A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Adams, Henry D.; Zeppel, Melanie J.  B.; Anderegg, William R.  L.; Hartmann, Henrik; Landhäusser, Simon M.; Tissue, David T.; Huxman, Travis E.; Hudson, Patrick J.; Franz, Trenton E.; Allen, Craig D.; Anderegg, Leander D.  L.; Barron-Gafford, Greg A.; Beerling, David J.; Breshears, David D.; Brodribb, Timothy J.; Bugmann, Harald; Cobb, Richard C.; Collins, Adam D.; Dickman, L. Turin; Duan, Honglang; Ewers, Brent E.; Galiano, Lucía; Galvez, David A.; Garcia-Forner, Núria; Gaylord, Monica L.; Germino, Matthew J.; Gessler, Arthur; Hacke, Uwe G.; Hakamada, Rodrigo; Hector, Andy; Jenkins, Michael W.; Kane, Jeffrey M.; Kolb, Thomas E.; Law, Darin J.; Lewis, James D.; Limousin, Jean-Marc; Love, David M.; Macalady, Alison K.; Martínez-Vilalta, Jordi; Mencuccini, Maurizio; Mitchell, Patrick J.; Muss, Jordan D.; O’Brien, Michael J.; O’Grady, Anthony P.; Pangle, Robert E.; Pinkard, Elizabeth A.; Piper, Frida I.; Plaut, Jennifer A.; Pockman, William T.; Quirk, Joe; Reinhardt, Keith; Ripullone, Francesco; Ryan, Michael G.; Sala, Anna; Sevanto, Sanna; Sperry, John S.; Vargas, Rodrigo; Vennetier, Michel; Way, Danielle A.; Xu, Chonggang; Yepez, Enrico A.; McDowell, Nate G.

doi:10.1038/s41559-017-0248-x

Title: A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Journal Article · Mon Aug 07 00:00:00 EDT 2017 · Nature Ecology and Evolution

DOI:https://doi.org/10.1038/s41559-017-0248-x· OSTI ID:1431408

Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L.; Hartmann, Henrik; Landhäusser, Simon M.; Tissue, David T.; Huxman, Travis E.; Hudson, Patrick J.; Franz, Trenton E.; Allen, Craig D.; Anderegg, Leander D. L.; Barron-Gafford, Greg A.; Beerling, David J.; Breshears, David D.;

; Bugmann, Harald; Cobb, Richard C.; Collins, Adam D.; Dickman, L. Turin; Duan, Honglang more »

Widespread tree mortality associated with drought has been observed on all forested continents, and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water, and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analyzed across species and biomes using a standardized physiological framework. Here we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or greater loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrates at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in hydraulic deterioration. The consistent Our finding that across species of hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1431408

Report Number(s):: PNNL-SA-130231

Journal Information:: Nature Ecology and Evolution, Vol. 1, Issue 9; Related Information: 1285-1291; ISSN 2397-334X

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

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Lateral Transport of Organic and Inorganic Solutes Aubry, Emilie; Dinant, Sylvie; Vilaine, Françoise Plants, Vol. 8, Issue 1 https://doi.org/10.3390/plants8010020	journal	January 2019
Early-Warning Signals of Individual Tree Mortality Based on Annual Radial Growth Cailleret, Maxime; Dakos, Vasilis; Jansen, Steven ETH Zurich https://doi.org/10.3929/ethz-b-000315307	text	January 2019
The Role of Nonstructural Carbohydrates Storage in Forest Resilience under Climate Change Piper, Frida I.; Paula, Susana Current Forestry Reports, Vol. 6, Issue 1 https://doi.org/10.1007/s40725-019-00109-z	journal	January 2020
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Initial hydraulic failure followed by late-stage carbon starvation leads to drought-induced death in the tree Trema orientalis Kono, Yuri; Ishida, Atsushi; Saiki, Shin-Taro Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-018-0256-7	journal	January 2019
Plant height and hydraulic vulnerability to drought and cold Olson, Mark E.; Soriano, Diana; Rosell, Julieta A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 29 https://doi.org/10.1073/pnas.1721728115	journal	July 2018
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Plant water content integrates hydraulics and carbon depletion to predict drought-induced seedling mortality Sapes, Gerard; Roskilly, Beth; Dobrowski, Solomon Tree Physiology, Vol. 39, Issue 8 https://doi.org/10.1093/treephys/tpz062	journal	July 2019
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Early-Warning Signals of Individual Tree Mortality Based on Annual Radial Growth Cailleret, Maxime; Dakos, Vasilis; Jansen, Steven Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01964	journal	January 2019
Forest Decline Triggered by Phloem Parasitism-Related Biotic Factors in Aleppo Pine (Pinus halepensis) Morcillo, Luna; Gallego, Diego; González, Eudaldo Forests, Vol. 10, Issue 8 https://doi.org/10.3390/f10080608	journal	July 2019
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Insular woody daisies ( Argyranthemum, Asteraceae) are more resistant to drought-induced hydraulic failure than their herbaceous relatives Dória, Larissa C.; Podadera, Diego S.; del Arco, Marcelino Functional Ecology, Vol. 32, Issue 6 https://doi.org/10.1111/1365-2435.13085	journal	March 2018
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Drivers and mechanisms of tree mortality in moist tropical forests McDowell, Nate; Allen, Craig D.; Anderson-Teixeira, Kristina New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15027	journal	February 2018
In vivo quantification of plant starch reserves at micrometer resolution using X-ray microCT imaging and machine learning Earles, J. Mason; Knipfer, Thorsten; Tixier, Aude New Phytologist, Vol. 218, Issue 3 https://doi.org/10.1111/nph.15068	journal	March 2018
Coupling between the terrestrial carbon and water cycles-a review Gentine, Pierre; Green, Julia K.; Guérin, Marceau ETH Zurich https://doi.org/10.3929/ethz-b-000359131	text	January 2019
The stomatal response to rising CO2 concentration and drought is predicted by a hydraulic trait-based optimization model Wang, Yujie; Sperry, John S.; Venturas, Martin D. Tree Physiology, Vol. 39, Issue 8 https://doi.org/10.1093/treephys/tpz038	journal	May 2019
Geographical adaptation prevails over species‐specific determinism in trees’ vulnerability to climate change at Mediterranean rear‐edge forests Dorado‐Liñán, Isabel; Piovesan, Gianluca; Martínez‐Sancho, Elisabet Global Change Biology, Vol. 25, Issue 4 https://doi.org/10.1111/gcb.14544	journal	February 2019
Recent decadal drought reverts warming‐triggered growth enhancement in contrasting climates in the southern Andes tree line Fajardo, Alex; Gazol, Antonio; Mayr, Christoph Journal of Biogeography https://doi.org/10.1111/jbi.13580	journal	May 2019
A new mechanism for tree mortality due to drought and heatwaves Cochard, Hervé Peer Community Journal, Vol. 1 https://doi.org/10.24072/pcjournal.45	journal	January 2021
Low growth resilience to drought is related to future mortality risk in trees Desoto, Lucía; Cailleret, Maxime; Sterck, Frank ETH Zurich https://doi.org/10.3929/ethz-b-000394905	text	January 2020
Xylem embolism measured retrospectively is linked to canopy dieback in natural populations of Eucalyptus piperita following drought Li, Ximeng; Blackman, Chris J.; Rymer, Paul D. Tree Physiology, Vol. 38, Issue 8 https://doi.org/10.1093/treephys/tpy052	journal	May 2018
The effects of persistent drought and waterlogging on the dynamics of nonstructural carbohydrates of Robinia pseudoacacia L. seedlings in Northwest China Yang, Bin; Peng, Changhui; Zhu, Qiuan Forest Ecosystems, Vol. 6, Issue 1 https://doi.org/10.1186/s40663-019-0181-3	journal	April 2019
Embolism resistance in stems of herbaceous Brassicaceae and Asteraceae is linked to differences in woodiness and precipitation Dória, Larissa Chacon; Meijs, Cynthia; Podadera, Diego Sotto Annals of Botany, Vol. 124, Issue 1 https://doi.org/10.1093/aob/mcy233	journal	December 2018
Plant hydraulic traits reveal islands as refugia from worsening drought Ramirez, Aaron R.; De Guzman, Mark E.; Dawson, Todd E. Conservation Physiology, Vol. 8, Issue 1 https://doi.org/10.1093/conphys/coz115	journal	January 2020
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A Structure Shaped by Fire, but Also Water: Ecological Consequences of the Variability in Bark Properties Across 31 Species From the Brazilian Cerrado Loram-Lourenço, Lucas; Farnese, Fernanda dos Santos; Sousa, Letícia Ferreira de Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01718	journal	January 2020
One Century of Forest Monitoring Data in Switzerland Reveals Species- and Site-Specific Trends of Climate-Induced Tree Mortality Sophia, Etzold,; Kasia, Zieminska,; Brigitte, Rohner, ETH Zurich https://doi.org/10.3929/ethz-b-000336595	text	January 2019

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