Abstract

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.

Alternative stable states in forests have implications for the biosphere. Here, the authors combine forest biodiversity observations and simulations revealing that leaf types across temperate regions of the NH follow a bimodal distribution suggesting signatures of alternative forest states.

Details

Title
Positive feedbacks and alternative stable states in forest leaf types
Author
Zou, Yibiao 1   VIAFID ORCID Logo  ; Zohner, Constantin M. 1   VIAFID ORCID Logo  ; Averill, Colin 1   VIAFID ORCID Logo  ; Ma, Haozhi 1   VIAFID ORCID Logo  ; Merder, Julian 2   VIAFID ORCID Logo  ; Berdugo, Miguel 1   VIAFID ORCID Logo  ; Bialic-Murphy, Lalasia 1 ; Mo, Lidong 1   VIAFID ORCID Logo  ; Brun, Philipp 3   VIAFID ORCID Logo  ; Zimmermann, Niklaus E. 3   VIAFID ORCID Logo  ; Liang, Jingjing 4   VIAFID ORCID Logo  ; de-Miguel, Sergio 5   VIAFID ORCID Logo  ; Nabuurs, Gert-Jan 6   VIAFID ORCID Logo  ; Reich, Peter B. 7   VIAFID ORCID Logo  ; Niinements, Ulo 8 ; Dahlgren, Jonas 9 ; Kändler, Gerald 10 ; Ratcliffe, Sophia 11 ; Ruiz-Benito, Paloma 12 ; de Zavala, Miguel Angel 12   VIAFID ORCID Logo  ; Abegg, Meinrad 3 ; Adou Yao, Yves C. 13 ; Alberti, Giorgio 14 ; Almeyda Zambrano, Angelica M. 15 ; Alvarado, Braulio Vilchez 16 ; Alvarez-Dávila, Esteban 17 ; Alvarez-Loayza, Patricia 18 ; Alves, Luciana F. 19 ; Ammer, Christian 20 ; Antón-Fernández, Clara 21 ; Araujo-Murakami, Alejandro 22 ; Arroyo, Luzmila 22 ; Avitabile, Valerio 23 ; Aymard, Gerardo A. 24 ; Baker, Timothy R. 25 ; Bałazy, Radomir 26 ; Banki, Olaf 27 ; Barroso, Jorcely G. 28 ; Bastian, Meredith L. 29 ; Bastin, Jean-Francois 30 ; Birigazzi, Luca 31 ; Birnbaum, Philippe 32 ; Bitariho, Robert 33 ; Boeckx, Pascal 34 ; Bongers, Frans 6 ; Bouriaud, Olivier 35 ; Brancalion, Pedro H. S. 36 ; Brandl, Susanne 37 ; Brearley, Francis Q. 38 ; Brienen, Roel 25 ; Broadbent, Eben N. 39 ; Bruelheide, Helge 40 ; Bussotti, Filippo 41 ; Gatti, Roberto Cazzolla 42 ; César, Ricardo G. 36 ; Cesljar, Goran 43 ; Chazdon, Robin 44 ; Chen, Han Y. H. 45 ; Chisholm, Chelsea 1 ; Cho, Hyunkook 46 ; Cienciala, Emil 47 ; Clark, Connie 48 ; Clark, David 49 ; Colletta, Gabriel D. 50 ; Coomes, David A. 51 ; Valverde, Fernando Cornejo 52 ; Corral-Rivas, José J. 53 ; Crim, Philip M. 54 ; Cumming, Jonathan R. 55 ; Dayanandan, Selvadurai 56 ; de Gasper, André L. 57 ; Decuyper, Mathieu 58 ; Derroire, Géraldine 59 ; DeVries, Ben 60 ; Djordjevic, Ilija 61 ; Dolezal, Jiri 62 ; Dourdain, Aurélie 59 ; Obiang, Nestor Laurier Engone 63 ; Enquist, Brian J. 64 ; Eyre, Teresa J. 65 ; Fandohan, Adandé Belarmain 66 ; Fayle, Tom M. 67 ; Feldpausch, Ted R. 68 ; Ferreira, Leandro V. 69 ; Finér, Leena 70 ; Fischer, Markus 71 ; Fletcher, Christine 72 ; Fridman, Jonas 73 ; Frizzera, Lorenzo 74 ; Gamarra, Javier G. P. 75 ; Gianelle, Damiano 74 ; Glick, Henry B. 76 ; Harris, David J. 77 ; Hector, Andrew 78 ; Hemp, Andreas 79 ; Hengeveld, Geerten 6 ; Hérault, Bruno 80 ; Herbohn, John L. 81 ; Herold, Martin 82 ; Hillers, Annika 83 ; Honorio Coronado, Eurídice N. 84 ; Hui, Cang 85 ; Ibanez, Thomas 86 ; Iêda, Amaral 87 ; Imai, Nobuo 88 ; Jagodziński, Andrzej M. 89 ; Jaroszewicz, Bogdan 90 ; Johannsen, Vivian Kvist 91 ; Joly, Carlos A. 92 ; Jucker, Tommaso 93 ; Jung, Ilbin 94 ; Karminov, Viktor 95 ; Kartawinata, Kuswata 18 ; Kearsley, Elizabeth 96 ; Kenfack, David 97 ; Kennard, Deborah K. 98 ; Kepfer-Rojas, Sebastian 91 ; Keppel, Gunnar 99 ; Khan, Mohammed Latif 100 ; Killeen, Timothy J. 22 ; Kim, Hyun Seok 101 ; Kitayama, Kanehiro 102 ; Köhl, Michael 103 ; Korjus, Henn 104 ; Kraxner, Florian 105 ; Laarmann, Diana 104 ; Lang, Mait 104 ; Lewis, Simon L. 106 ; Lu, Huicui 107 ; Lukina, Natalia V. 108 ; Maitner, Brian S. 109 ; Malhi, Yadvinder 110 ; Marcon, Eric 111 ; Marimon, Beatriz Schwantes 112 ; Marimon-Junior, Ben Hur 112 ; Marshall, Andrew R. 113 ; Martin, Emanuel H. 114 ; Kucher, Dmitry 115 ; Meave, Jorge A. 116 ; Melo-Cruz, Omar 117 ; Mendoza, Casimiro 118 ; Merow, Cory 119 ; Mendoza, Abel Monteagudo 120 ; Moreno, Vanessa S. 36 ; Mukul, Sharif A. 121 ; Mundhenk, Philip 103 ; Nava-Miranda, María Guadalupe 122 ; Neill, David 123 ; Neldner, Victor J. 124 ; Nevenic, Radovan V. 61 ; Ngugi, Michael R. 125 ; Niklaus, Pascal A. 126 ; Oleksyn, Jacek 127 ; Ontikov, Petr 95 ; Ortiz-Malavasi, Edgar 16 ; Pan, Yude 128 ; Paquette, Alain 129 ; Parada-Gutierrez, Alexander 22 ; Parfenova, Elena I. 130 ; Park, Minjee 131 ; Parren, Marc 132 ; Parthasarathy, Narayanaswamy 133 ; Peri, Pablo L. 134 ; Pfautsch, Sebastian 135 ; Phillips, Oliver L. 25 ; Picard, Nicolas 136 ; Piedade, Maria Teresa T. F. 137 ; Piotto, Daniel 138 ; Pitman, Nigel C. A. 18 ; Polo, Irina 139 ; Poorter, Lourens 6 ; Poulsen, Axel D. 77 ; Poulsen, John R. 140 ; Pretzsch, Hans 141 ; Arevalo, Freddy Ramirez 142 ; Restrepo-Correa, Zorayda 143 ; Rodeghiero, Mirco 144 ; Rolim, Samir G. 138 ; Roopsind, Anand 145 ; Rovero, Francesco 146 ; Rutishauser, Ervan 147 ; Saikia, Purabi 148 ; Salas-Eljatib, Christian 149 ; Saner, Philippe 150 ; Schall, Peter 20 ; Schelhaas, Mart-Jan 6 ; Schepaschenko, Dmitry 151 ; Scherer-Lorenzen, Michael 152 ; Schmid, Bernhard 126 ; Schöngart, Jochen 137 ; Searle, Eric B. 129 ; Seben, Vladimír 153 ; Serra-Diaz, Josep M. 154 ; Sheil, Douglas 155 ; Shvidenko, Anatoly Z. 156 ; Silva-Espejo, Javier E. 157 ; Silveira, Marcos 158 ; Singh, James 159 ; Sist, Plinio 160 ; Slik, Ferry 161 ; Sonké, Bonaventure 162 ; Souza, Alexandre F. 163 ; Miscicki, Stanislaw 164 ; Stereńczak, Krzysztof J. 26 ; Svenning, Jens-Christian 165 ; Svoboda, Miroslav 166 ; Swanepoel, Ben 167 ; Targhetta, Natalia 137 ; Tchebakova, Nadja 130 ; ter Steege, Hans 168 ; Thomas, Raquel 169 ; Tikhonova, Elena 108 ; Umunay, Peter M. 170 ; Usoltsev, Vladimir A. 171 ; Valencia, Renato 172 ; Valladares, Fernando 173 ; van der Plas, Fons 174 ; Van Do, Tran 175 ; van Nuland, Michael E. 176 ; Vasquez, Rodolfo M. 177 ; Verbeeck, Hans 178 ; Viana, Helder 179 ; Vibrans, Alexander C. 180 ; Vieira, Simone 181 ; von Gadow, Klaus 182 ; Wang, Hua-Feng 183 ; Watson, James V. 184 ; Werner, Gijsbert D. A. 185 ; Westerlund, Bertil 73 ; Wiser, Susan K. 186 ; Wittmann, Florian 187 ; Woell, Hannsjoerg 188 ; Wortel, Verginia 189 ; Zagt, Roderik 190 ; Zawiła-Niedźwiecki, Tomasz 191 ; Zhang, Chunyu 192 ; Zhao, Xiuhai 192 ; Zhou, Mo 4 ; Zhu, Zhi-Xin 183 ; Zo-Bi, Irie C. 193 ; Crowther, Thomas W. 1   VIAFID ORCID Logo 

 ETH Zurich (Swiss Federal Institute of Technology), Institute of Integrative Biology, Zurich, Switzerland (GRID:grid.5801.c) (ISNI:0000 0001 2156 2780) 
 Carnegie Institution for Science, Department of Global Ecology, Stanford, USA (GRID:grid.418276.e) (ISNI:0000 0001 2323 7340) 
 Snow and Landscape Research WSL, Swiss Federal Institute for Forest, Birmensdorf, Switzerland (GRID:grid.419754.a) (ISNI:0000 0001 2259 5533) 
 Purdue University, Department of Forestry and Natural Resources, West Lafayette, USA (GRID:grid.169077.e) (ISNI:0000 0004 1937 2197) 
 University of Lleida, Department of Agricultural and Forest Sciences and Engineering, Lleida, Spain (GRID:grid.15043.33) (ISNI:0000 0001 2163 1432); Forest Science and Technology Centre of Catalonia (CTFC), Solsona, Spain (GRID:grid.423822.d) (ISNI:0000 0000 9161 2635) 
 Wageningen University and Research, Wageningen, The Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666) 
 University of Minnesota, Department of Forest Resources, St. Paul, USA (GRID:grid.17635.36) (ISNI:0000 0004 1936 8657); Western Sydney University, Hawkesbury Institute for the Environment, Penrith, Australia (GRID:grid.1029.a) (ISNI:0000 0000 9939 5719); University of Michigan, Institute for Global Change Biology, and School for Environment and Sustainability, Ann Arbor, USA (GRID:grid.214458.e) (ISNI:0000 0004 1936 7347) 
 Estonian University of Life Sciences, Plant Physiology work group, Tartu, Estonia (GRID:grid.16697.3f) (ISNI:0000 0001 0671 1127) 
 Swedish University of Agricultural Sciences, Department of Forest Resource Management, Umeå, Sweden (GRID:grid.6341.0) (ISNI:0000 0000 8578 2742) 
10  Forstliche Versuchs- und Forschungsanstalt Baden-Württemberg, Freiburg im Breisgau, Germany (GRID:grid.424546.5) (ISNI:0000 0001 0727 5435) 
11  NBN Trust, Nottingham, UK (GRID:grid.516332.0) (ISNI:0000 0004 6335 2396) 
12  Universidad de Alcalá, Alcala de Henares, Spain (GRID:grid.7159.a) (ISNI:0000 0004 1937 0239) 
13  University Félix Houphouët-Boigny, UFR Biosciences, Abidjan, Côte d’Ivoire (GRID:grid.410694.e) (ISNI:0000 0001 2176 6353) 
14  University of Udine, Department of Agricultural, Food, Environmental and Animal Sciences, Udine, Italy (GRID:grid.5390.f) (ISNI:0000 0001 2113 062X); Free University of Bolzano, Faculty of Science and Technology, Bolzano, Italy (GRID:grid.34988.3e) (ISNI:0000 0001 1482 2038) 
15  University of Florida, Spatial Ecology and Conservation Laboratory, Department of Tourism, Recreation and Sport Management, Gainesville, USA (GRID:grid.15276.37) (ISNI:0000 0004 1936 8091) 
16  Tecnológico de Costa Rica TEC, Forestry School, Cartago, Costa Rica (GRID:grid.441034.6) (ISNI:0000 0004 0485 9920) 
17  UNAD, Fundacion ConVida, Universidad Nacional Abierta y a Distancia, Medellin, Colombia (GRID:grid.442181.a) (ISNI:0000 0000 9497 122X) 
18  Field Museum of Natural History, Chicago, USA (GRID:grid.299784.9) (ISNI:0000 0001 0476 8496) 
19  UCLA, Center for Tropical Research, Institute of the Environment and Sustainability, Los Angeles, USA (GRID:grid.19006.3e) (ISNI:0000 0000 9632 6718) 
20  University of Göttingen, Silviculture and Forest Ecology of the Temperate Zones, Göttingen, Germany (GRID:grid.7450.6) (ISNI:0000 0001 2364 4210) 
21  Norwegian Institute of Bioeconomy Research (NIBIO), Division of Forest and Forest Resources, Ås, Norway (GRID:grid.454322.6) (ISNI:0000 0004 4910 9859) 
22  Museo de Historia natural Noel kempff Mercado, Santa Cruz, Bolivia (GRID:grid.500626.7) 
23  Joint Research Center, European Commission, Ispra, Italy (GRID:grid.434554.7) (ISNI:0000 0004 1758 4137) 
24  Herbario Universitario (PORT), UNELLEZ-Guanare, Programa de Ciencias del Agro y el Mar, Portuguesa, Venezuela (GRID:grid.434554.7); Compensation International S. A. Ci Progress-GreenLife, Bogotá, Colombia (GRID:grid.434554.7) 
25  University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403) 
26  Forest Research Institute, Department of Geomatics, Raszyn, Poland (GRID:grid.425286.f) (ISNI:0000 0001 2159 6489) 
27  Naturalis Biodiversity Center, Leiden, The Netherlands (GRID:grid.425948.6) (ISNI:0000 0001 2159 802X) 
28  Universidade Federal do Acre, Centro Multidisciplinar, Rio Branco, Brazil (GRID:grid.412369.b) (ISNI:0000 0000 9887 315X) 
29  Proceedings of the National Academy of Sciences, Washington, USA (GRID:grid.275752.0); Duke University, Department of Evolutionary Anthropology, Durham, USA (GRID:grid.26009.3d) (ISNI:0000 0004 1936 7961) 
30  University of Liege, TERRA Teach and Research Centre, Gembloux Agro Bio-Tech, Liege, Belgium (GRID:grid.4861.b) (ISNI:0000 0001 0805 7253) 
31  Forestry Consultant, Grosseto, Italy (GRID:grid.4861.b) 
32  Institut Agronomique néo-Calédonien (IAC), Nouméa, New Caledonia (GRID:grid.4861.b); Univ Montpellier, AMAP, Montpellier, France (GRID:grid.121334.6) (ISNI:0000 0001 2097 0141); IRD, CIRAD, CNRS, INRAE, Montpellier, France (GRID:grid.4399.7) (ISNI:0000000122879528) 
33  Mbarara University of Sciences and Technology, Institute of Tropical Forest Conservation, Mbarara, Uganda (GRID:grid.33440.30) (ISNI:0000 0001 0232 6272) 
34  Ghent University, Isotope Bioscience Laboratory - ISOFYS, Ghent, Belgium (GRID:grid.5342.0) (ISNI:0000 0001 2069 7798) 
35  Stefan cel Mare University of Suceava, Integrated Center for Research, Development and Innovation in Advanced Materials, Nanotechnologies, and Distributed Systems for Fabrication and Control (MANSiD), Suceava, Romania (GRID:grid.12056.30) (ISNI:0000 0001 2163 6372) 
36  University of São Paulo, Department of Forest Sciences, Luiz de Queiroz College of Agriculture, Piracicaba, Brazil (GRID:grid.11899.38) (ISNI:0000 0004 1937 0722) 
37  Bavarian State Institute of Forestry, Freising, Germany (GRID:grid.500073.1) (ISNI:0000 0001 1015 5020) 
38  Manchester Metropolitan University, Department of Natural Sciences, Manchester, UK (GRID:grid.25627.34) (ISNI:0000 0001 0790 5329) 
39  University of Florida, Spatial Ecology and Conservation Laboratory, School of Forest Resources and Conservation, Gainesville, USA (GRID:grid.15276.37) (ISNI:0000 0004 1936 8091) 
40  Halle-, Institute of Biology, Geobotany and Botanical Garden, Martin Luther University Halle-Wittenberg, Wittenberg, Germany (GRID:grid.9018.0) (ISNI:0000 0001 0679 2801); German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany (GRID:grid.421064.5) (ISNI:0000 0004 7470 3956) 
41  University of Firenze, Department of Agriculture, Food, Environment and Forest (DAGRI), Florence, Italy (GRID:grid.8404.8) (ISNI:0000 0004 1757 2304) 
42  University of Bologna, Department of Biological, Geological, and Environmental Sciences, Bologna, Italy (GRID:grid.6292.f) (ISNI:0000 0004 1757 1758) 
43  Institute of Forestry, Department of Spatial Regulation, GIS and Forest Policy, Belgrade, Serbia (GRID:grid.512559.f) 
44  University of Connecticut, Department of Ecology and Evolutionary Biology, Storrs, USA (GRID:grid.63054.34) (ISNI:0000 0001 0860 4915); Sippy Downs, Forest Research Institute, University of the Sunshine Coast, Queensland, Australia (GRID:grid.1034.6) (ISNI:0000 0001 1555 3415) 
45  Lakehead University, Faculty of Natural Resources Management, Thunder Bay, Canada (GRID:grid.258900.6) (ISNI:0000 0001 0687 7127) 
46  Korea Forest Promotion Institute, Division of Forest Resources Information, Seoul, South Korea (GRID:grid.5801.c) 
47  IFER - Institute of Forest Ecosystem Research, Jilove u Prahy, Czech Republic (GRID:grid.435210.1); Global Change Research Institute CAS, Brno, Czech Republic (GRID:grid.426587.a) (ISNI:0000 0001 1091 957X) 
48  Duke University, Nicholas School of the Environment, Durham, USA (GRID:grid.26009.3d) (ISNI:0000 0004 1936 7961) 
49  University of Missouri-St Louis, Department of Biology, St. Louis, USA (GRID:grid.266757.7) (ISNI:0000 0001 1480 9378) 
50  Universidade Estadual de Campinas, Programa de Pós-graduação em Biologia Vegetal, Instituto de Biologia, Campinas, Brazil (GRID:grid.411087.b) (ISNI:0000 0001 0723 2494) 
51  University of Cambridge, Department of Plant Sciences and Conservation Research Institute, Cambridge, UK (GRID:grid.5335.0) (ISNI:0000 0001 2188 5934) 
52  Andes to Amazon Biodiversity Program, Madre de Dios, Peru (GRID:grid.5335.0) 
53  Universidad Juárez del Estado de Durango, Facultad de Ciencias Forestales y Ambientales, Durango, Mexico (GRID:grid.412198.7) (ISNI:0000 0000 8724 8383) 
54  West Virginia University, Department of Biology, Morgantown, USA (GRID:grid.268154.c) (ISNI:0000 0001 2156 6140); The College of Saint Rose, Department of Physical and Biological Sciences, Albany, USA (GRID:grid.421322.4) (ISNI:0000 0004 0367 5388) 
55  West Virginia University, Department of Biology, Morgantown, USA (GRID:grid.268154.c) (ISNI:0000 0001 2156 6140) 
56  Concordia University, Biology Department, Centre for Structural and Functional Genomics, Montreal, Canada (GRID:grid.410319.e) (ISNI:0000 0004 1936 8630) 
57  Universidade Regional de Blumenau, Natural Science Department, Blumenau, Brazil (GRID:grid.412404.7) (ISNI:0000 0000 9143 5704) 
58  World Agroforestry (ICRAF), Nairobi, Kenya (GRID:grid.435643.3) (ISNI:0000 0000 9972 1350) 
59  Campus Agronomique, Cirad, UMR EcoFoG (AgroParisTech, CNRS, INRAE, Université des Antilles, Université de la Guyane), Kourou, French Guiana (GRID:grid.460797.b) 
60  University of Maryland, Department of Geographical Sciences, College Park, USA (GRID:grid.164295.d) (ISNI:0000 0001 0941 7177) 
61  Institute of Forestry, Belgrade, Serbia (GRID:grid.512559.f) 
62  The Czech Academy of Sciences, Institute of Botany, Třeboň, Czech Republic (GRID:grid.418095.1) (ISNI:0000 0001 1015 3316); University of South Bohemia, Department of Botany, Faculty of Science, České Budějovice, Czech Republic (GRID:grid.14509.39) (ISNI:0000 0001 2166 4904) 
63  Herbier National du Gabon (CENAREST), IRET, Libreville, Gabon (GRID:grid.518436.d) (ISNI:0000 0001 0297 742X) 
64  University of Arizona, Department of Ecology and Evolutionary Biology, Tucson, USA (GRID:grid.134563.6) (ISNI:0000 0001 2168 186X); The Santa Fe Institute, Santa Fe, USA (GRID:grid.209665.e) (ISNI:0000 0001 1941 1940) 
65  Department of Environment and Science, Queensland Herbarium, Toowong, Australia (GRID:grid.209665.e) 
66  Université Nationale d’Agriculture, Ecole de Foresterie et Ingénierie du Bois, Kétou, Benin (GRID:grid.209665.e) 
67  Queen Mary University of London, School of Biological and Behavioural Sciences, London, UK (GRID:grid.4868.2) (ISNI:0000 0001 2171 1133); Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic (GRID:grid.447761.7) (ISNI:0000 0004 0396 9503) 
68  University of Exeter, Geography, College of Life and Environmental Sciences, Exeter, UK (GRID:grid.8391.3) (ISNI:0000 0004 1936 8024) 
69  Museu Paraense Emílio Goeldi. Coordenação de Ciências da Terra e Ecologia, Belém, Brasil (GRID:grid.452671.3) (ISNI:0000 0001 2175 1274) 
70  Natural Resources Institute Finland (Luke), Joensuu, Finland (GRID:grid.22642.30) (ISNI:0000 0004 4668 6757) 
71  University of Bern, Institute of Plant Sciences, Bern, Switzerland (GRID:grid.5734.5) (ISNI:0000 0001 0726 5157) 
72  Forest Research Institute Malaysia, Kuala Lumpur, Malaysia (GRID:grid.434305.5) (ISNI:0000 0001 2231 3604) 
73  Swedish University of Agricultural Sciences SLU, Department of Forest Resource Management, Umea, Sweden (GRID:grid.6341.0) (ISNI:0000 0000 8578 2742) 
74  Fondazione Edmund Mach, Research and Innovation Center, San Michele All’adige, Italy (GRID:grid.424414.3) (ISNI:0000 0004 1755 6224) 
75  Food and Agriculture Organization of the United Nations, Forestry Division, Rome, Italy (GRID:grid.420153.1) (ISNI:0000 0004 1937 0300) 
76  Glick Designs LLC, Hadley, USA (GRID:grid.424414.3) 
77  Royal Botanic Garden Edinburgh, Edinburgh, UK (GRID:grid.426106.7) (ISNI:0000 0004 0598 2103) 
78  University of Oxford, Department of Plant Sciences, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948) 
79  University of Bayreuth, Department of Plant Systematics, Bayreuth, Germany (GRID:grid.7384.8) (ISNI:0000 0004 0467 6972) 
80  University of Montpellier, Cirad, UPR Forêts et Sociétés, Montpellier, France (GRID:grid.121334.6) (ISNI:0000 0001 2097 0141); National Polytechnic Institute (INP-HB), Department of Forestry and Environment, Yamoussoukro, Côte d’Ivoire (GRID:grid.121334.6) 
81  Sippy Downs, Forest Research Institute, University of the Sunshine Coast, Queensland, Australia (GRID:grid.1034.6) (ISNI:0000 0001 1555 3415) 
82  Helmholtz GeoResearch Center (GFZ), Potsdam, Germany (GRID:grid.23731.34) (ISNI:0000 0000 9195 2461) 
83  The Royal Society for the Protection of Birds, Centre for Conservation Science, Sandy, UK (GRID:grid.421630.2) (ISNI:0000 0001 2110 3189); Liberia Office, Wild Chimpanzee Foundation, Monrovia, Liberia (GRID:grid.421630.2) 
84  Instituto de Investigaciones de la Amazonía Peruana, Iquitos, Peru (GRID:grid.493484.6) (ISNI:0000 0001 2177 4732) 
85  Stellenbosch University, Centre for Invasion Biology, Department of Mathematical Sciences, Stellenbosch, South Africa (GRID:grid.11956.3a) (ISNI:0000 0001 2214 904X); African Institute for Mathematical Sciences, Theoretical Ecology Unit, Cape Town, South Africa (GRID:grid.452296.e) (ISNI:0000 0000 9027 9156) 
86  France, AMAP, Univ Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, Montpellier, France (GRID:grid.503016.1) (ISNI:0000 0001 2160 870X) 
87  National Institute of Amazonian Research, Manaus, Brazil (GRID:grid.419220.c) (ISNI:0000 0004 0427 0577) 
88  Tokyo University of Agriculture, Department of Forest Science, Tokyo, Japan (GRID:grid.410772.7) (ISNI:0000 0001 0807 3368) 
89  Polish Academy of Sciences, Institute of Dendrology, Kórnik, Poland (GRID:grid.413454.3) (ISNI:0000 0001 1958 0162); Department of Game Management and Forest Protection, Poznań University of Life Sciences, Poznań, Poland (GRID:grid.410688.3) (ISNI:0000 0001 2157 4669) 
90  University of Warsaw, Faculty of Biology, Białowieża Geobotanical Station, Białowieża, Poland (GRID:grid.12847.38) (ISNI:0000 0004 1937 1290) 
91  University of Copenhagen, Department of Geosciences and Natural Resource Management, Copenhagen, Denmark (GRID:grid.5254.6) (ISNI:0000 0001 0674 042X) 
92  UNICAMP, Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, Brazil (GRID:grid.411087.b) (ISNI:0000 0001 0723 2494) 
93  University of Bristol, School of Biological Sciences, Bristol, UK (GRID:grid.5337.2) (ISNI:0000 0004 1936 7603) 
94  Korea Forest Promotion Institute, Division of Forest Resources Information, Seoul, South Korea (GRID:grid.5337.2) 
95  Bauman Moscow State Technical University, Forestry Faculty, Moscow, Russia (GRID:grid.61569.3d) (ISNI:0000 0001 0405 5955) 
96  Ghent University, CAVElab-Computational and Applied Vegetation Ecology, Department of Environment, Ghent, Belgium (GRID:grid.5342.0) (ISNI:0000 0001 2069 7798) 
97  Smithsonian Tropical Research Institute, CTFS-ForestGEO, Balboa, Panama (GRID:grid.438006.9) (ISNI:0000 0001 2296 9689) 
98  Colorado Mesa University, Department of Physical and Environmental Sciences, Grand Junction, USA (GRID:grid.419760.d) (ISNI:0000 0000 8544 1139) 
99  University of South Australia, UniSA STEM and Future Industries Institute, Adelaide, Australia (GRID:grid.1026.5) (ISNI:0000 0000 8994 5086) 
100  Dr Harisingh Gour Vishwavidyalaya (A Central University), Department of Botany, Sagar, India (GRID:grid.444707.4) (ISNI:0000 0001 0562 4048) 
101  Seoul National University, Department of Agriculture, Forestry and Bioresources, Seoul, South Korea (GRID:grid.31501.36) (ISNI:0000 0004 0470 5905); Seoul National University, Interdisciplinary Program in Agricultural and Forest Meteorology, Seoul, South Korea (GRID:grid.31501.36) (ISNI:0000 0004 0470 5905); National Center for Agro Meteorology, Seoul, South Korea (GRID:grid.31501.36); Seoul National University, Research Institute for Agriculture and Life Sciences, Seoul, South Korea (GRID:grid.31501.36) (ISNI:0000 0004 0470 5905) 
102  Kyoto University, Graduate School of Agriculture, Kyoto, Japan (GRID:grid.258799.8) (ISNI:0000 0004 0372 2033) 
103  University of Hamburg, Institute for World Forestry, Hamburg, Germany (GRID:grid.9026.d) (ISNI:0000 0001 2287 2617) 
104  Estonian University of Life Sciences, Institute of Forestry and Engineering, Tartu, Estonia (GRID:grid.16697.3f) (ISNI:0000 0001 0671 1127) 
105  International Institute for Applied Systems Analysis, Ecosystems Services and Management, Laxenburg, Austria (GRID:grid.75276.31) (ISNI:0000 0001 1955 9478) 
106  University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403); University College London, Department of Geography, London, UK (GRID:grid.83440.3b) (ISNI:0000 0001 2190 1201) 
107  Qingdao Agricultural University, Faculty of Forestry, Qingdao, China (GRID:grid.412608.9) (ISNI:0000 0000 9526 6338) 
108  Russian Academy of Sciences, Center for Forest Ecology and Productivity, Moscow, Russia (GRID:grid.4886.2) (ISNI:0000 0001 2192 9124) 
109  University of Arizona, Department of Ecology and Evolutionary Biology, Tucson, USA (GRID:grid.134563.6) (ISNI:0000 0001 2168 186X) 
110  University of Oxford, School of Geography, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948) 
111  Université de Montpellier, AgroParisTech, UMR-AMAP, Cirad, CNRS, INRA, IRD, Montpellier, France (GRID:grid.121334.6) (ISNI:0000 0001 2097 0141) 
112  Universidade do Estado de Mato Grosso, Departamento de Ciências Biológicas, Nova Xavantina, Brazil (GRID:grid.442109.a) (ISNI:0000 0001 0302 3978) 
113  Sippy Downs, Forest Research Institute, University of the Sunshine Coast, Queensland, Australia (GRID:grid.1034.6) (ISNI:0000 0001 1555 3415); University of York, Department of Environment and Geography, York, UK (GRID:grid.5685.e) (ISNI:0000 0004 1936 9668); Flamingo Land Ltd, Kirby Misperton, UK (GRID:grid.5685.e) 
114  College of African Wildlife Management, Department of Wildlife Management, Mweka, Tanzania (GRID:grid.442468.8) (ISNI:0000 0001 0566 9529) 
115  Peoples Friendship University of Russia (RUDN University), Moscow, Russia (GRID:grid.77642.30) (ISNI:0000 0004 0645 517X) 
116  Universidad Nacional Autónoma de México, Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Mexico City, Mexico (GRID:grid.9486.3) (ISNI:0000 0001 2159 0001) 
117  Universidad del Tolima, Ibagué, Colombia (GRID:grid.412192.d) (ISNI:0000 0001 2168 0760) 
118  Colegio de Profesionales Forestales de Cochabamba, Universidad Mayor de San Simón, Escuela de Ciencias Forestales, Cochabamba, Bolivia (GRID:grid.10491.3d) (ISNI:0000 0001 2176 4059) 
119  University of Connecticut, Department of Ecology and Evolutionary Biology, Storrs, USA (GRID:grid.63054.34) (ISNI:0000 0001 0860 4915) 
120  Jardín Botánico de Missouri, Pasco, Peru (GRID:grid.63054.34); Universidad Nacional de San Antonio Abad del Cusco, Cusco, Peru (GRID:grid.449379.4) (ISNI:0000 0001 2198 6786) 
121  United International University, Department of Environment and Development Studies, Dhaka, Bangladesh (GRID:grid.443055.3) (ISNI:0000 0001 2289 6109); Centre for Research on Land-use Sustainability, Dhaka, Bangladesh (GRID:grid.443055.3) 
122  Colegio de Ciencias y Humanidades. Universidad Juárez del Estado de Durango, Durango, Mexico (GRID:grid.412198.7) (ISNI:0000 0000 8724 8383); Programa de doctorado en Ingeniería para el desarrollo rural y civil. Escuela de Doctorado Internacional de la Universidad de Santiago de Compostela (EDIUS), Santiago de Compostela, Spain (GRID:grid.11794.3a) (ISNI:0000000109410645) 
123  Universidad Estatal Amazónica, Puyo, Ecuador (GRID:grid.440858.5) (ISNI:0000 0004 0381 4018) 
124  Department of Environment and Science, Queensland Herbarium, Toowong, Australia (GRID:grid.440858.5) 
125  Department of Environment and Science, Queensland Herbarium, Toowong, Australia (GRID:grid.512559.f) 
126  University of Zürich, Department of Geography, Remote Sensing Laboratories, Zurich, Switzerland (GRID:grid.7400.3) (ISNI:0000 0004 1937 0650) 
127  Polish Academy of Sciences, Institute of Dendrology, Kórnik, Poland (GRID:grid.413454.3) (ISNI:0000 0001 1958 0162) 
128  USDA Forest Service, Climate, Fire, and Carbon Cycle Sciences, Durham, USA (GRID:grid.472551.0) (ISNI:0000 0004 0404 3120) 
129  Université du Québec à Montréal, Centre for Forest Research, Montréal, Canada (GRID:grid.38678.32) (ISNI:0000 0001 2181 0211) 
130  Siberian Branch of the Russian Academy of Sciences, V. N. Sukachev Institute of Forest, FRC KSC, Krasnoyarsk, Russia (GRID:grid.415877.8) (ISNI:0000 0001 2254 1834) 
131  Purdue University, Department of Forestry and Natural Resources, West Lafayette, USA (GRID:grid.169077.e) (ISNI:0000 0004 1937 2197); Seoul National University, Department of Agriculture, Forestry and Bioresources, Seoul, South Korea (GRID:grid.31501.36) (ISNI:0000 0004 0470 5905) 
132  Wageningen University & Research, Forest Ecology and Forest Management Group, Wageningen, The Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666) 
133  Pondicherry University, Department of Ecology and Environmental Sciences, Puducherry, India (GRID:grid.412517.4) (ISNI:0000 0001 2152 9956) 
134  Consejo Nacional de Investigaciones Científicas y Tecnicas (CONICET), Instituto Nacional de Tecnología Agropecuaria (INTA), Universidad Nacional de la Patagonia Austral (UNPA), Río Gallegos, Argentina (GRID:grid.423606.5) (ISNI:0000 0001 1945 2152) 
135  Western Sydney University, School of Social Sciences (Urban Studies), Penrith, Australia (GRID:grid.1029.a) (ISNI:0000 0000 9939 5719) 
136  Food and Agriculture Organization of the United Nations, Forestry Department, Rome, Italy (GRID:grid.420153.1) (ISNI:0000 0004 1937 0300) 
137  Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil (GRID:grid.419220.c) (ISNI:0000 0004 0427 0577) 
138  Universidade Federal do Sul da Bahia, Laboratório de Dendrologia e Silvicultura Tropical, Centro de Formação em Ciências Agroflorestais, Itabuna, Brazil (GRID:grid.473011.0) (ISNI:0000 0004 4685 7624) 
139  Jardín Botánico de Medellín, Medellin, Colombia (GRID:grid.299784.9) 
140  Duke University, Nicholas School of the Environment, Durham, USA (GRID:grid.26009.3d) (ISNI:0000 0004 1936 7961); The Nature Conservancy, Boulder, USA (GRID:grid.422375.5) (ISNI:0000 0004 0591 6771) 
141  Technical University of Munich, Chair for Forest Growth and Yield Science, TUM School for Life Sciences, Munich, Germany (GRID:grid.6936.a) (ISNI:0000 0001 2322 2966) 
142  Universidad Nacional de la Amazonía Peruana, Iquitos, Peru (GRID:grid.440594.8) (ISNI:0000 0000 8866 0281) 
143  Fundación Con Vida & Corporación COL-TREE, Servicios Ecosistémicos y Cambio Climático (SECC), Medellín, Colombia (GRID:grid.511000.5) 
144  Fondazione Edmund Mach, Research and Innovation Center, San Michele All’adige, Italy (GRID:grid.424414.3) (ISNI:0000 0004 1755 6224); University of Trento, Centro Agricoltura, Alimenti, Ambiente, San Michele All’adige, Italy (GRID:grid.11696.39) (ISNI:0000 0004 1937 0351) 
145  Boise State University, Department of Biological Sciences, Boise, USA (GRID:grid.184764.8) (ISNI:0000 0001 0670 228X) 
146  University of Florence, Department of Biology, Florence, Italy (GRID:grid.8404.8) (ISNI:0000 0004 1757 2304); MUSE - Museo delle Scienze, Tropical Biodiversity, Trento, Italy (GRID:grid.436694.a) (ISNI:0000 0001 2154 5833) 
147  Info Flora, Geneva, Switzerland (GRID:grid.436694.a) 
148  Central University of Jharkhand, Department of Environmental Sciences, Ranchi, India (GRID:grid.448765.c) (ISNI:0000 0004 1764 7388) 
149  Universidad Mayor, Centro de Modelación y Monitoreo de Ecosistemas, Santiago, Chile (GRID:grid.412199.6) (ISNI:0000 0004 0487 8785); Universidad de La Frontera, Vicerrectoria de Investigacion y Postgrado, Temuco, Chile (GRID:grid.412163.3) (ISNI:0000 0001 2287 9552); Universidad de Chile, Depto. de Silvicultura y Conservacion de la Naturaleza, Temuco, Chile (GRID:grid.443909.3) (ISNI:0000 0004 0385 4466) 
150  Datascientist.ch, Wallisellen, Switzerland (GRID:grid.443909.3) 
151  International Institute for Applied Systems Analysis, Ecosystems Services and Management, Laxenburg, Austria (GRID:grid.75276.31) (ISNI:0000 0001 1955 9478); Peoples Friendship University of Russia (RUDN University), Moscow, Russia (GRID:grid.77642.30) (ISNI:0000 0004 0645 517X) 
152  University of Freiburg, Geobotany, Faculty of Biology, Freiburg im Breisgau, Germany (GRID:grid.5963.9) (ISNI:0000 0004 0491 7203) 
153  Forest Research Institute Zvolen, National Forest Centre, Zvolen, Slovakia (GRID:grid.454939.6) (ISNI:0000 0004 0371 4164) 
154  University of Connecticut, Department of Ecology and Evolutionary Biology, Storrs, USA (GRID:grid.63054.34) (ISNI:0000 0001 0860 4915); INRAE, Université de Lorraine, AgroParisTech, Silva, France (GRID:grid.507621.7) 
155  Wageningen University & Research, Forest Ecology and Forest Management Group, Wageningen, The Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666); Norwegian University of Life Sciences, Faculty of Environmental Sciences and Natural Resource Management, Ås, Norway (GRID:grid.19477.3c) (ISNI:0000 0004 0607 975X) 
156  International Institute for Applied Systems Analysis, Ecosystems Services and Management, Laxenburg, Austria (GRID:grid.75276.31) (ISNI:0000 0001 1955 9478); Russian Academy of Sciences, Center for Forest Ecology and Productivity, Moscow, Russia (GRID:grid.4886.2) (ISNI:0000 0001 2192 9124) 
157  Universidad de la Serena, Departamento de Biología, La Serena, Chile (GRID:grid.19208.32) (ISNI:0000 0001 0161 9268) 
158  Universidade Federal do Acre, Centro de Ciências Biológicas e da Natureza, Rio Branco, Brazil (GRID:grid.412369.b) (ISNI:0000 0000 9887 315X) 
159  Guyana Forestry Commission, Georgetown, French Guiana (GRID:grid.494195.4) 
160  University of Montpellier, Cirad, UPR Forêts et Sociétés, Montpellier, France (GRID:grid.121334.6) (ISNI:0000 0001 2097 0141) 
161  Universiti Brunei Darussalam, Environmental and Life Sciences, Faculty of Science, Bandar Seri Begawan, Brunei Darussalam (GRID:grid.440600.6) (ISNI:0000 0001 2170 1621) 
162  University of Yaoundé I, Plant Systematic and Ecology Laboratory, Department of Biology, Higher Teachers’ Training College, Yaoundé, Cameroon (GRID:grid.412661.6) (ISNI:0000 0001 2173 8504) 
163  Universidade Federal do Rio Grande do Norte, Departamento de Ecologia, Natal, Brazil (GRID:grid.411233.6) (ISNI:0000 0000 9687 399X) 
164  Warsaw University of Life Sciences, Department of Forest Management, Dendrometry and Forest Economics, Warsaw, Poland (GRID:grid.13276.31) (ISNI:0000 0001 1955 7966) 
165  Aarhus University, Center for Ecological Dynamics in a Novel Biosphere (ECONOVO), Department of Biology, Aarhus, Denmark (GRID:grid.7048.b) (ISNI:0000 0001 1956 2722) 
166  Czech University of Life Sciences, Faculty of Forestry and Wood Sciences, Prague, Czech Republic (GRID:grid.15866.3c) (ISNI:0000 0001 2238 631X) 
167  Wildlife Conservation Society, New York, USA (GRID:grid.269823.4) (ISNI:0000 0001 2164 6888) 
168  Naturalis Biodiversity Center, Leiden, The Netherlands (GRID:grid.425948.6) (ISNI:0000 0001 2159 802X); Utrecht University, Quantitative Biodiversity Dynamics, Dept. of Biology, Utrecht, The Netherlands (GRID:grid.5477.1) (ISNI:0000 0000 9637 0671) 
169  Iwokrama International Centre for Rain Forest Conservation and Development, Kurupukari, Guyana (GRID:grid.510980.5) (ISNI:0000 0000 8818 8351) 
170  Yale University, School of Forestry and Environmental Studies, New Haven, USA (GRID:grid.47100.32) (ISNI:0000 0004 1936 8710) 
171  Ural State Forest Engineering University, Botanical Garden of Ural Branch of Russian Academy of Sciences, Yekaterinburg, Russia (GRID:grid.446276.5) (ISNI:0000 0004 0543 9127) 
172  Pontificia Universidad Católica del Ecuador, Quito, Ecuador (GRID:grid.412527.7) (ISNI:0000 0001 1941 7306) 
173  CSIC, LINCGlobal, Museo Nacional de Ciencias Naturales, Madrid, Spain (GRID:grid.420025.1) (ISNI:0000 0004 1768 463X) 
174  Wageningen University, Plant Ecology and Nature Conservation Group, Wageningen, The Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666) 
175  Vietnamese Academy of Forest Sciences, Silviculture Research Institute, Hanoi, Vietnam (GRID:grid.4818.5) 
176  Stanford University, Department of Biology, Stanford, USA (GRID:grid.168010.e) (ISNI:0000 0004 1936 8956) 
177  Jardín Botánico de Missouri, Pasco, Peru (GRID:grid.168010.e) 
178  Ghent University, Q-ForestLab, Department of Environment, Ghent, Belgium (GRID:grid.5342.0) (ISNI:0000 0001 2069 7798) 
179  UTAD, Centre for the Research and Technology of Agro-Environmental and Biological Sciences, CITAB, University of Trás-os-Montes and Alto Douro, Vila Real, Portugal (GRID:grid.12341.35) (ISNI:0000 0001 2182 1287); Polytechnic Institute of Viseu, Department of Ecology and Sustainable Agriculture, Agricultural High School, Viseu, Portugal (GRID:grid.410929.7) (ISNI:0000 0000 9512 0160) 
180  Universidade Regional de Blumenau, Natural Science Department, Blumenau, Brazil (GRID:grid.412404.7) (ISNI:0000 0000 9143 5704); Department of Forest Engineering Universidade Regional de Blumenau, Blumenau, Brazil (GRID:grid.412404.7) (ISNI:0000 0000 9143 5704) 
181  UNICAMP, Environmental Studies and Research Center, University of Campinas, Campinas, Brazil (GRID:grid.411087.b) (ISNI:0000 0001 0723 2494) 
182  University of Stellenbosch, Department of Forest and Wood Science, Stellenbosch, South Africa (GRID:grid.11956.3a) (ISNI:0000 0001 2214 904X) 
183  Hainan University, Key Laboratory of Tropical Biological Resources, Ministry of Education, School of Life and Pharmaceutical Sciences, Haikou, China (GRID:grid.428986.9) (ISNI:0000 0001 0373 6302) 
184  West Virginia University, Division of Forestry and Natural Resources, Morgantown, USA (GRID:grid.268154.c) (ISNI:0000 0001 2156 6140) 
185  University of Oxford, Department of Zoology, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948) 
186  Manaaki Whenua–Landcare Research, Lincoln, New Zealand (GRID:grid.419186.3) (ISNI:0000 0001 0747 5306) 
187  Karlsruhe Institute for Technology, Department of Wetland Ecology, Institute for Geography and Geoecology, Karlsruhe, Germany (GRID:grid.7892.4) (ISNI:0000 0001 0075 5874) 
188  Sommersbergseestrasse, Independent Researcher, Bad Aussee, Austria (GRID:grid.7892.4) 
189  Centre for Agricultural Research in Suriname (CELOS), Paramaribo, Suriname (GRID:grid.7892.4) 
190  Tropenbos International, Wageningen, The Netherlands (GRID:grid.510994.0) 
191  Coordination Center for Environmental Projects, Polish State Forests, Warsaw, Poland (GRID:grid.510994.0) 
192  Beijing Forestry University, Research Center of Forest Management Engineering of State Forestry and Grassland Administration, Beijing, China (GRID:grid.66741.32) (ISNI:0000 0001 1456 856X) 
193  National Polytechnic Institute (INP-HB), Department of Forestry and Environment, Yamoussoukro, Côte d’Ivoire (GRID:grid.428986.9) 
Pages
4658
Publication year
2024
Publication date
2024
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
3062789476
Copyright
© The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.