Abstract

The carbon sink capacity of tropical forests is substantially affected by tree mortality. However, the main drivers of tropical tree death remain largely unknown. Here we present a pan-Amazonian assessment of how and why trees die, analysing over 120,000 trees representing > 3800 species from 189 long-term RAINFOR forest plots. While tree mortality rates vary greatly Amazon-wide, on average trees are as likely to die standing as they are broken or uprooted—modes of death with different ecological consequences. Species-level growth rate is the single most important predictor of tree death in Amazonia, with faster-growing species being at higher risk. Within species, however, the slowest-growing trees are at greatest risk while the effect of tree size varies across the basin. In the driest Amazonian region species-level bioclimatic distributional patterns also predict the risk of death, suggesting that these forests are experiencing climatic conditions beyond their adaptative limits. These results provide not only a holistic pan-Amazonian picture of tree death but large-scale evidence for the overarching importance of the growth–survival trade-off in driving tropical tree mortality.

Tree mortality has been shown to be the dominant control on carbon storage in Amazon forests, but little is known of how and why Amazon forest trees die. Here the authors analyse a large Amazon-wide dataset, finding that fast-growing species face greater mortality risk, but that slower-growing individuals within a species are more likely to die, regardless of size.

Details

Title
Tree mode of death and mortality risk factors across Amazon forests
Author
Esquivel-Muelbert Adriane 1   VIAFID ORCID Logo  ; Phillips, Oliver L 2   VIAFID ORCID Logo  ; Brienen Roel J W 2   VIAFID ORCID Logo  ; Fauset Sophie 3   VIAFID ORCID Logo  ; Sullivan Martin J P 4   VIAFID ORCID Logo  ; Baker, Timothy R 2 ; Kuo-Jung, Chao 5 ; Feldpausch, Ted R 6   VIAFID ORCID Logo  ; Gloor Emanuel 2 ; Higuchi Niro 7 ; Houwing-Duistermaat Jeanne 8   VIAFID ORCID Logo  ; Lloyd, Jon 9   VIAFID ORCID Logo  ; Liu, Haiyan 8 ; Malhi Yadvinder 10   VIAFID ORCID Logo  ; Marimon Beatriz 11 ; Marimon Junior Ben Hur 11 ; Monteagudo-Mendoza, Abel 12 ; Poorter Lourens 13   VIAFID ORCID Logo  ; Silveira Marcos 14   VIAFID ORCID Logo  ; Torre Emilio Vilanova 15 ; Dávila Esteban Alvarez 16   VIAFID ORCID Logo  ; del Aguila Pasquel Jhon 17 ; Almeida Everton 18   VIAFID ORCID Logo  ; Loayza Patricia Alvarez 19 ; Andrade, Ana 20   VIAFID ORCID Logo  ; Aragão Luiz E O C 21 ; Araujo-Murakami, Alejandro 22 ; Arets, Eric 23   VIAFID ORCID Logo  ; Arroyo Luzmila 24 ; Aymard C Gerardo A 25 ; Baisie Michel 26 ; Baraloto, Christopher 27 ; Camargo, Plínio Barbosa 28 ; Barroso Jorcely 29 ; Blanc Lilian 30 ; Bonal Damien 31 ; Bongers Frans 13   VIAFID ORCID Logo  ; Boot René 32 ; Brown, Foster 33 ; Burban Benoit 34 ; Camargo, José Luís 20 ; Castro Wendeson 35   VIAFID ORCID Logo  ; Moscoso Victor Chama 36 ; Chave, Jerome 37   VIAFID ORCID Logo  ; Comiskey, James 38   VIAFID ORCID Logo  ; Valverde, Fernando Cornejo 39 ; da Costa Antonio Lola 40 ; Cardozo Nallaret Davila 17 ; Di Fiore Anthony 41   VIAFID ORCID Logo  ; Dourdain Aurélie 42 ; Erwin, Terry 43 ; Llampazo Gerardo Flores 44 ; Vieira Ima Célia Guimarães 45 ; Herrera, Rafael 46   VIAFID ORCID Logo  ; Honorio Coronado Eurídice 17   VIAFID ORCID Logo  ; Isau, Huamantupa-Chuquimaco 47   VIAFID ORCID Logo  ; Jimenez-Rojas, Eliana 48   VIAFID ORCID Logo  ; Killeen, Timothy 49 ; Laurance, Susan 50   VIAFID ORCID Logo  ; Laurance, William 50   VIAFID ORCID Logo  ; Levesley Aurora 2 ; Lewis, Simon L 51   VIAFID ORCID Logo  ; Ladvocat Karina Liana Lisboa Melgaço 2 ; Lopez-Gonzalez, Gabriela 2 ; Lovejoy, Thomas 52   VIAFID ORCID Logo  ; Meir, Patrick 53 ; Mendoza Casimiro 54 ; Morandi, Paulo 55   VIAFID ORCID Logo  ; Neill, David 56   VIAFID ORCID Logo  ; Nogueira Lima Adriano José 7 ; Vargas Percy Nuñez 57 ; de Oliveira Edmar Almeida 58   VIAFID ORCID Logo  ; Camacho, Nadir Pallqui 59   VIAFID ORCID Logo  ; Pardo, Guido 60 ; Peacock, Julie 2 ; Peña-Claros Marielos 13 ; Peñuela-Mora, Maria Cristina 61 ; Pickavance Georgia 2 ; Pipoly, John 62 ; Pitman, Nigel 63 ; Prieto, Adriana 64 ; Pugh Thomas A M 65   VIAFID ORCID Logo  ; Quesada, Carlos 7 ; Ramirez-Angulo Hirma 66 ; de Almeida Reis Simone Matias 67   VIAFID ORCID Logo  ; Rejou-Machain Maxime 68   VIAFID ORCID Logo  ; Correa, Zorayda Restrepo 69 ; Bayona Lily Rodriguez 70 ; Rudas Agustín 64 ; Salomão Rafael 71 ; Serrano, Julio 72 ; Espejo Javier Silva 73 ; Silva Natalino 74 ; Singh, James 75 ; Stahl, Clement 76 ; Stropp Juliana 77 ; Swamy Varun 78 ; Talbot, Joey 79 ; ter Steege Hans 80   VIAFID ORCID Logo  ; Terborgh, John 81 ; Thomas, Raquel 82 ; Toledo Marisol 22 ; Torres-Lezama, Armando 83 ; Gamarra, Luis Valenzuela 84 ; van der Heijden Geertje 85   VIAFID ORCID Logo  ; van der Meer Peter 86 ; van der Hout Peter 87 ; Martinez, Rodolfo Vasquez 88 ; Vieira, Simone Aparecida 89   VIAFID ORCID Logo  ; Cayo Jeanneth Villalobos 90 ; Vos, Vincent 60   VIAFID ORCID Logo  ; Zagt Roderick 91 ; Zuidema Pieter 13   VIAFID ORCID Logo  ; Galbraith, David 2   VIAFID ORCID Logo 

 University of Birmingham, School of Geography, Earth and Enviornmental Sciences, Birmingham, UK (GRID:grid.6572.6) (ISNI:0000 0004 1936 7486); University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403); University of Birmingham, Birmingham Institute of Forest Research, Birmingham, UK (GRID:grid.6572.6) (ISNI:0000 0004 1936 7486) 
 University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403) 
 University of Plymouth, School of Geography, Earth and Environmental Sciences, Plymouth, UK (GRID:grid.11201.33) (ISNI:0000 0001 2219 0747) 
 University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403); Manchester Metropolitan University, Department of Natural Sciences, Manchester, UK (GRID:grid.25627.34) (ISNI:0000 0001 0790 5329) 
 National Chung Hsing University, International Master Program of Agriculture, Taichung, Taiwan (GRID:grid.260542.7) (ISNI:0000 0004 0532 3749) 
 University of Exeter, Geography, College of Life and Environmental Sciences, Exeter, UK (GRID:grid.8391.3) (ISNI:0000 0004 1936 8024) 
 Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil (GRID:grid.419220.c) (ISNI:0000 0004 0427 0577) 
 University of Leeds, School of Mathematics, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403) 
 Imperial College London Sciences, Faculty of Natural Sciences, Department of Life, London, UK (GRID:grid.7445.2) (ISNI:0000 0001 2113 8111) 
10  University of Oxford, Environmental Change Institute, School of Geography and the Environment, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948) 
11  UNEMAT – Universidade do Estado de Mato Grosso PPG-Ecologia e Conservação, Nova Xavantina, Brazil (GRID:grid.4991.5) 
12  Jardín Botánico de Missouri, Oxapampa, Peru (GRID:grid.4991.5) 
13  Wageningen University and Research, Forest Ecology and Forest Management Group, Wageningen, Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666) 
14  Universidade Federal do Acre, Centro de Ciências Biológicas e da Natureza, Rio Branco, Brazil (GRID:grid.412369.b) 
15  Universidad de Los Andes, Instituto de Investigaciones para el Desarrollo Forestal (INDEFOR), Mérida, Venezuela (GRID:grid.267525.1) (ISNI:0000 0004 1937 0853); University of California, Berkeley, USA (GRID:grid.47840.3f) (ISNI:0000 0001 2181 7878) 
16  Universidad Nacional Abierta y a Distancia, Escuela de Ciencias Agropecuarias y Ambientales, Boyacá, Colombia (GRID:grid.442181.a) (ISNI:0000 0000 9497 122X); Fundación ConVida, Medellín, Colombia (GRID:grid.442181.a) 
17  Instituto de Investigaciones de la Amazonia Peruana, Iquitos, Peru (GRID:grid.493484.6) (ISNI:0000 0001 2177 4732) 
18  Universidade Federal do Oeste do Pará, Instituto de Biodiversidade e Florestas, Santarém, Brazil (GRID:grid.448725.8) (ISNI:0000 0004 0509 0076) 
19  University in Durham, Center for Tropical Conservation, Nicholas School of the Environment, Durham, USA (GRID:grid.448725.8) 
20  Instituto Nacional de Pesquisas da Amazônia Florestais, Projeto Dinâmica Biológica de Fragmentos, Manaus, Brazil (GRID:grid.419220.c) (ISNI:0000 0004 0427 0577) 
21  National Institute for Space Research (INPE), São José dos Campos, Brazil (GRID:grid.419222.e) (ISNI:0000 0001 2116 4512) 
22  Universidad Autónoma Gabriel Rene Moreno, Museo de Historia Natural Noel Kempff Mercado, Santa Cruz de la Sierra, Bolivia (GRID:grid.440538.e) (ISNI:0000 0001 2114 3869) 
23  Wageningen University and Research, Wageningen Environmental Research, Wageningen, Netherlands (GRID:grid.4818.5) (ISNI:0000 0001 0791 5666) 
24  Universidad Autónoma Gabriel René Moreno, Dirección de la Carrera de Biología, Santa Cruz de la Sierra, Bolivia (GRID:grid.440538.e) (ISNI:0000 0001 2114 3869) 
25  Portuguesa, Venezuela Compensation International Progress S.A. Ciprogress–Greenlife, Bogotá, UNELLEZ-Guanare, Herbario Universitario (PORT), D.C., Colombia (GRID:grid.440538.e) 
26  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.440538.e) 
27  Florida International University, Department of Biological Sciences, International Center for Tropical Botany, Miami, USA (GRID:grid.65456.34) (ISNI:0000 0001 2110 1845) 
28  Universidade de São Paulo, Centro de Energia Nuclear na Agricultura, Piracicaba, Brazil (GRID:grid.11899.38) (ISNI:0000 0004 1937 0722) 
29  Universidade Federal do Acre, Cruzeiro do Sul, Brazil (GRID:grid.412369.b) 
30  CIRAD, UR Forest & Societies, Montpellier, France (GRID:grid.8183.2) (ISNI:0000 0001 2153 9871) 
31  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.8183.2) 
32  Department of Biology, Utrecht, Netherlands (GRID:grid.4818.5) 
33  Woods Hole Research Center, Falmouth, USA (GRID:grid.251079.8) (ISNI:0000 0001 2185 0926) 
34  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.251079.8) 
35  Universidade Federal do Acre, Laboratório de Botânica e Ecologia Vegetal, Rio Branco, Brazil (GRID:grid.412369.b) 
36  Jardín Botánico de Missouri, Oxapampa, Peru (GRID:grid.412369.b) 
37  CNRS, Laboratoire Evolution et Diversite Biologique, Toulouse, France (GRID:grid.4444.0) (ISNI:0000 0001 2112 9282) 
38  National Park Service, Inventory and Monitoring Program, Fort Collins, USA (GRID:grid.454846.f) (ISNI:0000 0001 2331 3972) 
39  Proyecto Castaña, Madre de Dios, Peru (GRID:grid.454846.f) 
40  Universidade Federal do Para, Instituto de Geociências, Faculdade de Meteorologia, Belém, Brazil (GRID:grid.271300.7) (ISNI:0000 0001 2171 5249) 
41  University of Texas, Department of Anthropology and Primate Molecular Ecology and Evolution Laboratory, Austin, USA (GRID:grid.55460.32) (ISNI:0000000121548364) 
42  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.55460.32) 
43  Smithsonian Institute, National Museum of Natural History, Washington, USA (GRID:grid.1214.6) (ISNI:0000 0000 8716 3312) 
44  Universidad Nacional Jorge Basadre de Grohmann, Tacna, Peru (GRID:grid.441963.d) (ISNI:0000 0004 0541 9249) 
45  Museu Paraense Emílio Goeldi, Belém, Brazil (GRID:grid.452671.3) (ISNI:0000 0001 2175 1274) 
46  Instituto Venezolano de Investigaciones Científicas (IVIC), Caracas, Venezuela (GRID:grid.418243.8) (ISNI:0000 0001 2181 3287); IIAMA, Universitat Politécnica de València, València, Spain (GRID:grid.157927.f) (ISNI:0000 0004 1770 5832) 
47  Universidad Nacional de San Antonio Abad del Cusco, Cusco, Peru (GRID:grid.449379.4) (ISNI:0000 0001 2198 6786) 
48  Universidad Nacional de Colombia Sede Amazonia, Instituto Amazónico de Investigaciones Imani, Leticia, Colombia (GRID:grid.10689.36) (ISNI:0000 0001 0286 3748) 
49  Agteca, Santa Cruz, Bolivia (GRID:grid.10689.36) 
50  James Cook University, College of Science and Engineering, Cairns, Australia (GRID:grid.1011.1) (ISNI:0000 0004 0474 1797) 
51  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:0000000121901201) 
52  George Mason University, Environmental Science and Policy, Fairfax, USA (GRID:grid.22448.38) (ISNI:0000 0004 1936 8032) 
53  Australian National University, Research School of Biology, Canberra, Australia (GRID:grid.1001.0) (ISNI:0000 0001 2180 7477); University of Edinburgh, School of Geosciences, Edinburgh, UK (GRID:grid.4305.2) (ISNI:0000 0004 1936 7988) 
54  Universidad Mayor de San Simón, Escuela de Ciencias Forestales, Unidad Académica del Trópico, Cochabamba, Bolivia (GRID:grid.10491.3d) (ISNI:0000 0001 2176 4059) 
55  UNEMAT – Universidade do Estado de Mato Grosso PPG-Ecologia e Conservação, Nova Xavantina, Brazil (GRID:grid.10491.3d) 
56  Universidad Estatal Amazónica, Facultad de Ingeniería Ambiental, Puyo, Ecuador (GRID:grid.440858.5) (ISNI:0000 0004 0381 4018) 
57  Universidad Nacional de San Antonio Abad del Cusco, Cusco, Perú (GRID:grid.449379.4) (ISNI:0000 0001 2198 6786) 
58  UNEMAT – Universidade do Estado de Mato Grosso PPG-Ecologia e Conservação, Nova Xavantina, Brazil (GRID:grid.449379.4) 
59  University of Leeds, School of Geography, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403); Universidad Nacional de San Antonio Abad del Cusco, Cusco, Perú (GRID:grid.449379.4) (ISNI:0000 0001 2198 6786) 
60  Universidad Autónoma del Beni José Ballivián, Trinidad, Bolivia (GRID:grid.440545.4) (ISNI:0000 0004 1756 4689) 
61  Universidad Regional Amazónica Ikiam, Ikiam, Ecuador (GRID:grid.499611.2) (ISNI:0000 0004 4909 487X) 
62  Broward County Parks Recreation, Oakland Park, USA (GRID:grid.9909.9) 
63  Field Museum, Keller Science Action Center, Chicago, USA (GRID:grid.299784.9) (ISNI:0000 0001 0476 8496) 
64  Universidad Nacional de Colombia, Instituto de Ciencias Naturales, Bogotá, Colombia (GRID:grid.10689.36) (ISNI:0000 0001 0286 3748) 
65  University of Birmingham, School of Geography, Earth and Enviornmental Sciences, Birmingham, UK (GRID:grid.6572.6) (ISNI:0000 0004 1936 7486); University of Birmingham, Birmingham Institute of Forest Research, Birmingham, UK (GRID:grid.6572.6) (ISNI:0000 0004 1936 7486) 
66  Universidad de los Andes, Institute of Research for Forestry Development (INDEFOR), Mérida, Venezuela (GRID:grid.267525.1) (ISNI:0000 0004 1937 0853) 
67  University of Oxford, Environmental Change Institute, School of Geography and the Environment, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948); UNEMAT – Universidade do Estado de Mato Grosso PPG-Ecologia e Conservação, Nova Xavantina, Brazil (GRID:grid.4991.5) 
68  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.4991.5) 
69  Fundacion Con Vida, Socioecosistemas y Cambio Climatico, Medellín, Colombia (GRID:grid.4991.5) 
70  CIMA Cordillera Azul, Centro de Conservacion, Investigacion y Manejo de Areas Naturales, Lima, Peru (GRID:grid.4991.5) 
71  Museu Paraense Emílio Goeldi, Belém, Brazil (GRID:grid.452671.3) (ISNI:0000 0001 2175 1274); Universidade Federal Rural da Amazônia, Belém, Brazil (GRID:grid.440587.a) (ISNI:0000 0001 2186 5976) 
72  Universidad de Los Andes, Instituto de Investigaciones para el Desarrollo Forestal (INDEFOR), Mérida, Venezuela (GRID:grid.267525.1) (ISNI:0000 0004 1937 0853) 
73  Universidad Nacional de San Antonio Abad del Cusco, Cusco, Perú (GRID:grid.449379.4) (ISNI:0000 0001 2198 6786); Universidad de La Serena, Departamento de Biología, La Serena, Chile (GRID:grid.19208.32) (ISNI:0000 0001 0161 9268) 
74  Universidade Federal Rural da Amazônia, Belém, Brazil (GRID:grid.440587.a) (ISNI:0000 0001 2186 5976) 
75  Guyana Forestry Commission, Georgetown, Guyana (GRID:grid.494195.4) 
76  Université de Guyane, INRAE, UMR EcoFoG, CNRS, Cirad, AgroParisTech, Université des Antilles, Kourou, France (GRID:grid.494195.4) 
77  Federal University of Alagoas, Maceió, Brazil (GRID:grid.411179.b) (ISNI:0000 0001 2154 120X) 
78  Institute for Conservation Research, Escondido, USA (GRID:grid.411179.b) 
79  University of Leeds, Institute for Transport Studies, Leeds, UK (GRID:grid.9909.9) (ISNI:0000 0004 1936 8403) 
80  Naturalis Biodiversity Center, Biodiversity Dynamics, Leiden, The Netherlands (GRID:grid.425948.6) (ISNI:0000 0001 2159 802X); Free University, Systems Ecology, Amsterdam, Netherlands (GRID:grid.12380.38) (ISNI:0000 0004 1754 9227) 
81  University of Florida, Department of Biology, Gainesville, USA (GRID:grid.15276.37) (ISNI:0000 0004 1936 8091) 
82  Iwokrama International Centre for Rainforest Conservation and Development, Georgetown, Guyana (GRID:grid.15276.37) 
83  Universidad de los Andes, Mérida, Venezuela (GRID:grid.267525.1) (ISNI:0000 0004 1937 0853) 
84  Jardín Botánico de Missouri, Oxapampa, Peru (GRID:grid.267525.1) 
85  University of Nottingham, School of Geography, Nottingham, UK (GRID:grid.4563.4) (ISNI:0000 0004 1936 8868) 
86  Van Hall Larenstein University of Applied Sciences, Leeuwarden, Netherlands (GRID:grid.450080.9) (ISNI:0000 0004 1793 4571) 
87  Van der Hoult Forestry Consulting, Leeuwarden, The Netherlands (GRID:grid.450080.9) 
88  Jardín Botánico de Missouri, Oxapampa, Peru (GRID:grid.450080.9) 
89  Núcleo de Estudos e Pesquisas Ambientais – Universidade Estadual de Campinas, Campinas, Brazil (GRID:grid.411087.b) (ISNI:0000 0001 0723 2494) 
90  Universidad de San Francisco Xavier de Chuquisaca, Herbario del Sur de Bolivia, Sucre, Bolivia (GRID:grid.441965.b) (ISNI:0000 0001 2116 8986) 
91  Tropenbos International, Wageningen, Netherlands (GRID:grid.440545.4) 
Publication year
2020
Publication date
2020
Publisher
Nature Publishing Group
e-ISSN
20411723
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2471553268
Copyright
© The Author(s) 2020. corrected publication 2021. This work is published under https://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.