Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest

Rutuja Chitra-Tarak; Chonggang Xu; Salomón Aguilar; Kristina J. Anderson-Teixeira; Jeff Chambers; Matteo Detto; Boris Faybishenko; Rosie A. Fisher; Ryan G. Knox; Charles D. Koven; Lara M. Kueppers; Nobert Kunert; Stefan J. Kupers; Nate G. McDowell; Brent D. Newman; Steven R. Paton; Rolando Pérez; Laurent Ruiz; Lawren Sack; Jeffrey M. Warren; Brett T. Wolfe; Cynthia Wright; S. Joseph Wright; Joseph Zailaa; Sean M. McMahon

doi:10.1111/nph.17464

Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest

Rutuja Chitra-Tarak, Chonggang Xu, Salomón Aguilar, Kristina J. Anderson-Teixeira, Jeff Chambers, Matteo Detto, Boris Faybishenko, Rosie A. Fisher, Ryan G. Knox, Charles D. Koven, Lara M. Kueppers, Nobert Kunert, Stefan J. Kupers, Nate G. McDowell, Brent D. Newman, Steven R. Paton, Rolando Pérez, Laurent Ruiz, Lawren Sack, Jeffrey M. WarrenBrett T. Wolfe, Cynthia Wright, S. Joseph Wright, Joseph Zailaa, Sean M. McMahon

Ecosystem Processes

Research output: Contribution to journal › Article › peer-review

68 Scopus citations

Abstract

Deep-water access is arguably the most effective, but under-studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep-water access may delay plant dehydration. Here, we tested the role of deep-water access in enabling survival within a diverse tropical forest community in Panama using a novel data-model approach. We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole-soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water-access depths. Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress-related mortality risk through deep-water access. The role of deep-water access in mitigating mortality of hydraulically-vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.

Original language	English
Pages (from-to)	1798-1813
Number of pages	16
Journal	New Phytologist
Volume	231
Issue number	5
DOIs	https://doi.org/10.1111/nph.17464
State	Published - Sep 2021

Funding

This research was supported as part of the Next Generation Ecosystem Experiments-Tropics, funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. Funding also was provided to RC-T and SMM through an NSF grant (1137366). LR was deputed to Indo-French Cell for Water Sciences on an IRD Fellowship. An NSF grant to Smithsonian Institution’s ForestGEO (Dimensions 1046113) partially supported this work via RC-T and SMM. BTW was supported by the National Institute of Food and Agriculture, US Department of Agriculture, McIntire Stennis project under LAB94493. LS was supported by the National Science Foundation award 2017949. RAF was supported by the National Center for Atmospheric Research, which is funded by the National Science Foundation. MD was supported by the Carbon Mitigation Initiative at Princeton University. The BCI forest dynamics research project, founded by Stephen P. Hubbell and Robin B. Foster and sustained for many years by Richard Condit, is now managed by Rolando Pérez (RP), Suzanne Lao and Stuart Davies under the ForestGEO program of the Smithsonian Tropical Research in Panama. Numerous organizations have provided funding, principally the US National Science Foundation, and hundreds of field workers have contributed. Comments from editor Jarmila Pitterman and three anonymous reviewers helped improve and clarify this manuscript. This research was supported as part of the Next Generation Ecosystem Experiments‐Tropics, funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. Funding also was provided to RC‐T and SMM through an NSF grant (1137366). LR was deputed to Indo‐French Cell for Water Sciences on an IRD Fellowship. An NSF grant to Smithsonian Institution’s ForestGEO (Dimensions 1046113) partially supported this work via RC‐T and SMM. BTW was supported by the National Institute of Food and Agriculture, US Department of Agriculture, McIntire Stennis project under LAB94493. LS was supported by the National Science Foundation award 2017949. RAF was supported by the National Center for Atmospheric Research, which is funded by the National Science Foundation. MD was supported by the Carbon Mitigation Initiative at Princeton University. The BCI forest dynamics research project, founded by Stephen P. Hubbell and Robin B. Foster and sustained for many years by Richard Condit, is now managed by Rolando Pérez (RP), Suzanne Lao and Stuart Davies under the ForestGEO program of the Smithsonian Tropical Research in Panama. Numerous organizations have provided funding, principally the US National Science Foundation, and hundreds of field workers have contributed. Comments from editor Jarmila Pitterman and three anonymous reviewers helped improve and clarify this manuscript.

Funders	Funder number
Smithsonian Tropical Research in Panama
National Science Foundation	2017949
Smithsonian Institution
U.S. Department of Energy
Directorate for Biological Sciences	1046113, 1137366
U.S. Department of Agriculture	LAB94493
National Center for Atmospheric Research
National Institute of Food and Agriculture
Office of Science
Biological and Environmental Research
Princeton University

Keywords

deep-water access
drought tolerance
drought-induced mortality
hydraulic vulnerability and safety margins
hydrological droughts
rooting depths
safety-efficiency trade-off
tropical forest

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1111/nph.17464

Cite this

Chitra-Tarak, R., Xu, C., Aguilar, S., Anderson-Teixeira, K. J., Chambers, J., Detto, M., Faybishenko, B., Fisher, R. A., Knox, R. G., Koven, C. D., Kueppers, L. M., Kunert, N., Kupers, S. J., McDowell, N. G., Newman, B. D., Paton, S. R., Pérez, R., Ruiz, L., Sack, L., ... McMahon, S. M. (2021). Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest. New Phytologist, 231(5), 1798-1813. https://doi.org/10.1111/nph.17464

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title = "Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest",

abstract = "Deep-water access is arguably the most effective, but under-studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep-water access may delay plant dehydration. Here, we tested the role of deep-water access in enabling survival within a diverse tropical forest community in Panama using a novel data-model approach. We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole-soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water-access depths. Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress-related mortality risk through deep-water access. The role of deep-water access in mitigating mortality of hydraulically-vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.",

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author = "Rutuja Chitra-Tarak and Chonggang Xu and Salom{\'o}n Aguilar and Anderson-Teixeira, {Kristina J.} and Jeff Chambers and Matteo Detto and Boris Faybishenko and Fisher, {Rosie A.} and Knox, {Ryan G.} and Koven, {Charles D.} and Kueppers, {Lara M.} and Nobert Kunert and Kupers, {Stefan J.} and McDowell, {Nate G.} and Newman, {Brent D.} and Paton, {Steven R.} and Rolando P{\'e}rez and Laurent Ruiz and Lawren Sack and Warren, {Jeffrey M.} and Wolfe, {Brett T.} and Cynthia Wright and Wright, {S. Joseph} and Joseph Zailaa and McMahon, {Sean M.}",

note = "Publisher Copyright: No claim to original US Government works New Phytologist {\textcopyright} 2021 New Phytologist Foundation",

year = "2021",

month = sep,

doi = "10.1111/nph.17464",

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Chitra-Tarak, R, Xu, C, Aguilar, S, Anderson-Teixeira, KJ, Chambers, J, Detto, M, Faybishenko, B, Fisher, RA, Knox, RG, Koven, CD, Kueppers, LM, Kunert, N, Kupers, SJ, McDowell, NG, Newman, BD, Paton, SR, Pérez, R, Ruiz, L, Sack, L, Warren, JM, Wolfe, BT, Wright, C, Wright, SJ, Zailaa, J & McMahon, SM 2021, 'Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest', New Phytologist, vol. 231, no. 5, pp. 1798-1813. https://doi.org/10.1111/nph.17464

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T1 - Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest

AU - Chitra-Tarak, Rutuja

AU - Xu, Chonggang

AU - Aguilar, Salomón

AU - Anderson-Teixeira, Kristina J.

AU - Chambers, Jeff

AU - Detto, Matteo

AU - Faybishenko, Boris

AU - Fisher, Rosie A.

AU - Knox, Ryan G.

AU - Koven, Charles D.

AU - Kueppers, Lara M.

AU - Kunert, Nobert

AU - Kupers, Stefan J.

AU - McDowell, Nate G.

AU - Newman, Brent D.

AU - Paton, Steven R.

AU - Pérez, Rolando

AU - Ruiz, Laurent

AU - Sack, Lawren

AU - Warren, Jeffrey M.

AU - Wolfe, Brett T.

AU - Wright, Cynthia

AU - Wright, S. Joseph

AU - Zailaa, Joseph

AU - McMahon, Sean M.

PY - 2021/9

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N2 - Deep-water access is arguably the most effective, but under-studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep-water access may delay plant dehydration. Here, we tested the role of deep-water access in enabling survival within a diverse tropical forest community in Panama using a novel data-model approach. We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole-soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water-access depths. Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress-related mortality risk through deep-water access. The role of deep-water access in mitigating mortality of hydraulically-vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.

AB - Deep-water access is arguably the most effective, but under-studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep-water access may delay plant dehydration. Here, we tested the role of deep-water access in enabling survival within a diverse tropical forest community in Panama using a novel data-model approach. We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole-soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water-access depths. Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress-related mortality risk through deep-water access. The role of deep-water access in mitigating mortality of hydraulically-vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.

KW - deep-water access

KW - drought tolerance

KW - drought-induced mortality

KW - hydraulic vulnerability and safety margins

KW - hydrological droughts

KW - rooting depths

KW - safety-efficiency trade-off

KW - tropical forest

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JO - New Phytologist

JF - New Phytologist

IS - 5

ER -

Hydraulically-vulnerable trees survive on deep-water access during droughts in a tropical forest

Abstract

Funding

Keywords

UN SDGs

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