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Title: Drivers and mechanisms of tree mortality in moist tropical forests

Abstract

Tree mortality rates appear to be increasing in moist tropical forests (MTFs) with significant carbon cycle consequences. We review the state of knowledge regarding MTF tree mortality, create a conceptual framework with testable hypotheses regarding the drivers, mechanisms, and interactions that may underlie increasing MTF mortality rates, and identify next steps for improved understanding and reduced prediction. Increasing mortality rates are associated with rising temperature and vapor pressure deficit, liana abundance, drought, wind events, fire, and possibly CO2 fertilization-induced increases in stand thinning or acceleration of trees reaching larger, more vulnerable heights. The majority of these mortality drivers may kill trees in part through carbon starvation and hydraulic failure. The relative importance of each driver is unknown. High species diversity may buffer MTFs against large-scale mortality events, but recent and expected trends in mortality drivers give reason for concern regarding increasing mortality within MTFs. Models of tropical tree mortality are advancing representation of hydraulics, carbon, and demography, but require more empirical knowledge regarding the most common drivers and their subsequent mechanisms. We outline critical datasets and model developments required to test hypotheses regarding the underlying causes of increasing MTF mortality rates, and improve prediction of future mortality under climate change.

Authors:
 [1];  [2];  [3];  [4];  [5];  [6]; ORCiD logo [7];  [8];  [9];  [10];  [11];  [12];  [13];  [14];  [15];  [15];  [16];  [6];  [15];  [17] more »;  [18];  [6];  [19];  [20];  [21];  [22];  [23];  [24];  [25];  [26];  [14]; ORCiD logo [6];  [16];  [27];  [28];  [15]; ORCiD logo [29] « less
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. US Geological Survey, Los Alamos NM (United States). Fort Collins Science Center, New Mexico Landscapes Field Station
  3. Smithsonian Tropical Research Inst., Washington, DC (United States). Center for Tropical Forest Science-Forest Global Earth Observatory; Smithsonian Conservation Biology Inst., National Zoological Park, Front Royal, VA (United States). Conservation Ecology Center
  4. Woods Hole Research Center, Falmouth, MA (United States); Inst. de Pesquisa Ambiental de Amazonia, Lago Norte, Brasilia (Brazil)
  5. Univ. of Leeds, Woodhouse Lane Leeds (United Kingdom). School of Geography,
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of Texas Rio Grande Valley, Edinburg, TX (United States)
  8. Smithsonian Tropical Research Inst., Washington, DC (United States). Center for Tropical Forest Science-Forest Global Earth Observatory
  9. Northern Arizona Univ., Flagstaff, AZ (United States)
  10. Univ. Nacional de Columbia, Medellin (Columbia)
  11. Univ. of Lancaster, Lancaster (United Kingdom)
  12. National Center for Atmospheric Research, Boulder, CO (United States)
  13. Univ. of California, Berkeley, CA (United States)
  14. Univ. of Leeds, Leeds (United Kingdom)
  15. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  16. Max Plank Institute for Biogeochemistry, Jena (Germany)
  17. Forest Research Institute Malaysia, Selangor (Malaysia)
  18. USDA Jardin Botanico Sur, San Juan (Puerto Rico); Embrapa Agricultural Informatics, Brasilia (Brazil); Jet Propulsion Lab., Pasadena, CA (United States)
  19. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  20. The Univ. of Tokyo, Tokyo (Japan)
  21. Univ. of Oxford, Oxford (United Kingdom)
  22. Smithsonian Tropical Research Institute, Washington, D.C. (United States)
  23. Univ. of Barcelona, Barcelona (Spain)
  24. Australian National Univ., Canberra, ACT (Australia); Univ. of Edinburgh, Edinburgh (United Kingdom)
  25. Harvard Univ., Cambridge, MA (United States)
  26. Smithsonian Tropical Research Institute (Panama Republica de Panama)
  27. Univ. of Utah, Salt Lake City, UT (United States)
  28. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  29. Princeton Univ., NJ (United States). Dept. of Geosciences
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1506341
Alternate Identifier(s):
OSTI ID: 1421573; OSTI ID: 1461063; OSTI ID: 1529987
Report Number(s):
PNNL-SA-132031
Journal ID: ISSN 0028-646X; ark:/13030/qt6f92q2mv
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 219; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbon (C) starvation; CO 2 fertilization; forest mortality; hydraulic failure; tropical forests; carbon starvation, CO2 fertilization, hydraulic failure, forest mortality, tropical forests

Citation Formats

McDowell, Nate, Allen, Craig D., Anderson-Teixeira, Kristina, Brando, Paulo, Brienen, Roel, Chambers, Jeff, Christoffersen, Brad, Davies, Stuart, Doughty, Chris, Duque, Alvaro, Espirito-Santo, Fernando, Fisher, Rosie, Fontes, Clarissa G., Galbraith, David, Goodsman, Devin, Grossiord, Charlotte, Hartmann, Henrik, Holm, Jennifer, Johnson, Daniel J., Kassim, Abd. Rahman, Keller, Michael, Koven, Charlie, Kueppers, Lara, Kumagai, Tomo'omi, Malhi, Yadvinder, McMahon, Sean M., Mencuccini, Maurizio, Meir, Patrick, Moorcroft, Paul, Muller-Landau, Helene C., Phillips, Oliver L., Powell, Thomas, Sierra, Carlos A., Sperry, John, Warren, Jeff, Xu, Chonggang, and Xu, Xiangtao. Drivers and mechanisms of tree mortality in moist tropical forests. United States: N. p., 2018. Web. doi:10.1111/nph.15027.
McDowell, Nate, Allen, Craig D., Anderson-Teixeira, Kristina, Brando, Paulo, Brienen, Roel, Chambers, Jeff, Christoffersen, Brad, Davies, Stuart, Doughty, Chris, Duque, Alvaro, Espirito-Santo, Fernando, Fisher, Rosie, Fontes, Clarissa G., Galbraith, David, Goodsman, Devin, Grossiord, Charlotte, Hartmann, Henrik, Holm, Jennifer, Johnson, Daniel J., Kassim, Abd. Rahman, Keller, Michael, Koven, Charlie, Kueppers, Lara, Kumagai, Tomo'omi, Malhi, Yadvinder, McMahon, Sean M., Mencuccini, Maurizio, Meir, Patrick, Moorcroft, Paul, Muller-Landau, Helene C., Phillips, Oliver L., Powell, Thomas, Sierra, Carlos A., Sperry, John, Warren, Jeff, Xu, Chonggang, & Xu, Xiangtao. Drivers and mechanisms of tree mortality in moist tropical forests. United States. https://doi.org/10.1111/nph.15027
McDowell, Nate, Allen, Craig D., Anderson-Teixeira, Kristina, Brando, Paulo, Brienen, Roel, Chambers, Jeff, Christoffersen, Brad, Davies, Stuart, Doughty, Chris, Duque, Alvaro, Espirito-Santo, Fernando, Fisher, Rosie, Fontes, Clarissa G., Galbraith, David, Goodsman, Devin, Grossiord, Charlotte, Hartmann, Henrik, Holm, Jennifer, Johnson, Daniel J., Kassim, Abd. Rahman, Keller, Michael, Koven, Charlie, Kueppers, Lara, Kumagai, Tomo'omi, Malhi, Yadvinder, McMahon, Sean M., Mencuccini, Maurizio, Meir, Patrick, Moorcroft, Paul, Muller-Landau, Helene C., Phillips, Oliver L., Powell, Thomas, Sierra, Carlos A., Sperry, John, Warren, Jeff, Xu, Chonggang, and Xu, Xiangtao. Fri . "Drivers and mechanisms of tree mortality in moist tropical forests". United States. https://doi.org/10.1111/nph.15027. https://www.osti.gov/servlets/purl/1506341.
@article{osti_1506341,
title = {Drivers and mechanisms of tree mortality in moist tropical forests},
author = {McDowell, Nate and Allen, Craig D. and Anderson-Teixeira, Kristina and Brando, Paulo and Brienen, Roel and Chambers, Jeff and Christoffersen, Brad and Davies, Stuart and Doughty, Chris and Duque, Alvaro and Espirito-Santo, Fernando and Fisher, Rosie and Fontes, Clarissa G. and Galbraith, David and Goodsman, Devin and Grossiord, Charlotte and Hartmann, Henrik and Holm, Jennifer and Johnson, Daniel J. and Kassim, Abd. Rahman and Keller, Michael and Koven, Charlie and Kueppers, Lara and Kumagai, Tomo'omi and Malhi, Yadvinder and McMahon, Sean M. and Mencuccini, Maurizio and Meir, Patrick and Moorcroft, Paul and Muller-Landau, Helene C. and Phillips, Oliver L. and Powell, Thomas and Sierra, Carlos A. and Sperry, John and Warren, Jeff and Xu, Chonggang and Xu, Xiangtao},
abstractNote = {Tree mortality rates appear to be increasing in moist tropical forests (MTFs) with significant carbon cycle consequences. We review the state of knowledge regarding MTF tree mortality, create a conceptual framework with testable hypotheses regarding the drivers, mechanisms, and interactions that may underlie increasing MTF mortality rates, and identify next steps for improved understanding and reduced prediction. Increasing mortality rates are associated with rising temperature and vapor pressure deficit, liana abundance, drought, wind events, fire, and possibly CO2 fertilization-induced increases in stand thinning or acceleration of trees reaching larger, more vulnerable heights. The majority of these mortality drivers may kill trees in part through carbon starvation and hydraulic failure. The relative importance of each driver is unknown. High species diversity may buffer MTFs against large-scale mortality events, but recent and expected trends in mortality drivers give reason for concern regarding increasing mortality within MTFs. Models of tropical tree mortality are advancing representation of hydraulics, carbon, and demography, but require more empirical knowledge regarding the most common drivers and their subsequent mechanisms. We outline critical datasets and model developments required to test hypotheses regarding the underlying causes of increasing MTF mortality rates, and improve prediction of future mortality under climate change.},
doi = {10.1111/nph.15027},
journal = {New Phytologist},
number = 3,
volume = 219,
place = {United States},
year = {Fri Feb 16 00:00:00 EST 2018},
month = {Fri Feb 16 00:00:00 EST 2018}
}

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Figures / Tables:

Fig. 1 Fig. 1: Axes of variability in tropical tree mortality. (a) Mortality rate (as log(initial number) – log(number survivors))/(years)) vs stem diameter in Pasoh, Malaysia and Barro Colorado, Panama (bars are 95% confidence intervals (CIs), no major droughts during censuses); this highlights that both negative and positive mortality rates as amore » function of diameter can be found (data from Muller-Landau et al., 2006). (b) Mortality rates (number of individuals died per number of total individuals per year; all subsequent figures use this calculation; see Box 1 Glossary and Supporting Information Methods S1 on mortality rate calculations) plotted as the ratio of mortality rate during drought relative to a control period across a range of stem diameters for 12 sites across the tropics (symbols represent different sites), showing the clear pattern of size–mortality relationships during droughts (data from Bennett et al., 2015). (c) The mortality rates in forests in Borneo and the Amazon measured post-drought, highlighting regional differences (data from Phillips et al., 2010). (d) Mortality rate vs lifehistory strategy in Barro Colorado, Panama, highlighting the role of successional strategy on long-term mortality rates (data from Condit et al., 1995). (e) Mortality rate vs wood density in Barro Colorado, Panama, highlighting a significant but weak relationship (P < 0.05; data from Wright et al., 2010). (f) Mortality rate as a function of liana cover class in Pasoh, Malaysia, highlighting the influence of lianas on mortality. Liana cover class: 0, no lianas; 1, up to25%of the crown covered by lianas; 2, 26–50%; 3, 51–75%; 4, 76–100% (data from Wright et al., 2015). All error bars are $\pm$ SE.« less

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The gathering firestorm in southern Amazonia
journal, January 2020

  • Brando, P. M.; Soares-Filho, B.; Rodrigues, L.
  • Science Advances, Vol. 6, Issue 2
  • DOI: 10.1126/sciadv.aay1632

Carbon Stock Growth in a Secondary Atlantic Forest
journal, January 2019

  • Villanova, Paulo Henrique; Torres, Carlos Moreira Miquelino Eleto; Jacovine, Laércio Antônio Gonçalves
  • Revista Árvore, Vol. 43, Issue 4
  • DOI: 10.1590/1806-90882019000400002

High ecosystem stability of evergreen broadleaf forests under severe droughts
journal, July 2019

  • Huang, Kun; Xia, Jianyang
  • Global Change Biology, Vol. 25, Issue 10
  • DOI: 10.1111/gcb.14748

Diversity, distribution and dynamics of large trees across an old-growth lowland tropical rain forest landscape
journal, November 2019


Crown damage and the mortality of tropical trees
journal, August 2018

  • Arellano, Gabriel; Medina, Nagore G.; Tan, Sylvester
  • New Phytologist, Vol. 221, Issue 1
  • DOI: 10.1111/nph.15381

Pre-Columbian human occupation of Amazonia and its influence on current landscapes and biodiversity
journal, January 2019


Functional perspectives on tropical tree demography and forest dynamics
journal, January 2019


Fire, fragmentation, and windstorms: A recipe for tropical forest degradation
journal, October 2018

  • Silvério, Divino V.; Brando, Paulo M.; Bustamante, Mercedes M. C.
  • Journal of Ecology, Vol. 107, Issue 2
  • DOI: 10.1111/1365-2745.13076

The importance and challenges of detecting changes in forest mortality rates
journal, February 2019

  • McMahon, Sean M.; Arellano, Gabriel; Davies, Stuart J.
  • Ecosphere, Vol. 10, Issue 2
  • DOI: 10.1002/ecs2.2615

Canopy structure and topography jointly constrain the microclimate of human-modified tropical landscapes.
text, January 2018

  • Jucker, Tommaso; Hardwick, Stephen R.; Both, Sabine
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.32489

Identification of key parameters controlling demographically structured vegetation dynamics in a land surface model: CLM4.5(FATES)
journal, January 2019

  • Massoud, Elias C.; Xu, Chonggang; Fisher, Rosie A.
  • Geoscientific Model Development, Vol. 12, Issue 9
  • DOI: 10.5194/gmd-12-4133-2019

Mechanisms of a coniferous woodland persistence under drought and heat
journal, April 2019

  • McDowell, Nate G.; Grossiord, Charlotte; Adams, Henry D.
  • Environmental Research Letters, Vol. 14, Issue 4
  • DOI: 10.1088/1748-9326/ab0921

Carbon exchange in an Amazon forest: from hours to years
journal, January 2018


Homoeostatic maintenance of nonstructural carbohydrates during the 2015–2016 El Niño drought across a tropical forest precipitation gradient
journal, January 2019

  • Dickman, Lee Turin; McDowell, Nate G.; Grossiord, Charlotte
  • Plant, Cell & Environment, Vol. 42, Issue 5
  • DOI: 10.1111/pce.13501

Testing for changes in biomass dynamics in large‐scale forest datasets
journal, October 2019

  • Rutishauser, Ervan; Wright, Stuart J.; Condit, Richard
  • Global Change Biology, Vol. 26, Issue 3
  • DOI: 10.1111/gcb.14833

Atlantic forest and leaf traits: an overview
journal, May 2019


Drought and the interannual variability of stem growth in an aseasonal, everwet forest
journal, February 2019

  • Hogan, J. Aaron; McMahon, Sean M.; Buzzard, Vanessa
  • Biotropica, Vol. 51, Issue 2
  • DOI: 10.1111/btp.12624

Lightning is a major cause of large tree mortality in a lowland neotropical forest
journal, October 2019

  • Yanoviak, Stephen P.; Gora, Evan M.; Bitzer, Phillip M.
  • New Phytologist, Vol. 225, Issue 5
  • DOI: 10.1111/nph.16260

Forecasting semi‐arid biome shifts in the Anthropocene
journal, January 2020

  • Kulmatiski, Andrew; Yu, Kailiang; Mackay, D. Scott
  • New Phytologist, Vol. 226, Issue 2
  • DOI: 10.1111/nph.16381

Tree species and size influence soil water partitioning in coffee agroforestry
journal, March 2019


An extensive suite of functional traits distinguishes Hawaiian wet and dry forests and enables prediction of species vital rates
journal, December 2018

  • Medeiros, Camila D.; Scoffoni, Christine; John, Grace P.
  • Functional Ecology, Vol. 33, Issue 4
  • DOI: 10.1111/1365-2435.13229

Contrasting Response to Drought and Climate of Planted and Natural Pinus pinaster Aiton Forests in Southern Spain
journal, July 2019

  • Rodriguez-Vallejo, Carlos; Navarro-Cerrillo, Rafael M.
  • Forests, Vol. 10, Issue 7
  • DOI: 10.3390/f10070603

Ecosystem heterogeneity and diversity mitigate Amazon forest resilience to frequent extreme droughts
journal, May 2018

  • Longo, Marcos; Knox, Ryan G.; Levine, Naomi M.
  • New Phytologist, Vol. 219, Issue 3
  • DOI: 10.1111/nph.15185

Canopy structure and topography jointly constrain the microclimate of human-modified tropical landscapes
journal, September 2018

  • Jucker, Tommaso; Hardwick, Stephen R.; Both, Sabine
  • Global Change Biology, Vol. 24, Issue 11
  • DOI: 10.1111/gcb.14415

Molecular bases of responses to abiotic stress in trees
journal, November 2019

  • Estravis-Barcala, Maximiliano; Mattera, María Gabriela; Soliani, Carolina
  • Journal of Experimental Botany, Vol. 71, Issue 13
  • DOI: 10.1093/jxb/erz532

Drought Sensitiveness on Forest Growth in Peninsular Spain and the Balearic Islands
journal, August 2018

  • Peña-Gallardo, Marina; Vicente-Serrano, Sergio; Camarero, J.
  • Forests, Vol. 9, Issue 9
  • DOI: 10.3390/f9090524

Performance of tropical forest seedlings under shade and drought: an interspecific trade-off in demographic responses
journal, December 2019

  • Kupers, Stefan J.; Wirth, Christian; Engelbrecht, Bettina M. J.
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-019-55256-x

Understanding and predicting frost‐induced tropical tree mortality patterns
journal, August 2019

  • Bojórquez, Adrián; Álvarez‐Yépiz, Juan C.; Búrquez, Alberto
  • Global Change Biology, Vol. 25, Issue 11
  • DOI: 10.1111/gcb.14775

Carbon Dynamics in a Human-Modified Tropical Forest: A Case Study Using Multi-Temporal LiDAR Data
journal, January 2020

  • Moura, Yhasmin Mendes de; Balzter, Heiko; Galvão, Lênio S.
  • Remote Sensing, Vol. 12, Issue 3
  • DOI: 10.3390/rs12030430

Wood allocation trade‐offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees
journal, February 2020

  • Janssen, Thomas A. J.; Hölttä, Teemu; Fleischer, Katrin
  • Plant, Cell & Environment, Vol. 43, Issue 4
  • DOI: 10.1111/pce.13687

Windthrows control biomass patterns and functional composition of Amazon forests
journal, October 2018

  • Magnabosco Marra, Daniel; Trumbore, Susan E.; Higuchi, Niro
  • Global Change Biology, Vol. 24, Issue 12
  • DOI: 10.1111/gcb.14457

Climatic and local stressor interactions threaten tropical forests and coral reefs
journal, January 2020

  • França, Filipe M.; Benkwitt, Cassandra E.; Peralta, Guadalupe
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1794
  • DOI: 10.1098/rstb.2019.0116

Estimation of coarse dead wood stocks in intact and degraded forests in the Brazilian Amazon using airborne lidar
journal, January 2019

  • Scaranello, Marcos A. S.; Keller, Michael; Longo, Marcos
  • Biogeosciences, Vol. 16, Issue 17
  • DOI: 10.5194/bg-16-3457-2019

Asynchronous carbon sink saturation in African and Amazonian tropical forests
journal, March 2020


One Century of Forest Monitoring Data in Switzerland Reveals Species- and Site-Specific Trends of Climate-Induced Tree Mortality
journal, March 2019

  • Etzold, Sophia; Ziemińska, Kasia; Rohner, Brigitte
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00307

Amazonian rainforest tree mortality driven by climate and functional traits
journal, April 2019


Performance of tropical forest seedlings under shade and drought: an interspecific trade-off in demographic responses
journal, December 2019

  • Kupers, Stefan J.; Wirth, Christian; Engelbrecht, Bettina M. J.
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-019-55256-x

Slow-growing species cope best with drought: evidence from long-term measurements in a tropical semi-deciduous moist forest of Central Africa
journal, October 2013

  • Ouédraogo, Dakis-Yaoba; Mortier, Frédéric; Gourlet-Fleury, Sylvie
  • Journal of Ecology, Vol. 101, Issue 6
  • DOI: 10.1111/1365-2745.12165

Diversity, distribution and dynamics of large trees across an old-growth lowland tropical rain forest landscape
journal, November 2019


Interactions Between Land-Use Change and Climate-Carbon Cycle Feedbacks
journal, April 2018


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.