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1. Co-limitation towards lower latitudes shapes global forest diversity gradients

Author

Liang, J., Gamarra, J.G.P., Picard, N., Zhou, M., Pijanowski, B., Jacobs, D.F., Reich, P.B., Crowther, T.W., Nabuurs, G.-J., de-Miguel, S., Fang, J., Woodall, C.W., Svenning, J.-C., Jucker, T., Bastin, J.-F., Wiser, S.K., Slik, F., Hérault, B., Alberti, G., Keppel, G., Hengeveld, G.M., Ibisch, P.L., Silva, C.A., ter Steege, H., Peri, P.L., Coomes, D.A., Searle, E.B., von Gadow, K., Jaroszewicz, B., Abbasi, A.O., Abegg, M., Yao, Y.C. A., Aguirre-Gutiérrez, J., Zambrano, A.M.A., Altman, J., Alvarez-Dávila, E., Álvarez-González, J.G., Alves, L.F., Amani, B.H.K., Amani, C.A., Ammer, C., Ilondea, B.A., Antón-Fernández, C., Avitabile, V., Aymard, G.A., Azihou, A.F., Baard, J.A., Baker, T.R., Balazy, R., Bastian, M.L., Batumike, R., Bauters, M., Beeckman, H., Benu, N.M.H., Bitariho, R., Boeckx, P., Bogaert, J., Bongers, F., Bouriaud, O., Brancalion, P.H.S., Brandl, S., Brearley, F. Q., Briseno-Reyes, J., Broadbent, E.N., Bruelheide, H., Bulte, E., Catlin, A.C., Cazzolla Gatti, R., César, R.G., Chen, H.Y. H., Chisholm, C., Cienciala, E., Colletta, G.D., Corral-Rivas, J.J., Cuchietti, A., Cuni-Sanchez, A., Dar, J.A., Dayanandan, S., de Haulleville, T., Decuyper, M., Delabye, S., Derroire, G., DeVries, B., Diisi, J., Do, T.V., Dolezal, J., Dourdain, A., Durrheim, G.P., Obiang, N.L.E., Ewango, C.E.N., Eyre, T.J., Fayle, T.M., Feunang, L.F.N., Finér, L., Fischer, M., Fridman, J., Frizzera, Lorenzo., de Gasper, A.L., Gianelle, D., Glick, H.B., Gonzalez-Elizondo, M.S., Gorenstein, Lev., Habonayo, R., Hardy, O.J., Harris, D.J., Hector, A., Hemp, A., Herold, M., Hillers, A., Hubau, W., Ibanez, T., Imai, N., Imani, G., Jagodzinski, A.M., Janecek, S., Johannsen, V.K., Joly, C.A., Jumbam, B., Kabelong, B. L. P. R., Kahsay, G.A., Karminov, V., Kartawinata, K., Kassi, J.ustin N., Kearsley, E., Kennard, D.K., Kepfer-Rojas, S., Khan, M. L., Kigomo, J.N., Kim, H.S., Klauberg, C., Klomberg, Y., Korjus, H., Kothandaraman, S., Kraxner, F., Kumar, A., Kuswandi, R., Lang, M., Lawes, M.J., Leite, R.V., Lentner, G., Lewis, S.L., Libalah, M.B., Lisingo, Janvier, López-Serrano, P.M., Lu, H., Lukina, N.V., Lykke, A.M., Maicher, V., Maitner, B.S., Marcon, E., Marshall, A.R., Martin, E. H., Martynenko, O., Mbayu, F.M., Mbuvi, M. T. E., Meave, J. A., Merow, C., Miscicki, S., Moreno, V. S., Morera, A., Mukul, S.A., Müller, J.C., Murdjoko, A., Nava-Miranda, M.G., Ndive, L.E., Neldner, V.J., Nevenic, R.V., Nforbelie, L.N., Ngoh, M.L., N’Guessan, A.E., Ngugi, M.R., Ngute, A. S. K., Njila, E. N. N., Nyako, M.C., Ochuodho, T.O., Oleksyn, J., Paquette, A., Parfenova, E.I., Park, M., Parren, M., Parthasarathy, N., Pfautsch, S., Phillips, O. L., Piedade, M.T. F., Piotto, D., Pollastrini, M., Poorter, L., Poulsen, J. R., Poulsen, A.D., Pretzsch, H., Rodeghiero, M., Rolim, S.G., Rovero, F., Rutishauser, E., Sagheb-Talebi, K., Saikia, P., Sainge, M.N., Salas-Eljatib, C., Salis, A., Schall, P., Shchepashchenko, D., Scherer-Lorenzen, M., Schmid, B., Schöngart, J., Šebeň, V., Sellan, G., Selvi, F., Serra-Diaz, J.M., Sheil, D., Shvidenko, A., Sist, P., Souza, A.F., Stereńczak, K.J., Sullivan, M. J. P., Sundarapandian, S., Svoboda, M., Swaine, M.D., Targhetta, N., Tchebakova, N., Trethowan, L.A., Tropek, R., Mukendi, J.T., Umunay, P.M., Usoltsev, V.A., Vaglio Laurin, G., Valentini, R., Valladares, F., van der Plas, F., Vega-Nieva, D.J., Verbeeck, H., Viana, H., Vibrans, A.C., Vieira, S.A., Vleminckx, J., Waite, C.E., Wang, H.-F., Wasingya, E.K., Wekesa, C., Westerlund, B., Wittmann, F., Wortel, V., Zawiła-Niedźwiecki, T., Zhang, C., Zhao, X., Zhu, J., Zhu, X., Zhu, Z.-X., Zo-Bi, I.C., Hui, C., Liang, J., Gamarra, J.G.P., Picard, N., Zhou, M., Pijanowski, B., Jacobs, D.F., Reich, P.B., Crowther, T.W., Nabuurs, G.-J., de-Miguel, S., Fang, J., Woodall, C.W., Svenning, J.-C., Jucker, T., Bastin, J.-F., Wiser, S.K., Slik, F., Hérault, B., Alberti, G., Keppel, G., Hengeveld, G.M., Ibisch, P.L., Silva, C.A., ter Steege, H., Peri, P.L., Coomes, D.A., Searle, E.B., von Gadow, K., Jaroszewicz, B., Abbasi, A.O., Abegg, M., Yao, Y.C. A., Aguirre-Gutiérrez, J., Zambrano, A.M.A., Altman, J., Alvarez-Dávila, E., Álvarez-González, J.G., Alves, L.F., Amani, B.H.K., Amani, C.A., Ammer, C., Ilondea, B.A., Antón-Fernández, C., Avitabile, V., Aymard, G.A., Azihou, A.F., Baard, J.A., Baker, T.R., Balazy, R., Bastian, M.L., Batumike, R., Bauters, M., Beeckman, H., Benu, N.M.H., Bitariho, R., Boeckx, P., Bogaert, J., Bongers, F., Bouriaud, O., Brancalion, P.H.S., Brandl, S., Brearley, F. Q., Briseno-Reyes, J., Broadbent, E.N., Bruelheide, H., Bulte, E., Catlin, A.C., Cazzolla Gatti, R., César, R.G., Chen, H.Y. H., Chisholm, C., Cienciala, E., Colletta, G.D., Corral-Rivas, J.J., Cuchietti, A., Cuni-Sanchez, A., Dar, J.A., Dayanandan, S., de Haulleville, T., Decuyper, M., Delabye, S., Derroire, G., DeVries, B., Diisi, J., Do, T.V., Dolezal, J., Dourdain, A., Durrheim, G.P., Obiang, N.L.E., Ewango, C.E.N., Eyre, T.J., Fayle, T.M., Feunang, L.F.N., Finér, L., Fischer, M., Fridman, J., Frizzera, Lorenzo., de Gasper, A.L., Gianelle, D., Glick, H.B., Gonzalez-Elizondo, M.S., Gorenstein, Lev., Habonayo, R., Hardy, O.J., Harris, D.J., Hector, A., Hemp, A., Herold, M., Hillers, A., Hubau, W., Ibanez, T., Imai, N., Imani, G., Jagodzinski, A.M., Janecek, S., Johannsen, V.K., Joly, C.A., Jumbam, B., Kabelong, B. L. P. R., Kahsay, G.A., Karminov, V., Kartawinata, K., Kassi, J.ustin N., Kearsley, E., Kennard, D.K., Kepfer-Rojas, S., Khan, M. L., Kigomo, J.N., Kim, H.S., Klauberg, C., Klomberg, Y., Korjus, H., Kothandaraman, S., Kraxner, F., Kumar, A., Kuswandi, R., Lang, M., Lawes, M.J., Leite, R.V., Lentner, G., Lewis, S.L., Libalah, M.B., Lisingo, Janvier, López-Serrano, P.M., Lu, H., Lukina, N.V., Lykke, A.M., Maicher, V., Maitner, B.S., Marcon, E., Marshall, A.R., Martin, E. H., Martynenko, O., Mbayu, F.M., Mbuvi, M. T. E., Meave, J. A., Merow, C., Miscicki, S., Moreno, V. S., Morera, A., Mukul, S.A., Müller, J.C., Murdjoko, A., Nava-Miranda, M.G., Ndive, L.E., Neldner, V.J., Nevenic, R.V., Nforbelie, L.N., Ngoh, M.L., N’Guessan, A.E., Ngugi, M.R., Ngute, A. S. K., Njila, E. N. N., Nyako, M.C., Ochuodho, T.O., Oleksyn, J., Paquette, A., Parfenova, E.I., Park, M., Parren, M., Parthasarathy, N., Pfautsch, S., Phillips, O. L., Piedade, M.T. F., Piotto, D., Pollastrini, M., Poorter, L., Poulsen, J. R., Poulsen, A.D., Pretzsch, H., Rodeghiero, M., Rolim, S.G., Rovero, F., Rutishauser, E., Sagheb-Talebi, K., Saikia, P., Sainge, M.N., Salas-Eljatib, C., Salis, A., Schall, P., Shchepashchenko, D., Scherer-Lorenzen, M., Schmid, B., Schöngart, J., Šebeň, V., Sellan, G., Selvi, F., Serra-Diaz, J.M., Sheil, D., Shvidenko, A., Sist, P., Souza, A.F., Stereńczak, K.J., Sullivan, M. J. P., Sundarapandian, S., Svoboda, M., Swaine, M.D., Targhetta, N., Tchebakova, N., Trethowan, L.A., Tropek, R., Mukendi, J.T., Umunay, P.M., Usoltsev, V.A., Vaglio Laurin, G., Valentini, R., Valladares, F., van der Plas, F., Vega-Nieva, D.J., Verbeeck, H., Viana, H., Vibrans, A.C., Vieira, S.A., Vleminckx, J., Waite, C.E., Wang, H.-F., Wasingya, E.K., Wekesa, C., Westerlund, B., Wittmann, F., Wortel, V., Zawiła-Niedźwiecki, T., Zhang, C., Zhao, X., Zhu, J., Zhu, X., Zhu, Z.-X., Zo-Bi, I.C., and Hui, C.

Published
2022
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2. High exposure of global tree diversity to human pressure

Author

Guo, W-Y, Serra-Diaz, J.M., Schrodt, F., Eiserhardt, W.L., Maitner, B.S., Merow, C., Violle, C., Anand, M., Belluau, M., Bruun, H.H., Byun, C., Catford, J.A., Cerabolini, B.E.L., Chacón-Madrigal, E., Ciccarelli, D., Cornelissen, J.H.C., Dang-Le, A.T., De Frutos, A., Dias, A.S., Giroldo, A.B., Guo, K., Gutiérrez, A.G., Hattingh, W., He, T., Hietz, P., Hough-Snee, N., Jansen, S., Kattge, J., Klein, T., Komac, B., Kraft, N.J.B., Kramer, K., Lavorel, S., Lusk, C.H., Martin, A.R., Mencuccini, M., Michaletz, S.T., Minden, V., Mori, A.S., Niinemets, Ü., Onoda, Y., Peñuelas, J., Pillar, V.D., Pisek, J., Robroek, B.J.M., Schamp, B., Slot, M., Sosinski, E.E., Soudzilovskaia, N.A., Thiffault, N., van Bodegom, P., van der Plas, F., Wright, I.J., Xu, W-B, Zheng, J., Enquist, B.J., Svenning, J-C, Guo, W-Y, Serra-Diaz, J.M., Schrodt, F., Eiserhardt, W.L., Maitner, B.S., Merow, C., Violle, C., Anand, M., Belluau, M., Bruun, H.H., Byun, C., Catford, J.A., Cerabolini, B.E.L., Chacón-Madrigal, E., Ciccarelli, D., Cornelissen, J.H.C., Dang-Le, A.T., De Frutos, A., Dias, A.S., Giroldo, A.B., Guo, K., Gutiérrez, A.G., Hattingh, W., He, T., Hietz, P., Hough-Snee, N., Jansen, S., Kattge, J., Klein, T., Komac, B., Kraft, N.J.B., Kramer, K., Lavorel, S., Lusk, C.H., Martin, A.R., Mencuccini, M., Michaletz, S.T., Minden, V., Mori, A.S., Niinemets, Ü., Onoda, Y., Peñuelas, J., Pillar, V.D., Pisek, J., Robroek, B.J.M., Schamp, B., Slot, M., Sosinski, E.E., Soudzilovskaia, N.A., Thiffault, N., van Bodegom, P., van der Plas, F., Wright, I.J., Xu, W-B, Zheng, J., Enquist, B.J., and Svenning, J-C

Abstract

Safeguarding Earth’s tree diversity is a conservation priority due to the importance of trees for biodiversity and ecosystem functions and services such as carbon sequestration. Here, we improve the foundation for effective conservation of global tree diversity by analyzing a recently developed database of tree species covering 46,752 species. We quantify range protection and anthropogenic pressures for each species and develop conservation priorities across taxonomic, phylogenetic, and functional diversity dimensions. We also assess the effectiveness of several influential proposed conservation prioritization frameworks to protect the top 17% and top 50% of tree priority areas. We find that an average of 50.2% of a tree species’ range occurs in 110-km grid cells without any protected areas (PAs), with 6,377 small-range tree species fully unprotected, and that 83% of tree species experience nonnegligible human pressure across their range on average. Protecting high-priority areas for the top 17% and 50% priority thresholds would increase the average protected proportion of each tree species’ range to 65.5% and 82.6%, respectively, leaving many fewer species (2,151 and 2,010) completely unprotected. The priority areas identified for trees match well to the Global 200 Ecoregions framework, revealing that priority areas for trees would in large part also optimize protection for terrestrial biodiversity overall. Based on range estimates for >46,000 tree species, our findings show that a large proportion of tree species receive limited protection by current PAs and are under substantial human pressure. Improved protection of biodiversity overall would also strongly benefit global tree diversity.

Published
2022

3. The number of tree species on Earth

Author

Roberto Cazzolla Gatti, Peter B. Reich, Javier G. P. Gamarra, Tom Crowther, Cang Hui, Albert Morera, Jean-Francois Bastin, Sergio de-Miguel, Gert-Jan Nabuurs, Jens-Christian Svenning, Josep M. Serra-Diaz, Cory Merow, Brian Enquist, Maria Kamenetsky, Junho Lee, Jun Zhu, Jinyun Fang, Douglass F. Jacobs, Bryan Pijanowski, Arindam Banerjee, Robert A. Giaquinto, Giorgio Alberti, Angelica Maria Almeyda Zambrano, Esteban Alvarez-Davila, Alejandro Araujo-Murakami, Valerio Avitabile, Gerardo A. Aymard, Radomir Balazy, Chris Baraloto, Jorcely G. Barroso, Meredith L. Bastian, Philippe Birnbaum, Robert Bitariho, Jan Bogaert, Frans Bongers, Olivier Bouriaud, Pedro H. S. Brancalion, Francis Q. Brearley, Eben North Broadbent, Filippo Bussotti, Wendeson Castro da Silva, Ricardo Gomes César, Goran Češljar, Víctor Chama Moscoso, Han Y. H. Chen, Emil Cienciala, Connie J. Clark, David A. Coomes, Selvadurai Dayanandan, Mathieu Decuyper, Laura E. Dee, Jhon Del Aguila Pasquel, Géraldine Derroire, Marie Noel Kamdem Djuikouo, Tran Van Do, Jiri Dolezal, Ilija Đ. Đorđević, Julien Engel, Tom M. Fayle, Ted R. Feldpausch, Jonas K. Fridman, David J. Harris, Andreas Hemp, Geerten Hengeveld, Bruno Herault, Martin Herold, Thomas Ibanez, Andrzej M. Jagodzinski, Bogdan Jaroszewicz, Kathryn J. Jeffery, Vivian Kvist Johannsen, Tommaso Jucker, Ahto Kangur, Victor N. Karminov, Kuswata Kartawinata, Deborah K. Kennard, Sebastian Kepfer-Rojas, Gunnar Keppel, Mohammed Latif Khan, Pramod Kumar Khare, Timothy J. Kileen, Hyun Seok Kim, Henn Korjus, Amit Kumar, Ashwani Kumar, Diana Laarmann, Nicolas Labrière, Mait Lang, Simon L. Lewis, Natalia Lukina, Brian S. Maitner, Yadvinder Malhi, Andrew R. Marshall, Olga V. Martynenko, Abel L. Monteagudo Mendoza, Petr V. Ontikov, Edgar Ortiz-Malavasi, Nadir C. Pallqui Camacho, Alain Paquette, Minjee Park, Narayanaswamy Parthasarathy, Pablo Luis Peri, Pascal Petronelli, Sebastian Pfautsch, Oliver L. Phillips, Nicolas Picard, Daniel Piotto, Lourens Poorter, John R. Poulsen, Hans Pretzsch, Hirma Ramírez-Angulo, Zorayda Restrepo Correa, Mirco Rodeghiero, Rocío Del Pilar Rojas Gonzáles, Samir G. Rolim, Francesco Rovero, Ervan Rutishauser, Purabi Saikia, Christian Salas-Eljatib, Dmitry Schepaschenko, Michael Scherer-Lorenzen, Vladimír Šebeň, Marcos Silveira, Ferry Slik, Bonaventure Sonké, Alexandre F. Souza, Krzysztof Jan Stereńczak, Miroslav Svoboda, Hermann Taedoumg, Nadja Tchebakova, John Terborgh, Elena Tikhonova, Armando Torres-Lezama, Fons van der Plas, Rodolfo Vásquez, Helder Viana, Alexander C. Vibrans, Emilio Vilanova, Vincent A. Vos, Hua-Feng Wang, Bertil Westerlund, Lee J. T. White, Susan K. Wiser, Tomasz Zawiła-Niedźwiecki, Lise Zemagho, Zhi-Xin Zhu, Irié C. Zo-Bi, Jingjing Liang, Cazzolla Gatti, Roberto, Reich, Peter B, Gamarra, Javier GP, Crowther, Tom, Keppel, Gunnar, Liang, Jingjing, Cazzolla Gatti R., Reich P.B., Gamarra J.G.P., Crowther T., Hui C., Morera A., Bastin J.-F., de-Miguel S., Nabuurs G.-J., Svenning J.-C., Serra-Diaz J.M., Merow C., Enquist B., Kamenetsky M., Lee J., Zhu J., Fang J., Jacobs D.F., Pijanowski B., Banerjee A., Giaquinto R.A., Alberti G., Almeyda Zambrano A.M., Alvarez-Davila E., Araujo-Murakami A., Avitabile V., Aymard G.A., Balazy R., Baraloto C., Barroso J.G., Bastian M.L., Birnbaum P., Bitariho R., Bogaert J., Bongers F., Bouriaud O., Brancalion P.H.S., Brearley F.Q., Broadbent E.N., Bussotti F., Castro da Silva W., Cesar R.G., Cesljar G., Chama Moscoso V., Chen H.Y.H., Cienciala E., Clark C.J., Coomes D.A., Dayanandan S., Decuyper M., Dee L.E., Del Aguila Pasquel J., Derroire G., Djuikouo M.N.K., Van Do T., Dolezal J., Dordevic I.D., Engel J., Fayle T.M., Feldpausch T.R., Fridman J.K., Harris D.J., Hemp A., Hengeveld G., Herault B., Herold M., Ibanez T., Jagodzinski A.M., Jaroszewicz B., Jeffery K.J., Johannsen V.K., Jucker T., Kangur A., Karminov V.N., Kartawinata K., Kennard D.K., Kepfer-Rojas S., Keppel G., Khan M.L., Khare P.K., Kileen T.J., Kim H.S., Korjus H., Kumar A., Laarmann D., Labriere N., Lang M., Lewis S.L., Lukina N., Maitner B.S., Malhi Y., Marshall A.R., Martynenko O.V., Monteagudo Mendoza A.L., Ontikov P.V., Ortiz-Malavasi E., Pallqui Camacho N.C., Paquette A., Park M., Parthasarathy N., Peri P.L., Petronelli P., Pfautsch S., Phillips O.L., Picard N., Piotto D., Poorter L., Poulsen J.R., Pretzsch H., Ramirez-Angulo H., Restrepo Correa Z., Rodeghiero M., Rojas Gonzales R.D.P., Rolim S.G., Rovero F., Rutishauser E., Saikia P., Salas-Eljatib C., Schepaschenko D., Scherer-Lorenzen M., Seben V., Silveira M., Slik F., Sonke B., Souza A.F., Sterenczak K.J., Svoboda M., Taedoumg H., Tchebakova N., Terborgh J., Tikhonova E., Torres-Lezama A., van der Plas F., Vasquez R., Viana H., Vibrans A.C., Vilanova E., Vos V.A., Wang H.-F., Westerlund B., White L.J.T., Wiser S.K., Zawila-Niedzwiecki T., Zemagho L., Zhu Z.-X., Zo-Bi I.C., Liang J., Purdue University [West Lafayette], University of Wisconsin-Madison, FAO Forestry, Food and Agriculture Organization of the United Nations [Rome, Italie] (FAO), SILVA (SILVA), AgroParisTech-Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Botanique et Modélisation de l'Architecture des Plantes et des Végétations (UMR AMAP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université de Montpellier (UM), Département Systèmes Biologiques (Cirad-BIOS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Institut de Recherche pour le Développement (IRD [Nouvelle-Calédonie]), Cazzolla Gatti, Roberto [0000-0001-5130-8492], Reich, Peter B [0000-0003-4424-662X], Hui, Cang [0000-0002-3660-8160], Morera, Albert [0000-0002-6777-169X], de-Miguel, Sergio [0000-0002-9738-0657], Svenning, Jens-Christian [0000-0002-3415-0862], Serra-Diaz, Josep M [0000-0003-1988-1154], Alberti, Giorgio [0000-0003-2422-3009], Bongers, Frans [0000-0002-8431-6189], Bouriaud, Olivier [0000-0002-8046-466X], Brancalion, Pedro HS [0000-0001-8245-4062], César, Ricardo Gomes [0000-0002-3392-8089], Chen, Han YH [0000-0001-9477-5541], Cienciala, Emil [0000-0002-1254-4254], Coomes, David [0000-0002-8261-2582], Djuikouo, Marie Noel Kamdem [0000-0003-0064-5151], Van Do, Tran [0000-0001-9059-5842], Feldpausch, Ted R [0000-0002-6631-7962], Jaroszewicz, Bogdan [0000-0002-2042-8245], Jeffery, Kathryn J [0000-0002-2632-0008], Kennard, Deborah K [0000-0003-4842-8260], Kim, Hyun Seok [0000-0002-3440-6071], Labrière, Nicolas [0000-0002-8037-2001], Maitner, Brian S [0000-0002-2118-9880], Malhi, Yadvinder [0000-0002-3503-4783], Peri, Pablo Luis [0000-0002-5398-4408], Phillips, Oliver L [0000-0002-8993-6168], Poorter, Lourens [0000-0003-1391-4875], Poulsen, John R [0000-0002-1532-9808], Salas-Eljatib, Christian [0000-0002-8468-0829], Schepaschenko, Dmitry [0000-0002-7814-4990], Silveira, Marcos [0000-0003-0485-7872], Slik, Ferry [0000-0003-3988-7019], Sonké, Bonaventure [0000-0002-4310-3603], Terborgh, John [0000-0003-1853-8311], Wiser, Susan K [0000-0002-8938-8181], Liang, Jingjing [0000-0001-9439-9320], Apollo - University of Cambridge Repository, and Coomes, David A [0000-0002-8261-2582]

Subjects
Cambios Antropogénicos, Richness, SAMPLE, Earth, Planet, Rarity, Bos- en Landschapsecologie, DIVERSITY, Forests, [SDV.BID.SPT]Life Sciences [q-bio]/Biodiversity/Systematics, Phylogenetics and taxonomy, Trees, forest, Bioma, Laboratory of Geo-information Science and Remote Sensing, Biome, espèce (taxon), HETEROGENEITY, Forest and Landscape Ecology, Forest Biodiversity, hyperdominance, Riqueza de Especies, Ecosystem Services, biodiversity, forests, hyperdominance, rarity, richness, biodiversity, Multidisciplinary, Hyperdominance, Overall Scale, F70 - Taxonomie végétale et phytogéographie, Biodiversity, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, Écologie des populations, PE&RC, COVERAGE, Boscos i silvicultura, Biometris, Forest Ecosystems, ABUNDANCE, Anthropogenic Changes, Vegetatie, Bos- en Landschapsecologie, Biodiversité, леса, Conservation of Natural Resources, F40 - Écologie végétale, Servicios de los Ecosistemas, Vulnerability, ECOLOGIA DE POPULAÇÕES, Arbre, ECOLOGY, Biodiversidad, forests, rarity, richness, Ecosistemas Forestales, [SDV.EE.ECO]Life Sciences [q-bio]/Ecology, environment/Ecosystems, COMPLETENESS, Árboles, Settore BIO/07 - ECOLOGIA, Richness Species, Bosecologie en Bosbeheer, Laboratorium voor Geo-informatiekunde en Remote Sensing, K70 - Dégâts causés aux forêts et leur protection, Biodiversidad Forestal, Escala Global, Vegetatie, деревья, Vegetation, Forest Ecology and Forest Management, biodiversité forestière, биоразнообразие, PATTERNS, Vegetation, Forest and Landscape Ecology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Vulnerabilidad
Abstract

One of the most fundamental questions in ecology is how many species inhabit the Earth. However, due to massive logistical and financial challenges and taxonomic difficulties connected to the species concept definition, the global numbers of species, including those of important and well-studied life forms such as trees, still remain largely unknown. Here, based on global ground-sourced data, we estimate the total tree species richness at global, continental, and biome levels. Our results indicate that there are ∼73,000 tree species globally, among which ∼9,000 tree species are yet to be discovered. Roughly 40% of undiscovered tree species are in South America. Moreover, almost one-third of all tree species to be discovered may be rare, with very low populations and limited spatial distribution (likely in remote tropical lowlands and mountains). These findings highlight the vulnerability of global forest biodiversity to anthropogenic changes in land use and climate, which disproportionately threaten rare species and thus, global tree richness., Proceedings of the National Academy of Sciences of the United States of America, 119 (6), ISSN:0027-8424, ISSN:1091-6490

Published
2022

4. Co-limitation towards lower latitudes shapes global forest diversity gradients

Author

Jingjing Liang, Javier G. P. Gamarra, Nicolas Picard, Mo Zhou, Bryan Pijanowski, Douglass F. Jacobs, Peter B. Reich, Thomas W. Crowther, Gert-Jan Nabuurs, Sergio de-Miguel, Jingyun Fang, Christopher W. Woodall, Jens-Christian Svenning, Tommaso Jucker, Jean-Francois Bastin, Susan K. Wiser, Ferry Slik, Bruno Hérault, Giorgio Alberti, Gunnar Keppel, Geerten M. Hengeveld, Pierre L. Ibisch, Carlos A. Silva, Hans ter Steege, Pablo L. Peri, David A. Coomes, Eric B. Searle, Klaus von Gadow, Bogdan Jaroszewicz, Akane O. Abbasi, Meinrad Abegg, Yves C. Adou Yao, Jesús Aguirre-Gutiérrez, Angelica M. Almeyda Zambrano, Jan Altman, Esteban Alvarez-Dávila, Juan Gabriel Álvarez-González, Luciana F. Alves, Bienvenu H. K. Amani, Christian A. Amani, Christian Ammer, Bhely Angoboy Ilondea, Clara Antón-Fernández, Valerio Avitabile, Gerardo A. Aymard, Akomian F. Azihou, Johan A. Baard, Timothy R. Baker, Radomir Balazy, Meredith L. Bastian, Rodrigue Batumike, Marijn Bauters, Hans Beeckman, Nithanel Mikael Hendrik Benu, Robert Bitariho, Pascal Boeckx, Jan Bogaert, Frans Bongers, Olivier Bouriaud, Pedro H. S. Brancalion, Susanne Brandl, Francis Q. Brearley, Jaime Briseno-Reyes, Eben N. Broadbent, Helge Bruelheide, Erwin Bulte, Ann Christine Catlin, Roberto Cazzolla Gatti, Ricardo G. César, Han Y. H. Chen, Chelsea Chisholm, Emil Cienciala, Gabriel D. Colletta, José Javier Corral-Rivas, Anibal Cuchietti, Aida Cuni-Sanchez, Javid A. Dar, Selvadurai Dayanandan, Thales de Haulleville, Mathieu Decuyper, Sylvain Delabye, Géraldine Derroire, Ben DeVries, John Diisi, Tran Van Do, Jiri Dolezal, Aurélie Dourdain, Graham P. Durrheim, Nestor Laurier Engone Obiang, Corneille E. N. Ewango, Teresa J. Eyre, Tom M. Fayle, Lethicia Flavine N. Feunang, Leena Finér, Markus Fischer, Jonas Fridman, Lorenzo Frizzera, André L. de Gasper, Damiano Gianelle, Henry B. Glick, Maria Socorro Gonzalez-Elizondo, Lev Gorenstein, Richard Habonayo, Olivier J. Hardy, David J. Harris, Andrew Hector, Andreas Hemp, Martin Herold, Annika Hillers, Wannes Hubau, Thomas Ibanez, Nobuo Imai, Gerard Imani, Andrzej M. Jagodzinski, Stepan Janecek, Vivian Kvist Johannsen, Carlos A. Joly, Blaise Jumbam, Banoho L. P. R. Kabelong, Goytom Abraha Kahsay, Viktor Karminov, Kuswata Kartawinata, Justin N. Kassi, Elizabeth Kearsley, Deborah K. Kennard, Sebastian Kepfer-Rojas, Mohammed Latif Khan, John N. Kigomo, Hyun Seok Kim, Carine Klauberg, Yannick Klomberg, Henn Korjus, Subashree Kothandaraman, Florian Kraxner, Amit Kumar, Relawan Kuswandi, Mait Lang, Michael J. Lawes, Rodrigo V. Leite, Geoffrey Lentner, Simon L. Lewis, Moses B. Libalah, Janvier Lisingo, Pablito Marcelo López-Serrano, Huicui Lu, Natalia V. Lukina, Anne Mette Lykke, Vincent Maicher, Brian S. Maitner, Eric Marcon, Andrew R. Marshall, Emanuel H. Martin, Olga Martynenko, Faustin M. Mbayu, Musingo T. E. Mbuvi, Jorge A. Meave, Cory Merow, Stanislaw Miscicki, Vanessa S. Moreno, Albert Morera, Sharif A. Mukul, Jörg C. Müller, Agustinus Murdjoko, Maria Guadalupe Nava-Miranda, Litonga Elias Ndive, Victor J. Neldner, Radovan V. Nevenic, Louis N. Nforbelie, Michael L. Ngoh, Anny E. N’Guessan, Michael R. Ngugi, Alain S. K. Ngute, Emile Narcisse N. Njila, Melanie C. Nyako, Thomas O. Ochuodho, Jacek Oleksyn, Alain Paquette, Elena I. Parfenova, Minjee Park, Marc Parren, Narayanaswamy Parthasarathy, Sebastian Pfautsch, Oliver L. Phillips, Maria T. F. Piedade, Daniel Piotto, Martina Pollastrini, Lourens Poorter, John R. Poulsen, Axel Dalberg Poulsen, Hans Pretzsch, Mirco Rodeghiero, Samir G. Rolim, Francesco Rovero, Ervan Rutishauser, Khosro Sagheb-Talebi, Purabi Saikia, Moses Nsanyi Sainge, Christian Salas-Eljatib, Antonello Salis, Peter Schall, Dmitry Schepaschenko, Michael Scherer-Lorenzen, Bernhard Schmid, Jochen Schöngart, Vladimír Šebeň, Giacomo Sellan, Federico Selvi, Josep M. Serra-Diaz, Douglas Sheil, Anatoly Z. Shvidenko, Plinio Sist, Alexandre F. Souza, Krzysztof J. Stereńczak, Martin J. P. Sullivan, Somaiah Sundarapandian, Miroslav Svoboda, Mike D. Swaine, Natalia Targhetta, Nadja Tchebakova, Liam A. Trethowan, Robert Tropek, John Tshibamba Mukendi, Peter Mbanda Umunay, Vladimir A. Usoltsev, Gaia Vaglio Laurin, Riccardo Valentini, Fernando Valladares, Fons van der Plas, Daniel José Vega-Nieva, Hans Verbeeck, Helder Viana, Alexander C. Vibrans, Simone A. Vieira, Jason Vleminckx, Catherine E. Waite, Hua-Feng Wang, Eric Katembo Wasingya, Chemuku Wekesa, Bertil Westerlund, Florian Wittmann, Verginia Wortel, Tomasz Zawiła-Niedźwiecki, Chunyu Zhang, Xiuhai Zhao, Jun Zhu, Xiao Zhu, Zhi-Xin Zhu, Irie C. Zo-Bi, Cang Hui, Liang, Jingjing, Gamarra, Javier GP, Picard, Nicolas, Zhou, Mo, Keppel, Gunnar, Hui, Cang, Liang J., Gamarra J.G.P., Picard N., Zhou M., Pijanowski B., Jacobs D.F., Reich P.B., Crowther T.W., Nabuurs G.-J., de-Miguel S., Fang J., Woodall C.W., Svenning J.-C., Jucker T., Bastin J.-F., Wiser S.K., Slik F., Herault B., Alberti G., Keppel G., Hengeveld G.M., Ibisch P.L., Silva C.A., ter Steege H., Peri P.L., Coomes D.A., Searle E.B., von Gadow K., Jaroszewicz B., Abbasi A.O., Abegg M., Yao Y.C.A., Aguirre-Gutierrez J., Zambrano A.M.A., Altman J., Alvarez-Davila E., Alvarez-Gonzalez J.G., Alves L.F., Amani B.H.K., Amani C.A., Ammer C., Ilondea B.A., Anton-Fernandez C., Avitabile V., Aymard G.A., Azihou A.F., Baard J.A., Baker T.R., Balazy R., Bastian M.L., Batumike R., Bauters M., Beeckman H., Benu N.M.H., Bitariho R., Boeckx P., Bogaert J., Bongers F., Bouriaud O., Brancalion P.H.S., Brandl S., Brearley F.Q., Briseno-Reyes J., Broadbent E.N., Bruelheide H., Bulte E., Catlin A.C., Cazzolla Gatti R., Cesar R.G., Chen H.Y.H., Chisholm C., Cienciala E., Colletta G.D., Corral-Rivas J.J., Cuchietti A., Cuni-Sanchez A., Dar J.A., Dayanandan S., de Haulleville T., Decuyper M., Delabye S., Derroire G., DeVries B., Diisi J., Do T.V., Dolezal J., Dourdain A., Durrheim G.P., Obiang N.L.E., Ewango C.E.N., Eyre T.J., Fayle T.M., Feunang L.F.N., Finer L., Fischer M., Fridman J., Frizzera L., de Gasper A.L., Gianelle D., Glick H.B., Gonzalez-Elizondo M.S., Gorenstein L., Habonayo R., Hardy O.J., Harris D.J., Hector A., Hemp A., Herold M., Hillers A., Hubau W., Ibanez T., Imai N., Imani G., Jagodzinski A.M., Janecek S., Johannsen V.K., Joly C.A., Jumbam B., Kabelong B.L.P.R., Kahsay G.A., Karminov V., Kartawinata K., Kassi J.N., Kearsley E., Kennard D.K., Kepfer-Rojas S., Khan M.L., Kigomo J.N., Kim H.S., Klauberg C., Klomberg Y., Korjus H., Kothandaraman S., Kraxner F., Kumar A., Kuswandi R., Lang M., Lawes M.J., Leite R.V., Lentner G., Lewis S.L., Libalah M.B., Lisingo J., Lopez-Serrano P.M., Lu H., Lukina N.V., Lykke A.M., Maicher V., Maitner B.S., Marcon E., Marshall A.R., Martin E.H., Martynenko O., Mbayu F.M., Mbuvi M.T.E., Meave J.A., Merow C., Miscicki S., Moreno V.S., Morera A., Mukul S.A., Muller J.C., Murdjoko A., Nava-Miranda M.G., Ndive L.E., Neldner V.J., Nevenic R.V., Nforbelie L.N., Ngoh M.L., N'Guessan A.E., Ngugi M.R., Ngute A.S.K., Njila E.N.N., Nyako M.C., Ochuodho T.O., Oleksyn J., Paquette A., Parfenova E.I., Park M., Parren M., Parthasarathy N., Pfautsch S., Phillips O.L., Piedade M.T.F., Piotto D., Pollastrini M., Poorter L., Poulsen J.R., Poulsen A.D., Pretzsch H., Rodeghiero M., Rolim S.G., Rovero F., Rutishauser E., Sagheb-Talebi K., Saikia P., Sainge M.N., Salas-Eljatib C., Salis A., Schall P., Schepaschenko D., Scherer-Lorenzen M., Schmid B., Schongart J., Seben V., Sellan G., Selvi F., Serra-Diaz J.M., Sheil D., Shvidenko A.Z., Sist P., Souza A.F., Sterenczak K.J., Sullivan M.J.P., Sundarapandian S., Svoboda M., Swaine M.D., Targhetta N., Tchebakova N., Trethowan L.A., Tropek R., Mukendi J.T., Umunay P.M., Usoltsev V.A., Vaglio Laurin G., Valentini R., Valladares F., van der Plas F., Vega-Nieva D.J., Verbeeck H., Viana H., Vibrans A.C., Vieira S.A., Vleminckx J., Waite C.E., Wang H.-F., Wasingya E.K., Wekesa C., Westerlund B., Wittmann F., Wortel V., Zawila-Niedzwiecki T., Zhang C., Zhao X., Zhu J., Zhu X., Zhu Z.-X., Zo-Bi I.C., Hui C., Purdue University [West Lafayette], Food and Agriculture Organization of the United Nations [Rome, Italie] (FAO), Groupement d'Interêt Public Ecosystèmes Forestiers GIP ECOFOR (GIP ECOFOR ), Forêts et Sociétés (UPR Forêts et Sociétés), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Département Environnements et Sociétés (Cirad-ES), Ecologie des forêts de Guyane (UMR ECOFOG), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Université de Guyane (UG)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Territoires, Environnement, Télédétection et Information Spatiale (UMR TETIS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Botanique et Modélisation de l'Architecture des Plantes et des Végétations (UMR AMAP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université de Montpellier (UM), SILVA (SILVA), AgroParisTech-Université de Lorraine (UL)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut National Polytechnique Félix Houphouët-Boigny, and Stellenbosch University

Subjects
Bos- en Landschapsecologie, WASS, Plant Ecology and Nature Conservation, Forests, [SDV.BID.SPT]Life Sciences [q-bio]/Biodiversity/Systematics, Phylogenetics and taxonomy, Co-limitation, Ontwikkelingseconomie, Forest and Nature Conservation Policy, Trees, Soil, [SDV.EE.ECO]Life Sciences [q-bio]/Ecology, environment/Ecosystems, Development Economics, Laboratory of Geo-information Science and Remote Sensing, Settore BIO/07 - ECOLOGIA, Life Science, Laboratorium voor Moleculaire Biologie, Bos- en Natuurbeleid, Forest and Landscape Ecology, Bosecologie en Bosbeheer, Laboratorium voor Geo-informatiekunde en Remote Sensing, BIOS Plant Development Systems, Vegetatie, Ecology, Evolution, Behavior and Systematics, biogeography, biodiversity, Vegetation, Ecology, Biodiversity, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, Latitudinal gradients, PE&RC, Forest Ecology and Forest Management, Bioclimatic dominance, Biogeography, LATITUDE, Plantenecologie en Natuurbeheer, Vegetatie, Bos- en Landschapsecologie, Vegetation, Forest and Landscape Ecology, Laboratory of Molecular Biology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Corporate Governance & Legal Services, Tree, Global LDG
Abstract

The latitudinal diversity gradient (LDG) is one of the most recognized global patterns of species richness exhibited across a wide range of taxa. Numerous hypotheses have been proposed in the past two centuries to explain LDG, but rigorous tests of the drivers of LDGs have been limited by a lack of high-quality global species richness data. Here we produce a high-resolution (0.025° × 0.025°) map of local tree species richness using a global forest inventory database with individual tree information and local biophysical characteristics from ~1.3 million sample plots. We then quantify drivers of local tree species richness patterns across latitudes. Generally, annual mean temperature was a dominant predictor of tree species richness, which is most consistent with the metabolic theory of biodiversity (MTB). However, MTB underestimated LDG in the tropics, where high species richness was also moderated by topographic, soil and anthropogenic factors operating at local scales. Given that local landscape variables operate synergistically with bioclimatic factors in shaping the global LDG pattern, we suggest that MTB be extended to account for co-limitation by subordinate drivers. The team collaboration and manuscript development are supported by the web-based team science platform: science-i.org, with the project number 202205GFB2. We thank the following initiatives, agencies, teams and individuals for data collection and other technical support: the Global Forest Biodiversity Initiative (GFBI) for establishing the data standards and collaborative framework; United States Department of Agriculture, Forest Service, Forest Inventory and Analysis (FIA) Program; University of Alaska Fairbanks; the SODEFOR, Ivory Coast; University Félix Houphouët-Boigny (UFHB, Ivory Coast); the Queensland Herbarium and past Queensland Government Forestry and Natural Resource Management departments and staff for data collection for over seven decades; and the National Forestry Commission of Mexico (CONAFOR). We thank M. Baker (Carbon Tanzania), together with a team of field assistants (Valentine and Lawrence); all persons who made the Third Spanish Forest Inventory possible, especially the main coordinator, J. A. Villanueva (IFN3); the French National Forest Inventory (NFI campaigns (raw data 2005 and following annual surveys, were downloaded by GFBI at https://inventaire-forestier.ign.fr/spip.php?rubrique159; site accessed on 1 January 2015)); the Italian Forest Inventory (NFI campaigns raw data 2005 and following surveys were downloaded by GFBI at https://inventarioforestale.org/; site accessed on 27 April 2019); Swiss National Forest Inventory, Swiss Federal Institute for Forest, Snow and Landscape Research WSL and Federal Office for the Environment FOEN, Switzerland; the Swedish NFI, Department of Forest Resource Management, Swedish University of Agricultural Sciences SLU; the National Research Foundation (NRF) of South Africa (89967 and 109244) and the South African Research Chair Initiative; the Danish National Forestry, Department of Geosciences and Natural Resource Management, UCPH; Coordination for the Improvement of Higher Education Personnel of Brazil (CAPES, grant number 88881.064976/2014-01); R. Ávila and S. van Tuylen, Instituto Nacional de Bosques (INAB), Guatemala, for facilitating Guatemalan data; the National Focal Center for Forest condition monitoring of Serbia (NFC), Institute of Forestry, Belgrade, Serbia; the Thünen Institute of Forest Ecosystems (Germany) for providing National Forest Inventory data; the FAO and the United Nations High Commissioner for Refugees (UNHCR) for undertaking the SAFE (Safe Access to Fuel and Energy) and CBIT-Forest projects; and the Amazon Forest Inventory Network (RAINFOR), the African Tropical Rainforest Observation Network (AfriTRON) and the ForestPlots.net initiative for their contributions from Amazonian and African forests. The Natural Forest plot data collected between January 2009 and March 2014 by the LUCAS programme for the New Zealand Ministry for the Environment are provided by the New Zealand National Vegetation Survey Databank https://nvs.landcareresearch.co.nz/. We thank the International Boreal Forest Research Association (IBFRA); the Forestry Corporation of New South Wales, Australia; the National Forest Directory of the Ministry of Environment and Sustainable Development of the Argentine Republic (MAyDS) for the plot data of the Second National Forest Inventory (INBN2); the National Forestry Authority and Ministry of Water and Environment of Uganda for their National Biomass Survey (NBS) dataset; and the Sabah Biodiversity Council and the staff from Sabah Forest Research Centre. All TEAM data are provided by the Tropical Ecology Assessment and Monitoring (TEAM) Network, a collaboration between Conservation International, the Missouri Botanical Garden, the Smithsonian Institution and the Wildlife Conservation Society, and partially funded by these institutions, the Gordon and Betty Moore Foundation and other donors, with thanks to all current and previous TEAM site manager and other collaborators that helped collect data. We thank the people of the Redidoti, Pierrekondre and Cassipora village who were instrumental in assisting with the collection of data and sharing local knowledge of their forest and the dedicated members of the field crew of Kabo 2012 census. We are also thankful to FAPESC, SFB, FAO and IMA/SC for supporting the IFFSC. This research was supported in part through computational resources provided by Information Technology at Purdue, West Lafayette, Indiana.This work is supported in part by the NASA grant number 12000401 ‘Multi-sensor biodiversity framework developed from bioacoustic and space based sensor platforms’ (J. Liang, B.P.); the USDA National Institute of Food and Agriculture McIntire Stennis projects 1017711 (J. Liang) and 1016676 (M.Z.); the US National Science Foundation Biological Integration Institutes grant NSF‐DBI‐2021898 (P.B.R.); the funding by H2020 VERIFY (contract 776810) and H2020 Resonate (contract 101000574) (G.-J.N.); the TEAM project in Uganda supported by the Moore foundation and Buffett Foundation through Conservation International (CI) and Wildlife Conservation Society (WCS); the Danish Council for Independent Research | Natural Sciences (TREECHANGE, grant 6108- 00078B) and VILLUM FONDEN grant number 16549 (J.-C.S.); the Natural Environment Research Council of the UK (NERC) project NE/T011084/1 awarded to J.A.-G. and NE/S011811/1; ERC Advanced Grant 291585 (‘T-FORCES’) and a Royal Society-Wolfson Research Merit Award (O.L.P.); RAINFOR plots supported by the Gordon and Betty Moore Foundation and the UK Natural Environment Research Council, notably NERC Consortium Grants ‘AMAZONICA’ (NE/F005806/1), ‘TROBIT’ (NE/D005590/1) and ‘BIO-RED’ (NE/N012542/1); CIFOR’s Global Comparative Study on REDD+ funded by the Norwegian Agency for Development Cooperation, the Australian Department of Foreign Affairs and Trade, the European Union, the International Climate Initiative (IKI) of the German Federal Ministry for the Environment, Nature Conservation, Building and Nuclear Safety and the CGIAR Research Program on Forests, Trees and Agroforestry (CRP-FTA) and donors to the CGIAR Fund; AfriTRON network plots funded by the local communities and NERC, ERC, European Union, Royal Society and Leverhume Trust; a grant from the Royal Society and the Natural Environment Research Council, UK (S.L.L.); National Science Foundation CIF21 DIBBs: EI: number 1724728 (A.C.C.); National Natural Science Foundation of China (31800374) and Shandong Provincial Natural Science Foundation (ZR2019BC083) (H.L.). UK NERC Independent Research Fellowship (grant code: NE/S01537X/1) (T.J.); a Serra-Húnter Fellowship provided by the Government of Catalonia (Spain) (S.d.-M.); the Brazilian National Council for Scientific and Technological Development (CNPq, grant 442640/2018-8, CNPq/Prevfogo-Ibama number 33/2018) (C.A.S.); a grant from the Franklinia Foundation (D.A.C.); Russian Science Foundation project number 19-77-300-12 (R.V.); the Takenaka Scholarship Foundation (A.O.A.); the German Research Foundation (DFG), grant number Am 149/16-4 (C.A.); the Romania National Council for Higher Education Funding, CNFIS, project number CNFIS-FDI-2022-0259 (O.B.); Natural Sciences and Engineering Research Council of Canada (RGPIN-2019-05109 and STPGP506284) and the Canadian Foundation for Innovation (36014) (H.Y.H.C.); the project SustES—Adaptation strategies for sustainable ecosystem services and food security under adverse environmental conditions (CZ.02.1.01/0.0/0.0/16_019/0000797) (E.C.); Consejo de Ciencia y Tecnología del estado de Durango (2019-01-155) (J.J.C.-R.); Science and Engineering Research Board (SERB), New Delhi, Government of India (file number PDF/2015/000447)— ‘Assessing the carbon sequestration potential of different forest types in Central India in response to climate change’ (J.A.D.); Investissement d’avenir grant of the ANR (CEBA: ANR-10-LABEX-0025) (G.D.); National Foundation for Science & Technology Development of Vietnam, 106-NN.06-2013.01 (T.V.D.); Queensland government, Department of Environment and Science (T.J.E.); a Czech Science Foundation Standard grant (19-14620S) (T.M.F.); European Union Seventh Framework Program (FP7/2007– 2013) under grant agreement number 265171 (L. Finer, M. Pollastrini, F. Selvi); grants from the Swedish National Forest Inventory, Swedish University of Agricultural Sciences (J.F.); CNPq productivity grant number 311303/2020-0 (A.L.d.G.); DFG grant HE 2719/11-1,2,3; HE 2719/14-1 (A. Hemp); European Union’s Horizon Europe research project OpenEarthMonitor grant number 101059548, CGIAR Fund INIT-32-MItigation and Transformation Initiative for GHG reductions of Agrifood systems RelaTed Emissions (MITIGATE+) (M.H.); General Directorate of the State Forests, Poland (1/07; OR-2717/3/11; OR.271.3.3.2017) and the National Centre for Research and Development, Poland (BIOSTRATEG1/267755/4/NCBR/2015) (A.M.J.); Czech Science Foundation 18-10781 S (S.J.); Danish of Ministry of Environment, the Danish Environmental Protection Agency, Integrated Forest Monitoring Program—NFI (V.K.J.); State of São Paulo Research Foundation/FAPESP as part of the BIOTA/FAPESP Program Project Functional Gradient-PELD/BIOTA-ECOFOR 2003/12595-7 & 2012/51872-5 (C.A.J.); Danish Council for Independent Research—social sciences—grant DFF 6109– 00296 (G.A.K.); Russian Science Foundation project 21-46-07002 for the plot data collected in the Krasnoyarsk region (V.K.); BOLFOR (D.K.K.); Department of Biotechnology, New Delhi, Government of India (grant number BT/PR7928/ NDB/52/9/2006, dated 29 September 2006) (M.L.K.); grant from Kenya Coastal Development Project (KCDP), which was funded by World Bank (J.N.K.); Korea Forest Service (2018113A00-1820-BB01, 2013069A00-1819-AA03, and 2020185D10- 2022-AA02) and Seoul National University Big Data Institute through the Data Science Research Project 2016 (H.S.K.); the Brazilian National Council for Scientific and Technological Development (CNPq, grant 442640/2018-8, CNPq/Prevfogo-Ibama number 33/2018) (C.K.); CSIR, New Delhi, government of India (grant number 38(1318)12/EMR-II, dated: 3 April 2012) (S.K.); Department of Biotechnology, New Delhi, government of India (grant number BT/ PR12899/ NDB/39/506/2015 dated 20 June 2017) (A.K.); Coordination for the Improvement of Higher Education Personnel (CAPES) #88887.463733/2019-00 (R.V.L.); National Natural Science Foundation of China (31800374) (H.L.); project of CEPF RAS ‘Methodological approaches to assessing the structural organization and functioning of forest ecosystems’ (AAAA-A18-118052590019-7) funded by the Ministry of Science and Higher Education of Russia (N.V.L.); Leverhulme Trust grant to Andrew Balmford, Simon Lewis and Jon Lovett (A.R.M.); Russian Science Foundation, project 19-77-30015 for European Russia data processing (O.M.); grant from Kenya Coastal Development Project (KCDP), which was funded by World Bank (M.T.E.M.); the National Centre for Research and Development, Poland (BIOSTRATEG1/267755/4/NCBR/2015) (S.M.); the Secretariat for Universities and of the Ministry of Business and Knowledge of the Government of Catalonia and the European Social Fund (A. Morera); Queensland government, Department of Environment and Science (V.J.N.); Pinnacle Group Cameroon PLC (L.N.N.); Queensland government, Department of Environment and Science (M.R.N.); the Natural Sciences and Engineering Research Council of Canada (RGPIN-2018-05201) (A.P.); the Russian Foundation for Basic Research, project number 20-05-00540 (E.I.P.); European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement number 778322 (H.P.); Science and Engineering Research Board, New Delhi, government of India (grant number YSS/2015/000479, dated 12 January 2016) (P.S.); the Chilean Government research grants Fondecyt number 1191816 and FONDEF number ID19 10421 (C.S.-E.); the Deutsche Forschungsgemeinschaft (DFG) Priority Program 1374 Biodiversity Exploratories (P.S.); European Space Agency projects IFBN (4000114425/15/NL/FF/gp) and CCI Biomass (4000123662/18/I-NB) (D. Schepaschenko); FunDivEUROPE, European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement number 265171 (M.S.-L.); APVV 20-0168 from the Slovak Research and Development Agency (V.S.); Manchester Metropolitan University’s Environmental Science Research Centre (G.S.); the project ‘LIFE+ ForBioSensing PL Comprehensive monitoring of stand dynamics in Białowieża Forest supported with remote sensing techniques’ which is co-funded by the EU Life Plus programme (contract number LIFE13 ENV/PL/000048) and the National Fund for Environmental Protection and Water Management in Poland (contract number 485/2014/WN10/OP-NM-LF/D) (K.J.S.); Global Challenges Research Fund (QR allocation, MMU) (M.J.P.S.); Czech Science Foundation project 21-27454S (M.S.); the Russian Foundation for Basic Research, project number 20-05-00540 (N. Tchebakova); Botanical Research Fund, Coalbourn Trust, Bentham Moxon Trust, Emily Holmes scholarship (L.A.T.); the programmes of the current scientific research of the Botanical Garden of the Ural Branch of Russian Academy of Sciences (V.A.U.); FCT—Portuguese Foundation for Science and Technology—Project UIDB/04033/2020. Inventário Florestal Nacional—ICNF (H. Viana); Grant from Kenya Coastal Development Project (KCDP), which was funded by World Bank (C.W.); grants from the Swedish National Forest Inventory, Swedish University of Agricultural Sciences (B.W.); ATTO project (grant number MCTI-FINEP 1759/10 and BMBF 01LB1001A, 01LK1602F) (F.W.); ReVaTene/ PReSeD-CI 2 is funded by the Education and Research Ministry of Côte d’Ivoire, as part of the Debt Reduction-Development Contracts (C2Ds) managed by IRD (I.C.Z.-B.); the National Research Foundation of South Africa (NRF, grant 89967) (C.H.). The Tropical Plant Exploration Group 70 1 ha plots in Continental Cameroon Mountains are supported by Rufford Small Grant Foundation, UK and 4 ha in Sierra Leone are supported by the Global Challenge Research Fund through Manchester Metropolitan University, UK; the National Geographic Explorer Grant, NGS-53344R-18 (A.C.-S.); University of KwaZulu-Natal Research Office grant (M.J.L.); Universidad Nacional Autónoma de México, Dirección General de Asuntos de Personal Académico, Grant PAPIIT IN-217620 (J.A.M.). Czech Science Foundation project 21-24186M (R.T., S. Delabye). Czech Science Foundation project 20-05840Y, the Czech Ministry of Education, Youth and Sports (LTAUSA19137) and the long-term research development project of the Czech Academy of Sciences no. RVO 67985939 (J.A.). The American Society of Primatologists, the Duke University Graduate School, the L.S.B. Leakey Foundation, the National Science Foundation (grant number 0452995) and the Wenner-Gren Foundation for Anthropological Research (grant number 7330) (M.B.). Research grants from Conselho Nacional de Desenvolvimento Científico e Tecnologico (CNPq, Brazil) (309764/2019; 311303/2020) (A.C.V., A.L.G.). The Project of Sanya Yazhou Bay Science and Technology City (grant number CKJ-JYRC-2022-83) (H.-F.W.). The Ugandan NBS was supported with funds from the Forest Carbon Partnership Facility (FCPF), the Austrian Development Agency (ADC) and FAO. FAO’s UN-REDD Program, together with the project on ‘Native Forests and Community’ Loan BIRF number 8493-AR UNDP ARG/15/004 and the National Program for the Protection of Native Forests under UNDP funded Argentina’s INBN2.

Published
2022

5. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses

Author

Steidinger, B. S., Crowther, T. W., Liang, J., Van Nuland, M. E., Werner, G. D. A., Reich, P. B., Nabuurs, G., de-Miguel, S., Zhou, M., Picard, N., Herault, B., Zhao, X., Zhang, C., Routh, D., Peay, K. G., Abegg, Meinrad, Yao, C. Yves Adou, Alberti, Giorgio, Zambrano, Angelica Almeyda, Alvarez-Davila, Esteban, Alvarez-Loayza, Patricia, Alves, Luciana F., Ammer, Christian, Anton-Fernandez, Clara, Araujo-Murakami, Alejandro, Arroyo, Luzmila, Avitabile, Valerio, Aymard, Gerardo, Baker, Timothy, Balazy, Radomir, Banki, Olaf, Barroso, Jorcely, Bastian, Meredith, Bastin, Jean-Francois, Birigazzi, Luca, Birnbaum, Philippe, Bitariho, Robert, Boeckx, Pascal, Bongers, Frans, Bouriaud, Olivier, Brancalion, Pedro H. S., Brandl, Susanne, Brearley, Francis Q., Brienen, Roel, Broadbent, Eben, Bruelheide, Helge, Bussotti, Filippo, Gatti, Roberto Cazzolla, Cesar, Ricardo, Cesljar, Goran, Chazdon, Robin, Chen, Han Y. H., Chisholm, Chelsea, Cienciala, Emil, Clark, Connie J., Clark, David, Colletta, Gabriel, Condit, Richard, Coomes, David, Cornejo Valverde, Fernando, Corral-Rivas, Jose J., Crim, Philip, Cumming, Jonathan, Dayanandan, Selvadurai, de Gasper, Andre L., Decuyper, Mathieu, Derroire, Geraldine, DeVries, Ben, Djordjevic, Ilija, Ieda, Amaral, Dourdain, Aurelie, Obiang, Nestor Laurier Engone, Enquist, Brian, Eyre, Teresa, Fandohan, Adande Belarmain, Fayle, Tom M., Feldpausch, Ted R., Finer, Leena, Fischer, Markus, Fletcher, Christine, Fridman, Jonas, Frizzera, Lorenzo, Gamarra, Javier G. P., Gianelle, Damiano, Glick, Henry B., Harris, David, Hector, Andrew, Hemp, Andreas, Hengeveld, Geerten, Herbohn, John, Herold, Martin, Hillers, Annika, Honorio Coronado, Euridice N., Huber, Markus, Hui, Cang, Cho, Hyunkook, Ibanez, Thomas, Jung, Ilbin, Imai, Nobuo, Jagodzinski, Andrzej M., Jaroszewicz, Bogdan, Johannsen, Vivian, Joly, Carlos A., Jucker, Tommaso, Karminov, Viktor, Kartawinata, Kuswata, Kearsley, Elizabeth, Kenfack, David, Kennard, Deborah, Kepfer-Rojas, Sebastian, Keppel, Gunnar, Khan, Mohammed Latif, Killeen, Timothy, Kim, Hyun Seok, Kitayama, Kanehiro, Kohl, Michael, Korjus, Henn, Kraxner, Florian, Laarmann, Diana, Lang, Mait, Lewis, Simon, Lu, Huicui, Lukina, Natalia, Maitner, Brian, Malhi, Yadvinder, Marcon, Eric, Marimon, Beatriz Schwantes, Marimon-Junior, Ben Hur, Marshall, Andrew Robert, Martin, Emanuel, Martynenko, Olga, Meave, Jorge A., Melo-Cruz, Omar, Mendoza, Casimiro, Merow, Cory, Mendoza, Abel Monteagudo, Moreno, Vanessa, Mukul, Sharif A., Mundhenk, Philip, Nava-Miranda, Maria G., Neill, David, Neldner, Victor, Nevenic, Radovan, Ngugi, Michael, Niklaus, Pascal, Oleksyn, Jacek, Ontikov, Petr, Ortiz-Malavasi, Edgar, Pan, Yude, Paquette, Alain, Parada-Gutierrez, Alexander, Parfenova, Elena, Park, Minjee, Parren, Marc, Parthasarathy, Narayanaswamy, Peri, Pablo L., Pfautsch, Sebastian, Phillips, Oliver, Piedade, Maria Teresa, Piotto, Daniel, Pitman, Nigel C. A., Polo, Irina, Poorter, Lourens, Poulsen, Axel Dalberg, Poulsen, John R., Pretzsch, Hans, Arevalo, Freddy Ramirez, Restrepo-Correa, Zorayda, Rodeghiero, Mirco, Rolim, Samir, Roopsind, Anand, Rovero, Francesco, Rutishauser, Ervan, Saikia, Purabi, Saner, Philippe, Schall, Peter, Schelhaas, Mart-Jan, Schepaschenko, Dmitry, Scherer-Lorenzen, Michael, Schmid, Bernhard, Schongart, Jochen, Searle, Eric, Seben, Vladimir, Serra-Diaz, Josep M., Salas-Eljatib, Christian, Sheil, Douglas, Shvidenko, Anatoly, Silva-Espejo, Javier, Silveira, Marcos, Singh, James, Sist, Plinio, Slik, Ferry, Sonke, Bonaventure, Souza, Alexandre F., Sterenczak, Krzysztof, Svenning, Jens-Christian, Svoboda, Miroslav, Targhetta, Natalia, Tchebakova, Nadja, ter Steege, Hans, Thomas, Raquel, Tikhonova, Elena, Umunay, Peter, Usoltsev, Vladimir, Valladares, Fernando, van der Plas, Fons, Tran Van Do, Vasquez Martinez, Rodolfo, Verbeeck, Hans, Viana, Helder, Vieira, Simone, von Gadow, Klaus, Wang, Hua-Feng, Watson, James, Westerlund, Bertil, Wiser, Susan, Wittmann, Florian, Wortel, Verginia, Zagt, Roderick, Zawila-Niedzwiecki, Tomasz, Zhu, Zhi-Xin, Zo-Bi, Irie Casimir, Valladares, Fernando, Stanford University, Department of Environmental Systems Science [ETH Zürich] (D-USYS), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), Purdue University [West Lafayette], Beijing Forestry University, University of Oxford [Oxford], University of Minnesota [Twin Cities] (UMN), University of Minnesota System, Western Sydney University, Wageningen University and Research [Wageningen] (WUR), Universitat de Lleida, Centre de Ciència i Tecnologia Forestal de Catalunya (CTFC), Food and Agriculture Organization of the United Nations [Rome, Italie] (FAO), Forêts et Sociétés (UPR Forêts et Sociétés), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Institut National Polytechnique Yamoussoukro, Ecologie des forêts de Guyane (UMR ECOFOG), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-AgroParisTech-Université de Guyane (UG)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), SILVA (SILVA), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL)-AgroParisTech, Stanford University [Stanford], Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology in Zürich [Zürich] (ETH Zürich), University of Minnesota [Twin Cities], Western Sydney University (UWS), Wageningen University and Research Centre [Wageningen] (WUR), Forest Science and Technology Centre of Catalonia, Food and Agricultural Organization of the United Nations (FAO), United Nations Organization, Forêts et Sociétés (Cirad-Es-UPR 105 Forêts et Sociétés), Département Environnements et Sociétés (Cirad-ES), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Institut National de la Recherche Agronomique (INRA)-AgroParisTech-Université de Lorraine (UL), Steidinger B.S., Crowther T.W., Liang J., Van Nuland M.E., Werner G.D.A., Reich P.B., Nabuurs G., de-Miguel S., Zhou M., Picard N., Herault B., Zhao X., Zhang C., Routh D., Peay K.G., Abegg M., AdouYao C.Y., Alberti G., AlmeydaZambrano A., Alvarez-Davila E., Alvarez-Loayza P., Alves L.F., Ammer C., Anton-Fernandez C., Araujo-Murakami A., Arroyo L., Avitabile V., Aymard G., Baker T., Balazy R., Banki O., Barroso J., Bastian M., Bastin J.-F., Birigazzi L., Birnbaum P., Bitariho R., Boeckx P., Bongers F., Bouriaud O., Brancalion P.H.S., Brandl S., Brearley F.Q., Brienen R., Broadbent E., Bruelheide H., Bussotti F., Cazzolla Gatti R., Cesar R., Cesljar G., Chazdon R., Chen H.Y.H., Chisholm C., Cienciala E., Clark C.J., Clark D., Colletta G., Condit R., Coomes D., CornejoValverde F., Corral-Rivas J.J., Crim P., Cumming J., Dayanandan S., de Gasper A.L., Decuyper M., Derroire G., DeVries B., Djordjevic I., Ieda A., Dourdain A., Obiang N.L.E., Enquist B., Eyre T., Fandohan A.B., Fayle T.M., Feldpausch T.R., Finer L., Fischer M., Fletcher C., Fridman J., Frizzera L., Gamarra J.G.P., Gianelle D., Glick H.B., Harris D., Hector A., Hemp A., Hengeveld G., Herbohn J., Herold M., Hillers A., Honorio Coronado E.N., Huber M., Hui C., Cho H., Ibanez T., Jung I., Imai N., Jagodzinski A.M., Jaroszewicz B., Johannsen V., Joly C.A., Jucker T., Karminov V., Kartawinata K., Kearsley E., Kenfack D., Kennard D., Kepfer-Rojas S., Keppel G., Khan M.L., Killeen T., Kim H.S., Kitayama K., Kohl M., Korjus H., Kraxner F., Laarmann D., Lang M., Lewis S., Lu H., Lukina N., Maitner B., Malhi Y., Marcon E., Marimon B.S., Marimon-Junior B.H., Marshall A.R., Martin E., Martynenko O., Meave J.A., Melo-Cruz O., Mendoza C., Merow C., MonteagudoMendoza A., Moreno V., Mukul S.A., Mundhenk P., Nava-Miranda M.G., Neill D., Neldner V., Nevenic R., Ngugi M., Niklaus P., Oleksyn J., Ontikov P., Ortiz-Malavasi E., Pan Y., Paquette A., Parada-Gutierrez A., Parfenova E., Park M., Parren M., Parthasarathy N., Peri P.L., Pfautsch S., Phillips O., Piedade M.T., Piotto D., Pitman N.C.A., Polo I., Poorter L., Poulsen A.D., Poulsen J.R., Pretzsch H., RamirezArevalo F., Restrepo-Correa Z., Rodeghiero M., Rolim S., Roopsind A., Rovero F., Rutishauser E., Saikia P., Saner P., Schall P., Schelhaas M.-J., Schepaschenko D., Scherer-Lorenzen M., Schmid B., Schongart J., Searle E., Seben V., Serra-Diaz J.M., Salas-Eljatib C., Sheil D., Shvidenko A., Silva-Espejo J., Silveira M., Singh J., Sist P., Slik F., Sonke B., Souza A.F., Sterenczak K., Svenning J.-C., Svoboda M., Targhetta N., Tchebakova N., Steege H., Thomas R., Tikhonova E., Umunay P., Usoltsev V., Valladares F., van der Plas F., Van Do T., VasquezMartinez R., Verbeeck H., Viana H., Vieira S., von Gadow K., Wang H.-F., Watson J., Westerlund B., Wiser S., Wittmann F., Wortel V., Zagt R., Zawila-Niedzwiecki T., Zhu Z.-X., Zo-Bi I.C., Systems Ecology, Steidinger, BS, Crowther, TW, Liang, J, Van Nuland, ME, Werner, GDA, Reich, PB, Nabuurs, G, de-Miguel, S, Zhou, M, Picard, N, Herault, B, Zhao, X, Zhang, C, Routh, D, Peay, KG, Keppel, G, GFBI consortium, and Valladares, Fernando [0000-0002-5374-4682]

Subjects
symbiosi, 0106 biological sciences, Forest Ecology, SOM decomposition, biogeography, forest-tree symbioses, Bos- en Landschapsecologie, Biome, 01 natural sciences, forest-tree symbioses, Microbial ecology, Laboratory of Geo-information Science and Remote Sensing, K01 - Foresterie - Considérations générales, Bos- en Natuurbeleid, Forest and Landscape Ecology, Multidisciplinary, Ecology, forest ecosystems, PE&RC, séquestration du carbone, Biometris, Biogeography, Forêt, Écosystème forestier, Vegetatie, Bos- en Landschapsecologie, P33 - Chimie et physique du sol, Climate control, Forest Ecology, P40 - Météorologie et climatologie, Symbiose, 010603 evolutionary biology, Forest and Nature Conservation Policy, Symbiosis, Settore BIO/07 - ECOLOGIA, Forest ecology, Temperate climate, Symbioses, Life Science, Bosecologie en Bosbeheer, Laboratorium voor Geo-informatiekunde en Remote Sensing, Forest, climate, Vegetatie, biogeography, Changement climatique, decomposition, Vegetation, Forest inventory, симбиозы, P34 - Biologie du sol, FUNGI, климат, 15. Life on land, Arid, Forest Ecology and Forest Management, SOM decomposition, forest inventory plots, лесные экосистемы, Environmental science, Vegetation, Forest and Landscape Ecology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, 010606 plant biology & botany
Abstract

[EN] The identity of the dominant root-associated microbial symbionts in a forest determines the ability of trees to access limiting nutrients from atmospheric or soil pools, sequester carbon and withstand the effects of climate change. Characterizing the global distribution of these symbioses and identifying the factors that control this distribution are thus integral to understanding the present and future functioning of forest ecosystems. Here we generate a spatially explicit global map of the symbiotic status of forests, using a database of over 1.1 million forest inventory plots that collectively contain over 28,000 tree species. Our analyses indicate that climate variables—in particular, climatically controlled variation in the rate of decomposition—are the primary drivers of the global distribution of major symbioses. We estimate that ectomycorrhizal trees, which represent only 2% of all plant species, constitute approximately 60% of tree stems on Earth. Ectomycorrhizal symbiosis dominates forests in which seasonally cold and dry climates inhibit decomposition, and is the predominant form of symbiosis at high latitudes and elevation. By contrast, arbuscular mycorrhizal trees dominate in aseasonal, warm tropical forests, and occur with ectomycorrhizal trees in temperate biomes in which seasonally warm-and-wet climates enhance decomposition. Continental transitions between forests dominated by ectomycorrhizal or arbuscular mycorrhizal trees occur relatively abruptly along climate-driven decomposition gradients; these transitions are probably caused by positive feedback effects between plants and microorganisms. Symbiotic nitrogen fixers—which are insensitive to climatic controls on decomposition (compared with mycorrhizal fungi)—are most abundant in arid biomes with alkaline soils and high maximum temperatures. The climatically driven global symbiosis gradient that we document provides a spatially explicit quantitative understanding of microbial symbioses at the global scale, and demonstrates the critical role of microbial mutualisms in shaping the distribution of plant species., This work was made possible by the Global Forest Biodiversity Database, which represents the work of over 200 independent investigators and their public and private funding agencies (see Supplementary Acknowledgements), Supplementary information is available for this paper at https://doi.org/10.1038/s41586-019-1128-0.

Published
2019

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