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

Abstract

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 analysed across species and biomes using a standardized physiological framework. Here in this work, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves 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 reducing hydraulic function. In conclusion, our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling canmore » be achieved using thresholds in hydraulic function.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10];  [11];  [12];  [13];  [12]; ORCiD logo [14];  [15];  [16];  [17];  [17];  [18] more »;  [19];  [20];  [5]; ORCiD logo [21];  [22];  [23];  [24];  [5];  [25];  [26];  [27];  [28];  [29];  [12];  [30];  [31];  [3];  [32];  [33];  [34];  [35];  [17]; ORCiD logo [36];  [35];  [8];  [35];  [37];  [8];  [8];  [13];  [38];  [39]; ORCiD logo [40];  [41]; ORCiD logo [17];  [3];  [42];  [43];  [44];  [17];  [45];  [46] « less
  1. Oklahoma State Univ., Stillwater, OK (United States)
  2. Macquarie Univ., NSW (Australia); Univ. of Sydney, NSW (Australia)
  3. Univ. of Utah, Salt Lake City, UT (United States)
  4. Max-Planck Institute for Biogeochemistry, Jena (Germany)
  5. Univ. of Alberta, Edmonton, AB (Canada)
  6. Western Sydney University, Penrith, NSW (Australia)
  7. Univ. of California, Irvine, CA (United States)
  8. Univ. of New Mexico, Albuquerque, NM (United States)
  9. Univ. of Nebraska, Lincoln, NE (United States)
  10. U.S. Geological Survey, Fort Collins Science Center, Jemez Mountains Field Station, Los Alamos, NM (United States)
  11. Univ. of Washington, Seattle, WA (United States)
  12. Univ. of Arizona, Tucson, AZ (United States)
  13. Univ. of Sheffield (United Kingdom)
  14. University of Tasmania, Hobart, TAS (Australia)
  15. ETH Zurich (Switzerland)
  16. Univ. of California, Davis, CA (United States)
  17. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  18. Nanchang Institute of Technology (China)
  19. Univ. of Wyoming, Laramie, WY (United States)
  20. Swedish University of Agricultural Sciences, Uppsala (Sweden)
  21. University of Coimbra (Portugal)
  22. Northern Arizona Univ., Flagstaff, AZ (United States); US Forest Service, Flagstaff, AZ (United States)
  23. U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Boise, ID (United States)
  24. Swiss Federal Research Institute WSL, Birmensdorf (Switzerland)
  25. University of Sao Paulo, Piracicaba (Brazil)
  26. Univ. of Oxford (United Kingdom)
  27. Univ. of California, Santa Cruz, CA (United States)
  28. Humboldt State University, Arcata, CA (United States)
  29. Northern Arizona Univ., Flagstaff, AZ (United States)
  30. Fordham University, Armonk, NY (United States)
  31. Centre d'Ecologie Fonctionnelle et Evolutive, CNRS, Montpellier (France)
  32. U.S. Agency for International Development, Washington, DC (United States)
  33. CREAF, Cerdanyola del Valles (Spain); Universitat Autònoma Barcelona, Cerdanyola del Valles (Spain)
  34. ICREA, ICREA-CREAF, Cerdanyola del Valles, Barcelona (Spain); Univ. of Edinburgh, Scotland (United Kingdom)
  35. CSIRO Land and Water, Hobart, TAS (Australia)
  36. Estación Experimental de Zonas Áridas, Consejo Superior de Investigaciones Científicas, La Cañada, Almería (Spain)
  37. Centro de Investigación en Ecosistemas de la Patagonia, Coyhaique (Chile); Instituto de Ecología y Biodiversidad, Santiago (Chile)
  38. Idaho State Univ., Pocatello, ID (United States)
  39. University of Basilicata, Potenza (Italy)
  40. Colorado State Univ., Fort Collins, CO (United States); USDA Forest Service, Rocky Mountain Research Station, Fort Collins, CO (United States)
  41. Univ. of Montana, Missoula, MT (United States)
  42. Univ. of Delaware, Newark, DE (United States)
  43. Irstea, UR RECOVER, Aix en Provence (France)
  44. Duke Univ., Durham, NC (United States); University of Western Ontario, London, ON (Canada)
  45. Instituto Tecnologico de Sonora, Ciudad Obregon, SO (Mexico)
  46. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1467333
Report Number(s):
LA-UR-17-25679
Journal ID: ISSN 2397-334X
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 1; Journal Issue: 9; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; drought; fores mortality; hydraulic failure; carbon starvation

Citation Formats

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 Annika, Sperry, John S., Vargas, Rodrigo, Vennetier, Michel, Way, Danielle A., Xu, Chonggang, Yepez, Enrico A., and McDowell, Nate G. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. United States: N. p., 2017. Web. doi:10.1038/s41559-017-0248-x.
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 Annika, Sperry, John S., Vargas, Rodrigo, Vennetier, Michel, Way, Danielle A., Xu, Chonggang, Yepez, Enrico A., & McDowell, Nate G. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. United States. doi:10.1038/s41559-017-0248-x.
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 Annika, Sperry, John S., Vargas, Rodrigo, Vennetier, Michel, Way, Danielle A., Xu, Chonggang, Yepez, Enrico A., and McDowell, Nate G. Mon . "A multi-species synthesis of physiological mechanisms in drought-induced tree mortality". United States. doi:10.1038/s41559-017-0248-x. https://www.osti.gov/servlets/purl/1467333.
@article{osti_1467333,
title = {A multi-species synthesis of physiological mechanisms in drought-induced tree mortality},
author = {Adams, Henry D. and Zeppel, Melanie J. B. and Anderegg, William R. L. and Hartmann, Henrik and Landhäusser, Simon M. and Tissue, David T. and Huxman, Travis E. and Hudson, Patrick J. and Franz, Trenton E. and Allen, Craig D. and Anderegg, Leander D. L. and Barron-Gafford, Greg A. and Beerling, David J. and Breshears, David D. and Brodribb, Timothy J. and Bugmann, Harald and Cobb, Richard C. and Collins, Adam D. and Dickman, L. Turin and Duan, Honglang and Ewers, Brent E. and Galiano, Lucía and Galvez, David A. and Garcia-Forner, Núria and Gaylord, Monica L. and Germino, Matthew J. and Gessler, Arthur and Hacke, Uwe G. and Hakamada, Rodrigo and Hector, Andy and Jenkins, Michael W. and Kane, Jeffrey M. and Kolb, Thomas E. and Law, Darin J. and Lewis, James D. and Limousin, Jean-Marc and Love, David M. and Macalady, Alison K. and Martínez-Vilalta, Jordi and Mencuccini, Maurizio and Mitchell, Patrick J. and Muss, Jordan D. and O’Brien, Michael J. and O’Grady, Anthony P. and Pangle, Robert E. and Pinkard, Elizabeth A. and Piper, Frida I. and Plaut, Jennifer A. and Pockman, William T. and Quirk, Joe and Reinhardt, Keith and Ripullone, Francesco and Ryan, Michael G. and Sala, Anna and Sevanto, Sanna Annika and Sperry, John S. and Vargas, Rodrigo and Vennetier, Michel and Way, Danielle A. and Xu, Chonggang and Yepez, Enrico A. and McDowell, Nate G.},
abstractNote = {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 analysed across species and biomes using a standardized physiological framework. Here in this work, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves 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 reducing hydraulic function. In conclusion, our finding that 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.},
doi = {10.1038/s41559-017-0248-x},
journal = {Nature Ecology and Evolution},
number = 9,
volume = 1,
place = {United States},
year = {2017},
month = {8}
}

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    • Ammitzboll, Hans; Vaillancourt, René E.; Potts, Brad M.
    • Plant, Cell & Environment, Vol. 43, Issue 1
    • DOI: 10.1111/pce.13649

    Geographically Structured Growth decline of Rear-Edge Iberian Fagus sylvatica Forests After the 1980s Shift Toward a Warmer Climate
    journal, January 2019


    Triggers of tree mortality under drought
    journal, June 2018


    Initial hydraulic failure followed by late-stage carbon starvation leads to drought-induced death in the tree Trema orientalis
    journal, January 2019


    Plant water content integrates hydraulics and carbon depletion to predict drought-induced seedling mortality
    journal, July 2019


    Modelling tropical forest responses to drought and El Niño with a stomatal optimization model based on xylem hydraulics
    journal, October 2018

    • Eller, Cleiton B.; Rowland, Lucy; Oliveira, Rafael S.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 373, Issue 1760
    • DOI: 10.1098/rstb.2017.0315

    Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes
    journal, May 2018

    • Griffin-Nolan, Robert J.; Bushey, Julie A.; Carroll, Charles J. W.
    • Functional Ecology, Vol. 32, Issue 7
    • DOI: 10.1111/1365-2435.13135

    More than iso/anisohydry: Hydroscapes integrate plant water use and drought tolerance traits in 10 eucalypt species from contrasting climates
    journal, April 2019

    • Li, Ximeng; Blackman, Chris J.; Peters, Jennifer M. R.
    • Functional Ecology, Vol. 33, Issue 6
    • DOI: 10.1111/1365-2435.13320

    No role for xylem embolism or carbohydrate shortage in temperate trees during the severe 2015 drought
    journal, August 2018

    • Dietrich, Lars; Delzon, Sylvain; Hoch, Guenter
    • Journal of Ecology, Vol. 107, Issue 1
    • DOI: 10.1111/1365-2745.13051

    Which trees die during drought? The key role of insect host‐tree selection
    journal, April 2019

    • Stephenson, Nathan L.; Das, Adrian J.; Ampersee, Nicholas J.
    • Journal of Ecology, Vol. 107, Issue 5
    • DOI: 10.1111/1365-2745.13176

    Resilience of seed production to a severe El Niño-induced drought across functional groups and dispersal types
    journal, August 2018

    • O'Brien, Michael J.; Peréz-Aviles, Daniel; Powers, Jennifer S.
    • Global Change Biology, Vol. 24, Issue 11
    • DOI: 10.1111/gcb.14416

    Legacies of more frequent drought in ponderosa pine across the western United States
    journal, July 2019

    • Peltier, Drew M. P.; Ogle, Kiona
    • Global Change Biology, Vol. 25, Issue 11
    • DOI: 10.1111/gcb.14720

    Recent decadal drought reverts warming‐triggered growth enhancement in contrasting climates in the southern Andes tree line
    journal, May 2019

    • Fajardo, Alex; Gazol, Antonio; Mayr, Christoph
    • Journal of Biogeography
    • DOI: 10.1111/jbi.13580

    Homeostatic levels of nonstructural carbohydrates after 13 yr of drought and irrigation in Pinus sylvestris
    journal, May 2018

    • Schönbeck, Leonie; Gessler, Arthur; Hoch, Günter
    • New Phytologist, Vol. 219, Issue 4
    • DOI: 10.1111/nph.15224

    Dead or dying? Quantifying the point of no return from hydraulic failure in drought‐induced tree mortality
    journal, April 2019

    • Hammond, William M.; Yu, Kailiang; Wilson, Luke A.
    • New Phytologist, Vol. 223, Issue 4
    • DOI: 10.1111/nph.15922

    Independent genetic control of drought resistance, recovery, and growth of Eucalyptus globulus seedlings
    journal, August 2019

    • Ammitzboll, Hans; Vaillancourt, René E.; Potts, Brad M.
    • Plant, Cell & Environment, Vol. 43, Issue 1
    • DOI: 10.1111/pce.13649

    Strengthened scientific support for the Endangerment Finding for atmospheric greenhouse gases
    journal, December 2018

    • Duffy, Philip B.; Field, Christopher B.; Diffenbaugh, Noah S.
    • Science, Vol. 363, Issue 6427
    • DOI: 10.1126/science.aat5982

    Climatic Suitability Derived From Species Distribution Models Captures Community Responses To An Extreme Drought Episode
    text, January 2018


    Northward migration of trembling aspen will increase growth but reduce resistance to drought-induced xylem cavitation
    journal, November 2019


    A Dirty Dozen Ways to Die: Metrics and Modifiers of Mortality Driven by Drought and Warming for a Tree Species
    journal, October 2018

    • Breshears, David D.; Carroll, Charles J. W.; Redmond, Miranda D.
    • Frontiers in Forests and Global Change, Vol. 1
    • DOI: 10.3389/ffgc.2018.00004

    Diversification rate vs. diversification density: Decoupled consequences of plant height for diversification of Alooideae in time and space
    journal, May 2020