[en] The emergence of alternative stable states in forest systems has significant implications for the functioning and structure of the terrestrial biosphere, yet empirical evidence remains scarce. Here, we combine global forest biodiversity observations and simulations to test for alternative stable states in the presence of evergreen and deciduous forest types. We reveal a bimodal distribution of forest leaf types across temperate regions of the Northern Hemisphere that cannot be explained by the environment alone, suggesting signatures of alternative forest states. Moreover, we empirically demonstrate the existence of positive feedbacks in tree growth, recruitment and mortality, with trees having 4-43% higher growth rates, 14-17% higher survival rates and 4-7 times higher recruitment rates when they are surrounded by trees of their own leaf type. Simulations show that the observed positive feedbacks are necessary and sufficient to generate alternative forest states, which also lead to dependency on history (hysteresis) during ecosystem transition from evergreen to deciduous forests and vice versa. We identify hotspots of bistable forest types in evergreen-deciduous ecotones, which are likely driven by soil-related positive feedbacks. These findings are integral to predicting the distribution of forest biomes, and aid to our understanding of biodiversity, carbon turnover, and terrestrial climate feedbacks.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Zou, Yibiao ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland. yibiao.zou@usys.ethz.ch
Zohner, Constantin M ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Averill, Colin ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Ma, Haozhi ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Merder, Julian ; Department of Global Ecology, Carnegie Institution for Science, Stanford, CA, USA
Berdugo, Miguel ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Bialic-Murphy, Lalasia; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Mo, Lidong ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
Brun, Philipp ; Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903, Birmensdorf, Switzerland
Zimmermann, Niklaus E ; Swiss Federal Institute for Forest, Snow and Landscape Research WSL, 8903, Birmensdorf, Switzerland
Liang, Jingjing ; Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, USA
de-Miguel, Sergio ; Department of Agricultural and Forest Sciences and Engineering, University of Lleida, Lleida, Spain ; Forest Science and Technology Centre of Catalonia (CTFC), Solsona, Spain
Nabuurs, Gert-Jan ; Wageningen University and Research, Wageningen, The Netherlands
Reich, Peter B ; Department of Forest Resources, University of Minnesota, St. Paul, MN, USA ; Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia ; Institute for Global Change Biology, and School for Environment and Sustainability, University of Michigan, Ann Arbor, MI, USA
Niinements, Ulo; Plant Physiology work group, Estonian University of Life Sciences, Tartu, Estonia
Dahlgren, Jonas; Department of Forest Resource Management, Swedish University of Agricultural Sciences, Umeå, Sweden
Kändler, Gerald; Forstliche Versuchs- und Forschungsanstalt Baden-Württemberg, Freiburg im Breisgau, Germany
Ratcliffe, Sophia; NBN Trust, Nottingham, UK
Ruiz-Benito, Paloma; Universidad de Alcalá, Alcala de Henares, Spain
de Zavala, Miguel Angel ; Universidad de Alcalá, Alcala de Henares, Spain
Crowther, Thomas W ; Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Universitätsstrasse 16, 8092, Zurich, Switzerland
SNF - Schweizerischer Nationalfonds zur Förderung der wissenschaftlichen Forschung
Funding text :
We warmly thank all members of the Crowther lab team, including those not listed as coauthors, for their invaluable support. The collaboration and development of the manuscript were supported by the web-based science platform, science-i.org. We thank the Global Forest Biodiversity Initiative (GFBI) for establishing the data standards and collaborative framework. This work was supported by grants to TWC from the Bernina Foundation and DOB Ecology, and CMZ from the Ambizione Fellowship program (#PZ00P3_193646). MB was supported by a Ram\u00F3n y Cajal grant (RYC2021-031797-I) from the Spanish Ministry of Sciences. The European forest inventory data was provided by the FunDivEUROPE project, which received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement no 265171. We thank the Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf, and Dr. Christian Temperli for providing Swiss National Forest Inventory (LFI) data for the periods 1983-85, 1993-95, 2004-06, and 2009-2017. This study was also supported by the TRY initiative that is maintained by the Max Planck Institute for Biogeochemistry in Jena, Germany, and currently supported by DIVERSITAS/Future Earth and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig. National Natural Science Foundation of China (31800374). The ReVaTene dataset is funded by the Education and Research Ministry of C\u00F4te d\u2019Ivoire, as part of the Debt Reduction-Development Contracts (C2Ds) managed by IRD. JCS considers this work a contribution to his VILLUM Investigator project \u201CBiodiversity Dynamics in a Changing World\u201D, funded by VILLUM FONDEN (grant 16549), and Center for Ecological Dynamics in a Novel Biosphere (ECONOVO), funded by the Danish National Research Foundation (grant DNRF173). AFS considers this work a contribution to his UFRN project PVA12722-2015, and is thankful to Solon J. Longhi for data sharing (Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico 520053/1998-2). ALG considers this work a contribution to his IFFSC project (FAPESC, SDE, IMA, and CNPq grants). VS thanks for support to APVV 20-0168 from the Slovak Research and Development Agency. We are thankful to the State of S\u00E3o Paulo Research Foundation (FAPESP) for supporting the Atlantic Forest plots through the BIOTA/FAPESP Program (Project Functional Gradient 2003/12595-7, 2010/20811-7 & ECOFOR 2012/51872-5), and the Brazilian National Research Council (CNPq grant 403710/2012-0). FCT \u2013 Portuguese Foundation for Science and Technology, project UIDB/04033/2020 and ICNF-Instituto da Conserva\u00E7\u00E3o da Natureza. RAINFOR plots here were supported by a major grant from the Gordon and Betty Moore Foundation. We also thank NERC for long-term support of RAINFOR and ForestPlots.net (including NE/X014347/1, NE/N012542/1, NE/N012542/1, NE/X014347/1) and additional sources to O.L.P. including the ERC (Advanced Grant 291585, T-FORCES). P.R.B. and M.A.Z. acknowledge funding from the CLIMB-FOREST Horizon Europe Project (No 101059888) that was funded by the European Union.We warmly thank all members of the Crowther lab team, including those not listed as coauthors, for their invaluable support. The collaboration and development of the manuscript\u00A0were supported by the web-based science platform, science-i.org. We thank the Global Forest Biodiversity Initiative (GFBI) for establishing the data standards and collaborative framework. This work was supported by grants to TWC from the Bernina Foundation and DOB Ecology, and CMZ from the Ambizione Fellowship program (#PZ00P3_193646). MB was supported by a Ram\u00F3n y Cajal grant (RYC2021-031797-I) from the Spanish Ministry of Sciences. The European forest inventory data was provided by the FunDivEUROPE project, which received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement no 265171. We thank the\u00A0Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf, and Dr. Christian Temperli for providing Swiss National Forest Inventory (LFI)\u00A0data for the periods 1983-85, 1993-95, 2004-06, and 2009-2017. This study was also supported by the TRY initiative that is maintained by the Max Planck Institute for Biogeochemistry in Jena, Germany, and currently supported by DIVERSITAS/Future Earth and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig. National Natural Science Foundation of China (31800374). The ReVaTene dataset is funded by the Education and Research Ministry of C\u00F4te d\u2019Ivoire, as part of the Debt Reduction-Development Contracts (C2Ds) managed by IRD. JCS considers this work a contribution to his VILLUM Investigator project \u201CBiodiversity Dynamics in a Changing World\u201D, funded by VILLUM FONDEN (grant 16549), and Center for Ecological Dynamics in a Novel Biosphere (ECONOVO), funded by the Danish National Research Foundation (grant DNRF173). AFS considers this work a contribution to his UFRN project PVA12722-2015, and is thankful to Solon J. Longhi for data sharing (Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico 520053/1998-2). ALG considers this work a contribution to his IFFSC project (FAPESC, SDE, IMA, and CNPq grants). VS thanks for support to APVV 20-0168 from the Slovak Research and Development Agency. We are thankful to the State of S\u00E3o Paulo Research Foundation (FAPESP) for supporting the Atlantic Forest plots through the BIOTA/FAPESP Program (Project Functional Gradient 2003/12595-7, 2010/20811-7 & ECOFOR 2012/51872-5), and the Brazilian National Research Council (CNPq grant 403710/2012-0). FCT \u2013 Portuguese Foundation for Science and Technology, project UIDB/04033/2020 and ICNF-Instituto da Conserva\u00E7\u00E3o da Natureza. RAINFOR plots here were supported by a major grant from the Gordon and Betty Moore Foundation. We also thank NERC for long-term support of RAINFOR and ForestPlots.net (including NE/X014347/1, NE/N012542/1, NE/N012542/1, NE/X014347/1) and additional sources to O.L.P. including the ERC (Advanced Grant 291585, T-FORCES). P.R.B. and M.A.Z. acknowledge funding from the CLIMB-FOREST Horizon Europe Project (No 101059888) that was funded by the European Union.
M. Scheffer S. Carpenter J.A. Foley C. Folke B. Walker Catastrophic shifts in ecosystems Nature 2001 413 591 596 2001Natur.413.591S 1:CAS:528:DC%2BD3MXnsleht7c%3D 11595939
Scheffer, M. Critical Transitions in Nature and Society. (Princeton University Press, 2009).
L. Yang et al. Sociocultural determinants of global mask-wearing behavior Proc. Natl Acad. Sci. 2022 119 1:CAS:528:DC%2BB38XivVSmu7rO 36191222 9565043
A.C. Staver S. Archibald S. Levin The global extent and determinants of savanna and forest as alternative biome states Science 2011 334 230 232 2011Sci..334.230S 1:CAS:528:DC%2BC3MXht1yktr7N 21998389
J.C. Aleman et al. Floristic evidence for alternative biome states in tropical Africa Proc. Natl Acad. Sci. 2020 117 28183 28190 2020PNAS.11728183A 1:CAS:528:DC%2BB3cXitlWmsr7N 33109722 7668043
G.B. Bonan Forests and climate change: forcings, feedbacks, and the climate benefits of forests Science 2008 320 1444 2008Sci..320.1444B 1:CAS:528:DC%2BD1cXntVWqs7s%3D 18556546
T.J. Givnish Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox Silva Fennica 2002 36 703 743
S. Sitch et al. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model Glob. Change Biol. 2003 9 161 185 2003GCBio..9.161S
R.A. Fisher et al. Vegetation demographics in Earth System Models: A review of progress and priorities Glob. Change Biol. 2018 24 35 54 2018GCBio.24..35F
E. Weng C.E. Farrior R. Dybzinski S.W. Pacala Predicting vegetation type through physiological and environmental interactions with leaf traits: evergreen and deciduous forests in an earth system modeling framework Glob. Chang Biol. 2017 23 2482 2498 2017GCBio.23.2482W 27782353
I.J. Wright et al. The worldwide leaf economics spectrum Nature 2004 428 821 827 2004Natur.428.821W 1:CAS:528:DC%2BD2cXjt1Crt74%3D 15103368
P.B. Reich M.B. Walters D.S. Ellsworth Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems Ecol. Monogr. 1992 62 365 392
M. Scheffer M. Hirota M. Holmgren E.H. Van Nes F.S. Chapin Thresholds for boreal biome transitions Proc. Natl Acad. Sci. 2012 109 21384 2012PNAS.10921384S 1:CAS:528:DC%2BC3sXoslSntA%3D%3D 23236159 3535627
J.G. Pausas W.J. Bond Alternative biome states in terrestrial ecosystems Trends Plant Sci. 2020 25 250 263 1:CAS:528:DC%2BC1MXisVaqsrzJ 31917105
Reich, P. & Bolstad, P. In Productivity of Evergreen and Deciduous Temperate Forests 245–283 (2001).
P.B. Reich R.L. Rich X. Lu Y.-P. Wang J. Oleksyn Biogeographic variation in evergreen conifer needle longevity and impacts on boreal forest carbon cycle projections Proc. Natl Acad. Sci. 2014 111 13703 2014PNAS.11113703R 1:CAS:528:DC%2BC2cXhsFCisbjO 25225397 4183309
J.H. Pedlar et al. Placing forestry in the assisted migration debate Bioscience 2012 62 835 842
G.B. Bonan Environmental factors and ecological processes controlling vegetation patterns in boreal forests Landsc. Ecol. 1989 3 111 130
H. Ma et al. The global biogeography of tree leaf form and habit Nat. Plants 2023 9 1795 1809 37872262 10654052
C.D. Monk An ecological significance of evergreenness Ecology 1966 47 504 505
S.T. Gower Y. Son Differences in soil and leaf litterfall nitrogen dynamics for five forest plantations Soil Sci. Soc. Am. J. 1992 56 1959 1966 1992SSASJ.56.1959G
P.B. Reich et al. Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species Ecol. Lett. 2005 8 811 818
B.F. Chabot D.J. Hicks The ecology of leaf life spans Annu. Rev. Ecol. Syst. 1982 13 229 259
J. Molofsky J.D. Bever A novel theory to explain species diversity in landscapes: positive frequency dependence and habitat suitability Proc. R. Soc. Lond. Ser. B: Biol. Sci. 2002 269 2389 2393
S. Kéfi M. Holmgren M. Scheffer When can positive interactions cause alternative stable states in ecosystems? Funct. Ecol. 2016 30 88 97
J. Pastor W.M. Post Response of northern forests to CO2-induced climate change Nature 1988 334 55 58 1988Natur.334..55P
M.W. Cadotte C.M. Tucker Should environmental filtering be abandoned? Trends Ecol. Evol. 2017 32 429 437 28363350
C.L.C. Liu O. Kuchma K.V. Krutovsky Mixed-species versus monocultures in plantation forestry: Development, benefits, ecosystem services and perspectives for the future Glob. Ecol. Conserv. 2018 15
H. Hillebrand et al. Thresholds for ecological responses to global change do not emerge from empirical data Nat. Ecol. Evol. 2020 4 1502 1509 32807945 7614041
C. Averill et al. Alternative stable states of the forest mycobiome are maintained through positive feedbacks Nat. Ecol. Evol. 2022 6 375 382 35210576 7612595
B.E. Beisner D.T. Haydon K. Cuddington Alternative stable states in ecology Front. Ecol. Environ. 2003 1 376 382
A. Gray T. Brandeis J. Shaw W. McWilliams P. Miles Forest Inventory and Analysis Database of the United States of America (FIA) Biodivers. Ecol. 2012 4 225 231
J. Liang et al. Positive biodiversity-productivity relationship predominant in global forests Science 2016 354 27738143
J. Kattge et al. TRY plant trait database – enhanced coverage and open access Glob. Change Biol. 2020 26 119 188 2020GCBio.26.119K
D.M. Stasinopoulos R.A. Rigby Generalized Additive Models for Location Scale and Shape (GAMLSS) in R J. Stat. Softw. 2007 23 1 46
K. Kikuzawa Y. Onoda I.J. Wright P.B. Reich Mechanisms underlying global temperature-related patterns in leaf longevity Glob. Ecol. Biogeogr. 2013 22 982 993
D.E. Goldberg The distribution of evergreen and deciduous trees relative to soil type: an example from the Sierra Madre, Mexico, and a general model Ecology 1982 63 942 951
K. Kikuzawa A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern Am. Naturalist 1991 138 1250 1263
L.E. Frelich R.R. Calcote M.B. Davis J. Pastor Patch formation and maintenance in an old-growth Hemlock-Hardwood forest Ecology 1993 74 513 527
M.R. Fulton I.C. Prentice Edaphic controls on the boreonemoral forest mosaic Oikos 1997 78 291 298 1997Oikos.78.291F
J. Pastor W.M. Post Influence of climate, soil moisture, and succession on forest carbon and nitrogen cycles Biogeochemistry 1986 2 3 27
Desie, E., Muys, B., Jansen, B., Vesterdal, L. & Vancampenhout, K. Pedogenic threshold in acidity explains context-dependent tree species effects on soil carbon. Front. Forests Glob. Change 4, 679813 (2021).
C. Strobl A.-L. Boulesteix T. Kneib T. Augustin A. Zeileis Conditional variable importance for random forests BMC Bioinforma. 2008 9
N.H. Batjes E. Ribeiro A. van Oostrum Standardised soil profile data to support global mapping and modelling (WoSIS snapshot 2019) Earth Syst. Sci. Data 2020 12 299 320 2020ESSD..12.299B
L. Baeten et al. A novel comparative research platform designed to determine the functional significance of tree species diversity in European forests Perspect. Plant Ecol., Evol. Syst. 2013 15 281 291
Rigby, R. A. & Stasinopoulos, D. M. Generalized additive models for location, scale and shape. Journal of the Royal Statistical Society: Series C (Applied Statistics 54, 507–554 (2005).
Dodge, Y. In The Concise Encyclopedia of Statistics 502–505 (Springer New York, 2008).
J.G. Masek et al. North American forest disturbance mapped from a decadal Landsat record Remote Sens. Environ. 2008 112 2914 2926 2008RSEnv.112.2914M
Strogatz, S. a. Nonlinear dynamics and chaos: with applications to physics, biology, chemistry, and engineering. (Second edition. Boulder, CO: Westview Press, a member of the Perseus Books Group, [2015], 2015).
P.B. Reich et al. Even modest climate change may lead to major transitions in boreal forests Nature 2022 608 540 545 2022Natur.608.540R 1:CAS:528:DC%2BB38XitFSjtbvP 35948640
J.A. Hartigan M.A. Wong Algorithm AS 136: A K-means clustering algorithm J. R. Stat. Soc. Ser. C. (Appl. Stat.) 1979 28 100 108
J.A. Hartigan P.M. Hartigan The dip test of unimodality Ann. Stat. 1985 13 70 84 773153
Zou, Y. Dataset for “Alternative stable states of forest types” [Data set]. Zenodo. https://doi.org/10.5281/zenodo.11048857 (2024).
Zou, Y. Yibiaozou/AltSS_ForestLeafPhenology: Alternative stable states of global forest types (AltSS_LP_NC). Zenodo. https://doi.org/10.5281/zenodo.11035706 (2024).
