Tree mode of death and mortality risk factors across Amazon forests

Adriane Esquivel-Muelbert; Oliver L. Phillips; Roel J.W. Brienen; Sophie Fauset; Martin J.P. Sullivan; Timothy R. Baker; Kuo Jung Chao; Ted R. Feldpausch; Emanuel Gloor; Niro Higuchi; Jeanne Houwing-Duistermaat; Jon Lloyd; Haiyan Liu; Yadvinder Malhi; Beatriz Marimon; Ben Hur Marimon Junior; Abel Monteagudo-Mendoza; Lourens Poorter; Marcos Silveira; Emilio Vilanova Torre; Esteban Alvarez Dávila; Jhon del Aguila Pasquel; Everton Almeida; Patricia Alvarez Loayza; Ana Andrade; Luiz E.O.C. Aragão; Alejandro Araujo-Murakami; Eric Arets; Luzmila Arroyo; Gerardo A. Aymard C; Michel Baisie; Christopher Baraloto; Plínio Barbosa Camargo; Jorcely Barroso; Lilian Blanc; Damien Bonal; Frans Bongers; René Boot; Foster Brown; Benoit Burban; José Luís Camargo; Wendeson Castro; Victor Chama Moscoso; Jerome Chave; James Comiskey; Fernando Cornejo Valverde; Antonio Lola da Costa; Nallaret Davila Cardozo; Anthony Di Fiore; Aurélie Dourdain; Terry Erwin; Gerardo Flores Llampazo; Ima Célia Guimarães Vieira; Rafael Herrera; Eurídice Honorio Coronado; Isau Huamantupa-Chuquimaco; Eliana Jimenez-Rojas; Timothy Killeen; Susan Laurance; William Laurance; Aurora Levesley; Simon L. Lewis; Karina Liana Lisboa Melgaço Ladvocat; Gabriela Lopez-Gonzalez; Thomas Lovejoy; Patrick Meir; Casimiro Mendoza; Paulo Morandi; David Neill; Adriano José Nogueira Lima; Percy Nuñez Vargas; Edmar Almeida de Oliveira; Nadir Pallqui Camacho; Guido Pardo; Julie Peacock; Marielos Peña-Claros; Maria Cristina Peñuela-Mora; Georgia Pickavance; John Pipoly; Nigel Pitman; Adriana Prieto; Thomas A.M. Pugh; Carlos Quesada; Hirma Ramirez-Angulo; Simone Matias de Almeida Reis; Maxime Rejou-Machain; Zorayda Restrepo Correa; Lily Rodriguez Bayona; Agustín Rudas; Rafael Salomão; Julio Serrano; Javier Silva Espejo; Natalino Silva; James Singh; Clement Stahl; Juliana Stropp; Varun Swamy; Joey Talbot; Hans ter Steege; John Terborgh; Raquel Thomas; Marisol Toledo; Armando Torres-Lezama; Luis Valenzuela Gamarra; Geertje van der Heijden; Peter van der Meer; Peter van der Hout; Rodolfo Vasquez Martinez; Simone Aparecida Vieira; Jeanneth Villalobos Cayo; Vincent Vos; Roderick Zagt; Pieter Zuidema; David Galbraith

doi:10.1038/s41467-020-18996-3

Tree mode of death and mortality risk factors across Amazon forests

Adriane Esquivel-Muelbert^*, Oliver L. Phillips, Roel J.W. Brienen, Sophie Fauset, Martin J.P. Sullivan, Timothy R. Baker, Kuo Jung Chao, Ted R. Feldpausch, Emanuel Gloor, Niro Higuchi, Jeanne Houwing-Duistermaat, Jon Lloyd, Haiyan Liu, Yadvinder Malhi, Beatriz Marimon, Ben Hur Marimon Junior, Abel Monteagudo-Mendoza, Lourens Poorter, Marcos Silveira, Emilio Vilanova TorreEsteban Alvarez Dávila, Jhon del Aguila Pasquel, Everton Almeida, Patricia Alvarez Loayza, Ana Andrade, Luiz E.O.C. Aragão, Alejandro Araujo-Murakami, Eric Arets, Luzmila Arroyo, Gerardo A. Aymard C, Michel Baisie, Christopher Baraloto, Plínio Barbosa Camargo, Jorcely Barroso, Lilian Blanc, Damien Bonal, Frans Bongers, René Boot, Foster Brown, Benoit Burban, José Luís Camargo, Wendeson Castro, Victor Chama Moscoso, Jerome Chave, James Comiskey, Fernando Cornejo Valverde, Antonio Lola da Costa, Nallaret Davila Cardozo, Anthony Di Fiore, Aurélie Dourdain, Terry Erwin, Gerardo Flores Llampazo, Ima Célia Guimarães Vieira, Rafael Herrera, Eurídice Honorio Coronado, Isau Huamantupa-Chuquimaco, Eliana Jimenez-Rojas, Timothy Killeen, Susan Laurance, William Laurance, Aurora Levesley, Simon L. Lewis, Karina Liana Lisboa Melgaço Ladvocat, Gabriela Lopez-Gonzalez, Thomas Lovejoy, Patrick Meir, Casimiro Mendoza, Paulo Morandi, David Neill, Adriano José Nogueira Lima, Percy Nuñez Vargas, Edmar Almeida de Oliveira, Nadir Pallqui Camacho, Guido Pardo, Julie Peacock, Marielos Peña-Claros, Maria Cristina Peñuela-Mora, Georgia Pickavance, John Pipoly, Nigel Pitman, Adriana Prieto, Thomas A.M. Pugh, Carlos Quesada, Hirma Ramirez-Angulo, Simone Matias de Almeida Reis, Maxime Rejou-Machain, Zorayda Restrepo Correa, Lily Rodriguez Bayona, Agustín Rudas, Rafael Salomão, Julio Serrano, Javier Silva Espejo, Natalino Silva, James Singh, Clement Stahl, Juliana Stropp, Varun Swamy, Joey Talbot, Hans ter Steege, John Terborgh, Raquel Thomas, Marisol Toledo, Armando Torres-Lezama, Luis Valenzuela Gamarra, Geertje van der Heijden, Peter van der Meer, Peter van der Hout, Rodolfo Vasquez Martinez, Simone Aparecida Vieira, Jeanneth Villalobos Cayo, Vincent Vos, Roderick Zagt, Pieter Zuidema, David Galbraith

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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.

Original language	English
Article number	5515
Pages (from-to)	1-11
Number of pages	11
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-18996-3
Publication status	Published - 9 Nov 2020

Funding

This manuscript is an outcome of efforts over three decades of hundreds of researchers across Amazonia as well as the sustained support of rural communities and Amazonian institutions and their funding agencies that make the RAINFOR network possible. We thank the following individuals in particular for their contribution to the long-term monitoring of South American forests: Alwyn Gentry, Sandra Patiño, Samuel Almeida, Miguel Alexiades, Olaf Banki, Desmo Betian, Vincent Bezard, Ezequiel Chavez, René Guillen Villaroel, Antonio S. Lima, Irina Mendoza Polo, Petrus Naisso, Atila Alves de Oliveira, Alexander Parada Gutierrez, Jean Pierre Veillon, Freddy Ramirez Arevalo and Marc Steininger. The analysis undertaken here was largely funded by the NERC-funded TREMOR project (NE/N004655/1) to D.G., R.J.W.B., E.G. and O.L.P. A.E.-M. was funded by TREMOR and by two ERC awards (T-FORCES 291585, TreeMort 758873). D.G. acknowledges further support from a Newton-funded consortium award (ARBOLES, NE/S011811/1). O.L.P. was supported by an ERC Advanced Grant and a Royal Society Wolfson Research Merit Award. T.A.M.P. was funded by the ERC award TreeMort 758873. This is paper number 47 of the Birmingham Institute of Forest Research. T.R.F., L.E.O.C.A. and O.L.P. were supported by NERC NE/N011570/1. Support for RAINFOR has come from the Natural Environment Research Council (NERC) Urgency Grants and NERC Consortium Grants AMAZONICA (NE/F005806/ 1), TROBIT (NE/D005590/1) and BIO-RED (NE/N012542/1), a European Research Council (ERC) grant T-FORCES (291585), the Gordon and Betty Moore Foundation (#1656), the European Union’s Seventh Framework Programme (282664, AMAZA-LERT) and the Royal Society (CH160091). This is paper #47 of the Birmingham Institute of Forest Research (BIFoR). A.E.-M. thanks LES female writing group. Data from RAINFOR and other tropical networks are stored and curated by ForestPlots.net, a collaborative cyber-infrastructure initiative developed at the University of Leeds that unites permanent plot records and their contributing scientists from the world’s tropical forests. All the bodies listed above have funded the development of ForestPlots.net and curation of data analysed here. This work is an outcome of the ForestPlots.net approved research project #8.

Funders	Funder number
BIO-RED	NE/N012542/1
NERC-funded
TREMOR	NE/S011811/1
TROBIT	NE/D005590/1
Gordon and Betty Moore Foundation	1656
Horizon 2020 Framework Programme	282664
H2020 European Research Council	291585, 758873
Seventh Framework Programme	CH160091
Natural Environment Research Council	NE/N004655/1, NE/F005806/ 1
Royal Society	NE/N011570/1
European Research Council

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Esquivel-Muelbert, A., Phillips, O. L., Brienen, R. J. W., Fauset, S., Sullivan, M. J. P., Baker, T. R., Chao, K. J., Feldpausch, T. R., Gloor, E., Higuchi, N., Houwing-Duistermaat, J., Lloyd, J., Liu, H., Malhi, Y., Marimon, B., Marimon Junior, B. H., Monteagudo-Mendoza, A., Poorter, L., Silveira, M., ... Galbraith, D. (2020). Tree mode of death and mortality risk factors across Amazon forests. Nature Communications, 11(1), 1-11. Article 5515. https://doi.org/10.1038/s41467-020-18996-3

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title = "Tree mode of death and mortality risk factors across Amazon forests",

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.",

author = "Adriane Esquivel-Muelbert and Phillips, {Oliver L.} and Brienen, {Roel J.W.} and Sophie Fauset and Sullivan, {Martin J.P.} and Baker, {Timothy R.} and Chao, {Kuo Jung} and Feldpausch, {Ted R.} and Emanuel Gloor and Niro Higuchi and Jeanne Houwing-Duistermaat and Jon Lloyd and Haiyan Liu and Yadvinder Malhi and Beatriz Marimon and {Marimon Junior}, {Ben Hur} and Abel Monteagudo-Mendoza and Lourens Poorter and Marcos Silveira and Torre, {Emilio Vilanova} and D{\'a}vila, {Esteban Alvarez} and {del Aguila Pasquel}, Jhon and Everton Almeida and Loayza, {Patricia Alvarez} and Ana Andrade and Arag{\~a}o, {Luiz E.O.C.} and Alejandro Araujo-Murakami and Eric Arets and Luzmila Arroyo and {Aymard C}, {Gerardo A.} and Michel Baisie and Christopher Baraloto and Camargo, {Pl{\'i}nio Barbosa} and Jorcely Barroso and Lilian Blanc and Damien Bonal and Frans Bongers and Ren{\'e} Boot and Foster Brown and Benoit Burban and Camargo, {Jos{\'e} Lu{\'i}s} and Wendeson Castro and Moscoso, {Victor Chama} and Jerome Chave and James Comiskey and Valverde, {Fernando Cornejo} and {da Costa}, {Antonio Lola} and Cardozo, {Nallaret Davila} and {Di Fiore}, Anthony and Aur{\'e}lie Dourdain and Terry Erwin and Llampazo, {Gerardo Flores} and Vieira, {Ima C{\'e}lia Guimar{\~a}es} and Rafael Herrera and {Honorio Coronado}, Eur{\'i}dice and Isau Huamantupa-Chuquimaco and Eliana Jimenez-Rojas and Timothy Killeen and Susan Laurance and William Laurance and Aurora Levesley and Lewis, {Simon L.} and Ladvocat, {Karina Liana Lisboa Melga{\c c}o} and Gabriela Lopez-Gonzalez and Thomas Lovejoy and Patrick Meir and Casimiro Mendoza and Paulo Morandi and David Neill and {Nogueira Lima}, {Adriano Jos{\'e}} and Vargas, {Percy Nu{\~n}ez} and {de Oliveira}, {Edmar Almeida} and Camacho, {Nadir Pallqui} and Guido Pardo and Julie Peacock and Marielos Pe{\~n}a-Claros and Pe{\~n}uela-Mora, {Maria Cristina} and Georgia Pickavance and John Pipoly and Nigel Pitman and Adriana Prieto and Pugh, {Thomas A.M.} and Carlos Quesada and Hirma Ramirez-Angulo and {de Almeida Reis}, {Simone Matias} and Maxime Rejou-Machain and Correa, {Zorayda Restrepo} and Bayona, {Lily Rodriguez} and Agust{\'i}n Rudas and Rafael Salom{\~a}o and Julio Serrano and Espejo, {Javier Silva} and Natalino Silva and James Singh and Clement Stahl and Juliana Stropp and Varun Swamy and Joey Talbot and {ter Steege}, Hans and John Terborgh and Raquel Thomas and Marisol Toledo and Armando Torres-Lezama and Gamarra, {Luis Valenzuela} and {van der Heijden}, Geertje and {van der Meer}, Peter and {van der Hout}, Peter and Martinez, {Rodolfo Vasquez} and Vieira, {Simone Aparecida} and Cayo, {Jeanneth Villalobos} and Vincent Vos and Roderick Zagt and Pieter Zuidema and David Galbraith",

year = "2020",

month = nov,

day = "9",

doi = "10.1038/s41467-020-18996-3",

language = "English",

volume = "11",

pages = "1--11",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

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Esquivel-Muelbert, A, Phillips, OL, Brienen, RJW, Fauset, S, Sullivan, MJP, Baker, TR, Chao, KJ, Feldpausch, TR, Gloor, E, Higuchi, N, Houwing-Duistermaat, J, Lloyd, J, Liu, H, Malhi, Y, Marimon, B, Marimon Junior, BH, Monteagudo-Mendoza, A, Poorter, L, Silveira, M, Torre, EV, Dávila, EA, del Aguila Pasquel, J, Almeida, E, Loayza, PA, Andrade, A, Aragão, LEOC, Araujo-Murakami, A, Arets, E, Arroyo, L, Aymard C, GA, Baisie, M, Baraloto, C, Camargo, PB, Barroso, J, Blanc, L, Bonal, D, Bongers, F, Boot, R, Brown, F, Burban, B, Camargo, JL, Castro, W, Moscoso, VC, Chave, J, Comiskey, J, Valverde, FC, da Costa, AL, Cardozo, ND, Di Fiore, A, Dourdain, A, Erwin, T, Llampazo, GF, Vieira, ICG, Herrera, R, Honorio Coronado, E, Huamantupa-Chuquimaco, I, Jimenez-Rojas, E, Killeen, T, Laurance, S, Laurance, W, Levesley, A, Lewis, SL, Ladvocat, KLLM, Lopez-Gonzalez, G, Lovejoy, T, Meir, P, Mendoza, C, Morandi, P, Neill, D, Nogueira Lima, AJ, Vargas, PN, de Oliveira, EA, Camacho, NP, Pardo, G, Peacock, J, Peña-Claros, M, Peñuela-Mora, MC, Pickavance, G, Pipoly, J, Pitman, N, Prieto, A, Pugh, TAM, Quesada, C, Ramirez-Angulo, H, de Almeida Reis, SM, Rejou-Machain, M, Correa, ZR, Bayona, LR, Rudas, A, Salomão, R, Serrano, J, Espejo, JS, Silva, N, Singh, J, Stahl, C, Stropp, J, Swamy, V, Talbot, J, ter Steege, H, Terborgh, J, Thomas, R, Toledo, M, Torres-Lezama, A, Gamarra, LV, van der Heijden, G, van der Meer, P, van der Hout, P, Martinez, RV, Vieira, SA, Cayo, JV, Vos, V, Zagt, R, Zuidema, P & Galbraith, D 2020, 'Tree mode of death and mortality risk factors across Amazon forests', Nature Communications, vol. 11, no. 1, 5515, pp. 1-11. https://doi.org/10.1038/s41467-020-18996-3

TY - JOUR

T1 - Tree mode of death and mortality risk factors across Amazon forests

AU - Esquivel-Muelbert, Adriane

AU - Phillips, Oliver L.

AU - Brienen, Roel J.W.

AU - Fauset, Sophie

AU - Sullivan, Martin J.P.

AU - Baker, Timothy R.

AU - Chao, Kuo Jung

AU - Feldpausch, Ted R.

AU - Gloor, Emanuel

AU - Higuchi, Niro

AU - Houwing-Duistermaat, Jeanne

AU - Lloyd, Jon

AU - Liu, Haiyan

AU - Malhi, Yadvinder

AU - Marimon, Beatriz

AU - Marimon Junior, Ben Hur

AU - Monteagudo-Mendoza, Abel

AU - Poorter, Lourens

AU - Silveira, Marcos

AU - Torre, Emilio Vilanova

AU - Dávila, Esteban Alvarez

AU - del Aguila Pasquel, Jhon

AU - Almeida, Everton

AU - Loayza, Patricia Alvarez

AU - Andrade, Ana

AU - Aragão, Luiz E.O.C.

AU - Araujo-Murakami, Alejandro

AU - Arets, Eric

AU - Arroyo, Luzmila

AU - Aymard C, Gerardo A.

AU - Baisie, Michel

AU - Baraloto, Christopher

AU - Camargo, Plínio Barbosa

AU - Barroso, Jorcely

AU - Blanc, Lilian

AU - Bonal, Damien

AU - Bongers, Frans

AU - Boot, René

AU - Brown, Foster

AU - Burban, Benoit

AU - Camargo, José Luís

AU - Castro, Wendeson

AU - Moscoso, Victor Chama

AU - Chave, Jerome

AU - Comiskey, James

AU - Valverde, Fernando Cornejo

AU - da Costa, Antonio Lola

AU - Cardozo, Nallaret Davila

AU - Di Fiore, Anthony

AU - Dourdain, Aurélie

AU - Erwin, Terry

AU - Llampazo, Gerardo Flores

AU - Vieira, Ima Célia Guimarães

AU - Herrera, Rafael

AU - Honorio Coronado, Eurídice

AU - Huamantupa-Chuquimaco, Isau

AU - Jimenez-Rojas, Eliana

AU - Killeen, Timothy

AU - Laurance, Susan

AU - Laurance, William

AU - Levesley, Aurora

AU - Lewis, Simon L.

AU - Ladvocat, Karina Liana Lisboa Melgaço

AU - Lopez-Gonzalez, Gabriela

AU - Lovejoy, Thomas

AU - Meir, Patrick

AU - Mendoza, Casimiro

AU - Morandi, Paulo

AU - Neill, David

AU - Nogueira Lima, Adriano José

AU - Vargas, Percy Nuñez

AU - de Oliveira, Edmar Almeida

AU - Camacho, Nadir Pallqui

AU - Pardo, Guido

AU - Peacock, Julie

AU - Peña-Claros, Marielos

AU - Peñuela-Mora, Maria Cristina

AU - Pickavance, Georgia

AU - Pipoly, John

AU - Pitman, Nigel

AU - Prieto, Adriana

AU - Pugh, Thomas A.M.

AU - Quesada, Carlos

AU - Ramirez-Angulo, Hirma

AU - de Almeida Reis, Simone Matias

AU - Rejou-Machain, Maxime

AU - Correa, Zorayda Restrepo

AU - Bayona, Lily Rodriguez

AU - Rudas, Agustín

AU - Salomão, Rafael

AU - Serrano, Julio

AU - Espejo, Javier Silva

AU - Silva, Natalino

AU - Singh, James

AU - Stahl, Clement

AU - Stropp, Juliana

AU - Swamy, Varun

AU - Talbot, Joey

AU - ter Steege, Hans

AU - Terborgh, John

AU - Thomas, Raquel

AU - Toledo, Marisol

AU - Torres-Lezama, Armando

AU - Gamarra, Luis Valenzuela

AU - van der Heijden, Geertje

AU - van der Meer, Peter

AU - van der Hout, Peter

AU - Martinez, Rodolfo Vasquez

AU - Vieira, Simone Aparecida

AU - Cayo, Jeanneth Villalobos

AU - Vos, Vincent

AU - Zagt, Roderick

AU - Zuidema, Pieter

AU - Galbraith, David

PY - 2020/11/9

Y1 - 2020/11/9

N2 - 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.

AB - 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.

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UR - http://www.scopus.com/inward/citedby.url?scp=85095701315&partnerID=8YFLogxK

U2 - 10.1038/s41467-020-18996-3

DO - 10.1038/s41467-020-18996-3

M3 - Article

C2 - 33168823

AN - SCOPUS:85095701315

SN - 2041-1723

VL - 11

SP - 1

EP - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 5515

ER -

Tree mode of death and mortality risk factors across Amazon forests

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