 108699 (2021).
De Lombaerde, E. et al. Maintaining forest cover to enhance temperature buffering under future climate change. Sci. Total Environ. 810, 151338 (2022).
Landuyt, D. et al. The functional role of temperate forest understorey vegetation in a changing world. Glob. Change Biol. 25, 3625–3641 (2019).
Kassuelke, S. R., Dymond, S. F., Feng, X., Savage, J. A. & Wagenbrenner, J. W. Understory evapotranspiration rates in a coast redwood forest. Ecohydrology 15, e2404 (2022).
De Lombaerde, E., Verheyen, K., Van Calster, H. & Baeten, L. Tree regeneration responds more to shade casting by the overstorey and competition in the understorey than to abundance per se. Ecol. Manage. 450, 117492 (2019).
Gasperini, C. et al. Edge effects on the realised soil seed bank along microclimatic gradients in temperate European forests. Sci. Total Environ. 798, 149373 (2021).
Potter, K. A., Woods, A. H. & Pincebourde, S. Microclimatic challenges in global change biology. Glob. Change Biol. 19, 2932–2939 (2013).
Hylander, K., Ehrlén, J., Luoto, M. & Meineri, E. Microrefugia: not for everyone. Ambio 44, 60–68 (2015).
De Pauw, K. et al. Forest understorey communities respond strongly to light in interaction with forest structure, but not to microclimate warming. N. Phytol. 233, 219–235 (2022).
De Frenne, P. et al. Light accelerates plant responses to warming. Nat. Plants 1, 4–6 (2015).
Govaert, S. et al. Rapid thermophilization of understorey plant communities in a 9 year-long temperate forest experiment. J. Ecology 109, 2434–2447 (2021).
De Frenne, P. et al. Forest microclimates and climate change: importance, drivers and future research agenda. Glob. Change Biol. 27, 2279–2297 (2021).
Senf, C. & Seidl, R. Persistent impacts of the 2018 drought on forest disturbance regimes in Europe. Biogeosciences 18, 5223–5230 (2021).
Büntgen, U. et al. Recent European drought extremes beyond Common Era background variability. Nat. Geosci. 14, 190–196 (2021).
Elith, J. et al. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57 (2011).
Merow, C. et al. On using integral projection models to generate demographically driven predictions of species’ distributions: development and validation using sparse data. Ecography 37, 1167–1183 (2014).
Merow, C., Treanor, S., Allen, J. M., Xie, Y. & Silander Jr, J. A. Climate change both facilitates and inhibits invasive plant ranges in New England. Proc. Natl Acad. Sci. USA 114, E3276–E3284 (2017).
Hargreaves, A. L., Samis, K. E. & Eckert, C. G. Are species’ range limits simply niche limits writ large? A review of transplant experiments beyond the range. Am. Nat. 183, 157–173 (2014).
Lee-Yaw, J. A. et al. A synthesis of transplant experiments and ecological niche models suggests that range limits are often niche limits. Ecol. Lett. 19, 710–722 (2016).
Dunne, J. A., Saleska, S. R., Fischer, M. L. & Harte, J. Integrating experimental and gradients methods in ecological climate change research. Ecology 85, 904–916 (2004).
Verheyen, K., Honnay, O., Motzkin, G., Hermy, M. & Foster, D. R. Response of forest plant species to land-use change: a life-history trait-based approach. J. Ecol. 91, 563–577 (2003).
Easterling, M. R., Ellner, S. P. & Dixon, P. M. Size-specific sensitivity: applying a new structured population model. Ecology 81, 694–708 (2000).
Merow, C. et al. Advancing population ecology with integral projection models: a practical guide. Methods Ecol. Evol. 5, 99–110 (2014).
Darwin, C. On the Origin of Species By Means of Natural Selection, or the Preservation of Favoured Races in the Struggle For Life (John Murray, 1859).
Brown, J. H. Macroecology (Univ. of Chicago Press, 1995).
Dobzhansky, T. Evolution in the Tropics (American Scientist, 1950).
MacArthur, R. H. Geographical Ecology: Patterns In the Distribution of Species (Princeton Univ. Press, 1972).
Araújo, M. B. & Luoto, M. The importance of biotic interactions for modelling species distributions under climate change. Glob. Ecol. Biogeogr. 16, 743–753 (2007).
Louthan, A. M., Doak, D. F. & Angert, A. L. Where and when do species interactions set range limits? Trends Ecol. Evol. 30, 780–792 (2015).
Wisz, M. S. et al. The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol. Rev. 88, 15–30 (2013).
Lembrechts, J. J., Nijs, I. & Lenoir, J. Incorporating microclimate into species distribution models. Ecography 42, 1267–1279 (2019).
Elemans, M. Light, nutrients and the growth of herbaceous forest species. Int. J. Ecol. 26, 197–202 (2004).
Senf, C. & Seidl, R. Mapping the forest disturbance regimes of Europe. Nat. Sustain. 4, 63–70 (2021).
Hartmann, H. et al. Climate change risks to global forest health: emergence of unexpected events of elevated tree mortality worldwide. Annu. Rev. Plant Biol. 73, 673–702 (2022).
Christiansen, D. M., Lønsmann, L., Johan, I. & Hylander, K. Changes in forest structure drive temperature preferences of boreal understorey plant communities. J. Ecology 110, 631–643 (2022).
Bertrand, R., Aubret, F., Grenouillet, G., Ribéron, A. & Blanchet, S. Comment on ‘Forest microclimate dynamics drive plant responses to warming’. Science 3850, eabd3850 (2020).
Norris, J. R. et al. Evidence for climate change in the satellite cloud record. Nature 536, 72–75 (2016).
Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51, 933–938 (2001).
Vangansbeke, P. et al. ClimPlant: realized climatic niches of vascular plants in European forest understoreys. Glob. Ecol. Biogeogr. 30, 1183–1190 (2021).
Sanczuk, P. et al. Microclimate and forest density drive plant population dynamics under climate change. figshare https://doi.org/10.6084/m9.figshare.23674521.v1 (2023).
Pérez-Harguindeguy, N. et al. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 20, 715–716 (2016).
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
Muñoz-sabater, J. et al. ERA5-Land: a state-of-the-art global reanalysis dataset for land applications. Earth Syst. Sci. Data Discuss. https://doi.org/10.5194/essd-2021-82 (2021).
Sanderson, B. M., Knutti, R. & Caldwell, P. A representative democracy to reduce interdependency in a multimodel ensemble. J. Clim. 28, 5171–5194 (2015).
Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 27, 27–46 (2013).
Fernández-Fernández, P. et al. Different effects of warming treatments in forests versus hedgerows on the understorey plant Geum urbanum. Plant Biol. 24, 734–744 (2022).
Barton, K. MuMIn: Multi-Model Inference (R version 4.1.0). CRAN https://cran.r-project.org/web/packages/MuMIn/index.html (2017).
Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods In Ecology And Evolution 4, 133–142 (2013).
Bürkner, P. Bayesian item response modeling in R with brms and Stan. J. Stat. Softw. 100, 1–54 (2021).
Childs, D. Z., Rees, M., Rose, K. E., Grubb, P. J. & Ellner, S. P. Evolution of complex flowering strategies: an age- and size-structured integral projection model. Proc. R. Soc. B 270, 1829–1838 (2003).
Ellner, S. P. & Rees, M. Integral projection models for species with complex demography. Am. Nat. 167, 410–428 (2006).
Meeussen, C. et al. Structural variation of forest edges across Europe. Ecol. Manage. 462, 117–929 (2020).
Microsoft & Weston, S. foreach: Provides Foreach Looping Construct (R version 4.1.0). CRAN https://cran.r-project.org/web/packages/foreach/index.html (2020).
Microsoft & Weston, S. doParallel: Foreach Parallel Adaptor for the ‘parallel’ Package (R version 4.1.0). CRAN https://cran.r-project.org/web/packages/doParallel/index.html (2020).
Tennekes, M. et al. tmap: thematic maps. J. Stat. Softw. 84, 1–39 (2018).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021).
Acknowledgements
We thank K. Ceunen, H. R. Schaffner, U. Johansson, S. Vaneenooghe, J. Van Loo, S. Van Bouchaute, L. G. Lundin, T. Augustijns and S. Haesen for fieldwork and technical assistance. This work was supported by the European Research Council (ERC) (ERC Starting Grant FORMICA 757833, 2018, http://www.formica.ugent.be), the Research Foundation Flanders (FWO) (K.D.P. ASP035-19, S.G. G0H1517N) and the FWO Scientific research network FLEUR (http://www.fleur.ugent.be).
Author information
Authors and Affiliations
Contributions
P.S., K.D.P., E.D.L., M.L., K.V., P.V. and P.D.F. conceived the ideas and designed methodology; all authors collected data; P.S. analysed data in collaboration with E.D.L., M.L., P.V. and P.D.F.; and P.S. led the writing of the manuscript in collaboration with K.D.P., E.D.F., P.V. and P.D.F. All authors contributed critically to the draft and gave final approval for publication.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Climate Change thanks Romain Bertrand, Ilya Maclean and Luiz Magnago for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 Overview of the experimental set up.
(top) Picture of the experimental site of the dense forest core plot in south Sweden with the full factorial heating and irradiation treatment. (bottom) Details of the plant protocol and design. ©Pieter Sanczuk.
Extended Data Fig. 2 Flowchart of the data.
Analytical framework of the study, data flow and modelling techniques used. Demographic data collected in the period 2019 – 2021 and plot-level environmental data was used to analyses the effects of the environment on all vital rates with (generalized) linear mixed-effect models (that is the vital rate models). The vital rate models were integrated in an integral projection modelling (IPM) approach to estimate population growth rates (λ). The final Demographic Distribution Models (DDM) resulted from projecting the IPM across the study area under the current (baseline) climate conditions and forest density, and under all combination of projected future climate conditions and simulated changes in forest density. For all future DDM predictions, temperature offsets were kept constant.
Extended Data Fig. 3 Plant vital rate responses.
Mixed-effect model coefficient estimates [± standard error] for the number of seeds (# seeds) and seedling size (recruit size) for the study species on which these vital rates could be measured in the experiment. Values are (generalized) linear mixed-effect model (LMM) coefficient estimates [± standard error] (after model selection; presented in horizontal way). Species are ranked following the Colonization Capacity Index (CCI). Significant effects (p < .05; obtained from the LMMs, not corrected) are in bold. Non-significant effects (p ≥ .05) are faded. Sample sizes for each species and vital rates are presented in Extended Data Fig. 4. See Supplementary Tables for model details.
Extended Data Fig. 4 Species-specific sample sizes.
Overview of species-specific sample sizes for the four main vital rates. (left) Species specific total sample size for each vital rate. (right) Annual sample sizes for each species and vital rate across the four experimental treatments (control [C], heating [H], illumination [L] and heating-illumination [LH]). The species are Anemone nemorosa (AneNem), Oxalis acetosella (OxaAce), Carex sylvatica (CarSyl), Vinca minor (VinMin), Poa nemoralis (PoaNem), Allium ursinum (AllUrs), Deschampsia cespitosa (DesCes), Geranium sylvaticum (GerSyl), Geranium robertianum (GerRob), Geum urbanum (GeuUrb), Alliaria petiolata (AllPet) and Urtica dioica (UrtDio).
Extended Data Fig. 5 Scenario analyses.
Predicted change in future population growth rate (λ) due to climate change under different simulated changes in forest density (from minus 50 % decrease to plus 50 % increase in forest density relative to the baseline conditions). Plotted are the continental-scale average % change [± Standard Deviation (SD)] in λ relative to the baseline climate and forest density predictions for 10,000 random locations across the study area. The grey dashed line represents no change.
Supplementary information
Supplementary Information
Supplementary Figs. 1–7 and Methods 1–6.
Supplementary Tables
Supplementary tables related to the study design, study area, study species and modelling decisions, and Bayesian linear regressions model output.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sanczuk, P., De Pauw, K., De Lombaerde, E. et al. Microclimate and forest density drive plant population dynamics under climate change. Nat. Clim. Chang. 13, 840–847 (2023). https://doi.org/10.1038/s41558-023-01744-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41558-023-01744-y
This article is cited by
-
Novel light regimes in European forests
Nature Ecology & Evolution (2023)